Coldest places on earth with angiosperm plant life

12 Pages·2011·0.68 MB·English

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AlpBotany(2011)121:11–22
DOI10.1007/s00035-011-0089-1
ORIGINAL PAPER
Coldest places on earth with angiosperm plant life
Christian Ko¨rner
Received:9December2010/Revised:26January2011/Accepted:1February2011/Publishedonline:25February2011
(cid:2)SwissBotanicalSociety2011
Abstract The highest elevation flowering plant ever Keywords Mountain climatology (cid:2) Saxifraga (cid:2)
recorded in Europe, a lush moss flora, one of the coldest Bryophytes (cid:2) Mites (cid:2) Collembola (cid:2) Fungi (cid:2) Isotopes
places of permanent animal life (collembola, mites) and
indications of mycorrhizal fungi were evidenced for the
Dom summit (4,545 m, central Swiss Alps) between solid Introduction
siliceous rock at 4,505–4,543 m, 46(cid:3) N. Cushions of
Saxifraga oppositifolia were found at 4,505 to 4,507 m While bacteria and actinomycetes can be found at around
a.s.l. A large individual (possibly[30 years old) was in 8,400 m,closetothesummitofMountEverest,andlichens
fullbloomon12August2009.The14C-datedoldestdebris were recorded at 7,400 m in the Himalayas and on top of
of the biggest moss, Tortula ruralis, suggests a 13 year Kilimanjaro (Swan 1992 and other references in Ko¨rner
litter turnover. The thermal conditions at this outpost of 2003) and in even more adverse conditions at 86(cid:3) S and
plant life were assessed with a miniature data logger. The 1,980 m elevation in Antarctica (Wise and Gressitt 1965),
2008/09 growing season had 66 days with a daily mean higherplantsneedtemperaturesabove5 (cid:3)Ctogrow,mature
rooting zone temperature [0 (cid:3)C in this high elevation their seasonal foliage and reproduce (Ko¨rner 2003).
micro-habitat (2–3 cm below ground). The degree hours Angiosperms have been recorded up to 6,400 m in the
[0 (cid:3)C during this period summed up to 4,277 (cid:3)h corre- centralHimalayan(30(cid:3) N),4,100 mintheCentralCaucasus
sponding to 178 (cid:3)d (degree days), the absolute winter (43(cid:3) N)andatseveralplacesintheAlpsat[4,200 mat46(cid:3)
minimum was -20.9 (cid:3)C and the absolute summer maxi- northernlatitude(compilationinKo¨rner2003)andatupto
mum 18.1 (cid:3)C. The mean temperature for the growing 81(cid:3) N in the Arctic (Bay 1992) or 68(cid:3) S in the Antarctic
period was ?2.6 (cid:3)C. All plant parts, including roots, (SmithandPoncet1987).Bryophytesholdanintermediate
experience temperatures below 0 (cid:3)C every night, even position, commonly found in higher locations/higher lati-
duringthewarmestpartoftheyear.Onclearsummerdays, tudes than the uppermost/highest latitude angiosperms.
plantsmaybephysiologicallyactiveforseveralhours,and Therearerecordsupto4,559 mfortheAlps(Vaccari1914)
minimumnighttemperaturesareclearlyabovethefreezing or for 84.4(cid:3) S at 700 m elevation, close to the South Pole
tolerance of Saxifraga oppositifolia in the active state. In (WiseandGressitt1965).Animalsandmicrobesarefound
comparison with climate data for other extreme plant wherever traces of plants or their debris occur, with mites
habitats in the Alps, Himalayas, in the Arctic and Antarc- holding the low temperature record at 85.3(cid:3) S and 975 m
tic, these data illustrate the life conditions at what is elevation in the Antarctic (Wise and Gressitt 1965). The
possibly the coldest place for angiosperm plant life on presentarticlereportswhatarelikelythehighesthabitatsfor
earth. an angiosperm and for perennial invertebrate animals in
Europe, and it explores the temperature conditions in rela-
tiontoreportsfromothersitesoflowtemperaturelimitsof
plant life. The data illustrate the life conditions at the cold
C.Ko¨rner(&)
edgeofhigherplantlifeanditsdependentanimalandfungal
InstituteofBotany,UniversityofBasel,Basel,Switzerland
e-mail:[email protected] decomposercommunity.
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12 AlpBotany(2011)121:11–22
Highelevationrecordshavetobeviewedfromaclima- although leaf photosynthesis is active at sub-zero tem-
tological, rather than an elevation perspective, simply peratures and may reach 30% of full capacity at 0 (cid:3)C
because it is the microhabitat’s climate rather than meters (references in Ko¨rner 2008).
above sea level that drive life. This is best exemplified by Successful reproduction is far more sensitive to both
the high elevation treeline, which may be found at 700 m actual temperaturesandtheirduration.Themere existence
a.s.l. near the northern latitude polar circle and reach offloweringplantswithflowersatwhatseemslikethecold
4,800–4,900 ma.s.l.inTibetandBoliviaatotherwiserather edge of life does not tell us whether these plants are able
similar growing season temperatures (Ko¨rner and Paulsen to produce viable seeds. The whole process from break
2004;HochandKo¨rner2005;Mieheetal.2007).Inthecase of dormancy, bud swelling, flowering, pollination (if nee-
of small stature plants, climatological data from weather ded), fertilization, histogenesis to seed maturation needs
stations are not useful, because temperature in low stature 5–6 weeks with above freezing temperatures at the mini-
vegetation,incombinationwithtopographyeffects,deviates mumformosthighelevationtaxa(WagnerandTengg1993;
systematicallyandpositivelyfromairtemperaturebyupto Wagner et al. 2010). Thus, quite often, plants at very high
8 Kacrossafullseason(ScherrerandKo¨rner2010a,b),with elevation may emerge from seeds introduced from lower
temperatures in sheltered locations during calm, sunny elevationsources.However,thefactthattheseplantsgrow
periods periodically not very different from low elevation where they are, indicates that germination and seedling
lifeconditions(Ko¨rner2003).Keytolifeinsuchcoldplaces establishmentwassuccessful.Successfulestablishmentmay
istheabilitytoutilizeveryshortspellsofwarmth,withthe havebeenconfinedtooneexceptionalseasonwithinseveral
longer-termmeantemperaturesortheinclusionoftemper- decades of unsuitable seasons, with the remainder of life
atures during dormant periods bearing little physiological being confined to vegetative spreading (clonal growth).
andecologicalmeaning.Hence,assessingthecoldlimitsof Such episodes are near to impossible to capture in a mea-
higher plant life needs in situ temperature records, at rea- surement campaign, and they may depend more on snow
sonabletemporalresolution,suchasofferedhere. coverpeculiaritiesthanontemperatureanomaliescaptured
Another important distinction is physiological activity byweatherstations.Successfulseedmaturationhasnotyet
versus growth and growth versus reproduction. Respira- been reported from any continental-scale high elevation
tion has been found to be ongoing in microorganisms limitofplantlife.
down to -39 (cid:3)C (Panikov et al. 2006), and there is no This study emerged from trying to verify an elevation
reason why this should not be the case in mitochondria of recordforhigherplantlifenearthesummitoftheDom,the
higher plants. Photosynthesis is known to continue in highestmountainwithintheSwissborder(4,545 ma.s.l.),in
chloroplasts for as long as the intercellular space is not sight of the Matterhorn (4,478 m a.s.l.). Anchisi (1985)
occluded with ice, which happens at around -5 to -8 (cid:3)C mentionsarecordofSaxifragabifloraobservedandreported
in cold-adapted plants (Larcher 1985; Ko¨rner 2003). If bythemountainguidesGregoireandPierreNicolierinthe
rated by temperature only, algae living in snow are pos- late1970sforanelevationof4,450 ma.s.l.PierreNicolier
sibly marking the cold ‘edge’ of eukaryotic life on earth stilllivesinSion(Valaise,Switzerland)andremembershis
(Kol 1935; Jones et al. 2001). To my knowledge, no climb,butalsothathecouldnotseetheplantsagainonthe
higher plant has ever been found to grow (i.e., form new occasionoftwolaterclimbs.Thelocationofthisfindingwas
cells or tissue) below 0 (cid:3)C, but some unicellular snow almost 200 m higher than the record until then for several
algae have been shown to exhibit optimal growth (as species on Finsterahorn at 4,270 m elevation reported
rated by increase in cell number) at temperatures as low by Werner (1988; several Saxifraga species, species of
as ?1.5 (cid:3)C (Leya 2004; cf. Ko¨rner 2008), and polar Androsace,Gentiana,AchilleaandRanunculus,referenceto
marine algae thrive at year round temperatures between 1 earlydiscoveriesbyLohmeier1872andCalberla1873).
and 4 (cid:3)C, supporting a rich animal food web. In addition, When I climbed the Dom in 2008 with Juerg Anderegg
collembola are known to live on snow and ice (Eisenbeis (Interlaken), fierce storm and dense fog prevented us from
and Meyer 1999; Kopeszki 2000). Higher plants, with descendingfromthesummittotheplantlocationdescribed
combinations of assimilatory and heterotrophic tissue tousbyPierreNicolier.Sowelefttwodataloggers(onenot
exhibit very little growth below 5 (cid:3)C, although roots in yetrecovered)attwopositions(at4,543 ma.s.l.)within3 m
some species had been found expanding very slowly even distance from the summit, collected samples from a sur-
at temperatures as low as 2 (cid:3)C (Alvarez-Uria and Ko¨rner prisinglylushmossfloraintheE-faceofthesummit(Fig. 1)
2007 and references therein). Temperatures between 5 anddescendedthenormalroutetotheDomcabinat2,960 m
and 7 (cid:3)C have often been treated as zero points of life (in a.s.l. During the following summer, 2009, Juerg Anderegg
the sense of growth and development), and this appears to climbedtheDomviaTa¨schhornusingthesouthroute.Just
hold for any cold-adapted plant from winter crops to 40 minelevationbelowthesummit,at4,505 ma.s.l.,55 m
treeline trees and to the nival flora in high mountains, abovethesupposedpreviousplantrecord,hefoundcushions
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AlpBotany(2011)121:11–22 13
Fig.2 SaxifragaoppositifoliaonDomdeMischabel(Switzerland)at
4,505–4,507melevation,12August2009
Sitesandtemperaturestudies
TheDommassif
The Dom summit (4,545 m, 46(cid:3)504000 N; 7(cid:3)51024 E00;
CentralSwissAlps,Fig. 2a)belongstotheMischabelgroup
andis locatedat themain divide ofthe Alps ca21 kmNE
from the Matterhorn (4,470 m) in Canton Valais. Due to
regular clouds, the summit is commonly accessed in a 6-h
climb via its NE snow flank from the Dom cabin via
Fig.1 Bryophytes(seeTable1)ontheE-faceoftheDomsummitat Festijoch(3,700 ma.s.l.)startingat3a.m.,andreachingthe
4,543m elevation and the annual course of hourly temperature
summitby9a.m.,justbeforecloudsfrequentlyclosesight.
readingsin2–3cmsoildepth.Below:diurnalcoursesbetween5and
Along this route, five temperature loggers were placed of
25 August 2008, including two good and one bad (12–18 August)
weatherperiods whichthreecouldberecoveredsofar:twoat3,060 ma.s.l.
andonefromthesummitat4,543 ma.s.l.
The low elevation reference site in the sub-nival belt
ofSaxifragaoppositifoliainfullbloom(Fig. 2).Hetooktwo (3,060 m) was at the edge of a glacier moraine above the
samples,onefromeachofthetwobiggestcushions,lessthan Dom cabin amongst open scree and rock flora, counting
5%oftheplants,withattacheddebris,andhecollectedone approximately 50 species of angiosperms in the surround-
ofthetwosummitdataloggers.Thesecondloggercouldnot ings of the two logger positions. The logging period was
be accessed because the weather turned bad again. An from 4 August 2008 to 22 August 2010. The loggers were
attempt to collect it in 2010 also failed. To place these buried2–3 cmbelowgroundundermossorgrass,oneneara
summitrecordsofplantsandtemperaturesincontext,Ialso Saxifragaoppositifoliacushion,inarocknichefacingSSW,
present records from the sub-nival belt at 3,060 m, just theotheroneat2 mdistancefromthefirst,attheedgeofa
abovetheDomcabin,andreadingstakenwiththesametype verticalrock,opentothewest,with20angiospermspecies
ofdeviceandinthesamewayatthelong-termobservatory counted within 1 m from the logger on the level ground
atJungfraujoch at3,460 m,anddatafromthearcticdesert around.
collected in Svalbard (78(cid:3) N). Hence, together with data Theloggeratmid-elevationonFestigrat,3,700 m,could
fromtheliterature,theanalysisaimsatnarrowingtherange notyetberecovered,butthispositionisworth mentioning
ofmostextremelowtemperaturesatwhichhigherplantscan for the uppermost location of an angiosperm on this route
live. to the summit: A very big (isolated) cushion of Saxifraga
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14 AlpBotany(2011)121:11–22
oppositifolia forming a sort of curtain, hanging 15–20 cm summitstoppedrecordingon17July2009,sowhenitwas
from a small rock under a larger protruding rock, facing collected on 12 August 2009, 18 days were missing to
WSW,receivinglotsofmeltwater. completethefullyear,beginningon5August2008.Given
Byitspeculiarshape,theDomofferssnowfreelocations thisdatagaprightinthemiddleoftheseason(statistically
withlosesubstrateatanelevationpermanentlycoveredby muchbetterthanifeithertheearlyorlatepartweremissing),
barerockoriceandsnowinmostother,evenhighersummits it was assumed that the frequency distribution of tempera-
such as those of Mont Blanc (France). However, the south turesduringthegapissimilartothatbeforeandafterthegap.
flanksoftheMonteRosaMassifshouldoffersimilarhabitats Hence,thelengthofthegrowingseasonandthermalsumsof
at similar or even slightly higher elevation (Italian side of the season were scaled to the period including the 18 day
the Dufourspitze summit 4,634 m a.s.l. or Punta Gnifetti datagap.
4,559 ma.s.l.).Loggerswereplacedon5August2008,and Thedefinitionofgrowingseasonisratherdelicateunder
the one from a narrow E-facing rock crevice, with a rich such extreme life conditions. Conventional thresholds for
bryophyte and lichen flora (Fig. 1), ca 2 m beneath the the onset and end of the season (e.g., last and first frost or
summit at 4,543 m, was collected on 5 August 2009. The absence of snow) would not work here. We adopted four
otherloggeronasmall,southfacingterraceamongrocks,ca definitions and offer data for all four. The first two defini-
3 msouthofthesummit(ca4,543 ma.s.l.)isstillinplace. tionsareusingthefirstandlastdaywitheitheramaximum
temperatureofatleast3 (cid:3)Coradailymeanof[0 (cid:3)Cirre-
ComparativelocationsatJungfraujochandinSvalbard spective of the weather between these dates. The third
definition represents the number of days per year with a
Rocks behind the Jungfraujoch research station (3,469 m maximumtemperatureofatleast3 (cid:3)C,andthefourthdefi-
a.s.l.,46(cid:3) N)offerverysimilarplanthabitatsincrevicesas nition stands for the number of days with a daily mean
foundneartheDomcabin.Twologgerswereinstalledunder temperatureof[0 (cid:3)C.Forthelattertwodefinitions,degree
light grass (Poalaxa),herb (Draba sp.) and moss cover in hoursanddegreedayswerecalculated(thesumoftemper-
summer 2010 (8 July to 22 September), but given their aturesabovethethreshold,with(cid:3)d = (cid:3)h/24).Astheresults
readings were identical, only readings of one are reported will show, these definitions have only moderate effects on
here. An additional logger was installed in complete theseasonlength,butsubstantialeffectsondegreehours.
shade,2 maboveground,behindthestationasareference
(meteorologicalairtemperaturestandard).
ThearchipelagoofSvalbardextendsto80(cid:3) Ntowardthe Biologicalsamples
North pole, and hosts polar deserts at its outskirts, where
only very few species can survive, among them Saxifraga TheSaxifragaoppositifoliavoucherfromtheDomsummit
oppositifolia,PapaverdahlianumandLuzulaconfusa.Iwill isdepositedattheHerbariumoftheInstituteofBotanyofthe
show temperature data from alocation at 450 ma.s.l. near University of Basel. Bryophytes had been identified and
Longyearbyen,where cafive species ofhigherplants have vouchersdepositedatthemossherbariumoftheInstituteof
been found (78(cid:3)140 N, 15(cid:3)140 E; Gruve three fjellet at SystematicBotanyattheUniversityofZu¨rich.
Plateau-Fjellet).Twodataloggersofthesametypeasused The debris and attached substrate under Saxifraga
ontheDomhadbeenplacedintheverysameway,2–3 cm oppositifoliacollectedat4,505 melevationwasexaminedfor
under the sparse vegetation of this arctic semi-desert animals, seeds and traces of fungal presence under a dis-
(readingshardlydiffered,soonlythemeanforbothloggers sectingandalightmicroscope.Theorganicdebriscontaineda
isshownhere). surprisingly high density of collembola and an incomplete
partofonemite,whichhadbeensentforidentificationtothe
Temperaturemeasurements Senkenberg-Museum(Go¨rlitz,Germany),andvouchersam-
ples of collembola in 70% ethanol are deposited there.
All temperatures were recorded with single channel tem- Ethanol-stored specimen were dried and used for scanning
peraturedataloggers(Tidbit;OnsetComputerCorporation, electronmicroscopy.Fungaltracesandseedswereidentified
Cape Cod, MA, USA; -30 to ?70 (cid:3)C, 0.2 K resolution, at the agricultural research center Agroscope (Reckenholz,
3 cmdiameter,1.5 cmthickness)astheyhadbeenusedfor Switzerland),picturestakenwithalightmicroscope.
previoussurveys(Ko¨rneretal.inNagyetal.2003;Ko¨rner MossesonDomformcompact,upto4 cmthickcushions
and Paulsen 2004). These completely sealed instruments withremainsofpreviousgrowingseasonswelllayered.This
wereprogrammedtorecordtemperaturesathourlyintervals made it tempting to explore the 14C age of the lowermost
andwerecalibratedinicewaterforzerodegreebeforeand layer using 14C signals from the 1956 atmospheric nuclear
afterinsituexposure,buttherewerenodeviationsfromzero explosions.ThisanalysiswasdoneattheLaboratoryforIon
[0.2 K. Unfortunately, the brand new logger on the Dom Beam Physics, Swiss Federal Institute of Technology,
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AlpBotany(2011)121:11–22 15
Zu¨rich using accelerated mass spectrometry. The stable far,andtheclimaticconditionsdescribedbelowplacethese
carbonisotoperatio(13C/12C)ofplanttissueindicatesCO plantsatthemostextremelifeconditionsobservedonearth,
2
uptakeefficiencyandithadbeenshown,thatthed13Csignal wherehigherplantsdooccur.Theexactlocationisanareaof
clearlyincreases(i.e.,becomeslessnegative)withelevation about12 mlengthonthesouthridge,afewmeterseastofthe
and, thus, atmospheric pressure, with the slope of change Swiss GPS coordinates 6320475/1040747, ca 50–100 m of
steeperinthegenusofSaxifragathaninothergenera(Zhu climbing distance to the summit, 2 m east from an out-
et al. 2009). Hence, this highest sample of the European standing rock column with a permanent steel loop for
continentwasexaminedforthissignalbymassspectrometry climbers,rightontheonlyfeasibleclimbingroute.Theslope
following the procedure as described by Zhu et al. (2009; with plants is SE- to E-exposed (sheltered by rocks in the
twomixedsamplesofgreenshootmaterialthatgavesimilar west).Thereareseveralindividualsallgrowingonshallow
numbers). pans of loose sand between the rocks. As one loosens the
sand, a dense felt of roots appears, attached to the rock
surface,similartowhatcanbeseenattheperipheryofpot-
Results boundplants.
Thed13CvalueforSaxifragafoliagecameatasurprise:
Organisms -29.6 ± 0.1%, an exceptionally negative value for high
elevationangiosperms,similartomeansforleavesoflowest
Lifeatthisextremelyhighhabitatturnedouttobequiterich elevationplants with good water supply. Hence, the signal
(Table 1).Themossesandlichensidentified(inlichensonly doesnotshowanupslopecontinuationofthecommonele-
thetwomostobvious),allbelongtorelativelywidespread vationalincreaseinCO -use-efficiency(assuggestedbyless
2
taxa. The small fraction of fresh moss cushions of Tortula negatived13C),despitetheca43%reductioninatmospheric
ruralis (the biggest species; Fig. 1) were 20–30 mm thick, pressure and partial pressure of CO at this elevation. The
2
shrunkto10–15 mmwhenair-dried,withannualincrements Tortula ruralis moss revealed a d13C of -25.66 ± 0.2%
of 0.5–1.5 mm in dry state (presumably 1–3 mm in fresh (two mixed samples) more similar to common high eleva-
conditions),asjudgedbythesizeofthecurrentseasongreen tiond13Cinangiosperms.
top. The active layer consisted of 5–15 scale-leaves per The plant shown in Fig. 2 had dead last year flowers,
shoot.Theoldestattacheddeadmaterialatthebottomofthe flowerbudsandopeningcurrentyearflowers.Thesubstrate
cushion was ca 13 years old, based on 14C-dating (mixed underneath contained seeds. Compared to a reference seed
samplefromca20mossshoots). collectionattheInstituteofBotany,Basel,theseseedswere
TheindividualsofSaxifragaoppositifolia(Fig. 2)found smaller and their base was clearly shrunken (narrowed),
arethehighestlivingangiospermplantsofEuropeknownso suggesting pre-mature shedding, although the brown testa
had the typical surface structure of S. oppositifolia seed
(Fig. 4).
Table1 List of organisms recorded at the summit of the Dom
(4,505–4,543m)on12August2009 The collembola species living in the Saxifraga debris
was identified as Thalassaphorura zschokkeii Handschin,
Group Species
a rare species, known from high elevations only (Figs. 3,
Angiosperms SaxifragaoppositifoliaL. 4; Kopeszki 2000). Its taxonomic nature came as a
Bryophytes Tortularuralis(Hedw.)P.Gaertn.,B.Mey& remarkable finding to experts, and this species can now be
Scherb.S.L.(Syn.T.norvegica)
attributed to be one of the highest living animal species in
BryumbicolorDickss.l.(Syn.B. a permanent habitat in Europe. The other animal found is
dichotomumHedw.)
a mite, belonging to the Oribatida group, with only one
unidentifiedspecies,cf.B.argenteum
individual in the debris examined, hence is occurring at
Lichens Xanthoriaelegans(Link.)Th.fr.
much lower density than collembola (Fig. 4). The sub-
Leprariaaff.caesioalba(B.deLesd.)
strate of the ca 5 9 5 cm cushion sample contained at
Laudon
least 30 collembola individuals (and only one mite), so
Otherunidentifiedspecies
the total collembola population on Dom will be several
Fungi Ascomycota,2speciesincl.onepathogenic
hundred individuals at least, indicating prosperous
(Sphaerotheca)Glomeromycota,5species
incl.Glomus,Diversispora,Archaeaspora reproduction.
andParaglomus FungiassociatedwithSaxifragaoppositifoliabelongtoat
Arthropods Collembola:Thalassaphorurazschokkei leasttwogroups,thedarkseptatehyphaetype(Ascomycota)
Handschin
and arbuscular mycorrhiza (Glomeromycota) as evidenced
Mites:Acariformes,Sarcoptida(including
by spores (Fig. 4). There were plenty of spores or similar
formerOribatidaspecies)
structures,someofunknownnature.Onallrootsrecovered,
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16 AlpBotany(2011)121:11–22
Fig.3 SEMphotographof
ethanolpreservedspringtails
(collembola)ofthespecies
Thalassaphorurazschokkei
(photobyD.Mathys,Zentrum
fu¨rMikroskopie,ZMB,
UniversityofBasel),ahabitus
ofT.zschokkei,seealsoFig.4b,
btibiotarsusandclaw,
csensoricpostantennalorgan
with19vesicles,dantennal
segmentIIIandIVwith
antennalIIIorgan,
epseudocellus(anepicuticular
structurefordefense),note:
cuticlewithtypicalhexagonal
arrangementoftriangular
granules
Fig.4 Microscopicorganisms
foundinloosesubstrateunder
Saxifragaoppositifolia:aan
Oribatidamite,bcollembolaas
inFig.3,cseedsofS.
oppositifolia,dCleistothecium
(ascomycota),eandfsporesof
arbuscularmycorrhiza
(Glomeromycota;photobyF.
Oehl,Reckenholz,Switzerland)
123
AlpBotany(2011)121:11–22 17
Table2 Soil temperature records (2–3cm depth) from the Dom summit 4,543m and the nival belt at 3,060m at the base of the Dom,
Jungfraujoch3,460m(soilandair),theHimalayan5,960mandSvalbard450mforthegrowingseason(variousdefinitions)
Domtopsoil Domlowsoil Jungfraujochsoil Jungfraujoch2m Himalayasoil Svalbard*soil
4,543m46(cid:3)N 3,060m46(cid:3)N 3,460m46(cid:3)N air3,460m46(cid:3)N 5,960m32(cid:3)N 450m78(cid:3)N
Absoluteminimum((cid:3)C) -20 -5.3 – – -20.0 -13.0
Absolutemaximum((cid:3)C) 18.1 25.1 25.8 12.4 11.8 12.0
Seasonalmean((cid:3)C) 2.6 6.7 5.3 0.6 4.0 4.8
Meanofwarmestmonth((cid:3)C) 2.8 9.5 7.2 2.3 – 4.7
Durationofgrowingseason
(a)first/lastdayT C3(cid:3)C 72 139 80 79 82 47
max
(b)first/lastdayT [0(cid:3)C 73 139 80 79 82 58
mean
(c)daysT C3(cid:3)C 62 122 60 43 80 46
max
(d)daysT [0(cid:3)C 66 122 79 37 81 51
mean
In(c)numberofhT C3(cid:3)C 585 2,200 969 546 1,085 893
max
In(d)numberofhT [0(cid:3)C 1,053 2,652 1,774 926 1,684 1,189
max
In(c)degreedays((cid:3)d) 103 620 261 60 144 99
In(d)degreedays((cid:3)d) 178 870 387 136 290 210
TheHimalayandatawereprovidedbyJ.Dolezˇal
*Svalbardexperiences24hdaylightinsummer
there was clear indication of mycorrhization. There were depth was quite remarkable, reaching a maximum of
alsopollengrains(includingconiferpollen). 18.1 (cid:3)C(6August2008),again,withlikelyhighertemper-
atures occurring amidst the cushions of mosses and of
Microclimate Saxifraga during periods of direct insolation. The lowest
everrecordedtemperatureduringtheyearwasthe-20.9 (cid:3)C
The temperature conditions on the Dom summit, as repre- winter minimum (15 February 2009), not as cold as one
sentedbythesignalsofthesingledataloggerthatcouldbe mightexpectatsuchhighelevation,mostlikelyduetosnow
recovered,shouldbesimilartowhatSaxifragaexperiences cover (Table 2). The transition between the dormant and
at only 35–40 m elevation below (Fig. 1). Both, Saxifraga growingperiodwasveryabruptduetothedisappearanceof
and the bryophyte community described above may profit snow as indicated by the strong diurnal oscillation of tem-
from the relatively long snow free conditions on this steep peratureswhensnowisabsent.
escarpment and from the more frequent sunshine hours on At3,060 m,i.e.,atca1.5 kmlowerelevationinthesub-
east-exposedsitesduringclearmorninghours(thesummitis nivalbelt,theclimateexperiencedbyplantsisclearlymuch
frequentlyincloudsfromlatemorningonwards). warmer (Table 2, Fig. 5). However, given the rather dif-
A detailed analysis of the temperature records for the ferent snow cover and microhabitats, there is no point by
growing period revealed that life at this elevation incurs pointordaybydaycorrelation,notevenduringthegrowing
daily exposure to freezing temperatures of all plant organs
from flowers, leaves, shoots to roots, including the micro-
fauna. Of the 62–73 days growing season (depending on
definition, Table 2), there was no frost-free day at 2–3 cm
substratedepth.Becauseofradiative coolingatnight,foli-
age and inflorescence temperatures will have been lower
thanwhatissuggestedbythedataoftheburiedlogger.Over
the66 dayperiodofdayswithatleastperiodicallyunfrozen
soil,themeantemperaturewas2.6 (cid:3)C.Degreedaysabove0,
5and7 (cid:3)Caccumulatedto178,60and35 (cid:3)doverthatsame
period.Whileseasonlengthisrelativelysimilarforthefour
different definitions, the total number of hours with tem-
peraturesabove 0 (cid:3)C is almost twice as high as that above Fig.5 Diurnal courses of plant temperatures at 2–3cm substrate
depth under vegetation at 3,060m in the sub-nival belt of the
3 (cid:3)Catthis4,543 mlocation,illustratingthedominanceof
Mischabel(Dom)massifduringaperiodofgoodweatherinAugust
ground temperatures between 0 and 3 (cid:3)C as seen in the
2008, dashed line, and the concurrent temperatures at the Dom
histogram inserted in Fig. 1. Ground warming at 2–3 cm summit(4,543m)
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18 AlpBotany(2011)121:11–22
Fig.7 Soil (plant) temperature, 2–3cm below ground in an arctic
semi-desertinSvalbard(450m),withSaxifragaoppositifolia,Luzula
confusaandPapaverdahlianum(note,thereis24hdaylight)
Table 2. The air at 3,460 m is substantially cooler
(136 (cid:3)d[0 (cid:3)C)thanthe2–3 cmrootingzonetemperature
ontheDomsummit(178 (cid:3)d)at1 kmhigherelevation.The
Fig.6 Air (2m) and plant temperature (2–3cm under sparse plant
airtemperaturesmeasuredatthesametimeattheJungfrau-
cover,S-exposed)atJungfraujoch(3,460m)duringthe2010growing
season. Note the higher plant temperatures compared to air joch meteorological station at 3,580 m correlated very
temperature closely with the air temperature measured here (T =
3460
1.01 ? 0.98T , r2 = 0.93), with the zero displacement
3580
season(datanotshown).Periodically,evenhighertemper- largelyreflectingthe120 mdifferenceinelevation(ca1 K).
aturesareobservedontheDomsummit(Fig. 5),illustrating Using the long-term meteorological records for June to
theeffectsofcloudsandexposure.Aremarkabledifference September temperature at Jungfraujoch, the summer tem-
is seen in winter: presumably due to the heavy snowpack, peratures during the 2008/2009 measurement period are
plants at this lower location hardly ever freeze, with root matchingthemeanforthelasttenyears(2000–2010),andare
zone temperatures for most of the winter around 0 (cid:3)C. slightly(\0.5 K)warmerthanthemeanoftheprevioustwo
Summertimemaximaarefarmorepronouncedatthislower decades(1979–1999).
elevationandreach25.0 (cid:3)C. ThesiteinthepolardesertinSvalbardisclearlywarmer
Seasonalanddiurnaltemperaturecoursesatthe3,460 m than the Dom summit with a mean growing season (only
a.s.l. Jungfraujoch (Fig. 6) and in Svalbard (Fig. 7) are 46–51 days,dependingondefinition)temperatureof4.7 (cid:3)C,
takingapositionbetweentheloweranduppermostlogging largely duetothe 24-hdaylength and thus, greatly dimin-
site at the Dom. The data from Jungfraujoch illustrate the ished radiative cooling during the polar ‘night’, although
large contrasts between air temperature (not available for with a lower solar angle than during the polar ‘day’, con-
any other location) and plant temperature (Fig. 6). Daily tributingtodiurnalvariationintemperature.
meantemperatures2–3 cmbelowplantsexceedthoseofair
temperatureonaverageby5 K,andmaximumtemperatures
(warmest hourly reading per day) are 13 K warmer in the Discussion
plants’ rooting zone than in air, hence, confirming that air
temperaturehaslittlepredictivevalueforplanttemperature It does not come at a surprise that Saxifraga oppositifolia
at such high elevations.For airtemperature, thisalso finds holds the high elevation and presumably low temperature
expressioninthelowestdegreedaysofalldatasetsshownin record of Europe. It also is one of the two polar high
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AlpBotany(2011)121:11–22 19
elevation record species in Svalbard (the other is Papaver undermossesstayscolderthanwithout(Gornalletal.2007).
dahlianum, at 915–940 m at 78(cid:3) N; Sunding 1962). The A similarly high elevation record for moss (Grimmia
Arctic high latitude record of angiosperm life including S. incurva) occurrence was reported by Vaccari (1914) for
oppositifolia is at Greenland, at 83(cid:3)380 N under maritime Punta Gnifetti (4,559 m, Monte Rosa). The species most
influence(Bay1992).Butatthislocation,onlyca7(cid:3)southof vigorously growing on the Dom summit, Tortula ruralis,
the North Pole, 50 angiospermspecies have been recorded was alsorecorded byVaccari(1914)ata maximum eleva-
accordingtoBay. tionof3,559 monMonteEmilius,alsointhewesternAlps.
Saxifraga oppositifolia had been examined intensively RecordmosselevationsfortheAlpswherealsoreportedfor
for its low temperature resistance, and it can be rated as the (lower) eastern part on the summit of Weisskugel
100% freezing resistant. During winter dormancy this spe- 3,734 m (Rhacomitrium lanuginosum, Grimmia doniana)
cies had been found to survive dipping in liquid nitrogen and the (higher) western part on Balmenhorn 4,231 m
(Larcheretal.2010),andlowtemperatureepisodesduring (G. doniana; Pitschmann and Reisigl 1954; Maier and
thegrowingseasonaremuchwarmerthanwhatthisspecies Geissler1997).Accordingtothe14Cdating,theoldestpart
can tolerate. On the one hand, its small size, slow clonal of individual 25 mm long shoots may not be older than
growth but lush flowering, soon after snowmelt (from pre- 13 years. However, in the light of its size and spreading
formed buds, early flowering phenotype, Molau 1993; (Fig. 1) and the slow growth, the hump-shaped cushion as
Gugerli 1998) appears well suited for life under such con- such must be much older. If one assumes a similar rate of
ditions. Yet, successful reproduction is highly unlikely. It vertical and horizontal expansion of the clone, a 75 mm
wasshownthatseedsmaytakeupto11 weekstomaturein cushion radius would correspond to half a century. During
thisspecies(WagnerandTengg1993),muchlongerthanin thisperiod,theclimateclearlybecamewarmerintheSwiss
other high elevation species (Ladinig and Wagner 2005) Alpsthanitwasbefore(Beniston2004).
suggesting that successful seed production must be rare (if In the study year (a rather ‘normal’ year, see Jungfrau-
possible at all) at such elevations, and,thus, recruitment is joch,below),thetemperaturesrecordedattheDomsummit
likely to depend on seed sources from lower elevation. wereharsherduringthegrowingseasonthanthosemeasured
Although Saxifraga oppositifolia had the shortest onMt.Brunnenkogel(3,440 m,O¨tztalAlps,Austria,similar
(6–10 days) pre-floration period (from snowmelt to flow- latitude)byLarcherandWagner(2009),andsimilartothose
ering)ofseveralextremehighelevationtaxa,itexhibitedthe measured in the Ladakh Himalayan (5,960–6,030 m) by
longest histogenesis period (32 d), and total seed develop- Klimesˇ and Dolezˇal (2010), in both cases at the regional
ment period (46 d, excluding the period until zygote upper limit of plant life. The Himalayan data have been
formation) of several other Saxifraga species in the sub- collecteddeeper(-5 cm)insoilabovepermafrostand,thus,
nivalbelt(Wagneretal.2010).However,wedonotknowif should be cooler than the corresponding 2–3 cm depth
theindividualsfoundatDombelongto‘faster’ecotypesas temperatures recorded in the Alps and in Svalbard. On
discussed by Wagner et al. (2010). Though traces of seeds Brunnenkogel minimum plant canopy temperature was
werefoundinthedebris,theverylatefloweringinthestudy mostly above zero (extreme -4.5) during midsummer,
year(midAugust)andthedistortedshapeoftheolderseeds maxima reached 28 (cid:3)C (extreme 31.4 (cid:3)C) with 43% of all
foundunderthecushionmakeitveryunlikelythatseedsare hoursbetween0and5 (cid:3)Candagrowingseason(inthiscase
abletomatureatthislocation,exceptperhapsunderunusual snow free period) mean of 3.6 (cid:3)C. The winter minimum
weatherconditions.Thefact thatnootherplantsarefound (undersnow)was-15 (cid:3)C.
than those within that ca 12 m zone on the ridge, suggests For the Himalayan site, the growing season, defined in
that local reproductive propagation is rather limited. The exactly the same way as on Dom (Table 2), lasted longer
extremely tiny seeds may facilitate spreading by wind and (80–82 days) and the hours above the same thresholds as
cause this to become a very successful pioneer species, well as the degree days indicate a substantially warmer
obligatorilycontributingtosummitflorasandtohigharctic microclimate,withaseasonalmeansoiltemperatureat5 cm
deserts. According to Wagner et al. (2010), Ranunculus depthof4.0 (cid:3)C(andaminimumof-18.1 (cid:3)Cinwinter).The
glacialisorSaxifragabiflorawouldbeinafarbetterposi- authorsnotedthatsoiltemperaturedroppedbelowfreezing
tiontoproducematureseedsatsuchanextremelocation. every night during summer, presumably also related to the
In contrast, the well developed bryophytes right at the permafrostclosetothesurface(mentionedbytheauthors).
Dom summit do not belong to a specialist category and Soil temperatures exceeded 2–4 (cid:3)C every day during the
reflectthegeneraltoleranceofmossestoveryshortgrowing growing season, but only for a few hours. Top soil and
seasonsandtoawidespectrumofharshhabitatconditions. canopy temperatures must have been considerably warmer
Their occurence rather seems to reflects random effects. thanthis-5 cmrecord.
Mossoccurrencealsodoesnotdependonsoiltemperature. Mahringer (1964) reported unsheltered soil temperature
Infactmossesinterceptsolarheatsoeffectively,thatthesoil at2 cmdepthfromSonnblick(3,100 mAustrianAlps)and
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20 AlpBotany(2011)121:11–22
foundAugustmeansof5.1 (cid:3)Cwithmaximabetween26and (Table 2), given that soils may warm by 5–13 K over air
28 (cid:3)C(11–12 (cid:3)Cforair)andaminimumformidsummerof temperature even under frosty conditions as shown here
only-0.7 (cid:3)C,becausebadweatherisassociatedwithsnow (Fig. 6),withtheshortplantcanopypresumablyevenwar-
coveratthiselevation.Duringtheday,canopytemperature mer.Periodic(night-time)freezingisnoproblemforplants
at the Dom summit will be warmer than the one reported like Saxifraga oppositifolia and they may use any single
here for substrate, due to trapping of solar heat among ‘warm’ hour during the day for growth, similar to winter
foliage (Ko¨rner and DeMoraes 1979; Larcher and Wagner crops(Ko¨rner2008).Assoonasleavesthaw(whichmeans
2009) and perhaps, enhanced by some re-radiation by the resorptionofwaterfromintercellularspacesfollowingfrom
surroundingrocks(Fig. 2). intercellular ice produced during freezing) photosynthesis
Substantiallywarmertemperaturesarereportedforhab- and all other life processes are resuming (Larcher and
itatsofthetwoonlyangiospermsinAntarctica.Duringlate Wagner1976;Ko¨rner2003).
summer, air temperature varied between 0 and 10 (cid:3)C and Thed13CvalueforSaxifragaoppositifoliafromtheDom
-2 cm soil temperature went up to 30 (cid:3)C with a mean of summit is placing this sample outside the multi-species
around 10–15 (cid:3)C for most of the days. Soils remained regression against elevation for other Saxifraga species,
unfrozenduringthisperiod(dataforColobanthusquitensis includingS.oppositifolia.ThemeanvaluefoundattheDom
andDeschampsiaantarcticaonSignyisland,60(cid:3) S,March is rather matching the signals from lowest elevation speci-
1989, by Smith 1994). Hence, the poor representation of men (Ko¨rner et al. 1991; Zhu et al. 2009). Hence, the
angiospermsinthisregionratherseemstoberelatedtothe increasinglythinatmosphereknowntocaused13Csignalsto
lack of hardy taxa than to the climate during the growing become less negative by 1–1.5% per km has not had any
season.Atcoolergrowingseasontemperatures,atthemost impact on the CO uptake efficiency of this specimen, and
2
northern edge of Greenland, 50 species were found (Bay therewasalsonowatershortageduringbiomassformation,
1992),andthefarcolderarcticdesertofnorthernSvalbardis asfarasonecantellfromsuchisotopedata.
also much richer in species ([20, personal observation). In conclusion, life on the Dom summit at [4,500 m
TemperaturesmeasuredinBryumargenteummosscushions includesatleast16differenteukaryotictaxa,lessthanhalf
in Antarctica (78(cid:3) S) during peak season (17–31 January of which autotrophic: 3 moss species,[3 lichen species, 1
2003; Burkhard Bu¨del, pers. com.) reached a maximum of angiosperm, 2 arthropod species, and 7 fungal species, 6
12.5 (cid:3)C and averaged around 4–6 (cid:3)C during the polar day symbiotic, 1 parasitic. A more in-depth study could bring
with freezing in almost every polar‘ night’ in midsummer. this list easily to much higher numbers (including further
Airtemperatureswere5–10 Klowerthanmosstemperature. fungiandlichensaswellasalgae)inwhatmightbeoneof
It is well known that ground and ground surface tem- thecoldest,ifnotthecoldestterrestrialmicroecosystemon
perature, as well as plant canopy temperature at high earth with angiosperms. Including prokaryotes (bacteria)
elevationarelargelycontrolledbyexposure(slopeinclina- might double species diversity to twice the eukaryotic one
tion and direction). Rock temperatures may hardly ever under such sheltering high elevation plant cover (Schinner
exceed0 (cid:3)ConaN-facingslopeat3,700 mintheAlps,but 1982).
riseabove30 (cid:3)C(recordedextreme?43 (cid:3)C)everydaywith A 60–70-day growing season (defined by days with at
sunshine on S-slopes, even at extremely high elevations of least 1 h[3 (cid:3)C or a daily mean[0 (cid:3)C in the uppermost
[3,700 m(Mathys1974;Wegmann1998). rooting zone), and a seasonal mean top soil (root zone)
Heatstorageindarkrockaroundcrevicesornicheswith temperature around 2.6 (cid:3)C at roughly 180 (cid:3)d[0 (cid:3)C over
plants may rise soil temperatures also during at least the the entire season seem like the minimum for persistent
earlypartofthenightandmayco-explaintherootcrowding (clonal)angiospermlife(disregardingsexualreproduction).
at the rock-sand interface observed under Saxifraga on the Klimesˇ and Dolezˇal (2010) tested whether plants can be
Domsummit.Hence,thelengthofthegrowingseasonisa transplantedbeyondtheircurrentupperelevationallimitin
matter of exposure rather than elevation and can only be theHimalayan,andtheyfailedwhenseasonlengthdropped
defined at a plant level as had been noted many times (an below 6 weeks in this otherwise slightly warmer, lower
earlysummarybyWinkler1953;Ko¨rner2003;Larcherand latitudeenvironment.TheDom’sSaxifragaoccurrencemay
Wagner 2009). In his synthesis, Winkler assumes air tem- beseenasaresultofanatural‘transplant’experimentthat
perature minima[0 (cid:3)C to be a good proxy for days with took advantage from one or few favorable seasons in the
growth conditions on sun exposed sites. Using this thresh- recentpast.Onceestablished,suchclonalplantscanpersist
old, the growth period lasted 40 days on Jungfraujoch evenbeyondthespecies’reproductiverange,pointingatthe
according to Winkler’s assessment, and 37 days, 60 years criticalroleofplantestablishment.Lichensneedonlyafew
later in the current assessment that started only on July 8, daysperyeartolive,accordingtoPannewitzetal.(2003),
hencewasmissingatleast2–3 weeks.Bothnumbersclearly 10–14 daysofmoist,abovezerotemperaturesaresufficient
underestimate the length of the actual growing season at 77(cid:3) S in the Antarctic. Moisture is far more critical in
123