Plant invasion alters community structure and decreases diversity of arbuscular mycorrhizal fungal communities

Highlights

• Plant invasion decreased arbuscular mycorrhizal (AM) fungal diversity.

• Plant invasion shifted composition of AM fungal communities.

• Invasion effect was independent of soil physico-chemical parameters.

Abstract

Invasive plants often pose serious threats to the natural biodiversity of invaded ecosystems and in this way are likely to alter ecosystem services. This applies to arbuscular mycorrhizal (AM) fungi, in which the invaders have been reported to modify community structure, which facilitates their further intrusion. Information as to the impact of such invasion on AM fungal communities is insufficient and therefore needed. In particular, little is known about how AM fungal communities shift in response to individual invasive species. To ascertain whether invasion changes the structure of indigenous AM fungal communities, we examined changes in AM fungal community composition and diversity in soil and in roots of native neighboring plants in response to incursion of five invasive plant species from the family Asteraceae: Conyza canadensis, Erigeron annuus, Echinops sphaerocephalus, Solidago canadensis, and Symphyotrichum novi-belgii. We found that invasions of tested invasive plant species altered composition of the AM fungal community and reduced the diversity of AM fungi in soil and in the roots of some native plants. Statistical significance of the invasions' effects depended on composition of AM fungal communities in roots of the native plant species and/or site and was not connected with changes in soil parameters. Our results confirm the notable influence of plant invasion on indigenous AM fungal biodiversity and the need for further study in various environmental conditions.

Introduction

Biodiversity generally characterizes the quality of natural ecosystems (Rawal and Agarwal, 2015). It provides many of the environmental services and restoration processes necessary for functioning of the Earth's ecosystems, such as recycling of nutrients, preventing soil erosion, controlling local microclimate, regulating unwelcome organisms, and detoxifying noxious chemicals (Kazemi et al., 2018; Wall and Nielsen, 2012). The persistence of these services and processes therefore depends on the maintenance of biodiversity.

Biological invasions are among the most important factors threatening natural biodiversity (Mirek et al., 2010). Because biological invasions are assumed to occur due to globalization (Hulme, 2009; Meyerson and Mooney, 2007; Seebens et al., 2015), agriculture, and other human activities (Reichard and White, 2001), it is essential to know the effects of the invasion on biodiversity at all levels. The group of organisms significantly affected by the spread of alien plant species includes arbuscular mycorrhizal (AM) fungi, which are the most widespread and important plant symbionts (Mummey and Rillig, 2006; Tanner and Gange, 2013; Vogelsang and Bever, 2009).

These fungi live in mycorrhizal symbiosis with a large majority (>60%) of land plant species (Smith and Read, 2008; van der Heijden et al., 2015) and constitute a key functional group of soil biota (Smith and Read, 2008). AM fungi increase the acquisition of nutrients (Lekberg et al., 2010; Mäder et al., 2000; Řezáčová et al., 2018) and water (Allen, 2007), as well as growth and vitality of their host plants (Druege et al., 2006; Hart and Reader, 2002). They provide resistance to pathogens (Newsham et al., 1995; Vigo et al., 2000), increase tolerance to drought and osmotic stresses (Aroca et al., 2007; Augé et al., 2014, Augé et al., 2015), stabilize soil aggregates (Miller and Jastrow, 2000), and have been found to determine plant community composition and function (Smith and Read, 2008; van der Heijden et al., 1998). Shifts in AM fungal diversity caused by plant invasion may thus be detrimental to native plant species and further accelerate invasion (Reinhart and Callaway, 2006; Shah et al., 2009), adversely affecting plant diversity and productivity. Despite their importance, AM fungal communities have not been sufficiently studied in this context.

Although the influence of several invasive plant species on AM fungal communities has been investigated (e.g., Betekhtina et al., 2016; Busby et al., 2012; Dong et al., 2021; Hawkes et al., 2006; Mummey et al., 2005; Shah et al., 2015), the influence of most invasive species on the biodiversity of AM fungi, and especially in natural habitats, has not yet been investigated. Also neglected to date have been comparisons as to effects of multiple invader species.

Whether invasive plants stimulate or inhibit AM fungal diversity thus remains an open question. Non-mycorrhizal invasive plant species, such as Alliaria petiolata, may disrupt mutualistic associations between native plants (Stinson et al., 2006) and thus open the way for their further invasion at the cost of native species. The majority (ca 82%) of invasive plant species, however, are associated with AM fungi (Cronk and Fuller, 1995). Interaction of alien plant species with the indigenous soil subsystem in an invaded range may facilitate not only their own establishment and spread but also invasion by other plant species (Simberloff and von Holle, 1999). The “mutualist hypothesis,” on the other hand, suggests that invasive species are introduced concurrently with their native mutualistic partners, thereby enhancing their ability to survive in new habitats (Rodríguez-Echeverría, 2010). Given variability in the degree to which host plants influence specific AM fungi (Sanders and Fitter, 1992), we especially need to know how particular invasive species influence AM fungal communities in invaded soils.

Here, we investigated effects from invasion of five alien plant species of the family Asteraceae, namely Canadian horseweed Conyza canadensis (L.), annual fleabane Erigeron annuus (L.) Pers., great globe-thistle Echinops sphaerocephalus L., Canada goldenrod Solidago canadensis L., and New York aster Symphyotrichum novi-belgii (L.) G. L. Nesom., into central European seminatural plant communities on indigenous AM fungal diversity and community structure. E. sphaerocephalus is native to Asia and southern and eastern Europe, while all the other invasive species are of American origin. All five of these invasive species belong to the most abundant plant invaders in Central Europe. They all form arbuscular mycorrhiza (Gucwa-Przepiora et al., 2016; Majewska et al., 2018; Štajerová et al., 2009), but data showing impacts of their invasions on AM fungal communities are scarce. The impacts of E. annuus and S. novi-belgii invasions on AM fungal communities have not been investigated to date. In the case of E. sphaerocephalus, such investigation has been conducted only once, that being in a greenhouse experiment with a synthetic community consisting of only three species of AM fungi (Řezáčová et al., 2020b). Effect of the presence of S. canadensis on indigenous AM fungal communities has been the subject of more but not enough studies (Dong et al., 2021; Jin et al., 2004; Yang et al., 2014; Zhang et al., 2007, Zhang et al., 2010), and C. canadensis has been studied only twice in this regard (Shah et al., 2010, Shah et al., 2015). Moreover, Shah et al. (2015) characterized the diversity of AM fungi based on the morphology of spores, and that may have reduced the ability to detect rare taxa.

We test here the hypothesis that invasive plants are associated with generalist AM fungal taxa in the new habitat, and as abundant plant species in invaded plots, will thus decrease the diversity of AM fungal communities at invaded sites. Other tested hypothesis says that AM fungal diversity decreases with the decreasing diversity of domestic plant species, while shifting the structure of the indigenous AM fungal community. The specific objectives of the work were to (i) describe diversity of AM fungal communities of five invasive plant species, and (ii) examine the effect of invasion by the five invasive plants on the community structure and diversity of indigenous AM fungi in soil and in roots of neighboring native plants.