Warren G. Gold,r KatherineA. Glew,'zand Leal G. Dickson,3Departmentof Botany Box 355325,UnversityoJ
Washngton Seatte Washngton981955325
FunctionalInfluences
of Cryptobiotic
SurfaceCrustsin an Alpine
Washington,
TundraBasinof the OlympicMountains,
U.S.A.
Abstract
L.r) ers oi cD probiotic organisnrs(lichens.mosses.funpi. rl8ae, cyanobacterialon the soil suriaccarc common lialu.cs ofundis
turbed sites in cold dc\crt\. scnri arid gras\lands.and arctic and alpine connunities. Lillle is kiown aboul thc rclationship
bet$een thesecrusts and lloscring plant communities in alpine ecosystems.This study conpared the soil enlironmcnl. associ
ated plant tenperarure parren1\lrnd crus! atnospheric nitrogen fixation acrilit! in rn alpine site with t$o dillerent typcs ol'
. f ) f r ' h . r i . , r u . r .l n . l o n i . , r es i r l r u ufrl u . 1 .
When cornpafed1()the noncnr\tedsite.bolh t,,-pes
ofcrusls $crc associalcdwith changesin soil iextLrre,increasedsoil organic
mairef (52 rnd 31.17.).incrc:rsedl.rre sumncr soil roisture (56 and 4l9i/.). and increasedsoil niirogen and phosphorus.Soil
,tudace\ ard ne:u surfrce soils at midda) icrc cooler by 5 to 8'C under moss-domin.rtedcrust and 10 to l1'C cooler undcr
fiuticose lichen dominrlcd cru\l asconrparedto noncrusted\ufaces. However lbliage lelnperalurcsoi aduh,Dr&g/a!i.r/.rrrisd/.?
cu\hioDsdid rol diiler in |h.sc rhrcc \itcs. Cooler and moister sudrce conditions:rssocialedwith $e crusls n1a| inllucncc sccd
ling enablishmenrand halc lc\s cffcct on adult plants with estrblishedroot systems.Despiregreacr soil nifogcn conccntrations
in the t$o clittefentcrusl sires.lealnifogcn conccntrationwas 25 to.].1% lolver in leavesof pianls grolving wi(h crustscomparcd
b the srLnespeciesgro$ing ir Lh. noncrustcdsiIe.Compeiition lbf nutfientsrt the crust sitesma) oifsetgreaternuricnl conccn
traiions in soils. Kno*ledge of speciiic lunclional allributlrsofdifltrent crtptobiotic sudaceswiil be inponant ibr lhe develop
ment of manrgenent and reslor tion planr in alpinc ecos\'stems.
lntroduction
Thin biologicalcruststhatcoverthe groundsurface are a common feature of pdstine areasin
andhigh
alpinetundra.cold dcsertshrub-steppe,
(West 1990,St. Clair
iatitudepolar ecosystems
and Johansen 1993, Dickson 2000). These
"cryptogamic"
cryptobioticcrusls(alsoknown as
"microbiotic"
or
crusts)\'arv in thicknessfrom
just a fe$'millimete$ to more than a tew ccntim e t e r sT. h e l i r r \ ' r ' o m P o \ coJf v c r l i n g p r o p o r tionsoflichens.mosses,greeneLlgae,
cyanobacteria,
fungi. and diatomsdcpendinguponthe envlronCryptobiotic
mentanddegreeof cmstdevelopmcnt.
crusts feach their greatestdevelopmentin cold
andolien seasonallydry locationswherethecover
of vascularplantsis sparscto modemte.Com
plcx plantcorur.runities
ofpatchylow shrubs,lbrbs
and grassesresidein thc cryptobioticmatrix. The
Currert Address: Llni!cr\ily of washington. Bothell. Interd i s c i p l i n a r yA r I s & S c i e n c e \P f o g f r l m ,B o x 3 5 8 5 3 0 .1 8 1 1 5
C a r n p u sw a ! \ 8 . B o t h e l l \ \ : A . 9 8 0 1 1 ' 8 2 1 6
'Cu||enr Addres\: Biologr- Deprrhcnr. Univcrsit,vof Puge!
Sound. 1500N. $'amef Slrcet. Trcomr. wA 9li.1l6
' C u r f e n t A d d f e s sB
: i o l o g yP r o g r a mU
. n i v c r s i ! vo f \ v a s h i n g ton. Se..irde.\\A 9it 195
crusts are highly susceptibleto damageand desmrction liom physical disturbance.Thc impact
of human tread can compressand dislodge sections of crust, u,ith recoveryproceedingvcry
slowly.if it occursat all (Brotherson
et al. 1983.
B e l n a p1 9 9 3 ) .
Despitetheirfragility andcommonoccurrence
in variousecosystems,
thefunctionalrolesofthese
crusts have not been extcnsively studied.Much
of the researchon cmstshasconcentratedon de(Shiclds1957,West1990,1991,
scriptiveanalyses
Grondin andJohansen1993,St. Clair et al. 1993)
and investigationsof the physiology of crust or
ganisms(MacGrcgorandJohnsoD
1971,R.vchefi
and Skujins 1974,Brock 1975.Fritz-Shcridan
1988.Jeffrieset al. 1993,1994,Lennihanet al.
The
1994)in cold deseftand arcticccosystems.
majority of detailedinvestigationsof crustorganismshasbeendoncunderhighly controlledcon
ditions in the laboratory.However,the int'luence
of crustson soil watef balance(Brothersonand
Rushforth 1983. Eldridge 1993), erosion
(Brotherson
et al. 1983),and seedlingestablish
ment (Woodet al. 1982.Harris et al. 1987,Parker
1996)havebeenexamincdin the field in semiarid desertsand prairies.The impact ot crustson
N o r t h $ ' e sSt c i e n c eV. o l . 7 5 ,N o . 3 . 2 0 0 1
O :001 b) llic N.dhnc{
S.trarii.A*o.i.rion
All rehtrresetred
315
ecos,ystemnutrient cvcling has been limited to
tield measurenenlsoftheir capacityfor nitrogen
fixation(RychenandSkujins197.1,
Wojciechowski
and Heimbrook 198,1.Fritz-Sheridan 1988.
Lennihanet al. 1994.Dickson2000) engendering considerable
speculation(Wcst 1990,1991,
Harper and Pendleton i993). The influence of
r ironc r )p l o b i oil( c ru . l . , ' n t h et h e r n t aI lni c r u c n
nent ()1\'ascularplantsgrowingwithin thesccrusts
hasbeenstudiedonly recentlyin theHigh Arctic
(Gold 1998).
There is accumulatingevidencethat indicates
cryptobiotic crusts plav an impofiant role in thc
developmentandnaintenanceofthe vasculilrplant
connrunitiesin certainhigh arctic polrr desert
ecosystems.
In this harshenvironmentsubstan
tial development
ol higherplantcommunitiesis
typically restrictedto arcasof considerablecrust
development.
This is a complexresultof many
effectsof the crvptobioticc[ust, includingthe
prevention of soil surfacc drying. enhancement
ofnineral nutrienl supplyandcycling (especially
nitogen). alterationsof the surtacethennal environment for thc vascular plants. and a reductiol of the physicalstresses
of soil movement
associatcdwith freeze-thawaction(Gold andBliss
1995a,1995b,Gold 1998,Blissand Gold 1999.
Dickson 2000). Like thesearctic locations.temperatealpinc ccosystemshlrve cool, short growing seasonsand poor nutrient availability.There
is litde intbnnationabouttherolesofcrypbbiotic
cruslsin alpineecosystems.
in part. becauseof
l , ' g i \ l i . u lL l i t l i c u l l i er\n d t h c i n ! o n . p i \ u o u \n ! r
ture of cmst or-sanisms.
Our broad objective was to study possiblc influencesof cryptobiotic crustson vascularplant
communitiesand alpine ccosystemfirnctions.An
alpinebasinin theBuckhomRangcof theOlympic
Mountains.Washingtonwas choscnfor study
becauseof its abundantand divcrse cryptobiotic
groundcoverWe specificallycomparedthethermal
cnvironment(soil and air tempcratures).
plant
tempcratures,and the nutrient statusof soils and
plants in siteswith diflerent typesof crustsand a
site without cl!sts. Thc potential1brcrust contribution to ecosystemnitrogcn was turther exam
ined throughlab studicsof nitrogenase
activity
in the different surfacctypes (two typesof crusts
and lack of crusts).
316
Gold. Glew.and Dickson
Methods
Study Area
The alpincbasinof Buckhom Mountain in the
O l l r n p i iM o u n t a i n w
' . i l \ h i n g r u ni .., r u n i q u e
atcr
of alpinetundraat 1982m elevation(47" 62'N.
123' 07' W). The gradualcentralslopesof the
basin,underlainby both sedimentaryand basaltic rock, aredeminatedby a cover of cryptobiotic
crustsandscatteredalpiDeplants(e.g..Afllenr.rri.i
rcsea-Arerutriu sp.,Caret sp.- D o uglasittlaevigata.
Lttzula sp.. Phlox hentlersortii-Salft nivali.s,
Snelowskia cuht:in ?).Although the presentsurface soil and rock appear relatively stable. the
undulating landscapesuggcstspast solifluction
(Glew l998.1.
Threesurfacetypeswere describedandinves
tigated at separatelocationsin the basin (Figure
l). The ''noncrusted" surlace site had a surface
of coarse-grainedmineral substratewith widely
scattered
vascularplants.This siteoccupieda gentle
concavitvwith late-lyingsnow.Much ofthe lower
basin slopeswere dominatedby a thin (< 2 cn,
surfacelayer of mossesand foliose lichens over
a very coane nincral substrate(the"crustedsite").
The vascuiarplant community wasdominatedby
Sdli.r nivalis. Just above theselower slopcs.the
nid-basin slopeswere charactcrized
by a relatively thick (3 10 cm) surfacemat of fruticose
lichens(thc"lichen 'site dominatedby cetrarioid
lichens)with vascularspeciessuchasCcraparrrla
rotundiJblia.and a numbcr of graminoids ( e.g.,
Ca rex p lne o t epltttLa, F esttrctt s(dinont autq,
TrisetLltnspicatL!m)and composites(e.g.. Seaecio lugens,SolidagomuLtirqdiata).Vasculxrplant
nomenclaturefbllows that in Buckingham et al.
( r99s).
Temperature
Reat onshps
Temperatures
were continuouslymodtorcd in thc
crustedand noncrustedsitesthrough pofiions of
the 1995growing seasonwith fine wire (.07 mrr
diameter) thermocouplesand an clcctronic
datalogger(CampbellScientilicCo.. Logan.UT).
This tempemturemonitoringincludedair temp e r a t u r ea.l 5 c m h e i g h rt r e t l e c l i n a
gi r r e r n p c r . r turesexpedencedat the height of thesclow stature alpineplants),sudacetemperatures,and soil
temperatures
at 5 cm depth.At temperatures
werc
nreasured
at eachsiteby oncsingle-ended,
shieldcd
Figure L Buckiom cirque froln rhe summir of Buclihom \{ountain. The localion of the rhree reseriih sjtes are indicated.rs
n . , n - r - ' L e dl.i r h e n .J - . r c n r ' r i d . u d - . ( . .
were
thennocouple.Surfaceandsoil temperatures
collected as mean valuesof three thermocouple
junctionswired in parallelandplacedat leastl0
cn-Iapart. Thirty instantaneousleadings of surface tcmperatures(each reading evenly spaced
by I rn in a,Xm by 5 m grid) weretakenat thrce
tines duringthe day (0800, 1200and 1800)for
three days during the study pedod in eachsite to
of the surfacetemverify the representaliveness
peraturesrecordedby the datalogger.Thesetemperatureswere measuredby a themocouple in
serted within 0.3 cm of the surface. Leaf
ol four Dnriql't'irr/.4 I lq.r/.i $ere
temperirlures
also monitored (mean tenrperatureof 3 leaves/
in
cushionusing prrallel-wiredthermocouples)
cach of tbe crustedand noncrustedsites.At all
threesites,surfacetemperaturesandI). /aerl8.ltul
(sensorjnsenedI cm rnto
cushiontemperaturcs
cushion) werc also monitored lbr that period using rubbel encasedthennistorsand Hoboo elec(OnsetComputerCorp..Boume,
tronicdataloggers
MA.).
,1samplesper sitc. Soil from 5 cm depthwas collected in sealedtins. transpoftedimmediately to
the laboratory,weighed. dried (80'C for 48 h),
and reu,eighed.Theseoollectionsoccurredatier
a period of at least one wcek $,itiout precipitation. Soil moisturc content was expressedon a
dry weightbasis.
Soil Characterlzatlon
u ere
Soilnitrugenrnd pho-phoru.corl(enltalionr
per
upsite
liom
thc
on
four
samplcs
measurcd
per 5 cm of soil. Soil samples$erc oven dried,
Gravimetdc soil water content was measuredin
the middlcofthe growingseason(August19)on
Soil texture was measurcdon 5 replicate
samplesf'rornthe upper5 cm ofsoil immediately
below the cryptogamiclayer (ifpresent).Samples
were dried as above and mcchanicallysievedttt
tiactions of gravel (> 2 mrr). sand(.05 to 2 mm).
and silt plus clay (< .05 mm).
Soil organicmattercontentwasestimatedftom
in a nuftle
measurcs
accomplished
loss-on-ignition
fumace. Four samplesfrorn each site were oven
dried as above.weighed,placcdinto a lurnace at
450"Ctbr 6 hours,and rewcighed.Organicmatter contentwlrsestimatedasthe proponion oldry
weight lost on ignition in the furnace.
NutrentAnayses
CryptobioticSurfaceCrustsin Alpine Tundm
317
digestedwith a modified Kjeldhal procedure
(ParkinsonandAllcn I 975), andcolorimelrically
assessed
on an autoanalyzerfor total N and P by
thc CollegeofForest ResourcesAnalytical Labo
ratory at the University of Washington,Seattle.
This proceduremeasurestotal phosphoms and
lntlogen of organicand inorganicammoniumforms
("Kjeldhal-N").asnitlate-Nis not included.
Net nitrogenmineralizationraleswereestimated
by examiningthe changcoforganic nitrogeninto
il'rorganicfoms in soil coresenclosedin poly
ethylenebagsandburiedh sir/ (Eno 1960.Marion
andBlack )987,Jonasson
et al. 1993).Fivebags
of soil wcre buried at eitchsite July 19 andparallel soil subsamples
taken1br analysisof inirial
nutnentconditions.Theseinitial sampleswere
divided in half, with onehalftiozen and the other
halfoven dried asabove.The oven dried samples
were analyzcdas above for Kjeldhal-N. The frozcn soil wassubsequently
thaFed,air-d edat20.C
in the presenccof indicatingsilicagel. and subjected to a 2M KCI exrractionu'ith agitation1br
I hr. This extract was colodmetrically analyzed
as above lbr estimatcsof 'available" inorganic
soil ammoniunr and nitrate. Organic N was ca1culatcd by subtractionof soil KCI extractable
ammonium fiom the Kjeldhal-N value.The buried bags of soil werc collected on Septembcr5
and subjcctedto the sameanalvscs.
Plant tissuenitrogenconcentrationswere analyzed for greenleavesof six Douglasiq laerigdta
plants and threeMlrLtartia obtusiloboin eachol
the duec sitesand tbr f\ve Phkn hendersonii pltnts
in eachofthe lichenandcrustedsites.Freshgreen
leaftissuewascollectcdonAugust l9 andtranspofied to the laboratoryfor oven-drying at 70'C
fbr 48 h. Dried plant matter was digested and
anaJyzedfor N concentrationasdescribedabove
fol soils.
C r u r ta n dI i c h e nl u l r i e n te o n c ( n t r a l i o n
\ \sc r e
alsomeasured
liom samplescollectedAugust
19.
Tu'o ofthc most common crust associationswere
chosenfronrthecmstedsite,bothwith a substantial
bryophytebase.differing principally in the doninant crustoselichen component.The nlost com
moncrustcontaineda lichenwithjust squalrules
ofthe genusCladoniaandthe othercollectedcmst
containedthe wh ite-colorccllichen Ochroleichiu
(L.) Massal..At the lichensite,three
tqtsaliensis
common fi'uticoselichen spccieswere collected:
Cetraria ericetorut Opiz.,F Iavocet ruriu t uculatct
318
Gold. Glerv,and Dickson
(Belladi) Kiirnefelt& Thell. and F nivulis (L.)
Klfncf'elt& Thell. (Clew 1997.I 998).The lauer
two specieswere collectcdtogetherand nutrient
(oncenlrillion\are thus |cporte,-lli,r composire
samplesof thosctwo lichens.
Nitrogen
Fixation
Eighteenintact samplesof crust (40 cm21werc
ercisedliom threedistinctsubarcas(6 sarrples
per subarea)of the crusted site on Septcmber5
and tmnsported immediately to thc labomtory.
Thesc subareaswcre defined by a visual assess
ment of the concentrationof a foliose lichen.
Peltigera rufescens(Weis) Humb. (kno$'n to bc
capablc of nitrogen flxation) in the crusl mate
rial. A closely-reiated.species,Peltigerauphthosa
( L . r \ \ i l l d . . h a sb e e n' h o u n t o h e a r c r ) i r n l u r tant sourceof nitrogen input to birch lbrests in
northemFinland (Kallio et al. 1976).The NoPehigerct(NP) crust conlained no to very little
Peltigerc. whereasthe Moderate-Pe/rigerz(MP)
and,High-Peltigerd (HP) crustscontainedmoderatc and considcrableamountsof the lichen re
spectively.These samplcswere initially held at
3'C in the dark for 4lJ h and subsequenrlytrans
fencd to a growth chambertbr three days of acclimationprior to experinentation.Growth cham
berconditionsweresetfor 16h daysand8 h nights
with air temperaturesof 25 / 5'C (day / nighg
and irradiancesof 1000/ 0 !rmol/m:/s PPFD, resultingin 35 /5'C crusttemperatures.
Crustswerc
maintainedat maximunr hydration and high humidity by partial plastic enclosuresand rcgulaLr
rristing with distilledwater On ScpternberI l,
the nitrogenfixationcapabilityof thescsrmples
was measuredby the cetylenc reduction tech
nique(Stewanet al. 1967).The nitLrgenase
cnzyme. which facilitatesnitrogenfixation. also
catalyzesthe rcduction of acetyleDeto ethylenc.
Thus.the conversionofacetyleneto ethylenccao
be uscd as a lleasure of thc relative activity of
the nitrogenaseenzyme,and hencethe potential
mte of nitrogcn fixation. Each cmst sanple was
tdmmedto 38.5cmr and enclosedin a glassjar
into which 20 ml of acctylenewas injected.The
jars were then incubatedfor 5 h in a grou'th cabinetat 25'C air tenpemture(35oCcrusttempcrature) and 600 Fmol/mr/s PPFD irradiancc.After
thc incubationperiod.4.0 ml sanplesofjar -qas
wele removedarrdanalyzedon a gas chromatop rdphfor cth)lenecon(enlratronI,,llo\\ingr pro
cedureusedby Chapinet trl.( l99l ). Calcularions
and 1l9c/c than the crustedand noncrustedsites
respeclively.
Soil Kjeldhal-nitrogen
and phosphorusconcentrationsvaried among tlle three sites (Table
2) in parallel with organic mattcr contcnt (Tablc
I ). Lichcn site soils had 9l c/rand l.:{906/cgreater
Kjeldhal N and 707r and 4757o greater P than
crustedand noncrustedsoilsrespectively.Pattcms
ol extractablesoil inorganicnitrogenfollowed those
of tot l N, but thc diffcrenceswere considerably
smaller.Soilsfrom the lichensitehad55 and 154%
greatcrconcentrationsof KCl-extractablenitro
gen than the crustedand l]oncrustedsitesrespecrateswcrc low
tively. Soil net N-mineralization
and did not dilfer statisticallyamongthe sites
(P=.07).thoughthereu'asa trendtowardhigher
rrrcr in the hchen rite lhl]n the oth<r t\\o 'ile\
(Table2).
of nitrogenfixrtion ratcs wcre done asdescribed
by Chapinet al. (1991).Each crustsrmple was
carefully scparatedinto P r-uferccr.r,other cryptogams.and soil/debristbllowing the acetylene
reductionassay.The living componeotswereoven
dried and weighed.
Results
SoilEnvironment
The soilsofthis alpinebasinarcgenerallycoarse
tertured. with little silt and clay (Table 1). The
noncrusted
site,which hada distinctgravclysurtace,hada higherproportionolgravel sizedpar
ticles than the crusted site other two sites.The
noncrustedsite alsohad a smal1,bul significantly
greater,silt andclay contentthaneitherthecrusted
or lichcn sitcs.Accordingly, the sandcontent of
soils was lessat the noncrustedsitethan the other
two sltes.
ps
Ternperature
Relationsh
On ;l rcprcscntaliveclear,waIm day (September
2, 1995) air temperaturesat 5 cm were similar
above crusted and noncrustedsufaces through
most of the day,reachinga maximumof about
25'C in the late aftemoon (Figure 2). Soil surlace temperaturesreachcdmaximaof 34.5'C and
38.3'C in the late aftemoon at the crusted and
The mean of 30
noncrustedsitesrespectively.
instantaneoussurf'acereadingsat each site was
Soil organicmattercontentand moisturewere
much less in the noncrustedsite than in either
sitewith a continuous biologicalcover(TableI.).
ofcrypLichensitesoils,with a greaterthickness
toganrs.and higher vascularplant density had
527oand314%greaterorganicmallcr contentthan
the crustcd and noncrustedsites respectively.
Followilg the patternof organic matter contcnt.
soil moisturewasgreaterin the lichen siteby 56clr.
TABLE L Soil gra|inetric \\'aier content (H.O) ofganic mafter (ONI). and lc\rurc tir thc 3 sitesin Buckhorn cirque on August
19. 1995. Means afe presentedI 1 SE. Dillerenr lcttcrs indicatc signiticani differences(P<0.05) among sites b]
Kru,ikal-$'al1isnonparametricANO\A and Tukcy's rultiple nreancomparisons.
-t H.O
\onc.u!Ied
Cruncd
Lichen
1 1 . . 1 1 0a. 6
69.5t 3.8c
.ii Gravel
?.,ON,I
t 7 . 3r l . r a
1 8 . 0 1 1b. 7
22.,116.7
ab
6 . 5r 0 . 2 a
r 7 . 7 1 1 .b2
1 6 . 9 1 1 .c9
t: Sand
% Sih + Clay
5 6 . 2 1 1 .a0
1J0.0
t 3.6b
76.5r 6.5b
6 . 5 11 . 7a
2 . 0 1 0 . b2
Llt0.tb
TABLE L Concentradois oI sojl Kjcldhal nitrogen (N) and phosphorus(P), Kcfertr.rctable anmonium (NH,) plus nilratc
(NO.). and net niuogcn lnincralizaiion rate,i for three re\errch sites in Buclhom cirque. Means (n =.1 5)arc prc
\ented t SE. Dillcrcnl lcttcrs indicatesignificant(l'<0.05 )differencesamongsites$ithir eachnutrienl conponcnt b)
eirherANOVA or Krulkal wallis nonpafametricANO\A rnd Tukey's muhiple mcJn lumpuLi .un\
7 N
Noncrustcd
Crustcd
l-ichen
0 . l l t 0 . 0 1a
0 . 8 7 1 0 . 0b2
L66 :i 0.05c
NH + NO. i[e/s)
0 . 0 8 1 0 . 0.1r
0.:7i 0.01b
0.,+6t 0.05c
5 . 0 1 0 . a6
E . l : t0 . 5b
1 2 . 7 1 0 c. 8
Ner N-Mineralization
(US/Sdry soil/d)
0 . 1 8 1 0 . 0a2
0.17
1 0 . 0 1a
0 . 1 5 1 0 . 0a3
CryptobioticSurfaceCrustsin Alpine Tundra 319
o
.
+5 cm
NoncrustedSite
crusredsite
10
0
600
1200
1800
2400
Time of Day
F i g u r c 2 . D i u r n a l c o u r s e so f r e n p e r a n r r e sm c a s u r e di n
crusledandnoncrusledsiteson September:, 1995.
N{eanhourly values arc indic:rtedfiom readings
recordedc!er! 10 seconds.Su.lace rcnpefarure
lalues e meansoft$o sensofsand D. l.r(1(ril.1
leal tcmpcraturesafe averagc\.dues offour cush
i o n s( l l e a v c \m e a s u r e p
d e r c u s h i o n ) . A i ar n ds o i l
tenperaiures !'aluesare fiom singtc sensors.
always less than 0.6'C dilferent fronr the mean
hourly surfacevalue recordedby the datalogger
fbr all threesitesat midday (datanot shown).The
rangeof tempcraturevadation among the 30 instantancoussurfacereadingsat eachsite wasless
than Ll'C at midday.The smallvariability among
thesetempenture rcadings and the close cone
spondenccof theil mean to the dataloggermean
supportsthe use of the dataloggcrsudace tem320
Gold, Glew.and Dickson
peraturesas representativeof surtircetenperature conditionswithin cachsite.Sudacctempera
tureswercgreaterby2.2to 6.5'C in the noncrusted
site than in the crusted sitc through most of the
day (Figure 2). The crusted surfacc lagged behind the noncrustedsite in the rate of its midday
temperaturerisc, with the maximun difference
in sites of 6.5'C reachedduring thc period of
midday surfacewarning. Thcse site differences
were alsopronouncedat shallowsoil dcpths,\\'ith
late aftemoon tcmperaturesfrorn 6.5 to 7.0'C
greaterin the noncmstedsite. Midday leaf tenperaturesof D. lcer,lgctacushionsu'ere only
slightly lessin the crustedsitethanthe noncrusted
site (l 2'C). Over the entire measurementperiod. midday surfaceand soil temperatureswerc
5 to 8 and 5 to 6.5'C greater,respecrively,at the
n o n c r u . l e\di t el h J nI h c . r u . t e d. i l c d u r i n F. u n n )
days(datanot shown).Thesedifferencesdisapp c u r e de n t i r e l li n c l o u t l lL u n d i r i o n . .
Thc ground surfaceofthe site coveredby fnr
ticoselichens(the "lichen" sitc) wasnuch cooler
thanthe surfaceofthe noncrustedsiteduring both
thedayandnight with clearskyconditions(middle
,1daysof periodshown in Figure 3). This surface
cooling providedby a biological cover was much
gleater for the lichen site than the crusted site.
The diflerences in surfacetemperaturesat midday betweenthe lichen and noncrustedsiteswere
around 10-l l cC on sunny days as comparedto
the 5-8'C difference between the crusted and
noncrustedsites(Figure 2). Hou'ever,as with the
crusted-noncmsted
sitc comparison.D. /cellgara
cushlon temperaturesat the lichen site $,erc not
different through nost of the day from cushions
at the noncrustedsite. The cushionsdid experi
ence a moderatelylower nighttime temperature
(l 3'C) at the lichen sitethan the noncrustedsire
follou'ingsunnydays.
Nitrogen Fixation
Significantnitrogenaseactivity was displayedbv
a numberofcrust samplesin the Iaboratory(Table
3). Averagenirogcn fixation acrivityin the NP
and LP crusts was minor, though some samples
had mederaterates(> 20 pmol C2H2/rnr/h).
Crust
sampleswith considerable
amountsofP nrfescear
(HP) displayedvariable.but quite substantialrates
of acetylenereduction. The large variability in
acetylene
reductionratesperunit sufaceareacould
not be attributedto vaqringamountsofP ruf! rcens
in the crusts(Figure4). In general,higherrates
40
Surtace
30
20
fl
ui;
a)
o , ^
Dougtasiataevisata f
LJ
i:il:|."r3,fj.j".
20
t0
l,\,p
\h]\I\v [/l
\i
30
3l
3
August
Septernber
Frgurc 3. Dail) inslanlaneoussurtaceandD. ld.r,lSdrdcushiontemperaturesin lhe lichcn
and noncrLrs!edsitcs,
TABLE 3. Eth)lene production rates of crust sampleson a
ground suface areabasis(Ltmol/mr/hl.Means(n
= 5-6) are expressed1SE. Different letlers indi
catesignificant differences(P<0.05)amongcrust
types by Kruskal Wallis nonparamctic ANOVA
a I d T u l ( \ ' . _ u l rf l e m . - n c o m p i n . . n ,
Ethylene Production
(umoYn:,4r)
CruslTlpe
High-Pchisera
M e a n1 S E
Range
I i . l 1 , 1 . 5a
9 . 2 1 3 . 3a
225.1
5 8 8 . 6b
1 . 22 5 . 7
2 . 32 l . 0
2 7 . l 5 3 5I.
ofnitrogenaseactivity werecorelated with crusts
that containedlargeramountsofP rulescet\,6Lrt
there was no signilicant linear conelalion.
I aa{
a n a i r-n . l- I. i..-h a. -n
N
. . i.t r. ^- .J e ' r
Leaf nitrogenconcentrations
of D. loeyigata.
Minuartia obtusiloba.andPhktt hertdersonii(.0.92.57c)weregenerallywithin the lowerportionof
the rangeoftypical leafN concentrationsfor vascular plants (Table.1).In both speciesexamincd
at the noncrustcdsite,leaf N ooncentrationswere
higher than the other two sites.despitcthe lower
CryptobioticSurfaceCrustsin Alpine Tundra 321
Discussion
E
100
200
tr!
500
1000
Pehigera tufescens
1500
1000
Dry Weight (mg)
Figure 4. Thc rclalionship belween ethylene pfoductrcn of
Lor. and High-Peht6'e,.rcrust samplesandthc dry
\leight ofPlrr,,qel'd /'rlerc€n.rin the crust sample.
A lincar regrcssion!vasno! signilicanr ()r = 0.13 x
+ 6 . 8 5 ;r r = 0 . 3 3 ;/ ' = 0 . 0 6 7 1 .
TABLE,I. Concentrarionsof leaf nirrogen (t dfy weight)
fbr lhree species at the thfee fe\earch sites in
Buckhom cirque. N{eansO = 3-6) are presented
I SE. Diflerenl letters indicale significanl
(P<0.1i5) dillerences among sites withir each
spcciesb! cither ANOVA and Tuke,"-'smuldple
mean comparisonsor Sludcnls ! lcn, ND indi
catesno data availablc.
Douglutia
Luerigata
Noncruslcd 1.6t 0.09a
Crusted
0.910.0.1
c
l.ichcn
1 . 2 1 0 . 0 b5
l,tintnrtitj
jbtusilL)bu
2 . 5 I 0 . 0 9a
l.l t 0.09b
1 . 7 1 0 . 0 b9
ND
L4 + 0.06a
1 . 6 1 0 . 0 a8
valuesof soil N at that noncrustedsite (Table2).
The leaf N concentrationof plants from crusted
and lichen siteswere generallysimilar,exceptfor
a lower value in the crustcdsite plants of D.
lae gatq.
Nitrogcnconcentrations
of sorneofthe dominant fruticoselichen speciesat the lichen site (C
er icelo rultl xnd a composite sampleof E cr. rlata
+ F. nirdlis) wcrc typically low as has beenreported for suchlichens,nnging from 0.28 to 0.65%.
Cmst nitrogen conccntrationswere higher than
values fbr the fiuticose lichens and similar for
both typesof crusts(1.3 and 1.,1%)collectedfrom
the crustedsite.Both crust typeswere dominated
by bryophytes (mosses).with one containilg a
Iichen of the gents Clatlonia and the other containingthe lichenOchroleichiaupuLLiensis.
322
Gold, Glew, and Dickson
Sudace biological crusts are conspicuouscom
ponentsof communitiesin a variety of semi-arid
and cool ecosystems(West 1990, St. Clair and
Johansen1993).The natureofthesecryptobiotic
'urfree: dcpcnd.greirll)on the 'peciescornpo
sition of the non-flowering plant elements.For
instance,the relative balanceof mossesand lichenscan modify the influenceof a crust on soil
moisturcbalance(BrothersonandRushforth1983).
Dark-colored,thin cruststhat increaseabsorption
of solar radiation can increasesudacetempera
tures (Gold 1998) though this may be quite dit'terent tbr crustsdominated by light colored organisms(Kershaw 1985). Furrher,the presence
of nitrogen-fixing cyanobacteriain such crusts
can greatly increasenitrogcn input to a biological community (Wojciechowskiand Heimbrook
1984,Kershaw1985,Fritz-Sheridan
1988,Dickson
2000). Despite the common presence of
c r y p t o b i o t ircu r { a c e i.n u l p i n el u n d r ac o m m u n i ties,detailedstudiesofcrust tunction and impact
have only taken place in cold desert(West 1990,
1991)and arctjc(Gold and Bliss 1995a.1995b
Gold 1998,Dickson 2000) regions.This study
demonstratesthat the presenceof cryptobiotic
. u r l a c e sr r e l s s o c i a l e u
d i t h r l r i a l i o ni n a n u m ber of factors of the soil environment in alpine
tundra.
CrustsandtheSoI N,4oisture
Environment
The timing, patternsand availabilityofsoil moisture have fundamentalinfluenceson the compositionandproductivityof alpinecornmunities(Isard
1986,Billings1988,Walkeretal. 1993).Thepresence of cryptobiotic crusts in this alpine basin
\\"ereassociated$,ith a number of soil propenies
that influence soil moisture. Soils that occurred
under cryptobiotic surtaceshad less coa$e tex
tured particles and greater organic matter. both
o l u h i c h u o u l d s e n e l o i n c r e a : el h e m o i \ l u r e holding capacityof the soil againstdrainage.
Furthemore, the cooler surfacetemperaturesassociatedwith both typesof cryptobiotlc crustsin
this alpine basin would serveto lower evaporative soil water loss.Our limited measuresindicatedsoil moisturewas greaterfor crust-covcred
soilsthansoils underbarrenmineralsurfaces.The
degreeto which crustprcsenceis directly responsible for soil moisture variation (as opposedto
being simply associated
with it) could only be
deteminedby nranipulativefield expcriments.
Anv
increases
in soil moisturecausedby cryptobiotic
surtacesshouldfacilitateplant colonizationand
development,resultingin feedbacksto further
nrodif,vthe soil environrnent.
continuedevaporationofrhis moisturcmi-shtoffset
any increasein radiantenergyabsorptionby the
dark-colored
crusts.
Crusts
andtheSoilThermal
Envronrnent
Thc moditlcationof soil and surfacetemperatures
by cryptobiotic crustshasdirect inplications fof
flou,cring plant survival and pertbrmance,particularly in the cool environmentof an alpine 1ocation. Root growth and nutrient uptake are restrictedin cold soils (Chapin 1983).High soil
surtacetempcraturescan also posc considerable
problen.nfor alpineplants.Surfaceitndplant tempemturesabove 40'C are not unusualin alpine
locations on warm. sunny days in the summer.
Evenwhenthesclernperatures
arenothigh enough
to be immediatelv lethal they can place direct
phvsiologicalstresson plantsas well aslncreasing plantwaterloss(Kcirncr1999).
In this alpinc basin both types ofcryptobiotic
crustswere associated
with cooler surt'acesoil
conditionsduring the daytinte.Instantaneous
surface tempcraturesreachednearl1,40'C at the
noncrusted
site.while surfacemaximaof 30 and
35'C were recorded tbr the lichen and crusted
sitesrespectively.This surfacetempenturereduction $'ith crustsis thc oppositeof effectsscenin
thc High Arctic (76'N), *here a thin, dark-colored cryptobioticsurfacecausedsuface tempera
ture maxina to bc up to l2'C highcr than
noncrustedsurfaces(Gold 1998).In the High
Arctic. the thin, dark surfacesincreasedabsorption of sdar radiation comparedto the lighFcolored mineral soil surfaces.ln contrast.the lichendominatedsurfacesof this alpine basin were
coveredbv a Ioosematrix ofboth light- and darkcoloredfruticoselichensin relativelyIoosethermal contactwith the undellyingsoil surlace,keep
ing the soil surlacerelativelycool.Coolersurfaces
(andIesswind) werelikely responsiblc
for maintainingmoistersoilsin the lichensitc.Enhanced
soil moisture late in the summerprovides a further icedback to cooling thc soil surfaceas that
moisture elaporates from the soil. The heavily
moss-dominated
crustcdsitealsohadcoolcrsurfacesthan the noncrustcdsite despitethe darker
' u r l a . ' e\ ' o l o rT
. h e h r d r o p h i l i im o . s m r r r i r n t r )
effcctivelyretainsoil moistureover most of lhe
slrnmcr (Brothersonand Rushtbrth1983).The
Although thc noncrustedsoil surfacercached
potentially stressfulhigh tempcratures(>35'C).
thecanopytemperatures
ofadultplants\r'eremuch
lower. more closelycoupledu'ith air tenlperature
thanthosesudacetcmperatures.
Foliagetempera
ture of matureplants in the High Arclic was also
unatlectedby the changesin surfacetemperature
broughtaboutby thepresence
ofcrvptobioticcrusts
(Gold 1998).Transpirationalandconvectivecool
i n p i n h i g hr r c t i . a n dJ I p i n ee n v i r o n m e nsl .e r \ e
to keep well-rooted adult plants from reaching
thehigh temperatures
experienced
by thesunounding noncrustedsurfaces.The data in this study
were recordedfbllowing a pcriod of significant
rainfall that providedmoisture10sustaintranspiration and its oonsequentcooling of plant lcaf
temperatures.During sustaineddrought pcriods
(conrnon in Pacific Nofthwest summcrs) adult
planttemperaturcs
may beginto approachelevated
sudace temperaturcsmore closely. ln any case.
youngplantsinthis environment
wouldlikely be
much more sensitiveto modificationsin surface
lcmperaturcs
thanadultplants(Bell andBliss 1980,
Chamberset al. 1990). Young plants are much
smaller and consequentlyare much more ther
mally coupled to the surrounding surlace temperaturcs(Cold 1998).Futhennore,with their limited root development,
seedlingslack accessto
water.reducingthepotcntialfor evapomtivecool
ing. Heatanddesiccationarentajor nortality factorsfor alpineseedlings(Krimer 1999).The lower
surfacetemperaturemaxima ofalpine sitesassociatedwith crust surlacesshouldreduceseedling
mortality (from desiccationand thernal sffess).
while not being of such a Iargemagnitudeto in
hibit plant perfbrmancedue to low temperatures.
Thesedataindicatethat onceplantsreachan adult
size, there is little efl'ectof crusls on plant tenrperature.
Crustsand Ecosystem
Nitrogen
Dynamics
In our study the presenceof crusts is associated
with greatertotalniffogenandavailable(inorganic.;
nitrogenin the soil. Nitrogen availabilitvand
dynamicshave profound inlluences on community shuclurcandecosystem
processes
in theRocky
Mountainalpine(Bowman1992,Theodoseer al.
1996.TheodoscandBowman 1997.Steltzerand
Cryptobiuic SudaceCrusts in Alpine Tundra
323
Bouman 1998).Potentialecosystemnitrogen
inputsfiom nitrogenfixrtion in cryptobieticcrusts
havebeenestimatedto range1'romsubstantial
to
predominantin cold descn(Rychcnet al. 1978.
West 1990. 1991,Evansand Ehlcringcr1993).
arcric (stutz 1977. Liengen and olsen 1997,
Dickson 2000). subalpine(Fritz Sheridan1988)
andalpine(Wo.jciechowski
andHeimbrook 198,1)
areas(see Kershaw 1985 for overvie*). These
cstimates\\'erelargely derivedfron ratesof crust
niffogenaseactivity (acet)lene rcduction). although
EvansandEhleringer(1993)usedstableisotope
(rsN) of soil material.The large varianal1,scs
ability in acetylenereductiondatawithin sitesfrom
this alpinebasjnpreventedus fiom makingmeaningful quantjtativeestimatesof the potential nitrogencontributionby thesecruststo thegcosystem. It is evident that substantitrlamountsof
nitrogen are being fixed by lichens and
cyanobacteriain some areasof the crust. and the
high spatialvariability suggeststhat resultingefItcts on soil nitrogen availability will be patchy
within thc tundra.
In additionto directnitrogeninputs,crustscould
nroditynitrogencyclin-uby changingratesofnitrogen transti)rnrationin the soil. Ratesof nitrogenmineralization,
nitrit'icittion,
anddenitrification aremediatedby soil microorganismsandare
consequentlysensitiveto temperatureand molsturc conditions.Data from this studyindicatethat
net nitrogen mincralizaLion(the amount of N
covertedtrom organicN kr inorganictbrms minus the amounttakenup b,vsoil microorganisms)
u r r r r o tr i g n i l ' r c r n t liln f l u e n e ebd5 c r y p t o g a m i c
cover It is possiblethat the cooler surlacetemperaturcsofthc cryptogamicsitesoffsettheil nore
favorablemoisturcconditions
fbr mineralization.
resulting in mineralization rates simiiar to
noncrusted
sites.
Lelf nitrogen
c o n e e n l r u l i oonl. m ! l n )\ p e \i e \
incrcascin soilswith greaternitrogenavailability (Chapin1980).However,in this alpinebasin,
r ' r l p t h i , r t i i . i t c s u i t h B r e a t esr o i l n i t r o g e na r c
with plrntshavinglowerleafnitrogen
associated
concentrations.Greater plant. cryptogam, and
microbial nass at the two crust sitesmay result
in grcater competition for soil nitlogen, leading
to lower tissuenitrogen concentrations.Altema-
32,1 Gold. Glew,andDickson
tively,lower tissuenitrogenhasbeenreportedwith
fefiilization studiesunderconditionswhereother
factorsgoveming photosynthesis(e.9.,temperaturc. moisture) are enhancedand carbon accumulation dilutes tissueritrogen (Jonassonet al.
1999).
Nlanagement
lmplicat
ons
Crytptobiotic crusts are generallyconsideredto
be fragile and slow to recoverfbllow disturbance
(Johansen
and St. Clair 1986.Harriset al. 1987,
St. Clair and Johansen1993,Evans and Belnap
1999).Cryptobioticcrustsoccurir many alpine
aleasand thesecrustsareparticularly vulnerable
to destructionby off'-trailtravel in popularalpine
hiking and climbing destinations(Bell and Bliss
1973,Grabher 1982).Thus far, assessments
of
recreationaldamagein alpine areas(Schreiner
1974,Edwardsi 980,Cole andTrull 1992.Cole
planshavefocusedmostly
1995)andmanagement
on (impacts to, preservationof. and restoration
of) vascularplantsratherthan cryptobiotic components.
Krowledgeol theluncLional
imponrnce
of thesecrustsis vital to assessthe broader.ecosystemlevelimpactof potentialdisturbanoes
to
alpine areas.This study and others suggestimpactscouldincludechanges
in soilthermal.moisture, andnutritionalpropefiies.soil stability,biogeochemicalprocesses.and the potential fbr
communityinvasionby alienweedyspecies(Harris
et al. 1987.Parker 1996).Further detailedinfor
mation is necessaryfor land managelsto assess
potentiirlconsequences
of cross-countrytraveland
possiblemanagementaltematives.
Acknowledgements
This study was supportedby a grant tiom the researchcommitteeof the Mazamas(Portland,Or
egon).Pennissionto usethe field sitewasgmnted
by the U.S. ForestService.The tield assistance
of Julia Gold and laboratoryassistanceof Nikki
Amato,JudithHillis, Ron SIetten.andBrian Witte
is gratefully acknowledged.The encouragement,
advice and review of this study by Larry Bliss,
Ji m E r a n s l.n d J o s c p A
h m m i r l t iu c r ci n . t r u m e n tal.The thoughtfulcommentsof two anonymous
r e ri e u e r sl c d l o m r n y i m p r o v e m e n t . .
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