Introduction Material and methods

Applied Soil Ecology 14 2000 27–36 Diversity and distribution of nematode communities in grasslands from Romania in relation to vegetation and soil characteristics Iuliana Popovici ∗ , Marcel Ciobanu Institute of Biological Research, PB 229, 3400 Cluj-Napoca, Romania Received 8 February 1999; received in revised form 8 October 1999; accepted 12 October 1999 Abstract The nematode communities of 36 grassland ecosystems in Romania, belonging to different plant associations and soil types, were studied. The abundance of nematodes, the species and trophic types present, as well as their distribution in relation to plant community and soil characteristics are analyzed and discussed. The abundance of nematodes from the 36 grasslands studied ranged between 0.41 × 10 6 and 8.57 × 10 6 individualsm 2 , and a total of 121 genera and 145 species of nematodes were found. The highest diversity was found in grasslands developed on brown earth soil 65–67 genera and 74–76 species, with least diversity in those evolving on podzol and lithosol 33–36 genera with 25–28 identified species. Most of the dominant taxa were found in specific soil layers; some obligate plant parasitic genera e.g., Paratylenchus, Rotylenchus, Criconema showed preference for deeper soil layers. The nematode diversity index H ′ , with values ranging between 2.38 and 3.47, did not differ significantly between the different types of grasslands. Plant feeding, bacterial feeding, hyphal feeding and omnivorous nematodes were the main groups in mountainous grasslands developed on different soil types. Plant feeding and bacterial feeding nematodes dominated the trophic structure and more plant feeders 62–69 were found in communities of subalpine and alpine grasslands developed on podzol and alpine meadow soil, than in those developed on rendzina and lithosol 27–33. The ratio of hyphal feeding to bacterial feeding nematodes HfBf is constantly in favour of the bacterial feeding group, the values being an indicator of good soil fertility for most studied grasslands. The nematode communities of grasslands are grouped into six main clusters according to their genera affinity and distinguished by different grassland and soil types. Communities from subalpine grasslands developed on rendzina, acid brown and lithosol have the greatest similarities. An ordination of nematode communities in relation to important environmental variables is presented. Environmental variables relevant in explaining the patterns of nematode composition in grasslands, using canonical correspondence analysis CCA, are: humus, pH, total nitrogen, exchangeable bases and soil type. No single factor could be selected. ©2000 Elsevier Science B.V. All rights reserved. Keywords: Nematode community structure; Clusters; CCA; Grasslands; Soil variables

1. Introduction

Better information on the soil nematode fauna of natural ecosystems or ecosystems that are relatively ∗ Corresponding author. Tel.: +40-64-191238; fax: +40-64-191238. E-mail address: icbmail.dntcj.ro I. Popovici. undisturbed by human activities is providing useful insights into soil conditions in terrestrial habitats Norton and Niblack, 1991; Hodda and Wanless, 1994b. The analysis of nematode community struc- ture is being used more frequently as a tool in ecolog- ical studies Bongers, 1990. Pertinent multivariate analyses of nematode fauna in relation to environ- mental variables have been published by De Goede 0929-139300 – see front matter ©2000 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 9 - 1 3 9 3 9 9 0 0 0 4 8 - 7 28 I. Popovici, M. Ciobanu Applied Soil Ecology 14 2000 27–36 Fig. 1. Geographical distribution using UTM grid of the 36 grasslands studied in Romania. A and B are enlarged areas; the numbers represent site numbers. 1993, De Goede and Bongers 1994 and Hanel 1995. A recent monographic compilation of the nema- tode faunal lists and soil conditions from grasslands in Europe 41 datasets and the USA three datasets, available also on a CD-disk, represents the most avail- able up-to-date information on these communities on a large geographical scale De Goede and Bongers, 1998. This work includes 32 sites from Romania Popovici, 1998. These data have not yet been anal- ysed or synthesized. In the present paper an analy- sis of the dataset from Romania including data from four additional sites Popovici and Ciobanu, 1998 is made. The paper describes nematode abundance, di- versity and affinity for specific plant associations and soil characteristics from all 36 investigated mountain grassland ecosystems in Romania. An extensive study on nematode communities from one protected area in Romania including data from both natural forest and grassland ecosystems has been presented previously Popovici, 1993.

2. Material and methods

2.1. Site descriptions The 36 grasslands Fig. 1 were distributed at altitudes from 350 to 2270 m above sea level and represented 15 different plant associations developed on different soil types Table 1. Half of the sites were sampled in the last decade, and 10 others be- tween 1981–1989, during an ecological project on the Carpathian fauna. The code of sites, given in Table 1, comprises a number for site 1–36 and an abbreviation for the mountainous massif e.g., 1 Bih = site no. 1 from the Bihor Mountains. Plant association is given according to Coldea 1991, 1997. Soil classification is given according to Conea et al. 1980. To avoid overcrowding of data on Fig. 1 and 3, the sites are represented only by their corresponding number. I. Popovici, M. Ciobanu Applied Soil Ecology 14 2000 27–36 29 Table 1 Sites descriptions Site No. Place Elevation m above sea level Soil type Plant association a 1 Bih Bihor Mts. b 1250 Brown earth Festuco rubrae –Agrostetum 2 Bih Bihor Mts. 1000 Rendzina Lolio –Trifolietum repentis 3 Bih Bihor Mts. 1000 Alluvial vermic soil Lolio –Trifolietum repentis 4 Vla Vladeasa Mts. 1400 Acid brown,andic soil Scorsonero –Festucetum nigricantis 5 Vla Vladeasa Mts. 1400 Feriilluvic podzol Scorsonero –Festucetum nigricantis 6 Vla Vladeasa Mts. 1640 Acid brown soil Scorsonero –Festucetum nigricantis 7 Vla Vladeasa Mts. 1400 Acid black,andic soil Scorsonero –Festucetum nigricantis 8 Vla Vladeasa Mts. 1250 Acid brown, andic soil Festuco rubrae –Agrostetum 9 Vla Vladeasa Mts. 1550 Rendzina Seslerietum rigidae 10 Vla Vladeasa Mts. 1100 Brown podzolic soil Violo declinatae –Nardetum 11 Tra Trascau Mts. 400 Lithic rendzina Melico –Phleetum montani 12 Tra Trascau Mts. 400 Rendzina Agrostio –Festucetum sulcatae 13 Tra Trascau Mts. 430 Acid brown soil Festuco rubrae –Agrostetum 14 Tra Trascau Mts. 675 Brown earth soil Asperulo capitatae –Seslerietum rigidae 15 Met Metaliferi Mts. 500 Brown earth soil Festuco rubrae –Agrostetum 16 Clu Cluj county 350 Chernozem Jurineo transsilvanicae –Stipetum pulcherimae 17 Sem Semenic Mts. 1380 Alpine meadow soil Festuco rubrae –Agrostetum 18 Cer Cernei Mts. 950 Typic lithosol Festuco rubrae –Agrostetum 19 Meh Mehedinti Mts. 970 Terra rossa Festuco rubrae –Agrostetum 20 Ret Retezat Mts. 1050 Acid black soil Festuco rubrae –Agrostetum 21 Ret Retezat Mts. 1100 Brown earth soil Festuco rubrae –Agrostetum 22 Ret Retezat Mts. 1830 Alpine meadow soil Campanulo –Juniperetum 23 Ret Retezat Mts. 1765 Typic lithosol Poetum mediae 24 Ret Retezat Mts. 1850 Acid brown soil Potentillo –Festucetum airoidis 25 Ret Retezat Mts. 1700 Rendzina Festucetum xanthinae 26 Ret Retezat Mts. 1850 Rendzinic lithosol Festucetum xanthinae 27 Par Parang Mts. 2050 Lithic podzol Violo declinatae –Nardetum 28 Par Parang Mts. 1850 Alpine meadow soil Violo declinatae –Nardetum 29 Ciu Ciucas Mts. 1500 Cambic rendzina Violo declinatae –Nardetum 30 Has Hasmas Mts. 1400 Acid brown soil Scorsonero –Festucetum nigricantis 31 Has Hasmas Mts. 1100 Acid brown soil Diantho –Festucetum amethistinae 32 Rod Rodnei Mts. 2270 Alpine meadow soil Primulo –Caricetum curvulae 33 Cal Caliman Mts. 1000 Argillic brown soil Scorsonero –Festucetum nigricantis 34 Cal Caliman Mts. 600 Argillic brown soil Potentillo –Festucetum airoidis 35 Bar Bargau Mts. 950 Argillic brown soil Festuco rubrae –Agrostetum 36 Gur Gurghiu Mts. 700 Acid black soil Festuco rubrae –Agrostetum a According to Coldea, 1991, 1997. b Mts. = Mountains. 2.2. Sampling, extraction, identification Five samples were taken separately from the sod layer and the A soil horizon, with an open corer 15 cm in length and 2.2 cm in diameter, down to a depth 10 or 15 cm. Each sample consisted of eight cores taken from 10 m 2 area and mixed for each soil layer. The centrifugation method De Grisse, 1969 was used for nematode extraction from each bulk sample the mixed cores from each soil layer. Nematodes were counted before fixing in 4 formaldehyde solu- tion. At least 150 individuals were identified for the five samples of each soil layer. The classification system is according to Andrássy 1984, Siddiqi 1986 and Bongers 1988 where appropriate and the contri- bution of trophic groups is established according to Yeates et al. 1993. 2.3. Data analysis Nematode abundance was estimated by counting the five replicate samples for each soil layer and adjust- ing to numbers per m 2 . The data set for relative abun- 30 I. Popovici, M. Ciobanu Applied Soil Ecology 14 2000 27–36 Table 2 The diversity index H ′ , numbers of taxa genera + species, abundance and trophic group ratios for nematode communities in Romanian grasslands a Site H ′ No. taxa Abundance No × 10 6 m 2 Ratio Bf + HfOPP OPPPf HfBf 1 Bih 3.35 98 0.98 1.4 0.4 0.4 2 Bih 2.48 83 0.80 1.4 0.3 0.2 3 Bih 2.98 76 0.59 3.7 0.4 0.2 4 Vla 2.90 52 1.44 2.7 0.7 0.1 5 Vla 2.87 56 3.13 1.5 0.3 0.3 6 Vla 2.38 50 3.25 5.0 1.0 0.1 7 Vla 3.19 63 1.72 2.2 0.5 0.4 8 Vla 3.32 75 1.01 1.7 0.6 0.3 9 Vla 3.47 67 0.97 1.7 0.5 0.4 10 Vla 2.60 76 1.20 3.9 0.8 0.2 11 Tra 3.12 58 9 0.6 0.4 0.5 12 Tra 2.81 62 0.81 3.2 0.6 0.6 13 Tra 2.60 50 0.60 0.5 0.7 0.8 14 Tra 2.83 61 0.77 0.4 0.6 0.3 15 Met 3.33 97 0.67 3.8 0.6 0.6 16 Clu 3.04 68 0.84 2.2 0.3 0.2 17 Sem 3.13 61 3.55 2.1 0.7 0.4 18 Cer 2.86 40 2.35 2.1 0.4 0.2 19 Meh 2.94 56 1.72 4.4 0.5 1.0 20 Ret 3.30 77 1.93 1.3 0.4 0.2 21 Ret 3.11 99 1.12 4.9 0.5 0.6 22 Ret 3.05 67 0.41 2.4 0.8 0.5 23 Ret 2.80 80 1.60 6.5 0.3 0.5 24 Ret 2.65 70 1.62 4.8 0.2 0.8 25 Ret 3.07 88 0.56 10.9 0.2 0.3 26 Ret 2.94 88 0.74 17.5 0.1 0.4 27 Par 2.65 46 1.35 0.8 0.6 0.1 28 Par 2.85 60 0.68 2.8 0.4 0.3 29 Ciu 3.33 70 4.26 4.4 0.6 0.3 30 Has 3.45 78 0.57 3.2 0.6 0.4 31 Has 3.26 54 3.24 2.9 0.6 0.3 32 Rod 2.66 55 8.57 2.0 0.2 0.3 33 Cal 3.44 82 1.03 2.1 0.4 0.3 34 Cal 3.31 67 0.83 1.7 0.6 0.2 35 Bar 3.08 80 0.54 1.7 0.3 0.4 36 Gur 3.16 71 3.24 3.4 0.9 0.1 a Bf + HfOPP — ratio of bacterial and hyphal feeding nematodes to obligatory plant parasites, OPPPf — ratio of obligatory plant parasites to total plant feeding nematodes, HfBf — ratio of hyphal feeding to bacterial feeding nematodes. dance of genera, Shannon’s diversity index H ′ and similarity of nematode communities were analyzed using the BIODIV program Baev and Penev, 1995. The ordination of samples 32 sites, nematode genera and their relationships with environmental variables were analyzed by the canonical correspondence anal- ysis method CCA using the CANOCO program Ter Braak, 1986, 1987. The genera abundance data were transformed to logx + 1. Four sites nos. 13, 14, 17 and 22, without environmental data, were left out of the CCA analysis.

3. Results