Structural and functional diversity of nematode fauna associated with habitats located in the Natura 2000 site Apuseni (Romania) Текст научной статьи по специальности «Биологические науки»

Russian Journal of Nematology, 2017, 25 (1), 23 - 36

Structural and functional diversity of nematode fauna associated with habitats located in the Natura 2000 site Apuseni (Romania)

Marcel Ciobanu and Iuliana Popovici

Institute of Biological Research, Branch of the National Institute of Research and Development for Biological Sciences, 48 Republicii Street, 400015, Cluj-Napoca, Romania e-mail: office@icbcluj.ro

Accepted for publication 3 June 2017

Summary. In five grasslands and six forests located in the 'Natura 2000' protected area Apuseni (Romania) 191 nematode taxa (132 species) were found. Nematode fauna differed according to geographical location of the sampling sites, ecosystems and 'Natura 2000' habitat types. Nematode fauna in forests was more diverse than in grasslands. Plant feeders, bacterial feeders and omnivorous nematodes dominated in the samples. General opportunists were more frequent in forests, as opposite to persisters, which were more abundant in grasslands. Maturing and structured conditions of the soil food web were revealed. The differentiation between types of ecosystems and habitats based on prevailing decomposition channel in soil was not possible.

Key words: ecology, environmental monitoring, soil conservation.

Protected areas are good models for natural ecosystems because they are affected very little by human impact due to conservation measures. Protected areas of community interest (also known as Natura 2000 sites) were created in Romania after its inclusion in the European Union (EU) in 2007 (Anonymous, 2007a). Their purpose is to conserve natural habitats and wild species listed in the Habitats Directive 92/43/EEC (Anonymous, 1992) and Birds Directive 79/409/EEC (Anonymous, 1979). Most of the habitats protected by the Habitats Directive were established taking into account vegetation communities and landscape units (Evans, 2006; Vanden Borre et al., 2011) but not soil biodiversity (Turbé et al., 2010), although the importance of soil organisms in ecosystem functioning and services has been largely accepted and recognised (Lazarova et al., 2011). Later on, the European Commission considered necessary to amend the list of soil-based habitats requiring special protection and complete the list of soil-dwelling species present in European soils, which are expected to receive more attention in the management plans for the Natura 2000 sites across Europe in the future (Montanarella, 2008).

Free-living soil nematodes are part of the soil food web and respond rapidly to changes in their

environment (Bongers & Bongers, 1998; Ferris et al., 2001). Their value and utility in assessing the condition and functioning of soil food webs has been widely acknowledged (Ferris et al., 2001, 2004; Neher et al., 2005; Sánchez-Moreno & Ferris, 2007; Sánchez-Moreno et al., 2008, 2011; Vonk et al., 2013).

The Natura 2000 site Apuseni (coded R0SCI0002 Apuseni) is located in the central northwestern part of the Apuseni Mountains (Romania) and has a surface of 76,150 ha (Anonymous, 2007a), almost totally overlapping the one of the Apuseni Natural Park (Anonymous, 2003). The site was designated to conserve the biodiversity associated with 39 types of natural habitats of community interest, nine of them being of priority conservation interest, i.e., natural habitat types in danger of disappearance, which are present within the EU and for whose conservation the Community has particular responsibility (Anonymous, 2007b).

In this work, we investigate the potential of nematode fauna in the soil-based assessment of the conservation status of terrestrial habitats of community interest from Natura 2000 protected areas. The objectives of this study are: i) to characterise and discuss the structural and functional

22'30'E 22°40'E 22*501= 23'E 23'10'E

Fig. 1. Distribution of the sampling sites within the Natura 2000 protected area Apuseni (ROSCI0002).

Table 1. Main characteristics of the sampled locations.

Site no.1 Ecosystem type Location Altitude (m a.s.l.) Natura 2000 habitat type (* — priority habitat) Soil type3

1 Deciduous forest (beech) Padi§, Bihor Mts2. 1300 91V0 Dacian beech forests (Symphyto-Fagion) Cambic rendzina

2 Coniferous forest Calineasa, 1200 9410 Acidophilous Picea forests of the montane Acid brown

(spruce) Bihor Mts. to alpine levels (Vaccinio-Piceetea)

3 Coniferous forest Chicera cu Colac, 1100 9410 Acidophilous Picea forests of the montane Acid brown

(spruce) Vladeasa Mts. to alpine levels (Vaccinio-Piceetea)

4 Grassland Ghejari-Scäri§oara, Bihor Mts. 1050 6430 Hydrophilous tall-herb fringe communities of plains and of the montane to alpine levels Rendzina

5 Grassland Ghejari-Scäri§oara, Bihor Mts. 1080 6230* Species-rich Nardus grasslands, on siliceous substrates in mountain areas (and sub- Rendzina

mountain areas, in Continental Europe)

6 Mixed forest (beech and Ghejari-Scäri§oara, Bihor Mts. 1050 91V0 Dacian beech forests (Symphyto-Fagion) Cambic rendzina

7 Grassland Ghejari-Scäri§oara, Bihor Mts. 1000 6230* Species-rich Nardus grasslands, on siliceous substrates in mountain areas (and sub- Argilluvic brown

mountain areas, in Continental Europe)

8 Grassland Ghejari-Scäri§oara, Bihor Mts. 1000 6230* Species-rich Nardus grasslands, on siliceous substrates in mountain areas (and sub- Rendzina

mountain areas, in Continental Europe)

9 Grassland Ghejari-Scäri§oara, Bihor Mts. 1000 6230* Species-rich Nardus grasslands, on siliceous substrates in mountain areas (and sub- Rendzina

mountain areas, in Continental Europe)

10 Mixed forest (beech and spruce) Ghejari-Scäri§oara, Bihor Mts. 1100 91V0 Dacian beech forests (Symphyto-Fagion) Lithic rendzina

11 Coniferous forest Ghejari-Scäri§oara, 1050 9410 Acidophilous Picea forests of the montane Typic rendzina

(spruce) Bihor Mts. to alpine levels (Vaccinio-Piceetea)

Note: 1 Correspondence with sites in Table 2; 2 Mountains; 3 According to the Romanian System of Soil Classification (Conea et al., 1980).

diversity of nematode fauna associated with selected ecosystems and habitats of community interest located in the Natura 2000 site Apuseni; and ii) to assess the ecological condition of soil food webs in these ecosystems and habitat types based on nematode faunal analysis.

MATERIALS AND METHODS

Eleven sites (five grasslands and six forests) located in four Natura 2000 habitat types (Gafta & Mountford, 2008) from the protected area R0SCI0002 Apuseni were surveyed between 1978 and 1998 (Fig. 1; Table 1).

Soil samples for nematodes were collected randomly from surface areas of approximately 500 m2 and consisted of up to eight cores (cores of 25 cm2 in area) taken from the endo-organic soil horizon and the top 10 cm of the ecto-organic soil horizon (cores of 3.8 cm2 in area). The endo-organic soil horizon in forests included litter, fermentation and humification layers, whereas in grasslands it consisted of sod (turf) and intertwined roots. Soil samples were placed in plastic bags, labelled and stored in a cool and dark place until nematode extraction was carried out.

The centrifugal flotation method (de Grisse, 1969) was used to extract nematodes from 85 g of soil, after removing small stones and root fragments. After extraction, nematodes were counted under a stereomicroscope, killed and fixed with a 4% formaldehyde solution at 65°C.

At least 150 nematode individuals were randomly identified under the microscope following Andrassy (1984) and Bongers (1988). Adults and most juveniles were identified to species level, but some of the juveniles were identified at supra-specific (genus, family) level. Nematode taxa were then ordered according to life history category from (c)oloniser to (p)ersister (c-p) scale between 1 and 5 (Bongers, 1990; Bongers & Bongers, 1998), allocated to trophic groups (Yeates et al., 1993; Bongers & Bongers, 1998) and assigned to functional guilds (Bongers & Bongers, 1998; Ferris et al., 2001).

BioDiversity Pro software (McAleece et al., 1997) was used to assess taxonomic diversity (total number of taxa and Shannon Diversity Index) of nematode fauna.

CANOCO 5 software (ter Braak & Smilauer, 2012) was employed to evaluate similarities between sites based on nematode composition by applying nonmetric multidimensional scaling (nMDS) of the Bray-Curtis distances (Bray & Curtis, 1957).

Enrichment Index (EI), Structure Index (SI) and Channel Index (CI) (Ferris et al., 2001; Ferris, 2010) were calculated based on nematode functional guilds and used for assessing the ecological condition of soil food webs in the aforementioned ecosystems and habitat types.

Maturity Indices for nematode communities (MI, PPI) were not used in the current study as their utility in comparing nematode fauna of contrasting ecosystems with different soil types was considered less relevant (Bongers, 1990).

RESULTS

Structural diversity of nematode fauna. The

nematode communities consisted of 191 taxa (132 species, 59 taxa identified at supra-specific level) (Table 2). The total number of taxa (TNT) ranged between 109 in beech forest (91V0) at Padi§ (site no. 1) and 42 in mixed forest (91V0) in the Ghe^ari-Scàriçoara area (site no. 6). In general, nematode communities in forest soils spanned a larger range of richness values (42-109 taxa) than those in grasslands (53-76 taxa) (Table 3).

Fig. 2. Total number of nematode taxa and Shannon Diversity Index according to Natura 2000 habitat types (* - priority habitat) (mean values, except habitat 6430; habitat names abridged).

Shannon Diversity Index (SDI) (Table 3) ranged between 1.498 in species-rich Nardus grassland (6230*) in the Ghetari-Scari§oara area (site no. 4) and 1.176 in spruce forest (9410) in the Ghe^ari-Scari§oara area (site no. 11). Of all Natura 2000 habitat types surveyed, nematode fauna associated with acidophilous Picea forests (9410) was the least diverse (Fig. 2).

Fifty-two nematode taxa were found in more than half of the total number of sites, whereas Anaplectus granulosus (Bastian, 1865) De Coninck

Table 2. Abundance (%) of nematode taxa from the Natura 2000 site Apuseni; Bee-beech forest, Spr-spruce forest, Gra-grassland, Mix-mixed forest; 6230* Species-rich Nardus grasslands, on siliceous substrates in mountain areas (and submountain areas, in Continental Europe), 6430 Hydrophilous tall-herb fringe communities of plains and of the montane to alpine levels, 91V0 Dacian beech forests (Symphyto-Fagion), 9410 Acidophilous Picea forests of the montane to alpine levels (Vaccinio-Piceetea), * - priority habitat; eudominant (D% > 10) taxa are marked in bold; taxa with D% < 0.1 have 0.0 values.

Site number 1 2 3 4 5 6 7 8 9 10 11

Ecosystem type Bee Spr Spr Gra Gra Mix Gra Gra Gra Mix Spr

Natura 2000 habitat type 91V0 9410 9410 6430 6230* 91V0 6230* 6230* 6230* 91V0 9410

Acrobeles ciliatus 2.0 2.9 0.1

Acrobeloides nanus 2.5 2.3 2.5 0.1 2.0 0.7 0.3 2.0

Acrobeloides sp. 0.8 0.1 0.8

Acrolobus emarginatus 0.1 0.1 0.5

Aglenchus agricola 0.1 0.2 0.5 0.1 2.5 0.1 0.1 0.1

Alaimus meyli 0.2 0.2 0.4 0.1 0.1 1.0 0.3

Alaimus parvus 0.1 0.2

Alaimus primitivus 0.2 0.6 0.4 0.1 0.4 0.1

Alaimus sp. 0.3 0.4 0.4 0.1 0.3 0.4 0.6 0.1

Allodorylaimus allgeni 0.1 0.2

Amplimerlinius socialis 0.5 0.1 1.0 0.1

Anaplectus granulosus 0.3 0.2 0.1 2.3 1.4 5.5 0.9 1.9 2.5 1.4 0.7

Anatonchus sp. 0.1

Anatonchus tridentatus 0.3

Aphanolaimus attentus 1.1

Aphelenchoides sp. 1.6 3.3 3.8 2.5 2.4 0.4 3.8 4.4 4.3 7.7 2.4

Aphelenchus avenae 0.5 1.4 0.8 0.4 1.6 0.7

Aporcelaimellus obtusicaudatus 1.8 0.4 0.5 5.7 4.2 10.1 5.4 0.3 0.4 2.4

Aporcelaimellus sp. 0.4 1.4 0.2

Aporcelaimus regius 0.1

Aporcelaimus romanicus 0.1

Aporcelaimus sp. 0.3 0.2

Aquatides intermedius 0.4 2.8 2.2

Aulolaimus oxycephalus 0.1 0.1

Aulolaimus sp. 0.2 0.1 0.3

Axonchium coronatum 0.1

Axonchium sp. 1.8 3.8 0.1

Bastiania gracilis 0.1 0.2 0.2 0.5 0.8 1.0 0.3 0.1 1.3 0.4

Bastiania longicaudata 0.1 0.2 0.1 0.1

Bastiania sp. 0.8 0.1

Boleodorus sp. 0.3 0.1

Bunonema reticulatum 0.7 1.4 1.5 1.4 1.6 0.4 0.5 0.5 1.6 3.3 1.6

Bunonema richtersi 0.1 0.6 0.5 0.9 1.0 0.1 0.5 1.3

Cephalobus persegnis 0.1 0.1 2.4 0.4 3.0

Cephalobus sp. 0.5 2.6 2.1 1.3 8.8 0.1 0.1

Chiloplacus sp. 0.4 1.7 0.1

Chiloplacus symmetricus 0.2 0.1 2.1

Chitwoodius sp. 0.1 0.1

Chronogaster typica 0.1

Clarkus papillatus 1.0 0.1 2.5 0.1 0.0 0.3

Clavicaudoides longicaudata 0.4 0.2 0.2 0.1

Coomansus menzeli 1.3 0.5 1.5 0.4 0.3

Coomansus parvus 0.3 4.6 0.4 0.5

Table 2. (continued)

Site number 1 2 3 4 5 6 7 8 9 10 11

Ecosystem type Bee Spr Spr Gra Gra Mix Gra Gra Gra Mix Spr

Natura 2000 habitat type 91V0 9410 9410 6430 6230* 91V0 6230* 6230* 6230* 91V0 9410

Coomansus sp. 0.2 0.5

Coslenchus costatus 0.1 0.6 1.7 0.7 0.2 0.5 0.1

Crassolabium ettersbergensis 0.1 0.1

Crassolabium nothus 0.4

Crassolabium sp. 0.8 4.8 3.4 1.3 0.7 0.2 0.3 0.1

Criconema annuliferum 0.4 0.2 0.5 0.1

Criconema orientale 0.1

Criconema princeps 0.1 0.1 0.1

Criconema sp. 0.1 0.5 0.1

Criconemella sp. 0.4 2.1 0.1

Criconemoides annulatum 0.5

Criconemoides informis 0.5 0.2 0.5

Cylindrolaimus communis 0.2 0.7 0.4 0.0 0.3

Cylindrolaimus sp. 0.2

Deladenus durus 0.1 0.1

Diphtherophora communis 0.5 0.5 4.2 0.1

Ditylenchus intermedius 1.0 3.3 4.3

Ditylenchus sp. 1.3 4.0 0.4 3.0 1.1 1.1 2.5 1.3

Dorylaimoides elegans 0.8 0.0

Dorylaimoides limnophilus 0.2 0.5

Dorylaimoides micoletzkyi 0.1 0.1 0.2

Dorylaimoides sp. 0.4

Ecphyadophora tenuissima 0.1 0.2 0.5 0.5 0.2 3.6

Ecumenicus monohystera 0.1 0.1 0.1

Enchodelus macrodorus 0.4 0.1 1.0

Enchodelus parateres 0.1 0.4

Enchodelus sp. 0.7 0.2

Epidorylaimus consobrinus 0.1

Epidorylaimus lugdunensis 0.4 0.2

Epidorylaimus pseudoagilis 0.8 0.2

Epidorylaimus sp. 0.4 1.7 0.3 0.6

Eucephalobus mucronatus 0.1

Eucephalobus oxyuroides 0.5 0.2 3.0 5.5 1.3 2.1 11.0 2.0 0.9

Eucephalobus striatus 2.6 2.5

Eudorylaimus acuticauda 0.3 0.2

Eudorylaimus carteri 0.1 5.3 2.5 0.1 0.2 0.3

Eudorylaimus leuckarti 0.1 0.1 0.2 0.3 0.3 0.1 0.1

Eudorylaimus longicardius 0.1

Eudorylaimus opistohystera 0.2

Eudorylaimus sp. 0.4 6.1 2.1 14.3 17.7 4.0 3.0 1.2 1.3 8.7

Eumonhystera filiformis 0.1 0.1 0.7

Eumonhystera sp. 0.3 0.0 0.1 0.6

Eumonhystera vulgaris 0.3 0.8 0.5 0.4

Filenchus sp. 26.1 10.5 5.0 7.9 2.8 8.0 23.0 7.4 13.8 25.2 35.8

Filenchus vulgaris 1.5 2.5 8.7

Geomonhystera villosa 0.4 0.1 0.2 2.4 0.1 0.5 0.4 0.3

Gracilacus acicula 0.1

Table 2. (continued)

Site number 1 2 3 4 5 6 7 8 9 10 11

Ecosystem type Bee Spr Spr Gra Gra Mix Gra Gra Gra Mix Spr

Natura 2000 habitat type 91V0 9410 9410 6430 6230* 91V0 6230* 6230* 6230* 91V0 9410

Gracilacus sp. 0.4 1.9

Hemicycliophora sp. 0.0 0.2

Heterocephalobus elongatus 0.2 0.7 3.2 0.4 1.0 1.3 1.0 0.1 0.5 0.6

Heterodera sp. 0.1

Hoplotylus femina 0.1

Iotonchus sp. 0.7 0.4

Lelenchus leptosoma 0.1 0.1 0.1

Leptonchidae 0.1

Longidorella microdorus 0.2

Longidorella parva 0.1

Longidorella sp. 0.7 0.8 0.2

Longidorus elongatus 3.2

Malenchus bryophilus 9.0 8.7 5.5 7.1 2.1 1.6 7.9

Malenchus pachycephalus 0.2

Mesocriconema rusticum 2.5 0.2 1.1

Mesodorylaimus bastiani 2.1 0.2 0.6 0.4 0.4

Mesodorylaimus sp. 2.9 0.2 0.8 0.1 0.4 2.7 2.3

Mesodorylaimus subtiliformis 0.1 0.1

Mesorhabditis sp. 0.4 1.1 0.3

Metateratocephalus crassidens 0.2 2.0 2.4 0.9 1.5 0.2 0.7 1.4

Metateratocephalus gracilicaudatus 1.3

Miconchus aquaticus 0.6

Miconchus hopperi 0.3 0.1 0.1 0.4

Miconchus sp. 0.5

Miconchus studeri 0.1 2.1

Mylonchulus brachyuris 1.0 0.2 0.6 1.6 4.4 4.6 0.5 3.2 1.0 0.8 0.3

Mylonchulus sigmaturellus 1.1

Mylonchulus sigmaturus 1.7 0.7 0.1 0.1

Nygolaimus sp. 0.1 0.4 0.9 0.1

Odontolaimus chlorurus 0.2 0.1 0.1

Ogma menzeli 0.5 0.2 0.8 0.2 1.7

Opistodorylaimus sylphoides 0.5 0.1

Oxydirus oxycephalus 0.1 0.1 5.4 2.8 0.4 0.1 2.8 2.4

Panagrolaimus rigidus 0.2 0.1 0.1 0.2 0.3 0.3 1.8 0.1

Paramphidelus dolichurus 0.7 0.1 0.1 0.0 0.3

Paramphidelus exilis 0.1 0.1

Paramphidelus sp. 0.2

Paraphelenchus pseudoparietinus 0.4 0.1 0.1 0.4

Paratylenchus sp. 0.2 0.5 1.7 2.5 0.1 2.5 0.3

Paraxonchium sp. 0.1

Plectus acuminatus 2.2 0.8 2.2 0.3 0.4 1.6 1.6

Plectus armatus 0.2 0.3 0.4 2.1 0.4 0.2 0.4 0.6

Plectus assimilis 2.0 0.7

Plectus cirratus 0.2 0.2 0.1 0.1

Plectus geophilus 0.6 0.2 0.8

Plectus longicaudatus 0.4 0.1 2.5 0.4 1.7 0.2 0.7 0.8 3.4

Plectus parietinus 1.6 0.1

Plectus parvus 0.1 0.3 0.4 0.4 0.4 2.7 3.0

Plectus rhizophilus 0.6 2.2 1.5

Table 2. (continued)

Site number 1 2 3 4 5 6 7 8 9 10 11

Ecosystem type Bee Spr Spr Gra Gra Mix Gra Gra Gra Mix Spr

Natura 2000 habitat type 91V0 9410 9410 6430 6230* 91V0 6230* 6230* 6230* 91V0 9410

Plectus silvaticus 0.1 0.7

Plectus sp. 0.3 2.5 3.3 1.8 3.4 1.7 2.3 1.5 5.2 6.9 2.7

Pratylenchoides sp. 0.0

Pratylenchus penetrans 0.1 0.6

Pratylenchus sp. 0.4 0.9 0.1 2.1

Prionchulus muscorum 0.1

Prionchulus punctatus 0.2 0.1 0.5 1.4 0.4 0.0 1.6

Prionchulus sp. 0.2 0.1 0.8

Prismatolaimus dolichurus 0.1

Prismatolaimus intermedius 0.1 0.2 0.2 0.1 0.8 2.5 0.7 0.4 2.1 0.9

Prismatolaimus sp. 0.2 0.1

Pristionchus lheritieri 0.7 0.3 0.2 0.2 0.1 0.4

Prodorylaimium brigdammense 0.1 0.3 1.8 0.9 1.8

Prodorylaimus sp. 1.7 0.1 0.1

Protorhabditis oxyuroides 0.1 1.2 0.6 1.5

Protorhabditis sp. 0.1

Pungentus silvestris 0.2 2.5 0.2 1.1 0.9

Rhabditidae dauer larvae 0.2 6.7 0.6 1.2

Rhabditis sp. 0.1 5.7 4.5 1.3 0.2 6.3 0.8 0.3

Rhabditis terrestris 3.0 0.4 0.1

Rhabdolaimus terrestris 0.2 0.1 0.1 2.6 0.1 0.2 0.2

Rotylenchus capitatus 15.0

Rotylenchus robustus 5.5 20.5 18.2

Rotylenchus sp. 17.5 3.8 7.9 34.5 8.9 5.6 6.2

Sectonema sp. 0.2

Steinernema sp. 0.2 0.4 0.4 0.9 0.1

Teratocephalus costatus 0.1 0.2 0.5 0.4

Teratocephalus sp. 0.1

Teratocephalus tenuis 0.1 0.3 0.5 0.4 0.1 0.8 0.1

Teratocephalus terrestris 0.1 0.8 1.5 8.7 0.5 0.1

Trichodorus sp. 1.3 0.1 0.7

Trichodorus sparsus 0.1 0.2 0.5

Tripyla affinis 2.0 1.8 2.7 0.1 1.6 0.2 0.4 4.1 1.4

Tripyla filicaudata 1.0 0.5 0.3 2.0 0.6 0.3

Tripyla setifera 1.0 0.6 0.6

Tripyla sp. 0.1 0.3 0.1

Tylencholaimellus sp. 0.1 2.0

Tylencholaimus minimus 4.0 0.1 3.5 0.6 1.7 6.6 2.6

Tylencholaimus mirabilis 0.3 0.5

Tylencholaimus sp. 0.4 0.3 0.1

Tylencholaimus stecki 1.0 0.5 0.7 0.4 0.3 0.6

Tylenchorhynchus sp. 1.7 0.4 0.5 1.8 0.2 0.1

Tylenchus davainei 1.2 0.8 1.5

Tylenchus sp. 0.1 3.8 0.5 0.2 3.2 0.1 0.7

Tylocephalus auriculatus 0.2 0.3 0.3 1.0 0.4 0.8

Tylolaimophorus sp. 0.3 0.1

Tylolaimophorus typicus 0.4 0.9 0.5

Wilsonema otophorum 0.1 0.4 0.6 0.3 2.2 1.7 0.3 0.2 0.5

Xenocriconemella macrodora 0.2 0.2 0.5

Xiphinema rotundatum 0.1

Xiphinema sp. 0.2

Ypsilonellus vexilliger 0.1 0.2 0.1

Table 3. Ecological parameters of the nematode communities from the Natura 2000 site Apuseni (ecosystem type

abbreviation and habitat type code as in Table 2).

Site number 1 2 3 4 5 6 7 8 9 10 11

Ecosystem type Bee Spr Spr Gra Gra Mix Gra Gra Gra Mix Spr

Natura 2000 habitat type 91V0 9410 9410 6430 6230* 91V0 6230* 6230* 6230* 91V0 9410

Total number of taxa 109 82 50 76 53 42 70 75 56 85 52

Shannon Diversity Index (Log 10) 1.483 1.4 1.428 1.498 1.461 1.348 1.343 1.297 1.401 1.446 1.176

Plant feeders (%) out of which: 52.5 45.9 44.4 46.7 15.7 15.5 54.7 51.9 34.3 35.1 57.3

Plant feeders sensu lato (%) 0.4 0.2 - 15.5 42.3 2.7 0.2 5.6 7.0 - -

Sedentary parasites (%) - - - 0.3 - - - - - - -

Migratory endoparasites (%) 0.4 1.3 - - - 2.7 1.6 0.2 6.2 0.0 0.0

Semiendoparasites (%) 10.5 44.7 41.0 37.4 24.4 - 41.9 66.5 26.0 15.9 10.7

Ectoparasites (%) 16.6 4.4 11.3 13.9 11.5 8.1 3.5 12.6 9.8 4.9 11.2

Epidermal cell and root feeders (%) 69.9 47.7 44.4 32.6 21.8 62.2 51.9 14.5 41.7 79.1 76.8

Algal, lichen or moss feeders (%) 2.3 1.7 3.4 0.3 - 24.3 0.9 0.5 9.3 0.2 1.3

Hyphal feeding (%) 9.4 8.7 9.3 9.7 13.3 2.5 7.7 13.8 8.5 13.2 4.6

Bacterial feeding (%) 22.3 25.7 33.1 17.1 36.0 34.9 17.9 15.3 45.8 37.5 20.5

Predators (%) 10.1 6.5 10.0 8.7 9.5 5.0 5.0 6.8 3.3 7.3 5.1

Unicellular eukaryote feeding (%) - - - - - - - - - - -

Insect parasites (%) - - - - - - - - - - -

Omnivorous (%) 5.7 13.2 3.2 17.9 25.2 34.9 13.7 11.4 8.1 6.9 11.3

B/F 2.37 2.95 3.56 1.76 2.72 13.83 2.31 1.11 5.40 2.83 4.48

Nematode Channel Ratio B/(B+HF) 0.70 0.75 0.78 0.64 0.73 0.93 0.70 0.53 0.84 0.74 0.82

c-p 1 (%) 4.90 8.10 6.70 3.87 2.21 7.98 2.71 2.27 11.67 6.47 4.31

c-p 2 (%) 55.1 41.9 52.6 34.1 32.8 42.4 47.4 29.9 56.4 60.0 66.0

c-p 3-5 (%) 40.0 50.0 40.7 62.0 64.8 49.2 49.5 66.9 31.8 33.5 29.7

Enrichment Index 57.6 67.9 54.4 56.7 35.3 16.9 46.2 47.7 57.7 53.1 48.1

Structure Index 86.1 85.1 70.8 90.6 87.1 87.7 83.6 86.7 64.1 75.0 81.6

Channel Index 14.0 17.1 23.2 25.0 48.7 14.3 46.5 44.0 12.1 28.3 22.8

& Schuurmans Stekhoven, 1933, Aphelenchoides sp., Bunonema reticulatum Richters, 1905, Filenchus sp., Mylonchulus brachyuris (Butschli, 1873) Altherr, 1953 and Plectus sp. were present in all of them, although in low numbers.

Eudominant (D > 10%, Tischler, 1949) nematode species were present in species-rich Nardus grasslands (6230*) (Eucephalobus oxyuroides (De Man, 1876) Steiner, 1936 and Rotylenchus capitatus Eroshenko, 1981), mixed forest (91V0) (Aporcelaimellus obtusicaudatus (Bastian, 1865) Altherr, 1968) and spruce forests (9410) (Rotylenchus robustus (De Man, 1876) Filipjev, 1936) (site nos 9, 7, 6, 2 and 3 in Table 2).

Aporcelaimus romanicus Popovici, 1978, collected from spruce forest at Calineasa (9410) (site no. 2) andMalenchuspachycephalus Andrassy, 1981, found in mixed forest (91V0) in the Ghe^ari-Scari§oara area (site no. 10) are rare species in the Romanian fauna.

Functional diversity of nematode fauna. Plant feeding nematodes, bacterial feeding nematodes and omnivores were the dominant trophic groups in the communities, whereas hyphal feeding nematodes and predators were less common. Plant feeding

nematodes were abundant (51.9-57.3%) in species-rich Nardus grasslands, beech and spruce forests (6230*, 91V0 and 9410) (site nos 1, 7, 8 and 11) (Table 3). Bacterial feeding nematodes were numerous (33.1-45.8%) in species-rich Nardus grasslands, mixed and spruce forests (6230*, 91V0 and 9410) (site nos 3, 5, 6, 9 and 10). Omnivorous were abundant (25.2% and 34.9%) in the species-rich Nardus grassland and mixed forest (6230* and 91V0) (site nos 5 and 6). Grouping samples according to Natura 2000 habitat types (Fig. 3) revealed comparable trophic structure of nematode communities in species-rich Nardus grasslands (6230*) and Dacian beech forests (91V0).

The structure of nematode communities based on coloniser-persister (c-p) scale (Table 3) showed that enrichment opportunists (c-p 1) were the least abundant nematode group in all samples, hardly reaching 11.6% of the nematode abundance. General opportunists (c-p 2) were the most numerous in spruce (9410) and mixed (91V0) forests (site nos 10 and 11), where they contributed 60-66% to the nematode abundance. Persisters (c-p 3-5) prevailed (62-66.9%) in species-rich Nardus grasslands (6230*) and in hydrophilous tall-herb

fringe communities (6430) (site nos 4, 5 and 8). Grouping nematode taxa according to c-p scale and Natura 2000 habitat types (Fig. 4) revealed the prevalence of general opportunists (c-p 2) in forest soils (91V0, 9410), whereas persisters (c-p 3-5) dominated in grasslands (6230*, 6430).

Fig. 3. Trophic structure of nematode communities according to Natura 2000 habitat types (mean values, except habitat 6430; habitat names abridged).

Enrichment Index (EI) showed a broad range of variation (16.9-67.9) and revealed contrasting resource conditions in cambic rendzina of mixed forest (91V0) (site no. 6, where the highest values of Bacterivore/Fungivore ratio (B/F) and Nematode Channel Ratio were noted) and acid brown soil of spruce forest (9410) (site no. 2) (Table 3).

Fig. 4. Structure of nematode communities based on coloniser-persister (c-p) scale according to Natura 2000 habitat types (mean values, except habitat 6430; habitat names abridged).

The values of Structure Index (SI) (64.1-90.6) characterised, in general, rather complex nematode assemblages, the one associated with hydrophilous

tall-herb fringe communities (6430) (site no. 4) being the best structured (Table 3).

The Channel Index (CI) differentiated nematode communities according to the contribution of bacterial and hyphal feeding nematodes to the decomposition pathway. Higher scores of CI (4448.7), indicating higher proportion of fungal decomposition were assessed in most species-rich Nardus grasslands (site nos 5, 7 and 8), whereas lower values of CI (12.1-17.1), implying higher proportion of bacterial decomposition were estimated in species-rich Nardus grassland (6230*) (site no. 9), beech forest (91V0) (site no. 1), mixed forest (91V0) (site no. 6) and spruce forest (9410) (site no. 2) (Table 3).

Degraded

Maturing

11

Structure Index

Fig. 5. Graphical representation of Enrichment Index and Structure Index (each quadrat corresponds to a distinct condition of soil food web) (Ferris et al., 2001); symbols indicate ecosystems types: O - beech forest, ♦ - spruce forest, ▲ - grassland (habitat 6230*), ■ -grassland (habitat 6430), • - mixed (beech and spruce) forest.

Site ordination according to nematode functional guilds along EI and SI (Fig. 5), enabled the condition of the soil food web to be determined (Ferris et al., 2001). Six sites were grouped in quadrat B (1-4, 9 and 10), implying a low to moderate degree of environmental disturbance, N-enriched, balanced decomposition channels, low C:N ratio in soil and a maturing food web. Five sites were grouped in quadrat C (5-8 and 11), suggesting undisturbed, moderately enriched environments with fungal-mediated decomposition pathway, moderate to high C:N ratio in soil and a structured food web.

The Bray-Curtis cluster analysis (Fig. 6) showed higher similarities between nematode communities in acid brown soils of spruce forests distributed at

Fig. 6. Bray-Curtis Cluster Analysis (Single Average Link); site labels as in Table 2.

Calineasa (Bihor Mountains) (site no. 2) and Chicera cu Colac (Vladeasa Mountains) (site no. 3). Less similar nematode communities were those associated with habitats located in the Ghe^ari-Scarisoara area (site nos 4-11) and Padi§ (site no. 1), both in the Bihor Mountains.

Nonmetric multidimensional scaling (nMDS) biplot (Fig. 7) illustrated a close grouping of spruce forests of various locations (site nos 2, 3 and 11), whereas grasslands were widely spread.

DISCUSSION

Previous research on free-living soil nematodes associated with different major ecosystems of several protected areas from the Romanian Carpathians revealed a diversified nematode fauna (Popovici, 1993; Popovici & Ciobanu, 1997; Ciobanu & Popovici, 1999, 2001, 2015). The total number of nematode species found in the Natura 2000 site Apuseni represents 34.2% of the number of nematode species (386) reported from Romania (Popovici et al., 2008). This may be a result of spatial heterogeneity of habitats due to the petrographic mosaic (alternation of carbonate and siliceous parent rocks and rendzinas/non-rendzinas soils), variation of vegetation cover and topo-climatic

CM

to

O

9 Gro-6230*

L

1 BefrBWO BGI»iZ30-

O i

10 Mi*91VQ * GntSMO

• +

♦ •

11 Epr-WIO A 6MK-91V0

* * 7 Gi^6230*

3 Spr-M10

A

5 Gra-6230*

-1.0

NMDS 1

2.0

Fig. 7. Non-metric multidimensional scaling (NMDS) using Bray-Curtis distances; site labels as in Table 2.

conditions associated with limestones. Spatial resource diversity as a consequence of habitat heterogeneity is known to be a driver of diversification in biotic communities, increasing functional redundance and stability of ecosystem functions (Wang & Loreau, 2014; Oliver et al., 2015) making possible niche segregation (Tokeshi, 2009). Ten nematode species new to science were

previously recorded (and tentatively considered as endemics) in the Bihorului and Vladeasa Mountains (Popovici, 1978, 1990a, b, 1995; Ciobanu et al., 2007, 2008, 2010) suggesting a hotspot of nematode diversity and possible accelerated speciation in relation to insular-like distribution of biotopes occurring there (e.g., Pop et al., 2010).

Nematode communities in the Natura 2000 site Apuseni differed according to geographical location of the sites, ecosystems and habitat types. The structure of nematode communities has been shown to be influenced by the nature of substrate, which affects soil properties, vegetation characteristics and climatic factors (Yeates, 1980; Bongers et al., 1989; Norton, 1989; de Goede, 1993; Popovici & Ciobanu, 2000; De Deyn et al., 2004; Viketoft et al., 2005; Ciobanu et al., 2015). A trend towards higher nematode taxa richness in forested habitats may suggest more abundant and heterogenous resources in relation to litter quality, although resource quality does not necessarily link to nematode richness.

This is the second report of A. romanicus Popovici, 1978 (tentatively considered an endemic species), originally described from beech-fir forest in the Vladeasa Mountains and beech forest in the Cernei Valley (Popovici, 1978) and M. pachycephalus Andrassy, 1981, collected from beech-spruce forest and spruce forest in the Some§ului Cald gorges (Ciobanu & Popovici, 2001).

The association of particular eudominant nematode taxa with certain ecosystems (grasslands and forests) and habitat types of community interest in Natura 2000 sites has been recently reported (Ciobanu & Popovici, 2015), suggesting preferences for certain environmental conditions. Several eudominant K-strategists associated with a single habitat type were found, as follows: R. capitatus Eroshenko, 1981 (species-rich Nardus grasslands, 6230*), A. obtusicaudatus (Bastian, 1865) Altherr, 1968 (Dacian beech forests, 91V0) and R. robustus (De Man, 1876) Filipjev, 1936 (acidophilous Picea forests, 9410). The omnivorous A. obtusicaudatus has potential in monitoring the condition in cambic rendzina of mixed forest at Ghe^ari-Scari§oara (site no. 6) and habitat stability, as Aporcelaimellus spp. are known to be sensitive to human environmental disturbance (Fiscus & Neher, 2002; McSorley, 2012).

Low numbers of enrichment opportunists (c-p 1) present in samples suggests organically-poor soils with low bacterial availability (de Goede et al., 1993; Bongers & Korthals, 1995; de Goede & Van Dijk, 1998) and monitoring the dynamics of abundance of this group may serve to assess soil food web nitrogen mineralisation and plant productivity (DuPont et al. , 2009) in locations

where plant species of community interest are present. General opportunists (c-p 2) and persisters (c-p 3-5) were the dominant groups in the samples, a situation that is considered to occur in natural ecosystems. Forest ecosystems favoured general opportunists, whereas herbaceous ones were more suitable for persisters, in line with previous findings (Ciobanu & Popovici, 2015). Eudominant persister species are useful indicators of soil conditions in habitats that might require priority conservation measures as they have narrow ecological ranges (Bongers & Ferris, 1999) and therefore the species belonging to Eudorylaimus have potential in monitoring soil status in the species-rich Nardus grasslands (EU-priority habitat).

EI and SI clearly differentiated conditions of the soil food webs and their use is therefore extremely valuable in monitoring the ecological status of soils after conservation measures for habitats in the Natura 2000 sites are implemented through management plans.

CI showed differences between sites and Natura 2000 habitat types, but failed to group ecosystems and Natura 2000 types based on dominant (bacterial- or fungal-mediated) decomposition pathway of organic matter in the soil food web.

The results offer further interesting perspectives to explore the relationships between the nematode fauna and plant species of community interest in the Natura 2000 sites whose conservation status needs to be monitored in Romania in the future. The analysis of nematode communities associated with Natura 2000 sites could also reveal preferences of certain nematodes for particular plant coenoses, making them useful bio-indicators, and might discriminate priority habitats from non-priority ones within the same ecosystem type.

ACKNOWLEDGEMENTS

Dr Jie Zhao (Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, China) is kindly thanked for carrying out the NMDS analysis and for providing the ordination diagram. Drs Ilie-Adrian Stoica and Bogdan-Iuliu Hurdu (Institute of Biological Research, Cluj-Napoca, Romania) are generously thanked for providing the map used in Fig. 1 (I-AS) and for the help in selecting the appropriate cluster analysis, in agreement with NMDS output (B-IH). The two anonymous reviewers are kindly acknowledged for their useful and constructive comments on an earlier draft, as is the editor for handling the manuscript. This study was funded by the Romanian Ministry of Education through the National Authority for

Scientific Research and Innovation (ANCSI) within

the national Program Nucleu (BIODIVERS 20162017).

REFERENCES

AndräSSY, I. 1984. Klasse Nematoda (Ordnungen Monhysterida, Desmoscolecida, Araeolaimida, Chromadorida, Rhabditida). Bestimmungsbücher zur Bodenfauna Europas, no. 9. Germany, Akademie Verlag. 509 pp.

Anonymous. 1979. Council Directive 79/409/EEC of 2 April 1979 on the conservation of wild birds. Official Journal of the European Union 103: 0001-0018.

Anonymous. 1992. Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Official Journal of the European Union 206: 7-50.

Anonymous. 2003. Government Decision no. 230/ of 4 March 2003 concerning the delimitation of biosphere reserves, national and natural parks and constituting their administrations. Monitorul Oficial 190:1-48.

Anonymous. 2007a. Order no. 776/ of 5 May 2007 of the Ministry of Environment and Sustainable Management for designating sites of community interest in Romania as a part of the European ecological network Natura 2000. Monitorul Oficial 615: 4-15.

Anonymous. 2007b. Interpretation Manual of European Union Habitats (EUR27 Version). 142 pp. URL: http://ec.europa.eu/ (accesed: September 23, 2015).

Bongers, T. 1988. De Nematoden van Nederland. The Netherlands, Natuurhistorische Bibliotheek van de Koninklijke Nederlandse Natuurhistorische Vereniging. 408 pp.

Bongers, T. 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83: 14-19.

Bongers, T. & Bongers, M. 1998. Functional diversity of nematodes. Applied Soil Ecology 10: 239-251.

Bongers, T. & Ferris, H. 1999. Nematode community structure as a bio-indicator in environmental monitoring. Trends in Ecology and Evolution 14: 224228.

Bongers, T. & Korthals, G. 1995. The behaviour of MI and PPI under enriched conditions. Nematologica 41: 286.

BONGERS, T., DE GOEDE, R.G.M., KAPPERS, F.I. & MANGER, R. 1989. Ecologische typologie van de Nederlandse bodem op basis van de vrijlevende nematodenfauna. RIVM Rapport 718602002, Landbouwuniversiteit, The Netherlands, 113 pp.

Bray, J.R. & Curtis, J.T. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27: 325-349.

Ciobanu, M. & Popovici, I. 1999. Diversity of soil nematode communities from the Suatu Natural Reserve. Studia Universitatis Babe§-Bolyai, Biología 44: 45-51.

Ciobanu, M. & Popovici, I. 2001. Soil nematode fauna from the upper part basin of the Some§ul Cald river. Lucrärile celei de-a XVI Conferinfe Nationale pentru §tiinja Solului, Suceava 30B: 80-86.

Ciobanu, M. & Popovici, I. 2015. Soil nematode communities in three Natura 2000 sites of the Trascäu Mountains (Romania). Annals of Forest Research 58: 311-322.

Ciobanu, M., Popovici, I., Abolafia, J. & Peña-Santiago, R. 2007. Nematodes of the order Dorylaimida from Romania. The genus Thonus Thorne, 1974. Part I. Nematology 9: 817-836.

Ciobanu, M., Popovici, I., Abolafia, J. & Peña-Santiago, R. 2008. Nematodes of the order Dorylaimida from Romania. The genus Thonus Thorne, 1974. Part II. Nematology 10: 167-188.

Ciobanu, M., Popovici, I., Guerrero, P. & Peña-Santiago, R. 2010. Nematodes of the order Dorylaimida from Romania. The genus Enchodelus Thorne, 1939. 3. Species with rounded tail and long odontostyle. Nematology 12: 609-618.

Ciobanu, M., Popovici, I., Zhao, J. & Stoica, I.-A. 2015. Patterns of relative magnitudes of soil energy channels and their relationships with environmental factors in different ecosystems in Romania. Scientific Reports 5: 17606.

Conea, A., Florea, N. & Puiu, S. 1980. Sistemul Román de Clasificare a Solurilor. Romania, Institutul de Cercetäri Pedologice §i Agronomice. 178 pp.

De Deyn, G.B., Raaijmakers, C.E. & Van der Putten, W.H. 2004. Plant community development is affected by nutrients and soil biota. Journal of Ecology 92: 824-834.

DE Goede, R.G.M. 1993. Terrestrial nematodes in a changing environment. Ph.D. Dissertation, Landbouwuniversiteit te Wageningen, Wageningen, The Netherlands, 138 pp.

de Goede, R.G.M., Bongers, T. & Ettema, C.H. 1993. Graphical presentation and interpretation of nematode community structure: c-p triangles. Mededelingen van de Rijksfakulteit Landbouwwetenschappen Gent 58: 743-750.

de Goede, R.G.M. & Van Dijk, T.S. 1998. Establishment of carabid beetle and nematode populations in a nature restoration project after the abandonment of arable land. Applied Soil Ecology 9: 355-360.

de Grisse, A.T. 1969. Redescription ou modifications de quelques techniques utilisées dans l'étude des nématodes phytoparasitaires. Mededelingen van de Rijksfakulteit Landbouwwetenschappen Gent 34: 351-369.

DuPont, S.T., Ferris, H. & Van Horn, M. 2009. Effects of cover crop quality and quantity on nematode-based soil food webs and nutrient cycling. Applied Soil Ecology 41: 157-167.

Evans, D. 2006. The habitats of the European Union habitats directive. Biology and Environment: Proceedings of the Royal Irish Academy 106B: 167-173.

Ferris, H. 2010. Form and function: metabolic footprints of nematodes in the soil food web. European Journal of Soil Biology 46: 97-104.

Ferris, H., Bongers, T. & 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.

Ferris, H., Bongers, T. & de Goede, R. 2004. Nematode faunal analyses to assess food web enrichment and connectance. in: Proceedings of the 4th International Congress of Nematology. Nematology Monographs and Perspectives, 2 (R.C. Cook & D.J. Hunt Eds). pp. 503-510. Brill, Leiden, The Netherlands.

Fiscus, D.A. & Neher, D.A. 2002. Distinguishing sensitivity of free-living soil nematode genera to physical and chemical disturbances. Ecological Applications 12: 565-575.

Gafta, D. & Mountford, J.O. 2008. Manual de Interpretare a Habitatelor Natura 2000 din Romania. Romania, Editura Risoprint. 101 pp.

Lazarova, S., Elshishka, M., Peneva, V. & Biserkov, V. 2011. Soil biodiversity in a changing environment. In: Proceedings of the International Conference "100 Years Bulgarian Soil Science". pp. 746-749. Sofia, Bulgaria, BSSS.

McAleece, N., Gage, J.D.G., Lambshead, P.J.D. & PATERSON, G.L.J. 1997. BioDiversity Professional Statistics Analysis Software (URL: http://www.sams.ac.uk/peter-lamont/biodiversity-pro/). UK, Scottish Association for Marine Science and Natural History Museum London.

McSorley, R. 2012. Ecology of the dorylaimid omnivore genera Aporcelaimellus, Eudorylaimus and Mesodorylaimus. Nematology 14: 645-663.

Montanarella, L. 2008. Towards protecting soil biodiversity in Europe: The EU thematic strategy for soil protection. Biodiversity 9: 75-77.

Neher, D.A., Wu, J., Barbercheck, M.E. & Anas, O. 2005. Ecosystem type affects interpretation of soil nematode community measures. Applied Soil Ecology 30: 47-64.

Norton, D.C. 1989. Abiotic soil factors and plant-parasitic nematode communities. Journal of Nematology 21: 299.

Oliver, T.H., Heard, M.S., Isaac, N.J., Roy, D.B., Procter, D., Eigenbrod, F., Freckleton, R., Hector, A., Orme, C.D.L., Petchey, O.L. &

Proenqa, V. 2015. Biodiversity and resilience of ecosystem functions. Trends in Ecology and Evolution 30: 673-684.

Pop, A.A., Pop, V.V. & Csuzdi, C. 2010. Significance of the Apuseni Mountains (the Carpathians) in the origin and distribution of Central European earthworm fauna: (Oligochaeta: Lumbricidae). Zoology in the Middle East 51: 89-110.

Popovici, I. 1978. New nematode species (Nematoda, Dorylaimida) from Romania. Nematologica 24: 404411.

Popovici, I. 1990a. New and known nematode species (Nematoda: Dorylaimida) from Romania. Nematologica 35: 438-454.

Popovici, I. 1990b. Studies on Mononchida (Nemata) from Romania. Nematologica 36: 161-180.

Popovici, I. 1993. Structura §i dinamica comunitä^ilor de nematode. In: Parcul National Retezat: Studii Ecologice (I. Popovici Ed.). pp. 200-214. Bra§ov, Romania, Editura West Side Computers.

Popovici, I. 1995. New species of Tubixaba and Enchodelus (Nematoda: Dorylaimida) from Romania. Nematologica 41: 435-448.

Popovici, I. & Ciobanu, M. 1997. Nematode diversity of vegetated cliffs of the Romanian Carpathians. In: Proceedings of the "Research, Conservation, Management" Conference, Volume 1 (E. Toth Ed.). pp. 447-459. Aggtelek, Hungary, Aggtelek National Park Directorate.

Popovici, I. & Ciobanu, M. 2000. Diversity and distribution of nematode communities in grasslands from Romania in relation to vegetation and soil characteristics. Applied Soil Ecology 14: 27-36.

Popovici, I., Ciobanu, M. & Pena-Santiago, R. 2008. Soil and Freshwater Nematodes (Nematoda) from Romania: a Compendium (Collection "Monographic Papers on Nematology", 4). Spain, Servicio de Publicaciones de la Universidad de Jaén. 142 pp.

Sánchez-Moreno, S. & Ferris, H. 2007. Suppressive service of the soil food web: effects of environmental management. Agriculture, Ecosystems and Environment 119: 75-87.

Sánchez-Moreno, S., Smukler, S., Ferris, H., O'geen, A.T. & Jackson, L.E. 2008. Nematode diversity, food web condition, and chemical and physical properties in different soil habitats of an organic farm. Biology and Fertility of Soils 44: 727-744.

Sánchez-Moreno, S., Ferris, H., Young-Mathews, A., Culman, S.W. & Jackson, L.E. 2011. Abundance, diversity and connectance of soil food web channels along environmental gradients in an agricultural landscape. Soil Biology and Biochemistry 43: 2374-2383.

TER Braak, C.J.F. & Smilauer, P. 2012. Canoco Reference Manual and User's Guide: Software for

Ordination (Version 5.0). The USA, Microcomputer Power. 496 pp.

Tischler, W. 1949. Grundzüge der terrestrischen Tierökologie. Germany, Friedrich Vieweg und Sohn. 219 pp.

TOKESHI, M. 2009. Species Coexistence: Ecological and Evolutionary Perspectives. The USA, John Wiley & Sons, Inc. 464 pp.

Turbé, A., De Toni, A., Benito, P., Lavelle, P., Lavelle P., Camacho, N.R., Van Der Putten, W.H., Labouze, E. & MUDGAL, S. 2010. Soil biodiversity: functions, threats and tools for policy makers. Final Report for European Commission DG Environment, Paris, France, 250 pp.

Vanden Borre, J., Paelinckx, D., Mücher, C.A., Kooistra, L., Haest, B., De Blust, G. & Schmidt, A.M. 2011. Integrating remote sensing in Natura 2000 habitat monitoring: Prospects on the way forward. Journal for Nature Conservation 19: 116-125.

Viketoft, M., Palmborg, C., Sohlenius, B., Huss-Danell, K. & Bengtsson, J. 2005. Plant species

effects on soil nematode communities in experimental grasslands. Applied Soil Ecology 30: 90-103.

Vonk, J.A., Breure, A.M. & Mulder, C. 2013. Environmentally-driven dissimilarity of trait-based indices of nematodes under different agricultural management and soil types. Agriculture, Ecosystems and Environment 179: 133-138.

Wang, S. & Loreau, M. 2014. Ecosystem stability in space: a, P and y variability. Ecology Letters 17: 891-901.

Yeates, G.W. 1980. Relation of generic nematode populations to soil and plant parameters. Journal of Nematology 12: 242-243.

Yeates, G.W., Bongers, T., de Goede, R.G.M., Freckman, D.W. & Georgieva, S.S. 1993. Feeding habits in soil nematode families and genera - An outline for soil ecologists. Journal of Nematology 25: 315-331.

M. Ciobanu and I. Popovici. Структурное и функциональное разнообразие фауны нематод, ассоциированных с различными местами обитания на участке «Natura 2000» в Национальном парке Апушени в Румынии.

Резюме. Изучение почвенных проб из луговых (n=5) и лесных (n=6) биотопов в Национальном парке Апушени выявило 191 таксон почвообитающих нематод (132 вида). Фауна нематод различалась в зависимости от местоположения точек отбора образцов, типов биоценоза и местобитаний. Выявлено, что почвенная нематодофауна лесных участков более разнообразна по сравнению с лугами. В сообществах нематод доминировали нематоды, ассоциированные с растениями, бактериотрофы и всеядные нематоды. Бактериотрофы со значением 2 по c-p-шкале Бонгерса (оппортунисты) чаще встречались в лесных почвах, тогда как нематоды с высокими (4, 5) c-p-значениями (персисторы) были более многочисленны в пробах из луговых биоценозов. Значения эколого-популяционных индексов, рассчитанных на основе сообществ нематод, свидетельствуют о наличии зрелой и структурированной почвенной трофической сети в исследованных биоценозах Национального парка. Показано, что использование индекса, характеризующего превалирующий путь разложения органического вещества в почвенной экосистеме, не позволяет разграничивать типы экосистем и местообитаний.