This article was downloaded by: [University of Haifa Library]On: 12 February 2013, At: 08:48Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK

Geomicrobiology JournalPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/ugmb20

The Effect of Dew and Fog on Lithic Lichens Along anAltitudinal Gradient in the Negev DesertGiora J. Kidron a & Marina Temina ba Institute of Earth Sciences, The Hebrew University, Jerusalem, Israelb Institute of Evolution, University of Haifa, Mount Carmel, Haifa, IsraelAccepted author version posted online: 21 May 2012.Version of record first published: 08Feb 2013.

To cite this article: Giora J. Kidron & Marina Temina (2013): The Effect of Dew and Fog on Lithic Lichens Along an AltitudinalGradient in the Negev Desert, Geomicrobiology Journal, 30:4, 281-290

To link to this article: http://dx.doi.org/10.1080/01490451.2012.672542

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form toanyone is expressly forbidden.

The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses shouldbe independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims,proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly inconnection with or arising out of the use of this material.

Geomicrobiology Journal (2013) 30, 281–290Copyright C© Taylor & Francis Group, LLCISSN: 0149-0451 print / 1521-0529 onlineDOI: 10.1080/01490451.2012.672542

The Effect of Dew and Fog on Lithic Lichens Alongan Altitudinal Gradient in the Negev Desert

GIORA J. KIDRON1∗ and MARINA TEMINA2

1Institute of Earth Sciences, The Hebrew University, Jerusalem, Israel2Institute of Evolution, University of Haifa, Mount Carmel, Haifa, Israel

Received October 2011, Accepted February 2012

The effect of dew upon lichen communities was studied in three sites along an altitudinal gradient in the Negev Desert. The sites[Nizzana, NIZ (250m a.s.l), Sede Boqer, SB (530m a.s.l.) and Har Harif, HH (990m a.s.l.)] have similar rain precipitation (∼100 mm)but different dew precipitation of 0.11, 0.21 and 0.32 mm, respectively. A clear gradient was found for the chlorophyll content withNIZ (38.6 mg m−2)<SB (52.6 mg m−2)<HH (71.3 mg m−2), and the epilithic growth form with NIZ (1.4%) < SB (4.3%) � HH(53.6%) highlighting the fundamental role played by dew in dictating the structure of lichen communities. The findings may assistus in identifying lichens that may serve as biomarkers for dew availability and in anticipating changes in the lichen communitiesfollowing global warming.

Keywords: dew point temperature, epilithic lichens, endolithic lichens, substrate temperatures

Introduction

Rock-dwelling microorganisms (lithobionts) play an impor-tant role in rock weathering (Aghamiri and Schwartzman2002; Danin and Garty 1983; Viles et al. 2000) and are im-portant carbon contributors (Lange et al. 1970). Their C con-tribution is particularly important in desert ecosystems, wherethey can benefit also from additional water sources other thanrain, e.g., from dew and fog.

Dew and fog have been reported to play an important role tomicrobiotic crusts and lithobionts in temperate (Tretiach 1995)and more importantly in a variety of hot deserts such as theNamib (Lange et al. 1994), the Atacama (Warren-Rhodes et al.2006), the Sonoran Desert (Nash et al. 1979), the Tabernas(del Prado and Sancho 2007) and even in the cold Antarcticdesert (Budel et al. 2008). Perhaps the most extensive researchhas been carried out at the Negev Desert, where dew mayeven exceed rain precipitation during extreme drought years(Evenari et al. 1982).

The research was supported by grant 1358/04 of the Israel Sci-ence Foundation (ISF). We would like to thank Uri Blya, ValeriMorozovsky, Itai Vonshak, Alex and Leon for their valuable fieldmeasurements, Yair Goldreich for providing essential data, andCarol A. Kidron for the editing. We would also like to thank twoanonymous reviewers for their most helpful comments.∗Address correspondence to Giora J. Kidron, Institute of EarthSciences. The Hebrew University, Jerusalem 91904, Israel; Email:kidron@vms.huji.ac.il

An amount of 33 mm per annum spread across 195 dewymornings has been measured in Avdat, in the heart of theNegev Desert Highlands (Evenari et al. 1982). The frequencyof periods during which dew condenses, and the relatively largeamounts precipitated in comparison to the ∼90–100 mm ofrain precipitation (with 20–25 rainy days) lead ecologists tothe conclusion that dew may serve as the main water sourcefor lithobionts (Friedmann and Galun 1974). This was ver-ified for lichens by a set of measurements conducted undercontrolled (Lange 1969) and field conditions (Kappen et al.1979; Lange et al. 1970). Field measurements were also con-ducted in order to examine possible variables that may affectdew condensation.

On a microscale, dew was found to depend upon vari-ous factors that influence the rate of substrate cooling suchas the substrate angle (Kidron 2005), height above ground(Kidron 2010), and substrate position, whether embedded orloose (Kidron 2000) or surrounded by other obstacles (Kidron2010). On a meso scale, high variability in dew distributionwas found within a single drainage basin. Dew was found tobe aspect- and slope-dependent (Kappen et al. 1980; Kidronet al. 2000), explained by differential input of daytime radia-tion (which affect nocturnal longwave radiational cooling), bythe exposure to the afternoon breeze (which serve as a coolingagent) or by the differential early morning shading (Kidronet al. 2000). On a macro (regional) scale, dew condensationwas also found to be altitude-dependent (Kidron 1999).

Concomitant dew measurements that were conducted dur-ing the late summer and fall of 1992 at Nizzana, NIZ (250 ma.s.l), Sede Boqer, SB (530 m a.s.l) and Har Harif, HH (990 ma.s.l) (Figure 1) yielded a daily average amount of 0.11, 0.21

Dow

nloa

ded

by [

Uni

vers

ity o

f H

aifa

Lib

rary

] at

08:

48 1

2 Fe

brua

ry 2

013

282 Kidron and Temina

Fig. 1. Location of research sites.

and 0.32 mm at NIZ, SB and HH, respectively (Figure 2;Kidron 1999). The increase in the dew amounts from NIZto HH took place albeit the fact that the mid- and high-altitude sites of SB and HH, respectively, are located at agreater distance from the Mediterranean Sea, i.e., from themain (and practically only) source of humidity, 75 and 97 km,respectively, in comparison to 45 km of NIZ. Due to the factthat specific humidity decrease with distance from the sea(Yoshikado and Kondo 1989), as is also the case in Israel dur-ing which specific humidity decrease from the Mediterraneancoast to the inland Negev (Goldreich 2003), and the expectedoutcome that the relative humidity should also decrease (Bateet al. 2008), the increase in dew and fog amounts was explainedby the combined effect of the sea breeze and altitude (Kidron1999).

By serving as an efficient carrier of vapor, the sea breeze pro-vided adequate specific humidity to the inland sites of SB andHH thus compensating for the expected decrease in specifichumidity with altitude (Tomasi and Paccagnella 1988; Tran-quillini 1964). Higher dew point temperatures at the higheraltitude facilitated in turn early dew and fog condensation atSB and especially at HH (Kidron 1999). Indeed, a substantialincrease in the fog events with altitude was recorded (Kidron1999), in agreement with the 20–25 and 50–55 foggy morningsrecorded at SB and HH, respectively (Bitan and Rubin 1991).

Fig. 2. Dew amounts at Nizzana (NIZ), Sede Boqer (SB) and HarHarif (HH) following concomitant measurements (after Kidron,1999). Bars represent one SE.

All sites showed clearly visible differences in their lichencommunities. Yet, whereas limited studies trying to establishthe relations between lichen cover, growth form and speciescomposition on a micro- (Kidron 2000) and a meso-scale(Kidron et al. 2000, 2011) have been conducted, no researchwas yet conducted on a macro- (regional) scale. With similaraverage rain precipitation of ∼90-100 mm (Rosenan and Gilad1985), we hypothesized that differences in the lichen communi-ties may reflect the variable dew regime (amount and duration)at these three sites.

We further hypothesized that the species composition ofnorth- and south-facing slopes of the mid altitude site of SB,may show high similarity to the high altitude (HH) and thelow altitude (NIZ) sites, respectively. By using previously mon-itored data regarding the dew amounts at these sites (Kidron1999) and by calculating the dew duration time based on therelationship found for Sede Boqer (Kidron et al. 2000), thepresent research aims to explore the relations between the dewregime and lichen cover, growth form, chlorophyll contentand species composition across an altitudinal gradient at themacro-scale.

Research Sites and Methodology

A pair of plots, 5 × 5 m each, was demarcated at flat hilltopsalong an altitudinal gradient of Nizzana (NIZ), Sede Boqer(SB) and Har Harif (HH), at 250, 530 and 990 m above sealevel, respectively (Figure 1). The plots, characterized by scat-tered cobbles (Figure 3), were demarcated near the sites whereconcomitant dew measurements were carried out during thelate summer and fall of 1992 (Kidron 1999).

In an attempt to verify whether differences in the minimumtemperatures may be responsible for the differences in the dewand fog amounts, a pair of thermistors was installed at eachplot and connected to a Hobo mini data logger (Onset Com-puter Corporation, MA, USA). The thermistors, protected

Dow

nloa

ded

by [

Uni

vers

ity o

f H

aifa

Lib

rary

] at

08:

48 1

2 Fe

brua

ry 2

013

Effect of Dew and Fog on Lithic Lichens 283

Fig. 3. Close view of the typical lithobiont-covered surfaces ofcobbles at the hilltops of (a) Nizzana, (b) Sede Boqer and (c) HarHarif (color figure available online).

from direct radiation by 1 × 1 × 0.5 cm Polyurethane, wereattached to a pair of randomly chosen ∼10 × 10 × 7 cm cob-bles, aiming at measuring the temperature regime of the cob-bles, especially the nocturnal temperatures that may largelydetermine the dew amounts.

Twenty randomly chosen cobbles, ∼10 × 10 × 5–10 cmeach were collected from each site (10 cobbles from each plot)for the determination of their species composition and the rel-ative cover. Each cobble was marked by a 1 × 1 cm grid andthe cover of lichens within each grid was measured. Obser-vations and measurements of the morphological characteris-tics of specimens for lichen identification were made under adissecting microscope. Anatomical details were obtained byexamining hand-cut sections or squash preparations under alight microscope.

Measurements of anatomical characters were made in wa-ter at x100-1000 magnification. The species were identifiedin accordance with Galun (1970), Alon and Galun (1971),Clauzade and Roux (1985) and Temina et al. (2005). Thelichen nomenclature follows Temina et al. (2005). Specimenswere deposited at the herbarium of the Institute of Evolution,University of Haifa (HAI, Israel).

An additional 10 cobbles were collected from each plot forchlorophyll determination and for the examination of theirlithological properties. From each cobble, a pair of randomlychosen 1 × 1 cm samples was scraped to ∼0.5 cm depth (toensure the collection of all photoautotrophs) for chlorophylldetermination. Chlorophyll a (hereafter chlorophyll) was ex-tracted by hot methanol (70◦C, 20 min) in the presence ofMgCO3 (0.1% w/v) in sealed test tubes and assayed accordingto Wetzel and Westlake (1969). Following chlorophyll deter-mination, ESEM-EDS examinations were carried out in orderto examine possible mineralogical differences.

In addition, in order to exclude the possibility that differ-ences in the water-holding capacity of the rocks may affect dewavailability and hence lichen composition, the upper surface of10 randomly taken pieces, ∼2 × 2 × 1 cm each, were immersedin deionized water and then allowed to dry under nocturnalfield condition (air temperature of 20.5◦C; average wind veloc-ity of 1.1 m s−1). Following weighing (in 10 min intervals), thewater-holding capacity of the rock was determined (Kidronand Temina 2008).

Biodiversity analysis of the lichen communities, at NIZ,SB and HH was based on the Shannon-Wiener index (H) andevenness (J = H/Hmax) (Krebs 1999). In addition, north- andsouth-facing stations with similar surface characteriatics (i.e.,having large loess-covered soil in between the rock outcrops)at the mid altitude site of SB were also analyzed in order toassess their possible similarity to HH and NIZ, respectively.For this end, the mesic stations SB-2 (upper slope) and SB-4(lower slope) of the northern aspect and the xeric stations SB-8 (mid-upper slope) and SB-9 (upper slope) and SB-6 (lowerslope) of the southern aspect (Table 1) were compared to HHand NIZ. Stations SB-3 (midslope of the northern aspect) andSB-7 (midslope of the southern aspect) that had a continuousrock cover were excluded from the analysis.

To estimate similarity between the lichen communities,the Bray and Curtis index and the Sørensen index (Mueller-Dombois and Ellenberg 1974) were used. While the Bray andCurtis index considers both the species composition and thespecies cover, the Sørensen index is based on the presence andabsence of species, i.e., it considers only the species composi-tion of the communities. The Bray and Curtis index is definedas: IS = 2Mω/ 200, where Mω is the sum of the smaller quan-titative values (calculated as a ratio between each species coverand the total cover of all identified lichens) of all the speciesthat characterize any given pair of habitats. The Sørensen

Table 1. Slope angle and the average daily dew amount and du-ration at north- and south-facing stations at the Sede Boqer (SB)drainage basin

Slope Dew DewStation Aspect (deg.) Amount (mm) Duration (h)

SB-2 North-Facing 15 0.21 4.1SB-4 19 0.24 5.1SB-6 South-Facing 13 0.17 2.9SB-8 14 0.21 3.0SB-9 10 0.24 3.3

Dow

nloa

ded

by [

Uni

vers

ity o

f H

aifa

Lib

rary

] at

08:

48 1

2 Fe

brua

ry 2

013

284 Kidron and Temina

index is defined as SI = 2C × 100/ (A + B), where A and Bare the number of species in habitats A and B, respectively,and C is the number of species shared by the two habitats.

The Canonical Correspondence Analysis (CCA) with theCANOCO for Windows 4.5 package (ter Braak 1990) wasused to clarify the relationship between environmental vari-ables and the cover of the different lichen species. Followingthe great influence of the surface temperatures on the dewamounts (Montieth 1957), temperatures were not examined asa separate variable. Similarly, due to the similar rain amountsreceived by all sites, rain was also not examined. The analy-sis was therefore performed on the basis of two microclimaticparameters: dew amounts and dew duration.

Results

All cobbles consisted of dense micritic limestone and had asimilar mineralogical composition (CaCO3), as verified byESEM-EDS (not shown). All cobbles also showed similar sat-urated water-holding capacity and similar evaporation curvesonce submerged in water and left to dry out (Figure 4), point-ing to the fact that structural and textural differences werenegligible in terms of substratum water-holding capacity.

Pronounced and significant differences (paired t-test) inthe substrate temperatures were found (Figure 5). The sitesshowed consistent daytime and nighttime differences. At SB,midday average temperatures were by 2–3◦C higher than atHH and lower than at NIZ, with average midday temperaturesat HH being up to 5.8◦C lower than at NIZ. Similar differencescharacterized also the nocturnal and dawn temperatures with

Fig. 4. Evaporation curves (average values taken during two ex-periments) of rock pieces taken from cobbles from Nizzana (NIZ),Sede Boqer (SB) and Har Harif (HH) following immersion in wa-ter and being left to dry out under nocturnal field conditions. Barsrepresent one SE.

Fig. 5. Thirty days of concomitant temperature measurementsat Nizzana (NIZ), Sede Boqer (SB) and Har Harif (HH) duringNovember 2010. Bars represent one SE.

temperatures at HH being by 1–2◦C lower than at SB andtemperatures at SB being by 2–3◦C lower than at NIZ, withaverage temperatures at HH being by up to 5.3◦C lower thanat NIZ. The relatively low and high minimal temperatures atHH and NIZ, respectively, closely corresponded to the highand low dew amounts at HH and NIZ, respectively. At thesame time, SB, which had intermediate minimal temperatures,exhibited also intermediate dew amounts, thus supporting ourinitial hypothesis.

The average dew amount, the calculated dew duration,species composition and growth forms of all lichens are sum-marized in Table 2 and biodiversity descriptors in Table 3. Aclear increase in the number of lichen species with altitude wasobserved (Table 2), together with a clear pattern of a gradualincrease in lichen cover, number of epilithic lichens, speciesdiversity, and evenness (Table 3). All these variables show agradual increase with altitude, with NIZ < SB < HH. A grad-ual increase was also observed in the chlorophyll content withNIZ (38.6 mg m−2) < SB (52.6 mg m−2) < HH (71.3 mg m−2)(Figure 6a). However, this was not the case with the cover ofthe epilithic lichens that increased substantially with altitudeat the expense of the endolithic lichens, with NIZ (1.4%) < SB(4.3%)� HH (53.6%) (Fig. 6b). And thus, while the relationsbetween the dew and fog duration and the chlorophyll contentacross the three sites best fitted a linear equation, the rela-tions with the epilithic lichen cover best fitted an exponentialequation (Fig. 7).

When all three sites were compared, the Bray and Curtisindex and the Sørensen index showed a relatively high simi-larity between NIZ and SB (Table 4). Yet, only the Sørensenindex showed high similarity between SB and HH, pointingto the likeness of the species composition at both sites.

The interrelation between dew amount, dew durationand species composition is shown in the Canonical Corre-spondence Analysis, CCA (Figure 8). While Caloplaca holo-carpa was better related to dew amount, most lichens andabove all, Candelariella minuta, Caloplaca lactea, Diplotommaepipolium, and Sarcogyne regularis, were better related to dew

Dow

nloa

ded

by [

Uni

vers

ity o

f H

aifa

Lib

rary

] at

08:

48 1

2 Fe

brua

ry 2

013

Effect of Dew and Fog on Lithic Lichens 285

Table 2. Dew amount and duration and the lichen composition and relative cover at Nizzana (NIZ), Sede Boqer (SB) and Har Harif(HH)

Dew and Species Composition Abbreviation Growth Form NIZ SB HH

Average daily dew and fog amount (mm) 0.11 0.21 0.32Average daily dew and fog duration (h) 2.8 3.41 4.52

Aspicilia farinosa (Florke) Arnold AspFar P 0 1.0 (1.0) 18.4 (4.8)Caloplaca alociza (A. Massal.) Migula CalAlo D 93.5 (1.5) 63.4 (3.1) 2.4 (1.2)Caloplaca aurantia (Pers.) Hellb. CalAur P 0 0 8.9 (2.8)Caloplaca circumalbata (Delile) Wunder var.

bicolor (Mull. Arg.) WunderCalBic P 0 0 3.0 (1.3)

Caloplaca circumalbata (Delile) Wunder var.circumalbata

CalCir P 0 0 1.7 (0.7)

Caloplaca citrina (Hoffm.) Th. Fr. CalCit P 0 0.9 (0.4) 0Caloplaca erythrina (Mull. Arg.) Zahlbr. var.

pulvinata (Mull. Arg.) Zahlbr.CalPul P 0 0 0.2 (0.2)

Caloplaca holocarpa (Ach.) A.E. Wade CalHol D, P3 0 0.8 (0.3) 1.0 (0.5)Caloplaca lactea (A. Massal.) Zahlbr. CalLac D 0 0.1 (0.1) 0.5 (0.2)Candelariella minuta Reichert & Galun CanMin P 0 0.8 (0.6) 1.6 (0.7)Diplotomma epipolium (Ach.) Arnold DipEpi P 0.1 (0.1 0.3 (0.3) 4.1 (1.3)Lecania subcaesia (Nyl.) Szatala LecSub D 2.7 (1.2) 0.9 (0.4) 1.0 (0.8)Lecania turicensis (Hepp) Mull. Arg. LecTur P 0.3 (0.3) 0 3.6 (1.3)Lecanora crenulata Hook. LecCre D, P4 0 0 0.2 (0.1)Rinodina bischoffii A. Massal. var. aegyptiaca

Mull. Arg.RinAeg D 0 0.5 (0.3) 10.0 (3.4)

Rinodina dubyana (Hepp) J. Steiner RinDub D 0 6.7 (2.8) 2.1 (2.1)Rinodina immersa (Korb.) Arnold RinImm D 0 7.2 (2.1) 0.4 (0.3)Sarcogyne regularis Korb. SarReg D 0 0 3.8(1.7)Verrucaria nigrescens Pers. VerNig P 0 0.7 (0.5) 0.1 (0.1)

One standard error in parenthesis.1. Based on the relations between dew amount and duration, see Kidron et al. (2000).2. Based on the above relations dew duration in HH is 3.9 h. Yet, the two fold occurrence of fogs in HH (which extends the daily moisture duration for anextra 2 h; see Kidron 1999) implies an extra daily duration of ∼15% to that of the 3.9 h, i.e., 4.5 h.3. While appearing as endolithic (D) and epilithic (P) in SB, it appeared as epilithic at HH.4. Appeared in both growth forms in HH.

duration. Yet, when both variables (dew amount and dura-tion) were grouped and referred to as dew availability, threedifferent groups of lichens could be identified. While the firstgroup, which included 13 out of the 19 species defined (such asAspicilia farinosa, Caloplaca circumalbata var. bicolor, Calo-placa holocarpa, Caloplaca lactea, Candelariella minuta, Diplo-

Table 3. Biodiversity characteristics of the lichen communitiesbetween Nizzana (NIZ), Sede Boqer (SB) and Har Harif (HH)

Sites

Biodiversity characteristics NIZ SB HH

Total species number 7 13 18Total number of endolithic species 4 8 9Total number of epilithic species 3 6 11Average cover by all lichen species (%) 91.6 94.1 95.7Average cover by endolithic species (%) 90.3 90 44.4Shannon index 0.22 0.94 2.28Evenness 0.11 0.37 0.79

tomma epipolium, Lecania turicensis, Lecanora crenulata, Rin-odina bischoffii var. aegyptiaca) exhibited a positive linear re-lation with dew availability (Fig. 9a), the second group, whichincluded two species (Caloplaca alociza, Lecania subcaesia)exhibited a negative linear relation with dew availability (Fig.9b), while the third group, which included 4 species (Calo-placa citrina, Rinodina dubyana, Rinodina immersa, Verrucarianigrescens) exhibited a parabolic pattern with the highest coverat medium dew availability (Fig. 9c).

The comparison of HH and NIZ sites to the mesic (north-facing) and xeric (south-facing) stations of SB are shown inTable 5. Although HH showed higher similarity to SB-2 bythe Bray and Curtis index, it showed higher similarity to SB-4 by the Sørensen index. As for NIZ, both indices showedhigh similarity between NIZ and SB-8. These results are notsurprising when the differences in the dew duration of thenorth- and the south-facing stations are considered. Althoughthe relatively high similarity between NIZ and SB-8 (of 63-73 scores) cannot possibly reflect the high differences in theaverage daily dew amount between NIZ (0.11 mm) and SB-8(0.21 mm), it can be better explained by the similar averagedaily dew duration at NIZ (2.8 h) and SB-8 (3.0 h).

Dow

nloa

ded

by [

Uni

vers

ity o

f H

aifa

Lib

rary

] at

08:

48 1

2 Fe

brua

ry 2

013

286 Kidron and Temina

Fig. 6. Average chlorophyll a content (a) and the percent ofepilithic lichens (b) at Nizzana (NIZ), Sede Boqer (SB) and HarHarif (HH). Bars represent one SD.

Similarly, although the high difference in the average dailydew amount between HH (0.33 mm) and SB-2 (0.21 mm)cannot account for the high similarity between these stationsaccording to the Sørensen index (of 71 scores), the similaraverage daily dew duration (of 4.5 h in HH and 4.1 h in SB-2) may better account for the high similarity between bothhabitats. One should note that HH was also similar to SB-4 (of 80 scores). In fact, the intermediate dew duration atHH (4.5 h) in comparison to SB-2 (4.1 h) and SB-4 (5.1 h)

Fig. 7. The relations between the dew duration and the chlorophyllcontent and the epilithic lichen cover at all habitats.

Table 4. A comparison between Nizzana (NIZ), Sede Boqer (SB)and Har Harif (HH) based on the similarity indices of Bray andCurtis and Sørensen

NIZ SB

Site Bray and Curtis Sørensen Bray and Curtis Sørensen

SB 65 60HH 6 56 9 77

may explain the similar results obtained by both indices, eachpointing to higher similarity with another SB station.

Discussion

Differences in the cobble lithology could not have explainedthe variable communities and chlorophyll content across thesites. The similar structure and texture excluded the possibilitythat either of these variables may significantly influence wateravailability, as discussed elsewhere (Kidron 2002). Therefore,microclimatological factors may thus be responsible for theobserved differences in lichen community composition andchlorophyll content.

Serving as the major (and practically the only) source ofhumidity, vapor which originates from the Mediterranean Seais brought inland by the daytime breeze that develops at theSea-land interface (Zangvil 1995). North northwestern windswith peak velocity at the late afternoon (Bitan and Rubin1991; Kidron et al. 2000), transport water vapor inland duringdaytime, and provide the necessary humidity for dew and fogcondensation (Bitan and Rubin 1991; Zangvil 1995). At thelate afternoon, average wind velocity is 5.5 m s−1 in SB and8.0 m s−1 in HH (Bitan and Rubin 1991). This wind may alsoserve as a cooling agent, causing efficient radiation loss of allsubstrates, reflected in the relatively low nocturnal substratetemperatures (Kidron et al. 2000).

The consistently lower nocturnal temperatures at HH incomparison to SB and NIZ attested indeed to the close linkbetween the dew point temperatures and the dew amounts atall three sites. Since all sites were located at the hilltops andthus exposed to the first sun beams, differential condensationdue to shading was avoided (Kidron et al. 2000). Subsequently,the recorded dew amounts reflected the substrate temperaturesat all sites. Since the rate of dew condensation is more or lessequal (Zangvil 1996), the lower the nocturnal temperatures,the higher the likelihood of the dew point temperatures to bereached (Monteith 1957).

And thus, although located farther away from the Mediter-ranean Sea and subsequently from the only significant sourceof vapor, higher dew amounts were recorded at SB and es-pecially at HH, explained by their higher altitude and conse-quently their lower nocturnal temperatures. Apparently, theorographic effect of the central mountain chain in the Negevmay also compensate for the expected reduction in rain precip-itation with distance from the sea and may explain the similaramount of rain precipitation at all sites.

Dow

nloa

ded

by [

Uni

vers

ity o

f H

aifa

Lib

rary

] at

08:

48 1

2 Fe

brua

ry 2

013

Effect of Dew and Fog on Lithic Lichens 287

-1.2 1.2

-1.2

1.2

AspFar

CalAlo

CalAurCalBic

CalCir

CalPul

CalCit

CalHol

CalLacCanMin

DipEpi

LecSub

LecTur

LecCreRinAeg

RinDub

RinImm

SarReg

VerNigD Am

D Dur

Fig. 8. Canonical correspondence analysis (CCA) ordination of the lichen species and environmental variables in the drainagebasins. Abbreviations of environmental variables: D Am – average daily dew amount, D Dur – average daily dew duration. Speciesabbreviations are given in Table 2.

Temperature control upon dew amounts was also mani-fested in SB once loose and partially embedded cobbles werecompared. Although having the same surface area and locatedat the same height above ground, more efficient longwave ra-diational cooling of the loose cobbles resulted in 1.0–1.2◦Clower substrate temperatures at dawn. Similar to the currentfindings, the small differences in the nocturnal temperaturesresulted in substantial differences in the dew amount. It re-sulted in a 1.9-fold increase in the dew amounts of the loosecobbles (Kidron 2000).

Following the higher amounts of dew, the mid-altitude siteof SB and especially the high-altitude site of HH will alsoexperience longer dew duration. As a result of the high oc-currence of fogs in HH (Bitan and Rubin 1991; Kidron 1999),and subsequently by providing an efficient screen against theearly morning radiation, fogs may substantially hinder des-iccation thus contributing to a lengthy wetness duration time(Duvdevani 1964; Levi 1967). Consequently, average daily dewand fog duration at HH may be even slightly longer than that

found based on the relations between dew amount and dewduration in SB (Table 1; Kidron et al. 2000).

By studying the interrelations between microclimatologicalvariables and the lichen communities, the findings thus high-light the potential use of species composition as biomarkersfor the dew regime, as was also previously reported (Teminaand Kidron 2011). By facilitating a distinction between dewamounts and duration, dew amounts were found to princi-pally control the distribution of Caloplaca holocarpa, whiledew duration may principally control most of the remaininglichens (Figure 8). Yet, the close link between dew amountsand duration may not facilitate an easy distinction betweenthese two factors and further research is needed. Neverthe-less, when both factors are combined and referred to as dewavailability, three groups of lichens could be detected.

Most lichens increase their cover with dew availability (Fig-ure 9a). Out of this group it is worth mentioning the lichensCaloplaca circumalbata var. bicolor, Lecania turicensis, andLecanora crenulata that were found at SB to reflect mesic

Dow

nloa

ded

by [

Uni

vers

ity o

f H

aifa

Lib

rary

] at

08:

48 1

2 Fe

brua

ry 2

013

288 Kidron and Temina

Table 5. A comparison between Har Harif (HH) and Nizzana(NIZ) and the north-facing stations (SB-2, SB-4) and the south-facing stations (SB-6, SB-8, SB-9) of Sede Boqer (SB) based on(a) Bray and Curtis index and (b) Sørensen index

(a)

Station HH NIZ SB-2 SB-4 SB-6 SB-8

SB-2 17 7SB-4 31 9 33SB-6 6 54 23 35SB-8 9 73 24 24 70SB-9 5 49 23 30 77 65(b)

Station HH NIZ SB-2 SB-4 SB-6 SB-8

SB-2 80 58SB-4 71 43 67SB-6 42 46 52 36SB-8 59 63 69 48 53SB-9 33 62 43 36 67 67

Fig. 9. Three schematic patterns describing the relations betweendew availability (amount and duration) and the species cover.Species with uncertain pattern (due for instance to their occur-rence in only one site) are indicated by a question mark. Forspecies abbreviation, see Table 2.

conditions (Temina and Kidron 2011). More interesting is thesecond group (Figure 9b), represented by Caloplaca alocizaand Lecania subcaesia that show a decrease in cover with dewavailability. Both species were found indeed to serve as possiblexeric biomarkers at SB (Temina and Kidron 2011), and mayreflect relatively low competitive power with the increase indew availability.

The third group (Figure 9c), which may also reflect a rela-tively low competitive power with the increase in dew availabil-ity, includes the lichens Caloplaca citrina, Rinodina dubyana,Rinodina immersa and Verucaria nigrescens, which show ahigher cover at intermediate dew availability. In this regardit is interesting to note that Rinodina dubyana was found tomainly inhabit hilltops in SB, being thus adapted to relativelyhigh dew amounts that last however for a relatively short time.Caloplaca citrina and Verucaria nigrescens were found to beamong the pioneer lichens to inhabit newly exposed cobbles(Kidron and Temina 2010).

Although previous assumptions that linked between highdew amounts and preferential growth of epilithic lichens (Tre-tiach 1995) were not supported by the current data, our datapointed however to the possible link between dew durationand epilithic lichen proliferation, as also reported elsewhere(Kidron et al. 2011). While performing similar photosyntheticactivity (Lange et al. 1970), by growing on top of the endolithiclichens and subsequently by blocking irradiance and possiblyalso dew, epilithic lichens may have an advantage over en-dolithic lichens. This is in agreement with data published inthe literature (Ivimey-Cook 1959; Tretiach 1995), and withdata recorded on newly exposed cobbles in SB where epilithiclichens were supplanting endolithic lichens at the north-facingslope (Kidron and Temina 2010).

The increase in lichen cover and especially in the epilithiclichen cover with altitude was also reflected in an increasein the chlorophyll content. This is in agreement with thehigh variability in chlorophyll content recorded within asmall drainage basin at SB, despite the similar rain amountsrecorded across the drainage basin (Kidron et al. 2011). Sim-ilar to the current results, the relation between chlorophyllcontent and dew duration best fitted a linear equation, whilethat of the epilithic lichen cover best fitted an exponentialequation.

Whether judging similarity in accordance with Bray andCurtis index (with SB-4 being the most similar to HH) or withthe Sørenson index (with SB-2 being the most similar to HH),the data indicate that HH is most similar to the north-facingstations in SB. Similarly, NIZ is most similar to SB-8 at thesouth-facing slope of SB.

With SB-2 and SB-4 having a slope gradient of 15–19 de-grees, and SB-8 having a slope gradient of 14 degrees, one cantherefore conclude that as far as the Negev is concerned, achange in the slope angle of ∼15◦ for each of the northernor the southern aspect may be equivalent to a difference of300–400 m in altitude. Being the main driving force for lichencomposition, both aspect and angle may play a very importantrole in species diversity. Moreover, dew duration may have animportant impact on the epilithic lichen cover (as can be seenin their increase in HH and at SB-2 and SB-4), thus being alsoresponsible for a sharp change in the lichen’s growth form.

Dow

nloa

ded

by [

Uni

vers

ity o

f H

aifa

Lib

rary

] at

08:

48 1

2 Fe

brua

ry 2

013

Effect of Dew and Fog on Lithic Lichens 289

By providing an additional source of water and by provid-ing additional nutrients (Kidron and Starinsky 2012), dew maythus play an important role in the establishment and growth ofphotoautotrophic microorganisms (Budel et al. 2008), and theterrestrial food chain (Jones and Shachak 1990). The currentfindings may thus assist us in anticipating the changes that mayoccur in the lichen chlorophyll content, cover, species compo-sition and diversity also following global warming. Followingthe close relationship between minimum temperatures and thedew point temperatures (Hubbard et al. 2003; Scherm and vanBruggen 1993), and numerous data indicating that the increasein global warming (Parmesan 2006) is principally reflected inan increase in the minimum temperatures (Beniston et al. 1994;Dessens 1995; Karl et al. 1991; Price et al. 1999; Peng et al.2004), global warming may imply a decrease in the dew pointtemperatures consequently resulting in a decrease in the dewand fog amounts. This in turn may result in more xeric lichencommunities and lower biomass which may affect the entirefood chain.

Conclusions

The different lichen populations, cover, growth form andchlorophyll content across an altitudinal gradient of NIZ (at250 m a.s.l.), SB (at 530 m a.s.l.) and HH (at 990 m a.s.l.) couldnot have been explained by the cobble lithology, nor by rain.It could have been explained by the variable dew regime, asalso verified by the gradual decrease in the minimum night-time temperature with altitude. The increase in chlorophyllcontent and the epilithic lichen cover with altitude were bestexplained by the dew duration. Population analysis showedhigh similarity between the population of a north-facing sta-tion (at 15–19◦) and a south-facing station (at 14◦) at SB withthe high-altitude HH site and the low-altitude NIZ site, re-spectively, pointing out that an angle of ∼15◦ to each of thesun-shaded or sun-exposed aspects may be similar to a differ-ence of 300–400 m in altitude. Global warming, which mayimply an increase in minimal nocturnal temperatures may re-sult in more xeric lichen communities and lower biomass andmay thus affect the entire food chain.

References

Aghamiri R, Schwartzman DW. 2002. Weathering rates of bedrock bylichens: A mini watershed study. Chem Geol 188:249–259.

Alon G, Galun M. 1971. The genus Caloplaca in Israel. Isr J Bot20:273–292.

Bate DB, Barrett JE, Poage MA, Virginia RA. 2008. Soil phosphoruscycling in an Antarctic polar desert. Geoderma 144:21–31.

Beniston M, Rebetez M, Giorgi F, Marinucci MR. 1994. An analysisof regional climate change in Switzerland. Theor Appl Climatol49:135–159.

Bitan A, Rubin S. 1991. Climatic Atlas of Israel for Physical and Envi-ronmental Planning and Design. Tel Aviv: Ramot Publishing.

Budel B, Bendix J, Bicker FR, Green TGA. 2008. Dewfall as a wa-ter source frequently activates the endolithic cyanobacterial com-munities in the granites of Taylor Valley, Antarctica. J Phycol44:1415–1424.

Clauzade G, Roux C. 1985. Likenoj de Okcidenta Europo. Ilistrita De-terminlibro. Bulletin de la Societe Botanique du Centre – Quest,Nouvelle Serie – Numero Special 7, Royan, France.

Danin A, Garty J. 1983. Distribution of cyanobacteria and lichens onhillsides of the Negev Highlands and their impact on biogenic weath-ering. Z Geomorph 27:423–444.

del Prado R, Sancho LG. 2007. Dew as a key factor for the distributionpattern of the lichen species Teloschistes lacunosus in the TabernasDesert (Spain). Flora 202:417–428.

Dessens J. 1995. Severe convective weather in the context of a nighttimeglobal warming. Geophys Res Lett 22:1241–1244.

Duvdevani S. 1964. Dew in Israel and its effect on plants. Soil Sci98:14–21.

Evenari M, Shanan L, Tadmor N. 1982. The Negev, the Challenge of aDesert. 2nd ed, Boston, MA: Harvard University Press.

Friedmann EI, Galun M. 1974. Desert algae, lichens and fungi. In:Brown GW, editor. Desert Biology II. New York: Academic Press.p165–212.

Galun M. 1970. The Lichens of Israel. Jerusalem: The Israel Academyof Sciences and Humanities.

Goldreich Y. 2003. The Climate of Israel: Observations, Research, andApplications. New York: Kluwer Academic/Plenum Publishers.

Hubbard KG, Mahmood R, Carlson C. 2003. Estimating daily dewpoint temperature for the northern Great Plains using maximumand minimum temperature. Agron J 95:323–328.

Ivimey Cook RB. 1959. The lichens of Ewenny Downs, Glamorganshire.Lichenologist 1:97–103.

Jones CG, Shachak M. 1990. Fertilization of the desert soil by rock-eatingsnails. Nature 346:839–841.

Kappen L, Lange OL, Schulze E-D, Buschbom V, Evenari M. 1980.Ecophysiological investigations on lichens in the Negev Desert, VII:The influence of the habitat exposure on dew imbibition and pho-tosynthetic productivity. Flora 169:216–229.

Kappen L, Lange OL, 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 maci-formis (Del.) Bory. Flora 168:85–105.

Karl TR, Kukla G, Razuvayev VN, Changery MJ, Quayle RG, Heim RR,Easterling DR, Fu CB. 1991. Global warming: evidence for symmet-rical diurnal temperature change. Geophys Res Lett 18:2253–2256.

Kidron GJ. 1999. Altitude dependent dew and fog in the Negev desert,Israel. Agric Forest Meteorol 96:1–8.

Kidron GJ. 2000. Dew moisture regime of endolithic and epilithic lichensinhabiting calcareous cobbles and rock outcrops, Negev Desert,Israel. Flora 195:145–153.

Kidron GJ. 2002. Causes of two patterns of lichen colonization on cobblesin the Negev Desert, Israel. Lichenologist 34:71–80.

Kidron GJ. 2005. Angle and aspect dependent dew precipitation in theNegev Desert, Israel. J Hydrol 301:66–74.

Kidron GJ. 2010. The effect of substrate properties, size, position, shel-tering and shading on dew: An experimental approach in the NegevDesert. Atmos Res 98:378–386.

Kidron GJ, Starinsky A. 2012. Chemical composition of dew and rainin an extreme desert (Negev): Cobbles serve as sink for nutrients.J Hydrol. 420–421:284–291.

Kidron GJ, Temina M. 2008. The mycobiont role in crustose lichenexpansion on cobbles in the Negev Desert. Geomicrobiol J 25:95–100.

Kidron GJ, Temina M. 2010. Lichen colonization on cobbles in theNegev Desert following 15 years in the field. Geomicrobiol J 27:455–463.

Kidron, GJ, Temina M, Starinsky A. 2011. An investigation of therole of water (rain and dew) in controlling the growth form oflichens on cobbles in the Negev Desert. Geomicrobiol J 28:335–346.

Kidron GJ, Yair A, Danin A. 2000. Dew variability within a small ariddrainage basin in the Negev highlands, Israel. QJR Meteorol Soc126:63–80.

Dow

nloa

ded

by [

Uni

vers

ity o

f H

aifa

Lib

rary

] at

08:

48 1

2 Fe

brua

ry 2

013

290 Kidron and Temina

Krebs CJ. 1999. Ecological Methodology. Petaluma, CA: Addison Wes-ley Longman.

Lange OL. 1969. Ecophysiological investigations on lichens of the NegevDesert. I. CO2 gas exchange of Ramalina maciformis (Del.) Boryunder controlled conditions in the laboratory. Flora 158:324–359.

Lange OL, Meyer A, Zellner H, Heber U. 1994. Photosynthesis and waterrelations of lichen soil crusts: Field measurements in the coastal fogzone of the Namib Desert. Func Ecol 8:253–264.

Lange OL, Schulze ED, Koch W. 1970. Ecophysiological investigationson lichens of the Negev Desert, III: CO2 gas exchange and watermetabolism of crustose and foliose lichens in their natural habitatduring the summer dry period. Flora 159:525–538.

Levi M. 1967. Fog in Israel. Isr J Earth Sci 16:7–21.Monteith JL. 1957. Dew. Quat J Royal Meteorol Soc 83:322–341.Mueller-Dombois D, Ellenberg H. 1974. Aims and Methods of Vegeta-

tion Ecology. New York: Wiley.Nash III TH, Nebeker GT, Moser TJ, Reeves T. 1979. Lichen vegeta-

tional gradients in relation to the Pacific coast of Baja California:the maritime influence. Madrono 26:149–163.

Parmesan C. 2006. Ecological and evolutionary responses to recent cli-mate change. Ann Rev Ecol Evol Syst 32:637–669.

Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, CentenoGS, Khush GS, Gassman KG. 2004. Rice yields decline with highernight temperature from global warming. Proc Natl Acad Sci (USA)101:9971–9975.

Price C, Michaelides S, Pashiardis S, Alpert P. 1999. Long term changesin diurnal temperature range in Cyprus. Atmos Res 51:85–98.

Rosenan N, Gilad M. 1985. Meteorological data. Atlas of Israel.Jerusalem: Carta.

Scherm H, van Bruggen AHC. 1993. Sensitivity of simulated dew du-ration to meteorological variations in different climatic regions ofCalifornia. Agric Forest Meteorol 66:229–245.

Temina M, Kidron GJ. 2011. Lichens as biomarkers for dew precipitationin the Negev Desert. Flora 206:646–652.

Temina M, Kondratyuk SY, Zelenko SD, Wasser SP, Nevo E. 2005.Lichen-forming, lichenicolous and allied fungi of Israel. In: WasserSP, Nevo E, editors. Ruggell: Ganter Verlag.

ter Braak CJF. 1990. Interpreting canonical correlation analysis throughbiplots of structural correlations and weights. Psychometrica55:519–531.

Tomasi C, Paccagnella T. 1988. Vertical distribution features of atmo-spheric water vapour in the Po Valley area. Pure Appl Geophys127:93–115.

Tranquillini W. 1964. The physiology of plants at high altitudes. AnnRev Plant Physiol 15:345–362.

Tretiach M. 1995. Ecophysiology of calcicolous endolithic lichens:progress and problems. Giornale Botanico Italiano 129:159–184.

Viles HA, Spencer T, Teleki K, Cox C. 2000. Observations on 16 yearsof microfloral recolonization data from limestone surfaces, AldabraAtoll, Indian Ocean: implications for biological weathering. EarthSurf Process Landf 25:1355–1370.

Warren-Rhodes KA, Rhodes KL, Pointing SB, Ewing SA, Lacap DC,Gomez-Silva B, Amundson R, Friedmann EI, McKay CP. 2006.Hypolithic cyanobacteria, dry limit of photosynthesis, and mi-crobial ecology in the hyperarid Atacama Desert. Microb Ecol52:389–398.

Wetzel RG, Westlake DF. 1969. Periphyton. In: Vollenweider RA, edi-tor. A Manual on Methods for Measuring Primary Production inAquatic Environments. Oxford, UK: Blackwell. p33–40.

Yoshikado H, Kondo H. 1989. Inland penetration of the sea breezeover the suburban area of Toky. Boundary-Layer Meteorol 48:389–407.

Zangvil A. 1996. Six years of dew observation in the Negev Desert, Israel.J Arid Environ 32:361–372.

Dow

nloa

ded

by [

Uni

vers

ity o

f H

aifa

Lib

rary

] at

08:

48 1

2 Fe

brua

ry 2

013