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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.

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]

Background: Plants are affected by several aspects of the soil, which have the potential to exert cascading effects on the performance of herbivorous insects. The effects of biotic and abiotic soil characteristics have however mostly been investigated in isolation, leaving their relative importance largely unexplored. Such is the case for the dune grass Ammophila, whose decline under decreasing sand accretion is argued to be caused by either biotic or abiotic soil properties. Methodology/Principal Findings: By manipulating dune soils from three different regions, we decoupled the contributions of region, the abiotic and biotic soil component to the variation in characteristics of Ammophila arenaria seedlings and Schizaphis rufula aphid populations. Root mass fraction and total dry biomass of plants were affected by soil biota, although the latter effect was not consistent across regions. None of the measured plant properties were significantly affected by the abiotic soil component. Aphid population characteristics all differed between regions, irrespective of whether soil biota were present or absent. Hence these effects were due to differences in abiotic soil properties between regions. Although several chemical properties of the soil mixtures were measured, none of these were consistent with results for plant or aphid traits. Conclusions/Significance: Plants were affected more strongly by soil biota than by abiotic soil properties, whereas the opposite was true for aphids. Our results thus demonstrate that the relative importance of the abiotic and biotic component of soils can differ for plants and their herbivores. The fact that not all effects of soil properties could be detected across regions moreover emphasizes the need for spatial replication in order to make sound conclusions about the generality of aboveground-belowground interactions.

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.