Plant invasions alter soil biota and microbial activities: A global meta-analysis

Negesse, Zebene 1 ; Pan, Kaiwen2 ; Guadie, Awoke3 ; Justine, Meta 2 ; Azene, Belayneh2 ; Pandey, Bikram4 ; Wu, Xiaogang2 ; Sun, Xiaoming2 ; Zhang, Lin2

Published Mar 03, 2025 on Dryad. https://doi.org/10.5061/dryad.hhmgqnkq5

Data files

Mar 03, 2025 version files 187.76 KB

Datasets.csv

142.96 KB
README.md

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Abstract

Plant invasion is a major component of global environmental change that can significantly alter soil biota, which are essential for organic matter decomposition and nutrient cycling in terrestrial ecosystems. However, the particular linkage between invasive plants, soil biotas, and enzymatic activities remains unclear. Here, we conducted a comprehensive meta-analysis using 688 paired observations from 107 studies to evaluate to the impact of plant invasion on soil biota, enzymatic activities and nutrient cycling. Our results showed that plant invasion significantly reduced herbivores (45%), detritivores (27%) and omnivores (45%) abundance, while allelopathy, woody invaders and forest ecosystems significantly reduced predator abundance by 47, 46, and 32%, respectively. Invasive plants also slightly reduced bacterial and fungal biomass, but significantly increased arbuscular mycorrhizal fungal (AMF) biomass, MBC and MBN by 29, 19 and 32%, respectively. Moreover, invasive plants had inconsistent impact on the activities of C-decomposing enzymes, but invertase, phenol oxidase and β-glucosidase were found significantly higher in invaded than uninvaded sites. Invaded sites had significantly higher activities of N- and P-releasing soil enzymes ranged from 18 to 27% than uninvaded sites. Soil microbial biomass, N-mineralization, soil respiration, available (N, P) nutrients, NH₄⁺-N and nutrient stocks were all higher in invasive than native plants rhizosphere soils. Our findings suggest that invasive plants had negative impact on soil functional groups, however, they enhanced soil nutrient-releasing enzymes and soil available nutrients. This in turn accelerates nutrient cycling and promote the persistence and success of invasive plants.

Data for plant invasion effects on soil biota functional groups and microbial activities research project. The dataset includes authors name and year, invasive species, native plant species, growth forms, allelopathy and ecosystem types. In addition, response variables for plant invasion with control and treated data with mean, standard deviation and number of samples, geographic coordinates, continent and country included. Meta-analysis was conducted on soil biota functional groups, microbial activities and nutrient cycling to assess the effect-sizes of plant invasion on the response variables.

Contact: Zebene Negesse (zedalem12@gmail.com) with any questions. This manuscript has been published (14 Feb 2025):

Zebene Negesse, Kaiwen Pan, Awoke Guadie, Meta Francis Justine, Belayneh Azene, Bikram Pandey, Xiaogang Wu, Xiaoming Sun, Lin Zhang. Plant invasions alter soil biota and microbial activities: A global meta-analysis. Plant and Soil (2025).

Datasets and associated with this data files can be found here: http://doi:10.5061/dryad.hhmgqnkq5.

Dataset

This file contains data on invasive and native plants. All data were collected by the authors. Blank cells represent missing data.

Variable	Unit	Description
Continent	Categorical	representing different continents or global regions (e.g., Europe, Latin America, Africa, Asia, North America, Oceania).
Study site	Categorical	Location of the study, see detail in Table S1
Ecosystem type	Categorical	Forest and non-forest ecosystems invaded by invasive plants
Allelopathic	Categorical	Plants with allelopathy = Yes and Without allelopathy = No, see in detail which invasive plants have allelopathy, and which is not.
Growth form	Categorical	Woody = (Trees, shrubs); and non-woody = (herbs, grasses)
Land use types	Categorical	Representing different ways land is utilized by humans or nature, such as agriculture, forests, urban areas, and wetlands.
Country	Categorical	Representing different nations where the study is conducted
ln (LRR)	Dimensionless	Natural logarithm (Ln) of the response ratio (RR).
In (V)	Dimensionless	Natural logarithm (Ln) of the variance
Microbial biomass	µg biomass C/g soil	The total mass of living microorganisms (bacteria, fungi, archaea) in a given amount of soil.
Bacteria biomass	CFU/g	Single-celled microorganisms found in various environments, including soil, water, air, and living organisms
Fungal biomass	µg C/g soil	The total mass of living fungi (including mycorrhizal fungi and decomposers) in a given amount of soil.
AMF biomass	µg C/g soil	The total biomass of Arbuscular Mycorrhizal Fungi (AMF) in soil
Soil respiration	g CO₂/m²/day	The process by which soil microorganisms (bacteria, fungi, and other soil organisms) and plant roots break down organic material, releasing carbon dioxide (CO₂) into the atmosphere
Acid phosphatase	µmol p-NP/g soil/hr	An enzyme produced by soil microorganisms, plants, and fungi that catalyzes the hydrolysis of phosphate esters, releasing inorganic phosphate
Alkaline phosphatase	µmol p-NP/g soil/hr	An enzyme that catalyzes the hydrolysis of organic phosphate esters, releasing inorganic phosphate
Urease	µmol NH₃/g soil/hr	an enzyme that catalyzes the hydrolysis of urea into ammonia (NH₃) and carbon dioxide (CO₂)
Peroxidase	µmol phenol/g soil/hr	an enzyme involved in the breakdown of hydrogen peroxide (H₂O₂) and the oxidation of a variety of organic substrates in soil
Phenol oxidase	µmol guaiacol/g soil/hr	an enzyme that catalyzes the oxidation of phenolic compounds to quinones and involved in the decomposition of organic matter
N-nitrification	µmol NO₃⁻/g soil/hr	Nitrogen nitrification: Ammonia (NH₃) is converted to nitrite (NO₂⁻) through the action of ammonia-oxidizing bacteria (AOB) or ammonia-oxidizing archaea (AOA)
N-mineralization	µmol NH₄⁺/g soil/hr	Nitrogen mineralization: microbial process by which organic nitrogen (found in plant residues, animal remains, and other organic matter) is converted into inorganic forms such as ammonium (NH₄⁺), which is available for plant uptake
β-glucosidase	µmol glucose/g soil/hr	an enzyme produced by soil microorganisms (bacteria, fungi) that plays a key role in the breakdown of complex organic matter in soils, especially in cellulose and lignocellulosic compounds
Abundance of soil invertebrates	mg/m²	organisms, which include earthworms, nematodes, arthropods (e.g., beetles, ants), mollusks (e.g., snails), and microarthropods (e.g., mites)
Actinomycete biomass	µg/g	the total mass of actinomycetes present in the soil
MBC	mg C/kg soil	Microbial biomass carbon (MC): - the total amount of carbon contained in the living microbial biomass (bacteria, fungi, actinomycetes) within the soil
MBN	mg N/kg soil	Microbial biomass nitrogen (MBN): - the total amount of nitrogen contained in the living microbial biomass (bacteria, fungi, actinomycetes) within the soil
Cellulase	µmol glucose/g soil/hr	An enzyme that breaks down cellulose, the primary structural component of plant cell walls, into simpler sugars like glucose
Catalase	µmol O₂/g soil/min	An enzyme that breaks down hydrogen peroxide (H₂O₂) into water (H₂O) and oxygen (O₂)
Invertase	µmol glucose/g soil/hr	An enzyme that catalyzes the hydrolysis of sucrose into glucose and fructose
Acetyl Glucosamidase	µmol NAG/g soil/hr	An enzyme involved in the decomposition of chitin, a major component of fungal cell walls, insect exoskeletons, and some microbial structures
Polyphenol oxidase	µmol quinone/g soil/hr	An enzyme that catalyzes the oxidation of phenolic compounds into quinones, which subsequently polymerize into humic substances
Glycine amino peptidase	µmol glycine/g soil/hr	An enzyme involved in protein degradation and nitrogen cycling in soil
Abundance of Herbivores	g/m²	The population density or biomass of herbivorous soil organisms, including invertebrates such as nematodes, collembolans, mites, and insect larvae that feed on plant roots, fungi, or microbial biomass
Abundance of Omnivores	g/m²	The population density or biomass of omnivorous soil organisms, which feed on a mix of plant material, microbes, fungi, and other small invertebrates
Abundance of predators	g/m²	The number or biomass of organisms that primarily feed on other organisms (e.g., herbivores, omnivores, or other predators) in an ecosystem
Abundance of Decomposers	g/m²	The number or biomass of organisms that break down organic matter in the soil, recycling nutrients and playing a key role in nutrient cycling
Protease	µmol amino acid/g soil/hr	Enzymes that catalyze the breakdown of proteins into smaller peptides and amino acids
abundance of microbivores	g/m²	soil organisms that feed primarily on microorganisms, including bacteria, fungi, and algae
SD_Control	SI unit of the measured variable	Standard deviation of the mean in the control groups
N_Control	Dimensionless	Number of sample size (N) in the control groups
SD_Treatment	SI unit of the measured variable	Standard deviation of the mean in the treatment groups
N_Treatment	Dimensionless	Number of sample size (N) in the treatment groups
Native plant species	Categorical	Plant species native to the region and listed by their scientific names
Soil response variables	Categorical	Soil response variables = soil parameters used in the effect size calculations
Mean_Treatment	SI unit of each soil response variable	The mean value in the treatment groups
Mean_Control	SI unit of each soil response variable	The mean value in the control groups
Geographic coordinates	degrees (°), minutes ('), and seconds (")	Shows the precise location of the studies on Earth's surface using latitude (Northing, Southing) and longitude (Easting, Westing).
Invader plant species	Categorical	Plant species non-native to the area, invading and displacing the native plant communities
Land use type	Categorical	Describe how land is utilized by humans and natural processes
Forest vs non-forest	Categorical	Ecosystem types invaded by exotic plants are classified as forest (temperate, tropical, plantation) or non-forest (grasslands, agricultural lands) etc

Woody vs non-woody	Categorical	Plant growth forms are categorized as woody plants (trees, shrubs) or non-woody plants (grasses, herbs).
ES	Dimensionless	ES = represents effect sizes
Northing	degrees (°), minutes ('), and seconds (")	Shows the location of the study in the north
Easting	degrees (°), minutes ('), and seconds (")	Shows the location of the study in the east
Case study	Discrete variable	It represents the number of studies within one article (Example: analyzing one invasive plant with two native plants results in two case studies because each native plant interacts separately with the invasive species)

Description of the data and file structure

The datasets structured by extracting from peer-reviewed journal articles as follows:
We conducted a comprehensive search for peer-reviewed journal articles that assessed how soil functional groups, microbial compositions and enzymatic activities respond to plant invasion in terrestrial ecosystems using Web of Science and Google Scholars. For each pair of response variables in invasive (i) and native (n) plants, the log response ratio (LRR) was calculated based on mean values (X) as a measurement of effect size.
lnV= natural logarism of variance.

ln (RR) = ln (Xt/Xc), Where Xt and Xc , are the results of the means in the treatment and control group, respectively. We calculated the variance (VR) that related with the effects computed by:

ln (V)= (Sc^2)/(nc*Xc2)+(St^2)/(nt*Xt2), where St and Sc are the standard deviations of the experimental and control treatments, respectively, where as nt and nc are the data points of the experimental and control treatments, respectively.

Sharing/Access information

Data was derived from the following sources:

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Code/Software

All the effect size calculations used Metawin Version 3 software. The forest plots produced using GraphPad Prism software.

We selected peer-reviewed journal articles using Web of Science and Google Scholars and screened the identified records using Preferred Reporting Items for Systematic Review and Meta-analysis procedure (PRISMA). Primary studies that satisfied the following selection criteria were included: (1) studies specifically described the identities of invasive and native plants and investigated either in the field observational or experimental studies, (2) at least one of the soil functional groups, or microbial composition or enzymatic activity was measured simultaneously in the invasive and native plants using the PLFA method (Kong et al., 2011), (3) invaded sites and control or native plants were found in the same biotic and abiotic conditions, (4) the means and sample sizes of the selected variables were available or could be calculated from the related publications. In our meta-analysis, we only used the soil microbial community composition and structure, soil microbial biomass and their enzymatic activities measured with PLFAs, the most used method for microbial measurements (G. Zhang et al., 2019). We applied the following criteria to identify independent case studies: (1) If multiple independent pairs of invasive and native plants from different ecosystems were reported in the same article, we treated each pair as a separate case study that complied with other meta-analyses' criteria and (2) if the study article reported one native plant and two more invasive plants, each invasive-native combination was considered as a separate case study. The data presented in the form of figures were extracted by using webplotdigitizer 4 https://automeris.io/WebPlotDigitizer.

For each pair of response variables in invasive (i) and native (n) plants, the log response ratio (LRR) was calculated based on mean values (X) as a measurement of effect size (Bakbergenuly et al., 2020; Lajeunesse, 2011). The LRR is a unit-free index that estimates the size of the impact and its directions. The values of LRR = 0, showed no difference in the measured response variable between invasive and native plants, a negative value indicates that the invaded site has a lower value than the noninvaded sites and a positive value presents that the invaded site has a greater value than the noninvaded site (Luo et al., 2006). The effect of plant invasion was estimated (Eq. 1) using the succeeding natural LRR (Bakbergenuly et al., 2020).

---------------------------------------------------- (1)

Where and _,are the results of the means in the treatment and control group, respectively. We calculated the variance (VR) that related with the effects computed by Eq. 2: -

-------------------------------------------------------------------------- (2)

Where S_t and S_c are the standard deviations of the experimental and control treatments, respectively, where as and are the data points of the experimental and control treatments, respectively. The standard error of the log response ratio calculated (Eq. 3) as follows: -

SE (lnR)= ----------------------------------------------------------------------------- (3)

We used Eq. 4, the weighted mean response ratio (R++) to identify the overall effects of the experimental versus the control group treatments, respectively (Hedges et al., 1999).

---------------------------------------------------------------------- (4)

Where is the weighting factor, and are th data points in the th dataset in each category group, , and are the number of datasets and data points in each dataset, respectively, in the category groups. The SE of R₊₊ was calculated by Eq. 5: -

------------------------------------------------------------------ (5)