Plant invasion impacts on fungal community structure and function depend on soil warming and nitrogen enrichment

Abstract

The impacts of invasive species on biodiversity may be mitigated or exacerbated by abiotic environmental changes. Invasive plants can restructure soil fungal communities with important implications for native biodiversity and nutrient cycling, yet fungal responses to invasion may depend on numerous anthropogenic stressors. In this study, we experimentally invaded a long-term soil warming and simulated nitrogen deposition experiment with the widespread invasive plant Alliaria petiolata (garlic mustard) and tested the responses of soil fungal communities to invasion, abiotic factors, and their interaction. We focused on the phytotoxic garlic mustard because it suppresses native mycorrhizae across forests of North America. We found that invasion in combination with warming, but not under ambient conditions or elevated nitrogen, significantly reduced soil fungal biomass and ectomycorrhizal relative abundances and increased relative abundances of general soil saprotrophs and fungal genes encoding for hydrolytic enzymes. These results suggest that warming potentially exacerbates fungal responses to plant invasion. Soils collected from uninvaded and invaded plots across eight forests spanning a 4 °C temperature gradient further demonstrated that the magnitude of fungal responses to invasion was positively correlated with mean annual temperature. Our study is one of the first empirical tests to show that the impacts of invasion on fungal communities depends on additional anthropogenic pressures and were greater in concert with warming than under elevated nitrogen or ambient conditions.

Fungal community and functional responses to soil warming are greater than for soil nitrogen enrichment

“…We also measured fungal functional genes using a gene capture approach which allowed us to target specific aspects of fungal decomposition which may be sensitive to environmental change and linked to SOM chemistry at the molecular level. Warming at our study site has enhanced soil respiration by 30%-50% (Contosta et al, 2011) and reduced C storage by 35% (Anthony et al, 2020). Nitrogen additions have had ephemeral effects on soil respiration and no significant effect on soil C storage.…”

“…All remaining soil was dried at 105 C for 48 h for analysis of soil pH (10 g soil: 20 mL deionized water) and total soil organic C and N using dry combustion (Perkin Elmer 2400 Series II CHN, Waltham, MA). A summary of the edaphic responses to the treatments can be found in Anthony et al (2020).…”

“…Because warming in combination with N has shifted SOM chemistry to be more similar to the heated compared to the N addition plots (vandenEnden et al, 2021), we expected fungal functional gene changes in the heating  N plots to be more similar to heated plots and distinct from the N addition plots. Earlier studies on fungi at this site were performed on a subset of the experimental plots (i.e., control vs. heated only plots) during the initial study phase (Pec et al, 2021) and in the context of an encroaching nonnative plant (Wheeler et al, 2017;Anthony et al, 2020), but the sensitivities of soil fungi to long-term warming, N additions, and their combination independent of plant invasion have not been explicitly investigated.…”

Soil microbial communities are not altered by garlic mustard in recently invaded central Illinois forests

“…Temporal factors are likely to be more influenced by short-term patterns, like weather or plant phenology, than spatial factors potentially making them more susceptible to future global change (Balser et al 2010). Further research on short-term temporal patterns, like phenology or warming, in invasive species-microbiome interactions (Anthony et al 2020) is needed to further understand how microbial communities respond to invasive species and their environment over time. Improving understanding of spatial and temporal variation in microbially mediated invasion dynamics could help predict the spread of future invasions and their responses to global change.…”

The pioneer effect advantage in plant invasions: site priming of native grasslands by invasive grasses

“…Invaders' seed exudates and products of germination also can interfere with native seed germination directly by production of allelochemicals (Laterra and Bazzalo 1999). Such impacts can be magnified when soil microbial communities render allelochemicals either more toxic or more recalcitrant to degradation (reviewed by Inderjit and van der Putten 2010) and can be enhanced under stressors related to climate change (see Anthony et al 2020). Granivores may preferentially consume seeds of natives, with differential seed predation changing the composition of local plant communities in ways that may be difficult to detect over short timeframes or at a landscape scale (e.g., Connolly et al 2014).…”