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Properties and spatial distribution of microbiotic crusts in the Negev Desert, Israel
Catena 82 (2010) 92–101
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Catena j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c a t e n a
Properties and spatial distribution of microbiotic crusts in the Negev Desert, Israel Giora J. Kidron a,⁎, Ahuva Vonshak b, Inka Dor c, Sophia Barinova d, Aharon Abeliovich e,1 a
Institute of Earth Sciences, The Hebrew University, Givat Ram Campus, Jerusalem 91904, Israel Dept. of Dryland Biotechnologies, The Jacob Blaustein Institute for Desert Research, Ben Gurion University of the Negev, Sede Boqer Campus 84993, Israel c Environmental Sciences Division, The Hebrew University, Givat Ram Campus, Jerusalem 91904, Israel d Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel e Dept. of Biotechnology Engineering, Faculty of Engineering, Institute of Biotechnology, Ben Gurion University of the Negev, Beer Sheva 84105, Israel b
a r t i c l e
i n f o
Article history: Received 24 June 2009 Received in revised form 12 May 2010 Accepted 18 May 2010 Keywords: Biological soil crust Sand dune Moisture Microbiotic crust Cyanobacteria Mosses Negev Desert
a b s t r a c t Playing a cardinal role in surface stabilization and in carbon and nitrogen fixation, microbiotic crusts play a crucial role in arid regions where they may serve as useful biomarkers for wind power and wetness duration. This is especially the case on relatively unstable and infertile sand dunes in the Negev Desert where high correlations between the crust chlorophyll content and the daytime wetness duration were found. Yet, only scarce data are available as to the possible link between the chlorophyll content and other physical (color, thickness, strength, crack density, surface roughness and infiltrability) and biological (protein, carbohydrate, organic matter and species composition) factors, which determine, in turn, the crust type and its effect upon geomorphological and ecological processes. No data are available on crust type distribution. These were the aims of the current research. When a cluster analysis was performed, five types of microbiotic crusts were defined, four of which were cyanobacterial (A–D) and one moss-dominated crust (E). The crusts differed in their physical and biological properties. They showed an increase in chlorophyll content, protein, carbohydrates and organic matter from A to E, with concomitant increase in species diversity, thickness, roughness and strength, but with some variables (crack density and infiltrability) showing a reversed trend at the moss-dominated crust. The increase in the biomass components of the crust and the gradual change of the physical properties are explained by the improved physical conditions (primarily wetness duration), which facilitates longer hours of photosynthetic activity and consequently the introduction of additional, more mesic species such as green algae, lichens and mosses. Extended wetness duration was found to shift the crust type from cyanobacterial to moss-dominated crust. The spatial distribution of the crusts, as verified by crust mapping, coincided with the daylight surface duration, which in turn was controlled by topography (aspect, angle and slope position). It implies that whereas initial physical conditions dictates species composition and thus crust type, the crust type in turn is responsible for characterizing the physical properties of the surface, which may largely affect ecological and geomorphological processes. © 2010 Elsevier B.V. All rights reserved.
1. Introduction As a result of the low cover of higher plants in arid regions, microbiotic crusts often fulfill similar functions such as surface stabilization (van den Ancker et al., 1985; McKenna Neuman et al., 1996) or organic carbon (Lange et al., 1992) and nitrogen (Mayland and McIntosh, 1966; Evans and Lange, 2001) fixation. Additionally, the crusts may significantly alter the hydrological properties of the surface (Booth, 1941; Kidron and Yair, 1997; Belnap, 2006), and affect plant germination and establishment (St. Clair et al., 1984; Prasse and Bornkamm, 2000). All the above functions may be largely dependent upon the crust biomass, its species composition and its physical ⁎ Corresponding author. Tel.: + 972 54 496 7271; fax: + 972 2 566 2581. E-mail address: [email protected] (G.J. Kidron). 1 Deceased. 0341-8162/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.catena.2010.05.006
properties, all of which may show a gradual increase, which may be difficult to sort into distinct categories. Nonetheless, these categories, namely, the definition of distinct crust types, are essential for ecologists and geomorphologist aiming to study abiotic–biotic relationships. In a previous study (Kidron et al., 2009) carried out at the Nizzana research station, at the Hallamish dune field, western Negev Desert (mean annual precipitation of 95 mm), a high correlation was found between crust cover and wind power and between the crusts chlorophyll content and the surface wetness duration. This study was conducted along a 12 point transect (hereafter stations, each having a pair of plots) that extended between two crests of active dunes, crossing a stabilized low dune and two interdunes (Figs. 1 and 2). While stations 1 and 12 were demarcated at the mobile dune crests (and therefore lacked crusts) and stations 2 and 11 were established on the semi-stable midslopes (having therefore a patchy and
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Fig. 1. Location and the experimental layout at the Nizzana research site.
fragmented crust cover), low wind power characterized the remaining stations (stations 3–10) where the crusts appeared homogeneous and where a clear topographically-induced zonation in the chlorophyll content was noted (Fig. 3). At these stations, a high correlation was obtained between the crust chlorophyll content and surface wetness duration (Kidron et al., 2009). Unlike disturbed habitats that are characterized by immature crusts that exhibit different stages of development (Belnap et al., 2008; Kidron et al., 2008), this research was conducted on surfaces or crusts found to be in a quasi equilibrium with the abiotic conditions. While high wind power at the dune crest and the upper dune slopes
was regarded as a negative factor that can cause crust death following its burial, extended wetness duration was seen as a positive factor responsible for the crusts' chlorophyll content, thus facilitating net photosynthetic carbon gain. The chlorophyll content is however only one of the biological properties of the crust. Wetness duration may well affect other crust properties. Furthermore, while a large-range continuum, ranging from several milligrams to almost 100 mg of chlorophyll a per square meter was monitored, any practical evaluation of the crust role will necessitate a relatively clear distinction of the crust types. Knowledge regarding the types of the crust may assist in highlighting the crust
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Fig. 2. Plots at the north facing slope of the stabilized dune. Note the mobile sand at the crest of the high altitude dune at the rare of the photograph (station 12 of transect).
role upon geomorphological and ecological processes, such as its impact upon runoff and infiltration, carbon and nitrogen fixation, plant germination and so forth. Based on the high correlation between daylight wetness duration and the crust chlorophyll content, we hypothesized that wetness duration may also determine other properties. We further hypothesized that a break down into discrete crust types may be possible and
consequently crust mapping. The objectives of the current research were therefore: (1) To classify the crusts into distinct types based on their overall characteristics. (2) To evaluate the pattern, rationale and spatial setting of the crusts.
Fig. 3. Mean chlorophyll content and wetness duration and the crust types A–E along a transect (modified from Kidron et al., 2009).
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2. Methodology The research was confined only to the crusted dune sections along a transect (i.e., stations 3–10) that extended between two crests of active dunes, crossing a stabilized low dune and two interdunes (Figs. 1 and 2 and see also Kidron et al., 2009). Each station consisted of a pair of plots having homogeneously looking crusts (Table 1). In order to characterize the crust properties, physical and biological variables were monitored. The physical variables monitored included color, thickness, compressional strength, crack density, roughness and water infiltrability. The biological variables included chlorophyll a, protein, total carbohydrates, organic matter and species composition. Color was determined in a dry and wet state with a Munsell color chart. Crust thickness was determined with 4–6 crust samples randomly taken from each plot. Following wax coating, crust thickness was measured with a caliper (micrometer) following the method outlined by Blake and Hartge (1986). Pieces of crusts were tied with a thin nylon thread and immersed for approximately 2–3 s into hot wax. After the wax cooled off, the crust thickness (i.e. overall thickness minus wax thickness) was calculated. The wax thickness was determined by a comparison to a wax coated piece of plywood of known thickness. The compressional strength of the crust was determined with 4–6 randomly chosen crusts taken from each plot. The crusts, 2 cm in diameter, were placed over a 1.4 mm opening and subjected to the weight imposed by 1.2 diameter plate (i.e., 1 cm2) attached to the end of a narrow container. Water was carefully filled into the container resulting in increasing pressure of the plate upon the crust. Crust strength was determined as the total weight of the container plus the amount of water responsible for breaking the crust, in accordance with the method proposed by Katznelson (1989). Crack density, determined as the crack length per surface area, was determined in 10–20 randomly chosen 10 × 10 cm squares in each plot. Six to twelve measurements were also carried out in each plot for surface roughness. Surface roughness was determined with 18.8 cmlong microrelief meter having rods spaced at 3.1 mm apart, as Table 1 Plot description. Only the crusted plots 3–10 were monitored during the current research. Plot Plot no.
Surface Interdune Aspectb Topographic Slope Plant Crust area or dune position (°) cover presence (m2) typea (%)
1
2.3 2.3 2.1 2.0 6.6 3.9 2.3 2.3 1.2 1.8 6.6 1.4 6.3 4.1 2.3 3.6 2.3 2.3 3.6 2.5 3.1 2.5 2.3 2.3
2 3 4 5 6 7 8 9 10 11 12 a b
1W 1E 2W 2E 3W 3E 4W 4E 5W 5E 6W 6E 7W 7E 8W 8E 9W 9E 10W 10E 11W 11E 12W 12E
Act Act Act Act Act Act ID
dune dune dune dune dune dune
SF SF SF SF SF SF SF
Top Top Mid Mid Lower Lower Lower
Stab dune NF
Lower
Stab dune NF
Mid
Stab dune NF
Up–Mid
Stab dune NF
Top
ID
SF
Lower
Act dune
NF
Lower
Act dune
NF
Mid
Act dune
NF
Top
5 3 13 17 9 8 2 1 7 10 16 17 13 14 8 10 1 2 11 13 21 23 4 3
Act = active dune; Stab = stabilized dune; ID = interdune. SF = south-facing; NF = north-facing.
0 0 0 0 1 10 2 4 0 0 0 5 1 6 0 2 3 2 2 2 2 1 0 0
None None Partially Partially Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Partially Partially None None
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described elsewhere (Kidron, 2007). The variance in rod height (in absolute values) represented roughness (Sanchez and Wood, 1987). Water infiltrability, sometimes referred to as hydrophobicity, was determined via 10–15 measurements taken at each plot. It was determined by measuring the time required for a drop of distilled water placed on the surface to penetrate the crust. According to this method, known as the Water Drop Penetration Time (WDPT), infiltration in excess of 60 s implies high hydrophobicity, 10–60 s implies medium hydrophobicity, while penetration time of less than 10 s indicates a lack of hydrophobicity (Adams et al., 1969). Chlorophyll a (hereafter chlorophyll) concentration was determined in 1.0 cm thick 18–24 cores of 1.2 cm diameter each taken from each plot. Chlorophyll was extracted by hot methanol (70 °C, 20 min) in the presence of MgCO3 (0.1% w/v) in sealed test tubes and assayed according to Wetzel and Westlake (1969). After the extraction of the chlorophyll, half of the samples were used for protein determination according to Lowry et al. (1951), and the other half for carbohydrate determination by the anthrone method (Hassid and Abraham, 1957). The organic matter (OM) was measured in six randomly chosen samples taken from each plot. The OM was determined by comparing the sample weight (approx. 25 g) prior and subsequent to oven ignition at 400 °C for 8 h (Tranter et al., 2007). Cyanobacteria and algae were defined according to Geitler (1932) and Starmach (1966). In certain cases, isolation and growth of the species (in BG11 medium, 1.5% agar) were necessary and consequently carried out. In order to evaluate the relative proportion of each of the identified cyanobacteria and algae species, 4 crusts, approximately 5 cm2 each, were taken from each plot, and the lichens within each sample were defined. The crusts were then immersed in water, thoroughly mixed and the dilution was examined under a light microscope. The number of cells per slide was counted and ranged according to Whitton et al. (1991). Moss stems were counted at 30 randomly chosen crust samples (1.2 cm diameter each) taken from each plot. Moss cover was also visually estimated (in percent). Crust types were determined using cluster analysis based on the various crust properties. The clustering was performed using the means of all the measured parameters. The centroid method was used with Euclidean distance as a measure of dissimilarity (van Tongeren, 1987). The small differences between the sample sizes facilitated the execution of an ANOVA. Because of the high heterogeneity of variance, a t-test was chosen for the comparison of all biomass components (chlorophyll, protein and carbohydrates) and for the total organic matter. Differences were significant at P b 0.05. 3. Results Measurements of each parameter within each plot showed great similarity, in agreement with the high visual homogeneity observed. As a result, we feel that the number of measurements that were carried out for each parameter, adequately represent the plot, despite the micro-scale spatial diversity that one may expect. In fact, biomass parameters exhibited the higher variability and consequently the relatively large number of repetition taken. High variability was nevertheless found between the plots. It included all parameters examined, such as crust thickness, color, compressional strength as well as the crust's biological parameters. These parameters were characterized by a gradual change that did not allow immediate classification. Thus for instance, a gradual thickening of the crust from 1 to 3 mm was noted within the cyanobacterial crusts, and likewise, all biological parameters such as chlorophyll, protein and carbohydrates showed a gradual increase in accordance with crust thickness. A cluster analysis was thus performed in order to better characterize the crust types. It was based on crust color (dry and wet), thickness, compressional strength, crack density, surface roughness, infiltrability (dry and wet), chlorophyll a, protein, total carbohydrate, OM, species composition and moss stem count.
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Five types of crusts were defined and labeled as crusts A, B, C, D and E (Fig. 4). The topographic setting and above all elevation contours played a cardinal role in crust clustering as pointed out by the fact that all plots within the same topographical position along the slope were clustered into the same crust type. Thus, north-facing plots with similar azimuth and slope angles and at similar slope section was clustered together while south-facing plots and interdunal plots were also clustered together. Whereas the difference between crusts B and C was the least pronounced, crust E differed markedly from the remaining crusts. ANOVA test showed significant differences between the crusts with: Chlorophyll: F (4, 459) = 43.2 P b 0.001 Protein: F (4, 446) = 238.7 P b 0.001 Carbohydrates: F (4, 459) = 146.5 P b 0.001 When a t-test was executed, all five crusts defined differed significantly from each other (P b 0.05) in their chlorophyll, protein and carbohydrate, as well as in their total organic matter (Fig. 5). Whereas chlorophyll, protein and carbohydrate content were 17 mg m− 2, 4.2 g m− 2 and 5.3 g m− 2 in crust A, respectively, values as high as 53 mg m− 2, 32.1 g m− 2 and 34.4 g m− 2 characterized the chlorophyll, protein and carbohydrate content of crust E, respectively, with intermediate values characterizing crusts B–D. A total of 7 genera of cyanobacteria were identified, three green algae and two mosses. In addition, several lichen genera were also identified (Table 2). Microcoleus vaginatus was found to be the dominant cyanobacterium. Microculeus sociatus, previously identified as the dominant species in the site (Lange et al., 1992) was not identified during the present research. Another species that was previously defined, Calothrix sp. was also not recorded during the current research. The change in the crust chlorophyll, protein and carbohydrates was accompanied by a change in species composition. Whereas M. vaginatus, Trentepholia sp. and Phormidium sp. were highly dominant in crust type A, higher abundance of species characterized crusts B–E with larger proportions of other species of cyanobacteria including Scytonema sp., Nostoc microscopicum, Oscillatoria sp., and Schizothrix friesii. Crusts B–E also had a larger proportion of green algae. One filamentous genus, Microspora sp. and two coccoid genera Clorococcum
Fig. 5. Mean values of Chlorophyll a, carbohydrates, protein, and organic matter of crust types. Bars represent one SD. All values within each variable differed significantly from each other (P b 0.05).
Fig. 4. Cluster analysis of crusts within the research site.
G.J. Kidron et al. / Catena 82 (2010) 92–101 Table 2 Species composition of mosses (number of moss stems and visual estimation of cover in parenthesis) and of cyanobacteria, algae and lichens of each crust type as determined after Whitton et al., 1991 (1 — Occasional with 1–5 cells per slide; 2 — rare with 5–15 cells; 3 — Common with 15–25 cells; 4 — Frequent with several cells over a slide transect; 5 — Abundant with cells in each field of view). Species composition
A
B
C
D
E
Microcoleus vaginatus Trentepohlia sp. Phormidium sp. Nostoc microscopicum Scytonema sp. Oscillatoria sp. Schizothrix friesii Green algae (Microspora sp., Chlorococcum sp., Stichococcus sp.) Lichens (Aspicilia sp. Fulgensia fulgens, Caloplaca holocarpa, C. tominii, Collema tenax) Mosses (Bryum dunense, Tortula brevissima)
5 4 3 1 1 1 1 1
5 4 2 1 2 1 1 1
4 5 2 2 3 2 2 1
4 2 1 3 4 3 3 2
3 – 1 3 3 3 3 3
1
1
1
2
1
5.5 × 102 (b0.1%)
8.3 × 102 (0.1%)
3.3 × 103 (1%)
4.7 × 104 (10%)
7.8 × 105 (80%)
sp. and Stichococcus sp. were defined. Two moss species, Bryum dunense and Tortula brevissima were also defined. Several species of lichens were also identified including Fulgensia fulgens, Caloplaca holocarpa, C. tominii and Collema tenax. The change in the biomass components and species composition was reflected in the crust physical and biological properties. Thus, the crust tends to become darker with the increase in chlorophyll, protein and carbohydrates and the change in species composition reflecting higher proportions of dark pigmented cyanobacteria such as Scytonema sp. and Nostoc sp. (Fig. 6). The increase in chlorophyll, protein and carbohydrates was accompanied also by an increase in crust thickness and OM. Crust thickness increased from 1.1 mm in crust A to 10.3 mm in crust E while the OM increased from 0.46% in crust A to 2.59% in crust E (Fig. 5). Likewise, crust roughness increased from crusts A and B (1.8 mm cm− 1) to E (3.1 mm cm− 1), whereas crack density increased from crust A (3.6 m m− 2) to D (18.9 m m− 2), but sharply decreased in crust E (6.7 m m− 2). Excluding crust B, The crust' compressional strength also showed an overall increase from crust A
97
(175.4 g cm− 2) to E (782.0 g cm− 2). As for water infiltrability, a gradual decrease was measured from crusts A (0.2 s) to E (1.1 s) under dry conditions. However, a sharp increase in water infiltrability was noted in crust E under wet conditions, from 1.1– 1.7 s in crusts A–D to 0.2 s in crust E (Table 3). Overall, these changes were relatively small on the hydrophobicity scale and below the threshold defined to indicate hydrophobicity. When the surface wetness duration was included in the cluster analysis, no change was detected in the clustering pattern (not shown), attesting to the close link between wetness duration and crust type (Fig. 3 and Kidron et al., 2009). A close link was also obtained between daylight wetness duration and the moss stem counts (Fig. 7). Consequently, daylight wetness duration may be regarded as the causal factor determining crust type and the change from cyanobacterial to moss-dominated crust. The link between daylight wetness duration and topography (aspect, angle and slope position) on the one hand and between daylight wetness duration and the crust chlorophyll content and hence crust type on the other hand facilitated crust mapping (Fig. 8). While crusts were absent from ∼ 40% of the area (mobile and semimobile dune sections and fine-grained playa surfaces), the remaining dunes and interdunes were inhabited by 5 types of microbiotic crusts. Out of the crusts, crust A was dominant (∼ 77% of the crusted surfaces), occupying the south-facing slopes and the interdunes, while crust D and E occupied each the lowest percentage of the surface (∼3–4% each), with crusts B and C occupying each ∼ 7–9% of the surface area (Table 4). 4. Discussion Cluster analysis showed 5 distinct crust types. All crusts showed high zonation in accordance with daylight wetness duration, which in turn may reflect photosynthetic activity. By controlling the crust type, wetness duration is responsible for a change in species composition, and the biological and physical properties of the crusts. The change in species composition, in accordance with moisture availability, is in agreement with other arid zones, in which crusts were mainly categorized into two types, xeric and mesic (Belnap, 2001). Thus, Microcoleus sp. that was found in Nizzana to predominate in the most xeric crust type was also found to predominate in the more xeric arid and semi-arid crusts of the North American deserts
Fig. 6. Dry (top) and wet (bottom) crust samples of the different crust types. Note that the moss yellow color (crust E) during summertime turns green during wintertime.
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Table 3 The physical properties and the amount of subsurface fines in all crust types. Number in parenthesis indicates one SD while N indicates the sample number. Different letters indicate significant differences (P b 0.05). Thickness
Crust strength
Roughness
Crack density
Hydrophobicity (WDPT)
Subsurface fines
Dry
Wet
(mm)
(g cm− 2)
(mm cm− 1)
(m m− 2)
(s)
(%)
A
10YR6/4
10YR5/4
B
10YR6/4
10YR5/3
C
10YR6/4
10YR4/4
D
10YR6/4 10YR6/3
10YR4/3 10YR3/3
E
10YR6/3
10YR3/3
1.1a (0.3) N = 24 1.5b (0.3) N = 12 2.0c (0.4) N = 12 2.8d (0.3) N = 18 10.3e (1.4) N = 12
175.4a (78.8) N = 24 95.5b (31.2) N = 12 293.7c (85.1) N = 12 438.7d (209.1) N = 14 782.0e (290.4) N = 12
1.81a (1.47) N = 30 1.78a (1.67) N = 24 2.02a (1.41) N = 24 2.59b (1.43) N = 24 3.07b (2.06) N = 24
3.6a (4.0) N = 120 8.8b (7.3) N = 40 13.0c (8.1) N = 56 18.9d (12.5) N = 46 6.7b (7.1) N = 20
Crust type
Color
(Campbell, 1979; Johansen, 1993). The increased presence of Scytonema, Nostoc, Oscillatoria, Chroococcidiopsis, Schizothrix from crust A to E, reflected an increase in mesic conditions, i.e., an increase in water availability. Thus, Nostoc (Booth, 1941) and Scytonema (Garcia-Pichel and Belnap, 1996) were reported to inhabit more mesic crusts in the semi-arid zones of the United States, whereas Schizotrix sp. was found to predominate in the much wetter environments of the Sahel (Malam Issa et al., 1999). Also the increase in green algae with the increase in mesic conditions is in agreement with similar observation made in The Netherlands (de Winder, 1990) and in the northeastern parts of the United States (Johansen 1993). The change in species composition and the increase in nitrogen fixing cyanobacteria such as Nostoc sp. and Scytonema sp. with crust biomass may have important ecological implications. Since microbiotic crusts were shown to fix nitrogen (Mayland and McIntosh, 1966; Belnap et al., 1994), which is available for higher plants (Mayland and McIntosh, 1966), nitrogen fixing cyanobacteria may have an important impact upon the biomass of higher plants. It is especially important for sandy soils, relatively poor in nutrients (Tsoar and Zohar, 1985). The change in species composition is also responsible for a change in crust color and thickness, all of which were apparent in the differential reflectance characteristics of the crusts (Karnieli et al., 1999). Thus, Nostoc and Scytonema, which are confined to the upper crust surface in Nizzana and possess dark pigments to protect them from high radiation (Potts, 1994) were also reported to occupy the upper parts of mesic crusts in the southwestern United States (Campbell, 1979; Garcia-Pichel and Belnap, 1996). With the increase in moisture availability, a gradual increase in the thickness of the
Fig. 7. The relationship between daylight wetness duration and moss stem density of each crust type (N = 60).
Dry
Wet
0.15a (0.27) N = 60 0.32b (0.31) N = 30 0.53bc (0.60) N = 30 1.02d (0.58) N = 40 1.08d (0.56) N = 30
1.1a (0.6) N = 60 1.2a (0.9) N = 30 1.7b (0.6) N = 30 1.5b (0.7) N = 40 0.2c (0.3) N = 30
7.6a (0.9) N = 12 3.7b (0.7) N=6 5.4c (0.4) N=6 5.6c (1.0) N=8 8.0a (1.2) N=6
cyanobacterial crusts was also noted. However, as far as cyanobacteria and algae are concerned, crust thickness is apparently limited by light penetration (Garcia-Pichel and Belnap, 2001). Crust thickness is however drastically increased with a further change in species composition to a moss-dominated crust. According to the current data, longer daylight wetness duration by a factor of up to 2–3 might be responsible for the change in crust composition from predominantly cyanobacterial crusts to a moss-dominated crust. The increase in crust biomass was accompanied by a change in the physical properties of the crust, both of which may have an important impact upon the hydrological behavior of the surface (Kidron et al., 2003) and upon the ecology of higher plants. While the hydrological behavior of the crust may determine water availability to higher plants (Kidron, 1999), crust strength (Valentin and Bresson, 1992), crust roughness (Belnap et al., 2001), and crack density (Prasse and Bornkamm, 2000) may largely affect plant germination. No hydrophobicity was detected either under dry or wet conditions and the crust exhibited similar WDPT values. The slight increase in WDPT from crust A to E under dry conditions may be attributed to the increase in biomass together with surface roughness. The sharp decrease in WDPT in crust E under wet conditions may be attributed to the lower proportion of exopolysaccharides, in comparison to the protein or chlorophyll content, as a result of the shift in population from cyanobacteria, known to excrete copious amounts of exopolysaccharides (Moore and Tischer, 1964; Mazor et al., 1996) to mosses which do not excrete exopolysaccharides (Harper and Marble, 1988). Since exopolysaccharides readily absorb water and thus clog the surface (Kidron et al., 1999), a reduction in exopolysaccharides may increase infiltrability (Kidron et al., 2003). In addition, increased infiltrability can be also a result of the channeling effect of the moss stems and rhizoids. Biomass increase and the change in species composition are believed to be responsible for the increase in the crust thickness that exhibited significant differences between the crust types. It is also believed to be expressed in the crust's compressional strength. Except for crust B (explained by its less stable position at the top of the stabilized dune), an increase in crust strength from crusts A to E took place in Nizzana, in agreement with other findings (Malam Issa et al., 2001). It is also seen responsible for the increase in surface roughness from crusts A to E, and the increase in crack density from crusts A to D. Being attributed to physical factors such as freezing and thawing (Booth, 1941; Williams et al., 1995), desiccation or tension action that result from surface weight (Finlayson et al., 1987) crack density pose an interesting phenomenon. Since temperatures seldom drop below freezing, cracks cannot be seen as resulting from freezing and thawing in Nizzana. Here, they are believed to reflect a bio-physical process as a consequence of high growth rate of the crust microorganisms and subsequent desiccation (Kidron et al., 1999). It is believed that as long
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Fig. 8. Mapping of the Nizzana crust types. Asterisks mark plot location. For crusts A–E see text, M denotes the mobile sections, S the semi-mobile sections, P denotes playa surfaces and Dis denotes disturbed areas. The letter N (upper left corner) denotes the north.
as moisture availability is not sufficient for the proliferation of mosses, but high enough for the proliferation of photoautotrophic cyanobacteria and green algae, extensive growth takes place at the thin upper surface. Growth is thus limited to the upper top surface (1–3 mm thick), subjected to sufficient radiation input for photosynthetic growth. With additional wetness duration, an extensive growth pressure may take place and may result in the curling up of the crust, thus increasing its roughness, but also its cracking density as a result of subsequent desiccation (Shields and Durrell, 1964; Campbell, 1979; Danin et al., 1998). Consequently, while crust strength may impede germination, germination may be facilitated by cracks (Danin, 1978;
Johansen, 1993; Prasse and Bornkamm, 2000). With the massive introduction of mosses in crust E (following more mesic conditions) a sharp decrease in crack density is however taking place. Indeed, the extended daylight wetness duration in the crust E habitat is suggested to promote moss growth, channeling the growth potential at this habitat to deeper subsurface horizons and to upper, above-ground sections. This in turn may change the hydrological behavior of the surface. It may also affect seed entrapment. The change in crust type from cyanobacterial to moss-dominated crust resulted in an increase in surface roughness which hinders runoff yield (Kidron, 2007). It also resulted in a decrease in the ratio
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Table 4 The proportion of the surface area occupied by each type of surface and crust. Surface properties and crust type
Cover (%) Out of the entire study site
Out of the crusted surface
Mobile Semi-mobile Playa Disturbed A B C D E
17.0 15.1 5.5 0.2 48.0 5.5 4.6 2.3 1.8
77.2 8.8 7.3 3.8 2.9
between total carbohydrates to chlorophyll, which in turn indicates lower exopolysaccharides within the crust. Considered crucial for clogging the surface (Mazor et al., 1996; Kidron et al., 1999), the decrease in exopolysaccharides may also explain the substantial decrease in runoff yield monitored at the moss-dominated crust (Kidron et al., 2003). As for the effect upon plant germination, whereas moss protonemata and rhizoids will bind and aggregate the top surface and thus retard cracking, the aerial moss growth on the other hand will increase surface roughness. Since both, crust roughness and cracks may promote seed trapping and germination (Shreve, 1942; Eckert et al., 1986; Prasse and Bornkamm, 2000), crust roughness may compensate for the decrease in crack density, thus facilitating seed trapping and germination. The longer wetness duration at crust E coupled with efficient seed trapping may increase annual cover at this habitat (Tielbörger, 1997). And thus, while the south-facing slope and the interdune may be regarded as the most xeric habitat, the interface between the northfacing slope and the interdune (Fig. 8) may be regarded as the most mesic habitat. With the increase in the organic matter following moss growth (Karnieli et al., 1999), it may result in accelerated soil formation (Amit and Harrison, 1995). The close link between topographical contours and crust types attests to the abiotic role and particularly the surface wetness duration in determining the crust type. Yet, the effect of the crust upon the surface wetness cannot be ignored especially due to the possible effect of the crust's polysaccharides upon water retention (Verrecchia et al., 1995). While these relationships deserve additional research, previous observations showed great similarity between the wetness duration of crusted and non-crusted surfaces at the same slope angle (Kidron et al., 2009), giving extra support to our findings concerning the cardinal role of surface wetness duration in crust establishment and in controlling the crust types. Localized areas of high-biomass crusts may serve as indicators of run-on zones. Zonation of high-biomass crusts may also serve as an indicator for areas receiving subsurface flow (Kidron et al., 2000). The data also imply that whereas aspect-dependent microclimatological conditions provide the adequate growth conditions which ultimately dictate crust type, the crust type in turn may be responsible for characterizing the physical properties of the surface, which affect geomorphological and ecological processes. Acknowledgment The research was supported by grant #00R-009 of the International Arid Land Consortium (IALC), by DISUM and the AERCMINERVA foundation. We would like to thank A. Yair for his support and E. Sachs for valuable field assistant. I. Herrnstadt and M. Temina are highly appreciated for their help in defining the microorganisms. We would like to sincerely thank O.L. Lange, D.H. Yaalon and J.B.J. Harrison for reviewing early versions of the manuscript, I. Einot for statistical advice, C.A. Kidron for the editing and two anonymous reviewers for their most valuable remarks.
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Contents lists available at ScienceDirect
Catena j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c a t e n a
Properties and spatial distribution of microbiotic crusts in the Negev Desert, Israel Giora J. Kidron a,⁎, Ahuva Vonshak b, Inka Dor c, Sophia Barinova d, Aharon Abeliovich e,1 a
Institute of Earth Sciences, The Hebrew University, Givat Ram Campus, Jerusalem 91904, Israel Dept. of Dryland Biotechnologies, The Jacob Blaustein Institute for Desert Research, Ben Gurion University of the Negev, Sede Boqer Campus 84993, Israel c Environmental Sciences Division, The Hebrew University, Givat Ram Campus, Jerusalem 91904, Israel d Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel e Dept. of Biotechnology Engineering, Faculty of Engineering, Institute of Biotechnology, Ben Gurion University of the Negev, Beer Sheva 84105, Israel b
a r t i c l e
i n f o
Article history: Received 24 June 2009 Received in revised form 12 May 2010 Accepted 18 May 2010 Keywords: Biological soil crust Sand dune Moisture Microbiotic crust Cyanobacteria Mosses Negev Desert
a b s t r a c t Playing a cardinal role in surface stabilization and in carbon and nitrogen fixation, microbiotic crusts play a crucial role in arid regions where they may serve as useful biomarkers for wind power and wetness duration. This is especially the case on relatively unstable and infertile sand dunes in the Negev Desert where high correlations between the crust chlorophyll content and the daytime wetness duration were found. Yet, only scarce data are available as to the possible link between the chlorophyll content and other physical (color, thickness, strength, crack density, surface roughness and infiltrability) and biological (protein, carbohydrate, organic matter and species composition) factors, which determine, in turn, the crust type and its effect upon geomorphological and ecological processes. No data are available on crust type distribution. These were the aims of the current research. When a cluster analysis was performed, five types of microbiotic crusts were defined, four of which were cyanobacterial (A–D) and one moss-dominated crust (E). The crusts differed in their physical and biological properties. They showed an increase in chlorophyll content, protein, carbohydrates and organic matter from A to E, with concomitant increase in species diversity, thickness, roughness and strength, but with some variables (crack density and infiltrability) showing a reversed trend at the moss-dominated crust. The increase in the biomass components of the crust and the gradual change of the physical properties are explained by the improved physical conditions (primarily wetness duration), which facilitates longer hours of photosynthetic activity and consequently the introduction of additional, more mesic species such as green algae, lichens and mosses. Extended wetness duration was found to shift the crust type from cyanobacterial to moss-dominated crust. The spatial distribution of the crusts, as verified by crust mapping, coincided with the daylight surface duration, which in turn was controlled by topography (aspect, angle and slope position). It implies that whereas initial physical conditions dictates species composition and thus crust type, the crust type in turn is responsible for characterizing the physical properties of the surface, which may largely affect ecological and geomorphological processes. © 2010 Elsevier B.V. All rights reserved.
1. Introduction As a result of the low cover of higher plants in arid regions, microbiotic crusts often fulfill similar functions such as surface stabilization (van den Ancker et al., 1985; McKenna Neuman et al., 1996) or organic carbon (Lange et al., 1992) and nitrogen (Mayland and McIntosh, 1966; Evans and Lange, 2001) fixation. Additionally, the crusts may significantly alter the hydrological properties of the surface (Booth, 1941; Kidron and Yair, 1997; Belnap, 2006), and affect plant germination and establishment (St. Clair et al., 1984; Prasse and Bornkamm, 2000). All the above functions may be largely dependent upon the crust biomass, its species composition and its physical ⁎ Corresponding author. Tel.: + 972 54 496 7271; fax: + 972 2 566 2581. E-mail address: [email protected] (G.J. Kidron). 1 Deceased. 0341-8162/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.catena.2010.05.006
properties, all of which may show a gradual increase, which may be difficult to sort into distinct categories. Nonetheless, these categories, namely, the definition of distinct crust types, are essential for ecologists and geomorphologist aiming to study abiotic–biotic relationships. In a previous study (Kidron et al., 2009) carried out at the Nizzana research station, at the Hallamish dune field, western Negev Desert (mean annual precipitation of 95 mm), a high correlation was found between crust cover and wind power and between the crusts chlorophyll content and the surface wetness duration. This study was conducted along a 12 point transect (hereafter stations, each having a pair of plots) that extended between two crests of active dunes, crossing a stabilized low dune and two interdunes (Figs. 1 and 2). While stations 1 and 12 were demarcated at the mobile dune crests (and therefore lacked crusts) and stations 2 and 11 were established on the semi-stable midslopes (having therefore a patchy and
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Fig. 1. Location and the experimental layout at the Nizzana research site.
fragmented crust cover), low wind power characterized the remaining stations (stations 3–10) where the crusts appeared homogeneous and where a clear topographically-induced zonation in the chlorophyll content was noted (Fig. 3). At these stations, a high correlation was obtained between the crust chlorophyll content and surface wetness duration (Kidron et al., 2009). Unlike disturbed habitats that are characterized by immature crusts that exhibit different stages of development (Belnap et al., 2008; Kidron et al., 2008), this research was conducted on surfaces or crusts found to be in a quasi equilibrium with the abiotic conditions. While high wind power at the dune crest and the upper dune slopes
was regarded as a negative factor that can cause crust death following its burial, extended wetness duration was seen as a positive factor responsible for the crusts' chlorophyll content, thus facilitating net photosynthetic carbon gain. The chlorophyll content is however only one of the biological properties of the crust. Wetness duration may well affect other crust properties. Furthermore, while a large-range continuum, ranging from several milligrams to almost 100 mg of chlorophyll a per square meter was monitored, any practical evaluation of the crust role will necessitate a relatively clear distinction of the crust types. Knowledge regarding the types of the crust may assist in highlighting the crust
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Fig. 2. Plots at the north facing slope of the stabilized dune. Note the mobile sand at the crest of the high altitude dune at the rare of the photograph (station 12 of transect).
role upon geomorphological and ecological processes, such as its impact upon runoff and infiltration, carbon and nitrogen fixation, plant germination and so forth. Based on the high correlation between daylight wetness duration and the crust chlorophyll content, we hypothesized that wetness duration may also determine other properties. We further hypothesized that a break down into discrete crust types may be possible and
consequently crust mapping. The objectives of the current research were therefore: (1) To classify the crusts into distinct types based on their overall characteristics. (2) To evaluate the pattern, rationale and spatial setting of the crusts.
Fig. 3. Mean chlorophyll content and wetness duration and the crust types A–E along a transect (modified from Kidron et al., 2009).
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2. Methodology The research was confined only to the crusted dune sections along a transect (i.e., stations 3–10) that extended between two crests of active dunes, crossing a stabilized low dune and two interdunes (Figs. 1 and 2 and see also Kidron et al., 2009). Each station consisted of a pair of plots having homogeneously looking crusts (Table 1). In order to characterize the crust properties, physical and biological variables were monitored. The physical variables monitored included color, thickness, compressional strength, crack density, roughness and water infiltrability. The biological variables included chlorophyll a, protein, total carbohydrates, organic matter and species composition. Color was determined in a dry and wet state with a Munsell color chart. Crust thickness was determined with 4–6 crust samples randomly taken from each plot. Following wax coating, crust thickness was measured with a caliper (micrometer) following the method outlined by Blake and Hartge (1986). Pieces of crusts were tied with a thin nylon thread and immersed for approximately 2–3 s into hot wax. After the wax cooled off, the crust thickness (i.e. overall thickness minus wax thickness) was calculated. The wax thickness was determined by a comparison to a wax coated piece of plywood of known thickness. The compressional strength of the crust was determined with 4–6 randomly chosen crusts taken from each plot. The crusts, 2 cm in diameter, were placed over a 1.4 mm opening and subjected to the weight imposed by 1.2 diameter plate (i.e., 1 cm2) attached to the end of a narrow container. Water was carefully filled into the container resulting in increasing pressure of the plate upon the crust. Crust strength was determined as the total weight of the container plus the amount of water responsible for breaking the crust, in accordance with the method proposed by Katznelson (1989). Crack density, determined as the crack length per surface area, was determined in 10–20 randomly chosen 10 × 10 cm squares in each plot. Six to twelve measurements were also carried out in each plot for surface roughness. Surface roughness was determined with 18.8 cmlong microrelief meter having rods spaced at 3.1 mm apart, as Table 1 Plot description. Only the crusted plots 3–10 were monitored during the current research. Plot Plot no.
Surface Interdune Aspectb Topographic Slope Plant Crust area or dune position (°) cover presence (m2) typea (%)
1
2.3 2.3 2.1 2.0 6.6 3.9 2.3 2.3 1.2 1.8 6.6 1.4 6.3 4.1 2.3 3.6 2.3 2.3 3.6 2.5 3.1 2.5 2.3 2.3
2 3 4 5 6 7 8 9 10 11 12 a b
1W 1E 2W 2E 3W 3E 4W 4E 5W 5E 6W 6E 7W 7E 8W 8E 9W 9E 10W 10E 11W 11E 12W 12E
Act Act Act Act Act Act ID
dune dune dune dune dune dune
SF SF SF SF SF SF SF
Top Top Mid Mid Lower Lower Lower
Stab dune NF
Lower
Stab dune NF
Mid
Stab dune NF
Up–Mid
Stab dune NF
Top
ID
SF
Lower
Act dune
NF
Lower
Act dune
NF
Mid
Act dune
NF
Top
5 3 13 17 9 8 2 1 7 10 16 17 13 14 8 10 1 2 11 13 21 23 4 3
Act = active dune; Stab = stabilized dune; ID = interdune. SF = south-facing; NF = north-facing.
0 0 0 0 1 10 2 4 0 0 0 5 1 6 0 2 3 2 2 2 2 1 0 0
None None Partially Partially Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Crusted Partially Partially None None
95
described elsewhere (Kidron, 2007). The variance in rod height (in absolute values) represented roughness (Sanchez and Wood, 1987). Water infiltrability, sometimes referred to as hydrophobicity, was determined via 10–15 measurements taken at each plot. It was determined by measuring the time required for a drop of distilled water placed on the surface to penetrate the crust. According to this method, known as the Water Drop Penetration Time (WDPT), infiltration in excess of 60 s implies high hydrophobicity, 10–60 s implies medium hydrophobicity, while penetration time of less than 10 s indicates a lack of hydrophobicity (Adams et al., 1969). Chlorophyll a (hereafter chlorophyll) concentration was determined in 1.0 cm thick 18–24 cores of 1.2 cm diameter each taken from each plot. Chlorophyll was extracted by hot methanol (70 °C, 20 min) in the presence of MgCO3 (0.1% w/v) in sealed test tubes and assayed according to Wetzel and Westlake (1969). After the extraction of the chlorophyll, half of the samples were used for protein determination according to Lowry et al. (1951), and the other half for carbohydrate determination by the anthrone method (Hassid and Abraham, 1957). The organic matter (OM) was measured in six randomly chosen samples taken from each plot. The OM was determined by comparing the sample weight (approx. 25 g) prior and subsequent to oven ignition at 400 °C for 8 h (Tranter et al., 2007). Cyanobacteria and algae were defined according to Geitler (1932) and Starmach (1966). In certain cases, isolation and growth of the species (in BG11 medium, 1.5% agar) were necessary and consequently carried out. In order to evaluate the relative proportion of each of the identified cyanobacteria and algae species, 4 crusts, approximately 5 cm2 each, were taken from each plot, and the lichens within each sample were defined. The crusts were then immersed in water, thoroughly mixed and the dilution was examined under a light microscope. The number of cells per slide was counted and ranged according to Whitton et al. (1991). Moss stems were counted at 30 randomly chosen crust samples (1.2 cm diameter each) taken from each plot. Moss cover was also visually estimated (in percent). Crust types were determined using cluster analysis based on the various crust properties. The clustering was performed using the means of all the measured parameters. The centroid method was used with Euclidean distance as a measure of dissimilarity (van Tongeren, 1987). The small differences between the sample sizes facilitated the execution of an ANOVA. Because of the high heterogeneity of variance, a t-test was chosen for the comparison of all biomass components (chlorophyll, protein and carbohydrates) and for the total organic matter. Differences were significant at P b 0.05. 3. Results Measurements of each parameter within each plot showed great similarity, in agreement with the high visual homogeneity observed. As a result, we feel that the number of measurements that were carried out for each parameter, adequately represent the plot, despite the micro-scale spatial diversity that one may expect. In fact, biomass parameters exhibited the higher variability and consequently the relatively large number of repetition taken. High variability was nevertheless found between the plots. It included all parameters examined, such as crust thickness, color, compressional strength as well as the crust's biological parameters. These parameters were characterized by a gradual change that did not allow immediate classification. Thus for instance, a gradual thickening of the crust from 1 to 3 mm was noted within the cyanobacterial crusts, and likewise, all biological parameters such as chlorophyll, protein and carbohydrates showed a gradual increase in accordance with crust thickness. A cluster analysis was thus performed in order to better characterize the crust types. It was based on crust color (dry and wet), thickness, compressional strength, crack density, surface roughness, infiltrability (dry and wet), chlorophyll a, protein, total carbohydrate, OM, species composition and moss stem count.
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Five types of crusts were defined and labeled as crusts A, B, C, D and E (Fig. 4). The topographic setting and above all elevation contours played a cardinal role in crust clustering as pointed out by the fact that all plots within the same topographical position along the slope were clustered into the same crust type. Thus, north-facing plots with similar azimuth and slope angles and at similar slope section was clustered together while south-facing plots and interdunal plots were also clustered together. Whereas the difference between crusts B and C was the least pronounced, crust E differed markedly from the remaining crusts. ANOVA test showed significant differences between the crusts with: Chlorophyll: F (4, 459) = 43.2 P b 0.001 Protein: F (4, 446) = 238.7 P b 0.001 Carbohydrates: F (4, 459) = 146.5 P b 0.001 When a t-test was executed, all five crusts defined differed significantly from each other (P b 0.05) in their chlorophyll, protein and carbohydrate, as well as in their total organic matter (Fig. 5). Whereas chlorophyll, protein and carbohydrate content were 17 mg m− 2, 4.2 g m− 2 and 5.3 g m− 2 in crust A, respectively, values as high as 53 mg m− 2, 32.1 g m− 2 and 34.4 g m− 2 characterized the chlorophyll, protein and carbohydrate content of crust E, respectively, with intermediate values characterizing crusts B–D. A total of 7 genera of cyanobacteria were identified, three green algae and two mosses. In addition, several lichen genera were also identified (Table 2). Microcoleus vaginatus was found to be the dominant cyanobacterium. Microculeus sociatus, previously identified as the dominant species in the site (Lange et al., 1992) was not identified during the present research. Another species that was previously defined, Calothrix sp. was also not recorded during the current research. The change in the crust chlorophyll, protein and carbohydrates was accompanied by a change in species composition. Whereas M. vaginatus, Trentepholia sp. and Phormidium sp. were highly dominant in crust type A, higher abundance of species characterized crusts B–E with larger proportions of other species of cyanobacteria including Scytonema sp., Nostoc microscopicum, Oscillatoria sp., and Schizothrix friesii. Crusts B–E also had a larger proportion of green algae. One filamentous genus, Microspora sp. and two coccoid genera Clorococcum
Fig. 5. Mean values of Chlorophyll a, carbohydrates, protein, and organic matter of crust types. Bars represent one SD. All values within each variable differed significantly from each other (P b 0.05).
Fig. 4. Cluster analysis of crusts within the research site.
G.J. Kidron et al. / Catena 82 (2010) 92–101 Table 2 Species composition of mosses (number of moss stems and visual estimation of cover in parenthesis) and of cyanobacteria, algae and lichens of each crust type as determined after Whitton et al., 1991 (1 — Occasional with 1–5 cells per slide; 2 — rare with 5–15 cells; 3 — Common with 15–25 cells; 4 — Frequent with several cells over a slide transect; 5 — Abundant with cells in each field of view). Species composition
A
B
C
D
E
Microcoleus vaginatus Trentepohlia sp. Phormidium sp. Nostoc microscopicum Scytonema sp. Oscillatoria sp. Schizothrix friesii Green algae (Microspora sp., Chlorococcum sp., Stichococcus sp.) Lichens (Aspicilia sp. Fulgensia fulgens, Caloplaca holocarpa, C. tominii, Collema tenax) Mosses (Bryum dunense, Tortula brevissima)
5 4 3 1 1 1 1 1
5 4 2 1 2 1 1 1
4 5 2 2 3 2 2 1
4 2 1 3 4 3 3 2
3 – 1 3 3 3 3 3
1
1
1
2
1
5.5 × 102 (b0.1%)
8.3 × 102 (0.1%)
3.3 × 103 (1%)
4.7 × 104 (10%)
7.8 × 105 (80%)
sp. and Stichococcus sp. were defined. Two moss species, Bryum dunense and Tortula brevissima were also defined. Several species of lichens were also identified including Fulgensia fulgens, Caloplaca holocarpa, C. tominii and Collema tenax. The change in the biomass components and species composition was reflected in the crust physical and biological properties. Thus, the crust tends to become darker with the increase in chlorophyll, protein and carbohydrates and the change in species composition reflecting higher proportions of dark pigmented cyanobacteria such as Scytonema sp. and Nostoc sp. (Fig. 6). The increase in chlorophyll, protein and carbohydrates was accompanied also by an increase in crust thickness and OM. Crust thickness increased from 1.1 mm in crust A to 10.3 mm in crust E while the OM increased from 0.46% in crust A to 2.59% in crust E (Fig. 5). Likewise, crust roughness increased from crusts A and B (1.8 mm cm− 1) to E (3.1 mm cm− 1), whereas crack density increased from crust A (3.6 m m− 2) to D (18.9 m m− 2), but sharply decreased in crust E (6.7 m m− 2). Excluding crust B, The crust' compressional strength also showed an overall increase from crust A
97
(175.4 g cm− 2) to E (782.0 g cm− 2). As for water infiltrability, a gradual decrease was measured from crusts A (0.2 s) to E (1.1 s) under dry conditions. However, a sharp increase in water infiltrability was noted in crust E under wet conditions, from 1.1– 1.7 s in crusts A–D to 0.2 s in crust E (Table 3). Overall, these changes were relatively small on the hydrophobicity scale and below the threshold defined to indicate hydrophobicity. When the surface wetness duration was included in the cluster analysis, no change was detected in the clustering pattern (not shown), attesting to the close link between wetness duration and crust type (Fig. 3 and Kidron et al., 2009). A close link was also obtained between daylight wetness duration and the moss stem counts (Fig. 7). Consequently, daylight wetness duration may be regarded as the causal factor determining crust type and the change from cyanobacterial to moss-dominated crust. The link between daylight wetness duration and topography (aspect, angle and slope position) on the one hand and between daylight wetness duration and the crust chlorophyll content and hence crust type on the other hand facilitated crust mapping (Fig. 8). While crusts were absent from ∼ 40% of the area (mobile and semimobile dune sections and fine-grained playa surfaces), the remaining dunes and interdunes were inhabited by 5 types of microbiotic crusts. Out of the crusts, crust A was dominant (∼ 77% of the crusted surfaces), occupying the south-facing slopes and the interdunes, while crust D and E occupied each the lowest percentage of the surface (∼3–4% each), with crusts B and C occupying each ∼ 7–9% of the surface area (Table 4). 4. Discussion Cluster analysis showed 5 distinct crust types. All crusts showed high zonation in accordance with daylight wetness duration, which in turn may reflect photosynthetic activity. By controlling the crust type, wetness duration is responsible for a change in species composition, and the biological and physical properties of the crusts. The change in species composition, in accordance with moisture availability, is in agreement with other arid zones, in which crusts were mainly categorized into two types, xeric and mesic (Belnap, 2001). Thus, Microcoleus sp. that was found in Nizzana to predominate in the most xeric crust type was also found to predominate in the more xeric arid and semi-arid crusts of the North American deserts
Fig. 6. Dry (top) and wet (bottom) crust samples of the different crust types. Note that the moss yellow color (crust E) during summertime turns green during wintertime.
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Table 3 The physical properties and the amount of subsurface fines in all crust types. Number in parenthesis indicates one SD while N indicates the sample number. Different letters indicate significant differences (P b 0.05). Thickness
Crust strength
Roughness
Crack density
Hydrophobicity (WDPT)
Subsurface fines
Dry
Wet
(mm)
(g cm− 2)
(mm cm− 1)
(m m− 2)
(s)
(%)
A
10YR6/4
10YR5/4
B
10YR6/4
10YR5/3
C
10YR6/4
10YR4/4
D
10YR6/4 10YR6/3
10YR4/3 10YR3/3
E
10YR6/3
10YR3/3
1.1a (0.3) N = 24 1.5b (0.3) N = 12 2.0c (0.4) N = 12 2.8d (0.3) N = 18 10.3e (1.4) N = 12
175.4a (78.8) N = 24 95.5b (31.2) N = 12 293.7c (85.1) N = 12 438.7d (209.1) N = 14 782.0e (290.4) N = 12
1.81a (1.47) N = 30 1.78a (1.67) N = 24 2.02a (1.41) N = 24 2.59b (1.43) N = 24 3.07b (2.06) N = 24
3.6a (4.0) N = 120 8.8b (7.3) N = 40 13.0c (8.1) N = 56 18.9d (12.5) N = 46 6.7b (7.1) N = 20
Crust type
Color
(Campbell, 1979; Johansen, 1993). The increased presence of Scytonema, Nostoc, Oscillatoria, Chroococcidiopsis, Schizothrix from crust A to E, reflected an increase in mesic conditions, i.e., an increase in water availability. Thus, Nostoc (Booth, 1941) and Scytonema (Garcia-Pichel and Belnap, 1996) were reported to inhabit more mesic crusts in the semi-arid zones of the United States, whereas Schizotrix sp. was found to predominate in the much wetter environments of the Sahel (Malam Issa et al., 1999). Also the increase in green algae with the increase in mesic conditions is in agreement with similar observation made in The Netherlands (de Winder, 1990) and in the northeastern parts of the United States (Johansen 1993). The change in species composition and the increase in nitrogen fixing cyanobacteria such as Nostoc sp. and Scytonema sp. with crust biomass may have important ecological implications. Since microbiotic crusts were shown to fix nitrogen (Mayland and McIntosh, 1966; Belnap et al., 1994), which is available for higher plants (Mayland and McIntosh, 1966), nitrogen fixing cyanobacteria may have an important impact upon the biomass of higher plants. It is especially important for sandy soils, relatively poor in nutrients (Tsoar and Zohar, 1985). The change in species composition is also responsible for a change in crust color and thickness, all of which were apparent in the differential reflectance characteristics of the crusts (Karnieli et al., 1999). Thus, Nostoc and Scytonema, which are confined to the upper crust surface in Nizzana and possess dark pigments to protect them from high radiation (Potts, 1994) were also reported to occupy the upper parts of mesic crusts in the southwestern United States (Campbell, 1979; Garcia-Pichel and Belnap, 1996). With the increase in moisture availability, a gradual increase in the thickness of the
Fig. 7. The relationship between daylight wetness duration and moss stem density of each crust type (N = 60).
Dry
Wet
0.15a (0.27) N = 60 0.32b (0.31) N = 30 0.53bc (0.60) N = 30 1.02d (0.58) N = 40 1.08d (0.56) N = 30
1.1a (0.6) N = 60 1.2a (0.9) N = 30 1.7b (0.6) N = 30 1.5b (0.7) N = 40 0.2c (0.3) N = 30
7.6a (0.9) N = 12 3.7b (0.7) N=6 5.4c (0.4) N=6 5.6c (1.0) N=8 8.0a (1.2) N=6
cyanobacterial crusts was also noted. However, as far as cyanobacteria and algae are concerned, crust thickness is apparently limited by light penetration (Garcia-Pichel and Belnap, 2001). Crust thickness is however drastically increased with a further change in species composition to a moss-dominated crust. According to the current data, longer daylight wetness duration by a factor of up to 2–3 might be responsible for the change in crust composition from predominantly cyanobacterial crusts to a moss-dominated crust. The increase in crust biomass was accompanied by a change in the physical properties of the crust, both of which may have an important impact upon the hydrological behavior of the surface (Kidron et al., 2003) and upon the ecology of higher plants. While the hydrological behavior of the crust may determine water availability to higher plants (Kidron, 1999), crust strength (Valentin and Bresson, 1992), crust roughness (Belnap et al., 2001), and crack density (Prasse and Bornkamm, 2000) may largely affect plant germination. No hydrophobicity was detected either under dry or wet conditions and the crust exhibited similar WDPT values. The slight increase in WDPT from crust A to E under dry conditions may be attributed to the increase in biomass together with surface roughness. The sharp decrease in WDPT in crust E under wet conditions may be attributed to the lower proportion of exopolysaccharides, in comparison to the protein or chlorophyll content, as a result of the shift in population from cyanobacteria, known to excrete copious amounts of exopolysaccharides (Moore and Tischer, 1964; Mazor et al., 1996) to mosses which do not excrete exopolysaccharides (Harper and Marble, 1988). Since exopolysaccharides readily absorb water and thus clog the surface (Kidron et al., 1999), a reduction in exopolysaccharides may increase infiltrability (Kidron et al., 2003). In addition, increased infiltrability can be also a result of the channeling effect of the moss stems and rhizoids. Biomass increase and the change in species composition are believed to be responsible for the increase in the crust thickness that exhibited significant differences between the crust types. It is also believed to be expressed in the crust's compressional strength. Except for crust B (explained by its less stable position at the top of the stabilized dune), an increase in crust strength from crusts A to E took place in Nizzana, in agreement with other findings (Malam Issa et al., 2001). It is also seen responsible for the increase in surface roughness from crusts A to E, and the increase in crack density from crusts A to D. Being attributed to physical factors such as freezing and thawing (Booth, 1941; Williams et al., 1995), desiccation or tension action that result from surface weight (Finlayson et al., 1987) crack density pose an interesting phenomenon. Since temperatures seldom drop below freezing, cracks cannot be seen as resulting from freezing and thawing in Nizzana. Here, they are believed to reflect a bio-physical process as a consequence of high growth rate of the crust microorganisms and subsequent desiccation (Kidron et al., 1999). It is believed that as long
G.J. Kidron et al. / Catena 82 (2010) 92–101
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Fig. 8. Mapping of the Nizzana crust types. Asterisks mark plot location. For crusts A–E see text, M denotes the mobile sections, S the semi-mobile sections, P denotes playa surfaces and Dis denotes disturbed areas. The letter N (upper left corner) denotes the north.
as moisture availability is not sufficient for the proliferation of mosses, but high enough for the proliferation of photoautotrophic cyanobacteria and green algae, extensive growth takes place at the thin upper surface. Growth is thus limited to the upper top surface (1–3 mm thick), subjected to sufficient radiation input for photosynthetic growth. With additional wetness duration, an extensive growth pressure may take place and may result in the curling up of the crust, thus increasing its roughness, but also its cracking density as a result of subsequent desiccation (Shields and Durrell, 1964; Campbell, 1979; Danin et al., 1998). Consequently, while crust strength may impede germination, germination may be facilitated by cracks (Danin, 1978;
Johansen, 1993; Prasse and Bornkamm, 2000). With the massive introduction of mosses in crust E (following more mesic conditions) a sharp decrease in crack density is however taking place. Indeed, the extended daylight wetness duration in the crust E habitat is suggested to promote moss growth, channeling the growth potential at this habitat to deeper subsurface horizons and to upper, above-ground sections. This in turn may change the hydrological behavior of the surface. It may also affect seed entrapment. The change in crust type from cyanobacterial to moss-dominated crust resulted in an increase in surface roughness which hinders runoff yield (Kidron, 2007). It also resulted in a decrease in the ratio
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Table 4 The proportion of the surface area occupied by each type of surface and crust. Surface properties and crust type
Cover (%) Out of the entire study site
Out of the crusted surface
Mobile Semi-mobile Playa Disturbed A B C D E
17.0 15.1 5.5 0.2 48.0 5.5 4.6 2.3 1.8
77.2 8.8 7.3 3.8 2.9
between total carbohydrates to chlorophyll, which in turn indicates lower exopolysaccharides within the crust. Considered crucial for clogging the surface (Mazor et al., 1996; Kidron et al., 1999), the decrease in exopolysaccharides may also explain the substantial decrease in runoff yield monitored at the moss-dominated crust (Kidron et al., 2003). As for the effect upon plant germination, whereas moss protonemata and rhizoids will bind and aggregate the top surface and thus retard cracking, the aerial moss growth on the other hand will increase surface roughness. Since both, crust roughness and cracks may promote seed trapping and germination (Shreve, 1942; Eckert et al., 1986; Prasse and Bornkamm, 2000), crust roughness may compensate for the decrease in crack density, thus facilitating seed trapping and germination. The longer wetness duration at crust E coupled with efficient seed trapping may increase annual cover at this habitat (Tielbörger, 1997). And thus, while the south-facing slope and the interdune may be regarded as the most xeric habitat, the interface between the northfacing slope and the interdune (Fig. 8) may be regarded as the most mesic habitat. With the increase in the organic matter following moss growth (Karnieli et al., 1999), it may result in accelerated soil formation (Amit and Harrison, 1995). The close link between topographical contours and crust types attests to the abiotic role and particularly the surface wetness duration in determining the crust type. Yet, the effect of the crust upon the surface wetness cannot be ignored especially due to the possible effect of the crust's polysaccharides upon water retention (Verrecchia et al., 1995). While these relationships deserve additional research, previous observations showed great similarity between the wetness duration of crusted and non-crusted surfaces at the same slope angle (Kidron et al., 2009), giving extra support to our findings concerning the cardinal role of surface wetness duration in crust establishment and in controlling the crust types. Localized areas of high-biomass crusts may serve as indicators of run-on zones. Zonation of high-biomass crusts may also serve as an indicator for areas receiving subsurface flow (Kidron et al., 2000). The data also imply that whereas aspect-dependent microclimatological conditions provide the adequate growth conditions which ultimately dictate crust type, the crust type in turn may be responsible for characterizing the physical properties of the surface, which affect geomorphological and ecological processes. Acknowledgment The research was supported by grant #00R-009 of the International Arid Land Consortium (IALC), by DISUM and the AERCMINERVA foundation. We would like to thank A. Yair for his support and E. Sachs for valuable field assistant. I. Herrnstadt and M. Temina are highly appreciated for their help in defining the microorganisms. We would like to sincerely thank O.L. Lange, D.H. Yaalon and J.B.J. Harrison for reviewing early versions of the manuscript, I. Einot for statistical advice, C.A. Kidron for the editing and two anonymous reviewers for their most valuable remarks.
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