Growth rings in herbs and shrubs

ISSN1424-5108ForestSnowandLandscapeResearchVolume79,Issue3,2005195–415GrowthRingsinHerbsandShrubs:lifespan,agedeterminationandstemanatomyFritzHansSchweingruberandPeterPoschlodPublishersSwissFederalResearchInstituteWSL,BirmensdorfHaupt,Berne,Stuttgart,ViennaCerastiumsemidecandrumL.,Caryophyllaceae.CollectedApril6th2005inavineyardinFully,Valais,Switzerland.Transversesectionofa0.9mmthickrootcollarstainedwithAstrablueandSafranin.Magnification120x.Thexyleminthecenterissurroundedbyacambium,aphloem,acortex,anexodermisandanepidermis.Thexylemischaracterizedbyarayless,unlignifiedparenchymatictissue(blue),inwhichslightlylignifiedvesselsareembedded(reddish).Theconcentrationofvesselsattheperipheryofthexylemindicatesthattheannualherbgerminatedinfall,stoppedgrowthinwinterandfinisheditslifeperiodinspring.Thecambiumisonetotwocellswide.Typicalforthephloemisthecompositionofverysmallsieveelementsandthesmallparenchymaticcells.Thethickbeltwithlargecellsrepresentsthecortex(darkblue).Itissurroundedbytheexodermis,wherethecellwallsareintensivelylignified(red).Theoutermostthin-walledcellsrepresenttheepidermis.197For.SnowLandsc.Res.79,3:195–415(2005)GrowthRingsinHerbsandShrubs:lifespan,agedeterminationandstemanatomyFritzHansSchweingruber1andPeterPoschlod21WSLSwissFederalResearchInstitute,Zürcherstrasse111,CH-8903Birmensdorf,Switzerland.fritz.schweingruber@wsl.ch2InstituteofBotany,FacultyofBiologyandPreclinicalMedicine,UniversityofRegensburg,D-93040Regensburg,Germany.peter.poschlod@biologie.uni-regensburg.deRevisedmanuscriptaccepted17October,2005AbstractGrowthRingsinHerbsandShrubs:lifespan,agedeterminationandstemanatomyCantheageofherbs,dwarfshrubsandshrubsbedetermined,andifso,howoldcantheyget?Andwhatpossibilitiesexistforansweringecologicalquestionsaboutplantsandpopulationsusingtheagesofsuchplants?TheseandmanymorequestionspromptedustoanalysethegrowthringsobservedincentralEuropeanherbs,dwarfshrubsandshrubs,andalso,moregenerally,toreviewthestateoftheartforclassifyinganddeterminingtheageofplants.Wealsoexplorehowtheknowl-edgeofthepresenceofgrowthringscanbeappliedtoecologicalandbiologicalconservationques-tions,andwhichfactorsmaylimitthelifespanofplants.Wepresenttechniquesandprerequisitesforidentifyinggrowthringsandforvalidatingthattheyareactuallyannualrings.Thelimitationsofgrowth-ringanalysisarediscussed.Theanatomyoftherootcollarsofabout800centralEuropeanspeciesisgiven.Themethodsofageclassification/determinationreviewedinclude:annualringandotherchrono-logicalmethods,growthformanalysis,permanentplotresearch,andhistoricalandgeneticanaly-ses.Theapplicationofgrowth-ringanalysistodescribepopulationstructuresallowsthecurrentstatusofapopulationtobeassessed.Severalexamplesaregiven.Physiologicalandenvironmentalfactorsthatmaylimitaplant’slifespanarereviewed.Preliminaryresultsevaluatingourdatasetshowthatlifespanmaybelimitedbytemperatureandnutrients.Keywords:lifespan,growth-ringanalysis,annualrings,plantanatomy,ontogeny,herbs,dwarfshrubs,shrubs,plantpopulationstructure,temperature,nutrients,moisture199For.SnowLandsc.Res.79,3(2005)PrefaceLifespanisakeytraitinthelifehistoryofplants.Whatdeterminesaplant’ssurvivalunderspecificenvironmentalconditions?Manyfactorsaffectaplant’slifespanandhelpusident-ifyitsage,suchas:morphological,anatomical,ontogenetic,physiologicalandecologicalfac-tors,andeventhestructureofpopulations.Untilnow,therehasbeennooverviewtakingintoaccountalltheseaspectsandonlyafewstudiesofthelifespanofnon-trees.Suchanoverviewwould,wethought,beanexcitingchallengeinwhichwecoulddrawonourexperienceindif-ferentfields.Forthefirstauthorthishasbeenindendrochronologyandwoodanatomy,andforthesecondinpopulationbiologyandvegetationecology.Thisoverviewis,inouropinion,longoverdue.Untilrecentlyecologistsseemtohavelargelyignoredthefactthattheageofnon-woodyplantscanalsobedetermined,andplantphysiologistsstillciteMOLISCH(1929,1938)whentheydiscussthelifespanofawholeplantorplantageing.Ourmainaimistoencouragescientistsfromdifferentdisciplinestoasknewquestionsbyofferingthemnotonlyacatalogueofspecieswhoseannualringscanbeanalysed,butalsotoencourageastate-of-the-artoverviewofhowtomeasurethelifespanandpersistenceofanumberofplantspecies.Inthefuturewehopethatitwillbepossibletodeterminethelifespanandpersistenceofplantswithprimaryrootspossessinggrowthrings,aswellastoanalysetheshort-termdemographyofperennialspecies.Whereannualgrowthratesandvegetationcarbonstoragecanbemeasuredintheherbandshrublayer,itshouldalsobepossibletoexamineissuessuchastheextenttowhichplantlifespandependsonhabitatqualityortheeffectofdifferentenvironmentalconditionsonpopulationstructures.Analysesofpopulationstructuresshouldalsohelpustoevaluatethesuccess,orotherwise,ofconservationorresto-rationmanagementtreatments.Finally,wehopethatthisoverviewandreviewwillencourageplantphysiologiststogivefurtherthoughtnotjusttothedeathofacelloranorgansuchasaleaf,butalsotothewholeplantandvariousrelatedaspects.Meetingthischallengewouldnothavebeenpossiblewithoutthehelpofmanycolleaguesandfriends:StephanKrebs(LEL,SchwäbischGmünd,Germany)introducedustoErnstRieger(Blaufelden,Germany),withoutwhosegeneroussupportwewouldnothavebeenabletoprovethatannualringsinherbsarereallyannualrings.Heletusdiginthefieldswherehecultivatesaninnumerablenumberof“wildspecies”,withexactsowingdatesrecordedforindividualsofabout30species.Anne-KathrinJackel(Regensburg,Germany)provideddataongrowthformsfromtheBioPopdatabaseand“managed”the“Swissdata”.ChristineRömermann(Regensburg,Germany)puttogetherdataonvegetationtypesandlifeforms.DuringtheliteraturesearchwefoundahugeamountofmaterialinRussianonthesetopics,whichwastranslatedfromRussianintoGermanbyWiolettaMoggert(Regensburg,Germany).HertelephonecallstoRussiaarealreadylegendary:theymadeitpossibleforustoconsultmissingvolumesoftheBiologicalFloraofMoscow.FrantisekKrahulec(PragueandPruhonice,Czechia),fromtheInstituteofBotanyattheCzechAcademyofSciences,providedthefirstpaperbyRabotnovontheontogeneticclassificationofspecies,whichwasavailableneitherinGermanynorinSwitzerland.NinaUlanova(Moscow)alsosentsomeRussianliterature.Thediscussionswehadwithher(bye-mail)ontheontogeneticconceptsofRabotnovwereveryhelpful.WealsothankBertilKrüsi,whoprovidedunpublisheddatafromstudiesonthegrowthrateandageofBrachypodiumpinnatumpatchesandJeremyFlower-Ellis,whoprovidedacopyofhisthesis.TanjaDonaubauer,OliverGeuss,IsabelHoffmann,JohnHoffmann(allRegensburg,Germany),ClaudiaBaumberger(Biel,Switzerland),MarionandRichardJoss-Petersdorf(Schlatt,Winterthur,Switzerland),AndreaMünchandRuthSchwarz(Würzburg,Germany)andYvonneSteiner(Basel,Switzerland)providedunpublisheddatafromtheirthesesandresearchwork.Karl-FriedrichSchreiberhelpedTanjaDonaubauerandthesecondauthorinthefieldtodigupindividualsforannual-200ringanalysis.SpecialthanksgototheSwissFederalInstituteforSnowandAvalancheResearch(SLF)inDavosandtheSwissFederalInstituteWSLinBirmensdorf.Bothinsti-tutionshaveallowedthefirstauthortoworkintheirlaboratoriessincehisretirement.TheSwissNationalScienceFoundationsupportedthefirstauthorfor15yearsinhiscollectionofplantmaterialandpreparationofslides.Finally,wehavetothankVanessaWinchester(Oxford,UK),andSilviaDingwall(Nussbaumen,Switzerland),whohavepatientlycorrectedourEnglish.Theirnicecommentshavebeenrefreshingandstimulating.Wearealsogratefulforthehelpfulfeedbackfromtwoanonymousreviewers.ManythanksalsotoRuthLandoltforeditingthelargemanuscriptandtoSandraGurzeler,MargritWiederkehr,andJacquelineAnnenfortheircarefullayout.BirmensdorfandRegensburg,October2005FritzSchweingruberandPeterPoschlod201For.SnowLandsc.Res.79,3(2005)ContentsAbstract197Preface1991Introduction2032Ageclassificationanddeterminationofherbs,dwarfshrubsandshrubs–205thestateoftheart2.1Softclassifications2052.2Hardclassifications2082.3Agedetermination2113Determiningtheageandgrowthdynamicsofherbsandshrubsbytheanalysis223ofgrowthrings3.1Areannualringsannualrings?2233.2Limitationsonusingringcountingtoestimatetheageofanindividual2283.3Crossdating2314Morphologicalpre-requisitesofgrowth-ringanalysis2335Analysisandanatomyofgrowthrings2375.1Preparationandmicroscopictechniques2375.2Stemanatomy2405.3Growth-ringcharacteristicsinthexylemandphloem2506AgestructureofCentralEuropeanherbsanddwarfshrubs2637Populationagestructure:examplesoftheapplicationofgrowth-ringanalysis265toissuesinecologicalandbiologicalconservation7.1Agestructureofpopulationsandsuccessionalstage2687.2Agestructureofpopulationsandmanagement2707.3Agestructureofpopulationsandrestorationmanagement2737.4Agestructureandreconstructionoflandscapehistory2758Whatrestrictsthelifespanofaplant?Stateoftheartandanalysisof277ourdataset8.1Physiologicalfactors2778.2Ecological/environmentalfactors2789Conclusions28510Summary28711References289Appendices301Glossary302TableA1306Atlas315203For.SnowLandsc.Res.79,3(2005)1IntroductionLifespanisoneofthemostimportantcharacteristicsinthelifehistoryofanorganism,ani-malorplant(WEIHERetal.1999).Thischaracteristiciscentraltotheoreticalconceptssuchasr-andK-selection(MACARTHURandWILSON1967;PIANKA1970)andC-S-Rselection(GRIME1979,2001).However,dataontheageofaplantoreventhepotentialmaximumageofaplantspeciesasawholeareoneoftheleastaccessibleparametersinthelifehistoryofplants(DIETZandSCHWEINGRUBER2002).Theageofnon-treesisalmostcompletelyignoredintheflorasoftheworld,exceptfordataonthe(maximum)ageoffewspecies,giveninthefirstbiologicalflora,the“LebensgeschichtederBlütenpflanzen”(KIRCHNERetal.1908ff),TheBiologicalFlorasoftheBritishIsles(SALISBURY1928;BritishEcologicalSociety1941;CLAPHAMetal.1958),TheBiologicalFloraofMoscow(RABOTNOV1974ff;PAVLOVetal.1990ff;PAVLOVandTIKHOMIROV1995ff;PAVLOV2000ff)andCentralEurope(MATTHIESandPOSCHLOD2000).AbibliographicaloverviewoftheseBiologicalFlorasisgiveninPOSCHLODetal.(1996).Todate,exactdataontheindividualageofalimitednumberofplantshavebeenpro-videdbygrowth-formanalysisbasedonannualmorphologicalmarkers(e.g.TROLL1937),theanalysisofannualringsinwoodyplants(e.g.SCHWEINGRUBER1990),orpermanentplotresearch(e.g.TAMM1948ff.).Lessdetailedinformationonindividualagehasbeenbasedeitherontheontogeneticstageofanindividualoritssize(e.g.LINKOLA1935,RABOTNOV1950).Thepresenceofannualgrowthringsinherbaceousplants,describedbyMOLISCH(1929,1938),VIDAL(1906),ZOLLER(1949),andKERSTER(1968),wassummarizedbyHARPER(1977)inthecontextofecologicalstudies.However,thisknowledgewasneglectedorevenignoreduntilitwas“rediscovered”recently(DIETZandULLMANN1997;SCHWEINGRUBERandDIETZ2001;DIETZandSCHWEINGRUBER2002)1.Theidentificationandanalysisofgrowthringsrequireshowever,adetailedknowledgeoftheanatomyoftherespectivespecies(SCHWEINGRUBER2001).Untilnow,therehasbeennooverviewoftheanatomyofgrowthringsinnon-trees.HARPER(1977p.557)statesthatitwouldbe“asnareanddelusiontobelievethatagestructuresofferaneasyshortcuttounderstandingpopulationdynamics”.Nevertheless,thepopulationdynamicsoflong-livingperennialscanbeanalysedifdetailsofapopulation’sagestructureareaddedtootherdemographicdatacollectedoverseveralyears.Inaddition,exactdataonlifespanscanalsobeusedtovalidatetheresultsofpredictiveapproachestolifespanmodelling(EHRLÉNandLEHTELÄ2002).RABOTNOV(1950ff)developedanalternativeapproachdescribingpopulationstructuresbasedontheontogeneticanalysisofplants.However,thisapproachhasstillbeenalmostcompletelyignoredoutsideRussian-speakingcountries,apartfromareferencetotheRussianschoolinHARPER(1977),severalpapersinEnglish(GATSUKetal.1980),severalchaptersinWHITE(1985)andthetranslationofatextbookinGerman(RABOTNOV1995).1DIETZandULLMANN(1997)createdanewtermforthestudyofannualringsinherbaceousspecies–“herbchronology”incontrastto“dendrochronology”.Thistermiscorrectaslongasstudiescon-centrateexclusivelyonherbs.However,theGreektermdendrosmeansonly“tree”,whereastheLatinnameherbameans“herbs”andalso“plants”.Thusweshouldreallyfindnewtermsforshrubsanddwarfshrubsaswell,asthetermsaretoobroad.Andwhataboutthechronologyofgrass-likespecieswhichalsohaveclearannualmorphologicalmarkers?Wewouldprefertouseatermthatiscleartoeverybody,e.g.:chronologyofherbs,dwarfshrubs,etc.Whereannualgrowthringsareusedtodeterminetheageofanindividual,wesuggestthetermshouldbechronologyoragedetermi-nationbygrowth-ringanalysis.Wedonotproposechangingthetermdendrochronologysinceitisalreadywellestablished.204FritzHansSchweingruber,PeterPoschlodThisRussianapproachis,therefore,alsoincludedinourreview.Todate,correlationsbetweenageandfecundityinherbsanddwarfshrubshavebeenlittlestudied.Nordoweknowmuchwhichfactorsaffectlifespan(THOMAS2002).Dotheseplantshaveaninternalclockoristheirlifespanstronglyaffectedbyenvironmentalfactorsand,ifso,bywhichenvironmentalfactors(LARSON2001)?Sinceherbsoftenoccupyhabi-tatswheretreesnevergrow,analysesofannualgrowthringsinherbsshouldallowusnotonlytoexaminetheoriesthatwereinitiallydevelopedfortreespeciesbutalsotodevelopnewtheories.ObjectivesInsummary,weknowlittleabouttheageandanatomyoftheshootsofdicotyledonousherbs,whileourcorrespondingknowledgeaboutdwarfshrubsandshrubsisalsolimited.Thisreview,therefore,hasfiveprincipalaims:1Toprovideanoverviewofpossiblewaysofdeterminingtheindividualageofaplant,includingtheontogeneticapproach.2ToprovideananatomicaloverviewandtodemonstratetheenormousvariabilityofthexylemseenintransversesectionsofhundredsofnativecentralEuropeanherbsanddwarfshrubs.3Toevaluatewhethergrowthringsaresufficientlydistincttobesuitableforagedetermi-nationinrootcollarsandplantrhizomes.4Toexplorethefactorslimitingthelifespanofherbsandshrubs.5Toprovidedataontheagestructureofplantpopulationsandtoshow,withexamples,theapplicationofgrowth-ringanalysisinecologicalandpopulationstudies.NomenclatureThenomenclatureisbasedontheoriginalnamesintherelevantliterature.Inchapters3to5,aswellasintheAtlaspartofthisbookweusethenomenclatureofLAUBERandWAGNER(2001).205For.SnowLandsc.Res.79,3(2005)2Ageclassificationanddeterminationofherbs,dwarfshrubsandshrubs–thestateoftheartAgedeterminationofplantsotherthantrees,namelyshrubs,dwarfshrubs,herbsandmono-cotyledonousplantsincludinggramineousorliliaceousspecies,hasbeencarriedoutbothinthepastandmorerecently(SCHLAGINTWEITHundSCHLAGINTWEITH1850,ROSENTHAL1904,KANNGIESSER1907ff,MOLISCH1929,RAUH1937,TROLL1937,ZOLLER1949,STEINGERetal.1996,DIETZandULLMANN1997).Previously,methodsofagedeterminationincludedlifeandgrowth-formanalysis,age-stateanalysis,dendrochronologyandthemoni-toringofindividualsonpermanentplots.Recently,thecombinationofgrowthratesandgeneticanalysishasevenallowedtheageingofclones.Inthefollowing,thepossibilitiesaswellasthelimitationsofthesedifferentmethodsaredescribed.2.1SoftclassificationsLifeformTheclassificationoflifeformsisarough,butverycommonmethodfordescribingthelifespanofaplantspecies.LifeformswerefirstdescribedbyWARMING(1895,1909).Hedis-tinguishedhapaxanthous(monocarpic)plants,includingannualsandbiennialsreproducingonlyonce,frompollacanthous(polycarpic)plants,whichreproducerepeatedlyandare,therefore,alwaysperennials(Table1).Table1.Life-formtypesaccordingtofloweringfrequency(WARMING1909).Onlythemaingroupsaredistinguished.FloweringfrequencyLifespanTypeMonocarpicannualAnnualsMonocarpicbiennialBiennialsMonocarpicperennialPluriennials,hapaxanthousPolycarpicperennialPollacanthousRAUNKIAER(1910,1934)developedanotherapproachfocusingonenvironmentallyadapt-ivemechanismsforplantsurvivalduringunsuitablegrowingperiods,suchassnowywintersintemperateregions.Raunkiaer’sclassificationofbudsandseedswasbasedonthepositionoftheregenerativeorgans(Fig.1):phanerophytes(regenerativebudsabovegroundandmorethan30cmabovethesoilsurface);chamaephytes(regenerativebudsabovegroundandlessthan30cmabovethesoilsurface);hemicryptophytes(regenerativebudsabovegroundandatthesoilsurface);crypto-orgeophytes(regenerativebudsbelowground–rhi-zomes,bulbs,onionsetc.),andtherophytes(annualswhichsurviveasseedsonthesoilsur-faceorbelowground).Inmanyfloras,allspecieshavealreadybeenclassifiedaccordingtotheirlifeforms.Furthermore,differentiationsaremadebetweenannuals,biennialsandperennials(e.g.thecentralEuropeanflora:ELLENBERGetal.1992).Annualplantsareplantsthatcompletetheirlifecycleanddiewithin12months,althoughthelifespansmayoverlaptwocalendaryears(winterannualsincontrasttosummerannuals,HARPER1977).Perennialsmaylivefortwoormoreyears.Biennialsarethosethatformvegetativerosettesinthefirstyear,andfloweranddieinthesecondyear.However,HARPER(1977)alsostates“therearenonaturalbreaksinthecontinuumofplantlifecycles(andthat)separationintothecategoriesofannual,biennialandperennialisratherarbitrary”.Healsoadds“itis,however,verydoubt-fulwhetherthiscategoryofbehaviourisclearlydefinedinnature:thebiennialhabitisonlyanextensionofthephenologyofthewinter-germinatingannualwhichalsomakessome206FritzHansSchweingruber,PeterPoschlodgrowthinthelateautumnofonecalendaryearandresumesandcompletesitsgrowthcycleinthespringofthesecondyear”.JÄGER(2000)notedthatmostoftheso-calledbiennials,whichareabletolivemorethantwoyearsbutwhichdieafterfirstflowering,aremono-carpicperennialsorso-calledhapaxanthousorsemelparousplants(incontrasttothepolla-canthousorpolycarpicoriteroparousperennials).Despiteacertainplasticity,thereareonlyafewspecieswhereecotypesaredifferentinlifeformorlifespan:lifeformsarespeciesspecific.Therefore,lifeformsprovideasuitablebasisfordescribingthe“agestructure”ofphytogeographicregions,ecosystems(e.g.RAUNKIAER1910,1934;WALTER1973)orplantcommunities(BRAUN-BLANQUET1964;DIERSCHKE1994),buttheyarenotsuitablefordescribingplantpopulations(Table2to4).Table2givesanoverviewoflifeformsinphytogeographiczonesorbiomes.Long-livedlifeforms,suchasphanerophytes,dominateintropicalzonesandhemicryptophytesdominateinnemoral,arcticoralpinezones,whereasshort-livedlifeformssuchastherophytesaremostfrequentindesertsandthemeridionalzone.Proportionally,thelifeformsincentralEuropeanplantformationsorcommunitiesfavourshort-livedlifeformsinarableweeds,ruderalformations/communitiesorpioneercommunities(Table3,4).Thisbiasreflectstheroleofthedisturbancefactorinthepro-portionofshort-livedlifeforms.Themoreintenseorthemorefrequentthedisturbanceis,theloweristheproportionoflong-livedlifeforms(seealsother/Kconcept,CSR-conceptetc.;PIANKA1970;GRIME1979,2001).Table2.Life-formspectraofselectedphytogeographiczones,beltsorecosystems(WALTER1973).P–phanerophytes,Ch–chamaephytes,H–hemicryptophytes,C–cryptophytes=geophytes,T–thero-phytes.Zone/ecosystemSitePChHCTTropicalzoneSeychelles61612516DesertsLibya122120542Cyrenaika91419850MeridionalzoneItaly126291142NemoralzoneParisbasin86.551.5259Swissmidland105501520Denmark73502218ArcticzoneSpitsbergen12260152AlpinebeltAlps–24.56843.5Fig.1.Life-formsaccordingtoRAUNKIAER(1937).1–phanerophyte,2aand2b–chamaephytes,3atoc–hemicryptophytes,4aand4b–crypto-orgeophytes,5–therophyte.207For.SnowLandsc.Res.79,3(2005)Table3.Life-formspectraofselectedcentralEuropeanplantformations,accordingtoELLENBERG(1996).No.–Numberofspecies;P–phanerophytes,NP–nanophanerophytes,wCh–woodychamae-phytes,hCh–semi-woodychamaephytes,H–hemicryptophytes,C–cryptophytes=geophytes,T–therophytes;Hyd–hydrophytes.PlantformationsNo.PNPwChhChHCTHydFreshwaterandmirevegetation2810.20.02.03.537.012.63.541.2Seawaterandsaltmarshvegetation2960.00.00.05.042.511.333.88.8Arableweedandruderalvegetation4710.00.00.02.135.56.754.41.1Rocksandalpinevegetation7320.00.32.922.464.16.34.20.0Heathsandgrasslands2800.00.03.18.360.613.015.10.0Tallperennialherbandshrubveget.931.26.63.63.075.37.83.00.0Coniferousforests2085.311.725.510.627.713.84.30.0Deciduousforests9919.233.32.76.949.029.52.70.4Table4.Life-formspectraofselectedcentralEuropeanplantcommunities,accordingtoKORNECKetal.(1996).No.–Numberofspecies;P–phanerophytes,NP–nanophanerophytes,wCh–woodychamae-phytes,hCh–semi-woodychamaephytes,H–hemicryptophytes,C–cryptophytes=geophytes,T–therophytes;Hyd–hydrophytes.communitiesPlantcommu