Influence of Asclepias Syriaca on Soil Nematode Communities

FOLIA OECOLOGICA – vol. 48, no. 1 (2021), doi: 10.2478/foecol-2021-0009

Influence of Asclepias syriaca on soil nematode communities

Michaela Jakubcsiková, Andrea Čerevková*, Marek Renčo

Institute of Parasitology SAS, Hlinková 3, 040 01 Košice, Slovak Republic

Abstract Jakubcsiková, M., Čerevková, A., Renčo, M., 2021. Influence of Asclepias syriaca on soil nematode communities. Folia Oecologica, 48 (1): 73–81.

The main goal of this study was to evaluate the impact of the invasive common milkweed (Asclepias syriaca L.) on soil nematode communities. The research was carried out in 2018 and 2019 in an ecosystem of permanent grassland in the basin of the Laborec River in land registries of Drahňov, a Vojany village in southeastern Slovakia. The ecosystem contained a total of 64 species of free-living and parasitic nematodes. The most prevalent trophic groups were bacterial feeders (Acrobeloides nanus), followed by plant parasites (Helicotylenchus digonicus and Pratylenchus pratensis), fungal feeders (Aphelenchus avenae), and omnivores (Eudorylaimus carteri). The number of nematode species, the composition of trophic groups and the structure of communities in areas with invasive plants were similar to those in areas with native vegetation during the two years of observation.

Keywords common milkweed, diversity, ecology, soil nematodes

Introduction Nematode occurrence and activity (movement) are conditioned by the presence of water and by food Common milkweed (Asclepias syriaca L.) is an invasive sources, consisting of a wide range of organisms such as species native to North America. A. syriaca is a broadleaf bacteria, fungi, plants, and other nematodes (Yeates et perennial herb, with simple stems sometimes as tall as 2 m. al., 1993). They are an important component of the soil The leaves are short, smooth, and oppositely arranged on biomass of all ecosystems. Nematodes are slow-moving the stem. The flowers are pinkish but can vary from white ubiquitous organisms that represent about 80% of all to dark red and are usually arranged on both sides of the multicellular organisms in soil (105–106 m-2). They have cymes. All parts of common milkweed contain a milky a thin permeable cuticle that allows direct contact with latex that contains toxic cardenolides (Bhowmik, 1994). the external environment. Some may survive or die in Invasive plant species are considered a major threat to unfavourable soil conditions, in anabiotic or cyst stages, so the diversity of the flora and fauna of ecosystems (Jose they are useful bioindicators (Freckman, 1988; Bongers et al., 2013), but their impact on soil nematofauna has and Ferris, 1999; Hugot et al., 2001). Recent preliminary rarely been studied worldwide (Belnap and Phillips, studies, however, have found that the impact of invasive 2001; Liang et al., 2007). Soil nematodes are small plant species on soil nematodes depends on the plant filamentous organisms, whose adults have body lengths of species and the ecosystem. 0.2–10.0 mm.

73 The main goal of this study was to use nematode Yeates (2003), and the Jaccard index of faunistic similarity communities as bioindicators to evaluate the impact of Js defined by Jaccard (1908), were also calculated. Data A. syriaca invasion on an ecosystem using functional and were statistically analysed using PlotIT Ver. 3.2 (Scientific ecological indices (identification, occurrence, abundance, Programming Enterprises, Haslett, USA) and were diversity, and community structure of nematode species) compared using Student’s t-tests. (Bongers, 1990; Ferris et al., 2001).

Results Materials and methods A total of 64 species of free-living and plant parasitic The impact of the non-indigenous A. syriaca on soil nematodes were found in the soil samples. The control nematodes was investigated in a permanent grassland in plots contained more species than the invaded plots (44 the southern part of eastern Slovakia in the Laborec River vs 41) in 2018 but fewer in 2019 (45 vs 48). The total basin. Soil samples were collected from five 20-m2 plots number of individuals in 2018 was 9,895 and was slightly dominated by A. syriaca in June 2018 (AS1) and June 2019 higher in the control plots (5,017) than the invaded plots (AS2) and from five adjacent control plots in (CO1) and (4,878) (Table 1). The total number of individuals was (CO2) dominated by the grasses Brachypodium pinnatum higher in 2019 (12,378) than 2018 (9,895). The differences and Bromus tectorum and containing no invasive plants. in abundance between the invaded and control plots, Motile nematodes were isolated using sieves and the however, were not significant. Baermann method with a set of two cotton propylene filters The eudominant (>10%) bacterial feeder Acrobeloides (Van Bezooijen, 2006). Nematodes were killed in a warm nanus (509 individuals, D = 10.4%, in 2018; 669 individuals, water bath (70 °C) and fixed with Ditlevsen’s solution D = 11.0%, in 2019) and the fungal feeder Aphelenchus (Van Bezooijen, 2006). Permanent glycerine slides avenae (486 individuals, D = 10.0%, in 2018 only) were were prepared for 100 individuals of randomly selected the most abundant nematodes in the invaded plots. The nematodes two weeks after fixation. Nematodes on the dominant (5–10%) omnivore Eudorylaimus carteri, the slides were identified to species using an Eclipse 90i light obligate plant parasites Helicotylenchus digonicus and microscope (Nikon Instruments Europe BV, Netherlands). Pratylenchus pratensis, some subdominant species (2–5%) Taxonomic and systematic monographs by Andrássy such as Oxydirus oxycephalus (predator), Aporcelaimellus (2005; 2007; 2009), Meyl (1960), Hunt (1993), Brzeski obtusicaudatus (omnivore), and the facultative plant (1998), Loof (1999), and Geraert (2008; 2010; 2011; parasites Aglenchus agricola and Boleodorus volutus were 2013) were used for identification. also relatively abundant in the invaded plots. The number Evaluation of the nematode communities was based and dominance of the nematodes were similar in the on the total number of nematodes per 100 g of soil, control plots. Some species were nevertheless present only occurrence and number of species, a species diversity in the invaded plots, regardless of year of observation, index (H’spp) (Shannon and Weaver, 1949), and the such as Acrolobus emarginatus, Anaplectus granulosus, number of individuals in various trophic groups (Yeates et Ereptonema arcticum, Clarkus papillatus, Tylencholaimus al., 1993; Wasilewska, 1997). The degree of dominance stecki, Campydora demonstrans, Microdorylaimus parvus, (D) of the species was determined using the scale proposed Pratylenchoides crenicauda, and Trophurus sculptus. In by Losos et al. (1984): eudominant (D > 10%), dominant contrast, other nematode species such as Prismatolaimus (D = 5–10%), subdominant (D = 2–5%), and recendent intermedius, Tylencholaimellus striatus, Mesocriconema (D < 2%). Species were divided into six trophic groups: curvatum, Heterodera sp. (juveniles), Longidorus sp. bacterial feeders, predators, fungal feeders, omnivores, (juveniles), and Tylenchus elegans were found only in the plant parasites, and root-fungal feeders (Yeates et al., control plots (Table 1). 1993; Wasilewska, 1997). They were also divided into All soil samples contained all nematode trophic functional guilds using the c-p (coloniser-persister) value, groups, regardless of the presence or absence of invasive which varies from 1 to 5 depending on the duration of their plants. Bacterial feeders and plant parasites followed by development cycle, trophic and reproductive strategies, fungal feeders were the most abundant trophic groups in and sensitivity to environmental alteration (Bongers, both years. The proportions of all trophic groups did not 1990). differ significantly between the invaded and control plots We used an automated calculation system NINJA (Fig. 1). (Sieriebriennikov et al., 2014) for nematode-based Maturity indices (MI, MI 2–5, and ΣMI) were slightly biological monitoring to calculate i) ecological indices higher in the control than the invaded plots in both years. (maturity index, MI; summary maturity index, ΣMI; CI and SI were slightly higher and lower, respectively, in maturity index for nematodes with c–p values of 2–5, MI the invaded plots in both years. Total nematode biomass 2–5; and a plant parasitic index, PPI), ii) functional indices and NCR were lower in the invaded than the control plots, (enrichment index, EI; structural index SI; and channel but not significantly. Js was 63.46 in 2018 and 63.16 in index CI, which provide information about the conditions 2019 (Table 2). of the soil environment), and iii) total nematode biomass When plotting the EI and SI, for analysis of food (Bongers, 1990; Bongers and Korthals, 1993; Ferris webs, the soil samples from invaded and control plots et al., 2001). The nematode channel ratio NCR defined by mostly (95% of samples) ended up in quadrats B and C

– – – – – 1.4 0.4 1.3 1.1 1.4 4.0 1.5 2.8 1.7 3.0 1.4 1.4 1.2 1.1 1.0 0.7 0.4 2.0 0.9

10.4 D %

Asclepias 250 ,

CO2

– – – – 87 22 80 73 86 94 91 86 75 67 64 41 A – 655 254 174 109 192 26 58

124 208

2019

– – – 0.6 1.3 0.9 3.1 0.5 0.1 1.2 2.4 3.8 1.7 0.2 0.7 0.8 1.2 0.4 0.5 1.0 – – 0.7 0.7 11.0 D %

917 ,

AS2

8 37 79 – 57 28 76 14 42 51 72 – 24 27 63 – – 40 40 – 80 A 669 190 148 232 100

– – – –

5.5 2.1 0.9 0.5 0.7 0.8 2.3 0.5 1.2 1.7 0.5 1.6 1.2 0.6 1.5 0.7 1.7 – – –

3.4 D

198 , CO1

– – – – 46 26 37 40 26 59 85 25 79 59 30 75 33 84 A 113 – – – 275 106

171 171 2018

– – – – – – – 1.5 0.8 3.3 0.2 0.4 1.4 2.4 3.1 2.8 1.6 0.8 1.1 0.6 0.5 0.3 0.7 4.3

10.4 D

493 , AS1

23 – – – 22 80 38 – – 56 – – 32 15 33 A 75 41 68

509 159 118 150 138 208 279

- 2 2 4 4 2 2 2 2 2 2 2 1 1 2 2 2 3 1 3 2 2 4 4 3 5 c

%) in samples collected in June 2018 and 2019 (n = 5) from areas with presence of

Cobb, 1917

Loof, 1971

Bastian, 1865 Bastian, Osche, 1952 Osche, de Man, 1880 Man, de Bastian, 1865 Bastian, .

(De Coninck, 1931) Zell, 1985 Zell, 1931) Coninck, (De de Man, 1880 Man, de

Andrássy, 1985 Andrássy, (1990) Bastian, 1865 Bastian,

(Bütschli, 1873) de Man, 1880 Man, de 1873) (Bütschli, (de Man, 1876) Steiner, 1936 Steiner, 1876) Man, (de

(de Man, 1921) Thorne, 1937 Thorne, 1921) Man, (de 1876 Man, de 1873) (Bütschli,

(Bütschli, 1873) Sudhaus, 1976 Sudhaus, 1873) (Bütschli, (Bastian, 1865) Thorne, 1937 1939 Thorne, 1885) Man, (de (de Man, 1880) Boström, 1986 Boström, 1880) Man, (de (de Man, 1880) Thorne, 1937 Thorne, 1880) Man, (de

(de Man, 1880) Andrássy, 1981 Andrássy, 1880) Man, (de

(Schneider, 1866) Thorne, 1937 Thorne, 1866) (Schneider,

(de Man, 1921) Thorne, 1939 Thorne, 1921) Man, (de

(de Man, 1880) Anderson, 1968 Anderson, 1880) Man, (de (Bastian, 1865) Jairajpuri, 1970 1865) Jairajpuri, (Bastian,

Bongers g of soil and dominance of nematode species (D Nematode species Nematode Plectus parvus Plectus Mesorhabditis sp Mesorhabditis Tripyla filiformis Tripyla Plectus parietinus Plectus Alaimus primitivus Alaimus Ereptonema arcticum Ereptonema Plectus silvaticus Plectus Cephalobus persegnis Cephalobus Mylonchulus sigmaturus Mylonchulus (Bastian, 1865) De Coninck & Schuurmans Stekhoven, 1933 Stekhoven, Schuurmans & Coninck De 1865) (Bastian,

Amphidelus elegans Amphidelus Clarkus papillatus Clarkus Cervidellus vexilliger Oxydirus oxycephalus Oxydirus Acrobeloides nanus nanus Acrobeloides Eucephalobus striatus Chiloplacus propinquus Chiloplacus Acrolobus emarginatus Acrolobus Eumonhystera vulgaris Eumonhystera Eucephalobus oxyuroides Eucephalobus rigidus Panagrolaimus Protorhabditis filiformis Protorhabditis terrestris Teratocephalus Prismatolaimus intermedius Prismatolaimus Wilsonema schuurmansstekhoveni Wilsonema Anaplectus granulosus Anaplectus – omnivores, PP – plant parasites, – plant PP O – omnivores, feeders, F – fungal – predators, P feeders, groups: B – bacterial TG – trophic (CO1, CO2). area) (control vegetation native AS2) and with (AS1,

P P P P B B B B B B B B B B B B B B B B B B B B B TG Table 1. Nematode total Table abundance (A) in 100 syriaca RFF – root-fungal feeders; c-p value according

8.6 0.4 – 4.4 2.5 – 1.7 3.1 – – 1.3 0.4 – – – – 0.4 – 4.7 1.6 0.6 3.5 4.2 1.2 0.4 1.6 1.8 0.8 1.0

– – – – 81 – – – – – 40 73 26 50 64 055 26 26

, 541 156 276 105 196 101 220 265 563 102 114 25 296 1

– – – – – – – – 3.0 5.7 1.2 0.2 1.4

8.7 1.1 1.3 2.2 1.3 3.5 1.0 0.9

0.8 1.7 0.7 0.3 1.1 0.2 0.5 3.9

– – 76 14 – – – – – – 128 , 527 66 80 136 83 78 213 63 54 181 347 51 101 43 17 452 67 12 27 239 1

– – – – – – – – – 0.3 5.1 4.4 4.1 5.6

11.3 1.7 1.0 2.1 1.3 2.2 1.0 3.1

2.0 0.2 4.4 0.8 2.4 0.7 1.7

– 17 – – – – – – – – 566 86 50 104 67 112 52 258 221 155 99 10 722 220 737 118 41 205 36 85 282

– – – – – – – – – – – – 8.3 0.6 0.9 5.0 1.6 1.5 0.3 3.2 1.0 0.2 0.5 1.1 3.4 2.8 0.6 0.9

10.0

– – 32 46 – – 28 43 – – 17 – – 50 – – – – 25 56 76 73

8 404

136 486 243

155

875 582

165

3 4 3 3 2 4 4 2 2 4 4 5 2 2 4 2 2 3 3 5 4 4 4 4 3 4 4 4 2

- Santiago & Ciobanu, 2008 Micoletzky, 1922 Micoletzky, Altherr, 1968 Altherr,

Franklin, 1957

Cobb, 1920 Thorne, 1939 Thorne, de Man, 1880 Man, de

Andrássy, 1959 Andrássy, Steiner, 1936 Steiner,

Steiner, 1914 Steiner, Cobb, 1920 Cobb,

Bastian, 1865 Bastian, Wasilewska, 1965 Wasilewska, Schmidt, 1871 Schmidt,

(Bastian, 1865) Altherr, 1968 Altherr, 1865) (Bastian, Micoletzky, 1922 Micoletzky,

(Bastian,1865) Steiner, 1932 Steiner, (Bastian,1865)

(de Man, 1880) Thorne, 1974 Thorne, 1880) Man, (de

(Bütschli, 1873) de Man, 1876 Man, de 1873) (Bütschli, (de Man, 1880) Filipjev, 1936 Filipjev, 1880) Man, (de

(de Man, 1880) Andrássy, 1986 (Bütschli, 1873) Andrássy, 1959 Andrássy, 1873) (Bütschli, (Allen, 1955) Siddiqi, 1970 Siddiqi, 1955) (Allen,

(Micoletzky, 1922) Taylor, 1936 Taylor, 1922) (Micoletzky,

(Bastian, 1865) Andrássy, 1959 Andrássy, 1865) (Bastian,

(Raski, 1952) Loof & De Grisse, 1989 Grisse, De & Loof 1952) (Raski, Perry in Perry, Darling & Thorne, 1959

microdorus

(de Man, 1921) Thornne & Swanger, 1936 Swanger, & Thornne 1921) Man, (de

(de Man, 1885) Peña 1885) Man, (de

(de Man, 1912) Coomans & Geraert, 1962 Geraert, & Coomans 1912) Man, (de

brevidens

Doryllium uniforme Doryllium Aphelenchus avenae Aphelenchus Heterodera sp. juvs. sp. Heterodera Tylencholaimus stecki Tylencholaimus Campydora demonstrans Campydora Aphelenchoides limberi Aphelenchoides Longidorus sp. sp. juvs. Longidorus Tylencholaimellus striatus Tylencholaimellus Diphtherophora communis Diphtherophora Paratylenchus Paratylenchus Ditylenchus medicaginis Ditylenchus Prodorylaimus longicaudatus Prodorylaimus Aphelenchoides composticola Aphelenchoides Merlinius Paraphelenchus pseudoparietinus Paraphelenchus Eudorylaimus carteri Ditylenchus intermedius Ditylenchus Ecumenicus monohystera Aphelenchoides parietinus Aphelenchoides Tylencholaimus mirabilis Tylencholaimus Microdorylaimus parvus Microdorylaimus Criconemoides informis Criconemoides Mesodorylaimus bastiani Mesodorylaimus Aporcelaimellus obtusicaudatus Aporcelaimellus Pungentus silvestris Pungentus Mesocriconema curvatum Mesocriconema Helicotylenchus digonicus Helicotylenchus Dorylaimoides micoletzkyi Dorylaimoides Crassolabium ettersbergense Crassolabium

F F F F F F F F F F F F F O O O O O O O O O PP PP PP PP PP PP PP Table 1. Continued Table

4.2 4.9 5.4 1.4 – – 1.1 – – –

– – – – – 523 314 45 91 68 , , 267 307 340 1 6

– – – 7.2 4.5 2.0 8.2 2.0 1.2 1.1

– – – 723 064 48 , , 435 500 124 71 273 120 69 1 6

– – – – 6.3 2.5 2.4 0.2 4.8 1.1

– – – – – 642 017 44 , , 317 124 119 241 54 1 5

– – – – 6.3 3.6 2.9 3.1 4.4 1.4

– – – – 180 69 878 41 ,

, 310 176 140 153 215 1 4

2 3 2 2 2 3 2 2 3 2

Winslow, 1958

Loof 1956

de Man, 1876 Man, de

Lima & Siddiqi, 1963 Siddiqi, & Lima

(de Man, 1880) Filipjev, 1936 Filipjev, 1880) Man, (de Khan, Prasat 1967 & Mathur, Khan,

(de Man, 1921) Siddiqi, 1978 Siddiqi, 1921) Man, (de

(de Man, 1884) Andrássy, 1954 Andrássy, 1884) Man, (de (Massey, 1969) Andrássy, 1980 Andrássy, 1969) (Massey,

(Brzeski, 1963) Lownsbery & Lownsbery, 1985 Lownsbery, & Lownsbery 1963) (Brzeski,

Trophurus sculptus Trophurus Tylenchus elegans Total number of nematodes of number Total Number of nematode species nematode of Number Boleodorus volutus Boleodorus Pratylenchoides crenicauda Pratylenchoides Coslenchus costatus Coslenchus Malenchus exiguus Malenchus Paratylenchus similis Paratylenchus Aglenchus agricola Aglenchus Pratylenchus pratensis Pratylenchus Filenchus vulgaris Filenchus

PP PP PP PP RFF RFF RFF RFF RFF RFF

77 Table 2. Ecological and functional indices of nematodes from soil samples collected in June 2018 and 2019 from plots with Tablepresence 2. Ecological of Asclepias and syriaca functional (AS1, indices AS2) ofand nematodes control plots from with soil native samples vegetation collected (CO1, in June CO2). 2018 Evaluated and 2019 indices: from plots diversity with presenceindex for of species Asclepias H' spp. syriaca and Jaccard (AS1, AS2)index and of faunistic control plotssimilarity with native vegetation (CO1, CO2). Evaluated indices: diversity index for species H‘spp. and Jaccard index of faunistic similarity 2018 2019 Evaluated indices AS1 CO1 AS2 CO2 Mean S.D Mean S.D Mean S.D Mean S.D Number of individuals 975.4ns 180.3 1003.5 167.7 1213.0ns 228.1 1267.7 169.6 H'spp. 2.8 ns 0.1 3.1 0.1 2.9 ns 0.2 3.0 0.220 Maturity index 2.6 ns 0.4 2.9 0.2 2.5 ns 0.1 2.6 0.2 Maturity index 2–5 2.8 ns 0.4 3.1 0.2 2.6 ns 0.1 2.6 0.2 Σ Maturity index 2.6 ns 0.3 2.8 0.1 2.5 ns 0.1 2.6 0.1 Plant parasitic index 2.7 ns 0.1 2.7 0.1 2.5 ns 0.2 2.6 0.2 Channel index 49.3 ns 29.3 48.5 21.5 68.3 ns 23.3 44.0 7.5 Enrichment index 51.9 ns 13.7 19.2 10.4 36.1 ns 8.6 47.1 5.5 Structure index 68.4 ns 13.9 80.1 4.5 60.8 ns 7.6 64.3 10.4 NCR (BF/BF + FF) 0.6 ns 0.6 0.7 0.6 0.6 ns 0.6 0.7 0.8 Total biomass (mg) 0.9 ns 0.7 1.2 0.5 1.1 ns 0.3 1.2 0.6 Jaccard index 63.5 63.2 ns, non-significant. ns, non-significant.

Trophic groups composition of nematode communities

100

40 Trophic groups (%) (%) groups Trophic

0 AS1 AS2 CO1 CO2 2018 2019 2018 2019 Plots Bacterial feeders Predators Fungal feeders

Omnivores Plant parasites Root-fungal feeders

Fig. 1. Percentage proportion of nematodes in trophic groups in invaded plots by Asclepias syriaca (AS1, AS2) and control plots with native vegetation (CO1, CO2) in June 2018 and 2019 (n = 5). Fig. 1. Percentage proportion of nematodes in trophic groups in invaded plots by Asclepias syriaca (AS1, AS2) and control plots with native vegetation (CO1, CO2) in June 2018 and 2019 (n = 5). (Fig. 2). These quadrants indicated that both types of soil equally involved in the decomposition of organic matter, environments had been little disturbed and had balanced and the food web was mature. nutrient supplies. Bacterial and fungal feeders were

Fig. 2. Graphical representation of trophic webs and conditions in soil environment by values of Enrichment Index and Structure Index in invaded plots by Asclepias syriaca (AS1, AS2) and control plots with native vegetation (CO1, CO2) in June 2018 and 2019 (n = 5). Fig. 2. Graphical representation of trophic webs and conditions in soil environment by values of Enrichment Index and Structure Index in invaded plots by Asclepias syriaca (AS1, AS2) and control plots with native vegetation (CO1, CO2) in June 2018 and 2019 (n = 5). Discussion and conclusions Nematodes of trophic groups omnivores and predators are the most sensitive to changes in their environment, Recent studies have found that the impact of invasive because they have a low reproductive capacity and long plant species on ecosystem soil nematofauna could be developmental cycles (Bongers, 1990; Ferris et al., 2001). positive, neutral, or negative. Nematode species diversity Restoring the numbers to levels before environmental was affected positively in conjunction with invasion by damage requires more time for omnivores and predators Impatiens parviflora and I. glandulifera (Renčo et al., than for bacterial or fungal feeders (r-strategists). The 2013) and negatively in conjunction with invasion by abundances of omnivores and predators during the two Solidago gigantea or Fallopia japonica (Čerevková et al., years of observation were not affected by the invasion by 2019a; 2019b). common milkweed in this permanent grassland. Omnivores Yeates (1999) reported that the species spectrum and predators in some cases can respond to invasion by of plant root composition in soil directly influenced the non-native plant species as typical K-strategists, and occurrence and behaviour of plant parasitic nematodes, sometimes vice versa (Renčo and Baležentiené 2015; consistent with the findings by De Deyn et al. (2004). Renčo et al. 2019). These groups are also characterised by Changes in the diversity of plant species and roots and their species diversity, food strategies, and species biology, the quality and quantity of biomass primarily affect plant which impede the interpretation of results (Cesarz et al., parasites and only indirectly (secondarily) affect other 2015). Fauna can also be differentially affected by various trophic groups, such as fungal feeders, predators, or environmental conditions, such as invasion by non-native bacterial feeders. In our study, the invasion by common plants, and the properties of these plants (Jose et al., 2013). milkweed had no effect on the numbers of bacterivorous Fungal feeders in our study ranged from 24 to 33% of nematodes. We found that the total abundance of obligate the total nematofauna. Fungal feeders of the c-p2 group plant parasitic nematodes was similar in the invaded and dominated, especially A. avenae and Aphelenchoides control plots, what was consistent with the results obtained parietinus. The proportion and number of fungal feeders, by Jurová et al. (2019) in a previous study of the effect of however, did not differ among the soils, indicating that A. syriaca on soil nematodes. We therefore hypothesised invasion by common milkweed did not affect the structure that the common milkweed or its roots may host some of the fungal communities. No data are available on the plant parasitic nematodes responsible for the reduction in impact of A. syriaca on soil fungal communities. Vannette yield of economically important crops. Many weeds are and Hunter (2011), though, found that mycorrhizal fungi important hosts for many plant parasitic nematodes (cyst- lived on the roots of common milkweed and positively forming nematodes and root-knot nematodes), so the roots affected its growth, the production of its milky exudate, of A. syriaca may also be hosts. and leaf area.

79 We also calculated various ecological and functional Brzeski, M.W., 1998. Nematodes of Tylenchina in Poland indices of communities to comprehensively evaluate our and temperate Europe. Warszawa: Muzeum i Instytut results, although changes to the abundance, number of Zoologii PAN. 395 p. species, species diversity, and representation of trophic Čerevková, A., Bobuľská, L., Miklisová, D., Renčo, M., and c-p groups were not confirmed in the nematode 2019a. A case study of soil food web components affected communities. The indices did not differ significantly by Fallopia japonica L. Polygonaceae in three natural between the invaded and control plots during the two habitats in central Europe. Journal of Nematology, 51: years of observation, as we assumed. The analysis of the art. no. e-2019-42: 1–16. doi: 10.21307/jofnem-2019-042 structures of food webs using EI and SI indicated that the Čerevková, A., Miklisová, D., Bobuľská, L., Renčo, soil environments of both types of plots was little disturbed M., 2019b. Impact of the invasive plant Solidago and had balanced supplies of nutrients. Bacterial and gigantea on soil nematodes in a semi-natural grassland fungal feeders were equally involved in the decomposition and a temperate broadleaved mixed forest. Journal of of organic matter, and the food web was mature. Helminthology, 94: art. no. e51, p. 1–14. https://doi. org/10.1017/S0022149X19000324 Cesarz, S., Reich, P.B., Scheu, S., Ruess, L., Schaefer, Acknowledgement M., Eisenhauer, N., 2015. Nematode functional guilds, not trophic groups, reflect shifts in soil food webs and The authors acknowledge the support of Slovak scientific processes in response to interacting global change factors. agency Vega project (Grant No. 2/0018/20). Pedobiologia, 58: 23–32. https://doi.org/10.1016/j. pedobi.2015.01.001 De Deyn, G.B., Raaijmakers, C.E., van Ruijven, J., References Berendse, F., van der Putten, W.H., 2004. Plant species identity and diversity effects on different trophic levels Andrássy, I., 2005. Free-living nematodes of Hungary of nematodes in the soil food web. Oikos, 106: 576–586. Nematoda errantia. Vol. I. Budapest: Hungarian Natural https://doi.org/10.1111/j.0030-1299.2004.13265.x History Museum and Systematic Zoology Research Ferris, H., Bongers, T., Goede, R.G.M., 2001. A framework Group of the Hungarian Academy of Sciences. 518 p. for soil food web diagnostics: extension of the nematode Andrássy, I., 2007. Free-living nematodes of Hungary faunal analysis concept. Applied Soil Ecology, 18: 13–29. Nematoda errantia. Vol. II. Budapest: Hungarian Natural https://doi.org/10.1016/S0929-1393(01)00152-4 History Museum and Systematic Zoology Research Freckman, D.W., 1988. Bacterivorous nematodes and organic- Group of the Hungarian Academy of Sciences. 496 p. matter decomposition. Agriculture, Ecosystems and Andrássy, I., 2009. Free-living nematodes of Hungary Environment, 24: 195–217. https://doi.org/10.1016/0167- Nematoda errantia., Vol. III. Budapest: Hungarian Natural 8809(88)90066-7 History Museum and Systematic Zoology Research Geraert, E., 2008. The Tylenchidae of the world: identification Group of the Hungarian Academy of Sciences. 608 p. of the family Tylenchidae (Nematoda). Gent: Academia Baniyamuddin, M., Tomar, V.V.S., Ahmad, W., 2007. Press. 454 p. Functional diversity of soil inhabiting nematodes in Geraert, E., 2010. The Criconematidae of the world: natural forests of Arunachal Pradesh, India. Nematologia identification of the family Criconematidae (Nematoda). Mediterranea, 35: 109–121. Gent: Academia Press. 615 p. Belnap, J., Phillips, S.L., 2001. Soil biota in an ungrazed Geraert, E., 2011. The Dolichodoridae of the world: grassland: response to annual grass (Bromus tectorum) identification of the family Dolichodoridae. Gent: invasion. Ecological Applications, 11: 1261–1275. Academia Press. 520 p. https://doi.org/10.1890/1051-0761(2001)011[1261:SBIA Geraert, E., 2013. The Pratylenchidae of the world: UG]2.0.CO;2 identification of the family Pratylenchidae (Nematoda: Bhowmik, P.C., 1994. Biology and control of common Tylenchida). Gent: Academia Press. 430 p. milkweed Asclepias syriaca. Reviews of Weed Science, 6: Hugot, J.-P., Baujard, P., Morand, S., 2001. Biodiversity 227–250. in helminths and nematodes as a field of study: Bongers, T., 1990. The maturity Index, the evolution of an overview. Nematology, 3: 199–208. ttps:/ doi. nematode life history traits, adaptive radiation and cp- org/10.1163/156854101750413270 scaling. Plant and Soil, 212: 13–22. Hunt, D.J., 1993. Aphelenchida, Longidoridae and Bongers, T., Ferris, H., 1999. Nematode community Trichodoridae: their systematics and bionomics. structure as a bioindicator in environmental monitoring. Wallingford: CABI. 368 p. Jaccard, P., 1908. Nouvelles recherches sur la distribution Trends in Ecology and Evolution, 14: 224–228. https:// florale [New research on the floral distribution]. Bulletin doi.org/10.1016/S0169-5347(98)01583-3 de la Societe Vaudoise des Sciences Naturelles, 44: 223– Bongers, T., Korthals, G., 1993. The Maturity Index, 270. doi:10.5169/seals-268384 an instrument to monitor changes in the nematode Jose, S., Singh, H.P., Batish, D.R., Kohli, R.K., 2013. The community structure. In Summaries of the 45th horse behind the cart? Invasive plant ecology. Boca international symposium on crop protection. May 4, Gent, Raton, FL, USA: CRC Press. 302 p. Belgium. Gent, p. 80.

80 Jurová, J., Renčo, M., Gömöryová, E., Čerevková, workshop on soil zoology held in Ceske Budejovice, A., 2019. Effects of the invasive common milkweed Czech Republic, 8-11 April 2013. Asclepias syriaca on nematode communities in natural Shannon, C., Weaver, W., 1949. The mathematical theory grasslands. Nematology, 22: 423–438. https://doi. of communication. Vol. 2. Urbana: University of Illinois org/10.1163/15685411-00003314 Press. Liang, W., Li, F., Li, Q., Zhang, W., 2007. Temporal dynamics Sieriebriennikov, B., Ferris, H., de Goede, R.G.M., 2014. NINJA: an automated calculation system for nematode- of soil nematode community structure under invasive based biological monitoring. European Journal of Ambrosia trifida and native Chenopodium serotinum. Soil Biology, 61: 90–93. https://doi.org/10.1016/j. Helminthologia, 44: 29–33. https://doi.org/10.2478/ ejsobi.2014.02.004 s11687-006-0053-6 Van Bezooijen, J., 2006. Methods and techniques for Loof, P.A.A., 1999. Nematoda, Adenophorea (Dorylaimida). nematology. Wageningen: Wageningen University. Berlin: Spektrum Akademischer Verlag. 264 p. Vannette, R L., Hunter, M.D., 2011. Plant defence theory re‐ Losos, B., Gulička, J., Lellák, J., Pelikán, J., 1984. examined: nonlinear expectations based on the costs and Ekologie živočichů [Animal ecology]. Praha: SPN. 320 p. benefits of resource mutualisms. Journal of Ecology, 99: Meyl, A., 1960. Die Tierwelt Mitteleuropas [The fauna of 66–76. https://doi.org/10.1111/j.1365-2745.2010.01755.x Central Europe]. Leipzig: Eds. Quelle and Meyer. Wasilewska, L., 1997. Soil invertebrates as bioindicators, Renčo, M., Baležentiené, L., 2015. Analysis of soilfree- with special reference to soil- inhabiting nematodes. living and plant-parasitic nematode communities in three Russian Journal of Nematology, 5: 113–126. habitats invaded by Heracleum sosnowskyi in central Yeates, G.W., 1999. Effects of plants on nematode community structure. Annual Review of Phytopathology, 37: 127– Lithuania. Biological Invasions, 17: 1025–1039. https:// 149. https://doi.org/10.1146/annurev.phyto.37.1.127 doi.org/10.1007/s10530-014-0773-3 Yeates, G.W., 2003. Nematodes as soil indicators: functional Renčo, M., Kornobis, F.W., Domaradzki, K., Jakubska- and biodiversity aspects. Biology and Fertility of Soils, Busse, A., Jurová, J., Homolová, Z., 2019. How does 37 (2): 199–210. https://doi.org/10.1007/s00374-003- an invasive Heracleum sosnowskyi affect soil nematode 0586-5 communities in natural conditions? Nematology: Yeates, G. W., Bongers, T., De Goede, R.G.M., Freckman, International Journal of Fundamental and Applied D.W., Georgieva, S.S., 1993. Feeding habits in soil Nematological Research, 21: 71-89. https://doi.org/ Nematode families and genera – an outline for soil 10.1163/15685411-00003196 ecologists. Journal of Nematology, 25: 315–331. Renčo, M., Krumpálová, Z., Galis, M., 2013. Changes within nematode communities after plant invasion in their Received October 21, 2020 native range. Paper presented at the 12th Central European Accepted November 26, 2020