Disrupting mycorrhizal mutualisms: a potential mechanism by which exotic tamarisk outcompetes native cottonwoods

Abstract

The disruption of mutualisms between plants and mycorrhizal fungi is a potentially powerful mechanism by which invasives can negatively impact native species, yet our understanding of this mechanism's role in exotic species invasion is still in its infancy. Here, we provide several lines of evidence indicating that invasive tamarisk (Tamarix sp.) negatively affects native cottonwoods (Populus fremontii) by disrupting their associations with arbuscular mycorrhizal (AM) and ectomycorrhizal (EM) fungi. At a field site in the early stages of tamarisk invasion, cottonwoods with tamarisk neighbors had reduced EM colonization and altered EM fungal community composition relative to cottonwoods with native neighbors, leading to reductions in EM propagule abundance in the soil beneath tamarisk. Similarly, AM colonization of cottonwoods was reduced with a tamarisk neighbor, but there were no significant changes in AM fungal spore communities or propagule abundance. Root colonization by nonmycorrhizal fungi, including potential pathogens, was higher in cottonwoods with tamarisk neighbors. A greenhouse experiment in which AM and EM inoculation and plant neighbor were manipulated in a fully factorial design showed that cottonwoods benefited from mycorrhizas, especially EM, in terms of shoot biomass when grown with a conspecific, but shoot biomass was similar to that of nonmycorrhizal controls when cottonwoods were grown with a tamarisk neighbor. These results are partially explained by a reduction in EM but not AM colonization of cottonwoods by a tamarisk neighbor. Tamarisk neighbors negatively affected cottonwood specific leaf area, but not chlorophyll content, in the field. To pinpoint a mechanism for these changes, we measured soil chemistry in the field and the growth response of an EM fungus (Hebeloma crustuliniforme) to salt-amended media in the laboratory. Tamarisk increased both NO3- concentrations and electrical conductivity 2.5-fold beneath neighboring cottonwoods in the field. Salt-amended media did not affect the growth of H. crustuliniforme. Our findings demonstrate that a nonnative species, even in the early stages of invasion, can negatively affect a native species by disrupting its mycorrhizal symbioses. Some of these changes in mycorrhizal fungal communities may remain as legacy effects of invasives, even after their removal, and should be considered in management and restoration efforts.

Arbuscular mycorrhizal colonisation of roots of grass species differing in invasiveness

“…Arbuscule occurence showed the same trend in the case of F. vaginata, whereas for S. borysthenica vesicle occurence was markedly lower in C. dactylon stands than in uninvaded habitats. Others also reported decreased mycorrhizal colonisation of plants near invaders (Stinson et al 2006, Zhang et al 2007, Meinhardt et al 2012. A possible mechanism responsible for our findings is explained by the degraded mutualist hypothesis, for which Bever et al (2010) suggested a conceptual model, namely that the dominant species inhibits the mutualists of the resident community.…”

“…For example, such a mechanism has been reported for the European Alliaria petiolata in North American forests (Stinson et al 2006, Hale et al 2011, but see Barto et al 2010). Alternatively, the soil microbial community may be changed indirectly via the mass effect of the invasive plant being non-mycorrhizal or having different AMF symbionts, hence local AMFs gradually attenuate (Niu et al 2007, van der Putten et al 2007, Vogelsang and Bever 2009, Meinhardt and Gehring 2012, Sanon et al 2012. Different AMF species may have different colonisation phenologies (see e.g.…”

Changes in soil microbial community and enzyme activity along an exotic plant Eupatorium adenophorum invasion in a Chinese secondary forest

“…Furthermore, these changes in soil communities usually promote the growth of invasive plants, yet inhibit native plant performance, mainly driven by the lack of soil pathogens to invasive plants in the new habitats [14,15], the preferential enrichment of microbial pathogens to native plants [16,17], or the inhibition of microbial mutualism with native plants [18][19][20].…”

Role and influence of soil microbial communities on plant invasion

“…A. petiolata reduced the diversity and abundance of AMF due to the production of allelochemicals (Roberts & Anderson, 2001). Another nonmycorrhizal exotic invasive plant species Tamarix retarded the growth of native plant Populus fremontii S. Watson by interrupting its mutualistic association with AM fungi and EMF (Meinhardt & Gehring, 2012). An invasive plant, Impatiens glandulifera Royle in a mixed deciduous forest had a negative effect on the mutualistic association between AM fungi and the native plant Acer pseudoplatanus L. (Ruckli et al, 2014).…”