- Email: [email protected]
The effects of heavy winter rains and rare summer rains on biological soil crusts in the Negev Desert
Catena 95 (2012) 6–11
Contents lists available at SciVerse ScienceDirect
Catena journal homepage: www.elsevier.com/locate/catena
The effects of heavy winter rains and rare summer rains on biological soil crusts in the Negev Desert Giora J. Kidron a,⁎, Sophia Barinova b, Ahuva Vonshak c a b c
Institute of Earth Sciences, The Hebrew University, Givat Ram Campus, Jerusalem 91904, Israel Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel Dept. of Dryland Biotechnologies, The Jacob Blaustein Institute for Desert Research, Ben Gurion University of the Negev, Sede Boqer Campus 84993, Israel
a r t i c l e
i n f o
Article history: Received 17 June 2011 Received in revised form 17 February 2012 Accepted 21 February 2012 Keywords: Microbiotic crust Biocrust Chlorophyll Carbohydrates Species composition Sand dune
a b s t r a c t Biological soil crusts (BSCs) abound in the Hallamish dune field in the western Negev Desert, Israel. While their abundance may imply high adaptability to environmental change, such as fluctuations between wet and dry conditions following winter rains, summer rains, although rare, may also occur in the Hallamish dune field. The aim of the present paper is to examine crust responses to winter and summer rains, focusing particularly on its biomass components, chlorophyll and carbohydrate. In addition, species composition, during summer and winter was examined. Analysis took place during an exceptionally wet winter (1994/95 with 172 mm) and a summer rainstorm (12.5.93 with 9.7 mm). The data showed a 2–3 fold increase in chlorophyll a and total carbohydrates and a much richer species composition following the heavy winter rains of 1994/ 95. Yet, the data also showed ~ 15–30% decrease in the chlorophyll content of the crust (with no concomitant significant decrease in total carbohydrates) following the summer rainstorm. Intense weathering by the summer rain coupled with cell mortality may explain the decrease in the chlorophyll content following the summer rainstorm, suggesting possible changes in the BSC following a potential change in the precipitation regime due to global climate change. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Biological soil crusts (BSCs) cover vast areas within arid and semi arid zones where they may often exceed the cover of higher plants (Büdel, 2001). Playing an important role in surface stability (McKenna Neuman et al., 1996), the hydrological properties of the surface (Kidron and Yair, 1997), CO2 sequestration (Metting et al., 2001), nitrogen fixation (Evans and Lange, 2001; Mayland and McIntosh, 1966) and seedling germination (Prasse and Bornkamm, 2000), any change in their cover or biomass may impact the entire ecosystem. Crust cover and biomass may be highly affected by surface stability and wetness duration (Kidron et al., 2009), both of which may be greatly impacted by the climatological conditions. A change in the temperature regime may extensively affect wetness duration, which in turn may alter species composition (Kappen et al., 1980; Kidron et al., 2010). Knowledge regarding the effect of climatological conditions upon crust properties is therefore of special importance. BSCs, whether cyanobacterial or moss-dominated crusts, abound in the Hallamish dune field in the western Negev Desert, Israel, where they cover all sandy interdunes and bottom dunes, absent
⁎ Corresponding author. Tel.: + 972 2 676 7271; fax: + 972 2 566 2581. E-mail address: [email protected] (G.J. Kidron). 0341-8162/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.catena.2012.02.021
only from the mobile dune summits, where wind velocity is too high to allow for crust establishment. Their abundance is rather surprising in this extreme desert. At the Hallamish dune field, long-term annual precipitation is only 95 mm, falling mainly during November to March. Occasionally, the area may also receive summer storms. Crust appearance differs substantially during winter and summer. During most of the dry period, a brownish color characterizes the cyanobacterial crusts and the dry mosses. A dark green color, characterizes cyanobacterial crusts when wet, while a bright green color characterizes mosses during its growth period in the winter. The dark green color of the cyanobacterial crusts may attest to an apparent substantial increase in their chlorophyll content and to the greening effect, sensu Brock (1975), during which the filamentous cyanobacteria tend to migrate to the surface (Fig. 1a). Since cyanobacteria motility was principally explained by filament gliding that takes place along with EPS excretion (Campbell, 1979), it may explain the close link between chlorophyll and the carbohydrate-constituted exopolysaccharides, EPS (Kidron et al., 2010). While the greening effect may be visible in the winter, no greening effect was noted in summer, raising the hypothesis that the crust response to wetting may be season-dependent. As such, it was hypothesized that the chlorophyll content of the crust may be variably affected by occasional, rather rare, summer rains, defined herein as rains falling during the hot months of May–August. Furthermore, since EPS excretion is triggered by motility (Campbell, 1979), the
G.J. Kidron et al. / Catena 95 (2012) 6–11
a
b
Fig. 1. The greening effect (manifested by the darker patches) at a cyanobacterial crust as photographed during November 20, 1994 (a), and the five crust types defined in Nizzana (b).
total carbohydrate content of the crust (which mainly constitute the EPS; see Ernst et al., 1987; Mazor et al., 1996) may also be affected. In an attempt to monitor rain-induced fluctuation, chlorophyll, carbohydrates and species composition of the BSCs were monitored. Monitoring included cyanobacteria, green algae and diatoms. They also included the lichen and moss cover. During the current research monitoring focused on the exceptionally wet winter of 1994/95, and on a rare summer rainstorm that took place in the summer of 1993.
2. Material and methods The research took place at the Nizzana research station of the Hallamish dune field in the western Negev Desert, Israel (34°23′E, 30°56′N). West–east longitudinal dunes, 15–20 m high, separated by 50–200 m wide interdunes characterize the dune field. Mean long-term precipitation is 95 mm, falling during the winter, mainly during November-March (Rosenan and Gilad, 1985). Five types of crusts, crusts A-E, were defined in the Hallamish dune field, four cyanobacteria-dominated (crusts A–D, 1–3 mm thick, with Microcoleus sp. predominating, Lange et al., 1992) and one (crust E, 10 mm thick), moss-dominated (Table 1; Fig. 1b). The crusts differed in a variety of physical and biological parameters, with their chlorophyll content and total carbohydrates exhibiting significant differences (Kidron et al., 2010). Whereas crust A extends over the interdunes and the south-facing footslopes, occupying the most xeric habitat of the dune field, crusts B–E extend over the north-facing slope. On a stabilized dune, crust B extends over the upper slope, being followed by crusts C (between the upper and mid slope), D at the mid slope
7
Table 1 Crust characteristics (One standard deviation in parenthesis). Crust Type
Aspect Location
Crust Thickness Chloro-phyll Carbo-hydrates (mm) (N = 12) mg m− 2 (g/ m− 2) (N = 103) (N = 206)
A
SF
Footslope
B
NF
Upper Slope
C
NF
D
NF
Upper-Mid Slope Mid Slope
E
NF
Footslope
1.1 (0.3) 1.5 (0.3) 2.0 (0.4) 2.8 (0.3) 10.3 (1.4)
16.7 (9.9) 20.7 (10.5) 28.5 (16.7) 43.4 (27.6) 53.2 (25.8)
5.28 (2.27) 7.65 (3.28) 9.15 (4.34) 15.92 (5.97) 33.16 (14.71)
and E which occupies the interface between the bottom of the northfacing dune and the interdune. Two plots, ~ 2 × 2 m, were demarcated on each of the five crust types, A–E. Following a rare rainstorm that fell during the summer of 1993 (12.5.93) and an exceptionally heavy rain event of 56.2 mm that fell during November 2nd and 6th, 1994 (followed by additional high-depth rainstorms), crust samples were collected for chlorophyll a and total carbohydrate measurements. While two sampling periods were executed during the 12.5.93 summer rain (prior and following the rain event), measurements during 1994/95 took place in 1–4 week intervals. Measurements for the crust biomass were executed on 12 crust cores, 1 cm2 and 1 cm thick. While taken weekly from each plot during the rainy period, they were taken in 2–4 week intervals during dry spells. Chlorophyll a (hereafter 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). Following chlorophyll extraction, total carbohydrates (hereafter termed carbohydrates) were determined using the anthrone method (Hassid and Abraham, 1957). In addition, the relative cover of the lichens and mosses was visually estimated in 1–2 mo intervals during the winter of 1994/95. Monitoring took place in ten 10 × 10 cm squares, 20 cm apart, that were marked along two 1 m-long transects that stretched ~ 20 cm from each side of each plot. Monitoring included mature lichens with fruiting bodies, as well as lichenized surfaces which did not yet have fruiting bodies. During winter (December 1994) and summer (July 1995) of the hydrological year of 1994/95, crusts were also sampled for the analysis of species composition. The December sampling was executed one week after the 33 mm rain event of 2–6.12.94, during which most crusts were wet, while the July sampling took place ~2 months following the last rain event, thus representing dry surface conditions. The 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. For the evaluation of the relative proportion of each of the identified cyanobacteria and algal species, four crusts, approximately 5 cm 2 each, were taken from each plot at each crust type. The crusts were crushed, immersed in water and homogenized, and the dilution was examined under a light microscope. The cyanobacteria, green algae and diatoms were identified, and the relative abundance of cells per species of each slide was assessed. The relative abundance of cells for each crust type was presented in a 6-score scale, in accordance with Korde (1956).
3. Results and discussion The winter of 1992/93 was slightly drier than the long-term mean with a total of 85.3 mm. Conversely, winter of 1994/95 was exceptionally
8
G.J. Kidron et al. / Catena 95 (2012) 6–11
wet, with three rainstorms having ≥30 mm. Rain precipitation amounted to 172.0, almost twice as high as the 95 mm mean (Fig. 2). As a result of the wet winter, extended wetness duration characterized all habitats during the winter of 1994/95. Cyanobacteria migration to the surface, i.e., the greening effect, was common. Moss growth was noted at newly-scalped surfaces (Kidron et al., 2008). Furthermore, moss establishment and growth took place also at the south-facing slope, in areas which did not have moss growth before, as noted as early as on December 10th. Moreover, extensive lichenization took place at all habitats, being especially pronounced at crust D and C. It was expressed by sterile coin and ring shaped lichen forms, several centimeters up to 15 cm in diameter (Fig. 3a, b). Contrarily, surface wetness was relatively short following the 12.5.93 rainstorm event. Yet, this event resulted in substantial surface erosion, reflected in a dome-shaped microrelief that characterized many of the surfaces and was explained by the sever impact that the rain drops had on the dry surface (Fig. 3c). As expected, high fluctuation characterizes the chlorophyll and carbohydrate content, with winter values of each crust type being significantly higher than the summer values (Fig. 4). This can be clearly seen for the most xeric (crust A) and mesic (crust D) cyanobacterial crusts, and for the moss-dominated crust (crust E). Chlorophyll content varied between 14.6, 35.7 and 53.8 mg m− 2 in the summer to 42.1, 100.4 and 134.3 mg m − 2 in the winter for crust A, D, and E, respectively. Similarly, carbohydrate content varied between 4.4, 13.3 and 27.7 g m − 2 in the summer to 11.1, 35.6 and 80.0 g m − 2 in the winter for crusts A, D and E, respectively. Both biomass components increased two to three fold following the winter rain events compared to summer values. The lichenized surface cover and the moss cover showed a similar trend, with up to 2–3 fold increase (Fig. 5). Yet, unlike the drop in the chlorophyll and carbohydrate content, the values remained more or less constant. One should however note, that field observations that took place three years later failed to detect mosses at the southfacing slope, pointing to the fact that the long-term conditions at this habitat were apparently not suited for long-term moss establishment. Also, many of the lichenized surfaces were not noted three years later indicating that licenization did not necessarily lead to the formation of lichens. Except for the moss-dominated crust, chlorophyll content increased relatively rapidly following the rain event, attesting to the rapid growth rate of the cyanobacteria, and to a slower growth rate of the moss. During many of the cloudy winter days, the greening effect was noted with Microcoleus sheaths being observed at the surface by the naked eye (Fig. 1b). A close link between chlorophyll and
a
b
c
Fig. 3. Lichenized surfaces (a) and a close-up of 12.5 cm-diameter ring-shaped lichenized surface (b) as photographed on the north-facing slope during December 17th, and high surface erosion which results in a dome-shaped microtopography (c) at the north-facing slope following the 12.5.93 rainstorm event.
Fig. 2. Rain distribution during 1992/93 and 1994/95.
carbohydrates was observed. It was also observed at the mossdominated crust, crust E. Yet, unlike the case with the cyanobacteria in which ≤70% of their dry weight are carbohydrate-constituted exopolysaccharides (Flaibani et al., 1989), the carbohydrates at crust E may primarily reflect the inner above- and below-surface (mainly the rhizoids) content of the moss cells. Following crust desiccation, during which crust microorganism enter an anhydrobiotic state (Potts, 1994), a decrease in the chlorophyll and carbohydrate content was noted. Yet, contrary to the rapid response of the chlorophyll content to surface wetting and desiccation (Fig. 4a), the change in the total carbohydrates was somewhat slower (Fig. 4b). Both responses, that of the chlorophyll and especially that of the carbohydrates, were substantially slower at the moss-dominated
G.J. Kidron et al. / Catena 95 (2012) 6–11
9
Table 2 Species composition of cyanobacteria, green algae and diatoms as determined during the winter (W) of 1994/95 and summer (S) of 1995 following Korde, 1956 (1 — Occassional 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 — Several cells over a slide transect, 6 — Abundant with few cells in each field of view). Species Composition
Fig. 4. Chlorophyll (a) and carbohydrate (b) fluctuation of crusts A-E during 1994/95. Bars represent one SE. Arrows at the abscissa indicate rain events with >10 mm.
crust, explained by the different physiological response of the moss, and its gradual growth during winter until reaching mature spores. It is also explained by the much longer wetness duration that characterized the surface of the crust E habitat (Kidron et al., 2000) and the ability of the moss to withdraw water from a deeper layer of ~10 mm (by using its rhizoids) compared to 1–3 mm layer utilized by the cyanobacteria. The change in crust biomass was also accompanied by a change in the microorganism species composition. High species diversity was noted during mid winter, at the time when the crust biomass was at its greatest (Table 2). The high diversity may attest to the relatively good edaphic and environmental conditions that prevail during
Fig. 5. Lichenized surface cover (a) and moss cover (b) during 1994/95. Bars represent one SE.
Cyanobacteria Microcoleus vaginatus (Vaucher) Gomont ex Gomont Microcoleus vaginatus var monticola (Kützing) Gomont Synechococcus sciophilus Skuja Chroococcus turgidus (Kützing) Nägeli Chroococcus sp. Phormidium sp. Nostoc microscopicum Carmichael ex Bornet & Flahault Nostoc sp. Scytonema sp. Oscillatoria sp. Schizothrix friesii (Gomont ex Gomont) Kirchner Chroococcidiopsis sp. Green algae Trentepohlia sp. Microspora sp., Stichococcus sp. Chlorococcum sp. Diatoms Luticola mutica (Kützing) D.G.Mann Luticola nivalis (Ehrenberg) D.G.Mann Nitzcshia sp. Naviculaceae
A
B
C
D
E
W
S
W
S
W
S
W
S
W
S
4
6
3
5
2
4
2
4
2
3
3 1
3 1
2 1
2 1
2 2
2 2
1 1 3
1 3
1 3
1 3
2 1 1 1
1 1 1
2 2 1 1
2 1 1
1 3 2 2
3 2 2
2 4 3 3
4 3 3
1 3 3 3
3 3 3
4 3 2
1 4 1 1
1 4 1
4 1 1
3 2 1 1
1 4 1
5 1 1
1 1
1 5 1
2 2 2 1
1 2 2
3 3 3
3
1 1 1 1
winter, during which, suitable conditions exist for the establishment of a wide variety of microorganisms. Nevertheless, the sharp drop in species diversity monitored during summer (Table 2) may attest to a limited adaptability of many species to the harsh conditions or the lengthy duration during which the crust remains dry during summer. This, in turn, resulted in the low abundance of some species. While 12 species of cyanobacteria and four species of diatoms were defined during winter, no diatoms and only six species of cyanobacteria were defined during summer. Apparently, only species that do not experience high mortality and their abundance does not drop substantially throughout summer may be regarded as species that are well adapted to the harsh conditions of the arid dune field. As for the lichens, only lichens with fruiting bodies could have been identified. The lichens identified within the research site were Fulgensia fulgens (Sw.) Elenkin, Caloplaca sp. and Collema sp. As for the mosses, two species were identified on the dune sand: Bryum dunense A.J.E. Smith & H. Whitehouse and Tortula brevissima Schiffner. Chlorophyll content following the 12.5.93 summer rain resulted in a substantial drop of ~ 15-30% of some cyanobacterial crusts (significant at P b 0.05 once a t-test was performed for crust C and at P b 0.1 for crust A). This was not the case with the moss-dominated crust, crust E (Fig. 6a). As for the carbohydrate content, although being lower, the summer rain did not significantly affect the carbohydrate content of crusts (Fig. 6b). The sharp drop in the chlorophyll content following the summer rain event is not yet fully understood. Although rather rare with four summer rainstorms that occurred during the last 20 (1991–2010) years (i.e, a summer rainstorm every 5 years), their implications upon the ecosystem may be high. While intense erosion caused by the rain drop impact on the dry crust, which is especially prone to erosion (and reflected in the rugged, dome-like microrelief, see also Kidron, 2001), may partially explain the phenomenon, high mortality, due to cell burst coupled with the high surface temperatures may provide additional explanation.
10
G.J. Kidron et al. / Catena 95 (2012) 6–11
Fig. 6. Chlorophyll (a) and carbohydrates (b) prior and following a summer rain event of May 12, 1993. Asterisks indicate significant differences within a pair at P b 0.05 (*) or P b 0.1 (**).
High cell mortality of microorganisms was noted following sudden soil wetting and explained by the incapability of the cells to adapt to the dramatic change in the osmotic pressure of the cell (Kieft et al., 1987). This threat may be alleviated by exopolysaccharide secretion, mainly by the formation of thick sheaths (Borken and Matzner, 2009), such as the sheaths that characterize the dominant species in Nizzana, Microcoleus vaginatus. Yet, the high cell mortality that we noted following the 12.5.93 rainstorm cannot be solely attributed to the same phenomenon. Thus, crust sampling following winter rains (such as the 2–6.11.94 rainstorm) did not monitor a substantial drop in the chlorophyll content. Although cell death apparently took place, it was not massive enough to be easily detected by the current method used for chlorophyll measurements. We therefore postulate that the significant drop in the chlorophyll content may be also explained by the high UV radiation during the summer (GarciaPichel and Castenholz, 1993) and by the surface temperatures which characterize the summer surfaces, which may exceed 50 °C. While rainwater and subsequent evaporation acted to cool the surface, surface temperatures may still be > 30 °C, i.e., within a temperature range that may limit cyanobacteria growth. Indeed, while exhibiting substantial endurance to high temperature when dry, cyanobacteria and green algae have low endurance to high temperatures when wet (Gao, 1998). In fact, cyanobacteria isolates from Nizzana died when incubated at ≥ 37 °C, while exhibiting very low growth rates already at ≥ 32 °C (Mazor et al., 1996). Yet, while some of the species, such as Microcoleus and Phormidium, may escape the harmful effect of the high temperatures due to their motility, other species, which do not posses motility, such as Nostoc and Scytonema, may not. Alternatively, high mortality may also stem from UV radiation against which the pigmented species Nostoc and Scytonema are well protected. This will result in high mortality of the less-pigmented species such as Microcoleus vaginatus as reported by Bowker et al. (2002). Yet, as far as the rain drop impact is concerned, the upper-surface dwellers Nostoc and Scytonema, which mostly prevail in the more mesic north-facing slope, may be much more susceptible to weathering and erosion. While more detailed examinations are needed in order to identify the most vulnerable species, the current findings nevertheless point to the sharp drop in chlorophyll content following
summer rains, which imply cyanobacteria and green algae death. In this regard it is worth mentioning that mortality of BSC components was also reported for mosses (Stark et al., 2011) and amoebae (Darby et al., 2011) followed summer rains. In this C-limiting environment (Dommergues et al., 1978), massive cell destruction may substantially add to C turnover, and may be readily taken up and utilized by microfauna and soil microorganisms. Yet, cell destruction takes place also following desiccation, as can be seen by the gradual decrease of chlorophyll during late winter and spring, with summer measurements apparently reflecting longterm quasi-equilibrium conditions. The 2–3-fold increase in microbial biomass (as reflected by the chlorophyll and carbohydrate content) during a single winter rain event may not only imply high C (and probably other nutrient) turnover but may also point to the crust capability to sustain a diverse microbial and microfauna population (Darby et al., 2007). In this regard, one should not overlook the fact that despite the low fertility of sand (Tsoar and Zohar, 1985), the Hallamish dune field is covered by relatively lush vegetation cover of 15–30%, reaching ≤ 80% in certain habitats (Kidron, 1999). While doubling time of bacteria in soil is assumed to take 40–50 h (Coleman et al., 1978), our current data, as far as cyanobacteria and green algae are concerned, point to longer doubling time under natural field conditions. Taking the September 1994 measurements as a benchmark, chlorophyll content on November 6th, 1994, following 3–4 days of precipitation, roughly doubled. It implies, that doubling time of the cyanobacteria and algae under field conditions may be somewhat longer, i.e., 70–80 h. Taking into consideration C loss during nocturnal respiration, this rough estimation may well agree with measurements of lichen photosynthesis that pointed to the fact that nocturnal respiration loss of C is ~ 1/3 of its gain (Kappen et al., 1979). These estimates also agree with chlorophyll measurements taken on the Nizzana crusts by Karnieli et al. (1999). As far as the ecosystem is concerned, cyanobacteria and algae doubling time is fast and may explain their high recovery rate, with the crust's chlorophyll content reaching maturity already within 6–7 years (Kidron et al., 2008). Albeit the substantial death rate of the cyanobacteria (and the green algae cells) that followed the summer rain, one may note that due to the motility capability of the filamentous cyanobacteria and their high responsiveness to small gradients of water (Garcia-Pichel and Pringault, 2001) and light (Campbell, 1979), the effect of the summer rain may be limited and may not result in crust elimination. Indeed, lush BSCs also characterize the deserts of the southwestern United States, which are also subjected to summer rains (Johansen, 1993; Rosentreter and Belnap, 2001). Yet, we hypothesize that summer rains may make a much smaller contribution to the crust's growth rate than winter rains. We further hypothesize that summer rains may trigger a change in species composition, rendering an advantage to species with higher endurance to high temperatures or to species with high motility capability. The data call for caution with regard to the collection time of BSC, whether for biomass or species composition. Dry season collection may thus be regarded as representing a “permanent” “quasi-equilibrium” crust population and biomass. As far as chlorophyll is concerned, winter values may be up to three-fold higher than under “permanent” “quasiequilibrium” conditions. Moreover, species composition and species diversity may be substantially different once executed during the winter growth period. The findings have also important implications concerning possible climate change. Thus, due to high surface temperatures, summer rains may result in relatively short wetness duration (Liu et al., 2009). Since wetness duration dictates species composition and hence crust types (Kidron et al., 2009, 2010), crust-dependent functioning, such as runoff generation (Kidron et al., 2003), may be affected. For arid ecosystems, where water redistribution may largely dictate perennial and annual plant establishment (Shmida et al., 1986), any change in runoff
G.J. Kidron et al. / Catena 95 (2012) 6–11
generation following changes in crust types may largely affect ecosystem health and productivity (Klopatek, 1992). 4. Conclusions A 2–3-fold increase in the chlorophyll and carbohydrate content of the BSCs was recorded in Nizzana following winter rains. Much higher species diversity was found during winter compared with summer, pointing to low adaptability (and hence low abundance) of some species to the harsh summer conditions prevailing in the Negev. A summer rainstorm resulted in a ~15–30% decrease in the chlorophyll content of crusts, explained by high erosion and cell destruction due to the high surface temperatures. The current findings also suggest that climate change that may lead to higher summer precipitation may decrease the crust's species composition and its chlorophyll content, which in turn may affect runoff and water redistribution within the ecosystem. Acknowledgments The work was supported by grant #00R-009 of the International Arid Land Consortium (IALC). We thank A, Starinsky and C.A. Monger for their help in acquiring the funds and C.A. Kidron for the editing. We also thank two anonymous reviewers for their most helpful comments. References Borken, W., Matzner, E., 2009. Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Global Change Biology 15, 808–824. Bowker, M.A., Reed, S.C., Belnap, J., Phillips, S.L., 2002. Temporal variation in community composition, pigmentation, and Fv/Fm of desert cyanobacterial soil crusts. Microbial Ecology 43, 13–25. Brock, T.D., 1975. Effect of water potential on a Microcoleous (Cyanophyceae) from a desert crust. Journal of Phycology 11, 316–320. Büdel, B., 2001. Synopsis: comparative biogeography of soil-crust biota. In: Belnap, J., Lange, O.L. (Eds.), Biological Soil Crusts: Structure, Function, and Management. Springer, Berlin, pp. 141–152. Campbell, S.E., 1979. Soil stabilization by prokaryotic desert crusts: implications for Precambrian land biota. Origins of Life 9, 335–348. Coleman, D.C., Anderson, R.V., Cole, C.V., Elliot, E.T., Woods, L., Campion, M.K., 1978. Trophic interactions as they affect energy and nutrient dynamics, IV. Flows of metabolic and biomass carbon. Microbial Ecology 4, 373–380. Darby, B.J., Neher, D.A., Belnap, J., 2007. Soil nematodes communities are ecologically more mature beneath late than early successional stage biological soil crusts. Applied Soil Ecology 35, 203–212. Darby, B.J., Neher, D.A., Housman, D.C., Belnap, J., 2011. Few apparent short-term effects of elevated soil temperature and increased frequency of summer precipitation on the abundance and taxonomic diversity of desert soil micro- and meso-fauna. Soil Biology and Biochemistry 43, 1474–1481. Dommergues, Y.R., Belser, L.W., Schmidt, E.L., 1978. Limiting factors for growth and activity in soil. Advances in Microbial Ecology 2, 49–104. Ernst, A., Chen, T.-W., Böger, P., 1987. Carbohydrate formation in rewetted terrestrial cyanobacteria. Oecologia 72, 574–576. Evans, R.D., Lange, O.L., 2001. Biological soil crusts and ecosystem nitrogen and carbon dynamics. In: Belnap, J., Lange, O.L. (Eds.), Biological Soil Crusts: Structure, Function, and Management. Springer, Berlin, pp. 263–279. Flaibani, A., Olsen, Y., Painter, T.J., 1989. Polysaccharides in desert reclamation: composition of exocellular proteoglycan complexes produced by filamentous blue-green and unicellular green edaphic algae. Carbohydrate Research 190, 235–248. Gao, K., 1998. Chinese studies on the edible blue-green alga Nostoc flagelliforme: a review. Journal of Applied Phycology 10, 37–49. Garcia-Pichel, F., Castenholz, R.W., 1993. Occurrence of UV-absorbing mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Applied and Environmental Microbiology 59, 163–169. Garcia-Pichel, F., Pringault, O., 2001. Cyanobacteria track water in desert soils. Nature 413, 380–381. Geitler, L., 1932. Cyanophyceae. In: Rabenhorst, L. (Ed.), Kryptogamen-flora von Deutschland, Östereich und der Schweiz, Vol. 14. Akad. Verlagsgesellschaft, Leipzig. Hassid, W.Z., Abraham, S., 1957. Chemical procedures for analysis of polysaccharides. In: Colowick, S.P., Kaplan, N.O. (Eds.), Methods in Enzymology, vol. III. Academic Press, New York, pp. 34–50.
11
Johansen, J.R., 1993. Cryptogamic crusts on semiarid and arid lands of North America. Journal of Phycology 29, 140–147. Kappen, L., Lange, O.L., Schulze, E.-D., Evenari, M., Buschbom, V., 1979. Ecophysiological investigations on lichens of the Negev Desert, IV: Annual course of the photosynthetic production of Ramalina maciformis (Del.) Bory. Flora 168, 85–108. Kappen, L., Lange, O.L., Schulze, E.-D., Buschbom, V., Evenari, M., 1980. Ecophysiological investigations on lichens of the Negev Desert, VII: The influence of the habitat exposure on dew imbibition and photosynthetic productivity. Flora 169, 216–229. Karnieli, A., Kidron, G.J., Glaesser, C., Ben Dor, E., 1999. Spectral characteristics of cyanobacteria soil crust in semiarid environments. Remote Sensing of Environment 69, 67–75. Kidron, G.J., 1999. Differential water distribution over dune slopes as affected by slope position and microbiotic crust, Negev Desert, Israel. Hydrological Processes 13, 1665–1682. Kidron, G.J., 2001. Runoff-induced sediment yield from dune slopes in the Negev Desert, 2: Texture, carbonate and organic matter. Earth Surface Processes and Landforms 26, 583–599. Kidron, G.J., Yair, A., 1997. Rainfall-runoff relationships over encrusted dune surfaces, Nizzana, western Negev, Israel. Earth Surface Processes and Landforms 22, 1169–1184. Kidron, G.J., Barzilay, E., Sachs, E., 2000. Microclimate control upon sand microbiotic crust, western Negev Desert, Israel. Geomorphology 36, 1–18. Kidron, G.J., Yair, A., Vonshak, A., Abeliovich, A., 2003. Microbiotic crust control of runoff generation on sand dunes in the Negev Desert. Water Resources Research 39, 1108–1112. Kidron, G.J., Vonshak, A., Abeliovich, A., 2008. Recovery rates of microbiotic crusts within a dune ecosystem in the Negev Desert. Geomorphology 100, 444–452. Kidron, G.J., Vonshak, A., Abeliovich, A., 2009. Microbiotic crusts as biomarkers for surface stability and wetness duration in the Negev Desert. Earth Surface Processes and Landforms 34, 1594–1604. Kidron, G.J., Vonshak, A., Dor, I., Barinova, S., Abeliovich, A., 2010. Properties and spatial distribution of microbiotic crusts in the Negev Desert. Catena 82, 92–101. Kieft, T.L., Soroker, E., Firestone, M.K., 1987. Microbial biomass response to rapid increase in water potential when dry soil is wetted. Soil Biology and Biochemistry 19, 119–126. Klopatek, J.M., 1992. Cryptogamic crusts as potential indicators of disturbance in semiarid landscapes. In: McKenzie, D.H., Hyatt, D.E., McDonald, V.J. (Eds.), Ecological Indicators, Vol. 1. Elsevier, London, pp. 773–786. Korde, N.V., 1956. The methods of biological studies for the bottom deposits of lakes (the field methods of biological analysis). Freshwater Life USSR 4, 383–413 (in Russian). Lange, O.L., Kidron, G.J., Büdel, B., Meyer, A., Kilian, E., Abeliovich, A., 1992. Taxonomic composition and photosynthetic characteristics of the biological soil crusts covering sand dunes in the Western Negev Desert. Functional Ecology 6, 519–527. Liu, W., Zhang, Z., Wan, S., 2009. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Global Change Biology 15, 184–195. Mayland, H.F., McIntosh, T.H., 1966. Availability of biologically fixed atmospheric nitrogen 15 to higher plants. Nature 209, 421–422. Mazor, G., Kidron, G.J., Vonshak, A., Abeliovich, A., 1996. The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microbiology Ecology 21, 121–130. McKenna Neuman, C., Maxwell, C.D., Boulton, J.W., 1996. Wind transport of sand surfaces crusted with photoautotrophic microorganisms. Catena 27, 229–247. Metting, F.B., Smith, J.L., Amthor, J.S., Izaurralde, R.C., 2001. Science needs and new technology for increasing soil carbon sequestration. Climatic Change 51, 11–34. Potts, M., 1994. Desiccation tolerance of prokaryotes. Microbiological Reviews 58, 755–805. Prasse, R., Bornkamm, R., 2000. Effect of microbiotic soil surface crusts on emergence of vascular plants. Plant Ecology 150, 65–75. Rosenan, N., Gilad, M., 1985. Atlas of Israel. Meteorological data, sheet IV/2. Carta, Jerusalem. Rosentreter, R., Belnap, J., 2001. Biological soil crusts of North America. In: Belnap, J., Lange, O.L. (Eds.), Biological Soil Crusts: Structure, Function, and Management. Springer, Berlin, pp. 31–50. Shmida, A., Evenari, M., Noy-Meir, I., 1986. Hot desert ecosystems: an integrated view. In: Evenari, M., Noy-Meir, I., Goodall, D.W. (Eds.), Hot Deserts and Arid Shrublands B. Elsevier Sci. Pub. B.V., Amsterdam, pp. 379–387. Stark, L.R., Brinda, J.C., McLetchie, D.N., 2011. Effects of increased summer precipitation and N deposition on Mojave Desert populations of the biological crust moss Syntrichia caninervis. Journal of Arid Environments 75, 457–463. Starmach, K., 1966. Cyanophyta-Sinice, Glaucophyta-Glaukofity. In: Starmach, K. (Ed.), Flora Slodkowodna Polski, Vol. II. Polska Akademia Nauk, Panstwowe Wydawnictwo Naukowe, Warszawa, pp. 1–808. Tsoar, H., Zohar, Y., 1985. Desert dune sand and its potential for modern agricultural development. In: Gradus, Y. (Ed.), Desert Development. Reidel, Dordrecht, pp. 184–200. Wetzel, R.G., Westlake, D.F., 1969. Periphyton. In: Vollenweider, R.A. (Ed.), A Manual on Methods for Measuring Primary Production in Aquatic Environments. Blackwell, Oxford, pp. 33–40.
Contents lists available at SciVerse ScienceDirect
Catena journal homepage: www.elsevier.com/locate/catena
The effects of heavy winter rains and rare summer rains on biological soil crusts in the Negev Desert Giora J. Kidron a,⁎, Sophia Barinova b, Ahuva Vonshak c a b c
Institute of Earth Sciences, The Hebrew University, Givat Ram Campus, Jerusalem 91904, Israel Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel Dept. of Dryland Biotechnologies, The Jacob Blaustein Institute for Desert Research, Ben Gurion University of the Negev, Sede Boqer Campus 84993, Israel
a r t i c l e
i n f o
Article history: Received 17 June 2011 Received in revised form 17 February 2012 Accepted 21 February 2012 Keywords: Microbiotic crust Biocrust Chlorophyll Carbohydrates Species composition Sand dune
a b s t r a c t Biological soil crusts (BSCs) abound in the Hallamish dune field in the western Negev Desert, Israel. While their abundance may imply high adaptability to environmental change, such as fluctuations between wet and dry conditions following winter rains, summer rains, although rare, may also occur in the Hallamish dune field. The aim of the present paper is to examine crust responses to winter and summer rains, focusing particularly on its biomass components, chlorophyll and carbohydrate. In addition, species composition, during summer and winter was examined. Analysis took place during an exceptionally wet winter (1994/95 with 172 mm) and a summer rainstorm (12.5.93 with 9.7 mm). The data showed a 2–3 fold increase in chlorophyll a and total carbohydrates and a much richer species composition following the heavy winter rains of 1994/ 95. Yet, the data also showed ~ 15–30% decrease in the chlorophyll content of the crust (with no concomitant significant decrease in total carbohydrates) following the summer rainstorm. Intense weathering by the summer rain coupled with cell mortality may explain the decrease in the chlorophyll content following the summer rainstorm, suggesting possible changes in the BSC following a potential change in the precipitation regime due to global climate change. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Biological soil crusts (BSCs) cover vast areas within arid and semi arid zones where they may often exceed the cover of higher plants (Büdel, 2001). Playing an important role in surface stability (McKenna Neuman et al., 1996), the hydrological properties of the surface (Kidron and Yair, 1997), CO2 sequestration (Metting et al., 2001), nitrogen fixation (Evans and Lange, 2001; Mayland and McIntosh, 1966) and seedling germination (Prasse and Bornkamm, 2000), any change in their cover or biomass may impact the entire ecosystem. Crust cover and biomass may be highly affected by surface stability and wetness duration (Kidron et al., 2009), both of which may be greatly impacted by the climatological conditions. A change in the temperature regime may extensively affect wetness duration, which in turn may alter species composition (Kappen et al., 1980; Kidron et al., 2010). Knowledge regarding the effect of climatological conditions upon crust properties is therefore of special importance. BSCs, whether cyanobacterial or moss-dominated crusts, abound in the Hallamish dune field in the western Negev Desert, Israel, where they cover all sandy interdunes and bottom dunes, absent
⁎ Corresponding author. Tel.: + 972 2 676 7271; fax: + 972 2 566 2581. E-mail address: [email protected] (G.J. Kidron). 0341-8162/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.catena.2012.02.021
only from the mobile dune summits, where wind velocity is too high to allow for crust establishment. Their abundance is rather surprising in this extreme desert. At the Hallamish dune field, long-term annual precipitation is only 95 mm, falling mainly during November to March. Occasionally, the area may also receive summer storms. Crust appearance differs substantially during winter and summer. During most of the dry period, a brownish color characterizes the cyanobacterial crusts and the dry mosses. A dark green color, characterizes cyanobacterial crusts when wet, while a bright green color characterizes mosses during its growth period in the winter. The dark green color of the cyanobacterial crusts may attest to an apparent substantial increase in their chlorophyll content and to the greening effect, sensu Brock (1975), during which the filamentous cyanobacteria tend to migrate to the surface (Fig. 1a). Since cyanobacteria motility was principally explained by filament gliding that takes place along with EPS excretion (Campbell, 1979), it may explain the close link between chlorophyll and the carbohydrate-constituted exopolysaccharides, EPS (Kidron et al., 2010). While the greening effect may be visible in the winter, no greening effect was noted in summer, raising the hypothesis that the crust response to wetting may be season-dependent. As such, it was hypothesized that the chlorophyll content of the crust may be variably affected by occasional, rather rare, summer rains, defined herein as rains falling during the hot months of May–August. Furthermore, since EPS excretion is triggered by motility (Campbell, 1979), the
G.J. Kidron et al. / Catena 95 (2012) 6–11
a
b
Fig. 1. The greening effect (manifested by the darker patches) at a cyanobacterial crust as photographed during November 20, 1994 (a), and the five crust types defined in Nizzana (b).
total carbohydrate content of the crust (which mainly constitute the EPS; see Ernst et al., 1987; Mazor et al., 1996) may also be affected. In an attempt to monitor rain-induced fluctuation, chlorophyll, carbohydrates and species composition of the BSCs were monitored. Monitoring included cyanobacteria, green algae and diatoms. They also included the lichen and moss cover. During the current research monitoring focused on the exceptionally wet winter of 1994/95, and on a rare summer rainstorm that took place in the summer of 1993.
2. Material and methods The research took place at the Nizzana research station of the Hallamish dune field in the western Negev Desert, Israel (34°23′E, 30°56′N). West–east longitudinal dunes, 15–20 m high, separated by 50–200 m wide interdunes characterize the dune field. Mean long-term precipitation is 95 mm, falling during the winter, mainly during November-March (Rosenan and Gilad, 1985). Five types of crusts, crusts A-E, were defined in the Hallamish dune field, four cyanobacteria-dominated (crusts A–D, 1–3 mm thick, with Microcoleus sp. predominating, Lange et al., 1992) and one (crust E, 10 mm thick), moss-dominated (Table 1; Fig. 1b). The crusts differed in a variety of physical and biological parameters, with their chlorophyll content and total carbohydrates exhibiting significant differences (Kidron et al., 2010). Whereas crust A extends over the interdunes and the south-facing footslopes, occupying the most xeric habitat of the dune field, crusts B–E extend over the north-facing slope. On a stabilized dune, crust B extends over the upper slope, being followed by crusts C (between the upper and mid slope), D at the mid slope
7
Table 1 Crust characteristics (One standard deviation in parenthesis). Crust Type
Aspect Location
Crust Thickness Chloro-phyll Carbo-hydrates (mm) (N = 12) mg m− 2 (g/ m− 2) (N = 103) (N = 206)
A
SF
Footslope
B
NF
Upper Slope
C
NF
D
NF
Upper-Mid Slope Mid Slope
E
NF
Footslope
1.1 (0.3) 1.5 (0.3) 2.0 (0.4) 2.8 (0.3) 10.3 (1.4)
16.7 (9.9) 20.7 (10.5) 28.5 (16.7) 43.4 (27.6) 53.2 (25.8)
5.28 (2.27) 7.65 (3.28) 9.15 (4.34) 15.92 (5.97) 33.16 (14.71)
and E which occupies the interface between the bottom of the northfacing dune and the interdune. Two plots, ~ 2 × 2 m, were demarcated on each of the five crust types, A–E. Following a rare rainstorm that fell during the summer of 1993 (12.5.93) and an exceptionally heavy rain event of 56.2 mm that fell during November 2nd and 6th, 1994 (followed by additional high-depth rainstorms), crust samples were collected for chlorophyll a and total carbohydrate measurements. While two sampling periods were executed during the 12.5.93 summer rain (prior and following the rain event), measurements during 1994/95 took place in 1–4 week intervals. Measurements for the crust biomass were executed on 12 crust cores, 1 cm2 and 1 cm thick. While taken weekly from each plot during the rainy period, they were taken in 2–4 week intervals during dry spells. Chlorophyll a (hereafter 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). Following chlorophyll extraction, total carbohydrates (hereafter termed carbohydrates) were determined using the anthrone method (Hassid and Abraham, 1957). In addition, the relative cover of the lichens and mosses was visually estimated in 1–2 mo intervals during the winter of 1994/95. Monitoring took place in ten 10 × 10 cm squares, 20 cm apart, that were marked along two 1 m-long transects that stretched ~ 20 cm from each side of each plot. Monitoring included mature lichens with fruiting bodies, as well as lichenized surfaces which did not yet have fruiting bodies. During winter (December 1994) and summer (July 1995) of the hydrological year of 1994/95, crusts were also sampled for the analysis of species composition. The December sampling was executed one week after the 33 mm rain event of 2–6.12.94, during which most crusts were wet, while the July sampling took place ~2 months following the last rain event, thus representing dry surface conditions. The 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. For the evaluation of the relative proportion of each of the identified cyanobacteria and algal species, four crusts, approximately 5 cm 2 each, were taken from each plot at each crust type. The crusts were crushed, immersed in water and homogenized, and the dilution was examined under a light microscope. The cyanobacteria, green algae and diatoms were identified, and the relative abundance of cells per species of each slide was assessed. The relative abundance of cells for each crust type was presented in a 6-score scale, in accordance with Korde (1956).
3. Results and discussion The winter of 1992/93 was slightly drier than the long-term mean with a total of 85.3 mm. Conversely, winter of 1994/95 was exceptionally
8
G.J. Kidron et al. / Catena 95 (2012) 6–11
wet, with three rainstorms having ≥30 mm. Rain precipitation amounted to 172.0, almost twice as high as the 95 mm mean (Fig. 2). As a result of the wet winter, extended wetness duration characterized all habitats during the winter of 1994/95. Cyanobacteria migration to the surface, i.e., the greening effect, was common. Moss growth was noted at newly-scalped surfaces (Kidron et al., 2008). Furthermore, moss establishment and growth took place also at the south-facing slope, in areas which did not have moss growth before, as noted as early as on December 10th. Moreover, extensive lichenization took place at all habitats, being especially pronounced at crust D and C. It was expressed by sterile coin and ring shaped lichen forms, several centimeters up to 15 cm in diameter (Fig. 3a, b). Contrarily, surface wetness was relatively short following the 12.5.93 rainstorm event. Yet, this event resulted in substantial surface erosion, reflected in a dome-shaped microrelief that characterized many of the surfaces and was explained by the sever impact that the rain drops had on the dry surface (Fig. 3c). As expected, high fluctuation characterizes the chlorophyll and carbohydrate content, with winter values of each crust type being significantly higher than the summer values (Fig. 4). This can be clearly seen for the most xeric (crust A) and mesic (crust D) cyanobacterial crusts, and for the moss-dominated crust (crust E). Chlorophyll content varied between 14.6, 35.7 and 53.8 mg m− 2 in the summer to 42.1, 100.4 and 134.3 mg m − 2 in the winter for crust A, D, and E, respectively. Similarly, carbohydrate content varied between 4.4, 13.3 and 27.7 g m − 2 in the summer to 11.1, 35.6 and 80.0 g m − 2 in the winter for crusts A, D and E, respectively. Both biomass components increased two to three fold following the winter rain events compared to summer values. The lichenized surface cover and the moss cover showed a similar trend, with up to 2–3 fold increase (Fig. 5). Yet, unlike the drop in the chlorophyll and carbohydrate content, the values remained more or less constant. One should however note, that field observations that took place three years later failed to detect mosses at the southfacing slope, pointing to the fact that the long-term conditions at this habitat were apparently not suited for long-term moss establishment. Also, many of the lichenized surfaces were not noted three years later indicating that licenization did not necessarily lead to the formation of lichens. Except for the moss-dominated crust, chlorophyll content increased relatively rapidly following the rain event, attesting to the rapid growth rate of the cyanobacteria, and to a slower growth rate of the moss. During many of the cloudy winter days, the greening effect was noted with Microcoleus sheaths being observed at the surface by the naked eye (Fig. 1b). A close link between chlorophyll and
a
b
c
Fig. 3. Lichenized surfaces (a) and a close-up of 12.5 cm-diameter ring-shaped lichenized surface (b) as photographed on the north-facing slope during December 17th, and high surface erosion which results in a dome-shaped microtopography (c) at the north-facing slope following the 12.5.93 rainstorm event.
Fig. 2. Rain distribution during 1992/93 and 1994/95.
carbohydrates was observed. It was also observed at the mossdominated crust, crust E. Yet, unlike the case with the cyanobacteria in which ≤70% of their dry weight are carbohydrate-constituted exopolysaccharides (Flaibani et al., 1989), the carbohydrates at crust E may primarily reflect the inner above- and below-surface (mainly the rhizoids) content of the moss cells. Following crust desiccation, during which crust microorganism enter an anhydrobiotic state (Potts, 1994), a decrease in the chlorophyll and carbohydrate content was noted. Yet, contrary to the rapid response of the chlorophyll content to surface wetting and desiccation (Fig. 4a), the change in the total carbohydrates was somewhat slower (Fig. 4b). Both responses, that of the chlorophyll and especially that of the carbohydrates, were substantially slower at the moss-dominated
G.J. Kidron et al. / Catena 95 (2012) 6–11
9
Table 2 Species composition of cyanobacteria, green algae and diatoms as determined during the winter (W) of 1994/95 and summer (S) of 1995 following Korde, 1956 (1 — Occassional 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 — Several cells over a slide transect, 6 — Abundant with few cells in each field of view). Species Composition
Fig. 4. Chlorophyll (a) and carbohydrate (b) fluctuation of crusts A-E during 1994/95. Bars represent one SE. Arrows at the abscissa indicate rain events with >10 mm.
crust, explained by the different physiological response of the moss, and its gradual growth during winter until reaching mature spores. It is also explained by the much longer wetness duration that characterized the surface of the crust E habitat (Kidron et al., 2000) and the ability of the moss to withdraw water from a deeper layer of ~10 mm (by using its rhizoids) compared to 1–3 mm layer utilized by the cyanobacteria. The change in crust biomass was also accompanied by a change in the microorganism species composition. High species diversity was noted during mid winter, at the time when the crust biomass was at its greatest (Table 2). The high diversity may attest to the relatively good edaphic and environmental conditions that prevail during
Fig. 5. Lichenized surface cover (a) and moss cover (b) during 1994/95. Bars represent one SE.
Cyanobacteria Microcoleus vaginatus (Vaucher) Gomont ex Gomont Microcoleus vaginatus var monticola (Kützing) Gomont Synechococcus sciophilus Skuja Chroococcus turgidus (Kützing) Nägeli Chroococcus sp. Phormidium sp. Nostoc microscopicum Carmichael ex Bornet & Flahault Nostoc sp. Scytonema sp. Oscillatoria sp. Schizothrix friesii (Gomont ex Gomont) Kirchner Chroococcidiopsis sp. Green algae Trentepohlia sp. Microspora sp., Stichococcus sp. Chlorococcum sp. Diatoms Luticola mutica (Kützing) D.G.Mann Luticola nivalis (Ehrenberg) D.G.Mann Nitzcshia sp. Naviculaceae
A
B
C
D
E
W
S
W
S
W
S
W
S
W
S
4
6
3
5
2
4
2
4
2
3
3 1
3 1
2 1
2 1
2 2
2 2
1 1 3
1 3
1 3
1 3
2 1 1 1
1 1 1
2 2 1 1
2 1 1
1 3 2 2
3 2 2
2 4 3 3
4 3 3
1 3 3 3
3 3 3
4 3 2
1 4 1 1
1 4 1
4 1 1
3 2 1 1
1 4 1
5 1 1
1 1
1 5 1
2 2 2 1
1 2 2
3 3 3
3
1 1 1 1
winter, during which, suitable conditions exist for the establishment of a wide variety of microorganisms. Nevertheless, the sharp drop in species diversity monitored during summer (Table 2) may attest to a limited adaptability of many species to the harsh conditions or the lengthy duration during which the crust remains dry during summer. This, in turn, resulted in the low abundance of some species. While 12 species of cyanobacteria and four species of diatoms were defined during winter, no diatoms and only six species of cyanobacteria were defined during summer. Apparently, only species that do not experience high mortality and their abundance does not drop substantially throughout summer may be regarded as species that are well adapted to the harsh conditions of the arid dune field. As for the lichens, only lichens with fruiting bodies could have been identified. The lichens identified within the research site were Fulgensia fulgens (Sw.) Elenkin, Caloplaca sp. and Collema sp. As for the mosses, two species were identified on the dune sand: Bryum dunense A.J.E. Smith & H. Whitehouse and Tortula brevissima Schiffner. Chlorophyll content following the 12.5.93 summer rain resulted in a substantial drop of ~ 15-30% of some cyanobacterial crusts (significant at P b 0.05 once a t-test was performed for crust C and at P b 0.1 for crust A). This was not the case with the moss-dominated crust, crust E (Fig. 6a). As for the carbohydrate content, although being lower, the summer rain did not significantly affect the carbohydrate content of crusts (Fig. 6b). The sharp drop in the chlorophyll content following the summer rain event is not yet fully understood. Although rather rare with four summer rainstorms that occurred during the last 20 (1991–2010) years (i.e, a summer rainstorm every 5 years), their implications upon the ecosystem may be high. While intense erosion caused by the rain drop impact on the dry crust, which is especially prone to erosion (and reflected in the rugged, dome-like microrelief, see also Kidron, 2001), may partially explain the phenomenon, high mortality, due to cell burst coupled with the high surface temperatures may provide additional explanation.
10
G.J. Kidron et al. / Catena 95 (2012) 6–11
Fig. 6. Chlorophyll (a) and carbohydrates (b) prior and following a summer rain event of May 12, 1993. Asterisks indicate significant differences within a pair at P b 0.05 (*) or P b 0.1 (**).
High cell mortality of microorganisms was noted following sudden soil wetting and explained by the incapability of the cells to adapt to the dramatic change in the osmotic pressure of the cell (Kieft et al., 1987). This threat may be alleviated by exopolysaccharide secretion, mainly by the formation of thick sheaths (Borken and Matzner, 2009), such as the sheaths that characterize the dominant species in Nizzana, Microcoleus vaginatus. Yet, the high cell mortality that we noted following the 12.5.93 rainstorm cannot be solely attributed to the same phenomenon. Thus, crust sampling following winter rains (such as the 2–6.11.94 rainstorm) did not monitor a substantial drop in the chlorophyll content. Although cell death apparently took place, it was not massive enough to be easily detected by the current method used for chlorophyll measurements. We therefore postulate that the significant drop in the chlorophyll content may be also explained by the high UV radiation during the summer (GarciaPichel and Castenholz, 1993) and by the surface temperatures which characterize the summer surfaces, which may exceed 50 °C. While rainwater and subsequent evaporation acted to cool the surface, surface temperatures may still be > 30 °C, i.e., within a temperature range that may limit cyanobacteria growth. Indeed, while exhibiting substantial endurance to high temperature when dry, cyanobacteria and green algae have low endurance to high temperatures when wet (Gao, 1998). In fact, cyanobacteria isolates from Nizzana died when incubated at ≥ 37 °C, while exhibiting very low growth rates already at ≥ 32 °C (Mazor et al., 1996). Yet, while some of the species, such as Microcoleus and Phormidium, may escape the harmful effect of the high temperatures due to their motility, other species, which do not posses motility, such as Nostoc and Scytonema, may not. Alternatively, high mortality may also stem from UV radiation against which the pigmented species Nostoc and Scytonema are well protected. This will result in high mortality of the less-pigmented species such as Microcoleus vaginatus as reported by Bowker et al. (2002). Yet, as far as the rain drop impact is concerned, the upper-surface dwellers Nostoc and Scytonema, which mostly prevail in the more mesic north-facing slope, may be much more susceptible to weathering and erosion. While more detailed examinations are needed in order to identify the most vulnerable species, the current findings nevertheless point to the sharp drop in chlorophyll content following
summer rains, which imply cyanobacteria and green algae death. In this regard it is worth mentioning that mortality of BSC components was also reported for mosses (Stark et al., 2011) and amoebae (Darby et al., 2011) followed summer rains. In this C-limiting environment (Dommergues et al., 1978), massive cell destruction may substantially add to C turnover, and may be readily taken up and utilized by microfauna and soil microorganisms. Yet, cell destruction takes place also following desiccation, as can be seen by the gradual decrease of chlorophyll during late winter and spring, with summer measurements apparently reflecting longterm quasi-equilibrium conditions. The 2–3-fold increase in microbial biomass (as reflected by the chlorophyll and carbohydrate content) during a single winter rain event may not only imply high C (and probably other nutrient) turnover but may also point to the crust capability to sustain a diverse microbial and microfauna population (Darby et al., 2007). In this regard, one should not overlook the fact that despite the low fertility of sand (Tsoar and Zohar, 1985), the Hallamish dune field is covered by relatively lush vegetation cover of 15–30%, reaching ≤ 80% in certain habitats (Kidron, 1999). While doubling time of bacteria in soil is assumed to take 40–50 h (Coleman et al., 1978), our current data, as far as cyanobacteria and green algae are concerned, point to longer doubling time under natural field conditions. Taking the September 1994 measurements as a benchmark, chlorophyll content on November 6th, 1994, following 3–4 days of precipitation, roughly doubled. It implies, that doubling time of the cyanobacteria and algae under field conditions may be somewhat longer, i.e., 70–80 h. Taking into consideration C loss during nocturnal respiration, this rough estimation may well agree with measurements of lichen photosynthesis that pointed to the fact that nocturnal respiration loss of C is ~ 1/3 of its gain (Kappen et al., 1979). These estimates also agree with chlorophyll measurements taken on the Nizzana crusts by Karnieli et al. (1999). As far as the ecosystem is concerned, cyanobacteria and algae doubling time is fast and may explain their high recovery rate, with the crust's chlorophyll content reaching maturity already within 6–7 years (Kidron et al., 2008). Albeit the substantial death rate of the cyanobacteria (and the green algae cells) that followed the summer rain, one may note that due to the motility capability of the filamentous cyanobacteria and their high responsiveness to small gradients of water (Garcia-Pichel and Pringault, 2001) and light (Campbell, 1979), the effect of the summer rain may be limited and may not result in crust elimination. Indeed, lush BSCs also characterize the deserts of the southwestern United States, which are also subjected to summer rains (Johansen, 1993; Rosentreter and Belnap, 2001). Yet, we hypothesize that summer rains may make a much smaller contribution to the crust's growth rate than winter rains. We further hypothesize that summer rains may trigger a change in species composition, rendering an advantage to species with higher endurance to high temperatures or to species with high motility capability. The data call for caution with regard to the collection time of BSC, whether for biomass or species composition. Dry season collection may thus be regarded as representing a “permanent” “quasi-equilibrium” crust population and biomass. As far as chlorophyll is concerned, winter values may be up to three-fold higher than under “permanent” “quasiequilibrium” conditions. Moreover, species composition and species diversity may be substantially different once executed during the winter growth period. The findings have also important implications concerning possible climate change. Thus, due to high surface temperatures, summer rains may result in relatively short wetness duration (Liu et al., 2009). Since wetness duration dictates species composition and hence crust types (Kidron et al., 2009, 2010), crust-dependent functioning, such as runoff generation (Kidron et al., 2003), may be affected. For arid ecosystems, where water redistribution may largely dictate perennial and annual plant establishment (Shmida et al., 1986), any change in runoff
G.J. Kidron et al. / Catena 95 (2012) 6–11
generation following changes in crust types may largely affect ecosystem health and productivity (Klopatek, 1992). 4. Conclusions A 2–3-fold increase in the chlorophyll and carbohydrate content of the BSCs was recorded in Nizzana following winter rains. Much higher species diversity was found during winter compared with summer, pointing to low adaptability (and hence low abundance) of some species to the harsh summer conditions prevailing in the Negev. A summer rainstorm resulted in a ~15–30% decrease in the chlorophyll content of crusts, explained by high erosion and cell destruction due to the high surface temperatures. The current findings also suggest that climate change that may lead to higher summer precipitation may decrease the crust's species composition and its chlorophyll content, which in turn may affect runoff and water redistribution within the ecosystem. Acknowledgments The work was supported by grant #00R-009 of the International Arid Land Consortium (IALC). We thank A, Starinsky and C.A. Monger for their help in acquiring the funds and C.A. Kidron for the editing. We also thank two anonymous reviewers for their most helpful comments. References Borken, W., Matzner, E., 2009. Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Global Change Biology 15, 808–824. Bowker, M.A., Reed, S.C., Belnap, J., Phillips, S.L., 2002. Temporal variation in community composition, pigmentation, and Fv/Fm of desert cyanobacterial soil crusts. Microbial Ecology 43, 13–25. Brock, T.D., 1975. Effect of water potential on a Microcoleous (Cyanophyceae) from a desert crust. Journal of Phycology 11, 316–320. Büdel, B., 2001. Synopsis: comparative biogeography of soil-crust biota. In: Belnap, J., Lange, O.L. (Eds.), Biological Soil Crusts: Structure, Function, and Management. Springer, Berlin, pp. 141–152. Campbell, S.E., 1979. Soil stabilization by prokaryotic desert crusts: implications for Precambrian land biota. Origins of Life 9, 335–348. Coleman, D.C., Anderson, R.V., Cole, C.V., Elliot, E.T., Woods, L., Campion, M.K., 1978. Trophic interactions as they affect energy and nutrient dynamics, IV. Flows of metabolic and biomass carbon. Microbial Ecology 4, 373–380. Darby, B.J., Neher, D.A., Belnap, J., 2007. Soil nematodes communities are ecologically more mature beneath late than early successional stage biological soil crusts. Applied Soil Ecology 35, 203–212. Darby, B.J., Neher, D.A., Housman, D.C., Belnap, J., 2011. Few apparent short-term effects of elevated soil temperature and increased frequency of summer precipitation on the abundance and taxonomic diversity of desert soil micro- and meso-fauna. Soil Biology and Biochemistry 43, 1474–1481. Dommergues, Y.R., Belser, L.W., Schmidt, E.L., 1978. Limiting factors for growth and activity in soil. Advances in Microbial Ecology 2, 49–104. Ernst, A., Chen, T.-W., Böger, P., 1987. Carbohydrate formation in rewetted terrestrial cyanobacteria. Oecologia 72, 574–576. Evans, R.D., Lange, O.L., 2001. Biological soil crusts and ecosystem nitrogen and carbon dynamics. In: Belnap, J., Lange, O.L. (Eds.), Biological Soil Crusts: Structure, Function, and Management. Springer, Berlin, pp. 263–279. Flaibani, A., Olsen, Y., Painter, T.J., 1989. Polysaccharides in desert reclamation: composition of exocellular proteoglycan complexes produced by filamentous blue-green and unicellular green edaphic algae. Carbohydrate Research 190, 235–248. Gao, K., 1998. Chinese studies on the edible blue-green alga Nostoc flagelliforme: a review. Journal of Applied Phycology 10, 37–49. Garcia-Pichel, F., Castenholz, R.W., 1993. Occurrence of UV-absorbing mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Applied and Environmental Microbiology 59, 163–169. Garcia-Pichel, F., Pringault, O., 2001. Cyanobacteria track water in desert soils. Nature 413, 380–381. Geitler, L., 1932. Cyanophyceae. In: Rabenhorst, L. (Ed.), Kryptogamen-flora von Deutschland, Östereich und der Schweiz, Vol. 14. Akad. Verlagsgesellschaft, Leipzig. Hassid, W.Z., Abraham, S., 1957. Chemical procedures for analysis of polysaccharides. In: Colowick, S.P., Kaplan, N.O. (Eds.), Methods in Enzymology, vol. III. Academic Press, New York, pp. 34–50.
11
Johansen, J.R., 1993. Cryptogamic crusts on semiarid and arid lands of North America. Journal of Phycology 29, 140–147. Kappen, L., Lange, O.L., Schulze, E.-D., Evenari, M., Buschbom, V., 1979. Ecophysiological investigations on lichens of the Negev Desert, IV: Annual course of the photosynthetic production of Ramalina maciformis (Del.) Bory. Flora 168, 85–108. Kappen, L., Lange, O.L., Schulze, E.-D., Buschbom, V., Evenari, M., 1980. Ecophysiological investigations on lichens of the Negev Desert, VII: The influence of the habitat exposure on dew imbibition and photosynthetic productivity. Flora 169, 216–229. Karnieli, A., Kidron, G.J., Glaesser, C., Ben Dor, E., 1999. Spectral characteristics of cyanobacteria soil crust in semiarid environments. Remote Sensing of Environment 69, 67–75. Kidron, G.J., 1999. Differential water distribution over dune slopes as affected by slope position and microbiotic crust, Negev Desert, Israel. Hydrological Processes 13, 1665–1682. Kidron, G.J., 2001. Runoff-induced sediment yield from dune slopes in the Negev Desert, 2: Texture, carbonate and organic matter. Earth Surface Processes and Landforms 26, 583–599. Kidron, G.J., Yair, A., 1997. Rainfall-runoff relationships over encrusted dune surfaces, Nizzana, western Negev, Israel. Earth Surface Processes and Landforms 22, 1169–1184. Kidron, G.J., Barzilay, E., Sachs, E., 2000. Microclimate control upon sand microbiotic crust, western Negev Desert, Israel. Geomorphology 36, 1–18. Kidron, G.J., Yair, A., Vonshak, A., Abeliovich, A., 2003. Microbiotic crust control of runoff generation on sand dunes in the Negev Desert. Water Resources Research 39, 1108–1112. Kidron, G.J., Vonshak, A., Abeliovich, A., 2008. Recovery rates of microbiotic crusts within a dune ecosystem in the Negev Desert. Geomorphology 100, 444–452. Kidron, G.J., Vonshak, A., Abeliovich, A., 2009. Microbiotic crusts as biomarkers for surface stability and wetness duration in the Negev Desert. Earth Surface Processes and Landforms 34, 1594–1604. Kidron, G.J., Vonshak, A., Dor, I., Barinova, S., Abeliovich, A., 2010. Properties and spatial distribution of microbiotic crusts in the Negev Desert. Catena 82, 92–101. Kieft, T.L., Soroker, E., Firestone, M.K., 1987. Microbial biomass response to rapid increase in water potential when dry soil is wetted. Soil Biology and Biochemistry 19, 119–126. Klopatek, J.M., 1992. Cryptogamic crusts as potential indicators of disturbance in semiarid landscapes. In: McKenzie, D.H., Hyatt, D.E., McDonald, V.J. (Eds.), Ecological Indicators, Vol. 1. Elsevier, London, pp. 773–786. Korde, N.V., 1956. The methods of biological studies for the bottom deposits of lakes (the field methods of biological analysis). Freshwater Life USSR 4, 383–413 (in Russian). Lange, O.L., Kidron, G.J., Büdel, B., Meyer, A., Kilian, E., Abeliovich, A., 1992. Taxonomic composition and photosynthetic characteristics of the biological soil crusts covering sand dunes in the Western Negev Desert. Functional Ecology 6, 519–527. Liu, W., Zhang, Z., Wan, S., 2009. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Global Change Biology 15, 184–195. Mayland, H.F., McIntosh, T.H., 1966. Availability of biologically fixed atmospheric nitrogen 15 to higher plants. Nature 209, 421–422. Mazor, G., Kidron, G.J., Vonshak, A., Abeliovich, A., 1996. The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microbiology Ecology 21, 121–130. McKenna Neuman, C., Maxwell, C.D., Boulton, J.W., 1996. Wind transport of sand surfaces crusted with photoautotrophic microorganisms. Catena 27, 229–247. Metting, F.B., Smith, J.L., Amthor, J.S., Izaurralde, R.C., 2001. Science needs and new technology for increasing soil carbon sequestration. Climatic Change 51, 11–34. Potts, M., 1994. Desiccation tolerance of prokaryotes. Microbiological Reviews 58, 755–805. Prasse, R., Bornkamm, R., 2000. Effect of microbiotic soil surface crusts on emergence of vascular plants. Plant Ecology 150, 65–75. Rosenan, N., Gilad, M., 1985. Atlas of Israel. Meteorological data, sheet IV/2. Carta, Jerusalem. Rosentreter, R., Belnap, J., 2001. Biological soil crusts of North America. In: Belnap, J., Lange, O.L. (Eds.), Biological Soil Crusts: Structure, Function, and Management. Springer, Berlin, pp. 31–50. Shmida, A., Evenari, M., Noy-Meir, I., 1986. Hot desert ecosystems: an integrated view. In: Evenari, M., Noy-Meir, I., Goodall, D.W. (Eds.), Hot Deserts and Arid Shrublands B. Elsevier Sci. Pub. B.V., Amsterdam, pp. 379–387. Stark, L.R., Brinda, J.C., McLetchie, D.N., 2011. Effects of increased summer precipitation and N deposition on Mojave Desert populations of the biological crust moss Syntrichia caninervis. Journal of Arid Environments 75, 457–463. Starmach, K., 1966. Cyanophyta-Sinice, Glaucophyta-Glaukofity. In: Starmach, K. (Ed.), Flora Slodkowodna Polski, Vol. II. Polska Akademia Nauk, Panstwowe Wydawnictwo Naukowe, Warszawa, pp. 1–808. Tsoar, H., Zohar, Y., 1985. Desert dune sand and its potential for modern agricultural development. In: Gradus, Y. (Ed.), Desert Development. Reidel, Dordrecht, pp. 184–200. Wetzel, R.G., Westlake, D.F., 1969. Periphyton. In: Vollenweider, R.A. (Ed.), A Manual on Methods for Measuring Primary Production in Aquatic Environments. Blackwell, Oxford, pp. 33–40.