The functional correlates of heteroblastic variation in leaves: Changes in form and ecophysiology with whole plant ontogeny - Sociedad Argentina de Botánica

Bol. Soc. Argent. Bot. 36(1-2):171

-

184. 2001

ARTICULO INVITADO

THE

FUNCTIONAL CORRELATES OF HETEROBLASTIC VARIATION IN LEAVES:

CHANGES

IN FORM ANDECOPHYSIOLOGY

WITH WHOLE PLANTONTOGENY CYNTHIA S.JONES1

Summary:Thisreview draws from literatureonplant heteroblastic developmentandecophysiologyto

examine how leaf form andfunction change withplant ontogeny. Within the context of leaftraits

identifiedasimportant forplantfunctionacross ecosystems,seedlingleaves decrease inspecificleaf area, butinitially increase inphotosynthetic rates(i.e.netassimilation rates)up toa pointwherethey

leveloff for aperiod. Seedlingleaves generally havelower wateruse efficiencies thanolder leaves,

andare predicted tohave very high time-discountingrates.Later stagesof plantontogeny involving shifts from“juvenile” to “adult” modes ofgrowthappeartoextend the trends establishedamong seedling-leaves, e.g. specific leafareasin“juvenile” foliage are higher thaninlater foliageand water use

efficienciesaregenerallylower.Photosynthetic ratesperunitareagenerally differbetweenjuvenileand

adultleaves,but the differencecan occur ineither direction, dependingon habitat. Developmental stages alsohavesignificantimpacton plant resistance toherbivores. The dramatic changes inleaf shapeduringontogeny that wouldberecognizedasheteroblastyappear to enhanceand extend the trends of ontogenetic functional changespresent inall plants. It is worth noting that functional

consequencesofheteroblasticvariationin leaf shapehave been examinedin remarkably few species. <

Keywords:heteroblasty,leaf form, leafecophysiology,ontogeny, phase change, specific leafarea, seedlings

Resumen:Los correlatos funcionalesde la variaciónheteroblásticaen hojas: Cambiosen laformay ecofisiologíacon laontogeniadejaplantacompleta. Esta revisiónse basa en laliteratura sobredesarrollo

heteroblásticoen plantasysu ecofisiologíapara examinar cómola formayla funcióndelahojacambian con la ontogeniade laplanta. Enelcontextode loscaracteresfoliares identificadoscomo importantes para la funciónde la plantaen los ecosistemas,las hojasde lasplántulas disminuyensu área foliar específica, peroinicialmenteaumentanen lastasasfotosintéticas (es decirtasasde asimilaciónnetas) hastaunpuntoen elcualse nivelan por un período.Las hojas delasplántulasgeneralmentetienen menor eficienciaen el usodel agua que lashojas másadultas, prediciéndosequetienen tasasde descuento de tiempomuy altas. Estadiosposterioresque involucrancambiosdemodos de crecimiento

de«juveniles»a«adultos» parecenextenderlastendenciasestablecidas entre las hojas de las plántulas,

e.g.áreas foliares específicasen follajes«juveniles»sonmayoresqueaquellas de follajestardíosyla eficiencia en el uso delaguaesgeneralmentemenor. Lastasasfotosintéticaspor unidad de área

generalmente difierenentrehojas juvenilesyadultas,pero la diferencia puede ocurrir encualquier

dirección,dependiendodelhábitat.Los estadiosdel desarrollo tambiéntienen,un impacto significativo en la resistencia de lasplantasalos herviboros.Los dramáticoscambiosen la forma de la hojadurante la

ontogenia,reconocidoscomo heteroblastia,parecenaumentaryextender las tendencias de cambios

ontogenéticosfuncionales presentesentodaslasplantas. Es interesantemencionar que las consecuencias funcionalesde lavariación heteroblástica de la formade lahojaha sido examinada en, increíblemente,

unas pocas especies.

Palabras clave:heteroblastia, forma foliar,ecofisiología foliar,ontogenia,cambio de fase, área foliar específica,plántulas

The modularormetamericnatureofplantgrowth offerstwocontrasting views of their form. Construc¬ tionally,plant growth appears relatively simple: simi¬ larunitsareadded sequentiallytopreviously exist¬ ing units inpatterns determined by theunderlying,

genetically determined architecturalpattern. Devel-opmentally, however,eachnewunit is initiated within

the physiological milieu established by the previous developmental history of the whole plant. Thus both the cost andpotential contribution ofthatunit are spatially and temporally contingentuponitsprevi¬ ousgrowth history.Itfollows, then, that develop¬ mentaloutcomesof uncommitted primordiaor mer-istemsdependonthe timing of deployment of these structureswithin the architectural framework of the plant, i.e. theconceptof “ontogenetically contingent” development (Diggle, 1994;Watsone/a/.,1995).

Like-Departmentof EcologyandEvolutionary Biology,Unit3043, UniversityofConnecticut, Storrs, Connecticut 06269USA e-mail: [email protected]

wise,atanygivenpoint in the lifetime ofaplant,the conflate heteroblasty with phase change. In addi-value ofanindividual organ suchas aleafdepends tion,“juvenile” and “adult”areoftenusedevenmore onwhen during wholeplant growththeleaftunc- generally(e.g.Lambers,Chapin & Pons, 1998)tora¬ tions (Harper, 1989) andonhow long itpersists rela- fertoyoung,post-seedlingplantsversusreproduc¬

tivetohowitfunctions (Westobyetal., 2000). Becauseeach interconnected and variously inte¬

gratedplant organ is at auniquepoint in itsown largely byadesiretounderstand itsdevelopmental developmental continuum frominitiation throughex- basis, and the emphasis has been largelyonleaves. pansion, differentiation, functional maturity andse- Researchapproaches have focusedonmorphological

nescence,there isacontinual change innumber,size developmentofdifferent leaf forms (e.g.Mueller,1982; and location of nutrientsourcesand sinks inan ac- Richards,1983;Merrill,1986; Jones, 1993; Gerrath& tively growingplant. Thus,it istobeexpectedthat Lacroix,1997),or onmechanisticcontrol overthepro-during thecourseof development fromseedling duction of different forms,using molecular,genetic, through reproductive maturity,aplant willexhibit hormonal, andphysiologicalapproaches (e.g. Roglers shifts inphysiologythat parallel its increasingsize, &Hackett, 1975; Horrell etal., 1990; Brand & andtoalesserextent,its age. Manytimes,whole Lineberger,1992b;Brand&Lineberger, 1992a; Tsukaya

plantdevelopment is accompaniedby changein form etal.

,

2000). Recently, there has beenmoreinterest along the shoot as well, where the vegetative amongecologists and evolutionistsindocumenting metamersdifferin theshapes, sizesorspecial quali- heteroblastic variation andtimingoftransitions inleaf tiesofsequentialorgans.Goebel(1900)usedtheterm formamongnaturalpopulations(Walker & Pate, 1986;

heteroblastytorefertomarked differences inthe “con- Andersson, 1989; Barghi &Gorenflot, 1989), afrd in figuration” of shoots between “juvenile”and“adult” understanding the population genetic basis of hetero¬ phases ofplant development. Differencesoriginally blasty (Wiltshireetal.

,

1998).

noted byGoebelwereleafshape, the ability of seed¬

lingsorcuttings of“juvenile” shootsto rootreadily, blastic development in leaves, there have been few and the ability of only “adult” shootstoreproduce, investigations of its

functional

consequences. All Laterreviews ofheteroblasty (Ashby,1948;Allsopp, plants exhibit changesinstructure,photosynthesis, 1965; 1967) point outthatthe transitions between andwateruseduringnormal plantontogeny. This “juvenile” and “adult”developmentareoften subtle short review considers heteroblasty withinthe con-andcanbeexpressedin bothmorphological and text of ontogenetic changes inecophysiology,

em-physiologicalparameters;hence thetermheteroblasty phasizingthe few studies that have examinedthe

eco--

hascome torefertoall features that change along the physiological consequences of changes inleaf shape. shoot duringplantontogeny.Mostcommonly, how- (Idonotaddress seasonal heteroblasty here). Ifo-ever, the termheteroblasty evokes ontogenetic cus firstonchanges within seedlings, and subse-changes thatcanbeobserved,i.e. changesinmor- quentlyonchanges

from

“juvenile”to“adult”phases ofplant growth. Iuse“juvenile” and “adult”asthe Goebel’soriginaluseofthe term “juvenile” and originalauthors usedthem,for lack of betterterms, “adult”contributedtothe initially implicit, and ulti- with thecaveatthat onlyafew ofthe original authors mately explicit, link between heteroblasty and phase have evaluated acquisition of reproductive compe-change (e.g.Poethig,1990). Theconceptofphase tency for the plants discussed. Myuseof

“seed-change recognizes stablephases ofplant develop- ling”refers ingeneraltothe first few leavesproduced mentthatoccur during the life ofaplant and ulti- afterthe Cotyledons,ortoperennialplants less than mately requires knowing reproductivecompetency, oneyearold,unlessdefinedotherwise by the origi-For severalreasons explained previously (Jones, nal authors.

1999),Ihave arguedthat heteroblasty and

phase

changerepresentdistinct aspectsofplant develop- Ontogenetic changesamongleaves in seedlings

inent.

Sequentialchangesinvegetativemetamers

arenotnecessarily correlated with changes in repro¬

ductive competency. Widespreaduseoftheterms tioninphotosynthesis,the first seedling leaves may “juvenile” and “adult” in the developmental litera- be the first significantsourceofnewly acquired car-ture to describe both phenomena continues to bon for the developingplant. This is especiallyhuein

fiveplants.

The literatureonheteroblasty has been motivated

Despiteourincreasing understanding of

hetero-phology.

func-fern sporlings,wheredevelopment isnotsupported extent towhich light-capturing leafareadeployed bystorage reservesinseeds. Thus,carbonacquisi- inthe immediate future ismorevaluabletotheplant tionisatapremium,anditfollowsthat theseedling than thesame areadeployedatadistanttime. The

phaseis oftencharacterizedas aperiodofrapidgrowth, factorsthatenterinto thetime-discountrateare sev-Butseedlingsarealsohighlyvulnerable:susceptible eral: (1) older leaves have reducedrevenuebecause todesiccation from minor soildryingevents, strong of accumulated damage anddebris,(2)older leaves

competitionfor lightwhere seedling densitiesarehigh, are morelikelytoexperienceshadingfrom surround-andherbivory (Lambersetal.,.1998). Thus,high ing vegetation,aswellasself shading, (3)there isa growthratesinseedlings leadtobotharapid acquisi- risk that the plant willnolonger be alivetobenefit, tion of carbon,andrapid passage throughoneofthe and (4)previouslysynthesized drymattercanitself mostvulnerable phasesof thelife cycle.

Acrossarangeof ages,plants have shownevi- interest)than thesimpleinterest from an individual

dence ofatradeoffbetweentraits thatfacilitaterapid leafoverthecourseofitslifespan(seealso Harper, growth and traitsthatpromotepersistence (Lambers 1989).

etal.,1998).RecentlyReich andcolleagues(Reichet

al., 1997;Ackerly&Reich,1999; Reichetal.,1999) particularlyrelevanttothe first fewleavesof seed-havedocumenteda fairly constrainedrelationship lings. Rapidproduction ofnewleafareawillincrease betweenspecificleafarea(SLA—the leafareaavail- thecompound interesteffect—thus overall relative able for lightcapturerelativetothe drymassofthe growthrates—muchmorethan delayeddeployment

leaf)and leaflongevityacross abroad range ofspe- ofthisnew area;this effect

would

be enhanced by cies andecosystems.The authorssuggestthat prop- higherratesofphotosynthesis. Secondly,the

first

erties of leavesacross awide rangeofecosystems seedlingleavesmightbe expectedtobe quickly shaded fallwithina“universaltradeoffsurface,” the dimen- by competing vegetation,or_{even by newly}deployed sions of whichresult frombiochemical andbiophysi- leavesonthesameplant.Finally,thelongertheplant

cal constraints imposed fromonedirection,andse- remainsinahighlyvulnerableseedlingstate,themore

lective constraintsfromthe other. Ononehand, likelyitwillnotsurvive.Thus,the leaves of seedlings

thicker, long-livedleavesfalloutside the tradeoffsur- should havecomparativelyhighervalues of the time-facebecausetheycanexperience internal self-shad-, discountratesrelativetolaterleavesonthesameplant ingtotheextentthattheyareunabletomaintain suf- asitages:

ficientlyhighrates ofphotosynthesis. Increased

structural investmentinthicker leaves andbiochemi- change in form, structure and ecophysiology of

,

cal protection also lowersproductionofphotosyn- leaves, i.e. features suchas shape and size thatare thates. On the other hand,thin, short-lived leaves traditionallycharacterizedasheteroblasty? Oneway withlowassimilationratesfalloutside the tradeoff toassessthevalueofaparticular leafataparticular

surfacebecause theyareataselectivedisadvantage position istoconsiderfactorsinfluencing the “rev-dueto costsof leafconstruction that exceedreturns enuestream”ofphotosynthatessuppliedby thatleaf

of photosynthates. Whilenostudies of similar scale tosubsequent growth of theplant.

havefocusedspecificallyonseedlings, it isexpected

that thesamesetsof constraints apply.

bereinvested,andgenerate moregrowth (compound

Interestingly, allof thetime-discounting factorsare

Whatdoes all of this havetodowith ontogenetic

Specific

_leaf

area—Overthe lastdecade,SLA has been showntobeamajordeterminant ofrelative

Westobyetal. (2000)suggestthatinsightsabout growthrateand has emergedas asignificant indica-thenatureof thetradeoff imposed by these con- torofmany aspectsof leaf function(Wright & straintscanbe gained whenan additional factot, Westoby, 2000). Atmultiple scales, rangingfrom the time-discountrate,is considered. Viewingplant variation within individualplantstoecosystem-level

growth as aprocess of investment wherereturns processes,higher SLAsareassociated with higher arereinvested,theauthors recognize three variables relative growthrates,higherrates ofmass-basedpho-that determine the benefit (revenue stream) ofan tosynthesis, highernitrogencontents,and shorter individual leaftothe plant: first,specificleaf area, leaflifespans (Reichetal.,1998;Reichetal.',1999). whichdetermines the potentialrateofrètumonin¬

vestment; second,leaf longevity or the expected areas(Turner, 1994), andithas been widely.observed duration oftherevenue stream;andthird,atime- that seedlingleaves tendtobe thinner than those discountrate. The time-discountratemeasuresthe subsequentlyproduced. Several studies have shown Thinnerleaves generally have higher specific leaf

that SLA ofindividualleaves decreasesprogressively

during wholeplantontogeny,generally inassocia¬ tion withincreasingtotalleafarea.Gunn(1999) found that the SLAofleaffour of barleywassignificantly lower than that ofthefirstthree leaves when these

PhotosynthesisRates in Com 170-1

160-I

Fi

140-I

f

130-8

120-110 -leaveswereharvestedatthesamephysiologicalage

(Fig. 1).SimilardecreasesinSLAwithincreasingleaf positions, i.e.increasingnodenumber,have been observed insoybean(Lugg &Sinclair,1981), wheat (Arausetal.,1986),and alfalfa (Ku & Hunt, 1973). Whenmeasuredatasinglepoint intime,rather than atthesamephysiologicalageof the leaf, decreases

inSLA(reportedasthe inverse of SLA,specificleaf Fig.2.Photosyntheticratesof newlymatureleaves of com

weight)withpositionoccurredinold field annuals, (Zea mays “Harrow 691”) withincreasingleafposition. butnotindesert annuals (Mooneyetal.,1981).

100

3 5 7 9 11 13 15

Node position

Plants were grownin growthcabinetsat10h photoperiods. Valuesare meansof4replicatesforeachposition. (Redrawn fromThiagarajah,etal.,1981.)

SpecificLeafArea (SLA) inBarley

0.5

1981). This increase inratesofphotosynthesisup

through leafposition six corresponds roughlytothe

juvenile phase ofplant development incorn (Bongard-Pierceetal.,1996). Mooneye/ al. (1981) also found thatphotosyntheticcapacity per unit leaf areaincreasedwith increasing node number in old-fieldannuals,andtoalesserextentindesert annuals. Onthe otherhand,maximumphotosyntheticrates were similaracrossnodes 6-14 intwocultivarsof

I

f

0.4-i

*

T

!>

0.3-i

0.2-V

soybean, but early seedling leaveswere notmeasured (Lugg& Sinclair, 1981).

The studies abovesuggestthat as seedlingsde¬

velop,SLAdecreaseswith increasing nodalposition number,butatthe sametime,photosynthetic rates initially increase (perunit area) untilthey leveloffat higherleafpositions,a patternnotpredicted bythe

broadscalecomparisonsofmatureleaves described

earlier.

Thus initialseedlingleaves may besothinthat

<

to

0.1-0.0

1

2

3

4

Nodeposition

Fig. 1.Changeinspecific leafareasof barley(Hordeum

vulgare L.cv.Klaxon)with,increasingleafpositionnumbered theyare

unable

toattain the highphotosyntheticrates

fromthe firstleaf. Plants were grownhydroponically.Leaves _{0flater, slightlythicker seedlingleaves,leadingto} were harvestedat thesamephysiological age, 2 d after

expansionofsuccessive leaves. Values are mean±standard

of 4replicatesforeachposition. (RedrawnfromGunn °fmatureplants. Very high time-discountratesfor

initialseedlingleaves may contributetothispattern. leaves that fall outside the “universaltradeoffsurface” errors

et'al.,1999.)

Exportpatterns—Incalculatingtheeffect of

time-Rates

of

photosynthesis

—

Inseveral species,

photosynthetic ratesper unitareainthe first-pro- discounting,therevenue streamistakenasthe spe-duced leavesarelowerthaninsubsequentleaves,so cific leafareamultipliedbytherateof export ofpho-thattherateincreaseswith each successive leaf. In tosynthatesper.unit area tothe rest oftheplant wheat,photosyntheticratesincreased progressively (Westobyetal.,2000). Becauseexportisawhole within the three leaves priortothe flagleaf(Dunstone plantproperty,rather than of thesourceleaf alone, etal.,1973). In com,photosyntheticrates(per unit dependentonthestrength of bothsourcesand sinks area),werelowest inleafthree,but increasedsteadily (Gunnetal.

,

1999),wemightalso expectontogenetic toleaf 5-6, after whichtheyremained fairlyconstant shiftsinpatternsofexport asplants

age.

For ex-forthenextseveral leaves (Fig. 2) (Thiagarajahetal.

,

ample,Bertinetal. (1999) found that fruit removal in

tomatoplantswithone“truss” andoneleafhada the earlieststageofdevelopment(4thleaf)showed

much larger effectoncarbohydratedynamicsofits stomatal closureathighertotalwaterpotentials than adjacentleafthan did fruit removal fromplantswith later leaves (Teareetal.,1982). Inafieldstudyofthe manysourcesand sinks.

.

Presumably,plants with arid landshrub,Chrysothamnusnauseosus(rubber fewersourcesandsinks,i.e.seedlings,wouldexperi- rabbitbrush), Donovan and Ehleringer (1992)found

ence moredramatic shifts incarbohydratebalance if that “juvenile” shrubs (older thanoneyear,but pre-the number of eipre-ther sources orsinks werealtered reproductive) had significantly lower instantaneous wateruseefficienciesas

well

ashighercarbon iso¬ tope discrimination (ameasureofiptegratedwater useefficiency when certainassumptionsaremet) than

larger, reproductive“adults.”While the wateruse efficiencies of seedlingwerenotmeasured directly, theirhigherdiscrimination valuessuggestthatthey hadevenlowerwateruseefficiencies. Interestingly, thephotosyntheticnitrogenuse efficiency of juve¬ niles washigher than for adults.Donovan and

Ehleringer(1992)suggestthatby havinglowerwater useefficiency, very youngplantspotentially gain “morecarbon,morebiomass anddeeperroots”so

thatjuvenileplantsmightbemorelikelytosurvive

subsequent summerdrought.

Leaf

size Acommonlyobserved feature ofseed¬

lingleavesisthat the first few leavesare smaller. Several investigatorshave arguedorassumed that

smaller, simpler leaves are a“consequence” of the smaller shoot apical meristemsofseedlings (e.g. Sinnott, 1921). Suchcorrelationsbetween meristem size andmetamer(generally leaf) complexityarewidely

appreciated(e.g.Allsopp, 1967; Lambersetal.,1998), but whether this correlationimplies causalityhasnot beendeterminedexperimentally—normay it bede¬ monstrable. It ispossiblethatatrait suchassmaller, simplerseedlingleaves does result fromadevelop¬ mentalconstraint,as suggested bythe correlations

above,butatthesametimehaspositive functional

consequences.

Onefunctional consequence ofproducingsmaller leaves relatestothe high time-discountingeffect of thefirst few seedlingleaves. Asmoreseedlingleaves areadded,thevalue of the first few leavesdecreases.

Shedding of small leaves thatarelikelytobe

self-shaded,shadedby others,ordamaged byherbivory

presentsproportionallyless cost to the plant than shedding largerleaves.

The sizeofseedlingleaves also influences the timing ofinitial photosynthateexport! Inseedlings, few sourceleavescoupled withpotentiallystrong sinks established byrapidgrowth predict that the first seedling leaveswillbeginexportingas soon as functionallypossible.Incucumber, the first leafafter thecotyledonsbecameanet exporterofcarbonat than wouldplantswithnumerous sourcesandsinks

that dilute the effect ofminor shifts in eitherstrength

ornumber.

Arelatedissue is thatintegrationpatterns arepre¬ dictedtochangewithplant development,such that one expectsseedlingstobemorefully integratedwith respect tocarbonmovementthan olderplants(Watson &Casper, 1984). While there have beenrelatively few

studiesoncarbonmovementinwholeseedlingscom¬

paredtoolder plants (Escobar-Gutiérrezetal.,1998), there issomeevidence that carbohydratetransportis well integratedinyoungplants(e.g. Preston, 1998).

Another consequence of decreas¬

ingSLAwithincreasingleafposition in seedlings is that later leaves withlower SLAgenerally havemore “xeromorphic” features. Inspring wheat,the last five leaves preceding the flag leaf,inorder ofincreasing

position, showed decreases inthickness, in

meso-phyllcell volume per unit leafarea

(Vmcs/A),

in

meso-phyllcellareaper unit leafarea

_(Ames/A),

andinre¬ sidual conductancewithincreasing position. Thus, cellsoflater leaveswereprogressivelymoreclosely

packedthanearlier leaves (Arausetal.,1986). Similaranatomical correlates have becomeknown asZalenski’s Law (Daoud & Brown,1956;Allsopp,

1967),the postulates of whichstatethatleavesbe¬ comeprogressivelymorexeromorphic with higher

positionsontheshoot,manifestedbysmaller

meso-phyll

cell

dimensions,thicker cuticles and epidermal cellwalls,greaterveinlength,andgreaternumber of

trichomes,all of which contribute tolower SLAs. While there is variation amongspecies intheextent to which individual characters change(Daoud & Brown, 1956),adecreasein SLAandacorrelatedin¬

creaseinwateruse

efficiency

from leaftoleaf (upto. apoint) seem to

be

general features of early plant

development.

Severalstudies have shownontogenetic changes inparametersdeterminingwaterrelationsandwater useefficiency, WUE—the ratio of carbon gain in

photosynthesis to waterloss duringtranspiration. Inspring wheat,interactionsamongtotalwaterpo¬

tential,osmotic potential, and stomatalresistance changedwithposition, such that leaves producedat

Wateruse

30%its final size. (Hoetal,1984). Ingeneral,export tostructuralsupportthanlarger leaves (e.g. Chazdon, ofphotosynthates fromolderleavesisreportedto 1986).Evenwithinbipinnate seedling leaves

oi'Aca-beginat30-60% of fullexpansion (Turgeon, 1989). ciamelanoxylon, later-producedlarger leaves

in-Evenwhenweconsider that the first few leavesex- vestedapproximately 35%moredryweight in sup-pandmoreslowly than subsequently initiated leaves port tissue than didearlier,smallerbipinnate leaves (e.g.Williams,1975),smaller leaves shouldbeginex- (Fig. 3) (Brodribb &Hill,1993).

porting carbonearlierin absolutetimethanlarger leavessimplybecausetheyachieve the criticalex¬ port sizesooner(seedatainLarson &Gordon, 1969). Consequently, carbon is available for subsequent

growth, and hence compounding, earlierversuslater

inaseedling’s life.

Themostcommonlyreported advantage for small leaves appearstobe that smallleavesmaintainleaf

temperatures closer toambient thanlargerleaves,

because leaf boundary layer thickness scaleswith leafsize(Lambersetal.,1998). For seedlingsinsome

environments,this effect may be significant,asair temperaturesarehighestatgroundlevel. Seedlings mustmaximize carbongaininthe face ofpossible droughtstressimposedbylowerrootsurfaceareas

andshorterrootssystemsdeployedinthemostrap¬

idly dryingsoillayers.Maintainingleaftemperatures

nearambient via smallersizesreduces theamountof 1993.)

waterlosttotranspiration, becausethe vapor pres¬ suredifferencebetweenwaterinthe leaf and thatin

Support Costs of Bipinnate Leaves inAcacia melanoxylon 40

Ê

_A A

AA

3 30

//A

g

20

£

10

0 20 40 60 80 100

Bipinnate leafarea(cm2)

Fig. 3.Increasingpercentageof leafdry weightdevotedto

support tissueasleafSizeincreases inbipinnate leavesof

Acaciamelanoxylon. (RedrawnfromBrodribb andHill,

Leaf

shape—Acommonobservation of the the atmosphere is reduced. Thuswaterloss is

mini-

firstseedlingleaves is that these leavesareoften of mizedevenifwateruseefficiencyis lower thanin “less complex” form. In some

species,

e.g.

Arabidopsis,thefirstfewleavesarevery similar in Finally,several studies have shownthat small shapetothecotyledons(Fig. 4) (Kerstetter&Poethig, leaves haveproportionatelyless leafmassdevoted 1998;Tsukayaetal.

,

2000).Changes inleaf shapeare later leaves.

Arabidopsis

thaliana

9P

UÍ

foliage, rosette leaves

cotyledons cauline

leaves

order

of

leaf

production

Fig.4.Theontogeneticsequenceof leafshapes produced in Arabidopsisthaliana (L.)Heynh.(Columbiawildtype). Plants were grownunder continuous whitelight. (Redrawn fromTsukayaetal.,2000.)

Quiina acutangula

seedling _transitional

adult juvenile shoot

n Fig.5.Ontogeneticvariation inleafshapeinQuiinaacutangula Ducke(Quiinaceae). (Drawn fromphotographsin

Foster, 1950.)

themostobvious expression ofheteroblasty,and of greatercarbongainper leaf.

thechanges inleafshape describedin theliterature, The genus Acacia (Leguminosae) comprises thevastmajority occurinseedlingsor duringthe woodytreesand shrubs. Members of thesubgenus Heterophyllumarewellknown foradramaticchange

In manyplants,seedlingleavesareunlobedor in leafshape during seedlingdevelopment. In

gen-weaklylobed when subsequent leaves arehighly. eral,the firstseedlingleaves of this subgenusare

lobed,“simple” whensubsequentleavesare“com- pinnatelyorbipinnately“compound,” with increas-pound,”orif“compound,”bearing fewer leaflets than ingnumbers ofpinnaeathigher leafpositions.Later later leaves. However, therearealso exceptionsto leaves of species in thisgroup are“phyllodinous.” this trend:

_Quiina

acutangula (Fig.5)(Foster, 1950); While,the nodalpositionof the transition inleaf shape Hakeatrifurcqta(Groometal.

,

1994);possiblymul- varies among species,it commonlyoccursinthe seed-berry (Gray & Gray, 1987);many aquatics, where early lingstage. Kaplan(1980) has shown thatphyllodinous

leavesarehighly dissected and later leaves less dis- leavesare not morphologically phyllodes, derived

sectedtoentire (Sculthorpe, 1967). Presumably, fromanelaboration of thepetioleandsuppressionof changesinleafshapeoccurinconjunctionwiththe the leaf bladeasisfrequentlyassumed,but instead anatomical and physiological changes described arisedevelopmentallyfromasuppression of the ini-above,but few studies have documented simulta- tiation oflateral leaflets andthe

simultaneous

expres-neous changes inshape, internal structure,and sionofanadaxialmeristem inthe leaf blade which physiologicalcharacter suites for successive leaves produces.ablade flattenedinthe medianplane.Con¬

sequently,theextentofthepetiole becomes reduced firstyearof growth.

inseedlings.

InDesmodium paniculatum, the firstseedling inthese leaves. leavesaresimpleandlaterleavesaretrifoliate. The

positionatwhichthetransition occurs, generally node inshape of the leafhas been examinedindependently

fourorfive,is influenced both byseedsize and by in two species, A. koa var. latifolia, and A. lightenvironment(Wulff, 1985). The transitionoc- melanoxylon.Interestingly,both species retain the curred earlierinseedlings arising fromlargerseeds in pinnate leaf form foralongerperiod during early de-ahigh lightenvironment,and resulted ina"30%in- velopmentthanother species (Kaplan,pers.comm.), creaseintheareaofindividual leaves. Bothleaftypes although the age at which the transition to the hadsimilarratesofphotosynthesisperunitarea, SLA phyllodinous formbegins in A.melanoxylonunder andconductance,sothe trifoliate leaves exhibited greenhouseconditions is correlated withmean an-The functional significance ofthis dramatic change

nual rainfallatthe site of origin of theseeds

bipinnate formpersistsfor longer inplants fromre¬ gionsofhigher rainfall(Farrell&Ashton,1978). Com¬ paredtophyllodinous leaves,bipinnateseedling

leaves ofA. melanoxylonwereshowntohavehigher ratesofphotosynthesisper unitmass,lowerwater useefficiency withincreasing leaf-air vapor pressure deficit, and lowersurvivalunderwaterstresscondi¬ tions. Thoseontogenetic changes in physiology

are expressed evenwithin thebipinnate leaves,

wherein the firstbipinnateleaves had higherrates of

photosynthesisthan laterbipinnate leaves,andmuch higherrates

than

phyllodinousleaves (Brodribb &

Hill,1993). In A. koavar.latifolia,anendemic of

Hawaii,bipinnateleaveswerethinner with higher Fig. 6.Photosyntheticratesasafunctionofphotosynthetic SLAsandmorerapidmoisture releaseatagivenwa- photonfluxdensityforbipinnateandphyllodinousleaves in ter Fpotential

measured'

under field conditions _(Redrawn

*"!

_{from Hansen,}“ed

_“

**

_1996.)Valuesare

_“

°f 3

rePlicates-(Hansen, 1986). When both leaftypes werepresent

on oneindividual(saplingsapproximately0.5-1.0m generallyparallel and extend those observedin seed-high)atthesame time,both instantaneous and inte- lings. InSolanumaviculare,awoodyspecieswith gratedwateruseefficiencies ofphyllodinousleaves dramatic leaf shape changesfromseedlingthrough

were greaterthanbipinnateleavesinpaired compari- reproductivematurity. (Fig. 7), leaf shape and leaf sons, partly due to lower conductance in thickness both changeas afunctionofplant ontog-phyllodinousleaves (Hansen & Steig, 1993). No dif- eny (James &Mantell,1994). Post-seedling “juve-ferencesinphotosyntheticratesper unitareabetween nile”leaves (e.g. nodal positions 7-9)were consider-leaftypes wereobservedinthis study(see also ablythinner and oflowermass thanlater“adult”

Walters&Bartholomew,1984).Usingfieldmeasures leaves.

ofphysiologicalparametersandestimates ofbound¬

ary layerconductance basedonleafmodels,Hansen response to tree age. Leavesproducedon

three-(1996)tested thehypothesisthat thebipinnateleaves year-oldindividualsof Sitka sprucewere narrower, of A. koa exhibited suites of characters favoring rounder,,and withlessprojectedsurface area than

-growth,while thephyllodinous leaves exhibitedchar- leavesonoldertrees(Steeleetal.,1989). Specific actersuites favoringpersistence. Differencesin leaf leafareaofleavesonthree-year-oldplantswasthree shape and orientation (horizontal inbipinnate leaves, tofour timeshigherthanonolder plants. Similar and verticalin phyllodinousleaves) apparentlyac- resultswerereportedfor Loblollypineby Greenwood counted for observed differences inphysiology. (1984),whoproposed that characteristics ofthese Higherconductance in the bipinnate leaveswasat- seedlingsmightbeadaptationstogrowth inthe un-tributedto differences in boundary layer conduc- derstory.

tance, adirect effect ofdifferencesinleafshape,rather

thantostomatálcontrol. This higher conductance chanicalsupport costsincrease(asstemmass)more resultedinlowerwateruseefficiencyinbipinnate rapidlywithplant size thancrown area(asleafmass),

leaves,but also in higherratesofmass-basedphoto- King(1999)has shown that leafmass perunit area,or

synthesisathigh lightintensities. Inphyllodinous LMA, theinverseofspecificleaf area, ispredictedto leaves, photosyntheticratesleveled offathigh light increase withincreasing plant

size.

Overa rangeof

intensities, suggestingdiffusional limitationson

_C02

modelformulations,youngplantsinopen environ-duetodecreasedboundáry layer conductance(Fig. 6). mentshave maximum growthratesatlower LMAs, assumingthat “the chemical and enzymatic”content of leaf tissueperunitmassdortotvary withplant

age. (Thisassumption resultsinacurvilinear rela-Inolderplants,changes in leafstructureand tionship betweenLMAahdlightuseefficiency).Leaf

physiologybetween “juvenile”and“adult”plants massesperareainyoungwoodyplantsunder similar the

NetAssimilationRates in Acacia koa 1.00

•

—bipinnate leaves

o

—

phyllodinous lea1res

C

0.75 7

•

•

”o>

_Vo

d _~

o

.0-

_

0.50

°v;

t 0.25

8 0.00

0 500 1000 1500 2000

PPFD(pmolem'2s"')

Leaves of gymnosperms also showchangesin

Inanelegantmodel basedonthefactthat

Solanum

aviculare

tf

1 2 ₃

8 (first flowering node)

10

14 ₁₅ 16 17

11

12 13

Fig. 7. Theontogeneticsequenceof leafshapesin Solanumaviculare Forst.numbered progressively fromthe firstleaves

following the cotyledons (not shown). Plants weregrown in controlledenvironment roomsunder8 hphotoperiods. (Redrawn from JamesandMantell,1994.)

Inthe classic exampleofaplantexhibitingamarked

lightandgrowthconditionswereapproximatelyhalf

ashighasthoseinmature treesinanumber of spe- phasechange, Hederáhelix,orEnglishIvy,

photo-cies (see referencesinKing(1999),and thus consis- syntheticrateshave beencomparedbetween juve¬ nile phaseandadultphaseleaves. InHederá,

het-Photosynthesisrates

have

also been compared eroblasticchangesinleaforientation,leafshape, and betweendifferentphases of plant growthinlonger- growthhabit have been correlated withanabilityof livedperennials. Inastudy ofsun versus shade thejuvenile phasecuttingsto rootand adult phase

adaptabilityinthe mangrove speciesRhizophora cuttings to flower. BecauseHederá

is

generally

mangle L.,Farnsworth andEllison(1996) demon- propagated fromcuttings,little information is avail-strateddifferences amongseedlings, saplings, and ableforseedlings. However, fully developed juve-adulttreesinleafmorphology,structureand photo- nile phase leaves of Hederá had higherSLAsthan

synthetic properties. Seedlingsshowed higher val- adultphaseleaves but lowerratesofnet photosyn-uesof SLA than saplingsortreesinbothsunand thesisperunitareaunder highlight (Bauer & Bauer, shade. Seedlings also showed the highestrates of 1980),both of whicharetraits characteristic of shade

photosynthesisper

unit

areaundersun,and the low- leaves. Thesedifferenceswereshowntobe corre-est levelsunder shade, suggesting thatleaves on latedwithlower stomatalconductance,lower

stomatal

seedlingshaveapronounced capacityto adjustto frequency, and fewer chloroplasts percell. In addi-lightlevel,acapacitythat leavesonolder plants.ap- tion, juvenileleaveswereconsiderablythinner, with parentlydidnotretain (Famsworth &Ellison, 1996).' tworather than three layers ofpalisade parenchyma.

Thatseedling leaves may havegreatercapacitiesto

respondtochangesingrowth conditions,i.e.-greater havingahighproportionofspeciesshowingmarked

.

plasticity,than leavesonolder plantswasalso sug- ontogeneticheteroblasty in leaf shape, planthabit,

gestedinastudy of sunflower byRawsonand Turner orboth(e.g. Godley,l985;Heenan,1997).Inmanyof

(1982),who found that leaves produced early in the theseplants,transitions in leaforhabitformoccur plant’slifehada greaterabilitytoresumeexpansion relativelylate in plantdevelopment. These changes afterwater wastemporarilywithheld than didleaves have been attributedtoavariety of factors, including changes inthe lightenvironment of youngversus tentwith thepredictionsofthemodel.

The floraofNewZealandarewidelyknown for

olderplants,andherbivory(Moabrowsing,seeDay, 1998, and references therein). Godley (1985),using

data fromCockayne (1928, originalnotseen),reports that of 200or soheteroblasticspeciesinthe New Zealand flora, 165 haveaprolonged“juvenile” growth period, andofthese,106speciesare more“mesomor¬

phic,”17are more“xerophytic,” and39 show “no appreciable difference,”inthejuvenileformcompared withthe older form. Day (1998)constructsanalter¬ nate setofargumentsfavoring the evolution of het-eroblasty inNew Zealandtreespeciesinresponseto differing lightlevels,and,moreimportantly, degrees oflight heterogeneity between the understory and canopyenvironments.

Few empirical studies on species fromNew Zealand have investigatedthe functional conse¬ quences of producing different leaf forms. Pseudopanax

_crassifolius

produces four categories ofleaftypesduringthecourseofits life (Fig. 8) (Gould, 1993). Seedling leavesareproducedonunbranched stems0-1meterhighand “juvenile”leaveson un¬ branchedstems1-4metershigh. Afterthetreebe¬ gins branching, it produces transitionalleaves,and ultimately theshorter “adult” leaves. Seedling leaves showadramatic increasein leafthicknesswithposi¬ tion, andacorrespondingdecrease in specific leaf area. The long,narrow“juvenile” leaves have the lowest specific leafareas,andwerethemostresis¬ tant tobreaking,inpartduetoxylary and extraxylary fibersinthe midrib. In theshorter,wider transitional leaves and adultleaves,SLA beginstoincrease again, eventhough those leavesaresimilarinthicknessto

juvenileandtransition leaves. Photosyntheticrates andwateruseefficiencieswerenotmeasured in this

Pseudopanax crassifolius cotyledon

progressively higher seedling

leaves

juvenile leaf

transitional leaf

adultleaf

Fig. 8.Representatives oftheontogenetic sequenceof leaf shapesin Pseudopanax_crassifolius(A. Cunn) C.Koch. (Araliaceae),aspecies endemictoNewZealand. (Redrawn fromGould,1993.)

Aswehave seen, both of these characters change withplantdevelopment, and thus it isnotsurprising thatdevelopmentalstageshavebeen showntohave strongeffectsonresistancetoherbivory,aswellas oninducedresistance (reviewedinKarban&

Baldwin,

1997). Incotton, seedling, “juvenile”and “adult” stages aredefined by differences in leaf shapes and nodalposition (Stephens, 1944). Ina recentstudy of miteperformanceoncottonleaves,Karban and

Thaler

study, butasubsequent studyshowedthat the juve¬

nile leavesaresteeplyinclined,aleaforientation that

simultaneouslydecreases direct light absorptionin

the open environmentinwhich these plantsgrow,

but increases the efficiency ofinterceptionof diffuse (1999)foundstrongeffects of leaftype,andhence developmentalstage, onmite population growth. Population size increasedmuchmorerapidlyon coty¬ ledons thanon“juvenile”or“adult”leaves,but there was no

difference

between population sizesonthe Onetrait oftenreported for seedlings andyoung lattertwoleaftypes. Several experiments revealed plants is thattheyare morevulnerabletoherbivory thatmites respondeddirectlytothehigher photo-because they invest in growth rather than structural syntheticrates ofthecotyledons.

Strong effects ofplant developmental stageon light (Clearwater & Gould, 1995).

Ontogenetic

_effects

onresistancetoherbivory

defenses. Irrespective of the developmentalstage,

leafanatomyand shape have both been showntobe insect resistance werealso

observed

in narrowleaf significantdeterminantsofinsect

feeding*

preferences cottonwood,Populus angustifolia, but thestagethat andoppositionbehavior (e.g.Brown & Lawton, 1991; was mostresistanttoherbivory dependedon the Matsuki & MacLean, 1994; Degen & Stãdler, 1997). herbivore (Kearsley &Whitham,1989).The juvenile

stagehosted much higher numbers ofaleaf feeding producedonseedlingshavehigher specificleaf ar-beetle than did the adultstage,but the trendwas easbut lowerratesof photosynthesisperunit area dramaticallyreversed foragall-formingaphid. Ina that increaseup to apoint;seedlingleaves also have subsequent study, Kearsley and Whitham (1997) lowerwateruseefficiencieswhichresultsinrelatively showed that fitness oftheaphidwaspositivelyre- greatercarbon gainforagiven leafarea. Seedling latedtoincreasingly “adult” phenotypes of thecot- leavesmaybe subjecttovery highratesof time-dis-tonwood,and that theaphids preferentiallycolonized counting. Giventhis,small leavesareless costlyto branchesbearing adult leaves; thepositions of constructandtheycanbegin exporting carbon rela-branchesbearing the “adult” phenotype alsowere tively early in their development. The dramatic foundtobestable fromyear to year. These authors changes in leafshape duringontogeny thatwould pointoutthatwithin-plant variation in host quality berecognizedasheteroblastyappeartofurther en-servestospatiallyconcentratetheherbivores, mak- hance the functional differences between the first

ingthemmoresusceptibletonegative effects ofcom- produced leaves and later leavesonthesameplant. petition, predation andparasitism. In thecaseof Acacia, forexample, changesin func-Becauseleafshapeisa commonexpressionofon- tion with leafshape are concordant with similar togenetic,heteroblastic change withinplants,it is criti- changes inmanyseedlingsthat donotexhibit such caltokeep in mind—instudies of resistancetoher- dramatic changes in shape. Whether changes in bivory—thatthat the effects of leaf shapemaybe shapearecorrelated with ultimate gains in plant fit-confounded withthe effects of developmentalstage, nessis just beginningtobe investigated. The stud-Forexample,Rivcro-Lynch etal. (1996) show that adult iesaretoo few to reveal generaltrends,buttodate fleabeetles (Phyllotreta spp.)prefer leaves ofCapsella Winn (,1999) suggests that the functional significance bursa-pastoris with deeply lobed margins relativeto of leafshape change may becasespecific. In any leaves withless lobedmargins. However, leaf shape in case,ontogenetic changes in leaf shapearejustone C.bursa-pastoris is heteroblastic (Allsopp, 1967),so expressionofthe continuum ofchange in

ecophysi-it is

difficult

to

know

whether the fleabeetles,are re- ological propertiesofleavesasplants age. spondingtoshapeperse,or tothe physiologicalcor¬

relates of ontogeneticstage. Inadditiontoeffects of tobe further perpetuated in later plant development leafshape, several factors could influence the effects asplantsmaturethrough “juvenile” developmentto of developmentalstage onresistancetoherbivory, in- reproductive maturing, i.e. SLA decreases andwater eludingdifferencesinphotosynthetic rates,nitrogen use efficiency increases. Photosyntheticratesper andwatercontent,production of chemical defenses, unit area are less easytointerpret and

show

both

typesofchemical defenses, and the correlate of these increases and decreasesinlater leaves. Greaterun¬

traits,specific leafareaandplant

relative

growthrates derstanding ofthe function of ontogenetic changeat the leaflevelwillbe gained when traits above the leaf

level,notconsideredinthisreview,aresimultaneously evaluated, e.g. ontogenetic changes inplant archi¬ tecture,leaf angleand orientation, and plant relative

growthrates. Finally, possible ontogenetic differ-Recent, broadcomparativestudies of plant traits eneesintime-discountingratesand in leaf longevity remain poorly understood. Attheveryleast, onto-Trends establishedamongseedlingleavesappear

(Coley, 1988;King, 1999).

.

CONCLUSIONS

have revealed suites of covarying

features

thatcan

nowbeinvestigatedat multiplelevels,including genetic changes in ecophysiologicaltraitsarelikely within-plant variation. This reviewattemptstobring toexplainasignificantamountof variationamong togetheradisparate literatureonplantdevelopment individuals withinspeciesin response to environ-andecophysiologytoexamine how character suites mentandmustbe consideredas significant param-change with plant ontogeny. To some extent,this etersinmodels of plant responsestoherbivory. reviewsupports theobvious, that leaves ofseeding

aregenerallythinner,smaller and less complex than

leaves produced when the plant is older. However, it

ACKNOWLEDGMENTS

also extends these observations by consideringa

diversity of functionalconsequencesof ontogenetic Ithank 'Charles Henry forproducingthe figures differencesinleaf formand function. Ingeneral,leaves and for carefulreading of

the

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Recibido el 20 deAbrilde 2001, aceptado el 08 de Mayo de 2001.