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Whole community invasions and the integration of novel ecosystems.

ABSTRACT: The impact of invasion by a single non-native species on the function and structure of ecological communities can be significant, and the effects can become more drastic-and harder to predict-when multiple species invade as a group. Here we modify a dynamic Boolean model of plant-pollinator community assembly to consider the invasion of native communities by multiple invasive species that are selected either randomly or such that the invaders constitute a stable community. We show that, compared to random invasion, whole community invasion leads to final stable communities (where the initial process of species turnover has given way to a static or near-static set of species in the community) including both native and non-native species that are larger, more likely to retain native species, and which experience smaller changes to the topological measures of nestedness and connectance. We consider the relationship between the prevalence of mutualistic interactions among native and invasive species in the final stable communities and demonstrate that mutualistic interactions may act as a buffer against significant disruptions to the native community.

SUBMITTER: Campbell C

PROVIDER: S-EPMC9173635 | biostudies-literature | 2022 Jun

REPOSITORIES: biostudies-literature

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Whole community invasions and the integration of novel ecosystems.

Campbell Colin C Russo Laura L Albert Réka R Buckling Angus A Shea Katriona K

PLoS computational biology 20220607 6

The impact of invasion by a single non-native species on the function and structure of ecological communities can be significant, and the effects can become more drastic-and harder to predict-when multiple species invade as a group. Here we modify a dynamic Boolean model of plant-pollinator community assembly to consider the invasion of native communities by multiple invasive species that are selected either randomly or such that the invaders constitute a stable community. We show that, compared ...[more]

PMID: 35671270

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Project description:BackgroundCommunity-driven invasion, also known as community coalescence, occurs widely in natural ecosystems. Despite that, our knowledge about the process and mechanisms controlling community-driven invasion in soil ecosystems is lacking. Here, we performed a set of coalescence experiments in soil microcosms and assessed impacts up to 60 days after coalescence by quantifying multiple traits (compositional, functional, and metabolic) of the invasive and coalescent communities.ResultsOur results showed that coalescences significantly triggered changes in the resident community's succession trajectory and functionality (carbohydrate metabolism), even when the size of the invasive community is small (~ 5% of the resident density) and 99% of the invaders failed to survive. The invasion impact was mainly due to the high suppression of constant residents (65% on average), leading to a lose-lose situation where both invaders and residents suffered with coalescence. Our results showed that surviving residents could benefit from the coalescence, which supports the theory of "competition-driven niche segregation" at the microbial community level. Furthermore, the result showed that both short- and long-term coalescence effects were predicted by similarity and unevenness indexes of compositional, functional, and metabolic traits of invasive communities. This indicates the power of multi-level traits in monitoring microbial community succession. In contrast, the varied importance of different levels of traits suggests that competitive processes depend on the composition of the invasive community.ConclusionsOur results shed light on the process and consequence of community coalescences and highlight that resource competition between invaders and residents plays a critical role in soil microbial community coalescences. These findings provide valuable insights for understanding and predicting soil microbial community succession in frequently disturbed natural and agroecosystems. Video Abstract.

Project description:Microbial probiotics are intended to improve functions in diverse ecosystems, yet probiotics often fail to establish in a preexisting microbiome. This is a species invasion problem. The relative importance of the two major factors controlling establishment in this context-propagule pressure (inoculation dose and frequency) and biotic interactions (composition of introduced and resident communities)-is unknown. We tested the effect of these factors in driving microbial composition and functioning following 12 microbial community invasions (e.g., introductions of many microbial invaders) in microcosms. Ecosystem functioning over a 30-day postinvasion period was assessed by measuring activity (respiration) and environment modification (dissolved organic carbon abundance). To test the dependence on environmental context, experiments were performed in two resource environments. In both environments, biotic interactions were more important than propagule pressure in driving microbial composition and community function, but the magnitude of effect varied by environment. Successful invaders comprised approximately 8% of the total number of operational taxonomic units (OTUs). Bacteria were better invaders than fungi, with average relative abundances of 7.4% ± 6.8% and 1.5% ± 1.4% of OTUs, respectively. Common bacterial invaders were associated with stress response traits. The most resilient bacterial and fungal families, in other words, those least impacted by invasions, were linked to antimicrobial resistance or production traits. Illuminating the principles that determine community composition and functioning following microbial invasions is key to efficient community engineering.IMPORTANCE With increasing frequency, humans are introducing new microbes into preexisting microbiomes to alter functioning. Example applications include modification of microflora in human guts for better health and those of soil for food security and/or climate management. Probiotic applications are often approached as trial-and-error endeavors and have mixed outcomes. We propose that increased success in microbiome engineering may be achieved with a better understanding of microbial invasions. We conducted a microbial community invasion experiment to test the relative importance of propagule pressure and biotic interactions in driving microbial community composition and ecosystem functioning in microcosms. We found that biotic interactions were more important than propagule pressure in determining the impact of microbial invasions. Furthermore, the principles for community engineering vary among organismal groups (bacteria versus fungi).

Project description:The importance of plant-microbe associations for the invasion of plant species have not been often tested under field conditions. The research sought to determine patterns of change in microbial communities associated with the establishment of invasive plants with different taxonomic and phenetic traits. Three independent locations in Virginia, USA were selected. One site was invaded by a grass (Microstegium vimineum), another by a shrub (Rhamnus davurica), and the third by a tree (Ailanthus altissima). The native vegetation from these sites was used as reference. 16S rRNA and ITS regions were sequenced to study root-zone bacterial and fungal communities, respectively, in invaded and non-invaded samples and analyzed using Quantitative Insights Into Microbial Ecology (QIIME). Though root-zone microbial community structure initially differed across locations, plant invasion shifted communities in similar ways. Indicator species analysis revealed that Operational Taxonomic Units (OTUs) closely related to Proteobacteria, Acidobacteria, Actinobacteria, and Ascomycota increased in abundance due to plant invasions. The Hyphomonadaceae family in the Rhodobacterales order and ammonia-oxidizing Nitrospirae phylum showed greater relative abundance in the invaded root-zone soils. Hyphomicrobiaceae, another bacterial family within the phyla Proteobacteria increased as a result of plant invasion, but the effect associated most strongly with root-zones of M. vimineum and R. davurica. Functional analysis using Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) showed bacteria responsible for nitrogen cycling in soil increased in relative abundance in association with plant invasion. In agreement with phylogenetic and functional analyses, greater turnover of ammonium and nitrate was associated with plant invasion. Overall, bacterial and fungal communities changed congruently across plant invaders, and support the hypothesis that nitrogen cycling bacteria and functions are important factors in plant invasions. Whether the changes in microbial communities are driven by direct plant microbial interactions or a result of plant-driven changes in soil properties remains to be determined.

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Whole community invasions and the integration of novel ecosystems.

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Whole community invasions and the integration of novel ecosystems.

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