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1. Feedback between plants and soil organisms has become widely recognized as a driving force of community composition and ecosystem functioning. However, there is little uniformity in quantification and analysis of plant–soil feedback effects. Meta-analysis suggested that the various experimental methods tend to result in different feedback values. Yet, a direct comparison of the different experimental approaches and their statistical analyses is lacking. 2. We used currently applied methods to calculate plant–soil feedback value ranges and compared their statistical analyses to those based on actual biomass data. Then, we re-analysed a case study to compare plant–soil feedback values obtained under the same environmental conditions, but using different experimental approaches: soil sterilization, addition of soil inoculum, and soil conditioning by ‘own’ vs. ‘foreign’ plant species. 3. Different measures to calculate plant–soil feedback values were more variable in positive than in negative feedback values. Analysis of calculated feedback values that are based on treatment averages can lead to a serious inflation of type I errors. 4. In our case study, both the strength and the direction of the feedback effects depended on the experimental approach that was chosen, leading to diverging conclusions on whether feedback to a certain soil was positive or negative. Soil sterilization and addition of soil organisms yielded larger feedback than comparison of own and foreign soil. 5. Synthesis. The ecological interpretation of plant–soil feedback effects strongly depends on the experimental procedure. When the research question focuses on the strength and the sign of plant–soil feedback, soil sterilization (presumed that the side effect of increased nutrient availability can be controlled) or addition of soil inoculum is to be preferred. When the research question concerns the specificity of soil feedback effects, plant performance can be better compared between own and foreign soil. We recommend that when using calculated feedback values, the original data need to be presented as well in order to trace the cause of the effect.

A growing number of studies point at the involvement of root herbivores in influencing plant performance, community composition and succession. However, little is known about the factors that control root herbivore abundance and the role of local variation in the effectiveness of these factors. Here, we performed a full factorial experiment with plants, root-feeding nematodes and rhizosphere microbial communities from two dune sites, to test the hypothesis that the outcome of belowground multitrophic interactions depends on local differences between the interacting organisms. The organisms included the marram grass Ammophila arenaria, the cyst nematode Heterodera arenaria, microbial plant pathogens and natural enemies of the nematodes from two coastal foredune systems, one in The Netherlands and one in Wales. The two plant populations differed at the molecular and phenotypic level, and the microbial communities from the two dune sites differed in the composition of the dominant soil fungi but not of the dominant bacteria. Plants were negatively affected by the rhizosphere microorganisms from one of the sites. Nevertheless, nematode performance was not affected by the origin of both the host plants and the microbial communities. The reproductive output of the cyst nematode depended on the presence of microorganisms, as well as on inter-population variability in the response of the nematode to these natural enemies. In the absence of microorganisms, the two nematode populations differed in the number and size of the produced cysts, although maternal effects cannot be excluded. Inter-population differences in the host plant were a secondary factor in the nematode–microorganisms interactions, and did not influence bottom–up control of the cyst nematodes. Our results did not reveal strong signals of coevolution in belowground multitrophic interactions of plants, cyst nematodes and soil microbial communities. We conclude that the interactions between the studied organisms do not necessarily depend on their local vs. non-local origin. Nevertheless, we were able to show that local variation in soil organism community composition can be an important factor in determining the outcome of interactions in belowground multitrophic systems.

Root-feeding nematodes are major soil-borne pests in agriculture. In natural ecosystems, their abundance can be strongly controlled by natural enemies. In coastal foredune soil, the abundance of the ectoparasitic nematode Tylenchorhynchus ventralis is controlled by local interactions with soil microorganisms. If not controlled, T. ventralis reduces growth and performance of the host plant Ammophila arenaria. In the present study, we examine if the nematodes may sense the presence of soil microorganisms and, if so, they are able to actively avoid their enemies. First, using Petri dishes with agar medium we examined if T. ventralis can choose between A. arenaria seedlings inoculated with or without soil microorganisms. We observed that there was a trend (although non-significant) in nematode migration towards the non-inoculated plants. If the seedlings were not present, the nematodes did not make any choice and stayed in the centre of the Petri dish. Then, using Y-tubes filled with sterilized dune soil, we examined if T. ventralis could choose between A. arenaria roots with or without microorganisms. We also included treatments of microbial suspensions without plants and a microbe-free filtrate. We observed that the nematodes preferred roots without microorganisms. Microorganisms alone or roots with microbial filtrate did not influence nematode choice significantly. We conclude that the nematode T. ventralis is able to choose roots without soil microorganisms when having roots with them as alternative. Such avoidance could explain why biological control of nematodes in field is not always effective, especially when microbial antagonists accumulate in specific parts of the rhizosphere.

1. As a result of global warming, species may spread into previously cool regions. Species that disperse faster than their natural enemies may become released from top-down control. We investigated whether plants originating from southern Europe and recently established in north-western Europe experience less soil pathogen effects than native species. 2. We selected three plant species originating from southern Europe that have immigrated into the Netherlands and three similar native Dutch species. All six plant species were grown in sterilized soils with a soil inoculum collected from the rhizospheres of field populations. As a control we grew a series of all six plant species with a sterilized rhizosphere inoculum. 3. We harvested the plants, added the conditioned soil to sterilized soil and grew a second generation of all six plant species in order to test for each plant pair feedback effects from the conditioned soil communities to conspecifics and heterospecifics. 4. The effect of the soil community is dependent on plant species, and is dependent on soil fertility in only one of the three pairs. 5. Soil conditioning caused less biomass reduction to exotic plant species than to native species, suggesting that exotic immigrants are less exposed to soil pathogens than similar native plant species. 6. Our results suggest that plant species that expand their range as a result of climate change may become released from soil pathogenic activity. Whether the exotics are released from soil pathogens, or whether they experience enhanced benefit from mutualistic symbionts remains to be studied. We conclude that range expansion may result in enemy release patterns that are similar to artificially introduced invasive exotic plant species. 7. The escape from enemies through range shifts changes key biotic interactions and complicates predictions of future distribution and dominance.

Recent studies have concluded that release from native soil pathogens may explain invasion of exotic plant species. However, release from soil enemies does not explain all plant invasions. The invasion of Ammophila arenaria (marram grass or European beach grass) in California provides an illustrative example for which the enemy release hypothesis has been refuted. To explore the possible role of plant–soil community interactions in this invasion, we developed a mathematical model. First, we analyzed the role of plant–soil community interactions in the succession of A. arenaria in its native range (north-western Europe). Then, we used our model to explore for California how alternative plant–soil community interactions may generate the same effect as if A. arenaria were released from soil enemies. This analysis was carried out by construction of a 'recovery plane' that discriminates between plant competition and plant–soil community interactions. Our model shows that in California, the accumulation of local pathogens by A. arenaria could result in exclusion of native plant species. Moreover, this mechanism could trigger the rate and spatial pattern of invasive spread generally observed in nature. We propose that our 'accumulation of local pathogens' hypothesis could serve as an alternative explanation for the enemy release hypothesis to be considered in further experimental studies on invasive plant species.

Plant-parasitic nematodes are major crop pests in agro-ecosystems while in nature their impact may range from substantial to no significant growth reduction. The aim of this review is to determine if nematode population control in natural ecosystems may provide us with a model for enhancing sustainable control of nematodes in crops. In agricultural systems, monocultures, narrow rotations, alteration of the soil habitat, and fertilization may alter plant-parasitic nematode dynamics and boost nematode numbers while reducing diversity and effectiveness of top-down control organisms and protective mutualisms (endophytes and arbuscular mycorrhizal fungi). Traditional agro-ecosystems (still applied in tropical regions) involve the development of complex practices such as a broad range of plant species of high genetic diversity grown in associations, rotations, and shifting cultivation, which all influence the complexity of plant-parasitic nematode communities and of control organisms. In nature, plant-parasitic nematodes (and other root feeders and soil pathogens) drive plant community processes, such as succession and plant species diversity. Natural soils contain a wide variety of potential nematode control organisms, but the consequences of this diversity are not known. Wild plant populations also contain more genetic variability than crops, but consequences for coevolution and Red Queen processes for nematode populations have not been studied. We conclude that integrated crop pest control may benefit from studying plant-parasitic nematode-natural antagonist interactions in natural systems, which have been coevolved for longer than crop-nematode-antagonist systems. Understanding how wild plants control their plant-parasitic nematodes may ultimately result in improving the sustainability of crop protection against plant-parasitic nematodes

In coastal foredunes, the cyst nematode Heterodera arenaria has been supposed to play a role in degeneration of the pioneer grass Ammophila arenaria (marram grass). However, recent field surveys and field inoculation experiments suggested that the abundance of this cyst nematode is controlled by the host plant. Here, we test pathogenicity of H. arenaria by inoculating a range of densities of second-stage juveniles (J2) onto A. arenaria in sterilised soil. Plant root biomass was reduced after 6 weeks of growth, but not after 13 weeks, when cyst formation was completed. Shoot biomass was not influenced. In the field, H. arenaria occurred in sand and on roots of Elymus farctus and A. arenaria in mobile dunes, but not on A. arenaria in stable dunes. Although we observed Heterodera cysts and juveniles in later succession stages, this cyst nematode appeared to be H. hordecalis. In a host suitability test, H. arenaria produced cysts on E. farctus and A. arenaria, while there were almost no cysts produced when J2 had been added to the later succession species Festuca rubra ssp. arenaria, Carex arenaria, Elymus athericus and Calamagrostis epigejos. Heterodera arenaria did not negatively affect its natural host plants. However, H. arenaria reduced root growth of one later succession plant species, E. athericus, which was a poor host for H. arenaria. The effects of H. arenaria inoculation on plant biomass production did not differ when J2 were added to plants growing in non-sterilised soil. We conclude that H. arenaria is specialised on the pioneer grasses E. farctus and A. arenaria, and also on mobile dunes as a habitat. Our results confirm recent suggestions that H. arenaria may cause little direct growth reduction to its natural host plants. [KEYWORDS: AMMOPHILA ARENARIA ; BIOTROPHIC PARASITE ; COASTAL FOREDUNE ; HETERODERA HORDECALIS ; HOST SPECIFICITY]

1. Feedback between plants and soil organisms has become widely recognized as a driving force of community composition and ecosystem functioning. However, there is little uniformity in quantification and analysis of plant–soil feedback effects. Meta-analysis suggested that the various experimental methods tend to result in different feedback values. Yet, a direct comparison of the different experimental approaches and their statistical analyses is lacking. 2. We used currently applied methods to calculate plant–soil feedback value ranges and compared their statistical analyses to those based on actual biomass data. Then, we re-analysed a case study to compare plant–soil feedback values obtained under the same environmental conditions, but using different experimental approaches: soil sterilization, addition of soil inoculum, and soil conditioning by ‘own’ vs. ‘foreign’ plant species. 3. Different measures to calculate plant–soil feedback values were more variable in positive than in negative feedback values. Analysis of calculated feedback values that are based on treatment averages can lead to a serious inflation of type I errors. 4. In our case study, both the strength and the direction of the feedback effects depended on the experimental approach that was chosen, leading to diverging conclusions on whether feedback to a certain soil was positive or negative. Soil sterilization and addition of soil organisms yielded larger feedback than comparison of own and foreign soil. 5. Synthesis. The ecological interpretation of plant–soil feedback effects strongly depends on the experimental procedure. When the research question focuses on the strength and the sign of plant–soil feedback, soil sterilization (presumed that the side effect of increased nutrient availability can be controlled) or addition of soil inoculum is to be preferred. When the research question concerns the specificity of soil feedback effects, plant performance can be better compared between own and foreign soil. We recommend that when using calculated feedback values, the original data need to be presented as well in order to trace the cause of the effect.

Soil communities can have profound effects on invasions of ecosystems by exotic plant species. We propose that there are three main pathways by which this can happen. First, plant–soil feedback interactions in the invaded range are neutral to positive, whereas native plants predominantly suffer from negative soil feedback effects. Second, exotic plants can manipulate local soil biota by enhancing pathogen levels or disrupting communities of root symbionts, while suffering less from this than native plants. Third, exotic plants produce allelochemicals toxic to native plants that cannot be detoxified by local soil communities, or that become more toxic following microbial conversion. We discuss the need for integrating these three pathways in order to further understand how soil communities influence exotic plant invasions.

1. In natural grassland ecosystems, root-feeding nematodes and insects are the dominant below-ground herbivores. In coastal foredunes, the ectoparasitic nematode Tylenchorhynchus ventralis would be a major root herbivore if not strongly controlled by soil microorganisms. Here, we examined if the suppressive effects of the microbial enemies of T. ventralis act by local interactions such as predation, parasitism or antagonism, or local induction of plant defence, or by non-local interactions, such as systemic effects when microorganisms in one section of the plant roots can affect nematode control in another section of the root system. We show that abundance of T. ventralis in the root zone of the grass Ammophila arenaria is suppressed by local interactions. 2. We compared local vs. non-local control of nematodes by a natural community of soil microorganisms in a split-root experiment, where nematodes and microbes were inoculated to the same, or to opposite root compartments. 3. The split-root experiment revealed that microorganisms affected T. ventralis numbers only when present in the same root compartment. Therefore, the effects of microorganisms on T. ventralis are due to local interactions and not due to induction of a systemic defence mechanism in the plant host. 4. When inoculated together with microorganisms, the nematodes were heavily infected with unknown bacteria and with fungi that resembled the genus Catenaria, suggesting that microorganisms control nematodes through parasitism. However, local defence induction cannot be completely excluded. 5. Besides microbial enemies of nematodes, the root zone of A. arenaria also contains plant pathogens. Root biomass was reduced by nematode infection, but also by the combination of nematodes and microorganisms, most likely because the soil pathogens overwhelmed the effects of nematode control on plant production. 6. We conclude that there may be a trade-off between beneficial effects of soil microorganisms on the plant host due to nematode control vs. pathogenic effects of soil microorganisms on the plant host. We propose that such trade-offs require more attention when studying below-ground multitrophic interactions.

One of the major limitations to enhance sustainability of crop production systems is the inability to control root-feeding nematodes without using chemical biocides. In soils under wild vegetation, however, root-feeding nematodes affect plant performance and plant community composition varying from substantially to insignificantly. Previous studies in natural ecosystems have already shown that mutualistic symbionts, such as arbuscular mycorrhizal fungi and endophytes, may influence plant exposure to root-feeding nematodes. In order to learn more from natural systems, we examined nematode control in the root zone of a wild coastal foredune grass by microorganisms, other nematodes and microarthropods. We cultured all eight root-feeding nematode species that occur in the root zone of marram grass (Ammophila arenaria) in coastal foredunes of the Netherlands. Then, in an indoor growth experiment we exposed each nematode species to the potential natural antagonists collected from the same dune soil. Most of the eight dominant root-feeding nematode species could be controlled to some extent by more than one group of soil organisms added. The effectiveness of control varied among nematode species, which seemed to be controlled in a species-specific way. We conclude that in a natural soil the effectiveness of control by microorganisms, other nematodes or microarthropods varies among root-feeding nematode species. Most are controlled, at least to some extent, by soil microbes. However, some root-feeding nematode species are controlled only by microarthropods. Our results strongly suggest that sustainable agriculture will benefit from using a range of biological control mechanisms when controlling root-feeding nematodes, rather than relying on single control agents. Our suggestion also implies that conserving soil biodiversity is crucial in order to enhance the reliability of biological crop protection against soil-borne pests and diseases.

Belowground herbivores can exert important controls on the composition of natural plant communities. Until now, relatively few studies have investigated which factors may control the abundance of belowground herbivores. In Dutch coastal foredunes, the root-feeding nematode Tylenchorhynchus ventralis is capable of reducing the performance of the dominant grass Ammophila arenaria (Marram grass). However, field surveys show that populations of this nematode usually are controlled to nondamaging densities, but the control mechanism is unknown. In the present study, we first established that T. ventralis populations are top-down controlled by soil biota. Then, selective removal of soil fauna suggested that soil microorganisms play an important role in controlling T. ventralis. This result was confirmed by an experiment where selective inoculation of microarthropods, nematodes and microbes together with T. ventralis into sterilized dune soil resulted in nematode control when microbes were present. Adding nematodes had some effect, whereas microarthropods did not have a significant effect on T. ventralis. Our results have important implications for the appreciation of herbivore controls in natural soils. Soil food web models assume that herbivorous nematodes are controlled by predaceous invertebrates, whereas many biological control studies focus on managing nematode abundance by soil microorganisms. We propose that soil microorganisms play a more important role than do carnivorous soil invertebrates in the top-down control of herbivorous ectoparasitic nematodes in natural ecosystems. This is opposite to many studies on factors controlling root-feeding insects, which are supposed to be controlled by carnivorous invertebrates, parasitoids, or entomopathogenic nematodes. Our conclusion is that the ectoparasitic nematode T. ventralis is potentially able to limit productivity of the dune grass A. arenaria but that soil organisms, mostly microorganisms, usually prevent the development of growth-reducing population densities. © 2007 Springer-Verlag.

Plant‐parasitic nematodes are major crop pests in agro‐ecosystems while in nature their impact may range from substantial to no significant growth reduction. The aim of this review is to determine if nematode population control in natural ecosystems may provide us with a model for enhancing sustainable control of nematodes in crops. In agricultural systems, monocultures, narrow rotations, alteration of the soil habitat, and fertilization may alter plant‐parasitic nematode dynamics and boost nematode numbers while reducing diversity and effectiveness of top–down control organisms and protective mutualisms (endophytes and arbuscular mycorrhizal fungi). Traditional agro‐ecosystems (still applied in tropical regions) involve the development of complex practices such as a broad range of plant species of high genetic diversity grown in associations, rotations, and shifting cultivation, which all influence the complexity of plant‐parasitic nematode communities and of control organisms. In nature, plant‐parasitic nematodes (and other root feeders and soil pathogens) drive plant community processes, such as succession and plant species diversity. Natural soils contain a wide variety of potential nematode control organisms, but the consequences of this diversity are not known. Wild plant populations also contain more genetic variability than crops, but consequences for coevolution and Red Queen processes for nematode populations have not been studied. We conclude that integrated crop pest control may benefit from studying plant‐parasitic nematode—natural antagonist interactions in natural systems, which have been coevolved for longer than crop‐nematode–antagonist systems. Understanding how wild plants control their plant‐parasitic nematodes may ultimately result in improving the sustainability of crop protection against plant‐parasitic nematodes.