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Cyanobacteria are confined to dewless habitats within a dew desert: Implications for past and future climate change for lithic microorganisms
Journal of Hydrology 519 (2014) 3606–3614
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Cyanobacteria are confined to dewless habitats within a dew desert: Implications for past and future climate change for lithic microorganisms Giora J. Kidron ⇑, Abraham Starinsky, Dan H. Yaalon 1 Institute of Earth Sciences, The Hebrew University, Jerusalem 91904, Israel
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Article history: Received 19 March 2014 Received in revised form 18 August 2014 Accepted 2 November 2014 Available online 12 November 2014 This manuscript was handled by Laurent Charlet, Editor-in-Chief, with the assistance of Rizlan Bernier-Latmani, Associate Editor Keywords: Colonization Cyanobacteria Dew Lichens Negev Neoproterozoic
s u m m a r y Although covering almost all rock outcrops around the world, little is known regarding the factors that govern the spatial distribution of lithic cyanobacteria and lichens. This is also the case in the Negev Desert, where cyanobacteria predominate on the rock outcrops of the south-facing slopes and lichens on the rock outcrops of the north-facing slopes. Hypothesizing that abiotic conditions determine their distribution, radiation, temperature, rain, dew and fog were monitored over a two-year period (2008– 2010) at cyanobacteria- and lichen-dwelling habitats within a first-order drainage basin in the Negev Highlands. While non-significant differences characterized the rain amounts, substantial differences in substrate temperatures were recorded which resulted in turn in fundamental differences in the non-rainfall water regime. While dew condensed at the rock outcrops of the lichen habitat, no condensation took place at the cyanobacteria habitat. Contrary to the common belief, cyanobacteria were found to inhabit dewless habitats. As a result, cyanobacteria solely rely on rain precipitation for growth and can therefore serve as bioindicators for dewless habitats within the dewy Negev Desert. The findings may have important implications regarding Earth colonization, soil forming processes and geochemical processes following climate warming. They may explain lichen expansion and subsequent O2 increase during the mid Neoproterozoic providing indirect support for substantial photosynthetic activity and high weathering rates during this era. Ó 2014 Elsevier B.V. All rights reserved.
1. Introduction As photoautotrophs, cyanobacteria and lichens (a symbiotic association between a photobiont and a mycobiont) are of outmost importance to primary production. Inhabiting the most harsh and extreme habitats, and almost all rocky substrates (Chen et al., 2000), they are primary producers of organic C and N (Evans and Lange, 2001). As such, their importance goes back to early Earth colonization, where both groups provided most of the primary production (Altermann et al., 2006; Yuan et al., 2005; Guo et al., 2011). They are also known for their high weathering capabilities (Schwartzman and Volk, 1989; Aghamiri and Schwartzman, 2002), therefore fulfilling an important role in soil formation (Wright, 1985). Both microorganisms are widely distributed. Lithic cyanobacteria and lichens occupy all continents. They abound around the ⇑ Corresponding author. Tel.: +972 544 967271; fax: +972 2 566 2581. E-mail addresses: [email protected] (G.J. Kidron), [email protected] (A. Starinsky), [email protected] (D.H. Yaalon). 1 Regrettably, Dan passed away during the preparation of the ms. http://dx.doi.org/10.1016/j.jhydrol.2014.11.010 0022-1694/Ó 2014 Elsevier B.V. All rights reserved.
Mediterranean Sea (Albertano and Urzi, 1999; de los Rios and Ascaso, 2005), Europe (Sigler et al., 2003), North America (Gerrath et al., 2000), South America, Africa, and Australia (Büdel, 1999), the Arctic (Cockell et al., 2003) and Antarctica (WynnWilliams et al., 1999; Casanovas et al., 2013). In light of the growing amount of evidence of past and possible present Martian life (Schulze-Makuch et al., 2005, 2008), and ongoing efforts to identify reliable biomarkers for Martian life (Jehlicˇka et al., 2009), such as microtunnels (Fisk et al., 2006), knowledge regarding the abiotic conditions necessary for cyanobacteria and lichen growth on Earth is essential for identifying comparable conditions on Mars. Although regarded as an extreme desert (with a mean annual precipitation of 90 mm), lithobiontic microorganisms including cyanobacteria and lichens occupy the bedrock of the Negev Desert Highlands, such as at Sede Boqer and Avdat (Fig. 1), subjected to extensive research (Lange et al., 1970; Danin and Garty, 1983). With epilithic lichens dwelling on top of the surface and with cyanobacteria occupying the upper several millimeters of the surface (triggering rock weathering and the subsequent formation of pits and tunnels) they render the surface a different appearance. While
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epilithic lichens (with green algae as photobionts such as Caloplaca aurantia (Pers.) Hellb., Aspicilia farinosa (Flörke) Arnold, and Lecanora albescens (Hoffm.) Branth and Rostr. predominating) (Fig. 2a) render the north-facing slopes (NFS) smooth, cyanobacteria (with the genus Gleocapsa predominating, see Friedmann and Galun, 1974; Danin and Garty, 1983; Kidron et al., 2011), occupying the south-facing slope (SFS), render the surface uneven, with a ragged, pit-like microtopography (Fig. 2b and c). The current view maintains that water provided by rain and dew is the driving force behind the growth of the cyanobacteria (Friedmann and Galun, 1974; Smith et al., 2000; but see also Danin and Garty, 1983 that report no dew condensation during two nights of measurements). In a dew desert with annual average dew and fog precipitation of 33 mm falling during 195 days a year, dew was assumed to be the major water source for these lithobionts (Friedmann and Galun, 1974). While lichen activity following high relative humidity and dew condensation (vapor condensation at the substrate surface) as well as fog precipitation (i.e., substrate wetting by water droplets that condensed in the air) was monitored (Lange et al., 1970), no such data were provided for the cyanobacteria and no explanation for the confinement of the cyanobacteria to the bedrocks of SFS was offered. Furthermore, as part of a larger project (Kidron, 1999), temperature measurements took place at different substrates along a north–south gradient of the Negev Desert. Temperatures of cyanobacteria-inhabited bedrocks were found to be consistently warmer by at least 3–4 °C than lichen-inhabited bedrocks, bringing about the notion that the cyanobacteria-inhabited bedrocks are subjected to much lower dew condensation. Hypothesizing that the confinement of the cyanobacteria to SFS may stem from microclimatological variables and that understanding these microclimatological conditions may explain past colonization conditions, the goal of the current research was to monitor the abiotic variables at the cyanobacteria and the lichen habitats. Towards this goal, irradiance, temperatures, rain, dew and fog were measured. Mornings with high relative humidity only were not monitored despite the fact that high relative humidity is also utilized by most lichens (Lange et al., 1986). Nevertheless, since high relative humidity culminates in dew condensation for over 90% of the nights (Kappen et al., 1979), its contribution may largely be seen reflected in the amounts of dew and fog. As for the research location, it was confined to a single drainage basin thus avoiding the introduction of multiple variables that may affect the results, such as cloudiness and lithology.
2. Methods The research site is located in Sede Boqer in the Negev Desert Highlands, Israel (34°460 E, 30°560 N), approximately 500 m above sea level (Fig. 1). Mean annual rain precipitation is 95 mm, limited to the winter months (November–April)). Average annual temperature is 17.9 °C; it is 24.7 °C during the hottest month of July and 9.3 °C during the coldest month of January (Bitan and Rubin, 1991). Annual potential evaporation is 2600 mm (Evenari, 1981). Vegetation is low, usually below 50 cm, covering 10–20% of the surface. A first-order drainage basin (5 ha), consisting of Turonian limestone (Kidron and Zohar, 2010; Kidron and Starinsky, 2012), and characterized by relatively steep slopes of up to 24° (for the mid NFS) and 31° (for the mid SFS) was chosen (Fig. 2d). A pair of plots, 2 2 m, was demarcated at the rock outcrops of each of the mid NFS and SFS, both of which were inhabited by distinct communities. While euendolithic cyanobacteria that actively penetrate into the upper 5–10 mm of the rock cover 88% of the bedrock at SFS (with bare surfaces with and without microcolonial fungi occupying the remaining area), epilithic lichens cover 86% of the
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Fig. 1. Location of research site.
bedrock at NFS with the remaining area occupied by endolithic lichens (7%) or cyanobacteria (7%). Temperatures were measured at the rock outcrops at each plot. In addition, in order to measure the actual rain reaching the slope, a small orifice rain gauge, 30 cm above ground, was installed next to each plot. Rain measurements took place following rain events with >1 mm of rain. Yet, due to technical difficulties, not all consecutive rain events, occurring within 1–3 days apart, were collected separately. Subsequently, the combined sum of the rain events was analyzed. Dew and fog were measured manually. Periodical measurements took place during 2008–2010. In order to avoid condensation due to distillation (i.e., vapor originating from the wet ground following rain) and ensure dew condensation which solely stems from atmospheric vapor (Monteith, 1957), dew measurements were carried out only when the ground was dry. Synthetic velvet-like 6 6 0.15 cm cloths (Universal company, Germany), directly attached to the rock surfaces with four adhesive stickers at their four corners, were used as a substrate for dew condensation. Passive absorbance of the atmospheric moisture by the lichens and the high correlation (with r2 = 0.88) obtained between cloths and lichen thalii (Ramalina maciformis (Del.) Nyl. which abound at the site), placed next to one another on rock substrates (with R. maciformis mimicking epilithic lichens) (Fig. 3) justified the use of cloths for the monitoring of atmospheric moisture. The cloths, attached in the afternoon, were collected
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a
0
b
5cm
c
0
5cm
0
5cm
d
NF
0
SF
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Fig. 2. Smooth-faced surfaces at the lichen-inhabiting bedrock at NFS (a), alternating elevated surfaces (ridges) and pits (b) and completely ragged microtopography (c) at the cyanobacteria-inhabiting bedrock at SFS and general view of the research site as photographed during the morning (note the shaded north-facing slope, NFS, and the sunexposed south-facing slope, SFS) (d).
0.5–1.0 h after sunrise on the following morning, when condensation was maximal (Kidron, 2005). The cloths were placed into preweighed flasks that were immediately sealed and then taken to a nearby lab at Sede Boqer, where they were weighed, oven dried at 70 °C, and then weighed again to determine their water content. Atmospheric moisture condensation was regarded as dew unless fog was visually observed. Fog was defined as vapor condensation in the air that limits visibility to <1 km lasting P0.5 h. We are aware of the fact that nighttime fogs were not always detected and therefore fogs on some nights may have been registered as dew. Irradiance and temperatures were measured during the late summer and fall of 2009. Irradiance was measured periodically with a LI-250 light meter (LI-COR, USA). Temperatures were measured between August and October 2009 in 20 min interval by means of a pair of calibrated thermistors that were attached to
the surface of the rock in each habitat (protected though from direct irradiance by 0.5 cm Polyurethane) and connected to Hobo (Onset Computer Corporation, MA, USA) mini data loggers. Surface temperatures were compared to the dew point temperature (Td) as measured at the Sede Boqer meteorological station, 1.5 km east of the research site. Two dozens samples, 1 cm2 each and approximately 1.0 cm thick, were randomly taken from each habitat at each aspect for chlorophyll a (CHLa) measurements. In addition, in order to study the cyanobacteria distribution at the ragged SFS, two 1 m-long transects were demarcated at each plot at SFS and 12 pairs of samples, one from a ridge and another from an adjacent groove were taken for CHLa measurements. All rock samples were immersed in water for 5 min to soften the substrate, and the top 10 mm of the rock was scraped using a sterile scalpel. CHLa 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). In order to study possible structural, textural and chemical differences, thin sections were prepared and rock samples were taken for microscopic examination by ESEM-EDS (Quanta 200, FEI Company, Oregon, USA). The microscope is equipped with a link 10000 energy dispersive X-ray spectrometry system which allows analysis without coating, taking advantage of the ESEM option to work in a low vacuum mode (1 torr). T-test and paired t-test (for dew and rain) were used in order to find significant differences (P < 0.05). 3. Results
Fig. 3. The relation between dew and fog that condense onto cloths and onto segments of R. maciformis thalii that were adjacently attached on different substrates.
Chlorophyll a content (CHLa) of both groups of lithobionts (cyanobacteria and lichens) showed significant differences. While CHLa reached an average of only 22.7 mg m2 at SFS, it was as high as 97.7 mg m2 at NFS (Fig. 4a). The high standard deviation of CHLa at SFS attested to high (at the pits) and low (at the ridges) concentration of the cyanobacterial cells (Fig. 4b), as clearly seen
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in Fig. 2b. This was also noted elsewhere (Garcia-Pichel, 2006) and verified by ESEM observations which disclosed numerous microtunnels at the grooved surfaces of SFS (Fig. 5a and b), but nevertheless absent from NFS (Fig. 5c). Tube regularity further attested to the biotic origin of the microtunnels (McLoughlin et al., 2010). No structural or textural differences were noted, either by the ESEM or by the thin sections (not shown), as also found elsewhere (Kidron, 2002). Similarly, rocks of both habitats exhibited almost identical chemical composition (Fig. 6), thus ruling out the possibility that structural, textural or chemical differences may account for the differences in population composition. Moreover, rain precipitation did not show any significant differences, with average rain amount per field measurement being 18.8 mm and 19.3 mm for NFS and SFS, respectively (N = 9). However, high variability in irradiance (with average of 1060 W m2 at SFS in comparison to only 598 W m2 at NFS; Fig. 7a) and consequently in the bedrock temperatures characterized both aspects. As a result of the higher irradiance, midday and nocturnal temperatures at SFS were consistently higher than that of NFS (Fig. 7b), as also indicated by the high variability in dew and fog amounts between these two sites (Fig. 7c). On average, maximal temperature of the bedrock at NFS was 32.4 °C, while being 45.8 °C at SFS (Fig. 8a). Higher nocturnal temperatures were consequently recorded at SFS throughout the night. Whereas average minimal temperature at dawn was 17.7 °C at NFS, it was 20.3 °C at SFS and up to 5.3 °C higher at SFS during certain nights. The great differences in nocturnal temperatures resulted in significant differences (P < 0.001) in dew and fog amounts between the slopes. While average dew and fog amounts yielded respectively 0.092 and 0.150 mm at NFS, it yielded only 0.022 and 0.030 mm at SFS (Fig. 8b). Even under fog conditions, the amount never exceeded 0.04 mm at SFS. This was the case at the SFS bedrock even during mornings with extreme precipitation during which maximal condensation at the hilltop (as measured by the cloth-plate method, CPM; see Kidron, 1998) substantially exceeded the mean precipitation recorded by the CPM of 0.21 mm (Kidron, 1999), reaching 0.35 (for dew) and 0.60 mm (for fog).
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a
b
c
Fig. 5. ESEM pictographs of the microtunnels at the surface of the bedrock of the south-facing slope (a and b) in comparison to the smooth bedrock subsurface of the north-facing slope (c). Bars equal 100 lm.
Fig. 4. Chlorophyll content at the south-facing slope, SFS and the north-facing slope, NFS (a) and at the ridges and pits at SFS (b). Bars represent one SD.
Fig. 9 shows the values received for 29 days during which dew condensation took place at the meteorological station. Minimal temperatures (Tmin) reached the dew-point temperature (Td) on 24 days at the NFS bedrock (implying possible condensation there for 24 days), and only for 4 days at the SFS bedrock. Yet, when the time duration during which Tmin remained below Td at the bedrocks of NFS and SFS was evaluated, it was on average 5.2 h (SD = 3.0) for NFS and only 0.4 h (SD = 0.2) for SFS.
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Ca
O C
SF NF Mg
Si
Ca
Fig. 6. The chemical composition of the north-facing (NF) and south-facing (SF) bedrocks. Note the almost perfect overlap of elements of both rocks.
Fig. 8. Average maximal (Tmax) and minimal (Tmin) temperatures (N = 63) (a) and average dew (N = 52) and fog (N = 9) amounts (b) at the bedrock of the south-facing slope (SFS) and the north-facing slope (NFS). Bars represent one SE.
4. Discussion
Fig. 7. Average daytime irradiance at north-facing slope (NFS) and the south-facing slope (SFS) based on 11 days of simultaneous measurements during September and October 2009 (a), average temperature cycle based on 33 days of consecutive measurements during August and September 2009 (b) and 17 days of simultaneous measurements of dew and fog (denoted by the letter F) (c). Bars represent one SE.
Rain could not have explained the differences in both populations. The current data were in agreement with rain measurements that took place during 2004–2008 (Kidron et al., 2011), during which average rain amounts at SFS and NFS were 14.2 and 13.6 mm, respectively (N = 28). The similar amounts received by both aspects were explained by the strong channeling effect of the west-east trending wadi (Weigel and Rotach, 2004), that distributed evenly the amounts of rain at both slopes. Significant differences were however monitored in the dew and fog amounts. The low dew and fog amounts received at the bedrocks of SFS were of special interest in light of the minimal dew value found necessary for net carbon assimilation by lichens of 20% of their dry weight, i.e., 0.03 mm (Lange, 1969). In contrast, cyanolichens or free-living cyanobacteria were found to require liquid water to
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Fig. 9. Dew amounts as measured during 29 dewy days at the meteorological station of Sede Boqer during August, September and October of 2009 (a) and the dew point temperature (Td, as measured at the meteorological station) and the minimum bedrock temperatures (Tmin) of the south-facing slope (SFS) and the north-facing slope (NFS) during these days (b).
perform net photosynthesis, which corresponds to 50% of the thallus’ water content of R. maciformis i.e., 0.1 mm (Lange et al., 1977, 1986). These thresholds of 0.03 mm and 0.1 mm (as further substantiated by Lange et al., 1992) were taken as minimal values for the performance of net photosynthesis for lichens (with green algae as photobiont) and cyanobacteria, respectively. Taking the above values as representative for thresholds of net carbon assimilation, our findings clearly indicate that the SFS habitat failed to meet these thresholds. In agreement with theoretical considerations which exclude a possibility of dew condensation once substrate temperature is higher than Td (Beysens, 1995, 2006), Fig. 9b highlights the unlikelihood for a meaningful dew condensation at SFS. Given an average condensation rate of 0.025 mm h1 (Kidron, 2000), the time duration during which Tmin remained below Td at the bedrock of SFS was substantially shorter than the time required to reach the 0.1 mm threshold necessary for the cyanobacteria’s net photosynthesis. It was also shorter than the time required to reach 0.03 mm necessary for net photosynthesis by the lichens. The data thus imply that bedrock surface temperatures at SFS are too high to allow condensation sufficiently above the required threshold for net carbon assimilation by either cyanobacteria or lichens. While substantial differences were found in water availability, differences in solar irradiance values which may be linked to UV radiation (Liakoura et al., 1997; Mosalam Shaltout et al., 1998; Krause et al., 2003), as well as differences in temperatures were ruled out as possible cause for the variability in species composition. Although attaining higher midday temperatures due to their small volume (Danin and Garty, 1983), cobbles in SFS are covered by lichens. Similarly, a lush community of epilithic lichens also covers the sun-exposed west-facing footslopes of Sede Boqer (Kidron et al., 2011), and the sun-exposed hilltops of Har Harif, approximately 40 km SSW of Sede Boqer. Due to its high altitude (1000 m above m.s.l), the Har Harif site may receive higher UV radiation than Sede Boqer (Kidron and Temina, 2013), leaving water availability as the primary driving force for the lithobiont’s distribution. The above conclusion may have important implications. Since liquid water was found necessary for cell turgidity and the activation of the photosynthetic apparatus of cyanobacteria (Lange et al., 1986), the amounts of water that condense at the SFS bedrock
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would not suffice for positive net photosynthesis either by lichens or cyanobacteria, implying that cyanobacteria, which prevail at the SFS bedrock, solely utilize rain for photosynthesis. One may thus conclude that in disagreement with previous assumptions (Friedmann and Galun, 1974), the cyanobacteria inhabiting the south-facing rock outcrops may solely rely on rain precipitation, and as such will experience a much narrower biotic window (sensu Williams and Hallsworth, 2009) than the lichens inhabiting the NFS bedrocks. Dew condensation which takes place at NFS thus facilitates lichen growth, a more complex life form with higher biomass. The data thus explain the distributional pattern of the lithobionts at the research site. Similarly to other research on vascular plants (Cutler et al., 2008; Richardson et al., 2012), it also highlights the importance of habitat heterogeneity in the spatial differentiation of rock-dwelling microorganisms. While rain amounts were too low to facilitate lush lichen growth at SFS (as also verified at other drainage basins in the Negev and in agreement with other reports stressing the xeric nature of cyanobacteria; see Büdel, 1999), lichen capability to use high relative humidity (which precede dew condensation) renders them an advantage over cyanobacteria which necessitate liquid water for growth. While surface temperatures at SFS are too high to facilitate high relative humidity and dew condensation, they were sufficiently low at NFS. Blocking the sun light, the epilithic lichens successfully outcompete the cyanobacteria at NFS. The cyanobacteria in turn are being confined to the bedrocks of SFS, where surface temperatures are too high to facilitate dew condensation and consequently lichen growth. Moreover, as can be seen in Fig. 7c, no surface wetting took place at SFS even during fogs. The transient nature and therefore short duration of the fog, coupled with the high surface temperatures did not facilitate surface wetting by fog, making rainwater the sole water source for the cyanobacteria at SFS. This was reflected in the chlorophyll content of the lithobionts. In agreement with soil-dwelling microorganisms (biocrusts) which showed a close link between water availability and crust biomass (Kidron et al., 2009), the substantially higher chlorophyll content of the lichens at NFS may reflect the additional source of water (dew and fog) at NFS. As a result, and in agreement with the fundamental role played by water availability to microorganisms (Hallsworth et al., 2003), a distinct population of lithobionts, with cyanobacteria at the SFS and lichens at the NFS, characterize the drainage basin. The findings highlight the high diversity in community structure, not only as a result of geography (Hodkinson et al., 2012; Janatková et al., 2013), topography (Zeleny´ et al., 2010) or disturbance (Le Roux et al., 2013a), but even within a small drainage basin of 5 hectares, and the importance of knowledge regarding microclimate variation, which are often ignored in large-scale models (Potter et al., 2013). The data may have important implications regarding the use of cyanobacteria as bio-indicators for dewless habitats within areas that receive dew precipitation (Lekouch et al., 2012; Hao et al., 2012). The data may also have important implications regarding global warming and past colonization of Earth. With anticipated temperature rise of 1.4–5.8 °C during the 21st century (Houghton et al., 2001), during which higher temperature increase is expected on land rather than the oceans (Hansen et al., 2006), and in line with the fact that nighttime temperatures exhibited the highest increase (Morak et al., 2011; Donat and Alexander, 2012; Martin et al., 2012; Min et al., 2013), a decrease in habitats subjected to dew condensation may result in a decrease in lichen cover and distribution, and subsequently in a decrease in biomass and C assimilation. Contrary to wetlands where temperature increase may result in biomass increase (Baldwin et al., 2013) and to tropical rainforest where the effects of moisture and temperatures are not strongly linked (Silva et al., 2013), our findings highlight the
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close link between temperature and moisture on lithobionts, and point to a possible substantial decrease in lichen distribution following nighttime temperature rise and its possible effect on dew condensation. And thus, in agreement with other publications (Le Roux et al., 2013b), increased temperatures may affect community composition and species richness, and may decrease organic matter production. Moreover, as found for biocrusts (Maestre et al., 2013), a decrease in lichen cover may also reduce CO2 sequestration, all leading to intensified aridization. The data may also have important implications for the colonization of early Earth and for soil forming processes. Although the current research focused on limestone, the physical processes during which cyanobacteria and lichens acquire their moistness (Rundel, 1988) allow us to apply the data to silicates and to a variety of climates. Since the mycobiont is responsible for most of the respiration and as warm conditions may largely restrict lichen expansion owing to the mycobiont nocturnal respiratory losses (Lange et al., 1994), cool conditions facilitate lichen expansion. We postulate that due to the extreme high (during midday) and low (during night) temperatures that characterized the mid Neoproterozoic (Pierrehumbert, 2005), nighttime condensation (of the high midday vapor content) took place, triggering in turn lichen expansion. With preferential growth on silicates (Barker and Banfield, 1996; Aghamiri and Schwartzman, 2002), and long nocturnal and diurnal activity (with >12 h of activity per dewy day; see Zangvil, 1996 as opposed to short wetness duration following rain; see Proctor and Tuba, 2002), a steady increase in lichen cover and activity may have taken place. With cool temperatures triggering eukaryote evolution (von Bloh et al., 2003), we postulate that the evolution of lichens may have triggered weathering, O2 production (Canfield, 2005; Sahoo et al., 2012) and CO2 sequestration (Boucot and Gray, 2001), yielding a positive feedback mechanism. Whereas the initial trigger for the Neoproterozoic cooling and glaciation is beyond the scope of the current research, our findings nevertheless point to the possible expansion of lichens upon cooling, i.e., conditions which facilitate nocturnal condensation of atmospheric moisture. This may have been triggered by the Rodinia breakup (which terminated long continental and therefore dry conditions, see Goddéris et al., 2003). Furthermore, following their high efficiency to scavenge phosphorus (Landeweert et al., 2001), lichens may have also overcome the main obstacle that apparently limited photosynthesis during the Neoproterozoic (Schidlowski, 1988), being responsible for the increase in the phosphorus supply to the Oceans. With potential weathering capability of up to three orders of magnitude higher than chemical weathering (Schwartzman and Volk, 1989), lichens may have triggered O2 production during the Neoproterozoic, an increase in 87Sr/86Sr and the gradual decrease of 13C/12C (Schidlowski, 1988; Horodyski and Knauth, 1994; Knauth and Kennedy, 2009; Pierrehumbert et al., 2011), all of which may attest to high phototosynthetic activity (Walter et al., 2000; Heckman et al., 2001; Fairchild and Kennedy, 2007). In agreement with other publications (Keller and Wood, 1993; Hoffman et al., 1998; Heckman et al., 2001; Hedges et al., 2001; Lenton and Watson, 2004; Boyle et al., 2007), our findings may support the biotic component for the CO2 decrease and O2 increase (rather than the abiotic component of glaciation, which is regarded as a possible mechanism explaining high weathering rates in the Neoproterozoic; see Canfield et al., 2007) and the 13C/12C decrease (rather than the suggested mechanism of methane release; see Schrag et al., 2002). Possible extended condensation and subsequently lichen expansion may also explain intensive silicate weathering leading to a gradual increase in phosphorous (Planavsky et al., 2010) already prior to glaciation, and the lack of an abrupt increase of O2 (and subsequent decrease in CO2) following the appearance of the first plants – 420 Myr (Boucot and
Gray, 2001; Lenton and Watson, 2004). Supporting recent publications which ascribe a more ancient origin for fungi and lichens (Butterfield, 2005; Honegger et al., 2013), our findings may also explain the presence of well developed soils prior to the evolution of the first plants (Wright, 1985). In agreement with data regarding lichen distribution in tropical climates (Wolseley and Aguirre-Hudson, 1997), biocrusts in deserts (Kidron et al., 2009; Kidron and Benenson, 2014), cryptogam communities at the Andean (Kessler, 2000), or plant distribution in alpine environment (Scherrer and Körner, 2011), our data highlights the role played by temperature and subsequently by water availability in the distribution of the rock-dwelling cyanobacteria and lichens. A clear distinction between two sources of water (rain versus dew and fog) and their variable contribution to these groups of microorganisms is made. Cyanobacteria may thus serve as biomarkers for dewless habitats within a dew desert such as the Negev. We argue that the close link between temperature and water availability on the one hand and community composition on the other hand is crucial for the understanding of present-day ecology. It is also crucial for understanding future as well as past ecological and geochemical processes. 5. Conclusions Hypothesizing that abiotic conditions determine the spatial distribution of lithic cyanobacteria and lichens in the Negev Desert, radiation, temperature, rain, dew and fog were measured on bedrocks at the south-facing slope (SFS) and north-facing slope (NFS) of a first order drainage basin, inhabited by cyanobacteria (at SFS) and lichens (at NFS). While non-significant differences characterized the rain amounts, substantial differences characterized the substrate temperatures and subsequently the amounts of dew and fog. While condensing at NFS, dew point temperatures were seldom attained at SFS, therefore averting dew and fog condensation. In disagreement with common belief, cyanobacteria were found to be confined to dewless habitats within the dewy Negev highlands and as such relying solely on rainwater for growth. Alternatively, addition of water by dew and fog at NFS allowed for lichen establishment and growth. These findings may have broad implications as they may facilitate the use of cyanobacteria as biomarkers for dewless habitats within a dew desert such as the Negev, increase our understanding regarding lithobiont distribution and the abiotic conditions on Mars (Hofmann et al., 2008), and allows us to assess the possible outcome of global warming upon lichen expansion. Moreover, the findings may have important implications also regarding early Earth colonization. Since cool nighttime conditions trigger dew condensation, extreme high (during midday) and low (during night) temperatures that characterized the mid Neoproterozoic may have promoted lichen expansion, which triggered in turn weathering and subsequently CO2 sequestration. We propose that lichen expansion and activity following cooling may explain the high O2 production, the increase in 87Sr/86Sr and the gradual decrease of 13C/12C already prior to the Neoproterozoic glaciation, and may explain the presence of well developed soils prior to the evolution of the first plants. Acknowledgments The research was supported by grant 1358/04 of the Israel Science Foundation (ISF). We wish to thank Avinoam Danin for his support in the early stages of the research, Shimon Y. Tal for his valuable technical advice, Evgenia Blayvas for the ESEM-EDS analysis, and Carol A. Kidron for the editing. The very valuable comments provided by two anonymous reviewers are highly appreciated.
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Cyanobacteria are confined to dewless habitats within a dew desert: Implications for past and future climate change for lithic microorganisms Giora J. Kidron ⇑, Abraham Starinsky, Dan H. Yaalon 1 Institute of Earth Sciences, The Hebrew University, Jerusalem 91904, Israel
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Article history: Received 19 March 2014 Received in revised form 18 August 2014 Accepted 2 November 2014 Available online 12 November 2014 This manuscript was handled by Laurent Charlet, Editor-in-Chief, with the assistance of Rizlan Bernier-Latmani, Associate Editor Keywords: Colonization Cyanobacteria Dew Lichens Negev Neoproterozoic
s u m m a r y Although covering almost all rock outcrops around the world, little is known regarding the factors that govern the spatial distribution of lithic cyanobacteria and lichens. This is also the case in the Negev Desert, where cyanobacteria predominate on the rock outcrops of the south-facing slopes and lichens on the rock outcrops of the north-facing slopes. Hypothesizing that abiotic conditions determine their distribution, radiation, temperature, rain, dew and fog were monitored over a two-year period (2008– 2010) at cyanobacteria- and lichen-dwelling habitats within a first-order drainage basin in the Negev Highlands. While non-significant differences characterized the rain amounts, substantial differences in substrate temperatures were recorded which resulted in turn in fundamental differences in the non-rainfall water regime. While dew condensed at the rock outcrops of the lichen habitat, no condensation took place at the cyanobacteria habitat. Contrary to the common belief, cyanobacteria were found to inhabit dewless habitats. As a result, cyanobacteria solely rely on rain precipitation for growth and can therefore serve as bioindicators for dewless habitats within the dewy Negev Desert. The findings may have important implications regarding Earth colonization, soil forming processes and geochemical processes following climate warming. They may explain lichen expansion and subsequent O2 increase during the mid Neoproterozoic providing indirect support for substantial photosynthetic activity and high weathering rates during this era. Ó 2014 Elsevier B.V. All rights reserved.
1. Introduction As photoautotrophs, cyanobacteria and lichens (a symbiotic association between a photobiont and a mycobiont) are of outmost importance to primary production. Inhabiting the most harsh and extreme habitats, and almost all rocky substrates (Chen et al., 2000), they are primary producers of organic C and N (Evans and Lange, 2001). As such, their importance goes back to early Earth colonization, where both groups provided most of the primary production (Altermann et al., 2006; Yuan et al., 2005; Guo et al., 2011). They are also known for their high weathering capabilities (Schwartzman and Volk, 1989; Aghamiri and Schwartzman, 2002), therefore fulfilling an important role in soil formation (Wright, 1985). Both microorganisms are widely distributed. Lithic cyanobacteria and lichens occupy all continents. They abound around the ⇑ Corresponding author. Tel.: +972 544 967271; fax: +972 2 566 2581. E-mail addresses: [email protected] (G.J. Kidron), [email protected] (A. Starinsky), [email protected] (D.H. Yaalon). 1 Regrettably, Dan passed away during the preparation of the ms. http://dx.doi.org/10.1016/j.jhydrol.2014.11.010 0022-1694/Ó 2014 Elsevier B.V. All rights reserved.
Mediterranean Sea (Albertano and Urzi, 1999; de los Rios and Ascaso, 2005), Europe (Sigler et al., 2003), North America (Gerrath et al., 2000), South America, Africa, and Australia (Büdel, 1999), the Arctic (Cockell et al., 2003) and Antarctica (WynnWilliams et al., 1999; Casanovas et al., 2013). In light of the growing amount of evidence of past and possible present Martian life (Schulze-Makuch et al., 2005, 2008), and ongoing efforts to identify reliable biomarkers for Martian life (Jehlicˇka et al., 2009), such as microtunnels (Fisk et al., 2006), knowledge regarding the abiotic conditions necessary for cyanobacteria and lichen growth on Earth is essential for identifying comparable conditions on Mars. Although regarded as an extreme desert (with a mean annual precipitation of 90 mm), lithobiontic microorganisms including cyanobacteria and lichens occupy the bedrock of the Negev Desert Highlands, such as at Sede Boqer and Avdat (Fig. 1), subjected to extensive research (Lange et al., 1970; Danin and Garty, 1983). With epilithic lichens dwelling on top of the surface and with cyanobacteria occupying the upper several millimeters of the surface (triggering rock weathering and the subsequent formation of pits and tunnels) they render the surface a different appearance. While
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epilithic lichens (with green algae as photobionts such as Caloplaca aurantia (Pers.) Hellb., Aspicilia farinosa (Flörke) Arnold, and Lecanora albescens (Hoffm.) Branth and Rostr. predominating) (Fig. 2a) render the north-facing slopes (NFS) smooth, cyanobacteria (with the genus Gleocapsa predominating, see Friedmann and Galun, 1974; Danin and Garty, 1983; Kidron et al., 2011), occupying the south-facing slope (SFS), render the surface uneven, with a ragged, pit-like microtopography (Fig. 2b and c). The current view maintains that water provided by rain and dew is the driving force behind the growth of the cyanobacteria (Friedmann and Galun, 1974; Smith et al., 2000; but see also Danin and Garty, 1983 that report no dew condensation during two nights of measurements). In a dew desert with annual average dew and fog precipitation of 33 mm falling during 195 days a year, dew was assumed to be the major water source for these lithobionts (Friedmann and Galun, 1974). While lichen activity following high relative humidity and dew condensation (vapor condensation at the substrate surface) as well as fog precipitation (i.e., substrate wetting by water droplets that condensed in the air) was monitored (Lange et al., 1970), no such data were provided for the cyanobacteria and no explanation for the confinement of the cyanobacteria to the bedrocks of SFS was offered. Furthermore, as part of a larger project (Kidron, 1999), temperature measurements took place at different substrates along a north–south gradient of the Negev Desert. Temperatures of cyanobacteria-inhabited bedrocks were found to be consistently warmer by at least 3–4 °C than lichen-inhabited bedrocks, bringing about the notion that the cyanobacteria-inhabited bedrocks are subjected to much lower dew condensation. Hypothesizing that the confinement of the cyanobacteria to SFS may stem from microclimatological variables and that understanding these microclimatological conditions may explain past colonization conditions, the goal of the current research was to monitor the abiotic variables at the cyanobacteria and the lichen habitats. Towards this goal, irradiance, temperatures, rain, dew and fog were measured. Mornings with high relative humidity only were not monitored despite the fact that high relative humidity is also utilized by most lichens (Lange et al., 1986). Nevertheless, since high relative humidity culminates in dew condensation for over 90% of the nights (Kappen et al., 1979), its contribution may largely be seen reflected in the amounts of dew and fog. As for the research location, it was confined to a single drainage basin thus avoiding the introduction of multiple variables that may affect the results, such as cloudiness and lithology.
2. Methods The research site is located in Sede Boqer in the Negev Desert Highlands, Israel (34°460 E, 30°560 N), approximately 500 m above sea level (Fig. 1). Mean annual rain precipitation is 95 mm, limited to the winter months (November–April)). Average annual temperature is 17.9 °C; it is 24.7 °C during the hottest month of July and 9.3 °C during the coldest month of January (Bitan and Rubin, 1991). Annual potential evaporation is 2600 mm (Evenari, 1981). Vegetation is low, usually below 50 cm, covering 10–20% of the surface. A first-order drainage basin (5 ha), consisting of Turonian limestone (Kidron and Zohar, 2010; Kidron and Starinsky, 2012), and characterized by relatively steep slopes of up to 24° (for the mid NFS) and 31° (for the mid SFS) was chosen (Fig. 2d). A pair of plots, 2 2 m, was demarcated at the rock outcrops of each of the mid NFS and SFS, both of which were inhabited by distinct communities. While euendolithic cyanobacteria that actively penetrate into the upper 5–10 mm of the rock cover 88% of the bedrock at SFS (with bare surfaces with and without microcolonial fungi occupying the remaining area), epilithic lichens cover 86% of the
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Fig. 1. Location of research site.
bedrock at NFS with the remaining area occupied by endolithic lichens (7%) or cyanobacteria (7%). Temperatures were measured at the rock outcrops at each plot. In addition, in order to measure the actual rain reaching the slope, a small orifice rain gauge, 30 cm above ground, was installed next to each plot. Rain measurements took place following rain events with >1 mm of rain. Yet, due to technical difficulties, not all consecutive rain events, occurring within 1–3 days apart, were collected separately. Subsequently, the combined sum of the rain events was analyzed. Dew and fog were measured manually. Periodical measurements took place during 2008–2010. In order to avoid condensation due to distillation (i.e., vapor originating from the wet ground following rain) and ensure dew condensation which solely stems from atmospheric vapor (Monteith, 1957), dew measurements were carried out only when the ground was dry. Synthetic velvet-like 6 6 0.15 cm cloths (Universal company, Germany), directly attached to the rock surfaces with four adhesive stickers at their four corners, were used as a substrate for dew condensation. Passive absorbance of the atmospheric moisture by the lichens and the high correlation (with r2 = 0.88) obtained between cloths and lichen thalii (Ramalina maciformis (Del.) Nyl. which abound at the site), placed next to one another on rock substrates (with R. maciformis mimicking epilithic lichens) (Fig. 3) justified the use of cloths for the monitoring of atmospheric moisture. The cloths, attached in the afternoon, were collected
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a
0
b
5cm
c
0
5cm
0
5cm
d
NF
0
SF
50m
Fig. 2. Smooth-faced surfaces at the lichen-inhabiting bedrock at NFS (a), alternating elevated surfaces (ridges) and pits (b) and completely ragged microtopography (c) at the cyanobacteria-inhabiting bedrock at SFS and general view of the research site as photographed during the morning (note the shaded north-facing slope, NFS, and the sunexposed south-facing slope, SFS) (d).
0.5–1.0 h after sunrise on the following morning, when condensation was maximal (Kidron, 2005). The cloths were placed into preweighed flasks that were immediately sealed and then taken to a nearby lab at Sede Boqer, where they were weighed, oven dried at 70 °C, and then weighed again to determine their water content. Atmospheric moisture condensation was regarded as dew unless fog was visually observed. Fog was defined as vapor condensation in the air that limits visibility to <1 km lasting P0.5 h. We are aware of the fact that nighttime fogs were not always detected and therefore fogs on some nights may have been registered as dew. Irradiance and temperatures were measured during the late summer and fall of 2009. Irradiance was measured periodically with a LI-250 light meter (LI-COR, USA). Temperatures were measured between August and October 2009 in 20 min interval by means of a pair of calibrated thermistors that were attached to
the surface of the rock in each habitat (protected though from direct irradiance by 0.5 cm Polyurethane) and connected to Hobo (Onset Computer Corporation, MA, USA) mini data loggers. Surface temperatures were compared to the dew point temperature (Td) as measured at the Sede Boqer meteorological station, 1.5 km east of the research site. Two dozens samples, 1 cm2 each and approximately 1.0 cm thick, were randomly taken from each habitat at each aspect for chlorophyll a (CHLa) measurements. In addition, in order to study the cyanobacteria distribution at the ragged SFS, two 1 m-long transects were demarcated at each plot at SFS and 12 pairs of samples, one from a ridge and another from an adjacent groove were taken for CHLa measurements. All rock samples were immersed in water for 5 min to soften the substrate, and the top 10 mm of the rock was scraped using a sterile scalpel. CHLa 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). In order to study possible structural, textural and chemical differences, thin sections were prepared and rock samples were taken for microscopic examination by ESEM-EDS (Quanta 200, FEI Company, Oregon, USA). The microscope is equipped with a link 10000 energy dispersive X-ray spectrometry system which allows analysis without coating, taking advantage of the ESEM option to work in a low vacuum mode (1 torr). T-test and paired t-test (for dew and rain) were used in order to find significant differences (P < 0.05). 3. Results
Fig. 3. The relation between dew and fog that condense onto cloths and onto segments of R. maciformis thalii that were adjacently attached on different substrates.
Chlorophyll a content (CHLa) of both groups of lithobionts (cyanobacteria and lichens) showed significant differences. While CHLa reached an average of only 22.7 mg m2 at SFS, it was as high as 97.7 mg m2 at NFS (Fig. 4a). The high standard deviation of CHLa at SFS attested to high (at the pits) and low (at the ridges) concentration of the cyanobacterial cells (Fig. 4b), as clearly seen
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in Fig. 2b. This was also noted elsewhere (Garcia-Pichel, 2006) and verified by ESEM observations which disclosed numerous microtunnels at the grooved surfaces of SFS (Fig. 5a and b), but nevertheless absent from NFS (Fig. 5c). Tube regularity further attested to the biotic origin of the microtunnels (McLoughlin et al., 2010). No structural or textural differences were noted, either by the ESEM or by the thin sections (not shown), as also found elsewhere (Kidron, 2002). Similarly, rocks of both habitats exhibited almost identical chemical composition (Fig. 6), thus ruling out the possibility that structural, textural or chemical differences may account for the differences in population composition. Moreover, rain precipitation did not show any significant differences, with average rain amount per field measurement being 18.8 mm and 19.3 mm for NFS and SFS, respectively (N = 9). However, high variability in irradiance (with average of 1060 W m2 at SFS in comparison to only 598 W m2 at NFS; Fig. 7a) and consequently in the bedrock temperatures characterized both aspects. As a result of the higher irradiance, midday and nocturnal temperatures at SFS were consistently higher than that of NFS (Fig. 7b), as also indicated by the high variability in dew and fog amounts between these two sites (Fig. 7c). On average, maximal temperature of the bedrock at NFS was 32.4 °C, while being 45.8 °C at SFS (Fig. 8a). Higher nocturnal temperatures were consequently recorded at SFS throughout the night. Whereas average minimal temperature at dawn was 17.7 °C at NFS, it was 20.3 °C at SFS and up to 5.3 °C higher at SFS during certain nights. The great differences in nocturnal temperatures resulted in significant differences (P < 0.001) in dew and fog amounts between the slopes. While average dew and fog amounts yielded respectively 0.092 and 0.150 mm at NFS, it yielded only 0.022 and 0.030 mm at SFS (Fig. 8b). Even under fog conditions, the amount never exceeded 0.04 mm at SFS. This was the case at the SFS bedrock even during mornings with extreme precipitation during which maximal condensation at the hilltop (as measured by the cloth-plate method, CPM; see Kidron, 1998) substantially exceeded the mean precipitation recorded by the CPM of 0.21 mm (Kidron, 1999), reaching 0.35 (for dew) and 0.60 mm (for fog).
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a
b
c
Fig. 5. ESEM pictographs of the microtunnels at the surface of the bedrock of the south-facing slope (a and b) in comparison to the smooth bedrock subsurface of the north-facing slope (c). Bars equal 100 lm.
Fig. 4. Chlorophyll content at the south-facing slope, SFS and the north-facing slope, NFS (a) and at the ridges and pits at SFS (b). Bars represent one SD.
Fig. 9 shows the values received for 29 days during which dew condensation took place at the meteorological station. Minimal temperatures (Tmin) reached the dew-point temperature (Td) on 24 days at the NFS bedrock (implying possible condensation there for 24 days), and only for 4 days at the SFS bedrock. Yet, when the time duration during which Tmin remained below Td at the bedrocks of NFS and SFS was evaluated, it was on average 5.2 h (SD = 3.0) for NFS and only 0.4 h (SD = 0.2) for SFS.
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Ca
O C
SF NF Mg
Si
Ca
Fig. 6. The chemical composition of the north-facing (NF) and south-facing (SF) bedrocks. Note the almost perfect overlap of elements of both rocks.
Fig. 8. Average maximal (Tmax) and minimal (Tmin) temperatures (N = 63) (a) and average dew (N = 52) and fog (N = 9) amounts (b) at the bedrock of the south-facing slope (SFS) and the north-facing slope (NFS). Bars represent one SE.
4. Discussion
Fig. 7. Average daytime irradiance at north-facing slope (NFS) and the south-facing slope (SFS) based on 11 days of simultaneous measurements during September and October 2009 (a), average temperature cycle based on 33 days of consecutive measurements during August and September 2009 (b) and 17 days of simultaneous measurements of dew and fog (denoted by the letter F) (c). Bars represent one SE.
Rain could not have explained the differences in both populations. The current data were in agreement with rain measurements that took place during 2004–2008 (Kidron et al., 2011), during which average rain amounts at SFS and NFS were 14.2 and 13.6 mm, respectively (N = 28). The similar amounts received by both aspects were explained by the strong channeling effect of the west-east trending wadi (Weigel and Rotach, 2004), that distributed evenly the amounts of rain at both slopes. Significant differences were however monitored in the dew and fog amounts. The low dew and fog amounts received at the bedrocks of SFS were of special interest in light of the minimal dew value found necessary for net carbon assimilation by lichens of 20% of their dry weight, i.e., 0.03 mm (Lange, 1969). In contrast, cyanolichens or free-living cyanobacteria were found to require liquid water to
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Fig. 9. Dew amounts as measured during 29 dewy days at the meteorological station of Sede Boqer during August, September and October of 2009 (a) and the dew point temperature (Td, as measured at the meteorological station) and the minimum bedrock temperatures (Tmin) of the south-facing slope (SFS) and the north-facing slope (NFS) during these days (b).
perform net photosynthesis, which corresponds to 50% of the thallus’ water content of R. maciformis i.e., 0.1 mm (Lange et al., 1977, 1986). These thresholds of 0.03 mm and 0.1 mm (as further substantiated by Lange et al., 1992) were taken as minimal values for the performance of net photosynthesis for lichens (with green algae as photobiont) and cyanobacteria, respectively. Taking the above values as representative for thresholds of net carbon assimilation, our findings clearly indicate that the SFS habitat failed to meet these thresholds. In agreement with theoretical considerations which exclude a possibility of dew condensation once substrate temperature is higher than Td (Beysens, 1995, 2006), Fig. 9b highlights the unlikelihood for a meaningful dew condensation at SFS. Given an average condensation rate of 0.025 mm h1 (Kidron, 2000), the time duration during which Tmin remained below Td at the bedrock of SFS was substantially shorter than the time required to reach the 0.1 mm threshold necessary for the cyanobacteria’s net photosynthesis. It was also shorter than the time required to reach 0.03 mm necessary for net photosynthesis by the lichens. The data thus imply that bedrock surface temperatures at SFS are too high to allow condensation sufficiently above the required threshold for net carbon assimilation by either cyanobacteria or lichens. While substantial differences were found in water availability, differences in solar irradiance values which may be linked to UV radiation (Liakoura et al., 1997; Mosalam Shaltout et al., 1998; Krause et al., 2003), as well as differences in temperatures were ruled out as possible cause for the variability in species composition. Although attaining higher midday temperatures due to their small volume (Danin and Garty, 1983), cobbles in SFS are covered by lichens. Similarly, a lush community of epilithic lichens also covers the sun-exposed west-facing footslopes of Sede Boqer (Kidron et al., 2011), and the sun-exposed hilltops of Har Harif, approximately 40 km SSW of Sede Boqer. Due to its high altitude (1000 m above m.s.l), the Har Harif site may receive higher UV radiation than Sede Boqer (Kidron and Temina, 2013), leaving water availability as the primary driving force for the lithobiont’s distribution. The above conclusion may have important implications. Since liquid water was found necessary for cell turgidity and the activation of the photosynthetic apparatus of cyanobacteria (Lange et al., 1986), the amounts of water that condense at the SFS bedrock
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would not suffice for positive net photosynthesis either by lichens or cyanobacteria, implying that cyanobacteria, which prevail at the SFS bedrock, solely utilize rain for photosynthesis. One may thus conclude that in disagreement with previous assumptions (Friedmann and Galun, 1974), the cyanobacteria inhabiting the south-facing rock outcrops may solely rely on rain precipitation, and as such will experience a much narrower biotic window (sensu Williams and Hallsworth, 2009) than the lichens inhabiting the NFS bedrocks. Dew condensation which takes place at NFS thus facilitates lichen growth, a more complex life form with higher biomass. The data thus explain the distributional pattern of the lithobionts at the research site. Similarly to other research on vascular plants (Cutler et al., 2008; Richardson et al., 2012), it also highlights the importance of habitat heterogeneity in the spatial differentiation of rock-dwelling microorganisms. While rain amounts were too low to facilitate lush lichen growth at SFS (as also verified at other drainage basins in the Negev and in agreement with other reports stressing the xeric nature of cyanobacteria; see Büdel, 1999), lichen capability to use high relative humidity (which precede dew condensation) renders them an advantage over cyanobacteria which necessitate liquid water for growth. While surface temperatures at SFS are too high to facilitate high relative humidity and dew condensation, they were sufficiently low at NFS. Blocking the sun light, the epilithic lichens successfully outcompete the cyanobacteria at NFS. The cyanobacteria in turn are being confined to the bedrocks of SFS, where surface temperatures are too high to facilitate dew condensation and consequently lichen growth. Moreover, as can be seen in Fig. 7c, no surface wetting took place at SFS even during fogs. The transient nature and therefore short duration of the fog, coupled with the high surface temperatures did not facilitate surface wetting by fog, making rainwater the sole water source for the cyanobacteria at SFS. This was reflected in the chlorophyll content of the lithobionts. In agreement with soil-dwelling microorganisms (biocrusts) which showed a close link between water availability and crust biomass (Kidron et al., 2009), the substantially higher chlorophyll content of the lichens at NFS may reflect the additional source of water (dew and fog) at NFS. As a result, and in agreement with the fundamental role played by water availability to microorganisms (Hallsworth et al., 2003), a distinct population of lithobionts, with cyanobacteria at the SFS and lichens at the NFS, characterize the drainage basin. The findings highlight the high diversity in community structure, not only as a result of geography (Hodkinson et al., 2012; Janatková et al., 2013), topography (Zeleny´ et al., 2010) or disturbance (Le Roux et al., 2013a), but even within a small drainage basin of 5 hectares, and the importance of knowledge regarding microclimate variation, which are often ignored in large-scale models (Potter et al., 2013). The data may have important implications regarding the use of cyanobacteria as bio-indicators for dewless habitats within areas that receive dew precipitation (Lekouch et al., 2012; Hao et al., 2012). The data may also have important implications regarding global warming and past colonization of Earth. With anticipated temperature rise of 1.4–5.8 °C during the 21st century (Houghton et al., 2001), during which higher temperature increase is expected on land rather than the oceans (Hansen et al., 2006), and in line with the fact that nighttime temperatures exhibited the highest increase (Morak et al., 2011; Donat and Alexander, 2012; Martin et al., 2012; Min et al., 2013), a decrease in habitats subjected to dew condensation may result in a decrease in lichen cover and distribution, and subsequently in a decrease in biomass and C assimilation. Contrary to wetlands where temperature increase may result in biomass increase (Baldwin et al., 2013) and to tropical rainforest where the effects of moisture and temperatures are not strongly linked (Silva et al., 2013), our findings highlight the
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close link between temperature and moisture on lithobionts, and point to a possible substantial decrease in lichen distribution following nighttime temperature rise and its possible effect on dew condensation. And thus, in agreement with other publications (Le Roux et al., 2013b), increased temperatures may affect community composition and species richness, and may decrease organic matter production. Moreover, as found for biocrusts (Maestre et al., 2013), a decrease in lichen cover may also reduce CO2 sequestration, all leading to intensified aridization. The data may also have important implications for the colonization of early Earth and for soil forming processes. Although the current research focused on limestone, the physical processes during which cyanobacteria and lichens acquire their moistness (Rundel, 1988) allow us to apply the data to silicates and to a variety of climates. Since the mycobiont is responsible for most of the respiration and as warm conditions may largely restrict lichen expansion owing to the mycobiont nocturnal respiratory losses (Lange et al., 1994), cool conditions facilitate lichen expansion. We postulate that due to the extreme high (during midday) and low (during night) temperatures that characterized the mid Neoproterozoic (Pierrehumbert, 2005), nighttime condensation (of the high midday vapor content) took place, triggering in turn lichen expansion. With preferential growth on silicates (Barker and Banfield, 1996; Aghamiri and Schwartzman, 2002), and long nocturnal and diurnal activity (with >12 h of activity per dewy day; see Zangvil, 1996 as opposed to short wetness duration following rain; see Proctor and Tuba, 2002), a steady increase in lichen cover and activity may have taken place. With cool temperatures triggering eukaryote evolution (von Bloh et al., 2003), we postulate that the evolution of lichens may have triggered weathering, O2 production (Canfield, 2005; Sahoo et al., 2012) and CO2 sequestration (Boucot and Gray, 2001), yielding a positive feedback mechanism. Whereas the initial trigger for the Neoproterozoic cooling and glaciation is beyond the scope of the current research, our findings nevertheless point to the possible expansion of lichens upon cooling, i.e., conditions which facilitate nocturnal condensation of atmospheric moisture. This may have been triggered by the Rodinia breakup (which terminated long continental and therefore dry conditions, see Goddéris et al., 2003). Furthermore, following their high efficiency to scavenge phosphorus (Landeweert et al., 2001), lichens may have also overcome the main obstacle that apparently limited photosynthesis during the Neoproterozoic (Schidlowski, 1988), being responsible for the increase in the phosphorus supply to the Oceans. With potential weathering capability of up to three orders of magnitude higher than chemical weathering (Schwartzman and Volk, 1989), lichens may have triggered O2 production during the Neoproterozoic, an increase in 87Sr/86Sr and the gradual decrease of 13C/12C (Schidlowski, 1988; Horodyski and Knauth, 1994; Knauth and Kennedy, 2009; Pierrehumbert et al., 2011), all of which may attest to high phototosynthetic activity (Walter et al., 2000; Heckman et al., 2001; Fairchild and Kennedy, 2007). In agreement with other publications (Keller and Wood, 1993; Hoffman et al., 1998; Heckman et al., 2001; Hedges et al., 2001; Lenton and Watson, 2004; Boyle et al., 2007), our findings may support the biotic component for the CO2 decrease and O2 increase (rather than the abiotic component of glaciation, which is regarded as a possible mechanism explaining high weathering rates in the Neoproterozoic; see Canfield et al., 2007) and the 13C/12C decrease (rather than the suggested mechanism of methane release; see Schrag et al., 2002). Possible extended condensation and subsequently lichen expansion may also explain intensive silicate weathering leading to a gradual increase in phosphorous (Planavsky et al., 2010) already prior to glaciation, and the lack of an abrupt increase of O2 (and subsequent decrease in CO2) following the appearance of the first plants – 420 Myr (Boucot and
Gray, 2001; Lenton and Watson, 2004). Supporting recent publications which ascribe a more ancient origin for fungi and lichens (Butterfield, 2005; Honegger et al., 2013), our findings may also explain the presence of well developed soils prior to the evolution of the first plants (Wright, 1985). In agreement with data regarding lichen distribution in tropical climates (Wolseley and Aguirre-Hudson, 1997), biocrusts in deserts (Kidron et al., 2009; Kidron and Benenson, 2014), cryptogam communities at the Andean (Kessler, 2000), or plant distribution in alpine environment (Scherrer and Körner, 2011), our data highlights the role played by temperature and subsequently by water availability in the distribution of the rock-dwelling cyanobacteria and lichens. A clear distinction between two sources of water (rain versus dew and fog) and their variable contribution to these groups of microorganisms is made. Cyanobacteria may thus serve as biomarkers for dewless habitats within a dew desert such as the Negev. We argue that the close link between temperature and water availability on the one hand and community composition on the other hand is crucial for the understanding of present-day ecology. It is also crucial for understanding future as well as past ecological and geochemical processes. 5. Conclusions Hypothesizing that abiotic conditions determine the spatial distribution of lithic cyanobacteria and lichens in the Negev Desert, radiation, temperature, rain, dew and fog were measured on bedrocks at the south-facing slope (SFS) and north-facing slope (NFS) of a first order drainage basin, inhabited by cyanobacteria (at SFS) and lichens (at NFS). While non-significant differences characterized the rain amounts, substantial differences characterized the substrate temperatures and subsequently the amounts of dew and fog. While condensing at NFS, dew point temperatures were seldom attained at SFS, therefore averting dew and fog condensation. In disagreement with common belief, cyanobacteria were found to be confined to dewless habitats within the dewy Negev highlands and as such relying solely on rainwater for growth. Alternatively, addition of water by dew and fog at NFS allowed for lichen establishment and growth. These findings may have broad implications as they may facilitate the use of cyanobacteria as biomarkers for dewless habitats within a dew desert such as the Negev, increase our understanding regarding lithobiont distribution and the abiotic conditions on Mars (Hofmann et al., 2008), and allows us to assess the possible outcome of global warming upon lichen expansion. Moreover, the findings may have important implications also regarding early Earth colonization. Since cool nighttime conditions trigger dew condensation, extreme high (during midday) and low (during night) temperatures that characterized the mid Neoproterozoic may have promoted lichen expansion, which triggered in turn weathering and subsequently CO2 sequestration. We propose that lichen expansion and activity following cooling may explain the high O2 production, the increase in 87Sr/86Sr and the gradual decrease of 13C/12C already prior to the Neoproterozoic glaciation, and may explain the presence of well developed soils prior to the evolution of the first plants. Acknowledgments The research was supported by grant 1358/04 of the Israel Science Foundation (ISF). We wish to thank Avinoam Danin for his support in the early stages of the research, Shimon Y. Tal for his valuable technical advice, Evgenia Blayvas for the ESEM-EDS analysis, and Carol A. Kidron for the editing. The very valuable comments provided by two anonymous reviewers are highly appreciated.
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