Anda di halaman 1dari 13

Accelerating Climate Change Impacts on Alpine Glacier Forefield Ecosystems in the European Alps Author(s): Nicoletta Cannone, Guglielmina

Diolaiuti, Mauro Guglielmin, Claudio Smiraglia Reviewed work(s): Source: Ecological Applications, Vol. 18, No. 3 (Apr., 2008), pp. 637-648 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/40062174 . Accessed: 07/02/2012 16:37
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.

Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecological Applications.

http://www.jstor.org

18(3), 2008, pp. 637-648 EcologicalApplications, 2008 by the Ecological Societyof America

ACCELERATING CLIMATE CHANGE IMPACTS ON ALPINE GLACIER FOREFIELD ECOSYSTEMS IN THE EUROPEAN ALPS
Nicoletta Cannone,1'4 Guglielmina Diolaiuti,2 Mauro Guglielmin,3 and Claudio Smiraglia2 1 Ferrara, of Ferrara, Department Biologyand Evolution, of Italy 2 University University Milan, "A. Desio" Department EarthSciences,Milan,Italy of of 1 and of University Insubria, of Department Structural Functional Biology,Varese,Italy

was Abstract. In theEuropeanAlps theincreasein air temperature morethantwicethe in over increase global meantemperature thelast 50 years.The abiotic(glacial) and thebiotic of environment showing are components (plantsand vegetation) themountain ampleevidence of climate (80% of totalglacialcoverageand changeimpacts.In theAlps mostsmallglaciers contribution waterresources) to could disappearin the nextdecades. an important climatechange was demonstrated affect to higherlevelsof ecological systems, Recently surfacearea changes,indicating thatalpine and nival vegetation withvegetation exhibiting way in responseto 1-2C warming. may be able to respondin a fastand flexible mass balances, surfacearea We analyzed the glacier evolution(terminus fluctuations, local climate,and vegetation successionon the forefield Sforzellina of Glacier variations), ItalianAlps) overthepast three decades.We aimedto quantify central the (Upper Valtellina, impacts of climate change on coupled biotic and abiotic componentsof high alpine to if was occurring themduringthe last decade (i.e., on ecosystems, verify an acceleration new specific wereadoptedforplantcolonization 1996-2006)and to assess whether strategies and development. All the glaciologicaldata indicatethata glacial retreat and shrinkage occurredand was muchstronger after 2002 thanduring last 35 years.Vegetation the started colonizesurfaces to for thanthatreported the in deglaciated onlyone year,witha rateat leastfourtimesgreater of individuals and about two timesgreater the literature the establishment scattered for for well-established discontinuousearly-successional The colonization strategy community. colonizers early-successional, are screeslopes,and perennial clonal species changed:thefirst withhighphenotypic rather thanpioneerand snowbedspecies. plasticity This impressive acceleration coincidedwithonly slightlocal summer wanning(approximately+0.5C) and a poorly documentedlocal decrease in the snow cover depth and duration. Are we facing accelerated to did ecologicalresponses climatic changesand/or we go overwhichmajorecosystem to changesmayoccurin response evenminor beyonda threshold climatic variations?
clonal plants; colonization strategies;Italian Alps; Key words: alpine glaciers; climate warming; mountain Glacier;vegetation. ecosystems; Sforzellina Introduction

of in The increasing recession thecryosphere theAlps in is probablyrelatedto important changes occurring such as the widelyrecogconditions, mid-tropospheric nized rapid increase in temperatureduring recent retreat glaciers, of decades(IPCC 2001). The worldwide from alpine areas (Haeberli and Beniston 1998) to Antarctica (Rott et al. 1996, Cook et al. 2005), in the courseof the last fewdecades,is frequently mentioned as a clear and unambiguoussign of global warming (Oerlemans 2005). Comparedwithotherclimateindicatorslike treerings, reactin a relatively glacial systems to climate thetransfer function does simple way change: not change in time and geometriceffectscan be
Manuscriptreceived19 July2007; accepted 16 November Editor:H. P. Schmid. 2007. Corresponding 4 E-mail: nicoletta.cannone@unife.it

addressed.Likewise, manyglaciers foundat high as are a in elevations, climatesignal reflected glacierfluctuationscan be studiedas a function height of (Oerlemans 2005). In the Alps atmosphericwarmingwas found to increasemorethandouble overthesame period(Bohm et al. 2001), witha significant summer which warming, was particularly severe since 1970(Castyet al. 2005). As a resultof this rapid climate evolution,many small withsurface area <1 km2)located (i.e., glaciers glaciers at mid-elevationcould disappear in the next few decades. These small glaciersare commonin the Alps, wheretheyrepresent 80% of total glacial coverageand make an importantcontribution water resources to (Oerlemansand Fortuin1992). The rapid "disintegration" alpine glaciers has of been pointed out in an analysis of the Swiss already GlacierInventory 2000 by Paul et al. (2004). Amongthe

637

638

NICOLETTA CANNONE ET AL.

EcologicalApplications Vol. 18,No. 3

werefoundto showbotha wider provideenvironments smaller others, subjectonlyto naturaldynamics, glaciers direct where is possible it scatter variation of withrespect the largerones, and without to anthropogenic impacts, to contribute morethanproportionally thearea they to compare the responses of related environmental to and to In 1973and components 44% of thearea loss between (glaciers vegetation) thesameclimatic represent. fact, in theirvariations responseto refers glaciersof lengthsof <1 km and inputsand to quantify to 1998/1999 18% of thetotal area in 1973 (Paul et al. climate changes. covering only the are was 2004). Thus smallglaciers showing sensitivity The aim ofour research to quantify bioticand higher than largerones due to theirveryfast reactiontime abiotic impactsof climatechange over the past three (sensu Haeberli and Hoelzle 1995) and are, hence, decades in an alpine glacier area without direct if has suitablesitesforassessment and monitoring climate anthropogenic of impacts,to verify an acceleration on and changeimpacts (Dyurgerov Meier2000). Moreover, been occurring them duringthe last decade (i.e., new and pressure 1996-2006), and to assesswhether specific at highelevationstemperature, moisture, strategies and development. trendsand anomalies are clearerthan at lower levels, wereadopted forplantcolonization where the large-scale climate signals tend to be and For thispurposewe analyzedthepatterns rateof dampened(Beniston2000, 20Q3). Also soil characteris- glacier evolution (abiotic component)and vegetation ticsof the glacierforefield wereused as climatechange succession on of (bioticcomponent) theforefield Sforzelindicators central ItalianAlps). lina Glacier(UpperValtellina, (i.e., Egli et al. 2006). Not only the abiotic (glacial) but also the biotic Study Area components(plants and vegetation)of the mountain The Sforzellina Glacier is a southwest-facing environment showing ample evidence of climate are cirque from2850 to 3100 m above sea level et changeimpacts(e.g., Grabherr al. 1994,Benistonet glacierextending al. 1997,Beniston et 2003,Walther al. 2005,Cannoneet (a.s.l.; 4620/55// 1030'50" E), located in Valfurva N, al. 2007). Accordingto quantitative estimatesof the Valley (Upper Valtellina),in the centralItalian Alps. of a extendsbetween 2850 and 2700 m biologicalimpacts theclimate change"fingerprint," The glacial forefield withdifferent by greateramplitude is expected at high latitudesand a.s.l., and it is characterized surfaces in fromone year to >80 altitudes (Root et al. 2003). In theAlps,theshifts the ages since deglaciation, ranging features such as altitudinal by range marginsof plant species and biocli- years,whileundisturbed periglacial maticzones in thelast 50 years,withupwardmigration sorted or unsortedpolygons. Only a few not welland lobes occuron the of alpineand nival-plant speciesat a rateof 8-10 m per developedterracettes solifluction at decade (Grabherr al. 1994,Walther al. 2005), and northeast-facing of themoraineridgedeposited et et slope of in community et al. 2000) the beginning the 20th century (1920-1925) on the (Keller changes composition of borderof theglacier. evidenceof the sensitivity mountain southern providethefirst habitatsto climatic Sforzellina Glacier representsa unique case of change. in Surface area changesof thevegetation a highalpine glaciologicalstudyin Italy because it has one of the fluctusite of the European Alps between 1953 and 2003 older and more continuousrecordsof terminus that demonstrated climate changeis able to affect higher ations(1925 to today)and massbalance(1987 to today). and levelsofecologicalsystems thateven 1-2C warming It is also one of the few glaciers of which thereis and of of air temperature may produce significant changesin relatively good knowledge itsthickness geometry. etal. 2007).As On SforzellinaGlacier different geophysicalsurveys (Cannone vegetation community dynamics and of and were applied in order to evaluate ice thickness thesechanges follow suddenwarming summer the that bedrockmorphology. Geoelectrical annualtemperatures 1980,theseresults after (VES [vertisurvey suggest and faster more cal electricalsounding];Resnati and Smiraglia 1989, mayrespond alpineand nivalvegetation et to climatic thanpreviously believed (Pavan et (Pauli Guglielmin al. 1995) and seismicreflection flexibly change of ice al. 2000) gave a maximum thickness 42 and 60 m, et al. 1999,Walther al. 2005). et In are to Glacierforefields suitableenvironments investi- respectively. 1999 a ground probingradar (GPR) to and devel- survey was performed obtain high-resolution of colonization topoggate the processes vegetation of to raphyof the glacierbed. The maximumice thickness becauseoftheage control thesurfaces, and, opment area of theglacier calculate the speed of primary succession and to calculatedwas of -60 m in thecentral understandtheir mechanisms(e.g., Whittaker1993, and this value agrees with seismicdata. In addition, werealso performed authors geomorphological (Rossi et surveys Chapinet al. 1994).In theEuropeanAlps several relatedto past have investigated and described al. 2003) to map the glacial landforms glacialchronosequences from different succession stagesof vegetation pioneerto glacialevolution. in to The studyarea is includedin the upper alpine belt climax communities relation siteage (e.g.,Pirolaand Credaro1993,1994,Burga1999,Caccianigaand Andreis (2600-2800 m a.s.l.) and in the nival belt (>2800 m and 2004,Raffl Erschbamer 2004) and to themechanisms a.s.l.). The vegetationis a mosaic of discontinuous of seedlingestablishment (e.g., Stocklinand Baumler alpine grasslands (includingthe climax communities 1996, Niederfriniger Schlag and Erschbamer2000). dominatedby Carex curvulaand the initialgrasslands in Moreover, highmountain areas,mostglacialforefields dominatedby Poa alpina), snowbed vegetation(with

April2008

CLIMATE CHANGE AND GLACIER ECOSYSTEMS

639

Salix herbacea, Veronica alpina, Sagina saginoides, data with the kriging In algorithm. addition,several Cerastium werepositioned near the cerastioides), pioneerand early-successional nodes withknowncoordinates communities (withRanunculus glacialis,Geumreptans, glaciersto improvethe accuracyof the measurements Cerastium GPS to uniflorum, Oxyriadigyna, Saxifragabryoides), takenby differential withshortbases according and, at the higheraltitudes,scatteredindividualsof Diolaiuti et al. (2004). vascular plants and cryptogams The glacier limits (see Plate 1). At the datingback to 2002,2003,and 2006 elevations our site,theeffects anthropogenic of of land were mapped on the fieldby DGPS surveys, and the use changeon vegetation mostly are werereconstructed themoraine (Kelleret 1920and 1980limits negligible by al. 2005). Previousstudieson theglacierforefield the ridgeboundarymarkedon the fieldby DGPS as well. of Sforzellina Glacierwerecarriedout by Caccianiga and The glacierlimits from1991to 2001 werereconstructed Andreis(2004) reporting occurrence a pioneer by a geographicinformation the of system(GIS) using the withCerasti- measuredfluctuation data and thepositionof the 1991 community digynae) (Sieversio-Oxyrietum umuniflorum, Geumreptans, Ranunculus benchmark used for measuringthe distancefromthe Oxyriadigyna, and Poa laxa on the 1980smorainic glacialis, ridgeand glacier snout. Orthophotosdating back to 1999 and of the initial grassland dominatedby Poa laxa and 2003 (Regione Lombardia2004) werealso used to map on the glacierboundaries.GIS mappingwas applied not Saxifragabryoides the LittleIce Age moraine. only to past glacierlimitsbut also to assign different Material and Methods on ages to theland surfaces the glacierforefield (1991Glaciermonitoring 2001). All the vegetation plots were located by DGPS Recent (last three decades) glacial changes were and included in the GIS mapping, allowing the reconstructed using all the available sources of data. vegetationcoveringof these areas to also be dated. by Terminus fluctuations were analyzed from1971 up to Surfacearea changesweredetermined GIS through of thus glacierboundaries now, in order to evaluate the glacier's behavior(i.e., thecomparison thehistorical obtained. The final planar accuracy value was then retreat advance),and to calculatethe ratesof these vs. to (1999). changes.These data have been collectedfrombench- evaluatedaccording Vogtleand Schilling markslocatedon theglacierforefield without interrupVegetation survey a for tions,providing data set on theglacier'sevolution The vegetation the glacierforefield described, of was the last 35 years(CGI 1971-1977,1978-2006).In 1991 a the benchmark used for the terminus variationmea- analyzing totalof 23 sampling plotsof 1 X 1 m. Their surements changedand the new one was set at -80 m positions were acquired through DGPS surveysas and then mapped by GIS. The (withan azimuthof 145N) fromthe present (summer describedpreviously wherethe plots weresampledwere ages of the surfaces 2006) glacierlimit. Mass balances were evaluated from the authors obtained fromthe glacieranalysis.Withineveryplot, cover and the cover of each vascular (Catasta and Smiraglia1993)from1987up to now using total vegetation thestandard method visuallyusing indicesto express glaciological (0stremand Brugman specieswas estimated abundanceofeach species(+, <1%; 1, 1-5%; of 1989,Kaser et al. 2003) based on a network ablation therelative stakesat different altitudes.Several differential global 2, 5-10%; 3, 10-15%; 4, 15-20%; 5, 20-25%; 6, 25-50%; (DGPS) campaignswereperformed 7, 50-75%; 8, >75%). Vascularplantspeciesnomenclapositioning system with kinematictechniquesaimed at obtainingdigital ture is in accordance with Pignatti (1982). Cover were also givenfor cryptogams, whichwere elevation models (DEM) of the glacier surface and estimates as as wellas to map theGPR not identified species but groupedinto threebroad (in altimetry 1999,2000,2002) and groundlichens. mosses,epilithic lichens, profiles.The fast static techniquewas employed on categories: for DGPS surveysthat focused on delimiting glacier Slope and aspectwererecorded each plot. the boundaries or on mapping moraine ridge positions Climate fewerpoints,in 2002, 2003, 2006). DGPS (requiring Local meteorological data were collectedand prowere also used to acquire the position of the surveys climatebehaviorand evolution benchmark used to measure the glacier terminus cessedto analyzerecent fluctuations from1991up to now and map themoraines in the studyarea. The closest and highestautomatic station(AWS), whichwas foundto be running of the 1920sand 1980s,whichservedto reconstruct the weather older and recentglacier advances, as well as to map during the last three decades without significant debris coverand thevegetation is supraglacial survey plots. interruptions, located at Forni dam at 2180 m a.s.l., The DGPS surveys werealwayscarried at theend ~5 km northwardfrom SforzellinaGlacier. Other out of thesummer overthelast 35 years, season,whentheablationzone is largest AWSs, whichhave been working and no snow is present the glaciersnout.To obtain are located at Santa CaterinaValfurva(1730 m a.s.l.) on DEMs of the glaciersurfaceand bedrockmorphology and Uzza (1250 m a.s.l.), respectively. thesestations At and liquid precipitationdata were (fromGPR data), the fieldsurveyswere carried out air temperature using high densityglobal positioningsystem(GPS) measuredeveryhour and thenrecordedon the general and the databaseoftheGeologicalMonitoring Service ARPA of pointdata (i.e., 8000 points/km2) interpolating

640

NICOLETTACANNONEET AL.

^^^dT^o

Fig. 1. (A) Sforzellina Glacier summer (Photo in with cover 40% whole 2006 credit Diolaiuti) debris G. exceeding ofthe glacier area.(B) Map showing location the in the of 2006glacier moraine and of and 1980s relation the to mountain ridges the1920s early and in ridges peaks(height given m a.s.l.). Lombardia (LombardyRegional Environmental Agenannual,and seasonal cy,Sondrio,Italy).Daily,monthly, and monthly, averages of hourly air temperatures annual, and seasonal cumulated liquid precipitation werecomputedfortheclimateanalysis. occurrenceof debris cover that now exceeds 40% of the whole glacierarea (Figs. 1 and 2). Two ice-contact lakes developedduring last 10 years,one of themis the active(at thewestside of theglacier;see map presently in Figs. 1 and 2) and calvingphenomena occurred the at area. Glacier volume was deterglacierwater-contact Results mined fromthe comparisonof the DEMs processed Glacier fromgeophysical(bedrock topography GPR) and by in Sforzellina Glacier suffered topographical by (glaciersurface GPS) data collected During the last century substantial reductions its lengthand surface, well 1999. The measuredvolumewas -8.1 x 106m3 of ice in as as changes in its supraglacial conditions, with the (i.e., 7.8 X 106m3 waterequivalent, w.e.).

April2008

CLIMATE CHANGE AND GLACIER ECOSYSTEMS

641

between1994 and 2006, the moraineridgesof the early 1920sand Fig. 2. Map showingthe glacierboundaryfluctuations 1980s,and the locationof thevegetation plots.

thusexceeds The analysis of the mass balance data collectedon w.e.). The wholeloss by ablationprocesses volumeestimated Sforzellinafrom the hydrological year 1986-1987 to 8 X 106m3(morethantheremaining that (withexceptionof the in 1999). The rate of the glaciervolumeloss increased present(Fig. 3) underlines w.e. in the period from0.30 X 106 m3/yr hydrological year2000-2001) the glacieralways lost in significantly w.e. in the to balance = -1.1 m 1986/1987-1999/2000 0.50 X 106 m3/yr mass (yearlyaverage of net specific

Fig. 3. Sforzellina Glaciernetspecific balance data (graycolumns, values in m waterequivalent, w.e.) and trends (thickgray line value (curve,in m a.s.l.) and trends (thinblack line). line),and the ELA (equilibrium altitude)yearly

642

NICOLETTA CANNONE ET AL.

Ecological Applications Vol.18, 3 No.

value. When the cumulative Fig.4. Glacier terminus fluctuations 1971 2006.Thebarsindicate from to values, linethe yearly = theglacier terminus found be stationary was to (change 0), no barsarereported. six area decreasedas following years.The accumulation the equilibriumline altitude (ELA), calculated from at yearlymass balance profileanalysis,shifted higher elevations(from3029 m a.s.l. in the hydrological year 1986-1987,to 3189 m a.s.l. in 2005-2006; Fig. 3), and almost the entireglacierarea lies below the presently ELA. The terminus fluctuations (Fig. 4) of Sforzellina Glaciershoweda generalretreat overthepast 35 years. During the 1971-2006period,the snout of Sforzellina Glacier retreated -75 m. The reductionin length by over the 35 years of surveysequals 9% of the 1971 The glacierretreated yearsout of the 25 glacierlength. 35 yearsanalyzed(equal to 71% ofthetime);theaverage -2 over the whole retreat ratewas approximately m/yr onlythe period(1971-2006),was -2.6 m/yr considering shorter timespan 1985-1995,and accelerated to -5 up in m/yr thelast decade (1996-2006). In spite of this reduction trend, the terminus fluctuations showeda small glacieradvance in the also 5 period1975-1984(+14.5 m equal to a rateof-hi. m/yr). It was followedby a transition whichthe phase during glacier alternatedretreatsand small advances, then, The from1992,theglaciershrinkage proceeded. starting of advance led to the formation small moraineridges 1977and theearly1990s(Rossi et al. 2003). The between limits from1991 to 2006 and themoraineridges glacier of 1920 and 1980 are reportedin Figs. 1 and 2. the to fluctuation, glaciated Corresponding theterminus 0.383 0.005 km2(mean SE) in area decreasedfrom of 1981to 0.2381 0.002 km2in 2006,witha reduction -38%. The yearlyrate of surfacearea loss (Table 1) remained almost constant (around -0.005 km2/yr) between1981 and 2002, while it doubled (to -0.0097 in km2/yr) theperiod2002-2006. Vegetation occursin all theproglacialarea (Tables 2 Vegetation and 3), showingdifferent patternsin relationto the column of Table 2), which surfaceage (Fig. 1; fourth was assigned on the basis of the GIS analysis,and rangingfrom terrainsdeglaciated after one year to morainedepositsof the 1920s. Colonizationstartsone year afterdeglaciationwith verylow coverage(althoughit reaches14% in generally area loss of Sforzellina Table 1. Yearlyrate of surface central Italian Glacier, Alps. Timeframe 1920-1981 1981-1985 1985-2002 2002-2006 area surface Yearly (km2/yr) change -0.0029 -0.0053 -0.0050 -0.0097 Accuracy (km2) 0.009 0.008 0.006 0.005

April2008

CLIMATE CHANGE AND GLACIER ECOSYSTEMS

643

to persist duringsuccessionas well as to carryout the first 1970,Matthews ' stagesof colonization)(Jochmisen No. Total Plot Slope 1992, Age since 1999). Moreover,these species belong to Burga cover(%) no. () (yr) deglaciation species different stages of vegetation developmentand to 0 0 10 series.In particular Geumreptans, different vegetation 10 2 16 and Cerastiumuniflorum, Poa laxa are characteristic 10 12 3 1 0 Poa alpina and 14 7 4 species of the scree slopes vegetation, 6 0.1 6 5 are alpine Saxifragabryoides typical speciesof theinitial 2 5 8 3 6 is and Sagina saginoides a snowbedspecies. grassland, 7 2 1 7 6-1 On surfaces 4 7 35 6 8 deglaciated 1 yearsago, thevegetation 11 2 7 5 9 is still scatteredwith low coverage (2-3% as average 2 7 25 22 10 sites),composed although to 35% in morefavorable up 25 11 45 8 of mosses and 12 species of vascular plants, and 18 8 25 12 65 25 20 18 5 13 dominatedby Geumreptansand Cerastium uniflorum. 2 25 4 3 14 Here we observeda changein speciescomposition with 25 20 5 15 withthedisappearance to theyounger of surface, 4 25 16 10 respect 4 25 17 18 Ranunculus different glacialis, and a slightly pool of 4 25 18 38 of early-successional species(withtheingression Oxyria 25 2 0.1 19 and snowbedspecies{Cerastium cerastioides). digyna) 2 25 15 20 9 >80 21 60 Vegetationcoverage and species richnessincreases 12 >80 65 22 whereclosed on surfaces, significantly the 25-year-old 12 >80 90 23 occur.The relatively coverage high patchesofvegetation similar thevalues of Geumreptans to of Oxyriadigyna, a of indicates further evolution some sheltered sites). Vegetation is composed of and Cerastium uniflorum, individuals eightspeciesof vascularplants thevegetation of scattered development. The initialgrasslandand the morematuregrassland and by mosses. It is remarkable that, instead of olderthan spadiceaeoccuron surfaces exclusively pioneerspecies (i.e., species that appear in of theLuzuletum but thefirst stagesofcolonization are notable to persist 80 years, where it is possible to observe a shiftin with the dominanceof Poa composition, during succession), the firstcolonizers are mainly community of able alpina and/orLuzula spicata, the ingression Salix of early-successional species(i.e., species composed
Table 2. Featuresof investigated vegetation plots. Table 3. Relativeabundanceof speciesin vegetation plots. Relativeabundanceby plot Species Ranunculus glacialis Cerastium uniflorum Mosses Poa laxa Geumreptans Leucanthemopsis alpina Saxifragabryoides Poa alpina Sagina saginoides Poa alpina vivipara Oxyriadigyna cerastioides Cerastium Cerastium pedunculatum 12 + + + + +1 + 3 4 + 1 + +1 5 + 6 1 1 7 8 9 10 11 12 13 14 15 16 17 18 19 20 .21 22 23 1112 11 2 + + 12 14 2 12 3 33 6 1 5 2 + 1 1 + + + 2 2171 1 1 1 1 +1 1121162111 2+ 1 1 + 3 + 11111 1

+ + 1 1 +1 + + +

21

34 111

1 12

Veronica alpina Linariaalpina anagallidifolium Epilobium Taraxacum alpinum Sedumalpestre Salix herbacea Saxifragaoppositifolia Armeria alpina Luzula spicata Cardamine resedifolia Groundlichens lichens Epilithic

Arabis caerulea

1 1

+
1

1 + 1 2

+ 1 +

+ 1 7 + 1 1

the abundanceof each species(+, <1%; 1, 1-5%; 2, 5-10%; 3, 10-15%; 4, 15-20%; 5, 20-25%; 6, Note: Indicesexpress relative 25-50%; 7, 50-75%; 8, >75%).

644

NICOLETTA CANNONE ET AL.

Ecological Applications Vol.18,No. 3

Fig. 5. Mean summer temperatures air in at (June-August) theperiod 1988-2005recorded Uzza (solid dots) and Forni(solid triangles).

herbacea and Sedum alpestre (snowbed species also in occurring frequently the climax grassland),and the persistenceof the early-successionalGeum reptans, Cerastium and uniflorum, Leucanthemopsis alpina, and average total coverageup 90%. Only at this stage do lichens maketheir as lichens ingression epilithic growing on bouldersas well as groundfolioselichens. Climate foundin theAlps strong warming Despitethegeneral (Beniston2000), in ValfurvaValley duringthe period 1988-2006 the mean annual air temperatures show a decrease(-0.2C at 2180 m a.s.l.), whilethe veryslight mean summer (June-August) air temperaturesare clearly increasing(+0.5C; Fig. 5). The precipitation we to pattern evaluatedonlyreferred liquidprecipitation (as theclosestAWS [Forni,2180 m a.s.l.] onlyrecorded water equivalentdata); in the areas surrounding the were not available, glacierdata for snow precipitation it to making difficult evaluateanychangein snowdepth In and duration. anycase, a remarkable decreasein total (around -10% at 2180 m a.s.l.) has been precipitation recorded since 1988. Discussion At a global scale,glaciers verysensitive climate are to change. In particular,the smaller ones seem to be consistent climate changeindicators, giventhattheyare showingfasterreactiontimes (Dyurgerovand Meier 2000, Paul et al. 2004). On the otherhand, previous it to studiessuggest would be inappropriate use length of a single glacier as being representative of changes climatechange(Chinn 1999). Our data show the trendof terminus fluctuations of withthe general Sforzellina Glacier to be in agreement patternof glaciers spread all over the Alps, which in resulted retreating from end of the LittleIce Age the

(LIA) up to now (Zemp et al. 2006) with a short that occurredbetweenthe 1970s and the interruption the 1980s(Patzelt1985,Wood 1988).In addition, record of glaciermass balances,whichare generally considered an unambiguous marker climatechange(Cogleyand of and Adams 1998,Haeberliet al. 1999,Dyurgerov Meier a volume 2000, Oerlemans2005), underlines stronger in value of reduction thelast decade (theaverageyearly the last 10 years was 66% largerwith respectto the 1987-1996averageyearly value). of GlaMoreover,the representativeness Sforzellina of cier as witness the ongoingalpine glacierchangesis between further relationship supportedby the striking and theSforzellina mass balance (1986/1987-2002/2003) in thoseof thealpineglaciers reported theGlacierMass Balance Bulletins (IAHS (ICSI)-UNEP-UNESCO, r correlation coefficient,= 1988-2005;Bravais-Pearson the 0.84). Furthermore, ELAs of SforzellinaGlacier (1986/1987-2002/2003) comparedwiththe mean alpine ELA (IAHS (ICSI)-UNEP-UNESCO, 1988-2005)also show a strong correlation = 0.82). (r An accelerating surfacearea loss was also foundfor the period 2002-2006, and the glaciersurfacein 2006 -14% with resultedin a decreased of approximately to respect the2002 glacierarea. demonstrated thesefindings The glacial reduction by mass balances,and surface fluctuations, (i.e., terminus as area changes) is interpreted a truthful impact of function climatechange.Indeed,as the transfer among does not change climatechangesand glaciervariations in time (Oerlemans 2005), an accelerationin glacial changesis suggested. the it Nevertheless, is less easy to identify climatic elementsdrivingthe glacier changes and, despite the on many investigations this topic (e.g., Hoelzle et al. debateis stillopen. 2003,Oerlemans 2005), thescientific most the and Air temperature precipitation, two factors

April2008

CLIMATE CHANGE AND GLACIER ECOSYSTEMS

645

Plate 1. Androsace the alpinais a pioneerspeciescolonizing alpineand nivalbeltsof theEuropeanAlps and is representative N. Photo credit: Cannone. of the speciesactuallysuffering highest the ecosystems. impactsof climatechangeon high-elevation

correlated withglacierfluctuations, only are commonly two elements the complexchain of processeslinking of climateand glacierfluctuations (Haeberli 1995, Chinn indicate a 1999). Therefore,the glacier fluctuations of complexcombination mass and energy exchangeat the Earth's surface. The air temperatureincrease in occurring the alpine areas since the end of the LIA activated a positive feedback, with the consequent increaseof both the downwardsensibleheat fluxand thelongwave radiation balance (Oerlemans al. 1998). et Furthermore, duringthe last two decades, Sforzellina Glacierexperienced strong a decreaseof surface albedo to increasing debriscoverage), whichsurely (due played a key role in increasingthe glacier absorption of thusmakinglargerthequantity fluxes, incoming energy of energy available forglaciermelting. To quantify possibleinfluence temperature the of on the recentevolutionof SforzellinaGlacier, neglecting thecontribution to changing due a precipitation, simple was followed, to Chinn(1999) and approach according Oerlemans all (2001). Analyzing theEL As of theperiod 1987-2006 (Fig. 3), the averagedifference betweenthe estimated ELA and the calculated annual steady-state ELAs, givesa mean increaseof -150 m. This upward shift, obtained using a standard lapse rate of - 0.0065C/m, a of represents generalwarming approxthat + 0.6C since 1987. Therefore, imately considering thesummer in thatoccurred thesame periodis warming

indicatesthatchangesin precip+0.5C, the difference itationalso have to be considered. In the context of vegetationsuccession,our data recent evidence (Cannoneet al. 2007) suggesting support that the significant community changes in vegetation dynamicswe foundare consequencesof an actual air of combinedwiththe reduction temperature warming and the shortening the snow season. of precipitation Like the glacier reduction,all processes seem to be the accelerated, including vegetation dynamics. The comparisonof our data withglacial chronosequences describedfor the European Alps allows an In rateof theseprocesses. assessment theacceleration of the alpine belt (>2200 m a.s.l.) the colonizationof the is to recently deglaciatedterrains reported startwithin and Baumler1996, 4-8 yearsafter (Stocklin deglaciation early Burga 1999,Tscherkoet al. 2005), withscattered for pioneerspecies.At least 10-25 yearsare required the ingressionof the early-successional species and the early-successional developmentof a well-established community (Pirola and Credaro 1993, Niederfriniger 2000, Caccianiga and Andreis Schlag and Erschbamer and Erschbamer et 2004, Raffl 2004,Tscherko al. 2005). Our data provideevidencethattheseearlystagesof colonization suffereda dramatic acceleration:plant only species are able to colonize the glacier forefield one year after the glacier retreat.Consideringthe differences colonizationtimebetweenour data and of the the existing literature, colonizationspeed increased

646

NICOLETTA

CANNONE

ET AL.

Ecologica^AppHcations

surfaces demonstrates of at least four timesfor the establishment scattered clonal plantson theone-year-old and explains how of in theSforzellina area vs. 4-8 years the correctness this hypothesis individuals (one year for and reported literature) about two times thewell- colonization could occur with such fast rates at an by established discontinuous early-successional community elevation>2800 m a.s.l. vs. Accelerationof dynamicsis evidentonly on recent (6-1 1 yearsat Sforzellina 10-25yearsreported the by the literature). vegetation; factthat older stages of successionare On theotherhand,thefollowing stagesof vegetation quite similar to those described by other glacial indicatesthatclimatechangeimpacts development(>25 years) do not show remarkable chronosequences with respect to the chronosequencesde- on these stages are not severe enough to induce differences in for scribed theliterature theAlps (such as Pirola anc significant changesand thatolder and moredeveloped Credaro 1993, Niederfriniger and Erschbamer stages are probably more resistantto, and buffered Schlag climatic 2000, Caccianiga and Andreis2004, Raffland Ersch- from, perturbation. increaseof air temperaWithinthe well-documented bamer2004,Tscherkoet al. 2005). The ecologicalrequirements the speciesoccurring ture duringthe 20th centuryover the planet (IPCC of on the one-year-old surfacemay explainthe abilityof 2001), the warmingwas significantly higher in the In thesespeciesto colonize such youngsubstrata. fact, European Alps (Beniston 2000, Bohm et al. 2001). mostof themare speciestypical thescreeslopesor of More recently of Casty et al. (2005) in theirtemperature for rocks, with only one snowbed species (Sagina sagi- reconstruction theAlps since 1500,foundthat1994, noides). The absence of snowbed species in a glacier 2000,2002,and 2003 werethewarmest yearssince1500. forefield appearsto be a paradox ifwe do not take into Moreover, they found that summer warming was severe after 1970, reaching,in 2003, the accountthe strong reduction snow cover abundance particularly of since 1500. Our and permanence documented a sitevery for close to the highestpeak of summertemperature of the of area (Cannone et al. 2007). The shortening the data confirm generalsummer warming the last study snowcoverlength the by supports hypothesis Galen and two decades, even if, at this site,verywarm summers also in 1991 and 1998. Stanton(1995) that climatechange may induce inter- wererecorded in The temperatureincrease we found (-K).5C in differences growthphenologyof coexisting specific in speciesand promoteshifts snowbedplantcommuni- summer)has to be consideredin the frame of the whichwas accom198 ties.Moreover, is Sagina saginoides a short-lived species generalpost- 5 climatewarming, on withabundantseed production, and it is possible that panied by reducedprecipitation the Alps. Whereas the successof thisspeciesmay be relatedto its efficient the numberof days withsnow on the groundshowed snow cover the littleevolution, durationof continuous dispersal strategies. in was clearly declining at all elevations. Although The functional ofmostof thespeciesinvolved types the earlystagesof colonizationmay also providesome continuoussnow cover tendedto startearlier,it also explanation for the accelerated rates of vegetation meltedmuch earlier(Benistonet al. 2003, Martinand All colonization. thesespeciesare long-lived perennials Durand 2006). This generaltrendseems relatedto a conditionsof the positiveNorth AtlanticOscillation(NAO) index (Upto the harshenvironmental adapted Most penbrink 1999) and to the summer warming.Our alpineand nival beltsand of the glacierforefield. data indicatea generaldecrease (-10%) of theearly-successional speciesthatare able to colonize precipitation with the general trend (Brunettiet al. the one-year-old terrains are clonal species,including in agreement that thereare not any snow clonal plants with widely spaced ramets(e.g., Geum 2000). It is unfortunate as Cerastium reptans, Saxifragabryoides, uniflorum) well depth and durationdata available for the Sforzellina but form(e.g., Poa Glacier forefield, if we considerother local data as clonal plantswitha clumpedgrowth alpina). Clonal growthis one of the most important recordedin another localityof the Upper Valtellina adaptationsto the severeclimaticconditionsand the since 1978,we findtheyagreewiththegeneralpatterns of nutrient shortagecharacteristic the alpine environ- of the snow coverdecrease(Cannone et al. 2007). ments(Stocklinand Baumler1996,Pluess and Stocklin Conclusions increases withaltitude 2005). Thus clonal reproduction the ice both in closed grasslandsand in pioneercommunities The stronger mass loss affecting Sforzellina the (Stocklin1992). Clonal growthis a key factorfor the Glacierduring last decade (1996-2006) may be due combinedwithreduced successful establishmentof the primarysuccession to the local summerwarming of and the shortening the snow season withtheability precipitation becauseit provides long-lived perennials witha (Cannone et al. 2007). This abiotic evidenceof climate to persist succession(e.g., Geumreptans) during of withchangesin the vegetation large amount of phenotypicplasticity(Stocklin and change is correlated of whichindicatedan acceleration is Baumler1996). Phenotypic plasticity one of themost the glacierforefield, ratesin thesameperiod.Herewe showthat mechanisms important hypothesized allowingplantsto colonization between abioticand the is in modified climaticchange there a strong correspondence by persist the environment and of and Guisan 2001), thus avoidingmigration bioticcomponents highaltitude ecosystems that, (Theurillat since and/or extinction.Therefore the preponderanceof overthelast decade (1996-2006) and, in particular

April2008

CLIMATE CHANGE AND GLACIER ECOSYSTEMS

647

a 2002, the impactsof climatechangehave undergone dramaticacceleration,much strongerthan any that occurredduring the last 35 years. This acceleration occurredin tandemwitha documented slightsummer and warming a possibledecreasein snowcover.Further in situ investigations requiredto directly are measure some of the influential involved(e.g., snow parameters and to analyze speciescover, avalanche frequency) to like snow coverreduction. specific responses factors
ACKNOWLEDGM ENTS

We thank Christian Korner and Renato Gerdol for the Wilfried Haeberli and reviewing paper beforesubmission, one anonymous refereewhose commentsand suggestions allowed us to improve the paper, and the Geological Serviceof ARPA Lombardia(LombardyRegional Monitoring Environmental Agency)forthe climaticdata. This paper was funded by the project "Increasing rate of climate change impactson high mountainareas: cryosphere shrinkageand environmental effects" (PRIN-MIUR 2005). Literature Cited Beniston,M. 2000. Environmental change in mountainsand uplands.Arnold,London, UK. Beniston,M. 2003. Climaticchange in mountainregions:a of review possibleimpacts.ClimaticChange 59:5-31. Beniston, M., H. F. Diaz, and R. S. Bradley.1997. Climatic sites:a review. ClimaticChange 36: changeat highelevation 233-251. Beniston, M., F. Keller,and A. Goyette.2003. Estimatesof snow accumulationand volume in the Swiss Alps under changing climatic conditions. Theoretical and Applied 76:125-140. Climatology M. Bohm,R., I. Auer,M. Brunetti, Maugeri,T. Nanni,and W. Schoner. 2001. Regional temperature variabilityin the instrumental European Alps: 1760-1998fromhomogenized Journalof Climatology 21:1779timeseries.International 1801. Brunetti, M. Maugeri,and T. Nanni. 2000. Variationsof M., and in temperature precipitation Italy from 1866 to 1995. Theoretical and AppliedClimatology 65:165-174. on Burga, C. A. 1999. Vegetationdevelopment the glacier forefield Morteratsch(Switzerland). Applied Vegetation Science2:17-24. Caccianiga, M., and C. Andreis. 2004. Pioneer herbaceous on in vegetation glacierforefields the Italian Alps. Phytocoenologia34(l):55-89. 2007. UnexCannone, N., S. Sgorbati,and M. Guglielmin. pected impacts of climaticchange on alpine vegetation. in Frontiers Ecologyand the Environment 7:360-364. J. Casty, C, H. Wanner,J. L. Luterbacher, Esper, and R. Bohm.2005. Temperature precipitation and in variability the Journalof ClimaEuropean Alps since 1500. International 25:1855-1880. tolology Catasta, G., and C. Smiraglia.1993. The mass balance of a in cirqueglacier theItalianAlps (Ghiacciaiodella Sforzellina, of Ortles-Cevedale Group). Journal Glaciology39:87-90. CGI (ComitatoGlaciologico Italiano). 1971-1977.Campagne Glaciologiche(Glaciological surveys).Bollettinodel ComitatoGlaciologicoItaliano SerieI and 11:18-25. CGI (ComitatoGlaciologico Italiano). 1978-2006.Campagne Glaciologiche (Glaciological surveys).Geografia Fisica e Dinamica Quaternaria:l-25. Chapin,F. S., L. R. Walker,C. L. Fastie,and L. C. Sharman. 1994. Mechanisms primary of successionfollowing deglaciation at Glacier Bay, Alaska. Ecological Monographs64: 149-175.

Chinn, T. J. 1999. New Zealand glacierresponseto climate changeof the past 2 decades. Global and Planetary Change 22:155-168. Cogley,J.G., and W. P. Adams. 1998.Mass balanceofglaciers otherthantheice sheets. Journal Glaciology44(147):315of 325. Cook, A. J., A. J. Fox, D. G. Vaughan, and J. G. Ferrigno. 2005. Retreating on Peninsula glacierfronts the Antarctic over thepast half-century. Science308:541-544. G. Diolaiuti,G., C. Smiraglia, Vassena, and M. Motta. 2004. of Glacier, Dry calvingprocessesat the ice cliff Strandline Northern VictoriaLand, Antarctica. Annals of Glaciology 39:201-208. M. Dyurgerov, B., and M. F. Meier. 2000. Twentieth century climatechange:evidencefrom smallglaciers. of Proceedings theNational Academyof Sciences(USA) 97:1407-1411. Egh, M., M. Wernh,C. Kneisel, and W. Haeberli. 2006. in Meltingglaciersand soil development the proglacialarea Morteratsch(Swiss Alps): I. Soil type chronosequence. and Arctic, Antarctic, Alpine Research38:499-509. Galen, C, and M. N. Stanton. 1995. Responsesof snowbed to season length.Ecology plant-species changesin growing 76:1546-1557. and Grabherr, M. Gottfried, H. Pauli. 1994.Climateeffects G., on mountain plants.Nature369:448. M., Guglielmin, A. Nardo, and C. Smiraglia.1995.Lo spessore dei ghiacciaidella Valfurva.Misurazionitramite Sondaggi Elettrici Verticali. Neve e Valanehe 24:58-67. and climatechange Haeberli, W. 1995. Glacier fluctuations detection operationalelements a worldwide of monitoring WorldMeteorological Bulletin 44:23strategy. Organisation 31. Haeberli,W., and M. Beniston.1998. Climatechangeand its in impactson glaciersand permafrost the Alps. Ambio 27: 258-265. M. Haeberli,W., R. Frauenfelder, Hoelzle, and M. Maisch. 1999.On ratesand acceleration trends global glacier of mass Annaler81A:585-591. changes.Geografiska of Haeberli,W., and M. Hoelzle. 1995. Application inventory data for estimating characteristics and regionalclimateof on changeeffects mountainglaciers:a pilot studywiththe EuropeanAlps. Annalsof Glaciology21:206-212. Hoelzle, M., W. Haeberli,M. Dischl, and W. Peschke.2003. Secularglacier massbalancesderived from cumulative glacier length changes.Global and Planetary Change 36:295-306. IAHS (ICSI)-UNEP-UNESCO. 1988-2005. Glacier Mass Balance Bulletins(GMBBs). Volumes 1-8. World Glacier Service, Zurich,Switzerland. Monitoring IPCC. 2001. ThirdAssessment Reportof the Intergovernmental Panel on ClimateChange. CambridgeUniversity Press, UK. Cambridge, M. auf Jochmisen, 1970. Die Vegetationsentwicklung Moraenenboden in Abhaengigkeit von einigen Umweltfaktoren. Innsbruck 1-22. 46: VerlagUniversitat Kaser, G., A. Fountain,and P. Jansson.2003. A manual for the mass balance of mountain glaciers. IHP monitoring Technical Docu(International HydrologicalProgramme), mentsin Hydrology, UNESCO, Paris,France. 59. Keller, F., S. Goyette,and M. Beniston. 2005. Sensitivity and their analysisof snowcoverto climatechangescenarios ClimaticChange impacton plant habitatsin alpine terrain. 72:299-319. Keller, F., F. Kienast, and M. Beniston.2000. Evidence of responseof vegetationto environmental change on highelevationsitesin the SwissAlps. Regionaland Environmental Change l(2):70-77. and Martin, and Y. Durand. 2006. Precipitation snowcover E., in variability the French Alps. Lecture Notes in Earth Sciences.Volume74. Springer, Berlin/Heidelberg, Germany.

648

NICOLETTA CANNONE ET AL.

EcologicalApplications Vol. 18,No. 3

Matthews,J. A. 1992. The ecology of recently deglaciated terrain. UK. Press,Cambridge, University Cambridge 2000. GerminaNiederfriniger Schlag,R., and B. Erschbamer. tion and establishment seedlings a glacierforeland of on in the Central Alps, Austria. Arctic,Antarctic, and Alpine Research32:270-277. Oerlemans,J. 2001. Glaciers and climatechange. Balkema, Netherlands. Rotterdam, J. a Oerlemans, 2005. Extracting climate signalfrom169glacier records. Science308:675-677. T. A. Oerlemans, B. Anderson, Hubbard,Ph. Huybrechts, J., A. W. Johannesson, H. Knap, M. Schmeits, P. Stroeven, R. S. W. van de Wai, J. Wallinga, and Z. Zuo. 1998. Modelling the response of glaciers to climate warming. ClimateDynamics14:267-274. of Oerlemans, and J.P. F. Fortuin.1992.Sensitivity glaciers J., and smallice caps to greenhouse Science258:115warming. 117. 0strem, G., and M. Brugman. 1989. Glacier mass-balance measurements.National Hydrology Research Institute, Canada. Saskatoon,Saskatchewan, Patzelt,G. 1985. The period of glacieradvances in the Alps, 1965to 1980.Zeitschrift Gletscherkunde Glazialgeofur und logie 21:403^07. and W. Paul, F., A. Kaab, M. Maisch, T. Kellenberger, Haeberli. 2004. Rapid disintegration Alpine glaciers of observedwith satellitedata. GeophysicalResearch Letters 31:L21402[doi: 10.1029/2004GL0208161. and 1999.Vascularplant Pauli, H., M. Gottfried, G. Grabherr. distribution at limitsof plant patterns the low temperature life theAlpine-nival ecotoneof Mount Schrankogel (Tyrol, 29:297-325. Austria).Phytocoenologia Pavan, M., G. Diolaiuti, V. Maggi, C. Smiraglia,and C. sul D'Agata. 2000. Prospezionigeofisiche Ghiacciaio della Sforzellina Ri(Alpi Lombarde,Gruppo Ortles-Cevedale). sultati Neve e Valanghe41:6-13. preliminari. S. Pignatti, 1982. Flora d'ltalia. Three volumes. Edagricole, Bologna,Italy. of Pirola,A., and V. Credaro.1993.Changesin thevegetation a recent glacial moraine in the Bernina group. Annali di BotanicaLI:145-153. sul Pirola,A., and V. Credaro. 1994. Osservazioni dinamismo della vegetazione morenarecente Gruppodel Bernina. di nel Fitosociologia27:139-149. Pluess, A. R., and J. Stocklin. 2005. The importanceof on population origin and environment clonal and sexual in reproduction the alpine plant Geum reptans.Functional Ecology 19:228-237.

2004. Comparativevegetation Raffl,C, and B. Erschbamer. crossinga characteristic glacier analyses of two transects 32:225-240. valleyin theCentralAlps. Phytocoenologia Glacierdata base. (www. RegioneLombardia.2004. Lombardy cartografia.regione.lombardia.it) Resnati,C, and C. Smiraglia.1989.Ghiacciaiodella Sforzelliversosondaggi na. Misuredello spessoredel ghiacciaioattra RivistaClub Alpino Italiano 110(6):70-75. geoelettrici. Root, T. L., J. T. Price, K. R. Hall, S. H. Scheider,C. of and A. J. Pounds. 2003. Fingerprints global Rosenzweig, on warming wildanimalsand plants.Nature421:57-60. C. Rossi, S., G. Diolaiuti,E. Forasacco, M. Pelfini, Smiraglia, della piu and P. Spreafico. 2003. Evidenzegeomorfologiche recenteespansione glaciale correlabileall'episodio freddo deglianni '50-70 del XX secolo sulleAlpi Lombarde.Pages editors. 377-395 in M. Motta and A. Biancotti, Rispostadei alle processi geomorfologici variazioniambientali.Glauco Genoa, Italy. Brigati, Rott, H., P. Skvarca,and T. Nagler. 1996. Rapid collapse of Antarctica. Science271:788-792. northern Larsen Ice Shelf, undWachstumsmuster J. Stocklin, 1992.Umwelt, Morphologie Pflanzen eineUbersicht. BotanicaHelvetica102:3klonaler 21. Stocklin, J., and E. Baumler. 1996. Seed rain, seedling establishment and clonal growthstrategieson a glacier Science7:45-56. foreland. Journal Vegetation of J. Theurillat, P., and A. Guisan. 2001. Potentialimpact of in climate changeon vegetation theEuropeanAlps: a review. ClimaticChange 50:77-109. E. and R. G. D., Tscherko, U. Hammesfahr, Zeltner, Kandeler, microbial Bocker. 2005. Plant successionand rhizosphere Basic in communities a recently deglaciatedalpine terrain. and AppliedEcology6:367-383. J. Uppenbrink, 1999. The NorthAtlanticOscillation.Science 283:948-949. 1999.Digitizing T., maps.Pages201Vogtle, and K. J.Schilling. editors. GIS forenvironmen216 inH.-P. Bahrand T. Vogtle, tal monitoring. Schweizerbart, Germany. Stuttgart, G. and C. A. Burga.2005. Trendsin Walther, R., S. BeiBner, the upward shiftof alpine plants. Journalof Vegetation Science 16:541-548. in R. Whittaker, J. 1993. Plant populationpatterns a glacier foreland succession: pioneer herbs and later-colonizing shrubs.Ecography16:117-136. Wood, F. 1988. Global alpine glaciertrends1960s to 1980s. and Arctic, Antarctic, AlpineResearch20:404-413. Zemp, M., W. Haeberli,M. Hoelzle,and F. Paul. 2006. Alpine decades?GeophysicalResearch glaciersto disappearwithin Letters 33:L13504. [doi: 10.1029/2006GL026319]

Anda mungkin juga menyukai