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Seasonal variation in the nematode communities associated with two halophytes in a desert ecosystem
Pedobiologia 46, 63–74 (2002) © Urban & Fischer Verlag http://www.urbanfischer.de/journals/pedo
Seasonal variation in the nematode communities associated with two halophytes in a desert ecosystem Wenju Liang1,2, Stanislav Mouratov1, Yocheved Pinhasi-Adiv1, Pnina Avigad1 and Yosef Steinberger1,* 1 Faculty
of Life Sciences, Bar-Ilan University, Ramat Gan 52900, Israel of Applied Ecology, Chinese Academy of Sciences, Shenyang 110015, P.R. China
2 Institute
Submitted: 20. May 2001 Accepted: 11. September 2001
Summary Seasonal variation in the soil nematode communities was investigated in a field study at the Avdat Research Farm, Israel. Soil samples from 0-10 cm soil were collected monthly between May 1998 and May 2000, under the canopy of two halophyte shrubs: Hammada scoparia and Zygophyllum dumosum. Ecological indices such as ratio of fungivores and bacterivores to plant parasites (WI), fungivore to bacterivore ratio (F/B), trophic diversity (TD), Shannon index (H’), dominance (λ) and richness (SR) were assessed and compared between treatments and between seasons. Twenty nematode families and 26 genera were observed. Acrobeles, Cephalobus, Aphelenchoides and Rhabditidae were found to be the dominant genera/family. Significant differences were found between seasons (P< 0.01) in the number of total nematodes, the four trophic groups and the indices, WI, T, H’, λ, and SR. Bacterivores were found to be the most abundant trophic group in four seasons, their mean relative abundance was 60.6 % of the nematode community. Among ecological indices tested, F/B and λ were effective in distinguishing differences in nematode community structure between treatments during the study period.
*E-mail corresponding author: [email protected]
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Key words: Nematode community, trophic groups, ecological indices, halophytes, desert ecosystem
Introduction Moisture availability in desert ecosystems varies greatly in time and space. Moisture is patchily distributed, with the highest concentration and longest duration under shrubs (Steinberger & Loboda 1991). Desert plants have developed various strategies for exploiting scarce water resources (Evenari et al. 1976). Two halophyte shrubs, Hammada scoparia [Pomel] Iljin. (Fam. Haloragaceae) and Zygophyllum dumosum Boiss. (Fam. Zygophyllaceae), are typical of the hot, dry Negev Desert (Steinberger & Loboda 1991; Sarig & Steinberger 1994; Liang et al. 2000). Steinberger and Loboda (1991) reported that root biomass of Z. dumosum had an important effect on root-nematode dynamics in the northern Negev Highland, at the Avdat Research Farm. Nematodes constitute a numerically important component of soil fauna in desert ecosystems (Freckman & Mankau 1986; Steinberger et al. 1989), but an understanding of the response of nematodes to the unpredictability of moisture availability is far from complete and requires study on a generic basis (Liang et al. 2000). Nematodes occupy an important position in the detritus food web (Ingham et al. 1985; Freckman 1988), taking a significant part in the decomposition of soil organic matter, mineralization of plant nutrients and nutrient cycling (Griffiths 1994). This organism group can be used as sensitive indicators of ecosystem change (Bongers 1990). Combining community analysis with ecosystem function has proved fruitful in the field of soil ecology (Wardle et al. 1995; Coleman & Crossley 1996; Wardle et al. 2000). The objectives of this study were to monitor seasonal variation in the soil nematode communities under the canopy of the two shrubs (H. scoparia and Z. dumosum), and to evaluate several ecological indices of the nematode community in the Negev desert ecosystem.
Materials and Methods The fieldwork in this study was conducted in the northern Negev Highland at the Avdat Research Farm (30° 47´ N, 34° 46´ E). This area has a temperate desert climate, i.e., mild, rainy winters (5–14 °C range 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, the rainfall fluctuates between 20 and 180 mm. An additional source of moisture comes from ca 35 mm of dew, which falls each night, but most heavily during late summer and autumn. The potential annual evaporation rate is ca 2615 mm (Evenari et al. 1982). The perennial vegetation is dominated by the desert shrub association, in which the most common species are H. scoparia and Z. dumosum (Steinberger & Loboda 1991; Sarig & Steinberger 1994; Liang et al. 2000). The soil is a deep, fine-textured loessial sierozem (Dan et al. 1972). A total of 264 soil samples from the upper soil layer (0–10 cm) were collected between May 1998 and May 2000 from a total of 22 months (except for July 1998, May 1999 and February 1999), under the canopy of four individual plants of each of the two species, H. scoparia and Z. dumosum. The control samples were taken from exposed areas between the plants. Af-
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ter sampling, the soil samples were placed in plastic bags, transported to the laboratory in an insulated container, and kept cool (4 °C) until processed. Subsamples were taken from each sample for estimation of nematode populations and soil chemistry. Soil moisture was determined gravimetrically by drying samples at 105 °C for 48 h and expressed as a percentage of dry weight (Liang et al. 2000). Nematodes were extracted from 100 g soil samples using the Baermann funnel procedure (Cairns 1960), and nematode populations were expressed per 100 g dry mass soil. The organisms recovered were counted and preserved in formalin (Steinberger & Sarig 1993). A randomly selected sample of the total organisms was identified, mainly to genus level if possible, using an inverted compound microscope. Trophic groups used were: (1) bacterivores (BF); (2) fungivores (FF); (3) plant-parasites (PP); and (4) omnivores-predators (OP) (Steinberger & Loboda 1991; Steinberger & Sarig 1993; Liang et al. 2000). The nematode community was analyzed by the following approaches: (1) absolute abundance of individuals 100 g-1 dry soil; (2) trophic structure; (3) WI=(FF+BF)/PP (Wasilewska 1994); (4) F/B = FF/BF (Twinn 1974); (5) T= 1/∑pi2, in which pi is the proportion of the ith trophic group (Heip et al. 1988); (6) H´= –∑pi(lnpi), where p is the proportion of individuals in the ith taxon (Shannon & Weaver 1979); (7) λ=∑pi2 (Simpson 1949); (8) SR=(S-1)/ln(N), where S is the number of taxa and N is the number of individuals identified (Yeates & King 1997). All the data were subjected to statistical analysis of variance (ANOVA). Differences with P<0.05 were considered statistically significant.
Results Soil moisture Significant differences in soil moisture content were observed between seasons (P< 0.01, n= 264), where winter > spring > autumn > summer (Fig. 1). However, no significant differences were found between treatments (P<0.05, n=264) during the study period (Table 1). Total number of nematodes The average total number of nematodes ranged between 25 and 143 individuals 100 g-1 dry soil (Fig. 1). The total number of nematodes under H. scoparia reached maximum values in spring of 143 ± 91, and those under Z. dumosum reached a peak value in winter of 131 ± 101 (Fig. 1). The values under Z. dumosum showed a similar trend to that of soil moisture throughout the four seasons. In spring, the mean number of total nematodes was higher under H. scoparia than under Z. dumosum. Overall, a significant difference was observed between seasons (P<0.01, n=264), however, no significant differences were found between vegetation types (P<0.05, n=264) during the study period (Table 1). Nematode taxa In our samples we found 28 genera belonging to three families and in addition the Rhabditinae family (Table 2). Acrobeles, Cephalobus, Aphelenchoides and Rhabditinae were the dominant taxa. Their mean relative abundance was 10.4 %, 12.8 %, 12.7 % and 27.4 % of the nematode community, respectively. The relative abundance of Cephalobus was higher under H. scoparia than under Z. dumosum throughout the
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Fig. 1. Seasonal variation in soil moisture and total number of nematodes (n = 264) under the canopy of two shrubs and at control (interplant) sites during the study period (May 1998 – May 2000). Error bars indicate standard deviation of sample replicates
four seasons. On the contrary, the relative abundance of Rhabditinae was higher under Z. dumosum than under M. scoparia for the same study period. Trophic groups The bacteriovore population under H. scoparia reached maximum values in winter, while those under Z. dumosum reached peak values in spring. These values of bacterivores exhibited a similar trend with those of total nematode number (Figs. 1, 2). Significant differences were found between seasons (P< 0.01, n=264) and treatments (P< 0.05, n=264) in the bacterivore group (Table 2).
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Table 1. Univariate analysis of variance (ANOVA) for soil nematodes under the canopy of two shrub species and in control soil during the study period (May 1998–May 2000) Index 1. Total nematode abundance 2. Trophic structure BF FF PP OP 3. WI 4. F/B 5. T 6. H´ 7. λ 8. SR
Season F-test P value
Vegetation F-test P value
11.09
0.001
1.38
NS
6.57 8.20 3.92 9.21 4.77 1.00 6.24 6.16 2.88 15.25
0.003 0.001 0.009 0.001 0.003 NS 0.004 0.005 0.037 0.001
3.06 0.04 0.96 3.07 1.60 5.89 1.02 0.22 3.14 0.96
0.049 NS NS 0.048 NS 0.003 NS NS 0.045 NS
Indices are: (1) Absolute total abundance: individuals 100 g-1 dry soil. (2) Trophic structure: BF, Bacterivores; FF, Fungivores; PP, Plant parasites; OP, Omnivorespredators. (3) WI, ratio of bacterivores and fungivores to plant parasites. (4) F/B, fungivore/bacterivore ratio. (5) T, trophic diversity. (6) H´, Shannon Index. (7) λ, dominance (8) SR, richness. Values of P< 0.05 were considered significant; NS, non-significant (n= 264)
The fungivore population under H. scoparia and Z. dumosum changed slightly during summer and autumn. The maximum value of fungivores under Z. dumosum was found in spring (Fig. 2). A significant difference was found between seasons (P< 0.01, n= 264), and no significant difference was found between treatments (P< 0.05, n= 264) in the fungivore group (Table 1). The plant parasite population between treatments exhibited a similar trend with those of fungivores during three seasons (spring, summer and autumn). Significant differences were found between seasons (P< 0.01, n=264) and no significant difference was found between treatments (P< 0.05, n=264) in the plant parasite group (Table 1). The omnivore-predator population under H. scoparia and Z. dumosum changed slightly during three seasons (winter, summer and autumn). The maximum value of omnivores-predators under Z. dumosum was found in spring (Fig. 2). Significant difference was found between seasons (P< 0.01, n=264) and between treatments (P<0.05, n= 264) in the omnivore-predator group (Table 1). Ecological indices The ratio of bacterivores and fungivores to plant parasites (WI) under Z. dumosum reached a maximum value in spring, while that under H. scoparia reached a minimum value in summer (Fig. 3). The values of WI were similar between the two shrubs, and
21.7 19.9 33.7 14.6 9.8 10.3 5.6 7.7 14.0 1.5 2.4 9.4 0.0 0.0 0.0
15.1 11.9 10.8 0.5 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Fungivores Aphelenchoides Aphelenchus Ditylenchus Nothotylenchus
Plant-parasites Filenchus Heterodera Meloidogyne
64.0 49.8 17.0 3.9 1.2 2.3 10.8 9.7 0.0 0.0 2.8 0.9 0.0 0.0 0.0 0.0 0.0 1.0 0.0 0.0 1.4 0.0 0.0 0.0 30.8 32.0
Winter ZD CT
60.0 9.4 0.4 20.7 0.0 1.8 0.0 0.0 0.0 0.0 0.0 0.0 27.7
HS
Bacterivores Acrobeles Acrobeloides Cephalobus Cervidellus Chiloplacus Diplogaster Diploscapter Eucephalobus Heterocephalobus Monhystera Plectus Rhabditinae
Season Treatment* trophic groups/ genus/family**
12.4 1.0 0.0 0.0
13.8 6.7 5.5 1.2 0.4
52.3 16.4 0.4 14.3 1.2 0.2 0.0 0.0 5.8 0.0 1.9 1.9 10.2
HS
13.8 1.0 0.0 0.0
17.2 12.7 3.5 1.0 0.0
61.1 16.5 0.3 9.6 0.9 2.3 0.0 0.0 9.3 3.8 0.0 0.0 18.4
16.1 0.5 0.0 0.2
25.2 18.6 2.9 2.0 1.7
39.1 9.6 2.6 9.4 0.0 0.0 0.0 0.0 5.6 0.0 3.3 0.0 8.6
Spring ZD CT
10.2 0.0 0.0 0.0
14.5 7.0 7.1 0.4 0.0
13.0 13.4 0.0 0.1 0.0 1.9 0.0 0.0
16.5 18.6 14.7 13.6 1.8 4.5 0.0 0.5 0.0 0.0
69.6 60.0 10.5 8.6 3.3 4.5 5.4 7.1 0.0 0.0 2.1 1.0 1.8 0.0 0.0 2.4 0.5 0.6 0.0 0.0 0.0 2.4 8.0 4.9 38.0 28.5
Summer ZD CT
73.4 10.7 2.6 19.2 0.0 3.9 0.0 0.0 5.2 0.0 1.1 7.2 23.5
HS
11.4 11.1 0.4 1.4 0.0 0.0 0.4 0.0
24.3 17.6 21.4 9.4 2.3 6.9 0.6 1.1 0.0 0.2
16.7 0.0 0.0 0.0
20.0 13.1 5.7 1.2 0.0
62.7 1.7 3.2 12.8 0.0 0.0 0.0 0.0 3.0 0.0 0.0 0.0 42.0
Autumn ZD CT
60.9 65.8 12.1 8.0 0.0 0.5 21.4 13.5 0.0 0.0 0.0 0.7 0.0 0.0 0.0 0.0 0.0 1.8 0.0 0.0 0.0 0.0 0.0 0.0 27.4 41.3
HS
13.0 0.4 0.2 0.1
20.3 12.7 5.6 1.8 0.2
59.9 10.4 1.8 12.8 0.2 1.3 0.2 0.2 2.7 0.3 0.8 1.8 27.4
Mean
Table 2. Mean relative abundance (%) of soil nematodes under 2 vegetations and control during four seasons (May 1998–May 2000)
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3.2 0.0 3.1 0.1 0.0 0.0
Omnivore-predators Discolaimus Dorylaimus Eudorylaimus Mononchus Nygolaimus
4.2 0.9 3.3 0.0 0.0 0.0
2.3 1.4 1.5 5.8 0.9 5.7 1.7 4.0 0.0 0.0 0.0
0.0 4.8 0.0 6.0 0.0 21.5 2.5 15.0 2.9 0.4 0.7
1.1 2.8 0.9 6.6 0.0 7.9 2.7 3.8 0.7 0.3 0.4
2.8 1.7 5.4 2.9 0.0 19.6 0.0 13.0 5.2 0.2 1.2
0.0 3.5 9.2 2.7 0.0
* HS, Hammada scoparia; ZD, Zygophyllum dumosum; CT, Control. ** By classification of Liang et al. (2000)and Yeates & King (1997)
2.3 5.5 2.3 4.5 0.0
Pratylenchus Tetylenchus Tylenchorhynchus Tylenchus Xiphinema 1.9 1.1 0.8 0.0 0.0 0.0
1.1 5.7 0.4 3.0 0.0 0.9 0.0 0.9 0.0 0.0 0.0
0.0 4.5 2.1 6.4 0.0 8.0 2.8 5.2 0.0 0.0 0.0
2.1 2.9 3.0 3.4 0.0 3.4 0.0 2.0 0.0 1.4 0.0
3.7 2.0 0.4 4.5 0.0 5.5 1.6 0.2 0.0 3.7 0.0
0.0 4.1 0.4 5.2 0.0 0.6 0.0 0.4 0.0 0.2 0.0
1.1 1.6 1.3 12.7 0.0 6.9 1.1 4.3 0.7 0.5 0.2
1.4 3.4 2.2 5.3 0.1
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Fig. 2. Distribution of nematode trophic groups under the canopy of two shrubs and control during the study period (May 1998–May 2000). Error bars indicate standard deviation of sample replicates were lower than those under the control soil during three seasons (winter, summer and autumn) (Fig. 3). Significant differences were found between seasons (P< 0.01, n= 264), and no significant differences were found between treatments (P< 0.05, n= 264) in the WI values (Table 1). The ratio of fungivores to bacterivores (F/B) under H. scoparia and Z. dumosum in our study site was found to be less than one (Fig. 3). The values of F/B under H. scoparia and Z. dumosum fluctuated slightly through three seasons (winter, spring and summer). Significant differences were observed between treatments (P< 0.01, n= 264), and no significant differences were found between seasons (P< 0.05, n = 264) in the F/B values (Table 1). Trophic diversity (T) under H. scoparia and Z. dumosum reached maximum values in spring, respectively (Fig. 3). The values of T under H. scoparia and Z. dumosum exhibited similar trends. Significant differences were observed between seasons
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Fig. 3. Variation of ecological indices of soil nematodes under the canopy of two shrubs and control during the study period (May 1998–May 2000). Error bars indicate standard deviation of sample replicates
(P< 0.01, n= 264), while no significant differences were found between treatments (P< 0.05, n= 264) in the T values (Table 1). The Shannon index (H´) (Fig. 3) exhibited similar trends between H. scoparia and Z. dumosum. The values of H´ were higher under Z. dumosum than under H. scoparia in spring. Significant differences were observed between seasons (P< 0.01, n = 264), while no significant differences were found between treatments (P<0.01, n=264) in the H´ values (Table 1). Genus dominance (λ) under H. scoparia exhibited maximum values in summer, and a minimum value in spring (Fig. 3). The values of λ under Z. dumosum fluctuated slightly across four seasons (Fig. 3). Significant difference was observed between seasons (P< 0.05, n=264) and between treatments (P<0.05, n=264) in the λ values (Table 1).
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Richness (SR) under H. scoparia and Z. dumosum reached maximum values in spring (Fig. 3). The values of SR were lower under the two shrubs than under the control soil in spring and summer. Significant differences were observed between seasons (P< 0.01, n= 264), while no significant differences were found between treatments (P< 0.01, n= 264) in the SR values (Table 1).
Discussion In this two-year study, seasonal fluctuations in soil moisture significantly influenced the temporal distribution of nematode communities under the canopy of two desert halophyte shrubs. An important feature observed across four seasons was that soil moisture content was higher in autumn than in summer. The reason for this may be due to the input of dew, which is an important moisture source in the Negev Desert (Evenari et al. 1982; Steinberger et al. 1989). Significant differences were found between seasons for total number of nematodes and four trophic groups. Significant differences were also observed between treatments for bacterivores and omnivorespredators. There was a significant correlation between the contents of soil moisture and the total number of nematodes, and four trophic groups (P<0.01, n=264) during the study period. The annual mean abundance of total number of nematodes in our experimental site was 74 individuals 100 g-1 dry soil, which was higher than that (48) under the canopy of three shrubs in the same site as reported by Liang et al. (2000), lower than that (272) under the canopy of Z. dumosum in the same site as observed by Steinberger and Loboda (1991), and also lower than that (912) in the northern Mojave Desert ecosystem (Freckman & Mankau 1986). Bacterivores were the most abundant trophic group and omnivores-predators were the least abundant group in treatments during the study period, averaging 60.6 % and 6.9 % of the nematode community, respectively. The mean relative abundance of omnivores-predators was lower than that found by Freckman and Mankau (1986) in the northern Mojave Desert ecosystem, which is classified as a ‘cold desert’ compared with the ‘hot Negev Desert’. Low proportions of omnivores-predators in the nematode population in the Negev Desert are indicative of a lower stability of the habitat (Liang et al. 2000). The mean value of WI in our study is 5.00, which is within the range (0.80-8.70) of values obtained by Wasilewska (1994) for meadow communities. The F/B ratio reflects the structure of the microflora community. Bacteria and fungi are the primary decomposers directly affecting nutrient cycling and nutrient supply to plants (Ingham et al. 1985). The mean F/B ratio value in this study was 0.47, which was similar to that reported in our study at the same site (Liang et al. 2000). This means that there is a high population of bacteria in the desert ecosystem, and a bacterial decomposition pathway was dominant (Hendrix et al. 1986). The trophic diversity index (T) describes the diversity of functional groups within the nematode populations. The average T value in our study (T=2.13) was comparable to the value (2.14) obtained at the same site by Liang et al. (2000), and lower than the value (2.01) observed by Liang et al. (2000) in the northern Negev at Bira-Sluge. The Shannon index (H´) gives more weight to rare species, and a higher index indicates greater diversity. The average H´ value in our experimental site was 1.26,
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which is lower than the value (1.53) obtained by Liang et al. (2000) in the northern Negev at Bira-Sluge. The average λ value in our study was 0.70, which was higher than the value (0.22) obtained by Yeates and King (1997) in the New England Tablelands. The average SR value was 1.07, which was lower than the value (3.03) observed by Yeates and King (1997) in the New England Tablelands. Our results suggest that the seasonal fluctuations of soil moisture in the Negev Desert significantly influenced the distribution of nematode communities. The ability of nematode communities to respond rapidly to variations in soil moisture partially explains their success in the harsh desert environment (Steinberger et al. 1989). The values of ecological indices of nematode communities have been shown to be sensitive indicators of seasonal changes in nematode community composition under the canopy of desert halophytes. Among ecological indices tested, F/B and were effective in distinguishing differences in nematode community structure between treatments during the study period.
Acknowledgments This research was supported in part by the Israel Science Foundation (Grant no. 506/99-17.3) to Prof. Y. Steinberger and by a Fred and Barbara Kort Sino-Israel Postdoctoral Fellowship and SRF for ROCS-SEM to Dr. Wenju Liang. The authors wish to express their appreciation to the staff at Avdat Research Farm. The authors wish to express their appreciation to Prof. G. Yeates for his helpful comments and Ms. Ginetta Barness and Ms. Irit Lavian for technical assistance.
References Bongers, T. (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83, 14–19. Cairns, E. J. (1960) Methods in nematology. In: Sasser, J. N., Jenkins, W. R. (eds) Nematology, fundamentals and recent advances with emphasis on plant parasitic and soil forms. University of North Carolina Press, Chapel Hill, pp. 33–84. Coleman, D. C., Crossley, D. A., Jr. (1996) Fundamentals of soil ecology. Academic Press, London. Dan, J., Yaalon, D. H., Royumdjisky, H., Raz, Z. (1972) The soil association map of Israel. Israel Journal of Earth Sciences 2, 29–49. Evenari, M., Schulze, E. D., Lange, O. L., Kappen, L., Buschbom, U. (1976) Plant production in arid and semi-arid areas. In: Lange, O. L. et al. (ed) Water and plant life. Springer-Verlag, Berlin, pp. 439–451. Evenari, M. E., Shanan, L., Tadmore, W. (1982) The Negev: The challenge of a desert. Harvard University Press, Cambridge, MA. Freckman, D. W. (1988) Bacterivorous nematodes and organic matter decomposition. Agriculture Ecosystems & Environment 24, 196–217. Freckman, D. W., Mankau, R. (1986) Abundance, distribution, biomass and energetics of soil nematodes in a northern Mojave Desert ecosystem. Pedobiologia 29, 129–142. Griffiths, B. S. (1994) Approaches to measuring the contribution of nematodes and protozoa to nitrogen mineralization in the rhizosphere. Soil Use and Management 6, 88–90. Heip, C., Herman, P. M. J., Soetaert, K. (1988) Data processing, evaluation and analysis. In: Higgins, R. P., Thiel, H. (eds) Introduction to the study of meiofauna. Smithsonian Institute Press, Washington, D. C., pp. 197–231.
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Hendrix, P. F., Parmelee, R. W., Crossley, D. A., Jr., Coleman, D. C., Odum, E. P., Groffman, P. M. (1986) Detritus food webs in conventional and no-tillage agroecosystems. BioScience 36, 374–380. Ingham, R. E., Trofymow, J. A., Ingham, E. R., Coleman, D. C. (1985) Interactions of bacteria, fungi and their nematode grazers: effects on nutrient cycling and plant growth. Ecological Monographs 55, 119–140. Liang, W., Pinhasi-Adiv, Y., Shultz, H., Steinberger, Y. (2000) Nematode population dynamics under the canopy of desert halophytes. Arid Soil Research and Rehabilitation 14, 183-192. Sarig, S., Steinberger, Y. (1994) Microbial biomass response to seasonal fluctuation in soil salinity under the canopy of desert halophytes. Soil Biology and Biochemistry 26, 1405–1408. Shannon, C. E., Weaver, W. (1979) The Mathematical Theory of Communication. University of Illinois Press, Urbana, IL. Simpson, E. H. (1949) Measurement of diversity. Nature 163, 668. Steinberger, Y., Loboda, I. (1991) Nematode population dynamics and trophic structure in a soil profile under the canopy of the desert shrub Zygophyllum dumosum. Pedobiologia 35, 191–197. Steinberger, Y., Sarig, S. (1993) Response by soil nematode populations in the soil microbial biomass to a rain episode in the hot, dry Negev Desert. Biology and Fertility of Soils 16, 188–192. Steinberger, Y., Loboda, I., Garner, W. (1989) The influence of autumn dewfall on spatial and temporal distribution of nematodes in the desert ecosystem. Journal of Arid Environments 16, 177–183. Twinn, D. C. (1974) Nematodes. In: Dickinson, C. H., Pugh, G. J. F. (eds) Biology of plant litter decomposition. Academic Press, London, pp. 421–465. Wardle, D. A., Bonner, K. J., Barker, G. M. (2000) Stability of ecosystem properties in response to above-ground functional group richness and composition. Oikos 89, 11–23. Wardle, D. A., Yeates, G. W., Watson, R. N., Nicholson, K. S. (1995) Development of decomposer food-web, trophic relationships and ecosystem properties during a three-year primary succession in sawdust. Oikos 73, 155–166. Wasilewska, L. (1994) The effect of age of meadows on succession and diversity in soil nematode communities. Pedobiologia 38, 1–11. Yeates, G. W., King, K. L. (1997) 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, 526–536.
Seasonal variation in the nematode communities associated with two halophytes in a desert ecosystem Wenju Liang1,2, Stanislav Mouratov1, Yocheved Pinhasi-Adiv1, Pnina Avigad1 and Yosef Steinberger1,* 1 Faculty
of Life Sciences, Bar-Ilan University, Ramat Gan 52900, Israel of Applied Ecology, Chinese Academy of Sciences, Shenyang 110015, P.R. China
2 Institute
Submitted: 20. May 2001 Accepted: 11. September 2001
Summary Seasonal variation in the soil nematode communities was investigated in a field study at the Avdat Research Farm, Israel. Soil samples from 0-10 cm soil were collected monthly between May 1998 and May 2000, under the canopy of two halophyte shrubs: Hammada scoparia and Zygophyllum dumosum. Ecological indices such as ratio of fungivores and bacterivores to plant parasites (WI), fungivore to bacterivore ratio (F/B), trophic diversity (TD), Shannon index (H’), dominance (λ) and richness (SR) were assessed and compared between treatments and between seasons. Twenty nematode families and 26 genera were observed. Acrobeles, Cephalobus, Aphelenchoides and Rhabditidae were found to be the dominant genera/family. Significant differences were found between seasons (P< 0.01) in the number of total nematodes, the four trophic groups and the indices, WI, T, H’, λ, and SR. Bacterivores were found to be the most abundant trophic group in four seasons, their mean relative abundance was 60.6 % of the nematode community. Among ecological indices tested, F/B and λ were effective in distinguishing differences in nematode community structure between treatments during the study period.
*E-mail corresponding author: [email protected]
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Key words: Nematode community, trophic groups, ecological indices, halophytes, desert ecosystem
Introduction Moisture availability in desert ecosystems varies greatly in time and space. Moisture is patchily distributed, with the highest concentration and longest duration under shrubs (Steinberger & Loboda 1991). Desert plants have developed various strategies for exploiting scarce water resources (Evenari et al. 1976). Two halophyte shrubs, Hammada scoparia [Pomel] Iljin. (Fam. Haloragaceae) and Zygophyllum dumosum Boiss. (Fam. Zygophyllaceae), are typical of the hot, dry Negev Desert (Steinberger & Loboda 1991; Sarig & Steinberger 1994; Liang et al. 2000). Steinberger and Loboda (1991) reported that root biomass of Z. dumosum had an important effect on root-nematode dynamics in the northern Negev Highland, at the Avdat Research Farm. Nematodes constitute a numerically important component of soil fauna in desert ecosystems (Freckman & Mankau 1986; Steinberger et al. 1989), but an understanding of the response of nematodes to the unpredictability of moisture availability is far from complete and requires study on a generic basis (Liang et al. 2000). Nematodes occupy an important position in the detritus food web (Ingham et al. 1985; Freckman 1988), taking a significant part in the decomposition of soil organic matter, mineralization of plant nutrients and nutrient cycling (Griffiths 1994). This organism group can be used as sensitive indicators of ecosystem change (Bongers 1990). Combining community analysis with ecosystem function has proved fruitful in the field of soil ecology (Wardle et al. 1995; Coleman & Crossley 1996; Wardle et al. 2000). The objectives of this study were to monitor seasonal variation in the soil nematode communities under the canopy of the two shrubs (H. scoparia and Z. dumosum), and to evaluate several ecological indices of the nematode community in the Negev desert ecosystem.
Materials and Methods The fieldwork in this study was conducted in the northern Negev Highland at the Avdat Research Farm (30° 47´ N, 34° 46´ E). This area has a temperate desert climate, i.e., mild, rainy winters (5–14 °C range 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, the rainfall fluctuates between 20 and 180 mm. An additional source of moisture comes from ca 35 mm of dew, which falls each night, but most heavily during late summer and autumn. The potential annual evaporation rate is ca 2615 mm (Evenari et al. 1982). The perennial vegetation is dominated by the desert shrub association, in which the most common species are H. scoparia and Z. dumosum (Steinberger & Loboda 1991; Sarig & Steinberger 1994; Liang et al. 2000). The soil is a deep, fine-textured loessial sierozem (Dan et al. 1972). A total of 264 soil samples from the upper soil layer (0–10 cm) were collected between May 1998 and May 2000 from a total of 22 months (except for July 1998, May 1999 and February 1999), under the canopy of four individual plants of each of the two species, H. scoparia and Z. dumosum. The control samples were taken from exposed areas between the plants. Af-
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ter sampling, the soil samples were placed in plastic bags, transported to the laboratory in an insulated container, and kept cool (4 °C) until processed. Subsamples were taken from each sample for estimation of nematode populations and soil chemistry. Soil moisture was determined gravimetrically by drying samples at 105 °C for 48 h and expressed as a percentage of dry weight (Liang et al. 2000). Nematodes were extracted from 100 g soil samples using the Baermann funnel procedure (Cairns 1960), and nematode populations were expressed per 100 g dry mass soil. The organisms recovered were counted and preserved in formalin (Steinberger & Sarig 1993). A randomly selected sample of the total organisms was identified, mainly to genus level if possible, using an inverted compound microscope. Trophic groups used were: (1) bacterivores (BF); (2) fungivores (FF); (3) plant-parasites (PP); and (4) omnivores-predators (OP) (Steinberger & Loboda 1991; Steinberger & Sarig 1993; Liang et al. 2000). The nematode community was analyzed by the following approaches: (1) absolute abundance of individuals 100 g-1 dry soil; (2) trophic structure; (3) WI=(FF+BF)/PP (Wasilewska 1994); (4) F/B = FF/BF (Twinn 1974); (5) T= 1/∑pi2, in which pi is the proportion of the ith trophic group (Heip et al. 1988); (6) H´= –∑pi(lnpi), where p is the proportion of individuals in the ith taxon (Shannon & Weaver 1979); (7) λ=∑pi2 (Simpson 1949); (8) SR=(S-1)/ln(N), where S is the number of taxa and N is the number of individuals identified (Yeates & King 1997). All the data were subjected to statistical analysis of variance (ANOVA). Differences with P<0.05 were considered statistically significant.
Results Soil moisture Significant differences in soil moisture content were observed between seasons (P< 0.01, n= 264), where winter > spring > autumn > summer (Fig. 1). However, no significant differences were found between treatments (P<0.05, n=264) during the study period (Table 1). Total number of nematodes The average total number of nematodes ranged between 25 and 143 individuals 100 g-1 dry soil (Fig. 1). The total number of nematodes under H. scoparia reached maximum values in spring of 143 ± 91, and those under Z. dumosum reached a peak value in winter of 131 ± 101 (Fig. 1). The values under Z. dumosum showed a similar trend to that of soil moisture throughout the four seasons. In spring, the mean number of total nematodes was higher under H. scoparia than under Z. dumosum. Overall, a significant difference was observed between seasons (P<0.01, n=264), however, no significant differences were found between vegetation types (P<0.05, n=264) during the study period (Table 1). Nematode taxa In our samples we found 28 genera belonging to three families and in addition the Rhabditinae family (Table 2). Acrobeles, Cephalobus, Aphelenchoides and Rhabditinae were the dominant taxa. Their mean relative abundance was 10.4 %, 12.8 %, 12.7 % and 27.4 % of the nematode community, respectively. The relative abundance of Cephalobus was higher under H. scoparia than under Z. dumosum throughout the
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Fig. 1. Seasonal variation in soil moisture and total number of nematodes (n = 264) under the canopy of two shrubs and at control (interplant) sites during the study period (May 1998 – May 2000). Error bars indicate standard deviation of sample replicates
four seasons. On the contrary, the relative abundance of Rhabditinae was higher under Z. dumosum than under M. scoparia for the same study period. Trophic groups The bacteriovore population under H. scoparia reached maximum values in winter, while those under Z. dumosum reached peak values in spring. These values of bacterivores exhibited a similar trend with those of total nematode number (Figs. 1, 2). Significant differences were found between seasons (P< 0.01, n=264) and treatments (P< 0.05, n=264) in the bacterivore group (Table 2).
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Table 1. Univariate analysis of variance (ANOVA) for soil nematodes under the canopy of two shrub species and in control soil during the study period (May 1998–May 2000) Index 1. Total nematode abundance 2. Trophic structure BF FF PP OP 3. WI 4. F/B 5. T 6. H´ 7. λ 8. SR
Season F-test P value
Vegetation F-test P value
11.09
0.001
1.38
NS
6.57 8.20 3.92 9.21 4.77 1.00 6.24 6.16 2.88 15.25
0.003 0.001 0.009 0.001 0.003 NS 0.004 0.005 0.037 0.001
3.06 0.04 0.96 3.07 1.60 5.89 1.02 0.22 3.14 0.96
0.049 NS NS 0.048 NS 0.003 NS NS 0.045 NS
Indices are: (1) Absolute total abundance: individuals 100 g-1 dry soil. (2) Trophic structure: BF, Bacterivores; FF, Fungivores; PP, Plant parasites; OP, Omnivorespredators. (3) WI, ratio of bacterivores and fungivores to plant parasites. (4) F/B, fungivore/bacterivore ratio. (5) T, trophic diversity. (6) H´, Shannon Index. (7) λ, dominance (8) SR, richness. Values of P< 0.05 were considered significant; NS, non-significant (n= 264)
The fungivore population under H. scoparia and Z. dumosum changed slightly during summer and autumn. The maximum value of fungivores under Z. dumosum was found in spring (Fig. 2). A significant difference was found between seasons (P< 0.01, n= 264), and no significant difference was found between treatments (P< 0.05, n= 264) in the fungivore group (Table 1). The plant parasite population between treatments exhibited a similar trend with those of fungivores during three seasons (spring, summer and autumn). Significant differences were found between seasons (P< 0.01, n=264) and no significant difference was found between treatments (P< 0.05, n=264) in the plant parasite group (Table 1). The omnivore-predator population under H. scoparia and Z. dumosum changed slightly during three seasons (winter, summer and autumn). The maximum value of omnivores-predators under Z. dumosum was found in spring (Fig. 2). Significant difference was found between seasons (P< 0.01, n=264) and between treatments (P<0.05, n= 264) in the omnivore-predator group (Table 1). Ecological indices The ratio of bacterivores and fungivores to plant parasites (WI) under Z. dumosum reached a maximum value in spring, while that under H. scoparia reached a minimum value in summer (Fig. 3). The values of WI were similar between the two shrubs, and
21.7 19.9 33.7 14.6 9.8 10.3 5.6 7.7 14.0 1.5 2.4 9.4 0.0 0.0 0.0
15.1 11.9 10.8 0.5 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Fungivores Aphelenchoides Aphelenchus Ditylenchus Nothotylenchus
Plant-parasites Filenchus Heterodera Meloidogyne
64.0 49.8 17.0 3.9 1.2 2.3 10.8 9.7 0.0 0.0 2.8 0.9 0.0 0.0 0.0 0.0 0.0 1.0 0.0 0.0 1.4 0.0 0.0 0.0 30.8 32.0
Winter ZD CT
60.0 9.4 0.4 20.7 0.0 1.8 0.0 0.0 0.0 0.0 0.0 0.0 27.7
HS
Bacterivores Acrobeles Acrobeloides Cephalobus Cervidellus Chiloplacus Diplogaster Diploscapter Eucephalobus Heterocephalobus Monhystera Plectus Rhabditinae
Season Treatment* trophic groups/ genus/family**
12.4 1.0 0.0 0.0
13.8 6.7 5.5 1.2 0.4
52.3 16.4 0.4 14.3 1.2 0.2 0.0 0.0 5.8 0.0 1.9 1.9 10.2
HS
13.8 1.0 0.0 0.0
17.2 12.7 3.5 1.0 0.0
61.1 16.5 0.3 9.6 0.9 2.3 0.0 0.0 9.3 3.8 0.0 0.0 18.4
16.1 0.5 0.0 0.2
25.2 18.6 2.9 2.0 1.7
39.1 9.6 2.6 9.4 0.0 0.0 0.0 0.0 5.6 0.0 3.3 0.0 8.6
Spring ZD CT
10.2 0.0 0.0 0.0
14.5 7.0 7.1 0.4 0.0
13.0 13.4 0.0 0.1 0.0 1.9 0.0 0.0
16.5 18.6 14.7 13.6 1.8 4.5 0.0 0.5 0.0 0.0
69.6 60.0 10.5 8.6 3.3 4.5 5.4 7.1 0.0 0.0 2.1 1.0 1.8 0.0 0.0 2.4 0.5 0.6 0.0 0.0 0.0 2.4 8.0 4.9 38.0 28.5
Summer ZD CT
73.4 10.7 2.6 19.2 0.0 3.9 0.0 0.0 5.2 0.0 1.1 7.2 23.5
HS
11.4 11.1 0.4 1.4 0.0 0.0 0.4 0.0
24.3 17.6 21.4 9.4 2.3 6.9 0.6 1.1 0.0 0.2
16.7 0.0 0.0 0.0
20.0 13.1 5.7 1.2 0.0
62.7 1.7 3.2 12.8 0.0 0.0 0.0 0.0 3.0 0.0 0.0 0.0 42.0
Autumn ZD CT
60.9 65.8 12.1 8.0 0.0 0.5 21.4 13.5 0.0 0.0 0.0 0.7 0.0 0.0 0.0 0.0 0.0 1.8 0.0 0.0 0.0 0.0 0.0 0.0 27.4 41.3
HS
13.0 0.4 0.2 0.1
20.3 12.7 5.6 1.8 0.2
59.9 10.4 1.8 12.8 0.2 1.3 0.2 0.2 2.7 0.3 0.8 1.8 27.4
Mean
Table 2. Mean relative abundance (%) of soil nematodes under 2 vegetations and control during four seasons (May 1998–May 2000)
68 Wenju Liang et al.
3.2 0.0 3.1 0.1 0.0 0.0
Omnivore-predators Discolaimus Dorylaimus Eudorylaimus Mononchus Nygolaimus
4.2 0.9 3.3 0.0 0.0 0.0
2.3 1.4 1.5 5.8 0.9 5.7 1.7 4.0 0.0 0.0 0.0
0.0 4.8 0.0 6.0 0.0 21.5 2.5 15.0 2.9 0.4 0.7
1.1 2.8 0.9 6.6 0.0 7.9 2.7 3.8 0.7 0.3 0.4
2.8 1.7 5.4 2.9 0.0 19.6 0.0 13.0 5.2 0.2 1.2
0.0 3.5 9.2 2.7 0.0
* HS, Hammada scoparia; ZD, Zygophyllum dumosum; CT, Control. ** By classification of Liang et al. (2000)and Yeates & King (1997)
2.3 5.5 2.3 4.5 0.0
Pratylenchus Tetylenchus Tylenchorhynchus Tylenchus Xiphinema 1.9 1.1 0.8 0.0 0.0 0.0
1.1 5.7 0.4 3.0 0.0 0.9 0.0 0.9 0.0 0.0 0.0
0.0 4.5 2.1 6.4 0.0 8.0 2.8 5.2 0.0 0.0 0.0
2.1 2.9 3.0 3.4 0.0 3.4 0.0 2.0 0.0 1.4 0.0
3.7 2.0 0.4 4.5 0.0 5.5 1.6 0.2 0.0 3.7 0.0
0.0 4.1 0.4 5.2 0.0 0.6 0.0 0.4 0.0 0.2 0.0
1.1 1.6 1.3 12.7 0.0 6.9 1.1 4.3 0.7 0.5 0.2
1.4 3.4 2.2 5.3 0.1
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Fig. 2. Distribution of nematode trophic groups under the canopy of two shrubs and control during the study period (May 1998–May 2000). Error bars indicate standard deviation of sample replicates were lower than those under the control soil during three seasons (winter, summer and autumn) (Fig. 3). Significant differences were found between seasons (P< 0.01, n= 264), and no significant differences were found between treatments (P< 0.05, n= 264) in the WI values (Table 1). The ratio of fungivores to bacterivores (F/B) under H. scoparia and Z. dumosum in our study site was found to be less than one (Fig. 3). The values of F/B under H. scoparia and Z. dumosum fluctuated slightly through three seasons (winter, spring and summer). Significant differences were observed between treatments (P< 0.01, n= 264), and no significant differences were found between seasons (P< 0.05, n = 264) in the F/B values (Table 1). Trophic diversity (T) under H. scoparia and Z. dumosum reached maximum values in spring, respectively (Fig. 3). The values of T under H. scoparia and Z. dumosum exhibited similar trends. Significant differences were observed between seasons
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Fig. 3. Variation of ecological indices of soil nematodes under the canopy of two shrubs and control during the study period (May 1998–May 2000). Error bars indicate standard deviation of sample replicates
(P< 0.01, n= 264), while no significant differences were found between treatments (P< 0.05, n= 264) in the T values (Table 1). The Shannon index (H´) (Fig. 3) exhibited similar trends between H. scoparia and Z. dumosum. The values of H´ were higher under Z. dumosum than under H. scoparia in spring. Significant differences were observed between seasons (P< 0.01, n = 264), while no significant differences were found between treatments (P<0.01, n=264) in the H´ values (Table 1). Genus dominance (λ) under H. scoparia exhibited maximum values in summer, and a minimum value in spring (Fig. 3). The values of λ under Z. dumosum fluctuated slightly across four seasons (Fig. 3). Significant difference was observed between seasons (P< 0.05, n=264) and between treatments (P<0.05, n=264) in the λ values (Table 1).
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Richness (SR) under H. scoparia and Z. dumosum reached maximum values in spring (Fig. 3). The values of SR were lower under the two shrubs than under the control soil in spring and summer. Significant differences were observed between seasons (P< 0.01, n= 264), while no significant differences were found between treatments (P< 0.01, n= 264) in the SR values (Table 1).
Discussion In this two-year study, seasonal fluctuations in soil moisture significantly influenced the temporal distribution of nematode communities under the canopy of two desert halophyte shrubs. An important feature observed across four seasons was that soil moisture content was higher in autumn than in summer. The reason for this may be due to the input of dew, which is an important moisture source in the Negev Desert (Evenari et al. 1982; Steinberger et al. 1989). Significant differences were found between seasons for total number of nematodes and four trophic groups. Significant differences were also observed between treatments for bacterivores and omnivorespredators. There was a significant correlation between the contents of soil moisture and the total number of nematodes, and four trophic groups (P<0.01, n=264) during the study period. The annual mean abundance of total number of nematodes in our experimental site was 74 individuals 100 g-1 dry soil, which was higher than that (48) under the canopy of three shrubs in the same site as reported by Liang et al. (2000), lower than that (272) under the canopy of Z. dumosum in the same site as observed by Steinberger and Loboda (1991), and also lower than that (912) in the northern Mojave Desert ecosystem (Freckman & Mankau 1986). Bacterivores were the most abundant trophic group and omnivores-predators were the least abundant group in treatments during the study period, averaging 60.6 % and 6.9 % of the nematode community, respectively. The mean relative abundance of omnivores-predators was lower than that found by Freckman and Mankau (1986) in the northern Mojave Desert ecosystem, which is classified as a ‘cold desert’ compared with the ‘hot Negev Desert’. Low proportions of omnivores-predators in the nematode population in the Negev Desert are indicative of a lower stability of the habitat (Liang et al. 2000). The mean value of WI in our study is 5.00, which is within the range (0.80-8.70) of values obtained by Wasilewska (1994) for meadow communities. The F/B ratio reflects the structure of the microflora community. Bacteria and fungi are the primary decomposers directly affecting nutrient cycling and nutrient supply to plants (Ingham et al. 1985). The mean F/B ratio value in this study was 0.47, which was similar to that reported in our study at the same site (Liang et al. 2000). This means that there is a high population of bacteria in the desert ecosystem, and a bacterial decomposition pathway was dominant (Hendrix et al. 1986). The trophic diversity index (T) describes the diversity of functional groups within the nematode populations. The average T value in our study (T=2.13) was comparable to the value (2.14) obtained at the same site by Liang et al. (2000), and lower than the value (2.01) observed by Liang et al. (2000) in the northern Negev at Bira-Sluge. The Shannon index (H´) gives more weight to rare species, and a higher index indicates greater diversity. The average H´ value in our experimental site was 1.26,
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which is lower than the value (1.53) obtained by Liang et al. (2000) in the northern Negev at Bira-Sluge. The average λ value in our study was 0.70, which was higher than the value (0.22) obtained by Yeates and King (1997) in the New England Tablelands. The average SR value was 1.07, which was lower than the value (3.03) observed by Yeates and King (1997) in the New England Tablelands. Our results suggest that the seasonal fluctuations of soil moisture in the Negev Desert significantly influenced the distribution of nematode communities. The ability of nematode communities to respond rapidly to variations in soil moisture partially explains their success in the harsh desert environment (Steinberger et al. 1989). The values of ecological indices of nematode communities have been shown to be sensitive indicators of seasonal changes in nematode community composition under the canopy of desert halophytes. Among ecological indices tested, F/B and were effective in distinguishing differences in nematode community structure between treatments during the study period.
Acknowledgments This research was supported in part by the Israel Science Foundation (Grant no. 506/99-17.3) to Prof. Y. Steinberger and by a Fred and Barbara Kort Sino-Israel Postdoctoral Fellowship and SRF for ROCS-SEM to Dr. Wenju Liang. The authors wish to express their appreciation to the staff at Avdat Research Farm. The authors wish to express their appreciation to Prof. G. Yeates for his helpful comments and Ms. Ginetta Barness and Ms. Irit Lavian for technical assistance.
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