Biol Fertil Soils (2007) 43:357–366 DOI 10.1007/s00374-006-0117-2
ORIGINAL PAPER
Ameba community dynamics and diversity in a desert ecosystem E. Mayzlish-Gati & Y. Steinberger
Received: 5 September 2005 / Revised: 27 April 2006 / Accepted: 28 April 2006 / Published online: 15 June 2006 # Springer-Verlag 2006
Abstract A field study was conducted to monitor the effect of different desert shrub ecophysiological adaptations on the composition, size, and diversity of soil free-living amebae. Population diversity was also analyzed using four morphological types. Samples were collected seasonally under the canopy of the common desert shrubs Artemisia herba alba, Reaumuria negevensis, and Noea mucronata. Control samples were taken from exposed interspace areas between shrubs. The composition and diversity of the ameba population were significantly affected by both season and plant species. Types 3 and 4 amebae were found to create a complementary system of adaptation in which type 3 was resistant and adapted to the harsh environment, whereas type 4 was much more vulnerable and existed for short periods of time when the environment allowed. The Reaumuria negevensis ecophysiological adaptation had a negative effect on type 4 amebae by creating a stressed environment. Keywords Soil . Desert . Protozoa . Soil free-living ameba
Introduction A desert ecosystem was defined by Noy-Meir (1973) as a “low productivity environment with extreme fluctuation of primary production due to lack of rain events and nutrient availability”. Water is one of the most limiting factors in arid and semi-arid terrestrial ecosystems. During 90% of the year, arid desert soil exists in a severe state of dryness E. Mayzlish-Gati (*) : Y. Steinberger Faculty of Life Sciences, Bar-Ilan University, 52900 Ramat-Gan, Israel e-mail:
[email protected]
(Odum 1985; Ashraf and McNeilly 1994). In the Negev Desert of Israel, water availability is unpredictable in frequency, time, and amount, and is limited to the rainy season (October–April). Rain events occur during very short periods and produce runoffs and floods. An additional source of water is dew formation, which occurs heavily during 210 nights of the year (Evenari et al. 1982). Biological processes in the world’s deserts and arid regions are mainly controlled by the water regime and its scarcity (Fliessbach et al. 1994). However, under the canopy of desert shrubs, biological activity lasts beyond the rainy season and also occurs during the dry periods. The desert perennial plants form “islands of prolonged activity” by creating heterogeneity in soil resources, with higher amounts of carbons, nitrogen, phosphates, and sulfur compared to the bare soil (Schlesinger et al. 1996; Rodriguez-Zaragoza and Garcia 1997; Robinson et al. 2002), due to continued plant nutrient cycling under the shrubs. Moreover, water content under the shrubs increases because the plant canopy guides the rainwater by stem flow into the ground around the shrub base, and partly because branch shedding reduces the transpiring surface, thus increasing water economy (Reynolds et al. 1999). Desert plants have developed different strategies for exploiting scarce water resources. Arido-passive plants, which are dormant during the dry periods, respond quickly to any rainfall event by rapid growth and reproduction (Evenari et al. 1982). Arido-active plants are metabolically active during the wet as well as during the dry seasons, and have structural and ecophysiological adaptations, which conserve moisture and exploit water resources. The various ecophysiological adaptations of desert shrubs can be defined by the ability to confront biotic or abiotic factors. Plant–plant interference due to a lack of water availability, nutrients, and organic matter and because
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of a surplus of radiation and temperature can result in the allelopathic phenomenon in which one plant inhibits other surrounding plants by producing toxic organic compounds that are released into the environment (Kruse et al. 2000). Escudero et al. (2000) found that this adaptation became more efficient as water stress increased. Desert soils contain high amounts of soluble salts with which the plants must cope (Sarig and Steinberger 1994). The plants must confront some restricted conditions due to this problem, mainly high osmotic pressure of the soil solution, which interferes with the ability of the plant to hold ground water (Tkatchenko 1951). Some plants have “solved” this problem by a mechanism of salt resistance by which they absorb salts through their root system, translocate them to the leaves, and redeposit the salts on the ground. This mechanism results in “islands of salinity” under the plant canopy (Flowers et al. 1977; Sarig and Steinberger 1994). Furthermore, this adaptation contributes to the plant’s water economy because of the hygroscopic nature of salt, which results in moisture absorption in the plant’s microhabitat (Simon et al. 1994). Understanding the influence of desert shrubs with different ecophysiological adaptations on soil biota is extremely important. Biogeochemical cycles that take place in the soil milieu are mainly triggered by soil biota and are, therefore, responsible for nutrient availability to the plant (Murray et al. 2001; Becker et al. 2001; Bardgett et al. 2002). However, the materials exuded into the soil by the resisting desert plants, i.e., toxic organic compounds or salt, may interfere with and modify natural biotic processes. Soil free-living amebae have been recognized (Anderson and Rogerson 1995; Rodriguez-Zaragoza and Garcia 1997; Bischoff 2002) as playing an important ecological role in terrestrial systems, including nutrient cycles, regulation of microflora populations, and as a possible food source for earthworms, nematodes, and other soil-dwelling invertebrates. Understanding the effects of ecophysiological adaptations of different desert shrubs on the dynamics and biodiversity of this important group can, therefore, be a milestone in the understanding of the dynamics of the main compartments of the food web under these conditions. Two common Negev shrubs representing the ecophysiological adaptations mentioned above were chosen for this study: Reaumuria negevensis, which has a mechanism of salt resistance (Tadmor et al. 1962), and Artemisia herba alba, as a representative of allelopathic plants (Friedman et al. 1977). The common shrub Noea mucronata was chosen as a control plant due to the fact that its ecophysiological adaptation does not affect its surroundings, unlike the other two above-mentioned plants. The aim of this study was to examine the effect of desert plant adaptations on the abundance, dynamics, and biodiversity of the soil free-living ameba population.
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Study site The study was conducted on the Avdat slopes (34°46′ E/ 30°47′ N) in the Negev Desert, Israel. This site is approximately 600 m above sea level, with a multi-annual average rainfall of 89.5 mm (at Avdat Station). The area consists of loess plain rocky slopes with shallow, saline gray lithogenic calcareous soils. The soil at the study site is an alkaline (pH 7.8), deep, fine-textured loessial sierozem (Dan et al. 1972), with small amounts of organic carbon (0.47%) and large amounts of carbonate (40%). The climate is Mediterranean, with mild, rainy winters (5–14°C in January) and hot summers (18–32°C in June). The annual evaporation rate is 2,615.3 mm (Evenari et al. 1982). Soil samples were collected randomly under each of four individual Artemisia herba alba, Reaumuria negevensis, and Noea mucronata plants at the 0–10 cm depth. Control samples were taken from exposed interspace areas between the shrubs. The samples were placed in individual plastic bags and transported to the laboratory in a cooler to avoid heating during the hot summer months. All soil samples were sieved (mesh size: 2 mm) to remove root particles and other organic debris. Sets of subsamples from each replicate were used to determine soil moisture, soil conductivity, total soil ameba populations, and soil ameba diversity. The soil samples were taken in midseason in winter, spring, summer, and autumn of 2002–2003.
Materials and methods a. Soil moisture was determined gravimetrically by drying a subsample of known weight at 105°C for 48 h, and was expressed as a percentage of dry weight. b. Soil conductivity was determined on a 5-gr subsample that was agitated (half-hour at room temperature) with 50 ml distilled water. The filtrated solution was analyzed using a conductivity meter. c. Total soil ameba abundance was measured using the most probable number (MPN) with the serial dilution method (APHA 1992). Soil extract at a dilution of 1:5 (working solution) was used for the MPN procedure. Soil extract was prepared by homogenizing 200 g soil in 1,000 ml tap water under continuous heating at 60°C for 2 h, after which it was filtered and autoclaved for 15 min (Singh 1975). Twenty-four well tissue-culture plates were inoculated as follows: a soil–water mixture was prepared by homogenizing 1 g soil in 10-ml soil extract. Five 15-s pulses of vigorous shaking in a vortex achieved homogenization. The homogenate was left undisturbed for 15 min. Tenfold serial dilutions were then made, beginning with 10−2 and ending with 10−7. These dilutions were prepared by taking 100 μl from the soil
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mixture and placing them in the first row of the 24-well tissue-culture plates previously filled with 900 μl soil extract. Six dilutions with four replicates were prepared for each dilution. The plates were incubated at 28°C for 7–10 days and reviewed under a phase contrast inverted microscope for the presence of amebae. d. Identification of free-living amebae was accomplished after cultivation on non-nutritive agar plates. No live or dead bacteria were added to the medium, to avoid the overgrowth of bacterial-feeder amebae over those that feed on different sources such as yeast, fungi, algae, protozoa, and/or other organisms. The initial cultivation was performed by homogenizing a 1-g soil sample in 10 ml soil extract to a final dilution of 1:10. Homogenates were then left untouched for 30 min for particle sedimentation and the supernatant was gently transferred onto the bacteria-free non-nutritive agar plates. The amebae were allowed to settle on the agar for 2 h before withdrawal of the excess water, avoiding ciliate and flagellate growth. Cultivates were identified under a binocular microscope after 15 days of incubation at 26°C. Amebae were identified morphologically using phase-contrast microscope, using the keys of Page (1976, 1988) and Patterson (1996). Species diversity was calculated by the Shannon–Weaver formula (Shannon and Weaver (1949). Amebae were assigned to the four morphological types described by Anderson and Rogerson (1995). e. All the data obtained in the study were subjected to statistical analysis of variance (ANOVA). Differences at the p
