Spatial and temporal dynamics of nematode populations under Zygophyllum dumosum in arid environments

European Journal of Soil Biology 40 (2004) 31–46 www.elsevier.com/locate/ejsobi

Original article

Spatial and temporal dynamics of nematode populations under Zygophyllum dumosum in arid environments Stanislav Pen-Mouratov a, Mirza Rakhimbaev b, Ginetta Barness a, Yosef Steinberger a,* a

Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 52900, Israel b Institute of Botany, Tashkent, Uzbekistan Received 25 August 2003; accepted 12 January 2004

Abstract Soil nematode activity in arid ecosystems is determined by well-known limiting factors such as soil moisture and organic matter. The main aim of our investigation was to determine the composition and distribution of the nematode community in response to soil water and organic content in the rhizosphere of the perennial plant Zygophyllum dumosum. The results demonstrated that soil moisture, organic matter, total nematode population and trophic groups differed under the plants and in the control samples. Significant differences in soil moisture, total nematode population and trophic groups were observed. Bacterial-feeders were found to be the dominant nematode trophic group at the research sites. Bacterial- and fungi-feeders were present in the upper 0–10 cm layer during most of the year. A negative correlation was found between nematodes and soil moisture and a positive correlation was found between nematodes and organic matter. Moreover, trophic structure changes and quantity changes in the nematode community were observed within 1 month after quantitative changes occurred in the organic matter. Generally accepted nematode fauna indices such as Wasilewska index (WI), F/B, T, H′, k, species richness (SR), PPI, maturity index (MI), and modified maturity index (MMI), reflect the temporal changes that occurred in the nematode community during the research period. This study illustrates the integrated effect of soil moisture and organic matter on the activity and structure of the nematode communities existing under plants. © 2004 Elsevier SAS. All rights reserved. Keywords: Free-living nematodes; Trophic groups; Halophytes; Ecological indices; Desert ecosystem

1. Introduction Free-living soil nematode communities represent the most abundant multicellular animal group on earth and are known to be an important component of the soil biota [5,29]. The abundance of nematodes in soil generally reaches several million individuals per square meter. Nematodes have a remarkable ability to resist environmental stress [23]. Certain community parameters such as density, biomass, and species diversity, therefore, tend to change locally on a temporal and * Corresponding author. Tel.: +972-3-531-8571; fax: +972-3-535-1824. E-mail address: [email protected] (Y. Steinberger). © 2004 Elsevier SAS. All rights reserved. doi:10.1016/j.ejsobi.2004.01.002

spatial scale along with changes in vegetation type. Because they intervene to a great extent in trophic chains in ecosystems, nematodes contribute substantially to soil formation and to the maintenance of soil fertility. The distribution and density of the nematode community has been found to correlate with plant distribution in different terrestrial ecosystems, including arid ecosystems [33]. Soil temperature, soil moisture [41], and organic matter content [38] have been found to be important factors directly or indirectly affecting seasonal population dynamics in the soil by altering the metabolic activity and quality of the food source. An additional important feature is the nematodes’ daily and seasonal vertical migration, which has been found to be controlled mainly by

32

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

physical–chemical soil factors such as moisture content, temperature, and texture [1,33,41]. Moreover, the major part of the nematode community can be found in the upper, densely rooted 0–10 cm soil layer [45]. However, some species, which are sensitive to dehydration, are often found in the deeper soil layers [11]. Since the soil nematode population responds to changes in environmental factors, it can be a useful indicator of soil conditions [45]. According to Bongers and Ferris [6], the development of nematode indices that integrate the responses of different taxa and trophic groups to perturbation provides a powerful basis for analysis of faunal assemblages in soil as in situ environmental assessment systems. Ecological indices of nematode community structure such as richness [44] genus dominance [28], as well as trophic diversity [16] and the Shannon–Weaver [27] indices are useful for the detection of changes occurring in the habitat. One of the potential parameters for measuring the impact of disturbances and monitoring changes in the structure and function of the below-ground ecosystem is the nematode maturity index (MI); an index based on the proportion of colonizers (r-strategists s.l.) and persisters (K-strategists s.l.) in the soil samples [4,42]. The objective of this study was to evaluate the response of nematode community ecological indices to spatial and temporal abiotic perturbations in the Zygophyllum dumosum plant rhizosphere in an arid ecosystem.

2. Materials and methods 2.1. Study site The fieldwork in this study was conducted at the Avdat Research Farm in the Negev highland (30°47′N; 34°46′E). This area has a temperate desert climate, i.e. mild, rainy winters (5–14 °C in January) and hot, dry summers (18– 32 °C in June). Radiation may reach 3.14 × 104 kJ m–2 d–1. The average annual rainfall is 90 mm. However, rainfall fluctuates between 20 and 180 mm. An additional source of moisture comes from approximately 35 mm of dew, which falls each night but most heavily during late summer and autumn. The perennial vegetation is dominated by the desert shrub association, in which the most common species is Z. dumosum [25,33]. The soil is a deep, fine-textured loessial sierozem [9].

kept in cold storage at 4 °C until processed. They were sieved (2-mm mesh size) before biological and chemical analysis in order to remove root particles and other organic debris. 2.3. Laboratory analysis A minimum of 5 g soil from each sample at each depth was used for soil moisture and organic matter determination. The weighed soil samples were dried at 105 °C for gravimetrical determination of soil water content, followed by organic matter determination by oxidization with dichromate in the presence of H2SO4, without application of external heat [24]. The nematodes were extracted from 100 g soil samples using the Baermann funnel procedure [8]. The recovered organisms were counted, preserved in formalin [35], and identified according to order, family and genus (if possible), using a compound microscope. 2.4. Ecological indices and statistical analysis The characteristics of the nematode communities were described using the following indices: (1) absolute abundance of individuals 100 g–1 dry soil; (2) abundance of omnivores-predators (OP), plant-parasitic (PP), fungalfeeding (FF) and bacterial-feeding (BF) nematodes (trophic structure) [20,33,35]; (3) Wasilewska index (WI), WI = (FF + BF)/PP [37]; (4) fungivore/bacterivore ratio (F/B), F/B = FF/BF [36]; (5) trophic diversity (T), T = 1/兺 Pi2, where Pi is the proportion of the i-th trophic group [16]; (6) genus dominance (k), k = 兺 Pi2 [28]; (7) Shannon index (H′), H′ = –兺 Pi(ln Pi), where P is the proportion of individuals in the i-th taxon [27]; (8) maturity index (MI), MI = 兺 tiqi, where ti, is the c-p value assigned by Bongers [4] of the i-th genus in the nematode and qi, the proportion of the genus in the nematode community. The c-p values describe the nematode life strategies, and range from 1 (colonizers, tolerant to disturbance) to 5 (persisters, sensitive to disturbance); (9) modified maturity index (MMI), including plant-feeding nematodes [42]; (10) evenness (J′), J′ = H′/ln(S), where S is the number of taxa; and (11) species richness, SR = (S – 1)/ln(N), where S is the number of taxa and N is the number of individuals identified [44]. All data were subjected to statistical analysis of variance using the SAS model (ANOVA, Duncan’s multiple range test and Pearson correlation coefficient) and were used to evaluate differences between separate means. Differences obtained at levels of P < 0.05 were considered significant.

2.2. Sampling A total of 352 soil samples from two layers (0–10 and 10–20 cm) and two sites [under Z. dumosum and between the shrubs (control)], were collected between November 1999 and November 2001. Soil samples were collected in individual plastic bags, which were placed in an insulated container and taken to the laboratory. These soil samples were

3. Results 3.1. Soil moisture and organic matter The distribution of soil moisture and monthly rainfall at the study site is presented in Fig. 1, and indicates severe

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46 30

26.45

Rainfall (mm)

20

A

24.1

25

33

19.5

15 10

7.7

6.2

7.7 3.1 3.1

5

0.75

0.2

N

ov . D 99 ec . Ja 99 n. F e 00 b. M 00 ar . A 00 pr M .00 ay . J u 00 n. 0 Ju 0 l A .00 ug . Se 0 0 p. O 00 ct . N 00 ov . D 00 ec . J a 00 n. Fe 01 b. M 01 ar . A 01 pr M .01 ay . Ju 01 n. 0 Ju 1 l A .01 ug . Se 0 1 p. O 01 ct . N 01 ov .0 1

0

B

8

9

6 6 4 3

2 0

Soil moisture (%)

12

Z. dumosum 10 - 20 cm

C

10 8

9

6 6 4 3

2

0

0

12

10

Control 0 - 10 cm

D 8

9

Soil moisture (%)

Organic matter (%)

0

6 6 4 3

2

0

0

12

Control 10 - 20 cm

E

10

6 6 4 3

Organic matter (%)

8

9 Soil moisture (%)

10 Organic matter (%)

Z. dumosum 0 - 10 cm

Organic matter (%)

Soil moisture (%)

12

2

0 Nov.99

Feb.00

May.00

Aug.00

Nov.00

Feb.01

May.01

Aug.01

0 Nov.01

Time (months) Fig. 1. Rainfall distribution (A), changes in percentage of soil moisture (h) and organic matter (◆) at 0–10 and 10–20 cm soil layers beneath Z. dumosum shrubs and control sites during the study period.

34

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

periods of drought before the rainy season (winter 1999– 2000), between May 2000 and October 2000, and after the rainy season—between March 2001and November 2001. The total amount of rainfall at the study site was 26.9 mm during the winter of 1999–2000 and 72.9 mm during the second year, between October 2000 and April 2001. These amounts accounted for 29.8% and 81.0% of the multi-annual average for the first and second winter, respectively. During the first year, the main shower events were concentrated in January with 20.5 mm, and in March, with one 6.2 mm shower. Six showers occurred during the second rainy season, with the highest amount obtained in October with 24.1 mm, the second in January with 26.5 mm. Two events of 7.7 mm and two of 3.1 mm occurred between the big events and after the rainy season, in April 2001. Soil moisture at the two sampling locations and the two depths was found to be low and constant (1.3–2.6% under the shrubs and 1.0–2.5% between the shrubs), except during the rainy season. Significant differences in soil moisture content were observed between the two sampling sites (P < 0.05; n = 268), depths (P < 0.05; n = 268) and years (P < 0.05; n = 268) (Fig. 1B–E). Soil moisture content during the study period reached a maximum of 7.6% in the upper (0–10 cm) layer and 10.3 mm in the 10–20 cm layer under the shrubs. In the open spaces between the shrubs, the mean maximum soil moisture measured was 7.9% and 7.3% in the upper and lower layers, respectively. Soil moisture was found to be higher (P < 0.05; n = 352) on a yearly basis in the lower 10–20 cm layer at both sampling sites under and between the shrubs than in the upper (0–10 cm) layer. A relatively higher moisture level was maintained for a longer period of time with mean yearly values of 3.3% and 2.7%, respectively. Soil organic matter content was found to be significantly different (P < 0.05; n = 268) between 2 years and the two sampling sites. However, no significant differences were found between the two soil layers (Fig. 1B–E). Higher organic matter levels were obtained in October 2000 towards the end of autumn, reaching a mean value of 8.5% in the upper layer under the shrubs. The organic matter content was found to be approximately 70–90% higher in autumn than during the other three seasons. During the second year the percentage of organic matter under and between shrubs as well as in both layers was found to be 1% and lower, although the total amount of rainfall was significantly higher than during the first year. 3.2. Nematode communities The total number of soil free-living nematodes during the study period ranged from 2 to 952 individuals 100 g–1 dry soil (Fig. 2). Significant differences (P < 0.01) were found between the years, locations (P < 0.01), and depths (P < 0.01). Seasonality was an additional variable that exhibited (P < 0.05) differences, with spring and summer values being significantly higher (P < 0.01; f = 10.8; n = 336) than the autumn and winter values.

The difference in the total number of nematodes during the study period, as presented in Fig. 2, elucidates this difference on a temporal as well as on a spatial scale. The total number of nematodes exhibited different maximum and minimum frequencies during the investigation period. During the period between November 1999 and November 2000, the mean total number of nematodes was maximal under the plants in the upper soil layer in March (671 individuals 100 g–1 soil) and in the lower layer in April (440 individuals 100 g–1 soil). The total number of nematodes reached a minimum density in January and February (2.0 and 79.4 individuals 100 g–1 soil, respectively) in both soil layers. During the second year (from November 2000 to November 2001), the total number of nematodes reached a mean maximum in autumn (August, 952 individuals 100 g–1 soil and November, 920 individuals 100 g–1 soil) under the plants in the upper soil layers. During the same period, the total number of individuals decreased to minimal values in February in both soil layers under the plants (79 and 81 individuals 100 g–1 soil, respectively). The change in the total nematode population in the control plot (between the shrub canopies) (Fig. 2) oscillated from 3 to 239 during the first year (November 1999–November 2000). The nematode population varied from 2 to 264 individuals 100 g–1 soil in the 0–10 cm and in the 10–20 cm layers, respectively. During the second year (November 2000–November 2001), the mean minimum nematode population in the upper layer was approximately 20-fold higher than during the previous year in both layers, with a maximum of 210 and 176 individuals 100 g–1 soil in the upper (0– 10 cm) and the lower (10–20 cm) layers, respectively. 3.3. Nematode trophic groups A total of 33 genera were found, including 11 bacterivores, four fungivores, 10 plant-parasites and eight OP (Table 1). The BF, FF, plant-parasite and OP trophic groups exhibited significant temporal as well as spatial fluctuations throughout the study period (Fig. 3). BF groups were found to be the most abundant trophic group under the shrubs in both layers throughout the study period (Fig. 3 ABF, BBF), reaching a mean density of 41.9% of the total nematode population (Table 1). Changes in relative abundance were observed on a temporal and spatial basis. During May 2000 and June 2001the total bacterialfeeders in the upper (0–10 cm) soil layers at both sampling sites reached a maximum level of 432 and 471 individuals 100 g–1 soil, respectively, under the shrubs. Two hundred and eighty-one and 466 individuals 100 g–1 soil, respectively, were observed at the control site. The nematode population density was lower (P < 0.05) in the deeper (10–20 cm) layers at both sampling sites, reaching maximal levels of 86 individuals 100 g–1 soil throughout the study period. The differences in the total amount of rainfall and its distribution between the two years had a strong effect on the BF population. During the second year, at the end of the

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

Year 1999 - 2000

Year 2000 - 2001 Z. dumosum 0 - 10 cm

Z. dumosum 0 - 10 cm Nov.99 1000

Nov.00

Dec.99

800

Oct.00

Nov.00 1000 800 600 400 200 0

Nov.01

Jan.00

600

Oct.01

400 200

Sep.00

Feb.00

Sept.01

0

Aug.00

Mar.00 Apr.00

Jul.00 Jun.00

Apr.01

Jun.01

Nov.01

Jan.00

600

Oct.01

400 200

Sep.00

Feb.00

0

Aug.00

Mar.00

Jul.00

Apr.00

Jun.00

Sept.01

Jul.01

Oct.00

Nov.01

Jan.00

Oct.01

400 200

Sep.00

Feb.00

0

Aug.00

Mar.00

Jul.00 Jun.00

Apr.00 May.00

Sept.01

Nov.00 1000 800 600 400 200 0

Oct.00

800

Jul.01 Jun.01

Jan.00

Apr.01 May.01

1000

Oct.01

800

Dec.00 Jan.01

600 400

200

Feb.00

0

Aug.00

Mar.00

Jun.00

Feb.01

Nov.00 Nov.01

400

Jul.00

Jan.01

Control 10 -20 cm

Dec.99

600

Sep.00

Dec.00

Mar.01

Nov.99 1000

May.01

Aug.01

Control 10 -20 cm Nov.00

Feb.01

Z. dumosum 10 - 20 cm

Dec.99

600

Jan.01

Apr.01

Jun.01

Nov.99 800

Dec.00

Mar.01

May.00

1000

Nov.00 1000 800 600 400 200 0

Aug.01

Z. dumosum 10 -20 cm Nov.00

May.01

Control 0 - 10 cm

Dec.99

800

Feb.01

Jul.01

Nov.99

Oct.00

Jan.01

Mar.01

May.00

1000

Dec.00

Aug.01

Control 0 -10 cm Nov.00

35

Apr.00 May.00

200

Sept.01

Feb.01

0

Aug.01

Mar.01

Jul.01 Jun.01

Apr.01 May.01

Fig. 2. Changes in total nematode population in the soil associated with Z. dumosum perennial shrub and control inter-shrub samples at 0–10 and 10–20 cm soil layers during the study period 1999–2001.

rainfall season, the bacterial-feeder population was represented by over 60% of the entire population (Fig. 3(3.1) ABF, BBF). In eight out of nine monthly samplings from beneath the shrubs, taken between May 2001 and November 2001, the population size was represented by a bacterial-feeder population of 200 individuals 100 g–1 soil and more. Only in September was the population found to be 115 individuals

100 g–1 soil. Similar trends occurred in the control intershrub sampling sites, with differences (P < 0.05) in population size. The mean abundance was 50–70% lower than in the upper layer of the shrub rhizosphere, so that in some cases they were as abundant as the fungi-feeders. The fungivore population under Z. dumosum and from the control plots fluctuated slightly during the 2-year period,

36

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

Table 1 Mean relative abundance (% monthly) of soil nematodes under Z. dumosum and control at two depths (0–10 and 10–20 cm) during the study period Month

November Plant

Depth (cm)

a

1

2

December Control

Plant

1

1

2

2

January Control

Plant

1

1

2

2

February Control

Plant

1

1

2

2

March Control

Plant

1

1

2

2

April Control

Plant

1

1

2

Control 2

1

2

Genus/family Bacterivores

c-p 63.6 53.8 20.4 29.7 63.7 62.4 19.5 17.4 51.0 67.8 35.5 44.6 36.3 53.7 20.1 09.6 47.5 48.1 14.3 18.7 65.5 72.1 21.3 35.5

Acrobeles

2

24.9 26.7 07.8 00.0 23.7 19.2 05.3 00.0 31.4 14.4 14.0 20.3 05.6 14.7 03.5 01.9 24.2 31.1 04.4 17.3 23.2 23.8 07.7 19.1

Acrobeloides

2

02.2 03.2 07.3 10.3 08.1 08.0 00.9 10.1 00.0 13.3 05.4 02.7 03.8 05.0 03.5 01.9 04.2 05.5 00.0 00.0 05.9 10.4 06.5 03.8

Cephalobus

2

00.0 00.9 01.5 04.9 00.0 00.0 01.8 00.0 00.0 03.3 00.0 00.0 00.6 00.9 00.0 00.0 01.3 00.9 03.8 01.4 04.9 02.9 00.0 01.6

Cervidellus

2

06.7 08.1 02.4 00.5 19.3 14.4 05.3 02.9 07.8 03.3 01.1 01.4 03.1 01.8 02.1 00.0 03.8 03.0 02.7 00.0 17.2 15.4 05.8 07.7

Chiloplacus

2

00.0 00.0 00.0 00.5 00.0 00.8 00.0 00.0 02.0 06.7 00.0 00.0 00.0 00.0 00.0 00.0 01.7 00.0 01.1 00.0 01.0 07.5 00.0 02.2

Eucephalobus

2

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 01.7 00.0 00.0 00.0 00.0 00.4 00.0 00.0

Mesorhabditis

1

08.0 05.4 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0

Panagrolaimus

1

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 01.4 01.9 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0

Plectus

2

00.4 01.8 00.0 05.4 03.0 04.8 00.0 00.0 02.0 08.9 00.0 06.8 01.3 04.6 02.8 00.0 02.1 00.4 00.0 00.0 00.5 00.4 00.0 00.0

Rhabditis

1

21.3 06.8 01.5 08.1 09.6 15.2 06.2 02.9 07.8 17.8 15.1 13.5 21.9 26.6 06.9 03.8 08.5 04.7 02.2 00.0 10.3 11.3 01.3 01.1

Wilsonema

2

00.0 00.9 00.0 00.0 00.0 00.0 00.0 01.4 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 02.6 00.0 00.0 02.5 00.0 00.0 00.0

Fungivores

08.0 05.4 13.6 12.4 01.5 05.6 04.4 02.9 23.5 00.0 29.0 09.5 31.9 19.7 43.8 28.8 12.3 09.4 07.7 06.5 08.9 08.3 14.2 06.6

Aphelenchoides

2

07.6 03.6 06.3 04.3 01.5 04.8 02.7 02.9 21.6 00.0 26.9 08.1 15.0 09.6 16.7 09.6 08.1 07.2 04.9 03.6 07.9 02.1 06.5 04.9

Aphelenchus

2

00.4 01.8 06.8 05.4 00.0 00.0 01.8 00.0 02.0 00.0 01.1 01.4 01.3 01.8 06.9 05.8 02.1 01.3 02.2 02.2 00.0 03.8 06.5 00.5

Ditylenchus

2

00.0 00.0 00.0 00.5 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 14.4 08.3 20.1 09.6 02.1 00.9 00.5 00.0 01.0 02.5 01.3 01.1

Nothotylenchus

2

00.0 00.0 00.5 02.2 00.0 00.8 00.0 00.0 00.0 00.0 01.1 00.0 01.3 00.0 00.0 03.8 00.0 00.0 00.0 00.7 00.0 00.0 00.0 00.0

Plant-parasites

10.7 23.1 40.3 11.4 17.8 17.6 46.9 37.7 03.9 31.1 22.6 21.6 19.4 25.2 27.1 51.9 21.2 31.1 43.4 43.2 18.7 07.5 40.0 25.7

Filenchus

2

00.9 01.4 00.5 00.0 00.0 01.6 00.0 00.0 00.0 00.0 01.1 00.0 05.0 00.5 00.0 00.0 00.4 00.4 05.5 05.0 02.0 00.0 01.9 03.8

Heterodera

3

00.0 00.0 01.5 00.5 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0

Meloidoginae

3

00.4 00.0 02.9 01.6 00.0 00.0 01.8 01.4 00.0 00.0 00.0 00.0 02.5 00.0 00.7 03.8 01.3 01.3 01.1 05.0 00.0 00.8 00.0 00.5

Longidorus

4

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 01.9 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0

Paratylenchus

2

01.3 01.4 02.4 01.1 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0

Pratylenchus

3

02.2 04.1 04.4 02.7 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 01.3 00.0

Tetylenchus

2

00.0 00.0 01.0 00.0 00.0 00.8 02.7 00.0 00.0 02.2 02.2 00.0 01.3 00.0 02.1 00.0 00.0 00.0 02.2 00.0 00.0 01.3 00.0 00.0

Tylenchorhynchus 2

04.9 13.1 26.2 04.9 17.8 07.2 42.5 36.2 03.9 28.9 19.4 21.6 07.5 21.1 14.6 40.4 17.4 28.9 25.8 27.3 15.3 04.6 31.0 16.9

Tylenchus

2

00.9 02.7 01.5 00.5 00.0 08.0 00.0 00.0 00.0 00.0 00.0 00.0 01.3 03.2 09.7 07.7 02.1 00.4 07.7 05.8 01.5 00.8 05.8 04.4

Xiphinema

5

00.0 00.5 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.5 00.0 00.0 00.0 00.0 01.1 00.0 00.0 00.0 00.0 00.0

OP

17.8 17.6 25.7 46.5 17.0 14.4 29.2 42.0 21.6 01.1 12.9 24.3 12.5 01.4 09.0 09.6 19.1 11.5 34.6 31.7 06.9 12.1 24.5 32.2

Discolaimus

4

02.7 00.9 00.0 05.9 01.5 00.0 00.0 00.0 03.9 00.0 01.1 00.0 01.3 00.0 00.0 00.0 00.0 00.4 02.7 02.2 00.5 02.1 00.0 02.7

Dorylaimus

4

09.3 06.3 15.0 27.6 08.1 11.2 12.4 18.8 05.9 01.1 04.3 10.8 05.6 01.4 03.5 07.7 11.4 08.9 14.8 16.5 03.9 09.2 14.2 15.3

Dorilaimoides

4

00.0 00.5 01.0 02.2 03.0 01.6 05.3 10.1 03.9 00.0 02.2 01.4 02.5 00.0 02.8 01.9 00.8 00.0 03.3 00.0 00.0 00.0 06.5 01.6

Dorylaimellus

5

00.0 00.5 03.4 01.6 00.0 00.0 00.9 01.4 00.0 00.0 00.0 00.0 00.6 00.0 00.7 00.0 00.0 00.0 00.5 00.0 00.0 00.0 00.6 00.0

Eudorylaimus

4

02.7 03.6 03.4 00.5 00.0 00.0 06.2 02.9 00.0 00.0 00.0 01.4 00.0 00.0 00.0 00.0 04.2 02.1 09.9 12.9 02.0 00.8 03.2 12.6

Leptonchidae

4

00.0 00.9 00.0 00.0 00.0 00.8 00.9 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 01.6 00.0 00.0 00.0 00.0 00.0

Mononchus

4

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0

Nygolaimus

5

03.1 05.0 02.9 08.6 04.4 00.8 03.5 08.7 07.8 00.0 05.4 10.8 02.5 00.0 02.1 00.0 02.5 00.0 01.6 00.0 00.5 00.0 00.0 00.0

(continued on next page)

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

37

Table 1 (continued) Month

May

Depth (cm) a

1

June

Plant 2

Control

Plant

1

1

2

July

2

Control

Plant

1

1

2

August

2

Control

Plant

1

1

2

2

September Control

Plant

1

1

2

2

October Control

Plant

1

1

2

Control 2

1

2 A (%) b

Genus/family Bacterivores

c-p 65.8 64.5 38.8 45.5 66.3 61.7 22.1 17.4 61.5 52.5 31.2 21.5 49.7 42.1 49.0 25.0 59.4 47.8 26.3 08.3 35.8 57.3 14.2 10.8 41.9

Acrobeles

2

12.5 07.2 17.6 13.3 17.9 33.8 05.3 05.6 15.9 11.2 07.4 07.3 13.8 12.6 09.1 09.3 25.3 16.4 10.5 00.0 10.0 28.2 05.3 00.0 14.3

Acrobeloides

2

07.9 11.6 05.9 10.5 32.5 10.4 10.6 07.2 31.4 17.2 20.8 08.5 19.2 10.5 30.1 12.9 14.7 13.8 08.4 06.9 16.7 20.9 04.4 09.2 10.2

Cephalobus

2

06.7 04.3 02.4 07.7 02.1 00.8 00.0 02.1 00.0 00.0 00.0 00.0 00.0 00.0 01.4 00.0 00.0 00.0 01.1 00.0 00.0 00.0 04.4 01.7 01.5

Cervidellus

2

08.8 21.7 04.7 06.3 05.4 10.4 04.3 02.1 06.4 15.2 02.9 05.6 04.8 07.9 01.4 00.7 11.8 10.1 00.0 00.0 09.2 08.2 00.0 00.0 06.2

Chiloplacus

2

03.8 05.8 05.9 02.1 02.1 03.3 01.9 00.5 02.7 05.2 00.0 00.0 01.8 02.6 02.1 01.4 04.1 04.4 05.3 01.4 00.0 00.0 00.0 00.0 01.7

Eucephalobus

2

11.7 06.5 02.4 05.6 04.6 01.7 00.0 00.0 05.1 03.7 00.0 00.0 06.6 04.7 03.5 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 01.4

Mesorhabditis

1

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 03.6 03.2 00.0 00.7 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.4

Panagrolaimus

1

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0

Plectus

2

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.8

Rhabditis

1

14.6 07.2 00.0 00.0 01.7 01.3 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 02.9 01.9 01.1 00.0 00.0 00.0 00.0 00.0 05.1

Wilsonema

2

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.5 01.4 00.0 00.6 01.3 00.0 00.0 00.0 00.0 00.0 00.0 00.3

Fungivores

09.6 02.2 09.4 19.6 05.8 01.7 20.7 20.5 07.0 03.0 17.5 19.2 21.6 18.9 10.5 12.9 07.6 08.2 08.4 09.7 05.8 03.6 10.6 10.0 11.6

Aphelenchoides

2

03.3 00.0 04.7 09.1 05.0 01.7 13.5 12.8 04.4 01.9 11.7 12.4 11.4 10.5 04.9 07.1 00.0 02.5 05.3 00.7 00.0 00.0 00.0 00.0 05.9

Aphelenchus

2

06.3 02.2 04.7 10.5 00.8 00.0 07.2 07.7 02.6 01.1 05.8 06.8 06.0 07.9 00.7 03.6 03.5 00.6 00.0 00.0 05.8 03.6 10.6 10.0 03.6

Ditylenchus

2

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.6 00.0 00.7 00.0 01.2 01.3 00.0 00.0 00.0 00.0 00.0 00.0 01.3

Nothotylenchus

2

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 03.6 00.5 04.2 02.1 02.9 03.8 03.2 09.0 00.0 00.0 00.0 00.0 00.7

Plant-parasites

18.3 31.2 30.6 23.1 19.2 22.9 20.7 41.5 23.0 29.4 20.4 25.4 15.0 17.9 30.8 32.9 21.8 32.7 57.9 60.0 39.2 26.4 32.7 36.7 27.4

Filenchus

2

00.0 00.0 01.2 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 01.1 02.8 01.4 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.8

Heterodera

3

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.7 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 03.3 00.2

Meloidoginae

3

00.0 00.0 01.2 02.1 00.0 00.0 00.0 01.0 00.0 00.0 00.0 00.0 00.0 00.5 00.7 02.9 00.0 00.0 00.0 02.1 00.0 00.0 00.0 01.7 00.7

Longidorus

4

00.0 00.0 00.0 00.0 00.0 00.4 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 01.7 00.1

Paratylenchus

2

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 02.8 00.0 00.0 00.0 12.6 03.4 00.0 00.0 00.0 00.0 00.4

Pratylenchus

3

00.0 00.0 02.4 01.4 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 02.8 02.1 01.2 00.6 05.3 01.4 00.0 00.0 00.0 00.0 00.5

Tetylenchus

2

00.4 00.0 02.4 02.8 00.0 00.4 00.5 02.1 00.0 00.0 00.0 02.8 00.0 02.1 04.2 02.9 05.3 06.9 02.1 09.0 00.0 00.0 05.3 05.0 01.5

Tylenchorhynchus 2

17.9 31.2 21.2 14.7 19.2 20.0 20.2 32.3 23.0 29.4 20.4 22.6 15.0 14.2 11.9 22.1 15.3 25.2 37.9 30.3 37.5 24.5 27.4 25.0 21.2

Tylenchus

2

00.0 00.0 02.4 01.4 00.0 02.1 00.0 06.2 00.0 00.0 00.0 00.0 00.0 00.0 04.9 01.4 00.0 00.0 00.0 13.8 01.7 01.8 00.0 00.0 02.0

Xiphinema

5

00.0 00.0 00.0 00.7 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.1

OP

06.3 02.2 21.2 11.9 08.8 13.8 36.5 20.5 08.4 15.2 30.9 33.9 13.8 21.1 09.8 29.3 11.2 11.3 07.4 22.1 19.2 12.7 42.5 42.5 19.1

Discolaimus

4

00.0 00.0 01.2 00.7 00.4 02.5 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 05.0 00.0 00.0 00.0 06.9 02.5 00.0 00.0 00.0 00.9

Dorylaimus

4

03.8 00.7 07.1 05.6 04.2 06.7 13.0 08.2 05.1 10.6 11.7 13.0 10.2 11.6 02.1 16.4 04.1 05.0 04.2 06.9 11.7 10.0 35.4 30.8 10.4

Dorilaimoides

4

00.8 01.4 01.2 00.0 00.8 00.0 00.0 00.0 00.0 00.0 00.0 00.0 01.2 00.0 00.7 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.9

Dorylaimellus

5

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.7 00.0 00.0 00.0 00.0 00.2

Eudorylaimus

4

00.4 00.0 04.7 03.5 02.1 00.8 13.5 07.7 02.6 02.0 08.8 10.7 01.2 02.1 02.1 02.1 01.2 00.6 00.0 00.7 02.5 02.7 07.1 03.3 03.3

Leptonchidae

4

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 01.1 00.7 00.0 00.0 00.0 01.1 00.0 00.0 00.0 00.0 00.0 00.1

Mononchus

4

00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.5 01.4 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0 00.0

Nygolaimus

5

01.3 00.0 07.1 02.1 01.3 03.8 10.1 04.6 00.8 02.6 10.5 10.2 01.2 05.8 02.8 05.7 05.9 05.7 02.1 06.9 02.5 00.0 00.0 08.3 03.2

a

(1) 0–10 cm; (2) 10–20 cm. b A (%), the mean of nematode density (percent) during the study period.

38

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

Individuals 100g-1 dry soil

500

ABF

400 300 200 100

Individuals 100g-1 dry soil

0 500

BBF

400 300 200 100

Individuals 100g-1 dry soil

0 500

AFF

400 300 200 100 0

Individuals 100g-1 dry soil

500

BFF

400 300 200 100 0 Nov.99

Feb.00

May.00

Aug.00

Nov.00

Feb.01

May.01

Aug.01

Nov.01

Time (months)

Fig. 3. (3.1) Changes in nematode trophic groups in the soil samples taken beneath the Z. dumosum ( ) shrubs and control samples (◆) 0–10 and 10–20 cm layers, during the study period (November 1999–November 2001). (ABF, bacterial feeding nematodes at the 0–10 cm layer; BBF, bacterial feeding nematodes at the 10–20 cm layer; AFF, fungi feeding nematodes at the 0–10 cm layer; BFF, fungi feeding nematodes at the 10–20 cm soil layer).

with a higher population density toward the summer season of the second year (Fig. 3(3.1) AFF, BFF). Maximum values of fungivores under and between the shrubs were found in July and August (123 and 219 individuals 100 g–1 soil under the shrubs; 67 and 134 individuals 100 g–1 soil in the control plots, respectively) of the second year. These values, as well as those of the first year, contributed to the significant differences (P < 0.01) between the late summer and the autumn months. No significant differences were found in the fungivore-feeding group between the samplings (Fig. 3 APP, BPP).

The plant-parasite population (Fig. 3(3.2) APP, BPP) exhibited similar trends in both samplings and depths, with a significantly higher (P < 0.05) population density in the second year than in the first, with 47 and 280 individuals 100 g–1 soil, respectively, which amounted to 27.4% of the total soil free-living nematode population during the study period (Table 1). No significant differences were found between the samples and soil layers (P > 0.05). The OP population under Z. dumosum exhibited a similar trend to that of the plant parasites, and represented 19% of the total population during the study period, with a signifi-

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

Individuals 100g-1 dry soil

300

39

APP

200

100

0

Individuals 100g-1 dry soil

300

BPP

200

100

0

Individuals 100g-1 dry soil

500

AOP

400 300 200 100 0

Individuals 100g-1 dry soil

500

BOP

400 300 200 100 0 Nov.99

Feb.00

May.00

Aug.00

Nov.00

Feb.01

May.01

Aug.01

Nov.01

Time (months)

Fig. 3. (continued) (3.2) Changes in nematode trophic groups in the soil samples taken beneath the Z. dumosum ( ) shrubs and control samples (◆) 0–10 and 10–20 cm layers, during the study period (November 1999–November 2001). APP, plant parasite population at 0–10 cm; BPP, plant parasite population at 10–20 cm; AOP, omnivore-predators population at 0–10 cm; BOP, omnivore-predators population at 10–20 cm soil layer).

cantly higher (P < 0.01) population during the second year in the upper (0–10 cm) layer (Fig. 3(3.2) AOP, BOP). No significant (P > 0.05) differences were found in the control samples between the different depths throughout the study period. 3.4. Nematode taxa Thirty-three nematode taxa were identified in the present investigation. We determined the presence of nematode spe-

cies in the samples throughout the study period with less than 1% subresident; 1–2% resident; 2–5% subdominant; 5–10% being considered dominant 10% and higher being considered eudominant [39]. Table 2 presents changes in the dominant density during the study period. According to this table, most dominant genera are found in the vicinity of Z. dumosum in both layers, while in the control between-shrub space, a more irregular presence was found. Acrobeles, a known bacterivore, was found to be the dominant genus in the monthly soil

40

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

Table 2 The mean dominant density (%) of soil nematodes under Z. dumosum and control samples at two depths (0–10 and 0–20 cm) a Trophic groups/genus/family b Depth (cm) Bacterivores Acrobeles

Acrobeloides

c-p

2

2

Cephalobus

2

Rhabditidae

1

Fungivores Aphelenchoides Ditylenchus Plant-parasites Tylenchorhynchus

OP Dorylaimus

Month

January February March April May June September October November December June July August October May December January February May November

2 2

January February

2

January February March April May June July September October November December

4

Plant 0–10

10–20

Control 0–10

++++ ++++ ++++ ++++ ++++ ++++ ++++ ++++ ++++ ++++ ++++ ++++

10–20 ++++

++++ ++++ ++++ ++++

++++ ++++ ++++ ++++ ++++

++++ ++++ ++++ ++++ ++++

+++++

++++ ++++

++++ ++++ ++++ ++++ ++++

++++ ++++ ++++ ++++ ++++ ++++ ++++ ++++

++++

October November

++++

++++

++++ ++++

++++ ++++ ++++ +++++ ++++

++++ ++++ ++++ ++++ ++++ ++++ ++++

+++++, eudominant (>10%); ++++, dominant (5–10%). a Trophic groups according to Yeates et al. [45]. b By classification Yeates [39].

samples under Z. dumosum. It accounted for the presence of nine out of a total of 25 months. A 36% presence of Acrobeles leads it to being considered an eudominant genus. However, the Tylenchorhynchus plant-parasite nematode exhibited a more general and widely divergent presence, ranging between 24% and 32% of the total plant-parasite population during the study period for all samplings and depths. These values indicate that these genera are dominant on a monthly basis and eudominant for the entire study period. Dominating nematode genera such as Acrobeloides, Rhabditis, Cephalo-

bus Aphelenchoides, Dorylaimus, and Ditylenchus were found less often (Table 2). 3.5. Ecological indices The c-p indices, which describe nematode life strategies and their sensitivity to environmental disturbances [4,7], with values ranging from 1 to 5 (for colonizers, tolerant to disturbance to persisters, sensitive to disturbance), were found to divide the genus/family belonging to the different

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

trophic groups into three distinct groups. The first group consists of all the bacteriovore and fungi-feeders, with c-p values of 1 and 2. Since they are more abiotic-dependent, they developed a colonizer strategy. The second group consists of the OP, with c-p values of 4 and 5. This group is higher in the hierarchy, and was found to develop a persisters strategy, which did not allow them to be food electors. The third group was represented by plant-parasites, including 50% colonizers, 20% persisters and the remaining 30% having a c-p value of 3, as intermediators. Following this grouping, we found that under the shrubs, 78%, 12% and 1% of the nematode population belong to groups 1, 2 and 3, respectively. In the control samples a decrease was found in group 1 to 69% and an increase of over 100% to values of 28% and 3% in groups 2 and 3. This means that unlike under-plant soil samples, a decrease in nematodes belonging to life-strategies 1 and 2 was found in the control soil samples, and an increase in nematodes belonging to life strategies 3–5. The Wasilewska index [37] (WI-ratio of fungivore + bacterivores to plant parasites), F/B-index (fungivore/ bacterivores ratio), trophic diversity (T), genus dominance (k), MMI, and SR exhibited differences under plants and in control samples throughout the study period, with no differences between the two sampling layers (Figs. 4 and 5). The WI index, ranging from 0 to 30, was found to reach a mean maximal value under the plants at both depths (10.3 and 12.9, respectively) in March, whereas mean minimal values decreased to 0.5 in late summer. WI values were found to reach a mean maximal value of 4 and 7.5 in the spring of the first year. During most of the sampling period of the second year, they were found to be significantly lower. The ratio of fungivores to bacterivores (F/B) under Z. dumosum in both layers was lower (P < 0.05) than in the between-shrub control samples. The values obtained throughout the study period beneath the shrubs were less than one most of the time, with one exception in March, with a value of 1.7 in the upper layer. However, the F/B ratio in the control samples between the shrubs was found to reach higher values than those obtained under the shrubs, reaching values of 2.5 and 3.4 in the 0–10 and 10–20 cm layers, respectively. The lowest values were obtained during the winter months (November–December) of the first study year, whereas during the second year this period was prolonged until the end of spring for both layers. T ranged from 1.00 to 3.4 (Fig. 4) with no differences (P > 0.05) between the depths and years throughout the study period. In general, the trends were similar, with decreasing values in winter (December–January) under plants at both depths and more gradual changes in the deeper layer compared to more severe changes in T values in the upper (0–10 cm) layer. Genus dominance (k) ranged between 0.1 and 1.0, reaching maximal values under the plants in January (at both depths) and December (at the 10–20 cm depth), and minimal values in August (at both depths) (Fig. 4). Mean values of dominance in the control samples were maximal in February

41

and March (10–20 cm depth), November (10–20 cm depth) and December (both depths). Minimal dominant index values in the control samples were obtained in May (10–20 cm depth). The mean dominant index value (0.35) was similar to values (0.09–0.70) observed in different parts of the world [19,21,43]. SR changed from 0 to 1.8 and its mean values were maximal under plants towards the end of the summer period and the beginning of autumn (August, September) for both years and depths (Fig. 5). In control samples, mean values of SR increased towards spring, reaching maximal values in March (0–10 cm depth) and May (10–20 cm depth), with a slight decrease toward summer and autumn. The Shannon index (H′) was different during the observed years and months, but there were no differences in the two observed depths between under-plant samples and the control (Fig. 4). Mean minimal values of the Shannon index were found under the plants in January (both depths) and in the control samples in February (10–20 cm depth) and December (both depths). MI behavior exhibited a temporal as well as a spatial difference throughout the study period (Fig. 5). In the samples taken from under-plants in the upper layer, more stable values (1.5–2.2) were obtained, with no significance differences during the year, while in samples taken from the deeper layer (10–20 cm), the values in the second year dropped to 0.6 in January, and failed to reach a value of 2.0 by the end of the study period. The patterns observed in the control samples were similar to those of under-shrub samples, with no significant differences between them. Values of the MMI ranged from 1.1 to 3.5, with higher values being observed in the control samples than in the samples taken from under-shrubs (Fig. 5). However, no significant differences were found between depths and sampling location throughout the study period. 4. Discussion The fluctuation in rainfall during this 2-year study reflected the unpredictability of this trigger, with an almost threefold increase in the total amount of rainfall in the second year compared to the first. This difference in total rainfall and its distribution was found to significantly influence soil moisture levels in all samplings and layers during the winter season. Moreover, the additional source of moisture from approximately 35 mm of dew, which falls each night but most heavily during late summer and autumn [12], significantly influenced the temporal distribution of nematode communities. However, the relatively high moisture levels during the second year did not result in a significant (P > 0.05) correlation between soil moisture content and total nematode population, as reported by Steinberger et al. [32] based on data obtained from a topoclimatic transect in a rain shadow Judean desert. An important feature observed throughout the study period was that although the total amount of rainfall and soil

42

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46 14

14

0 - 10 cm

10

10

8

8

WI

12

WI

12

6

6

4

4

2

2

0

0

4

4

0 - 10 cm

2

1

0

0 4

0 - 10 cm

10 - 20 cm

3 T'

T'

3 2

2

1

1

0

0 2

0 - 10 cm

y

y

1

0 4

2

1

2

0 - 10 cm

3 F/B

F/B

3

4

10 - 20 cm

10 - 20 cm

1

0

0 - 10 cm

4

H'

3

H'

3 2

2

1

1

0

0

Nov.99 Mar.00 Jul.00 Nov.00 Mar.01 Jul.01 Nov.0

Time

10 - 20 cm

Nov.99 Mar.00

Jul.00 Nov.00 Mar.01

Jul.01 Nov.0

Time

Fig. 4. Variation of ecological indices of soil nematodes during the study period in soil sample taken in the vicinity of Z. dumosum ( ) shrubs and control (◆) samples at two depths (0–10 and 10–20 cm). (WI, Wasilewska indices; F/B, fungi-feeders/bacterial-feeders; T, trophic diversity; k, genus dominance).

moisture availability during the second year was higher than during the first year, they did not increase soil organic matter. The differences in total organic matter can be attributed to the differences in primary production due to the high variability in the total amount and distribution of rainfall, as reported by Steinberger and Loboda [33] in their study on the Negev Desert. The annual abundance of the total number of nematodes during our study was found to be similar (272 individuals 100 g–1 soil) to those reported by Steinberger and Loboda

[33], higher (74 individuals 100 g–1 soil) than those reported by Liang et al. [19] for the Negev Desert. These values were also lower than those reported by Freckman and Mankau [14] with 912 individuals 100 g–1 soil in soil samples taken from the Mojave Desert. Trophic group distribution has been evaluated in a variety of environments without reaching a clear pattern of variation in functional structure for the different ecosystems [17]. However, in general, the BF population has been found to range between 12.9% and 72.0% of the total community,

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46 4

0 - 10 cm

4

MI

3

0

0 5

0 - 10 cm

4

4

3

3

MMI

MMI

MI

1

2

1

0

0 2

0 - 10 cm

J'

J'

10 - 20 cm

2

1

1

10 - 20 cm

1

0 4

2

1

2

10 - 20 cm

3

2

5

43

0 4

0 - 10 cm

3

10 - 20 cm

SR

SR

3

2

2

1

1

0

0

Nov.99 Mar.00 Jul.00 Nov.00 Mar.01 Jul.01 Nov.0

Time

Nov.99 Mar.00 Jul.00 Nov.00 Mar.01 Jul.01 Nov.0

Time

Fig. 5. Variation of ecological indices of soil nematodes during the study period in soil sample taken in the vicinity of Z. dumosum ( ) shrubs and control (◆) samples at two depths (0–10 and 10–20 cm). (MI, maturity index; MMI, modified maturity index; J′, evenness; SR, species richness).

with higher proportions in coniferous forests and crops (50%) compared to grasslands, with values ranging between 30% and 40%. Our mean values ranged between 10% and 72.1% in soil samples under and between the shrubs. These values are similar to those reported by Steinberger et al. [34]. The mean 2-year value of 24% in the control samples was lower than that in the grassland (30–40%), with twofold higher mean values of 56% under-shrubs, which can be compared with values reported for coniferous forests and agroecosystems [17,26]. Fungi-feeder nematodes were found to comprise a mean of 11.6% of the total nematode population at the study site with a mean value of 9.6% and 14.5%, under the shrubs and between them (control), respectively. These values are within the range reported by Arpin et al. [3], where the fungi-

feeding nematodes ranged from 3.1% to 50% of the total nematode density, with maximum abundance in forests. The plant parasitic nematodes were found to be represented by 10 taxa and comprised 27.4% of the total population, with a significantly higher presence in the second year. Although the total amount of organic matter was higher in the first year, which may be due to higher below-ground primary production, the plant-parasite nematodes were found to be significantly lower than low organic matter in the second year. These results are different than those obtained by Liang et al. [19], where the greatest presence of plant-parasite population was found to be related to plant production. The mean percentage of the total nematode assemblage accounted for by OPs was similar to the sum of fungivores, with plant-parasites counting for 1/3 of the entire population.

44

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

Freckman et al. [15], in their study on the effect of irrigation on the nematode population in the Chihuhuan Desert, found that the OP ranged between 17% and 25% of the total population. The changes in population densities and trophic group composition recorded in this study can be characterized as a wet and dry season response. In the wet season, the nematode population did not peak in response to soil moisture and organic matter. It is surprising that there was no correlation between nematode densities and precipitation or soil moisture availability, similar to the finding of Freckman et al. [15], whereas according to Sohlenius and Wasilewska [31], soil moisture availability is one of the important variables in nematode reproduction. According to Dash et al. [10], Yeates [40], and Freckman et al. [15], nematode communities vary on a local and temporal scale with changes in vegetation, probably through their effects on available food sources such as bacteria, fungi and some organic matter availability from fine root production, findings that are complementary to our present study. The mean fungivores and bacterivores to plant parasites ratio (WI) in our investigation amounted to 1.94, which is within the range (0.70–9.15) of values reported by Wasilewska [37], McSorley and Frederick [21], and Liang et al. [18,19] in various ecosystems. According to Sohlenius and Sandor [30] indicates the status of the decomposition pathway in detritus food webs. The mean F/B ratio in this study (0.41), with significant variations throughout the sampling period, emphasizes the nature of the available food source. Although the mean value was found within the range (0.15–2.3) of values reported by other investigators from different parts of world trophic diversity values (TD) in the present study (TD = 1.16) were found to be lower than values (2.01–2.94) obtained by investigators studying different systems [21,32,43]. The genus dominance (k) mean value (0.35) was found to be within the range (0.09–0.70) reported by Yeates and Bird [43] and McSorley and Frederick [21]. However, the mean SR (1.0) was found to be 50% lower than the value reported by Liang et al. [19] and almost fivefold lower (1.49–5.02) than the values obtained by Yeates and King [44]. The Shannon index (H′) gives more weight to rare species and a higher index indicates greater diversity. In the present study we reported a mean value of H′ = 1.26, which is higher that that observed by Sohlenius and Sandor [30] in a grass system and that reported by Wasilewska [37] for meadows. The MI is a measure based on the composition of the nematode community, and can reflect the degree of disturbance of the soil ecosystem [4]. The mean value of our investigation was 1.68, which is similar to data reported by Freckman and Ettema [13] for agroecosystems and lower than the value reported by Wasilewska [37] for meadows. The MMI value (2.3) was found to be 40% higher than the value (1.7) reported by Porazinska and Coleman [22] for an agricultural field in Georgia.

Being one of the most important components of soil biota, nematodes actively interact with both dead and live parts of the soil ecosystem, contributing to soil formation and maintaining soil fertility. This study elucidated that nematode population temporal and spatial dispersion is triggered by soil moisture available for activity and not by the total amount of rainfall. The density of the soil free-living nematode population is concentrated mainly in the upper layer following food source availability by taking advantage and utilizing the above-ground interface (litter–soil surface) organic resources, which have a strong effect on trophic composition. Our research showed that there were significant differences in soil moisture and organic matter during the investigated period not only under the plants but also in the control samples. Moreover, soil moisture and organic matter reached maximum peaks during different months of the year. In contrast to organic matter, there were significant differences in soil moisture in the different soil layers. During wet periods the increase in soil moisture was followed by an increase in the total number of nematodes. During dry periods a change in the total number of nematodes was more dependent on organic matter content than on soil moisture. Altieri [2], in his paper on biodiversity in agroecosystems, suggested that internal functional regulation depends mainly on the plant and animal biodiversity present in the system. In natural systems, the regulation of inputs is mediated by unpredictable abiotic inputs, biodiversity and the need to supply energy for maintaining ecological functions. These functions are largely biologically mediated, and are dependent on their plasticity for responding to and enhancing functional biodiversity. Soil nematode adaptation to the fluctuating environment may serve as a valuable mediator of plant-available nutrients, thus aiding in the conservation of nutrient flow in poor natural systems.

Acknowledgements This research was supported by the Israel Science Foundation (grant no. 506/99-17.3). The authors wish to express their appreciation to the staff at the M. Evenari Avdat Research Farm.

References [1]

A. Alon, Y. Steinberger, Response of the soil microbial biomass and nematode population to a wetting event in nitrogen-amended Negev desert plots, Biol. Fertil. Soils 30 (1999) 147–152.

[2]

M.A. Altieri, The ecological role of biodiversity in agroecosystems, Agric. Ecosyst. Environ. 74 (1999) 19–31.

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46 [3]

P. Arpin, J.F. David, G.G. Guittonneau, Influence du peuplement forestier sur la faune et la microflore du sol et des humus. 2. Microbiologie et experiences au laboratoire, Rev. Ecol. Biol. Sol. 23 (1986) 119–153.

[4]

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

[5]

T. Bongers, M. Bongers, Functional diversity of nematodes, Appl. Soil Ecol. 10 (1998) 239–251.

[6]

T. Bongers, H. Ferris, Nematode community structure as a bioindicator in environmental monitoring, Trends Ecol. Evol. 14 (1999) 224–228.

[7]

T. Bongers, K. Ilieva-Makulec, K. Ekschmitt, Acute sensitivity of nematode taxa to CuSO4 and relationships with feedingtype and life history classification, Environ. Toxicol. Chem. 20 (2001) 1511–1516.

[8]

E.J. Cairns, Methods in nematology, in: J.N. Sasser, W.R. Jenkins (Eds.), Nematology, Fundamentals and Recent Advances with Emphasis on Plant Parasitic and Soil Forms, University of North Carolina Press, Chapel Hill, 1960, pp. 33–84.

[9]

J. Dan, D.H. Yaalon, H. Royumdjisky, Z. Raz, The soil association map of Israel, Isr. J. Earth Sci. 2 (1972) 29–49.

[10] M.C. Dash, B.K. Senapati, C.C. Mishra, Nematode feeding by tropical earthworms, Oikos 34 (1980) 322–325. [11] Y. Demeure, D. Freckman, S.D. Van Gundy, Anhydrobiotic coiling of nematodes in soil, J. Nematol. 11 (1979) 189–195. [12] M. Evenari, The desert environment, in: M. Evenari, I. NoyMeir, E.W. Goodall (Eds.), Hot Deserts and Shrublands. Ecosystems of the World, 12A, Elsevier, Amsterdam, 1985, pp. 1–22. [13] D.W. Freckman, C.H. Ettema, Assessing nematode communities in agroecosystems of varying human intervention, Agric. Ecosyst. Environ. 45 (1993) 239–261. [14] D.W. Freckman, R. Mankau, Abundance, distribution, biomass and energetics of soil nematodes in a northern Mojave Desert ecosystem, Pedobiologia 29 (1986) 129–142. [15] D.W. Freckman, W.G. Whitford, Y. Steinberger, Effect of irrigation on nematode population dynamics and activity in desert soils, Biol. Fertil. Soils 3 (1987) 3–10. [16] C. Heip, P.M.J. Herman, K. Soetaert, Data processing, evaluation and analysis, in: R.P. Higgins, H. Thiel (Eds.), Introduction to the Study of Meiofauna, Smithsonian Institution Press, Washington, DC, 1988, pp. 197–231. [17] P. Lavelle, A.V. Spain, Soil Ecology, Kluwer Academic Publishers, The Netherlands, 2001. [18] W. Liang, I. Lavian, Y. Steinberger, Effect of agricultural management on nematode communities in a Mediterranean agroecosystem, J. Nematol. 33 (2001) 208–215. [19] W.J. Liang, S. Mouratov, Y. Pinhasi-Adiv, P. Avigad, Y. Steinberger, Seasonal variation in the nematode communities associated with two halophytes in a desert ecosystem, Pedobiologia 46 (2002) 63–74. [20] W.J. Liang, Y. Pinhasi-Adiv, H. Shtultz, Y. Steinberger, Nematode population dynamics under the canopy of desert halophytes, Arid Soil Res. Rehabil. 14 (2000) 183–192. [21] R. McSorley, J.J. Frederick, Nematode community structure in rows and between rows of a soybean field, Fundam. Appl. Nematol. 19 (1996) 251–261.

45

[22] D.L. Porazinska, D.C. Coleman, Ecology of nematodes under influence of Cucurbita spp. and different fertilizer types, J. Nematol. 27 (1995) 617–623. [23] D.L.C. Procter, Global overview of the functional roles of soil-living nematodes in terrestrial communities and ecosystems, J. Nematol. 22 (1990) 1–7. [24] D.L. Rowell, Soil Science: Methods and Applications, Longmans Group UK Ltd., London, 1994. [25] S. Sarig, Y. Steinberger, Microbial biomass response to seasonal fluctuation in soil salinity under the canopy of desert halophytes, Soil Biol. Biochem. 26 (1994) 1405–1408. [26] D.P. Schmitt, D.C. Norton, Relationship of plant parasitic nematodes to sites in native Iowa prairies, J. Nematol. 4 (1972) 200–206. [27] C.E. Shannon, W. Weaver, The Mathematical Theory of Communication, University of Illinois Press, Urbana, IL, 1949. [28] E.H. Simpson, Measurement of diversity, Nature 163 (1949) 668. [29] B. Sohlenius, Abundance, biomass and contribution to energy flow by soil nematodes in terrestrial ecosystems, Oikos 34 (1980) 186–194. [30] B. Sohlenius, A. Sandor, Vertical distribution of nematodes in soil under grass (Festuca pratensis) and barley (Hordeum distichum), Biol. Fertil. Soils 3 (1987) 19–25. [31] B. Sohlenius, L. Wasilewska, Influence of irrigation and fertilization on the nematode community in a Swedish pine forest soil, J. Appl. Ecol. 21 (1984) 327–342. [32] Y. Steinberger, W.J. Liang, E. Savkina, T. Meshi, G. Barness, Nematode community composition and diversity associated with a topoclimatic transect in a rain shadow desert, Eur. J. Soil Biol. 37 (2001) 315–320. [33] Y. Steinberger, I. Loboda, Nematode population dynamics and trophic structure in a soil profile under the canopy of the desert shrub Zygophyllum dumosum, Pedobiologia 35 (1991) 191– 197. [34] Y. Steinberger, D. Orion, W.G. Whitford, Population dynamics of nematodes in the Negev Desert soil, Pedobiologia 31 (1988) 223–228. [35] Y. Steinberger, S. Sarig, Response by soil nematode populations in the soil microbial biomass to a rain episode in the hot, dry Negev Desert, Biol. Fertil. Soils 16 (1993) 188–192. [36] D.C. Twinn, Nematodes, in: C.H. Dickinson, G.J.F. Pugh (Eds.), Biology of Plant Litter Decomposition, Academic Press, London, 1974, pp. 421–465. [37] L. Wasilewska, The effect of age of meadows on succession and diversity in soil nematode communities, Pedobiologia 38 (1994) 1–11. [38] C.J. Wright, D.C. Coleman, Cross-site comparison of soil microbial biomass, soil nutrient status, and nematode trophic groups, Pedobiologia 44 (2000) 2–23. [39] G.W. Yeates, The diversity of soil nematode faunas, Pedobiologia 10 (1970) 104–107. [40] G.W. Yeates, Soil nematode populations depressed in the presence of earthworms, Pedobiologia 22 (1981) 191–195.

46

S. Pen-Mouratov et al. / European Journal of Soil Biology 40 (2004) 31–46

[41] G.W. Yeates, Variation in pasture nematode populations over thirty-six months in a summer dry silt loam, Pedobiologia 24 (1982) 329–346. [42] G.W. Yeates, Modification and qualification of the nematode maturity index, Pedobiologia 38 (1994) 97–101. [43] G.W. Yeates, A.F. Bird, Some observations on the influence of agricultural practices on the nematode faunae of some South Australian soils, Fundam. Appl. Nematol. 17 (1994) 133–145.

[44] G.W. Yeates, K.L. King, Soil nematodes as indicators of the effect of management on grasslands in the New England Tablelands (NSW): comparison of native and improved grasslands, Pedobiologia 41 (1997) 526–536. [45] G.W. Yeates, D.A. Wardle, R.N. Watson, Responses of soil nematode populations, community structure, diversity and temporal variability to agricultural intensification over a seven-year period, Soil Biol. Biochem. 31 (1999) 1721–1733.