A case study of soil food web components affected by Fallopia japonica (Polygonaceae) in three natural habitats in Central Europe

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A case study of soil food web components affected by Fallopia japonica (Polygonaceae) in three natural habitats in Central Europe

Andrea Čerevková * / Lenka Bobuľská / Dana Miklisová / Marek Renčo

Keywords : Fallopia japonica , Soil physical properties, Microbial activity, Soil nematode communities, Ecology

Citation Information : Journal of Nematology. Volume 51, Pages 1-16, DOI: https://doi.org/10.21307/jofnem-2019-042

License : (CC-BY-4.0)

Received Date : 08-October-2018 / Published Online: 23-July-2019

ARTICLE

ABSTRACT

This study determined the effect of the invasive plant Fallopia japonica on soil physical properties, microbial respiration, microbial biomass carbon content, enzymatic activities, and soil nematode communities. We established in total 30 plots in three natural habitats (forest, grassland, wetland) that were either uninvaded or mostly monospecifically invaded by F. japonica. The soil physical and microbial properties differed among the investigated plots, but the differences were observed to be non-significant between the invaded and the uninvaded plots. Non-metric multidimensional scaling based on nematode species diversity indicated that the total number of identified nematode species and their abundance were higher in the uninvaded compare to the invaded plots. Negative effect of F. japonica on omnivores, plant parasites, and root-fungal feeder nematodes was confirmed by their lower abundance in the invaded compared to the uninvaded plots. In the invaded plots, we also confirmed lower Maturity and Channel index, but higher Enrichment index. Our results thus indicated that the invasive plant F. japonica could affect nematode communities, more than physical or microbial properties, regardless of habitat.

Graphical ABSTRACT

The impact of invasive plants on soil ecosystems in the last decades has attracted world-wide attention. Exotic plant invasions often have dramatic impacts on the resident vegetation by modifying its composition and structure (Levine et al., 2003). Invasive plants have been reported to alter abiotic properties (Rahmonov et al., 2014; Suseela et al. 2016; Stefanowicz et al., 2017), nutrient availability, organic carbon content (Bardon et al., 2014), soil microbiota (Scharfy et al., 2010; Coats and Rumpho, 2014), and soil mesofauna (Quist et al., 2014; Sterzyńska et al., 2017), with special references to variability and composition of arthropods (Moroń et al., 2009; Lenda et al., 2013; Baranová et al., 2014).

The clonal Japanese knotweed, Fallopia japonica (Houtt.) Ronse Decr., is considered to be one of the 100 worst invasive alien species in the world (Lowe et al., 2000). It was introduced into North America and Europe in the nineteenth century as an ornamental plant (Bailey and Conolly, 2000) and cattle fodder (Beerling et al., 1994). F. japonica produces a large amount of biomass and form monospecific stands that can have a major impact on ecosystem functions (Mincheva et al., 2014) and on soil biodiversity (Beerling et al., 1994; Muller, 2004). Most of the previous studies on F. japonica have focused on methods for their control and eradication (Kabat et al., 2006), effects on natural plants (Aguilera et al., 2010), changes in soil chemical properties (Dassonville et al., 2007), allelopathic effects in experimental conditions (Dommanget et al., 2014), or impact on invertebrate species richness (Beerling and Dawah, 1993; Gerber et al., 2008), but the responses of soil microbial or nematode communities on invasion by Fallopia spp. are largely understudied. Dassonville et al. (2010) found that Fallopia spp. decreased potential denitrification enzyme activity by reducing soil moisture, denitrifying bacteria density in the soil and potential ammonia and nitrite oxidizing bacteria enzyme activities. Fallopia spp. have also been shown to produce antimicrobial and antifungal substances (Kim et al., 2005; Kumaga et al., 2005) that could affect the soil bacterial community.

Soil nematodes are an important group of soil biota, constituting an essential trophic link between primary decomposers, such as soil microflora, and larger animals and are recognized as useful bioindicators of soil conditions (Ritz et al., 2009) due to their abundance, diversity, and trophic structure (Bongers, 1990; Yeates et al., 2009). Root tissues and soil microorganisms such as bacteria and fungi represent a primary energy sources for nematode communities, and the quantitative variation of these resources may affect the structural and trophic diversity of nematode communities (Biederman and Boutton, 2009; Ciobanu et al., 2015). Different ecosystems have specific compositions of soil microbial and nematode communities. Estimating the status of and related changes in the structures of microbes and soil nematode communities after the establishment of the invasive plant F. japonica must thus include the assessment of different habitats (Renčo and Baležentiené, 2011). For this case study, we chose three habitats (forest, grassland, and wetland) and adjacent territories invaded by F. japonica in a valley in Central Europe (Slovakia) to confirm or reverse the effect of F. japonica on selected food web components.

To our knowledge, this is the first study observing the impact of F. japonica on the soil microbial and nematode community structure. Our objectives were to (i) determine the impact of F. japonica on soil pH and moisture, soil microbial respiration, soil microbial biomass carbon content, enzymatic activities and (ii) compare the abundance, diversity, trophic structure of nematode communities and selected ecological indices in three different habitats in F. japonica, the invaded and the uninvaded plots. The hypothesis tested was that soil physical properties, microbial, and nematode communities change when the ecosystem is disrupted by the invasion.

Material and methods

Study area

The experiment was conducted in a valley near the village of Opátka in South Eastern Slovakia, Central Europe. This region has a temperate climate, with an annual average of 40 summer days per year and a warm, moderately dry sub-region with a mild winter. The average daily temperature in January ranges from 1.5 to 4.0°C, the average daily temperature in July ranges from 16.0 to 18.5°C, while the average annual temperature ranges from 5.0 to 7.0°C. The mean annual precipitation is 650 to 700 mm. The soils are characterized as Fluvisols, and the vegetation zone is characterized as Carpathian oak-hornbeam forest. The landscape is patchy, with deeply undulating uplands (Miklós, 2002). The first F. japonica specimens appeared in the village of Opátka around 1992 (personal communication with forester of the cadastre). It was later probably transferred to the entire valley (7 km) below the village, invaded the banks of the creek and then spread to adjacent habitats thus creating large monocultures.

For studying the impact of F. japonica on soil physical properties, microbial, and soil nematode communities, we selected three habitats in the valley, namely, forest, grassland, and wetland and corresponding areas adjacent to them invaded by F. japonica.

Forest (F) (48°47.63′N, 21°03.43′E; 455 m a.s.l.): covered by a natural, undisturbed, 100 years old deciduous Querco-Fagetea forest, mainly consisting of Quercus robur, Q. cerris, Carpinus betulus, Acer campestre, and many shrub species such as mostly Viburnum sp. and Prunus spinosa.

Forest edge invaded by F. japonica (FF): a nearly monospecific stand of F. japonica covering an area of 500 m2, with an estimated time of invasion of 15 years.

Grassland (G) (48°48.14′N, 21°03.40′E; 392 m a.s.l.): covered with indigenous multispecies vegetation dominated by Dactylis glomerata, Lolium perenne, Trifolium pratense, and Achillea millefolium; irregularly mown.

Grassland edge invaded by F. japonica (GF): an adjacent of F. japonica covering an area of 250 m2, with an estimated time of invasion of 15 years.

Wetland (W) (48°48.34′N, 21°03.35′E; 386 m a.s.l.): covered by Petasites hybridus, Caltha palustris, Galium aparine, Equisetum sp., Ranunculus sp., and Urtica sp.; the soil is regularly flooded mostly in the spring, and the vegetation is mown once a year in the autumn.

Wetland edge invaded by F. japonica (WF): an adjacent area of 200 m2, with an estimated time of invasion of 10 years, the soil is regularly flooded mostly in the spring.

We selected a 25 m × 25 m area of the three different habitats (F, G, and W) which was not yet colonized by F. japonica. The distance between F, G, and W along the valley was approximately 1,500 m. A pair of the invaded and the uninvaded areas which did not differ in elevation, inclination, exposition, or management were chosen and the distance between the invaded and the uninvaded areas was 50 m. In each invaded area, we installed five randomly chosen 1 × 1 m plots (approx. 10 m apart) which had similar cover of F. japonica. Similar, five 1 × 1 m plots with random distribution were installed in corresponding uninvaded F, G, and W areas. This resulted in 30 plots (five plots × two invasion state [invaded and uninvaded] × three habitats [F, G, and W]). The uninvaded areas were assumed to represent the situation prior to the invasion of F. japonica.

Sampling procedure

The soils were sampled using a garden trowel to depths of 0 to 20 cm in May 2016. A quadrat sampling method was used. Five soil subsamples were collected from each quadrat (1 m2), one from each corner and one from the center. The subsamples from each quadrat were then bulked to obtain five representative soil samples (1 kg) for each area. The soil samples were transferred to the laboratory in plastic bags. The bags were stored at 5°C until processing (storage time of soil samples were no longer than one week). Each sample was gently homogenized manually before processing

Soil physical properties

Soil pH was determined for air-dried soil samples in a 1:3 solution of soil: 0.01 M CaCl2 using a pH meter inoLab pH 720-WTW GmbH, Weilheim, Germany. Soil moisture content was measured gravimetrically after the soil had been dried to a constant weight in an oven at 105°C for 24 hr. All determinations were performed in triplicate.

Soil microbial properties

Soil microbial respiration (SMR) was measured by the amount of CO2 released from 100 g of field-moist soil and absorbed by NaOH (μg C-CO2/g soil) in hermetically sealed bottles (Alef and Nannipieri, 1995) at 25°C for 24 hr. Microbial biomass carbon (MBC) content was determined using the method of Islam and Weil (1998), as oven-dried equivalent (ODE) of field-moist soil adjusted to 80% water-filled porosity was irradiated twice by microwave (MW) energy at 400 J g-1 ODE soil to kill the microorganisms. The time settings and MW oven power depended on the total amount of soil in the MW oven. After cooling, soil samples were extracted with 0.5 M K2SO4. Carbon content (Cirradiated) in the extract was quantified by the oxidation with K2Cr2O7 dissolved in H2SO4 and titrimetrically by (NH4)2Fe(SO4)2. The same procedure was done with a non-irradiated sample (Cnon-irradiated). The microbial biomass carbon was then determined as MBC = (Cirradiated-Cnon-irradiated)/KME, whereby extraction efficiency factor KME = 0.213. The activities of acid and alkaline phosphatase were determined by the modified method of Grejtovský (1991) using p-nitrophenyl phosphate as a substrate with incubation at 37°C for 24 hr. Urease activity was determined using urea as a substrate with incubation at 37°C for 3 hr as described by Chazijev (1976), and invertase activity was determined using sucrose as a substrate with incubation at 37°C for 24 hr as described by Schinner and Vonmersi (1990). The control measurements for enzymatic activity did not use the substrate. The activity of all enzymes was measured spectrophotometrically by create a reference curve.

Nematode extraction and identification

Nematodes were isolated from 100 g of the mixed fresh soil samples by a combination of Cobb sieving and decanting (Cobb, 1918) and a modified Baermann techniques (Van Bezooijen, 2006). Nematodes were extracted from aqueous soil suspensions using a set of two cotton-propylene filters. Subsamples were removed after extraction for 48 hr at room temperature. The aqueous suspensions containing nematodes were examined under a stereomicroscope, excessive water was removed, and the nematodes were fixed in hot fixative 99:1 solution of 4% formaldehyde: pure glycerol and evaluated on permanent glycerine slides (Southey, 1986). All isolated nematodes were microscopically examined at 100, 200, 400, 600, and 1,000 × magnification, identified from permanent glycerine slides mostly to species level (juveniles were identified to genus level) using an Eclipse 90i Nikon, Japan light microscope, with original species descriptions, and several taxonomic keys: Brzeski (1998), Loof (1999), Siddiqi (2000), Andrássy (2005, 2007, 2009), and Geraert (2008, 2010).

Cysts of Heterodera juveniles were extracted by floatation (Sabová and Valocká, 1980) from 100 g of soil for species identification based on morphological markers and morphometric data for both cysts and juveniles.

Nematode community analysis and ecological and functional indices

Nematode species were assigned to trophic groups: bacterivores, fungivores, omnivores, predators, plant parasites, root-fungal feeders, and insect parasites, according to Yeates et al. (1993) and Wasilewska (1997).

The total number of species, total nematode abundance, mean number of nematodes per trophic group, and the Shannon and Weaver species diversity index (H’spp.) (Shannon and Weaver, 1949) were determined. Basic ecological indices were used to assess the status of the soil habitats using nematode communities. The maturity index (MI) for free-living taxa and the plant parasite index (PPI) for plant-parasitic taxa (Bongers, 1990), the enrichment (EI), structural (SI), channel (CI) (Ferris et al., 2001), and basal (BI) indices (Berkelmans et al., 2003) were calculated using the online program ‘NINJA: An automated calculation system for nematode-based biological monitoring’ (Sieriebriennikov et al., 2014; http://spark.rstudio.com/bsierieb/ninja).

Statistical analysis

The differences in nematode characteristics (total nematode abundance, abundance of nematodes per trophic group, and species diversity) and basic ecological characteristics (MI, PPI, EI, SI, CI, and BI) were analyzed with two-way ANOVA with ‘ecosystems’ (F, G, and W), ‘invasion status’ (invaded, uninvaded), and their interactions as factors. To meet the assumptions of these parametric tests, Box-Cox transformation was applied with the maximum likelihood approach and Golden Search iterative procedure on. If there was an interaction between ‘ecosystem’ and ‘invasion status’ (total nematode abundance and mean number of bacterivores), post hoc Fisher LSD test was applied separately for each ecosystem to determine the effect of ‘invasion status’. Otherwise, main factor ANOVA with two factors (without interaction) was applied. Consequently, in the case of confirmed significance of ‘ecosystem’, post hoc Fisher LSD test was used.

As untransformed soil physical and microbial properties (pH, SMR, MBC content, and enzymatic activities) were not normally distributed (Shapiro–Wilk test) and transformation did not improve normality, nonparametric statistics were applied. Differences among six combinations of ‘ecosystem’ and ‘invasion status’ were tested separately with Kruskal–Wallis ANOVA, followed by a post hoc multiple comparisons.

The above mentioned statistical analysis were performed using Statistica Cz, version 12.0 (Statsoft, Inc., 2013) and significance of all tests was determined at p<0.05, 0.01, and 0.001.

Relationships between plots, nematodes, and selected environmental characteristics (soil pH and soil microbial respiration as constrained variables) were analyzed by ordination techniques. Redundancy analysis (RDA) was performed using Canoco 5 (Ter Braak and Šmilauer, 2012), because response data were compositional and had a gradient of 1.7 standard deviations. The significance of the axis was tested by a Monte Carlo permutation test.

Non-metric multidimensional scaling (NMS) ordination was used to examine any changes in the structure of nematode community for the invaded and the uninvaded habitats. A three-dimensional solution was executed by Autopilot, with the slow and thorough mode and Sørensen (Bray-Curtis) distance (recommended for community data). PC-ORD (McCune and Grace, 2002; McCune and Mefford, 2011) was used for the NMS analysis.

Results

Soil physical properties

The soil physical properties, soil moisture, and pH differed substantially (Kruskal–Wallis statistics with p < 0.001) among the investigated plots (Table 1). The soil moisture content varied from 9.1% in F to 12.4% in W and from 11.7% in GF to 21.5% in WF. Multiple post hoc comparisons confirmed significantly (p < 0.05) higher soil moisture only in the invaded FF than the adjacent uninvaded F. The pH varied from 5.2 in F to 6.8 in W and from 6.4 in FF to 7.2 in WF, but no significant differences were observed between the invaded and the uninvaded plots.

Table 1.

Means and standard errors (SD) of the soil physical properties, microbial respiration, microbial biomass carbon, and enzymes in different ecosystems: forest F; forest with F. japonica FF; grassland G; grassland with F. japonica GF; wetland W; wetland with F. japonica WF.

10.21307_jofnem-2019-042-t001.jpg

Soil microbial respiration (SMR), microbial biomass carbon (MBC) content, and enzymatic activities

SMR and MBC content were higher (but not significantly) in all plots with F. japonica (FF, GF, WF) than in the uninvaded plots (F, G, W) (Table 1). Opposite trends were found for acid phosphatase; it was lower (but not significantly) in the invaded (FF, GF, WF) than the uninvaded plots (F, G, W). Urease, alkaline phosphatase, and invertase enzymes were influenced by F. japonica invasion in different ways in the different ecosystems, but no significant differences were found.

Nematode community analysis

A total of 9,452 individual nematodes were isolated and identified. The total number of species and genera of soil free-living and plant-parasitic nematodes was higher in the uninvaded (58 and 46) than in the invaded plots (49 and 40). The species found in the uninvaded (F, G and W) but absent in the invaded plots were as follows: six bacterivores Acrobeles cylindricus, Eucephalobus oxyuroides, Mesorhabditis sp. juv., Plectus tenuis, Prismatolaimus dolichurus, and Punctodora sp. juv.; one fungivore Tylencholaimus stecki; one omnivore Aporcelaimellus obtusicaudatus; two predators Coomansus parvus and Thonus ettersbergensis; two plant parasites Heterodera hordecalis and Meloidogyne hapla; and two root-fungal feeders Boleodorus thylactus and Coslenchus costatus. On the other hand, only the invaded plots (FF, GF, WF) contained the omnivore Axonchium coronatum (GF), the predators Coomansus zschokkei (GF) and Trischistoma monohystera (WF), and the plant parasites Hemicycliophora typica (WF) and Heterodera sp. 1 (FF) (Table 2). Mean nematode abundance was significantly higher in the uninvaded compare to the invaded plots (p < 0.001). Subsequent post hoc Fisher LSD test confirmed a significant effect of ‘invasion status’ for F compare to FF and for W compare to WF (both p<0.05), but not for G compare to GF. Species diversity index did not differ significantly between the invaded and the uninvaded plots (Table 3).

Table 2.

List of identified nematode species and their mean abundance in ind./100 g of soil (n = 5) and standard errors (SD) in different ecosystems: forest F; forest with F. japonica FF; grassland G; grassland with F. japonica GF; wetland W; wetland with F. japonica WF; c-p value of colonizer–persister nematode species from 1 to 5 according to Bongers (1990).

10.21307_jofnem-2019-042-t002.jpg
Table 3.

F-values from two-way ANOVAd or main effect ANOVA with factors ‘Ecosystem’ (forest, grassland, wetland) and ‘Invasion’ (invaded, uninvaded).

10.21307_jofnem-2019-042-t003.jpg

The ordination analysis identified two explanatory variables (pH and SMR) that accounted for 53.5% of the total variation of nematode species abundance (Fig. 1). Monte Carlo permutation tests identified statistical significance of all axes for this relation (pseudo F = 1.7, p = 0.01). Soil acidity and SMR were negatively correlated with the occurrence and abundance of most nematode species in F, G, and W, but soil pH positively correlated with the abundance of the predators A. coronatum and C. zschokkei in GF. The RDA partly separated the nematode communities of the uninvaded habitats from the invaded habitats. Cephalobus persegnis, Plectus parietinus, Prismatolaimus intermedius, and Mesodorylaimus bastiani were more abundant in the uninvaded plots, but Microdorylaimus parvus, Anatonchus tridentatus, and Rotylenchus robustus were more abundant in the invaded plots (Fig. 1, Table 2).

Figure 1:

RDA ordination diagram of nematode communities and Soil pH and Soil Microbial Respiration (Resp) as constrained variables in different ecosystems: forest F; forest with F. japonica FF; grassland G; grassland with F. japonica GF; wetland W; wetland with F. japonica WF with 53.5% 500 explained variance (eigenvalues of axis: 0.35; 0.19; pseudo F = 1.7; P = 0.01). For abbreviation of species see Table 2. Empty circles: biotopes without F. japonica, full triangles: biotopes with F. japonica.

10.21307_jofnem-2019-042-f001.jpg

The NMS analysis compared nematode composition based on species diversity. The best three-dimensional solution for the NMS ordination had a final stress of 10.40 (p < 0.0001) after 48 iterations, which was supported by a Monte Carlo permutation tests with a significance of p = 0.004 and a mean stress of 10.67 for real data and 250 runs for both real and randomised data. The variances explained by the first and second axes were 48 and 28%, respectively. The NMS analysis identified a notable impact of the invasive plants (Fig. 2). The samples from F, G, and W were clearly separated into one group, and the samples from FF, GF, and WF were separated into another group. Moreover, samples from forest (F) differed the most from the other samples, and were separated to the left in the figure, and were represented mostly by high abundances of Paratylenchus straeleni, Tripyla filicaudata, Filenchus misellus, and Prismatolaimus intermedius.

Figure 2:

NMS analysis of samples characterized by nematode species abundance, the grouping factor is presence/absence of F. japonica. Plus signs stand for centroids of two groups, lines around groups connect the outer points of a group. Empty circles represent soil samples from Control: forest F1 to F5, grassland G1 to G5, and wetland W1 to W5. Full triangles represent soil samples with invaded plan F. japonica: forest with F. japonica FF1 to FF5; grassland with F. japonica GF1 to GF5; wetland with F. japonica WF1 to WF5. For abbreviation of species see Table 2. Variance explained by axis 1 and 2 is 48 and 28%, respectively.

10.21307_jofnem-2019-042-f002.jpg

Ecological indices and trophic-group distribution of nematodes

A total of 62 nematode species were identified: 18 of which were bacterial feeders (29.0%), 15 were plant parasites (24.2%), 9 were omnivores (14.5%), 7 were predators (11.3%), 6 were fungivores and root-fungal feeders (both 9.7%), and 1 was an insect parasite (1.6%).

Plant parasites were the most abundant trophic group in F and G (Table 3). The abundance of plant parasites was significantly higher in the uninvaded rather than the invaded plots (p < 0.01). Bacterivores were the second most abundant trophic group in F and G and the most abundant trophic group in W. Subsequent post hoc Fisher LSD test confirmed a significantly higher bacterivore abundance (p < 0.05) in F compared to FF and in W relative to WF (p < 0.05), but not for G and GF was observed. The abundance of fungivores was very low in the forest compared to both the grassland and the wetland (p < 0.001), but without significant differences between the invaded and the uninvaded plots. The abundance of root-fungal feeders was significantly higher in the forest and grassland rather than the wetland (p < 0.05) and in the uninvaded than the invaded plots (p < 0.01). The abundance of omnivores was significantly higher in the uninvaded rather than the invaded plots (p < 0.001). No significant differences in the abundance of predators were found.

Maturity and Channel indices were significantly higher in the uninvaded compared to the invaded plots (p < 0.05). Structure and Basal indices did not significantly differ between the invaded and the uninvaded plots. When plotting the Enrichment and Structure Indices, most of the soil samples ended up in Quadrat B for both the invaded and the uninvaded plots (data not shown) suggesting that food webs were highly enriched and structured with both bacterial and fungal decomposition channels and maturing food web condition. No significant effect of ‘ecosystem’ was observed in the case of abovementioned nematode indices (Table 3).

Discussion

The recent exhaustive literature review on Japanese knotweed indicated that invasion may or may not alter chemical properties of the soil, suggesting that impacts depend on the native plant species that the knotweed replace (Lavoie, 2017). Native flora, as well as actual weather conditions, soil and ecosystem type, date of soil sampling, etc., are probably responsible for the variable impacts of invasion on soil acidity and moisture among studies. Dassonville et al. (2011) in Belgium and France and Suseela et al. (2016) in USA found that invasion of F. japonica can reduce soil moisture probably due to its great leaf area promoting high transpiration rate. Our results with significant higher soil moisture in the invaded forest FF than in the adjacent uninvaded plots contradict these findings. This result was probably due to shadow of the tree canopy; as we did not observe different soil moisture between the invaded and the uninvaded plots in grassland and wetland. These results are in agreement with those by Stefanowicz et al. (2017) in Poland who found that F. japonica invasion did not affect soil moisture in four river valleys. In our study, pH in the invaded plots varied from 6.4 to 7.2, and in the uninvaded plots ranged from 5.2 to 6.8 thus showing no significant differences between the invaded and the uninvaded plots. This finding is in agreement with the report of Stoll et al. (2012) in Switzerland, but contradictory to the results by Dassonville et al. (2011) who reported significant decrease of soil acidity after F. japonica invasion. Rahmonov et al. (2014) reported a high variable pH at sites invaded by F. japonica, and F. japonica can survive very harsh condition with a pH range of 3.0 to 8.5 (Sołtysiak and Brej 2014; Chmura et al., 2015).

Most previous studies detected a higher abundance, biomass and/or species richness of fungi, and a lower bacterial abundance or biomass in F. japonica stands than in the uninvaded sites (Lavoie, 2017). For example, Suseela et al. (2016) recorded up to eight times greater abundance of fungi and 61% lower bacterial biomass under F. japonica than in native vegetation attributed to the accumulation of slowly decomposing knotweed litter that favors fungi over bacteria. Stefanowicz et al. (2016) recorded significant decrease of microbial biomass, urease activity, fungal phospholipid fatty acids (PFLA), fungal:bacterial PLFA ratio, gram-negative bacterial PLFA, and soil microbial respiration under F. japonica under natural conditions. By contrast, in mesocosm pot experiments carried out by Stefanowicz et al. (2019), F. japonica did not reduce microbial activity or biomass but increased fungal biomass and fungal:bacterial ratio. The analyzed microbial characteristics in our study revealed that SMR and MBC content were slightly higher (but not significantly) in all ecosystems invaded by F. japonica in comparison to the uninvaded ones, suggesting that invasion did not affect microbial activity. This was in line with the measured enzyme activities, which remained unaffected by F. japonica invasion probably due the unchanged soil acidity, a factor affecting activity of soil enzymes (Dassonville et al., 2011).

To the best of our knowledge, nematode communities have never been studied in natural habitats invaded by F. japonica. Our study revealed a negative effect of F. japonica on nematode communities, with lower nematode abundance and species richness in the invaded than in the uninvaded plots. These results are consistent with those from an analysis of nematode communities in three habitats invaded by Heracleum sosnowskyi in central Lithuania (Renčo and Baležentiené, 2011). Lower diversity of plant species in ecosystems may affect the populations of plant-parasitic nematodes (Yeates, 1999). This is related to rich root system of higher plants that serves as a food source for plant nematodes (Bongers, 1990), therefore the assessment of nematode abundance and their species diversity reflects the variations in the nematode community due to changes in plant communities (Viketoft et al., 2005). These reports are in line with our findings of a negative impact of F. japonica on the abundance of plant-parasitic and root-fungal feeder nematodes in the invaded plots. Omnivores and predators tend to be more sensitive to environmental changes (Bongers, 1990; Yeates et al., 1993, Ferris et al., 2001) because of their longer generation times and lower fecundity. In our study, the abundance of omnivores was significantly lower in the invaded than in the adjacent uninvaded plots, contradicting the results from a laboratory experiment found by Abgrall et al. (2018), where knotweed rhizome extracts in different concentrations were applied to soil collected in an invasion-prone site. We can only speculate why omnivores in some cases behave to F. japonica invasion as typical K-strategist and why not in others (Abgrall’s extracts). It may be that their diverse and often unknown feeding strategies is hampering data interpretation (Cesarz et al., 2015), or the different study conditions (natural vs laboratory). In contrast, differences in predator abundances were not significantly different between the invaded and the non-invaded plots, confirming the findings by Abgrall et al. (2018) and De Deyn et al. (2004) that the change in plant communities, roots diversity, and biomass production do not affect the nematodes of higher trophic groups such as predators.

According to Bongers (1990), the Maturity index (MI) represents the degree of environmental disturbance, with lower values being indicative of a more disturbed and enriched environment, and higher values being characteristic of a less disturbed and stable environment. We observed lower MI only in the invaded compared to the uninvaded plots, thus conforming with results presented by Renčo and Baležentiené (2011) in sites invaded by H. sosnowskyi in Central Lithuania. Ferris et al. (2001) proposed the Enrichment index (EI) to be a measure of opportunistic bacterivores and fungivores nematodes; the higher EI values in the invaded plots indicative of an N-enriched, highly disturbed environment with low C:N ratio (Ferris et al., 2001). The Structure Index (SI) is the relative contribution of nematodes with higher cp-value (3–5) and indicates the state of food webs affected by stress or disturbance (Ferris et al., 2001). The value of SI can also specify the possibility of control of predators, but in our study, it did not differ significantly between the invaded and the uninvaded sites or ecosystems, confirming the findings by Renčo et al. (2019) and Čerevková et al. (2019) in ecosystems invaded by Heracleum sosnowskyi. Low values of the Channel index CI (<50%) indicates decomposition pathways dominated by bacteria whereas high CI (>50%) indicates a higher proportion of fungal decomposition (Ferris, et al., 2001). In the present study, significant differences in CI were found between the invaded and the uninvaded plots, but all observed value was lower than 50% indicating bacterial-dominated decomposition.

In conclusion, our study demonstrated that the invasive plant species F. japonica considerably negatively altered nematode communities (total abundance, species composition, the abundance of trophic groups) in all habitats. Surprisingly, F. japonica invasion negatively affected neither soil moisture nor soil acidity, and neither SMR and MBC content nor soil enzymes activity. But, there is some doubt that the abundant litter produced and the deep rhizome system of invasive F. japonica have an overall negative impact on soil moisture and pH to be the benefit of the invader, supported by our findings. Most of the studies performed were, however, local, including ours from three habitats. The extent of impact F. japonica invasion has on soil nematode communities, as well as microbial characteristics on the regional to national scale under a variety of natural conditions remains to be verified in future studies.

Acknowledgments

This study was supported by project Slovak scientific agency VEGA (Grant No. 2/0013/16) (0.8) and the project Environmental protection against parasitozoonoses under the influence of global climate and social changes (code IMTS: 26220220116) (0.2) supported by the ERDF-funded operational program Research and Development.

References


  1. Abgrall, C., Forey, E., Mignot, L. and Chauvat, M. 2018. Invasion by Fallopia japonica alters soil food webs through secondary metabolites. Soil Biology and Biochemistry 127:100–9.
    [CROSSREF]
  2. Aguilera, A. G., Alpert, P., Dukes, J. S. and Harrington, R. 2010. Impacts of the invasive plant Fallopia japonica (Houtt.) on plant communities and ecosystem processes. Biological Invasions 12:1243–52.
    [CROSSREF]
  3. Alef, K. and Nannipieri, P. 1995. Methods in applied soil microbiology and biochemistry Academic Press, London.
  4. Andrássy, I. 2005. Free-living nematodes of Hungary Nematoda errantia Vol. I, Hungarian Natural History Museum and Systematic Zoology Research Group of the Hungarian Academy of Sciences, Budapest.
  5. Andrássy, I. 2007. Free-living nematodes of Hungary Nematoda errantia Vol. II, Hungarian Natural History Museum and Systematic Zoology Research Group of the Hungarian Academy of Sciences, Budapest.
  6. Andrássy, I. 2009. Free-living nematodes of Hungary Nematoda errantia Vol. III, Hungarian Natural History Museum and Systematic Zoology Research Group of the Hungarian Academy of Sciences, Budapest.
  7. Bailey, J. P. and Conolly, A. P. 2000. Prize-winners to pariahs – a history of Japanese knotweed s.l. (Polygonaceae) in the British Isles. Watsonia 23:93–110.
  8. Baranová, B., Manko, P. and Jászay, T. 2014. Differences in surface-dwelling beetles of grasslands invaded and non-invaded by goldenrods (Solidago canadensis, S. gigantea) with special reference to Carabidae. Journal of Insect Conservation 18:623–35.
    [CROSSREF]
  9. Bardon, C., Piola, F., Bellvert, F., Haichar, F. Z., Comte, G., Meiffren, G., Pommier, T., Puijalon, S., Tsafack, N. and Poly, F. 2014. Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites. New Phytologist 204:620–30.
    [PUBMED] [CROSSREF]
  10. Beerling, D. J. and Dawah, H. A. 1993. Abundance and diversity of invertebrates with Fallopia japonica (Houtt. Ronse Decraene) and Impatiens glandulifera (Royle): two alien species in the British Isles. Enthomologist 112:127–39.
  11. Beerling, D. J., Bailey, J. P. and Conolly, A. P. 1994. Fallopia japonica (Houtt.) Ronse Decraene. Journal of Ecology 82:959–79.
    [CROSSREF]
  12. Berkelmans, R., Ferris, H., Tenuta, M. and van Bruggen, A. H. C. 2003. Effects of long term crop management on nematode trophic levels other than plant feeders disappear after 1 year of disruptive soil management. Applied Soil Ecology 23:223–35.
    [CROSSREF]
  13. Biederman, L. A. and Boutton, T. W. 2009. Biodiversity and trophic structure of soil nematode communities are altered following woody plant invasion of grassland. Soil Biology and Biochemistry 41:1943–50.
    [CROSSREF]
  14. Bongers, T. 1990. The maturity index, an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19.
    [PUBMED] [CROSSREF]
  15. Brzeski, M. W. 1998. Nematodes of Tylenchida in Poland and temperate Europe. Museum of Institute of Zoology, Polish Academy of Sciences, Warszawa.
  16. Čerevková, A., Miklisová, D., Bobuľská, L. and Renčo, M. 2019. Impact of the invasive plant Solidago gigantea on soil nematodes in a semi-natural grassland and a temperate broadleaved mixed forest. Journal of Helminthology 1–14, available at: https://doi.org/ 10.1017/S0022149X19000324..
  17. Cesarz, S., Reich, P. B., Scheu, S., Ruess, L., Schaefer, M. and Eisenhauer, N. 2015. Nematode functional guilds, not trophic groups, reflect shifts in soil food webs and processes in response to interacting global change factors. Pedobiologia 58:23–32.
    [CROSSREF]
  18. Coats, V. C. and Rumpho, M. E. 2014. The rhizosphere microbiota of plant invaders: an overview of recent advances in the microbiomics of invasive plants. Frontiers in Microbiology 5:368.
    [PUBMED] [CROSSREF]
  19. Chazijev, F. C. H. 1976. Fermentativnaja aktivnosť počv Nauka, Moskva.
  20. Chmura, D., Tokarska-Guzik, B., Nowak, T., Woźniak, G., Bzdęga, K., Koszela, K. and Gancarek, M. 2015. The influence of invasive Fallopia taxa on resident plant species in two river valleys (southern Poland). Acta Societatis Botanicorum Poloniae 84:23–33.
    [CROSSREF]
  21. Ciobanu, M., Popovici, I., Zhao, J. and Stoica, I. 2015. Patterns of relative magnitudes of soil energy channels and their relationships with environmental factors in different ecosystems in Romania. Scientific Reports 5:17606.
    [PUBMED] [CROSSREF]
  22. Cobb, N. A. 1918. Estimating the nematode population of the soil. Bulletin of the Bureau of Plant Industry, Agriculture and Technology. Circular 1. U.S. Department of Agriculture, Washington.
  23. Dassonville, N., Vanderhoeven, S., Gruber, W. and Meerts, P. 2007. Invasion by Fallopia japonica increases topsoil mineral nutrient concentration. Ecoscience 14:230–40.
    [CROSSREF]
  24. Dassonville, N., Domke, S., Herpigny, B., Poly, F. and Meerts, P. J. 2010. Impact of Fallopia spp. on ecosystem functioning: Nitrogen and organic matter cycling and implicated soil biota. Pp.19–22 in Segers, H. and Branquart, E. eds. Science Facing Aliens, Proceedings of a scientific meeting on Invasive Alien Species. Belgian Biodiversity Platform,Brussels.
  25. Dassonville, N., Guillaumaud, N., Piola, F., Meerts, P. and Poly, F. 2011. Niche construction by the invasive Asian knotweeds (species complex Fallopia): impact on activity, abundance and community structure of denitrifies and nitrifies. Biological Invasions 13:1115–33.
    [CROSSREF]
  26. De Deyn, G. B., Raaijmakers, C. E., Van Ruijven, J., Berendse, F. and Van der Putten, W. H. 2004. Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web. Oikos 106:576–86.
    [CROSSREF]
  27. Dommanget, F., Evette, A., Spiegelberger, T., Gallet, C., Pacé, M., Imber, M. and Navas, M. L. 2014. Differential allelopathic effects of Japanese knotweed on willow and cottonwood cuttings used in riverbank restoration techniques. Journal of Environmental Management 132:71–8.
    [PUBMED] [CROSSREF]
  28. Ferris, H., Bongers, T. and de Goede, R. G. M. 2001. A framework for soil food web diagnostics, extension of the nematode faunal analysis concept. Applied Soil Ecology 18:13–29.
    [CROSSREF]
  29. Geraert, E. 2008. The Tylenchidae of the world identification of the family Tylenchidae (Nematoda) Academia Press, Ghent.
  30. Geraert, E. 2010. The Criconematidae of the world identification of the family Criconematidae (Nematoda) Academia Press, Ghent.
  31. Gerber, E., Krebs, C., Murrell, C., Moretti, M., Rocklin, R. and Schaffner, U. 2008. Exotic invasive knotweeds (Fallopia spp.) negatively affect native plant and invertebrate assemblages in European riparian habitats. Biological Conservation 141:646–54.
    [CROSSREF]
  32. Grejtovský, A. 1991. Effect of soil improvers measures the enzymatic activity of heavy alluvial soil. Rostlinná Výroba 37:289–95, (In Slovak).
  33. Islam, K. R. and Weil, R. R. 1998. Microwave irradiation of soil for routine measurement of microbial biomass carbon. Biology and Fertility of Soils 27:408–16.
    [CROSSREF]
  34. Kabat, T. J., Stewart, G. B. and Pullin, A. S. 2006. Are Japanese knotweed (Fallopia japonica) control and eradication interventions effective? CEE review 05-015, University of Birmingham, Birmingham..
  35. Kim, Y. S., Hwang, C. S. and Shin, D. H. 2005. Volatile constituents from the leaves of Polygonum cuspidatum S. et Z. and their anti-bacterial activities. Food Microbiology 22:139–44.
    [CROSSREF]
  36. Kumaga, H., Kawai, Y., Sawano, R., Kurihara, H., Yamazaki, K. and Inoue, N. 2005. Antimicrobial substances from rhizomes of the giant knotweed Polygonum sachalinense against the fish pathogen Photobacterium danselae subsp; piscida. Zeitschrift für Naturforschung C. Journal of Biosciences 60:39–44.
    [PUBMED]
  37. Lavoie, C. 2017. The impact of invasive knotweed species (Reynoutria spp.) on the environment: review and research perspectives. Biological Invasions 19:2319–37.
    [CROSSREF]
  38. Lenda, M., Witek, M., Skórka, P., Moroń, D. and Wojciechowski, M. 2013. Invasive alien plants affect grassland ant communities, colony size and foraging behaviour. Biological Invasions 15:2403–14.
    [CROSSREF]
  39. Levine, J. M., Vilà, M., D’Antonio, C. M., Dukes, J. S., Grigulis, K. and Lavorel, S. 2003. Mechanisms underlying the impacts of exotic plant invasions. Proceedings of the Royal Society of London B 270:775–81.
    [CROSSREF]
  40. Lowe, S., Browne, M., Boudjelas, S. and De Poorter, M. 2000. 100 of the world’s worst invasive alien species a selection from the global invasive species database 12, Invasive Species Specialist Group, Auckland.
  41. Loof, P. A. A. 1999. Nematoda, Adenophorea (Dorylaimida) Spektrum Akademischer Verlag, Heidelberg and Berlin.
  42. McCune, B. and Grace, J. B. 2002. Analysis of ecological communities MjM Software Design, Gleneden Beach. Oregon, USA.
  43. McCune, B. and Mefford, M. J. 2011. PC-ORD multivariate analysis of ecological data version 6.0 MjM software Gleneden Beach. Oregon, USA.
  44. Miklós, L. 2002. Landscape atlas of the Slovak Republic Ministry of Environment of the Slovak Republic Slovak Environmental Agency, Banská Bystrica.
  45. Mincheva, T., Barni, E., Varese, G. C., Brusa, G., Cerabolini, B. and Siniscalco, C. 2014, Litter quality, decomposition rates and saprotrophic mycoflora in Fallopia japonica (Houtt. Ronse Decraene and in adjacent native grassland vegetation. Acta Oecologica 54:29–35.
    [CROSSREF]
  46. Moroń, D., Lenda, M., Skórka, P., Szentgyörgyi, H., Settele, J. and Woyciechowski, M. 2009. Wild pollinator communities are negatively affected by invasion of alien goldenrods in grassland landscapes. Biological Conservation 142:1322–32.
    [CROSSREF]
  47. Muller, S. 2004. Invasives en France Muséum d´Histoire Naturelle, Paris.
  48. Quist, C. W., Vervoort, M. T. W., Van Megen, H., Gort, G., Bakker, J., Van der Putten, W. H. and Helder, J. 2014. Selective alteration of soil food web components by invasive giant goldenrod Solidago gigantea in two distinct habitat types. Oikos 123:837–45.
    [CROSSREF]
  49. Rahmonov, O., Czylok, A., Orczewska, A., Majgier, L. and Parusel, T. 2014. Chemical composition of the leaves of Reynoutria japonica Houtt. and soil features in polluted areas. Central European Journal of Biology 9:320–30.
  50. Renčo, M. and Baležentiené, L. 2011. An analysis of soil free-living and plant-parasitic nematode communities in three habitats invaded by Heracleum sosnowskyi in central Lithuania. Biological Invasions 17:1025–39.
    [CROSSREF]
  51. Renčo, M. Kornobis, F.W., Domaradzki, K., Jakubska-Busse, A., Jurová, J. and Homolová, Z. 2019. How does an invasive Heracleum sosnowskyi affect soil nematode communities in natural conditions? Nematology: International Journal of Fundamental and Applied Nematological Research 21:71–89.
  52. Ritz, K., Black, H. I. J., Campbell, C. D., Harris, J. A. and Wood, C. 2009. Selecting biological indicators for monitoring soils: a framework for balancing scientific and technical opinion to assist policy development. Ecological Indicators 9:1212–21.
    [CROSSREF]
  53. Sabová, M. and Valocká, B. 1980. Parasitic nematodes of cereals in Slovak Republic. Agriculture 26:278–85.
  54. Scharfy, D., Güsewell, S., Gessner, M. O. and Olde Venterink, H. 2010. Invasion of Solidago gigantea in contrasting experimental plant communities: effects on soil microbes, nutrients and plant-soil feedbacks. Journal of Ecology 98:1379–88.
    [CROSSREF]
  55. Schinner, F. and Vonmersi, W. 1990. Xylanase-activity, CM-cellulase-activity and invertase activity in soil – an improved method. Soil Biology and Biochemistry 22:511–15.
    [CROSSREF]
  56. Shannon, C. E. and Weaver, W. 1949. The mathematical theory of communication University of Illinois Press, Urbana, IL.
  57. Siddiqi, M. R. 2000. Tylenchida, parasites of plants and insects 2nd ed., CABI Publishing, Wallingford.
    [CROSSREF]
  58. Sieriebriennikov, B., Ferris, H. and de Goede, R. G. M. 2014. NINJA: an automated calculation system for nematode-based biological monitoring. European Journal of Soil Biology 61:90–3.
    [CROSSREF]
  59. Sołtysiak, J. and Brej, T. 2014. Invasion of Fallopia genus plants in urban environment. Polish Journal of Environmental Studies 23:449–58.
  60. Southey, J. F. 1986. Laboratory methods for work with plant and soil nematodes Her Majesty’s Stationery Office, London.
  61. StatSoft, Inc 2013. STATISTICA (data analysis software system). version 12.0..
  62. Stefanowicz, A. M., Stanek, M., Nobis, M. and Zubek, S. 2016. Species-specific effects of plant invasions on activity, biomass, and composition of soil microbial communities. Biology and Fertility of Soils 52:841–52.
    [CROSSREF]
  63. Stefanowicz, A. M., Stanek, M., Nobis, M. and Zubek, S. 2017. Few effects of invasive plants Reynoutria japonica, Rudbeckia laciniata and Solidago gigantea on soil physical and chemical properties. Science of the Total Environment 574:938–46.
    [PUBMED] [CROSSREF]
  64. Stefanowicz, A. M., Stanek, M., Majewska, M. L., Nobis, M. and Zubek, S. 2019. Invasive plant species identity affects soil microbial communities in a mesocosm experiment. Applied Soil Ecology 136:168–77.
    [CROSSREF]
  65. Sterzyńska, M., Shrubovych, J. and Nicia, P. 2017. Impact of plant invasion (Solidago gigantea L.) on soil mesofauna in a riparian wet meadows. Pedobiologia 64:1–7.
    [CROSSREF]
  66. Stoll, P., Gatzsch, K., Rusterholz, H. P. and Baur, B. 2012. Response of plant and gastropod species to knotweed invasion. Basic and Applied Ecology 13:232–40.
    [CROSSREF]
  67. Suseela, V., Alpert, P., Nakatsu, C. H., Armstrong, A. and Tharayil, N. 2016. Plant-soil interactions regulate the identity of soil carbon in invaded ecosystems, implication for legacy effects. Functional Ecology 30:1227–38.
    [CROSSREF]
  68. Ter Braak, C. J. F. and Šmilauer, P. 2012. CANOCO reference manual and user’s guide, software for ordination. version 50 Microcomputer Power, Biometris, Ithaca, NY.
  69. Van Bezooijen, J. 2006. Methods and techniques for nematology Wageningen University, Wageningen.
  70. Viketoft, M., Palmborg, C., Sohlenius, B., Huss-Danell, K. and Bengtsson, J. 2005. Plant species effects on soil nematode communities in experimental grasslands. Applied Soil Ecology 30:90–103.
    [CROSSREF]
  71. Wasilewska, L. 1997. Soil invertebrates as bioindicators, with special reference to soil inhabiting nematodes. Russian Journal of Nematology 5:113–26.
  72. Yeates, G. W. 1999. Effects of plants on nematode community structure. Annual Review of Phytopathology 37:127–49.
  73. Yeates, G. W., Ferris, H., Moens, T. and van der Putten, W. H. 2009. The role of nematodes in Ecosystems. Pp. 19–22 in Wilson, M. J. and Kakouli-Duarte, T. eds. Nematodes as environmental indicators CABI, Wallingford.
  74. Yeates, G. W., Bongers, T., de Goede, R. G. M., Freckman, D. W. and Georgieva, S. S. 1993. Feeding habits in soil nematode families and genera, outline for soil ecologists. Journal of Nematology 25:315–31.May 11 19-24.
    [PUBMED]
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FIGURES & TABLES

Figure 1:

RDA ordination diagram of nematode communities and Soil pH and Soil Microbial Respiration (Resp) as constrained variables in different ecosystems: forest F; forest with F. japonica FF; grassland G; grassland with F. japonica GF; wetland W; wetland with F. japonica WF with 53.5% 500 explained variance (eigenvalues of axis: 0.35; 0.19; pseudo F = 1.7; P = 0.01). For abbreviation of species see Table 2. Empty circles: biotopes without F. japonica, full triangles: biotopes with F. japonica.

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Figure 2:

NMS analysis of samples characterized by nematode species abundance, the grouping factor is presence/absence of F. japonica. Plus signs stand for centroids of two groups, lines around groups connect the outer points of a group. Empty circles represent soil samples from Control: forest F1 to F5, grassland G1 to G5, and wetland W1 to W5. Full triangles represent soil samples with invaded plan F. japonica: forest with F. japonica FF1 to FF5; grassland with F. japonica GF1 to GF5; wetland with F. japonica WF1 to WF5. For abbreviation of species see Table 2. Variance explained by axis 1 and 2 is 48 and 28%, respectively.

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REFERENCES

  1. Abgrall, C., Forey, E., Mignot, L. and Chauvat, M. 2018. Invasion by Fallopia japonica alters soil food webs through secondary metabolites. Soil Biology and Biochemistry 127:100–9.
    [CROSSREF]
  2. Aguilera, A. G., Alpert, P., Dukes, J. S. and Harrington, R. 2010. Impacts of the invasive plant Fallopia japonica (Houtt.) on plant communities and ecosystem processes. Biological Invasions 12:1243–52.
    [CROSSREF]
  3. Alef, K. and Nannipieri, P. 1995. Methods in applied soil microbiology and biochemistry Academic Press, London.
  4. Andrássy, I. 2005. Free-living nematodes of Hungary Nematoda errantia Vol. I, Hungarian Natural History Museum and Systematic Zoology Research Group of the Hungarian Academy of Sciences, Budapest.
  5. Andrássy, I. 2007. Free-living nematodes of Hungary Nematoda errantia Vol. II, Hungarian Natural History Museum and Systematic Zoology Research Group of the Hungarian Academy of Sciences, Budapest.
  6. Andrássy, I. 2009. Free-living nematodes of Hungary Nematoda errantia Vol. III, Hungarian Natural History Museum and Systematic Zoology Research Group of the Hungarian Academy of Sciences, Budapest.
  7. Bailey, J. P. and Conolly, A. P. 2000. Prize-winners to pariahs – a history of Japanese knotweed s.l. (Polygonaceae) in the British Isles. Watsonia 23:93–110.
  8. Baranová, B., Manko, P. and Jászay, T. 2014. Differences in surface-dwelling beetles of grasslands invaded and non-invaded by goldenrods (Solidago canadensis, S. gigantea) with special reference to Carabidae. Journal of Insect Conservation 18:623–35.
    [CROSSREF]
  9. Bardon, C., Piola, F., Bellvert, F., Haichar, F. Z., Comte, G., Meiffren, G., Pommier, T., Puijalon, S., Tsafack, N. and Poly, F. 2014. Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites. New Phytologist 204:620–30.
    [PUBMED] [CROSSREF]
  10. Beerling, D. J. and Dawah, H. A. 1993. Abundance and diversity of invertebrates with Fallopia japonica (Houtt. Ronse Decraene) and Impatiens glandulifera (Royle): two alien species in the British Isles. Enthomologist 112:127–39.
  11. Beerling, D. J., Bailey, J. P. and Conolly, A. P. 1994. Fallopia japonica (Houtt.) Ronse Decraene. Journal of Ecology 82:959–79.
    [CROSSREF]
  12. Berkelmans, R., Ferris, H., Tenuta, M. and van Bruggen, A. H. C. 2003. Effects of long term crop management on nematode trophic levels other than plant feeders disappear after 1 year of disruptive soil management. Applied Soil Ecology 23:223–35.
    [CROSSREF]
  13. Biederman, L. A. and Boutton, T. W. 2009. Biodiversity and trophic structure of soil nematode communities are altered following woody plant invasion of grassland. Soil Biology and Biochemistry 41:1943–50.
    [CROSSREF]
  14. Bongers, T. 1990. The maturity index, an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19.
    [PUBMED] [CROSSREF]
  15. Brzeski, M. W. 1998. Nematodes of Tylenchida in Poland and temperate Europe. Museum of Institute of Zoology, Polish Academy of Sciences, Warszawa.
  16. Čerevková, A., Miklisová, D., Bobuľská, L. and Renčo, M. 2019. Impact of the invasive plant Solidago gigantea on soil nematodes in a semi-natural grassland and a temperate broadleaved mixed forest. Journal of Helminthology 1–14, available at: https://doi.org/ 10.1017/S0022149X19000324..
  17. Cesarz, S., Reich, P. B., Scheu, S., Ruess, L., Schaefer, M. and Eisenhauer, N. 2015. Nematode functional guilds, not trophic groups, reflect shifts in soil food webs and processes in response to interacting global change factors. Pedobiologia 58:23–32.
    [CROSSREF]
  18. Coats, V. C. and Rumpho, M. E. 2014. The rhizosphere microbiota of plant invaders: an overview of recent advances in the microbiomics of invasive plants. Frontiers in Microbiology 5:368.
    [PUBMED] [CROSSREF]
  19. Chazijev, F. C. H. 1976. Fermentativnaja aktivnosť počv Nauka, Moskva.
  20. Chmura, D., Tokarska-Guzik, B., Nowak, T., Woźniak, G., Bzdęga, K., Koszela, K. and Gancarek, M. 2015. The influence of invasive Fallopia taxa on resident plant species in two river valleys (southern Poland). Acta Societatis Botanicorum Poloniae 84:23–33.
    [CROSSREF]
  21. Ciobanu, M., Popovici, I., Zhao, J. and Stoica, I. 2015. Patterns of relative magnitudes of soil energy channels and their relationships with environmental factors in different ecosystems in Romania. Scientific Reports 5:17606.
    [PUBMED] [CROSSREF]
  22. Cobb, N. A. 1918. Estimating the nematode population of the soil. Bulletin of the Bureau of Plant Industry, Agriculture and Technology. Circular 1. U.S. Department of Agriculture, Washington.
  23. Dassonville, N., Vanderhoeven, S., Gruber, W. and Meerts, P. 2007. Invasion by Fallopia japonica increases topsoil mineral nutrient concentration. Ecoscience 14:230–40.
    [CROSSREF]
  24. Dassonville, N., Domke, S., Herpigny, B., Poly, F. and Meerts, P. J. 2010. Impact of Fallopia spp. on ecosystem functioning: Nitrogen and organic matter cycling and implicated soil biota. Pp.19–22 in Segers, H. and Branquart, E. eds. Science Facing Aliens, Proceedings of a scientific meeting on Invasive Alien Species. Belgian Biodiversity Platform,Brussels.
  25. Dassonville, N., Guillaumaud, N., Piola, F., Meerts, P. and Poly, F. 2011. Niche construction by the invasive Asian knotweeds (species complex Fallopia): impact on activity, abundance and community structure of denitrifies and nitrifies. Biological Invasions 13:1115–33.
    [CROSSREF]
  26. De Deyn, G. B., Raaijmakers, C. E., Van Ruijven, J., Berendse, F. and Van der Putten, W. H. 2004. Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web. Oikos 106:576–86.
    [CROSSREF]
  27. Dommanget, F., Evette, A., Spiegelberger, T., Gallet, C., Pacé, M., Imber, M. and Navas, M. L. 2014. Differential allelopathic effects of Japanese knotweed on willow and cottonwood cuttings used in riverbank restoration techniques. Journal of Environmental Management 132:71–8.
    [PUBMED] [CROSSREF]
  28. Ferris, H., Bongers, T. and de Goede, R. G. M. 2001. A framework for soil food web diagnostics, extension of the nematode faunal analysis concept. Applied Soil Ecology 18:13–29.
    [CROSSREF]
  29. Geraert, E. 2008. The Tylenchidae of the world identification of the family Tylenchidae (Nematoda) Academia Press, Ghent.
  30. Geraert, E. 2010. The Criconematidae of the world identification of the family Criconematidae (Nematoda) Academia Press, Ghent.
  31. Gerber, E., Krebs, C., Murrell, C., Moretti, M., Rocklin, R. and Schaffner, U. 2008. Exotic invasive knotweeds (Fallopia spp.) negatively affect native plant and invertebrate assemblages in European riparian habitats. Biological Conservation 141:646–54.
    [CROSSREF]
  32. Grejtovský, A. 1991. Effect of soil improvers measures the enzymatic activity of heavy alluvial soil. Rostlinná Výroba 37:289–95, (In Slovak).
  33. Islam, K. R. and Weil, R. R. 1998. Microwave irradiation of soil for routine measurement of microbial biomass carbon. Biology and Fertility of Soils 27:408–16.
    [CROSSREF]
  34. Kabat, T. J., Stewart, G. B. and Pullin, A. S. 2006. Are Japanese knotweed (Fallopia japonica) control and eradication interventions effective? CEE review 05-015, University of Birmingham, Birmingham..
  35. Kim, Y. S., Hwang, C. S. and Shin, D. H. 2005. Volatile constituents from the leaves of Polygonum cuspidatum S. et Z. and their anti-bacterial activities. Food Microbiology 22:139–44.
    [CROSSREF]
  36. Kumaga, H., Kawai, Y., Sawano, R., Kurihara, H., Yamazaki, K. and Inoue, N. 2005. Antimicrobial substances from rhizomes of the giant knotweed Polygonum sachalinense against the fish pathogen Photobacterium danselae subsp; piscida. Zeitschrift für Naturforschung C. Journal of Biosciences 60:39–44.
    [PUBMED]
  37. Lavoie, C. 2017. The impact of invasive knotweed species (Reynoutria spp.) on the environment: review and research perspectives. Biological Invasions 19:2319–37.
    [CROSSREF]
  38. Lenda, M., Witek, M., Skórka, P., Moroń, D. and Wojciechowski, M. 2013. Invasive alien plants affect grassland ant communities, colony size and foraging behaviour. Biological Invasions 15:2403–14.
    [CROSSREF]
  39. Levine, J. M., Vilà, M., D’Antonio, C. M., Dukes, J. S., Grigulis, K. and Lavorel, S. 2003. Mechanisms underlying the impacts of exotic plant invasions. Proceedings of the Royal Society of London B 270:775–81.
    [CROSSREF]
  40. Lowe, S., Browne, M., Boudjelas, S. and De Poorter, M. 2000. 100 of the world’s worst invasive alien species a selection from the global invasive species database 12, Invasive Species Specialist Group, Auckland.
  41. Loof, P. A. A. 1999. Nematoda, Adenophorea (Dorylaimida) Spektrum Akademischer Verlag, Heidelberg and Berlin.
  42. McCune, B. and Grace, J. B. 2002. Analysis of ecological communities MjM Software Design, Gleneden Beach. Oregon, USA.
  43. McCune, B. and Mefford, M. J. 2011. PC-ORD multivariate analysis of ecological data version 6.0 MjM software Gleneden Beach. Oregon, USA.
  44. Miklós, L. 2002. Landscape atlas of the Slovak Republic Ministry of Environment of the Slovak Republic Slovak Environmental Agency, Banská Bystrica.
  45. Mincheva, T., Barni, E., Varese, G. C., Brusa, G., Cerabolini, B. and Siniscalco, C. 2014, Litter quality, decomposition rates and saprotrophic mycoflora in Fallopia japonica (Houtt. Ronse Decraene and in adjacent native grassland vegetation. Acta Oecologica 54:29–35.
    [CROSSREF]
  46. Moroń, D., Lenda, M., Skórka, P., Szentgyörgyi, H., Settele, J. and Woyciechowski, M. 2009. Wild pollinator communities are negatively affected by invasion of alien goldenrods in grassland landscapes. Biological Conservation 142:1322–32.
    [CROSSREF]
  47. Muller, S. 2004. Invasives en France Muséum d´Histoire Naturelle, Paris.
  48. Quist, C. W., Vervoort, M. T. W., Van Megen, H., Gort, G., Bakker, J., Van der Putten, W. H. and Helder, J. 2014. Selective alteration of soil food web components by invasive giant goldenrod Solidago gigantea in two distinct habitat types. Oikos 123:837–45.
    [CROSSREF]
  49. Rahmonov, O., Czylok, A., Orczewska, A., Majgier, L. and Parusel, T. 2014. Chemical composition of the leaves of Reynoutria japonica Houtt. and soil features in polluted areas. Central European Journal of Biology 9:320–30.
  50. Renčo, M. and Baležentiené, L. 2011. An analysis of soil free-living and plant-parasitic nematode communities in three habitats invaded by Heracleum sosnowskyi in central Lithuania. Biological Invasions 17:1025–39.
    [CROSSREF]
  51. Renčo, M. Kornobis, F.W., Domaradzki, K., Jakubska-Busse, A., Jurová, J. and Homolová, Z. 2019. How does an invasive Heracleum sosnowskyi affect soil nematode communities in natural conditions? Nematology: International Journal of Fundamental and Applied Nematological Research 21:71–89.
  52. Ritz, K., Black, H. I. J., Campbell, C. D., Harris, J. A. and Wood, C. 2009. Selecting biological indicators for monitoring soils: a framework for balancing scientific and technical opinion to assist policy development. Ecological Indicators 9:1212–21.
    [CROSSREF]
  53. Sabová, M. and Valocká, B. 1980. Parasitic nematodes of cereals in Slovak Republic. Agriculture 26:278–85.
  54. Scharfy, D., Güsewell, S., Gessner, M. O. and Olde Venterink, H. 2010. Invasion of Solidago gigantea in contrasting experimental plant communities: effects on soil microbes, nutrients and plant-soil feedbacks. Journal of Ecology 98:1379–88.
    [CROSSREF]
  55. Schinner, F. and Vonmersi, W. 1990. Xylanase-activity, CM-cellulase-activity and invertase activity in soil – an improved method. Soil Biology and Biochemistry 22:511–15.
    [CROSSREF]
  56. Shannon, C. E. and Weaver, W. 1949. The mathematical theory of communication University of Illinois Press, Urbana, IL.
  57. Siddiqi, M. R. 2000. Tylenchida, parasites of plants and insects 2nd ed., CABI Publishing, Wallingford.
    [CROSSREF]
  58. Sieriebriennikov, B., Ferris, H. and de Goede, R. G. M. 2014. NINJA: an automated calculation system for nematode-based biological monitoring. European Journal of Soil Biology 61:90–3.
    [CROSSREF]
  59. Sołtysiak, J. and Brej, T. 2014. Invasion of Fallopia genus plants in urban environment. Polish Journal of Environmental Studies 23:449–58.
  60. Southey, J. F. 1986. Laboratory methods for work with plant and soil nematodes Her Majesty’s Stationery Office, London.
  61. StatSoft, Inc 2013. STATISTICA (data analysis software system). version 12.0..
  62. Stefanowicz, A. M., Stanek, M., Nobis, M. and Zubek, S. 2016. Species-specific effects of plant invasions on activity, biomass, and composition of soil microbial communities. Biology and Fertility of Soils 52:841–52.
    [CROSSREF]
  63. Stefanowicz, A. M., Stanek, M., Nobis, M. and Zubek, S. 2017. Few effects of invasive plants Reynoutria japonica, Rudbeckia laciniata and Solidago gigantea on soil physical and chemical properties. Science of the Total Environment 574:938–46.
    [PUBMED] [CROSSREF]
  64. Stefanowicz, A. M., Stanek, M., Majewska, M. L., Nobis, M. and Zubek, S. 2019. Invasive plant species identity affects soil microbial communities in a mesocosm experiment. Applied Soil Ecology 136:168–77.
    [CROSSREF]
  65. Sterzyńska, M., Shrubovych, J. and Nicia, P. 2017. Impact of plant invasion (Solidago gigantea L.) on soil mesofauna in a riparian wet meadows. Pedobiologia 64:1–7.
    [CROSSREF]
  66. Stoll, P., Gatzsch, K., Rusterholz, H. P. and Baur, B. 2012. Response of plant and gastropod species to knotweed invasion. Basic and Applied Ecology 13:232–40.
    [CROSSREF]
  67. Suseela, V., Alpert, P., Nakatsu, C. H., Armstrong, A. and Tharayil, N. 2016. Plant-soil interactions regulate the identity of soil carbon in invaded ecosystems, implication for legacy effects. Functional Ecology 30:1227–38.
    [CROSSREF]
  68. Ter Braak, C. J. F. and Šmilauer, P. 2012. CANOCO reference manual and user’s guide, software for ordination. version 50 Microcomputer Power, Biometris, Ithaca, NY.
  69. Van Bezooijen, J. 2006. Methods and techniques for nematology Wageningen University, Wageningen.
  70. Viketoft, M., Palmborg, C., Sohlenius, B., Huss-Danell, K. and Bengtsson, J. 2005. Plant species effects on soil nematode communities in experimental grasslands. Applied Soil Ecology 30:90–103.
    [CROSSREF]
  71. Wasilewska, L. 1997. Soil invertebrates as bioindicators, with special reference to soil inhabiting nematodes. Russian Journal of Nematology 5:113–26.
  72. Yeates, G. W. 1999. Effects of plants on nematode community structure. Annual Review of Phytopathology 37:127–49.
  73. Yeates, G. W., Ferris, H., Moens, T. and van der Putten, W. H. 2009. The role of nematodes in Ecosystems. Pp. 19–22 in Wilson, M. J. and Kakouli-Duarte, T. eds. Nematodes as environmental indicators CABI, Wallingford.
  74. Yeates, G. W., Bongers, T., de Goede, R. G. M., Freckman, D. W. and Georgieva, S. S. 1993. Feeding habits in soil nematode families and genera, outline for soil ecologists. Journal of Nematology 25:315–31.May 11 19-24.
    [PUBMED]

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