Soil-microorganism-mediated invasional meltdown in plants

Abstract

While most alien species fail to establish, some invade native communities and become widespread. Our understanding of invasion success is derived mainly from pairwise interactions between aliens and natives, while interactions among more than two species remain largely unexplored. Here, we experimentally tested whether and how a third plant species, either native or alien, affected the competitive outcomes between alien and native plants through its soil legacy. We first conditioned soil with one of ten species (six natives and four aliens) or without plants. We then grew on these 11 soils five aliens and five natives without competition, or with intra-or interspecific competition. We found that aliens were not more competitive than natives when grown on soil conditioned by other natives or on non-conditioned soil. However, aliens were more competitive than natives on soil conditioned by other aliens (that is, invasional meltdown). Soil conditioning did not change competitive outcomes by affecting the strength of competition between later plants. lnstead, soil conditioned by aliens pushed competitive outcomes towards later aliens by affecting the growth of aliens less negatively than that of natives. Microbiome analysis verified this finding, as we showed that the soil-legacy effects of a species on later species were less negative when their fungal endophyte communities were less similar, and that fungal endophyte communities were less similar between two aliens than between aliens and natives. Our study reveals invasional meltdown in multispecies communities and identifies soil microorganisms as a driver of the invasion success of alien plants.

Biogeography of global drylands

“…Plant–plant and plant–soil interactions are involved in macroecological processes, including range expansions (e.g. Zhang et al ., 2020), or plant evolution (e.g. Thorpe et al ., 2011), in many biomes worldwide.…”

“…Delavaux et al ., 2019). Conversely, if plant species manage to disperse far enough so as to escape their soil antagonists, they can outcompete their neighbors and successfully invade new habitats (Zhang et al ., 2020). Thus, existing empirical evidence leaves little doubt about the importance of plant–plant and plant–soil interactions in shaping species’ niches, and therefore in influencing dryland biodiversity and biogeographical patterns.…”

Increases in multiple resources promote plant invasion

“…This would tell us the competitive outcome between aliens and natives across different resource availabilities. ‘Competitive outcome’ here refers to which species will exclude or dominate over the other species at the end point for the community 25,26 . For example, an overall higher level of biomass production of alien species would indicate that aliens would dominate when competing with natives.…”

“…To determine the 'competitive outcome', i.e. which species will exclude or dominate over the other species at the end point for the community (Gibson et al 1999;Zhang et al 2020), one should ideally conduct a long-term experiment. Alternatively, one could vary the density of each species, which mimics the dynamics of species populations across time (space-for-time-substitution method; see Hart et al 2012;Zhang & van Kleunen 2019 for examples).…”

Widely naturalized species are not more promiscuous in the use of different nitrogen forms, but benefit more from inorganic nitrogen

“…The rise in the number of naturalized alien plant species still shows no sign of saturation (Seebens et al ., 2017) and is projected to increase from 2005 to 2050 by about 18 % (Seebens et al ., 2021). Concerns over the impacts of plant invasions have stimulated considerable interest in the mechanisms underlying plant invasions (van Kleunen et al ., 2010; Funk, 2013; Zhang et al ., 2020a; Zhang et al ., 2020b; Liu et al ., 2021). However, despite considerable progress in our understanding of invasions, it is still unclear why some alien plant species are more successful than others.…”