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Single introductions of soil biota and plants generate long-term legacies in soil and plant community assembly
Wubs, E.R.J. ; Putten, Wim H. van der; Mortimer, Simon R. ; Korthals, Gerard W. ; Duyts, Henk ; Wagenaar, Roel ; Bezemer, Martijn - \ 2019
Ecology Letters (2019). - ISSN 1461-023X
Community assembly - nature restoration - plant–soil biota interactions - soil legacy - whole-soil inoculation
Recent demonstrations of the role of plant–soil biota interactions have challenged the conventional view that vegetation changes are mainly driven by changing abiotic conditions. However, while this concept has been validated under natural conditions, our understanding of the long-term consequences of plant–soil interactions for above-belowground community assembly is restricted to mathematical and conceptual model projections. Here, we demonstrate experimentally that one-time additions of soil biota and plant seeds alter soil-borne nematode and plant community composition in semi-natural grassland for 20 years. Over time, aboveground and belowground community composition became increasingly correlated, suggesting an increasing connectedness of soil biota and plants. We conclude that the initial composition of not only plant communities, but also soil communities has a long-lasting impact on the trajectory of community assembly.
Data from: Integrating quantitative morphological and qualitative molecular methods to analyze soil nematode community responses to plant range expansion
Geisen, Stefan ; Snoek, L.B. ; Hooven, Freddy C. ten; Duyts, Henk ; Kostenko, Olga ; Bloem, J. ; Martens, H.J. ; Quist, C.W. ; Helder, J. ; Putten, W.H. van der - \ 2018
1. Belowground nematodes are important for soil functioning, as they are ubiquitous and operate at various trophic levels in the soil food web. However, morphological nematode community analysis is time consuming and requires ample training. qPCR-based nematode identification techniques are well available, but high throughput sequencing (HTS) might be more suitable for non-targeted nematode community analysis. 2. We compared effectiveness of qPCR and HTS-based approaches with morphological nematode identification while examining how climate warming-induced plant range expansion may influence belowground nematode assemblages. We extracted nematodes from soil of Centaurea stoebe and C. jacea populations in Slovenia, where both plant species are native, and Germany, where C. stoebe is range expander and C. jacea is native. Half of each nematode sample was identified morphologically and the other half was analysed using targeted qPCR and a novel HTS approach. 3. HTS produced the highest taxonomic resolution of the nematode community. Nematode taxa abundances correlated between the methods. Therefore, especially relative HTS and relative morphological data revealed nearly identical ecological patterns. All methods showed lower numbers of plant feeding nematodes in rhizosphere soils of C. stoebe compared to C. jacea. However, a profound difference was observed between absolute and relative abundance data; both sampling origin and plant species affected relative abundances of bacterivorous nematodes, whereas there was no effect on absolute abundances. 4. Taken together, as HTS correlates with relative analyses of soil nematode communities, while providing highest taxonomic resolution and sample throughput, we propose a combination of HTS with microscopic counting to supplement important quantitative data on soil nematode communities. This provides the most cost-effective, in-depths methodology to study soil nematode community responses to changes in the environment. This methodology will also be applicable to nematode analyses in aquatic systems.
Integrating quantitative morphological and qualitative molecular methods to analyze soil nematode community responses to plant range expansion
Geisen, Stefan ; Snoek, L.B. ; Hooven, Freddy C. ten; Duyts, Henk ; Kostenko, Olga ; Bloem, J. ; Martens, H.J. ; Quist, C.W. ; Helder, J. ; Putten, W.H. van der - \ 2018
PRJEB24755 - ERP106607 - Nematode method calibration
Nematodes were extracted from soils of a range expanding and related plant species in the native region of both and the expanded region of the range expanding plant species. we then identified half of the extracted nematodes morphologically and extracted DNA from the other half to apply qPCR with groups specific primers and high throughput amplicon sequencing (HTS). The aim was to compare the methods which overall showed strong correlations. However, different methods had distinct strengths (e.g. providing absolute abundances for morphology, the ease of specific quantification of nematode groups for qPCR and the high resolution of all nematode taxa simultaneously for HTS). Therefore we propose a method combination for in depths studies of soil nematode communities.
Integrating quantitative morphological and qualitative molecular methods to analyse soil nematode community responses to plant range expansion
Geisen, Stefan ; Snoek, L.B. ; Hooven, Freddy C. ten; Duyts, Henk ; Kostenko, Olga ; Bloem, Janneke ; Martens, Henk ; Quist, Casper W. ; Helder, Johannes A. ; Putten, Wim H. van der - \ 2018
Methods in Ecology and Evolution 9 (2018)6. - ISSN 2041-210X - p. 1366 - 1378.
Biodiversity - High-throughput sequencing - Microscopy - Molecular approaches - Nematodes - QPCR - Soils
Below-ground nematodes are important for soil functioning, as they are ubiquitous and operate at various trophic levels in the soil food web. However, morphological nematode community analysis is time consuming and requires ample training. qPCR-based nematode identification techniques are well available, but high-throughput sequencing (HTS) might be more suitable for non-targeted nematode community analyses. We compared effectiveness of qPCR- and HTS-based approaches with morphological nematode identification while examining how climate warming-induced plant range expansion may influence below-ground nematode assemblages. We extracted nematodes from soil of Centaurea stoebe and C. jacea populations in Slovenia, where both plant species are native, and Germany, where C. stoebe is a range expander and C. jacea is native. Half of each nematode sample was identified morphologically and the other half was analysed using targeted qPCR and a novel HTS approach. HTS produced the highest taxonomic resolution of the nematode community. Nematode taxa abundances correlated between the methods. Therefore, especially relative HTS and relative morphological data revealed nearly identical ecological patterns. All methods showed lower numbers of plant-feeding nematodes in rhizosphere soils of C. stoebe compared to C. jacea. However, a profound difference was observed between absolute and relative abundance data; both sampling origin and plant species affected relative abundances of bacterivorous nematodes, whereas there was no effect on absolute abundances. Taken together, as HTS correlates with relative analyses of soil nematode communities, while providing highest taxonomic resolution and sample throughput, we propose a combination of HTS with microscopic counting to supplement important quantitative data on soil nematode communities. This provides the most cost-effective, in-depth methodology to study soil nematode community responses to changes in the environment. This methodology will also be applicable to nematode analyses in aquatic systems.
Possible mechanisms underlying abundance and diversity responses of nematode communities to plant diversity
Cortois, R. ; Veen, G.F. ; Duyts, Henk ; Abbas, Maike ; Strecker, Tanja ; Kostenko, Olga ; Eisenhauer, Nico ; Scheu, Stefan ; Gleixner, Gerd ; Deyn, Gerlinde B. De; Putten, Wim H. van der - \ 2017
Ecosphere 8 (2017)5. - ISSN 2150-8925
C:N ratio - Functional diversity - Mechanistic linkages - Nematode diversity - Plant diversity - Plant-soil interaction - Resource quality - Resource quantity - Structural equation modeling
Plant diversity is known to influence the abundance and diversity of belowground biota; however, patterns are not well predictable and there is still much unknown about the driving mechanisms. We analyzed changes in soil nematode community composition as affected by long-term manipulations of plant species and functional group diversity in a field experiment with plant species diversity controlled by sowing a range of 1-60 species mixtures and controlling non-sown species by hand weeding. Nematode communities contain a variety of species feeding on bacteria, fungi, plants, invertebrates, while some are omnivorous. We analyzed responses of nematode abundance and diversity to plant species and functional diversity, and used structural equation modeling (SEM) to explore the possible mechanisms underlying the observed patterns. The abundance of individuals of all nematode feeding types, except for predatory nematodes, increased with both plant species and plant functional group diversity. The abundance of microbial-feeding nematodes was related positively to aboveground plant community biomass, whereas abundance of plant-feeding nematodes was related positively to shoot C:N ratio. The abundance of predatory nematodes, in turn, was positively related to numbers of plant-feeding nematodes, but not to the abundance of microbial feeders. Interestingly, the numbers of plant-feeding nematodes per unit root mass were lowest in the high-diversity plant communities, pointing at reduced exposure to belowground herbivores when plants grow in species-diverse communities. Taxon richness of plant-feeding and microbialfeeding nematodes increased with plant species and plant functional group diversity. Increasing plant functional group diversity also enhanced taxon richness of predatory nematodes. The SEM suggests that bottom-up control effects of plant species and plant functional group diversity on abundance of nematodes in the various feeding types predominantly involve mechanistic linkages related to plant quality instead of plant quantity; especially, C:N ratios of the shoot tissues, and/or effects of plants on the soil habitat, rather than shoot quantity explained nematode abundance. Although aboveground plant properties may only partly serve as a proxy for belowground resource quality and quantity, our results encourage further studies on nematode responses to variations in plant species and plant functional diversity in relation to both quantity and quality of the belowground resources.
Soil networks become more connected and take up more carbon as nature restoration progresses
Morriën, W.E. ; Hannula, S.E. ; Snoek, L.B. ; Helmsing, N.R. ; Zweers, Hans ; Hollander, M. de; Soto, Raquel Luján ; Bouffaud, Marie Lara ; Buée, M. ; Dimmers, W.J. ; Duyts, Henk ; Geisen, Stefan ; Girlanda, Mariangela ; Griffiths, R.I. ; Jorgensen, H.B. ; Jensen, J. ; Plassart, P. ; Redecker, Dirk ; Schmelz, R.M. ; Schmidt, Olaf ; Thomson, Bruce C. ; Tisserant, Emilie ; Uroz, Stephane ; Winding, Anne ; Bailey, M.J. ; Bonkowski, M. ; Faber, J.H. ; Martin, F. ; Lemanceau, Philippe ; Boer, W. de; Veen, J.A. van; Putten, W.H. van der - \ 2017
Nature Communications 8 (2017). - ISSN 2041-1723 - 10 p.
Soil organisms have an important role in aboveground community dynamics and ecosystem functioning in terrestrial ecosystems. However, most studies have considered soil biota as a black box or focussed on specific groups, whereas little is known about entire soil networks. Here we show that during the course of nature restoration on abandoned arable land a compositional shift in soil biota, preceded by tightening of the belowground networks, corresponds with enhanced efficiency of carbon uptake. In mid- and long-term abandoned field soil, carbon uptake by fungi increases without an increase in fungal biomass or shift in bacterial-to-fungal ratio. The implication of our findings is that during nature restoration the efficiency of nutrient cycling and carbon uptake can increase by a shift in fungal composition and/or fungal activity. Therefore, we propose that relationships between soil food web structure and carbon cycling in soils need to be reconsidered.
Aboveground mammal and invertebrate exclusions cause consistent changes in soil food webs of two subalpine grassland types, but mechanisms are system-specific
Vandegehuchte, Martijn L. ; Putten, Wim H. Van Der; Duyts, Henk ; Schütz, Martin ; Risch, Anita C. - \ 2017
Oikos 126 (2017)2. - ISSN 0030-1299 - p. 212 - 223.
Ungulates, smaller mammals, and invertebrates can each affect soil biota through their influence on vegetation and soil characteristics. However, direct and indirect effects of the aboveground biota on soil food webs remain to be unraveled. We assessed effects of progressively excluding aboveground large-, medium- and small-sized mammals as well as invertebrates on soil nematode diversity and feeding type abundances in two subalpine grassland types: short- and tall-grass vegetation. We explored pathways that link exclusions of aboveground biota to nematode feeding type abundances via changes in plants, soil environment, soil microbial biomass, and soil nutrients.
In both vegetation types, exclusions caused a similar shift toward higher abundance of all nematode feeding types, except plant feeders, lower Shannon diversity, and lower evenness. These effects were strongest when small mammals, or both small mammals and invertebrates were excluded in addition to excluding larger mammals. Exclusions resulted in a changed abiotic soil environment that only affected nematodes in the short-grass vegetation. In each vegetation type, exclusion effects on nematode abundances were mediated by different drivers related to plant quantity and quality. In the short-grass vegetation, not all exclusion effects on omni–carnivorous nematodes were mediated by the abundance of lower trophic level nematodes, suggesting that omni–carnivores also depended on other prey than nematodes.
We conclude that small aboveground herbivores have major impacts on the soil food web of subalpine short- and tall-grass ecosystems. Excluding aboveground animals caused similar shifts in soil nematode assemblages in both subalpine vegetation types, however, mechanisms turned out to be system-specific.
Data from: Aboveground mammal and invertebrate exclusions cause consistent changes in soil food webs of two subalpine grassland types, but mechanisms are system-specific
Vandegehuchte, Martijn L. ; Putten, W.H. van der; Duyts, H. ; Schütz, Martin ; Risch, Anita C. - \ 2016
soil ecology - above-belowground interactions - herbivory
Data_OIK-03341.R2.csv contains the data on nematode feeding type abundances and community indices, as well as the data used in the Structural Equation Models of the progressive aboveground mammal and invertebrate exclusion effects on the abundance of bacterivorous, fungivorous, plant-feeding and omni-carnivorous nematode abundance via pathways of plants, soil nutrients, soil microbial biomass, and soil environment in both short- and tall-grass vegetation
Aboveground vertebrate and invertebrate herbivore impact on net N mineralization in subalpine grasslands
Risch, A.C. ; Schütz, Martin ; Vandegehuchte, Martijn L. ; Putten, W.H. Van Der; Duyts, Henk ; Raschein, Ursina ; Gwiazdowicz, D.J. ; Busse, M.D. ; Page-Dumroese, D.S. ; Zimmermann, Stephan - \ 2015
Ecology 96 (2015)12. - ISSN 0012-9658 - p. 3312 - 3322.
Above-belowground interactions - Exclosure types - Functionally different herbivores - Herbivory - Nutrient cycling - Plant biomass - Plant properties - Soil arthropods - Soil mites - Soil properties - Subalpine grasslands - Switzerland
Aboveground herbivores have strong effects on grassland nitrogen (N) cycling. They can accelerate or slow down soil net N mineralization depending on ecosystem productivity and grazing intensity. Yet, most studies only consider either ungulates or invertebrate herbivores, but not the combined effect of several functionally different vertebrate and invertebrate herbivore species or guilds. We assessed how a diverse herbivore community affects net N mineralization in subalpine grasslands. By using size-selective fences, we progressively excluded large, medium, and small mammals, as well as invertebrates from two vegetation types, and assessed how the exclosure types (ET) affected net N mineralization. The two vegetation types differed in long-term management (centuries), forage quality, and grazing history and intensity. To gain a more mechanistic understanding of how herbivores affect net N mineralization, we linked mineralization to soil abiotic (temperature; moisture; NO3 -, NH4 +, and total inorganic N concentrations/pools; C, N, P concentrations; pH; bulk density), soil biotic (microbial biomass; abundance of collembolans, mites, and nematodes) and plant (shoot and root biomass; consumption; plant C, N, and fiber content; plant N pool) properties. Net N mineralization differed between ET, but not between vegetation types. Thus, shortterm changes in herbivore community composition and, therefore, in grazing intensity had a stronger effect on net N mineralization than long-term management and grazing history. We found highest N mineralization values when only invertebrates were present, suggesting that mammals had a negative effect on net N mineralization. Of the variables included in our analyses, only mite abundance and aboveground plant biomass explained variation in net N mineralization among ET. Abundances of both mites and leaf-sucking invertebrates were positively correlated with aboveground plant biomass, and biomass increased with progressive exclusion. The negative impact of mammals on net N mineralization may be related partially to (1) differences in the amount of plant material (litter) returned to the belowground subsystem, which induced a positive bottom-up effect on mite abundance, and (2) alterations in the amount and/or distribution of dung, urine, and food waste. Thus, our results clearly show that short-term alterations of the aboveground herbivore community can strongly impact nutrient cycling within ecosystems independent of long-term management and grazing history.
Plant-feeding nematodes in coastal sand dunes: occurrence, host specificity and effects on plant growth
Brinkman, E.P. ; Duyts, H. ; Karssen, G. ; Stoel, C.D. ; Putten, W.H. van der - \ 2015
Plant and Soil 397 (2015)1. - ISSN 0032-079X - p. 17 - 30.
Ammophila arenaria - Ectoparasite - Endoparasite - Foredune - Generalist - Specialist
Aims Coastal sand dunes have a well-established abiotic gradient from beach to land and a corresponding spatial gradient of plant species representing succession in time. Here, we relate the distribution of plant-feeding nematodes with dominant plant species in the field to host specialization and impacts on plant species under controlled greenhouse conditions. Methods We assessed plant-feeding nematodes in soil and roots of six plant species that dominate the vegetation at successional positions along the gradient. In controlled conditions, we determined performance of all plant-feeding nematodes on each plant species and their effects on plant biomass. Results Specialist feeding type nematodes were confined to plant species in either foredunes or landward dunes. Generalist feeding type nematodes were found in highest numbers in the landward dunes. Most tested nematode species decreased root, but not shoot or rhizome biomass. Conclusions Host plant suitability determined occurrence of some plant-feeding nematodes in dunes, but abiotic and biotic soil conditions may play a role as well. Generalist feeding type nematodes were able to reproduce on all plant species. Feeding specialists, which are more protected by plant roots, might prefer host plants in the foredunes for the same reason as their host plants: to escape from natural enemies.
Plant diversity and identity effects on predatory nematodes and their prey
Kostenko, O. ; Duyts, H. ; Grootemaat, S. ; Deyn, G.B. de; Bezemer, T.M. - \ 2015
Ecology and Evolution 5 (2015)4. - ISSN 2045-7758 - p. 836 - 847.
entomopathogenic nematodes - biological-control - biodiversity experiment - parasitic nematodes - food-web - soil - communities - grasslands - steinernema - populations
There is considerable evidence that both plant diversity and plant identity can influence the level of predation and predator abundance aboveground. However, how the level of predation in the soil and the abundance of predatory soil fauna are related to plant diversity and identity remains largely unknown. In a biodiversity field experiment, we examined the effects of plant diversity and identity on the infectivity of entomopathogenic nematodes (EPNs, Heterorhabditis and Steinernema spp.), which prey on soil arthropods, and abundance of carnivorous non-EPNs, which are predators of other nematode groups. To obtain a comprehensive view of the potential prey/food availability, we also quantified the abundance of soil insects and nonpredatory nematodes and the root biomass in the experimental plots. We used structural equation modeling (SEM) to investigate possible pathways by which plant diversity and identity may affect EPN infectivity and the abundance of carnivorous non-EPNs. Heterorhabditis spp. infectivity and the abundance of carnivorous non-EPNs were not directly related to plant diversity or the proportion of legumes, grasses and forbs in the plant community. However, Steinernema spp. infectivity was higher in monocultures of Festuca rubra and Trifolium pratense than in monocultures of the other six plant species. SEM revealed that legumes positively affected Steinernema infectivity, whereas plant diversity indirectly affected the infectivity of Heterorhabditis EPNs via effects on the abundance of soil insects. The abundance of prey (soil insects and root-feeding, bacterivorous, and fungivorous nematodes) increased with higher plant diversity. The abundance of prey nematodes was also positively affected by legumes. These plant community effects could not be explained by changes in root biomass. Our results show that plant diversity and identity effects on belowground biota (particularly soil nematode community) can differ between organisms that belong to the same feeding guild and that generalizations about plant diversity effects on soil organisms should be made with great caution.
Community patterns of soil bacteria and nematodes in relation to geographic distance
Monroy, F. ; Putten, W.H. van der; Yergeau, E. ; Duyts, H. ; Mortimer, S.R. ; Bezemer, T.M. - \ 2012
Soil Biology and Biochemistry 45 (2012). - ISSN 0038-0717 - p. 1 - 7.
cooccurrence patterns - microbial communities - global diversity - chalk grassland - spatial scales - biogeography - ecology - microorganisms - biodiversity - gradient
Ecosystems consist of aboveground and belowground subsystems and the structure of their communities is known to change with distance. However, most of this knowledge originates from visible, aboveground components, whereas relatively little is known about how soil community structure varies with distance and if this variability depends on the group of organisms considered. In the present study, we analyzed 30 grasslands from three neighboring chalk hill ridges in southern UK to determine the effect of geographic distance (1–198 km) on the similarity of bacterial communities and of nematode communities in the soil. We found that for both groups, community similarity decayed with distance and that this spatial pattern was not related to changes either in plant community composition or soil chemistry. Site history may have contributed to the observed pattern in the case of nematodes, since the distance effect depended on the presence of different nematode taxa at one of the hill ridges. On the other hand, site-related differences in bacterial community composition alone could not explain the spatial turnover, suggesting that other factors, such as biotic gradients and local dispersal processes that we did not include in our analysis, may be involved in the observed pattern. We conclude that, independently of the variety of causal factors that may be involved, the decay in similarity with geographic distance is a characteristic feature of both communities of soil bacteria and nematodes.
Effects of native and exotic range-expanding plant species on taxonomic and functional composition of nematodes in the soil food web
Morriën, W.E. ; Duyts, H. ; Putten, W.H. van der - \ 2012
Oikos 121 (2012)2. - ISSN 0030-1299 - p. 181 - 190.
parasitic nematodes - climate-change - ammophila-arenaria - ecosystem function - natural enemies - diversity - communities - biodiversity - grasslands - tolerance
Due to climate warming, many plant species shift ranges towards higher latitudes. Plants can disperse faster than most soil biota, however, little is known about how range-expanding plants in the new range will establish interactions with the resident soil food web. In this paper we examine how the soil nematode community from the new range responds to range-expanding plant species compared to related natives. We focused on nematodes, because they are important components in various trophic levels of the soil food web, some feeding on plant roots, others on microbes or on invertebrates. We expected that range expanding plant species have fewer root-feeding nematodes, as predicted by enemy release hypothesis. We therefore expected that range expanders affect the taxonomic and functional composition of the nematode community, but that these effects would diminish with increasing trophic position of nematodes in the soil food web. We exposed six range expanders (including three intercontinental exotics) and nine related native plant species to soil from the invaded range and show that range expanders on average had fewer root-feeding nematodes per unit root biomass than related natives. The range expanders showed resistance against rather than tolerance for root-feeding nematodes from the new range. On the other hand, the overall taxonomic and functional nematode community composition was influenced by plant species rather than by plant origin. The plant identity effects declined with trophic position of nematodes in the soil food web, as plant feeders were influenced more than other feeding guilds. We conclude that range-expanding plant species can have fewer root-feeding nematodes per unit root biomass than related natives, but that the taxonomic and functional nematode community composition is determined more by plant identity than by plant origin. Plant species identity effects decreased with trophic position of nematodes in the soil food web.
|Climate change induced range expanding plants experience less belowground enemy impact
Morriën, W.E. ; Engelkes, T. ; Duyts, H. ; Putten, W.H. van der - \ 2010
In: Plant Population Biology: Crossing Borders, Nijmegen 13-15 May 2010, Netherlands. - Nijmegen : - p. 64 - 64.
Divergent composition but similar function of soil food webs of individual plants: plant species and community effects
Bezemer, T.M. ; Fountain, T. ; Barea, J.M. ; Christensen, S. ; Dekker, S.C. ; Duyts, H. ; Hal, R. van; Harvey, J.A. ; Hedlund, K. ; Maraun, M. ; Mikola, J. ; Mladenov, A.G. ; Robin, C. ; Ruiter, P.C. de; Scheu, H. ; Setälä, S. ; šmilauer, P. ; Putten, W.H. van der - \ 2010
Ecology 91 (2010)10. - ISSN 0012-9658 - p. 3027 - 3036.
microbial communities - diversity - stability - biodiversity - grassland - feedback - ecology - real - ecosystems - succession
Soils are extremely rich in biodiversity, and soil organisms play pivotal roles in supporting terrestrial life, but the role that individual plants and plant communities play in influencing the diversity and functioning of soil food webs remains highly debated. Plants, as primary producers and providers of resources to the soil food web, are of vital importance for the composition, structure, and functioning of soil communities. However, whether natural soil food webs that are completely open to immigration and emigration differ underneath individual plants remains unknown. In a biodiversity restoration experiment we first compared the soil nematode communities of 228 individual plants belonging to eight herbaceous species. We included grass, leguminous, and non-leguminous species. Each individual plant grew intermingled with other species, but all plant species had a different nematode community. Moreover, nematode communities were more similar when plant individuals were growing in the same as compared to different plant communities, and these effects were most apparent for the groups of bacterivorous, carnivorous, and omnivorous nematodes. Subsequently, we analyzed the composition, structure, and functioning of the complete soil food webs of 58 individual plants, belonging to two of the plant species, Lotus corniculatus (Fabaceae) and Plantago lanceolata (Plantaginaceae). We isolated and identified more than 150 taxa/groups of soil organisms. The soil community composition and structure of the entire food webs were influenced both by the species identity of the plant individual and the surrounding plant community. Unexpectedly, plant identity had the strongest effects on decomposing soil organisms, widely believed to be generalist feeders. In contrast, quantitative food web modeling showed that the composition of the plant community influenced nitrogen mineralization under individual plants, but that plant species identity did not affect nitrogen or carbon mineralization or food web stability. Hence, the composition and structure of entire soil food webs vary at the scale of individual plants and are strongly influenced by the species identity of the plant. However, the ecosystem functions these food webs provide are determined by the identity of the entire plant community. Read More: http://www.esajournals.org/doi/abs/10.1890/09-2198.1
Vertebrate herbivores influence soil nematodes by modifying plant communities
Veen, C.F. ; Olff, H. ; Duyts, H. ; Putten, W.H. van der - \ 2010
Ecology 91 (2010)3. - ISSN 0012-9658 - p. 828 - 835.
below-ground biota - microbial responses - grassland ecosystem - food-web - diversity - vegetation - nitrogen - defoliation - nutrients - patterns
Abiotic soil properties, plant community composition, and herbivory all have been reported as important factors influencing the composition of soil communities. However, most studies thus far have considered these factors in isolation, whereas they strongly interact in the field. Here, we study how grazing by vertebrate herbivores influences the soil nematode community composition of a floodplain grassland while we account for effects of grazing on plant community composition and abiotic soil properties. Nematodes are the most ubiquitous invertebrates in the soil. They include a variety of feeding types, ranging from microbial feeders to herbivores and carnivores, and they perform key functions in soil food webs. Our hypothesis was that grazing affects nematode community structure and composition through altering plant community structure and composition. Alternatively, we tested whether the effects of grazing may, directly or indirectly, run via changes in soil abiotic properties. We used a long-term field experiment containing plots with and without vertebrate grazers (cattle and rabbits). We compared plant and nematode community structure and composition, as well as a number of key soil abiotic properties, and we applied structural equation modeling to investigate four possible pathways by which grazing may change nematode community composition. Aboveground grazing increased plant species richness and reduced both plant and nematode community heterogeneity. There was a positive relationship between plant and nematode diversity indices. Grazing decreased the number of bacterial-feeding nematodes, indicating that in these grasslands, top-down control of plant production by grazing leads to bottom-up control in the basal part of the bacterial channel of the soil food web. According to the structural equation model, grazing had a strong effect on soil abiotic properties and plant community composition, whereas plant community composition was the main determinant of nematode community composition. Other pathways, which assumed that grazing influenced nematode community composition by inducing changes in soil abiotic properties, did not significantly explain variation in nematode community composition. We conclude that grazing-induced changes in nematode community composition mainly operated via changes in plant community composition. Influences of vertebrate grazers on soil nematodes through modification of abiotic soil properties were of less importance.
First record of Helicotylenchus varicaudatus Yuen, 1964 (Nematoda: Hoplolaimidae) parasitizing Ammophila arenaria (L.) Link in Portuguese coastal sand dunes
Schreck Reis, C. ; Vieira Dos Santos, M.C. ; Marais, M. ; A.Santos, M.S.N. de; Duyts, H. ; Freitas, H. ; Putten, W.H. van der; Abrantes, I.M.O. de - \ 2010
Phytopathologia Mediterranea 49 (2010)2. - ISSN 0031-9465 - p. 212 - 226.
new-zealand - tylenchida - steiner - evolution - region - soils
A spiral nematode, Helicotylenchus varicaudatus Yuen, 1964, parasitizing Ammophila arenaria (L.) Link, the dominant grass in the Portuguese coastal sand dunes, is reported from Portugal for the first time and raises to seven the number of Helicotylenchus species detected in Portugal. A redescription of the species, with illustrations, and light and scanning electron microscope images of both female and male specimens, is presented. The rDNA containing the internal transcribed spacer regions (ITS) of H. varicaudatus was analysed with ITS-RFLP using the restriction endonuclease Hinf I. Molecular data from the ribosomal small subunit (SSU) (18S) confirmed the identification
Soil microorganisms in coastal foredunes control the ectoparasitic root-feeding nematode Tylenchorchynchus ventralis by local interactions
Piskiewicz, A.M. ; Duyts, H. ; Putten, W.H. van der - \ 2009
Functional Ecology 23 (2009)3. - ISSN 0269-8463 - p. 621 - 626.
plant-parasitic nematodes - grass ammophila-arenaria - biological-control - marram grass - borne fungi - endoparasitic nematodes - systemic resistance - mycorrhizal fungi - clonal grass - l. link
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
Plant ectoparasitic nematodes prefer roots without their microbial enemies
Piskiewicz, A.M. ; Milliano, M.J.K. de; Duyts, H. ; Putten, W.H. van der - \ 2009
Plant and Soil 316 (2009)1-2. - ISSN 0032-079X - p. 277 - 284.
grass ammophila-arenaria - soil-borne fungi - parasitic nematodes - rotylenchulus-reniformis - meloidogyne-incognita - biological-control - coastal foredunes - feeding nematodes - clonal grass - community
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.
Interactions between root-feeding nematodes depend on plant species identity
Brinkman, E.P. ; Duyts, H. ; Putten, W.H. van der - \ 2008
Soil Biology and Biochemistry 40 (2008)9. - ISSN 0038-0717 - p. 2186 - 2193.
soil-borne fungi - ammophila-arenaria - parasitic nematodes - ectoparasitic nematodes - pratylenchus-neglectus - coastal foredunes - marram grass - diversity - growth - herbivores
Root-feeding nematodes play an important role in structuring the composition of natural plant communities. Little is known about the role of intra- and interspecific interactions in determining the abundance of root-feeding nematodes in natural ecosystems. We examined interactions between two ectoparasitic root-feeding nematodes on two plant species: a good host plant for both nematode species and a good host for only one of the nematodes. We tested the hypothesis that root herbivore competitiveness depends on host suitability and related the experimental results to field data. In a greenhouse, we added different densities of the nematodes Tylenchorhynchus microphasmis and Tylenchorhynchus ventralis to Ammophila arenaria (the good host for both) and Carex arenaria (a good host for T. microphasmis only). Addition of T. ventralis did not significantly affect multiplication of T. microphasmis on both plant species. In contrast, on A. arenaria, T. ventralis experienced interspecific competition. However, on C. arenaria, T. microphasmis facilitated multiplication of T. ventralis. To explain this effect, we studied systemic plant-mediated effects in a split-root experiment. Nematode addition to one root compartment did not significantly influence nematode multiplication in the other root compartment, irrespective of nematode species identity. Therefore, the observed nematode interactions were not related to induced changes in the roots. In a two-choice experiment we tested whether host suitability was related to root attractiveness. Both nematode species were attracted to seedlings of A. arenaria, but not to C. arenaria. The low multiplication of T. ventralis on C. arenaria could be related to poor attraction to the roots. However, the poor attraction of T. microphasmis cannot be related to poor host suitability. Adding T. ventralis reduced shoot biomass of A. arenaria more than T. microphasmis did, whereas for C. arenaria the effect was the reverse. The interaction of the two nematodes on A. arenaria and C. arenaria shoot biomass was insignificant. However, the effect on root biomass of A. arenaria was interactive; adding T. ventralis to plants with high inoculation densities of T. microphasmis further decreased root biomass. Adding T. microphasmis further decreased root biomass of plants inoculated with low levels of T. ventralis. Depending on host plant identity, interactions between root-feeding nematodes may lead to competition or facilitation. Our results suggest that facilitation by T. microphasmis contributes to persistence of T. ventralis on C. arenaria. Thus, the population dynamics of root-feeding nematodes is influenced both by host plant identity and the presence of other root-feeding nematodes.