Can root-feeders alter the composition of AMF communities? Experimental evidence from the dune grass Ammophila arenaria

doi:10.1016/j.baae.2008.01.004

Basic and Applied Ecology

Volume 10, Issue 2, March 2009, Pages 131-140

https://doi.org/10.1016/j.baae.2008.01.004 Get rights and content

Abstract

Root herbivores and plant mutualists, such as arbuscular mycorrhizal fungi (AMF), have a significant effect on the structure and dynamic of plant communities. Nevertheless, the interactions between the two groups of organisms in natural ecosystems are far from understood. We carried out an inoculation experiment to examine the effect of two root herbivores, Pratylenchus penetrans and P. dunensis (Nematoda), on the composition of the AMF communities associated with two populations of the dune grass Ammophila arenaria. The outcome of the interaction in terms of plant and nematode performance was also analyzed. The total percentage of AMF colonization was not affected by the presence of root-feeders, but they did alter the composition of the AMF communities inside the roots. These changes were dependent on the root-feeder species and the original AMF community: the most severe alterations were observed in the mycorrhizal plants from Wales attacked by P. penetrans. Plant growth was impaired in plants from Wales inoculated with AMF and P. dunensis, which suggests a highly species-specific synergistic interaction with negative consequences for the plant. Root infection by the nematodes was reduced in all mycorrhizal plants when compared to non-mycorrhizal plants. However, a significant reduction of the final number of nematodes was observed only in the mycorrhizal plants from one population.

Zusammenfassung

Wurzelfresser und Pflanzenmutualisten, wie arbuskuläre Mykorrhizapilze (AMF), haben einen signifikanten Effekt auf die Struktur und Dynamik von Pflanzengesellschaften. Dennoch sind die Interaktionen zwischen den beiden Gruppen von Organismen in natürlichen Ökosystemen weit von einem Verständnis entfernt. Wir führten ein Inokulationsexperiment durch, um die Effekte von zwei Wurzelherbivoren, Pratylenchus penetrans und P. dunensis (Nematoda) auf die Zusammensetzung von AMF-Gesellschaften zu untersuchen, die mit zwei Populationen des Dünengrases Ammophila arenaria assoziiert waren. Das Ergebnis der Interaktionen in Bezug auf die Pflanzen- und Nematodenperformanz wurde ebenfalls analysiert. Die gesamte prozentuale Kolonisation durch AMF wurde durch die Anwesenheit der Wurzelfresser nicht beeinflusst. Sie veränderten jedoch die Zusammensetzung der AMF-Gesellschaften in den Wurzeln. Diese Änderungen hingen vom Wurzelfresser und der ursprünglichen AMF-Gesellschaft ab: die heftigsten Veränderungen wurden bei Mykorrhizapflanzen aus Wales festgestellt, die von P. penetrans befallen wurden. Das Pflanzenwachstum war bei Pflanzen aus Wales verringert, die mit AMF und P. dunensis inokuliert waren. Dies lässt eine sehr artspezifische synergistische Interaktion mit negativen Konsequenzen für die Pflanzen vermuten. Der Nematodenbefall war bei allen Pflanzen mit Mykorrhiza im Vergleich zu Pflanzen ohne Mykorrhiza reduziert. Eine signifikante Reduktion der endgültigen Anzahl der Nematoden wurde jedoch nur bei Pflanzen mit Mykorrhiza aus einer Population beobachtet.

Introduction

In the last 10 years, there has been an increased research effort to unravel the belowground complexity and to link it with aboveground ecology (Wardle et al., 2004). The interactions between plant roots and soil organisms have a significant effect on the structure and dynamic of both belowground and aboveground communities (Bever, Westover, & Antonovics, 1997; De Deyn et al., 2003; Van der Putten, Vet, Harvey, & Wackers, 2001; Wardle et al., 2004). Root-feeders, pathogens and plant mutualists coexist in the rhizosphere of plants and their interactions can lead to changes in the belowground community, which in turn affect plant performance and community structure (Bezemer et al., 2005; Van der Putten, Van Dijk, & Peters, 1993). Nevertheless, these belowground interactions and their ecological relevance in natural systems are far from being fully understood (Borowicz, 2006).

The role of root-feeders in the decline of Ammophila arenaria in coastal sand dunes is one of the best documented cases illustrating how soil biota affect aboveground processes in natural systems (Van der Putten, Maas, Van Gulik, & Brinkman, 1990). This is a good system for ecological studies on belowground interactions because of the large amount of data available on plant–soil interactions and soil diversity (Costa, Davies, Bardgett, & Kerry, 2003; de Rooij-van der Goes, 1995; Kowalchuk, Gerards, & Woldendorp, 1997; Rodriguez-Echeverria & Freitas, 2006; Van der Putten et al., 1990), and because the sandy soil is a relatively easy substrate for soil ecological studies. Initially, it was thought that root-feeding nematodes could play a significant role as belowground grazers in coastal sand dunes (Van der Putten et al., 1990). However, nematode abundance in the foredunes is usually low and subsequent work showed that root-feeding nematodes are strongly controlled in this soil (De Rooij-Van der Goes, 1995). Recent studies have demonstrated that a wide array of nematode control mechanisms can be found in the foredunes. Different root-feeding nematode species are ruled out by bottom-up processes (Van der Stoel & van der Putten, 2006), horizontal competition (Brinkman, Duyts, & van der Putten, 2005), plant mutualists (de la Peña, Rodriguez-Echeverria, van der Putten, Freitas, & Moens, 2006; Greipsson & El-Mayas, 2002; Hol, de la Peña, Moens, & Cook, 2007; Little & Maun, 1996) and/or natural enemies (Piśkiewicz, Duyts, Berg, Costa, & van der Putten, 2007). However, little is known about the effect of root-feeding nematodes on other rhizosphere organisms in natural systems. Among these, arbuscular mycorrhizal fungi (AMF) are the most likely to be affected by root herbivores because of the close relationship between them and plant roots.

AMF are ubiquitous plant mutualists which represent a large fraction of the fungal biomass of the rhizosphere. AMF are particularly beneficial for plants in sand dunes because they facilitate nutrient uptake in these low-fertility soils and play a key role in sand stabilization (Koske & Gemma, 1997). AMF can also act as mediators between plants and above and belowground herbivores (Brown & Gange, 2002). The outcome of this interaction depends mainly on the life history traits of the herbivore, the physiological status of the host plant and the composition of the AMF community (Hol & Cook, 2005). Different AMF species can have different effects on plant growth and chemistry and, therefore, on herbivore performance (Gange, Brown, & Aplin, 2005). In addition, the effect of mixtures of AMF species on herbivore performance can differ from the effects of single AMF (Gange, 2001). In terms of the consequences of the interaction for the AMF community, aboveground herbivory can reduce the extent of root colonization by the fungal mutualists (Gange, Bower, & Brown, 2002), although this effect seems to be species-specific (Klironomos, McCune, & Moutoglis, 2004). For belowground herbivores, de la Peña et al. (2006) showed that the root-feeding nematode Pratylenchus penetrans did not affect root colonization by AMF. Nevertheless, whether belowground herbivores also have differential effects on different fungal species is not clear yet (Borowicz, 2006). The composition of the AMF communities in natural systems is relevant for ecosystem dynamics because of the functional and physiological differences among AMF (Maherali & Klironomos, 2007). In the case of A. arenaria, distinctive AMF communities have been found in association with the plant roots in either different locations or dune succession stages (Blaszkowski, 1994; Kowalchuk, De Souza, & Van Veen, 2002; Rodriguez-Echeverria, Hol, Freitas, Eason, & Cook, 2007). Kowalchuk et al. (2002) also showed that the AMF communities associated with A. arenaria in healthy stands were different from those of degenerating plants, suggesting a link between plant performance, changes in the AMF community and changes in the populations of other rhizosphere organisms. When A. arenaria degenerates, it is replaced by later successional plant species (Van der Putten et al., 1993). Therefore, the causes that lead to changes in the AMF communities can have important consequences for the ecosystem.

In the present study, we tested the hypothesis that root-feeders can change the AMF community structure in the roots of the attacked plant. In order to test this hypothesis, we designed an experiment using two genetically different populations of A. arenaria (Rodriguez-Echeverria, Freitas, & van der Putten in press) inoculated with their native AMF communities, and two species of root-feeding nematodes, P. penetrans and P. dunensis, which occur frequently in the rhizosphere of A. arenaria (de la Peña, Karssen, & Moens, 2007). We discuss our results in relation to the dynamics of root herbivores and AMF communities in natural ecosystems and the aboveground consequences of this interaction.

Section snippets

Collection and preparation of plants, AMF and nematodes

Seeds of A. arenaria were collected in Ynyslas (Wales, UK) and Het Zwin Nature Reserve (Knokke, Belgium). Seeds were germinated in a glasshouse with a 16 h/8 h light/dark regime and 25 °C/16 °C day/night temperature on 2-mm-diameter glass beads with demineralized water. Two-week-old seedlings with 2-cm-tall shoots were used in the bioassays.

Soil was collected from the rhizosphere of four different A. arenaria plants in Het Zwin and Ynyslas to set up separate trap cultures of the AMF community with

Effect of AMF on the root-feeders

Root infection by nematodes was reduced from values of 70% in non-mycorrhizal plants to about 50% in mycorrhizal plants (Fig. 1A). The three-way ANOVA showed a significant effect of the presence of AMF on root colonization by nematodes (F_1,32=41.41, P<0.001) (Table 1, Fig. 1B). The two other factors considered in the analysis, origin of plant/AMF and identity of the herbivore species, did not have any significant effect on this variable (Table 1).

The final number of nematodes in all treatments

Discussion

The presence of AMF always reduced root infection by both nematode species, a result that agrees with previous data for P. penetrans (de la Peña et al., 2006). Nevertheless, the multiplication of the two nematode species was differently affected by AMF. One of the AMF communities only suppressed the generalist P. penetrans while the AMF from Wales impaired the reproduction of both root-feeding nematodes. Direct competition for space might be responsible for the suppression of root infection by

Acknowledgments

This study is part of the EcoTrain project (HPRN-CT 2002 00210) funded by the European Union. The authors thank Kris Struyf, curator of Het Zwin Nature Reserve, for allowing collection of samples. Eduardo de la Peña is a post doctoral fellow of the Flemish Science Foundation (FWO).

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In a diverse AMF community, abundance shifts among AMF species may occur that cancel each other out at the level of quantitative AMF measures. Similarly, Rodríguez-Echeverría, de la Peňa, Moens, Freitas, and van der Putten (2009) reported alterations in the composition of natural AMF communities in the presence of plant parasitic nematodes at unchanged levels of root colonization in Ammophila arenaria. Investigation of the AMF community composition was beyond the scope of this study, but shifts would potentially have affected plant performances (van der Heijden et al. 1998) and thus added to the effect of Agriotes herbivory.
Insect root herbivores can alter plant community structure by affecting the competitive ability of single plants. Our study aims at increasing knowledge on the impact of click beetle larvae (Elateridae, genus Agriotes) on grassland plant communities, by determining biomass responses as well as responses of the arbuscular mycorrhizal fungi (AMF) symbiosis to this widespread generalist root herbivore for eight common grassland plant species (Festuca rubra, Holcus lanatus, Poa pratensis, Achillea millefolium, Plantago lanceolata, Veronica arvensis, Medicago lupulina, Trifolium repens), belonging to three functional groups (grasses, herbs, legumes).
The presence of larvae in the rhizosphere of individual plants had an overall negative effect on root biomass, which varied in degree between plant species, with more root biomass being removed from larger root systems. The effect of larvae on shoot biomass, total plant biomass and shoot/root ratio also differed in strength between plant species. Relative changes in root and total plant biomass ranged from a 71% and 55% loss, respectively, in V. arvensis to an 11% and 1% increase in T. repens, but were not related to root- or plant size. Root colonization by AMF and the length of extraradical AMF hyphae were not affected by larvae. The plant's functional group did not determine the response of the plant to feeding by larvae. Growth of larvae was positively correlated with root biomass, but did not depend on plant species or group identity.
The results confirm the generalist nature of Agriotes spp. larvae, which depend on sufficient root quantity and are likely to feed most on those plant species whose roots are most abundant in their habitat. Their effect on the plant community may be generated through the ability of the respective plant species to cope with the herbivore damage, with tolerances being plant species rather than plant group specific.
Wurzelherbivore Insekten können die Struktur einer Pflanzengemeinschaft beeinflussen, indem sie die Konkurrenzstärke einzelner Pflanzen verändern. Diese Studie trägt zum Verständnis des Einflusses von Elateridenlarven (Coleoptera, genus Agriotes) auf Grünlandpflanzengemeinschaften bei, indem sie die Reaktion von typischen Grünlandpflanzen auf diesen weitverbreiteten Wurzelherbivoren untersucht. Im Einzelnen wurden Agriotes-Effekte auf ober- und unterirdische Biomassen sowie die Symbiose mit arbuskulären Mykorrhiza Pilzen (AMF) für acht Pflanzenarten (Festuca rubra, Holcus lanatus, Poa pratensis, Achillea millefolium, Plantago lanceolata, Veronica arvensis, Medicago lupulina, Trifolium repens) bestimmt, die drei verschiedenen funktionellen Gruppen angehören (Kräuter, Gräser, Leguminosen).
Die Anwesenheit von Agriotes-Larven im Wurzelraum individueller Pflanzen führte zu einer generellen Reduktion der Wurzelbiomasse. Der Grad der Reduktion variierte in Abhängigkeit von der Pflanzenspezies, und war höher für solche Spezies, die im Durchschnitt ein größeres Wurzelsystem hatten. Auch der Einfluss auf die Spross- und Gesamtbiomasse sowie das Spross/Wurzelverhältnis unterschied sich für die einzelnen Pflanzenspezies. Relative Änderungen der Wurzel- und Gesamtbiomasse reichten von einer 71%igen bzw. 55%igen Reduktion für V. arvensis bis zu einer 11%igen bzw. 1%igen Erhöhung für T. repens und waren unabhängig von der Pflanzengröße. Wurzelkolonisation durch AMF sowie die Länge der extraradikalen Hyphen der AMF wurden nicht beeinflusst. Auf dem Level der Pflanzengruppen beeinflussten die Larven keinen der gemessen Biomasse- oder AMF Parameter. Das Wachstum der Agriotes-Larven korrelierte positiv mit der Wurzelbiomasse, war aber unabhängig von der Identität der Pflanzenspezies oder–gruppe.
Die Ergebnisse bestätigen den generalistischen Charakter der Agriotes-Larven. Sie sind offenbar vor allem auf eine ausreichende Nahrungsmenge angewiesen und fressen vermutlich hauptsächlich von den Wurzeln, die in ihrem Habitat am abundantesten sind. Ihr Einfluss auf die Pflanzengemeinschaft ergibt sich somit aus der Toleranz der entsprechenden Pflanzenspezies gegenüber dem Wurzelherbivoren.
Molecular diversity of arbuscular mycorrhizal fungi associated with two dominant xerophytes in a valley-type savanna, southwest China
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The diversity of arbuscular mycorrhizal fungi (AMF) colonizing the roots and rhizosphere soils of Heteropogon contortus and Dodonaea viscose growing in a valley-type savanna, southwest China, were analyzed by the large subunit ribosomal RNA genes (LSU). A total of 547 AMF sequences were screened for establishment of four clone libraries. Phylogenetic analysis revealed that the sequences clustered in at least 8 discrete sequence groups, all belonging to the genus Glomus. Among the Glomus spp., Glo 1 (GlGr A) and Glo 7 (GlGr B) were the most common in all root and soil samples of the two xerophytes, accounting for 42% and 33% of all screened clones, respectively. The ∫-LIBSHUFF analysis revealed that the composition of AMF communities associated with the two xerophytic hosts varied greatly both in roots and their rhizosphere soils.

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Can root-feeders alter the composition of AMF communities? Experimental evidence from the dune grass Ammophila arenaria

Abstract

Zusammenfassung

Introduction

Section snippets

Collection and preparation of plants, AMF and nematodes

Effect of AMF on the root-feeders

Discussion

Acknowledgments

Basic and Applied Ecology

Applied Soil Ecology

Soil Biology and Biochemistry

Trends in Ecology & Evolution

Applied Soil Ecology

Diversity and ecology of soil fungal communities: Increased understanding through the application of molecular techniques

Environmental Microbiology

Staining nematodes and arbuscular mycorrhizae in the same root sample

Fundamental and Applied Nematology

Incorporating the soil community into plant population dynamics: The utility of the feedback approach

Journal of Ecology

Soil community composition drives aboveground plant-herbivore-parasitoid interactions

Ecology Letters

Arbuscular fungi and mycorrhizae (Glomales) of the Hel Peninsula, Poland

Mycorrhiza

Do arbuscular mycorrhizal fungi alter plant–pathogen relations?

Ecology

When enemies attack do plants get by with a little help from their friends?

New Phytologist

Consequences of variation in species diversity in a community of root-feeding herbivores for nematode dynamics and host plant biomass

Oikos

Tritrophic below- and above-ground interactions in succession

Soil invertebrate fauna enhances grassland succession and diversity

Nature

Diversity and distribution of root-lesion nematodes (Pratytlenchus spp.) associated with Ammophila arenaria L. (Link) in coastal dunes of Western Europe

Nematology

Mycorrhizal fungi control migratory endoparasitic nematodes in Ammophila arenaria

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The role of plant-parasitic nematodes and soil-borne fungi in the decline of Ammophila arenaria (L) Link

New Phytologist

Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant

New Phytologist

Differential effects of insect herbivory on arbuscular mycorrhizal colonization

Oecologia