Interactions between plant-parasitic nematodes and their natural enemies in foredunes

Ectoparasitic nematodes are important soil-dwelling herbivores. In her PhD thesis, Anna Pískiewicz set out to clarify the interactions between the ectoparasite Tylenchorhynchus ventralis, its host plant Ammophila arenaria (marram grass) and the nematode’s natural enemies. Her work formed part of the EU EcoTrain project, which involved three PhD candidates and four postdocs and investigated the most important processes determining the nematode population in foredunes.

Pískiewicz studied how the populations of T. ventralis are regulated in the root zone of A. arenaria. If its numbers are not restricted, this nematode species is able to severely suppress the growth of the grass. In the wild, however, the numbers of T. ventralis are usually too low to depress the host plant’s growth – which suggests that the density of the T. ventralis population is suppressed to a non-harmful level. Pískiewicz’s PhD research objective was to shed light on the mechanisms responsible for this suppression.

Infection of the nematode Tylenchorhynchus ventralis with an unknown bacterium (A) and with fungus similar to Catenaria (B). (Source: Piskiewicz, A.M., Duyts, H., Berg, M.P., Costa, S.R. and Van der Putten, W.H. 2007 Soil microorganisms control plant ectoparasitic nematodes in natural coastal foredunes. Oecologia 152: 505-514.)

Mechanisms of suppression
Nematodes might be suppressed as a result of the host plant limiting their supply of food (so-called “bottom–up” mechanisms), or because of competition from other nematodes (“horizontal” mechanisms), or because they are under pressure from their natural enemies (“top–down” mechanisms). Pískiewicz demonstrated that what limits the populations of T. ventralis are their microbial antagonists. Other organisms, such as other nematode species and micro-arthropods, play no significant role in these interactions.
After investigating how the populations of T. ventralis were suppressed by soil microorganisms, she concluded that the impact of these microbial antagonists is probably the result of local or systemic interactions. Local interactions might be caused by microbial parasitism, predation, or antagonism, or by locally inducing anti-nematode defensive responses. Systemic interactions are caused by defence responses induced by the benign microorganisms in parts of the plant where the antagonistic microorganisms are not present. She demonstrated that it was the local interactions that were responsible for suppressing the effects of the microorganisms on T. ventralis.
To test the hypothesis that T. ventralis is able to intercept and interpret signals from its microbial enemies and so avoid these antagonists, Pískiewicz conducted experiments using a Y-tube olfactometer on agar medium and dune sand. She demonstrated that in dune sand, T. ventralis is able to avoid plant roots containing microorganisms. The three possible reasons for this are:

it is repelled by aromatic compounds produced by the microorganisms
it is more strongly attracted to “clean” roots
it is repelled by roots containing micro organisms.

Microorganisms alone did not affect which roots the nematodes went for. The question remains: which part of the microbial community is responsible for repelling the nematodes?

Figure: Number of individuals of the plant-parasitic nematode Tylenchorhynchus ventralis (per 100 g soil): in dune sand that contains all soil organisms (Non-sterilised � >T. ventralis); in the same dune sand, but after inoculation and multiplication of the nematode (Non-sterilised + T. ventralis); and in sterilised dune sand after nematode inoculation. It can clearly be seen that nematode inoculation increases the numbers, but that that there is a growth-retarding factor in unsterilised dune sand. (Source: Piśkiewicz, A.M., Duyts, H., Berg, M.P., Costa, S.R. and Van der Putten, W.H. 2007 Soil microorganisms control plant ectoparasitic nematodes in natural coastal foredunes. Oecologia 152: 505-514.)

Finally, the top–down suppression of eight dominant plant-parasitic nematode species from foredunes by soil microorganisms, nematodes and microarthropods was investigated. Six of the eight nematode species were ectoparasitic and two were endoparasitic. In order to obtain a more complete picture of nematode-controlling mechanisms in foredunes, each nematode species was exposed to microorganisms, nematodes and microarthropods obtained from foredunes, and to sterilised water (the control). It was concluded that for most of the plant-parasitic nematodes, the most important top–down factor was microorganisms. The finding that two of the eight nematode species investigated were completely uninfluenced by the nematodes suggests that microorganisms are not an important control factor for certain nematode species. Pískiewicz also found that some nematode species were suppressed by other nematodes, or by microarthropods – or by both – or, as reported by other researchers, by competition from other nematodes, by arbuscular mycorrhizal fungi, or by endophytic fungi.

Conclusions
The results of the experiments in this PhD research, coupled with the available data from the EcoTrain project on nematode suppression in foredunes show that the regulation of nematodes is more complex than previously thought. The regulatory mechanism depends not only on the type of food, but also on the nematode species. A conclusion is that often more than one factor is involved in the successful suppression of nematodes. Yet although nematode populations can be successfully controlled in natural ecosystems, this is not always the case in agriculture. The findings of the EcoTrain project make it highly likely that a range of control mechanisms would be needed to control nematodes in agriculture and other production systems.