|.I

1296 _15_

Allocation of current photosynthate and changesin tissue dry weight within northern red oakseedlings: individual leaf and flush carboncontribution during episodic growth

Richard E. Dickson, Patricia T. Tomlinson, and J.G. Isebrands

tO•

--5 ._ "_ .

"°_ to __ _ _ Abstract: Relatively little is known about the changing carbon allocation patterns in species with episodic growth ey-e0 .= cles such as northern red oak (Quercus rubra L.). To examine such changing allocation and growth patterns, northern

_o =_n" red oak plants were grown from seed in controlled environment chambers through four cycles of growth. 14CO2 was

._._ e- ._ ,_, supplied to leaves of the first, second, or third flushes at different Quercus morphological index growth sta._eswithin-- _ "_ o _, each flush, and the distribution of Z4Cwithin the plant was analyzed. Carbon allocation from source leaves of the firsttot'N

i..2 _ "_.-,-- and second flush was primarily upward during the subsequent cycle of shoot growth and downward during lag and bud.,o_ v _ _5 growth stages. All leaves within a flush did not respond the same. Upper leaves allocated most 14C-photosynthateup-"5 eo 00 _ 14C,'- o ,- . ward during leaf and shoot growth while lower leaves supplied more

xa "_ -_ to lower stem and roots. During the third and_>_ ® fourth flushes, differential allocation from leaves within a flush resulted in essentially equal upward and downward car-,.. no _ bon allocation. Growth and allometric relationships reflected these changes in carbon allocation.-O e-

o£_ .-_to _ s= "" R_sum6 : On connait relativement peu de choses sur la variation des patrons d'allocation du carbone chez les esp_cese- Q. _ "-'__ comme le chine rouge (Quercus rubra L.) qui ont des cycles de croissance @isodique. Des plants de cMne rouge ont

_- _ _ 6t_ cultiv_s _tpartir de la graine dans des chambres _ environnement contr61_pendant quatre cycles de croissance dansi-- '_ t_ u. le but d'&udier les changements dans l'allocation et les patrons de croissance. Les feuilles des premiere, deuxi_me etLid,_ _ o o troisieme pousses ont 6t6 exposres h lnco, h diffrrentes 6tapes de croissance sur la base de l'indice morphologique de

_- sc _ m= Quercus et la distribution de 14Cdans la plante a _t6 analysre. L'allocation du carbone en provenance des feuilles desco .2 ._a_ _ _ <a _ premiere et seconde pousses se faisait principalement vers le haut pendant le cycle subsequent de croissance ramrale et

I_ _ _., _ vers le bas durant les p_riodes de latence et de croissance des bourgeons. Toutes les feuilles d'une m_me pousse ne,_ ._ ,-'co rragissaient pas de la marne fa_on. Les feuilles du haut allouaient la plus _°-randepattie des produits marqurs de lato . _ "- photosynth_se vers le haut, pendant la croissance des feuilles et des rameaux, tandis que les feuilles du bas fournis-

t_ _ _ saient plus de _4C& la pattie infErieure de la tige et aux racines. Lors des troisi_me et quatri_me pousses, l'allocation_._.-o to '*"__ du carbone en provenance des feuilles d'une m_me pousse 6tait r@artie 6galement vers le haut et vers le bas. La crois-_C,

sance et les relations allomrtriques refldtaient ces variations darts l'allocation du carbone.

[Traduit par la Rrdaction]

Introduction Plant growth strategies and the resultant carbon allocationpatterns are inherent but are modified by environmental

Northern red oak (Quercus rubra L.) is one of the most change (Chapin 1991). Crop scientists have long recognizedvaluable and widespread tree species in eastern North Amer- that carbon allocation to various plant parts is a major deter-ica. It is highly valued for timber and veneer, wildlife food minant of growth and yield (Gifford and Evans 1981). Forestand habitat, and forest aesthetics (Johnson 1994). Northern scientists also recognize this fact, and much information isred oak also is an important component of the biodiverse available for trees used in intensive culture such as Populuseastern forest ecosystems of North America and widely used (Isebrands 1982; Dickson 1986) and conifers (Gower et al. 'in forest and urban plantings in western Europe. particularly 1995; Luxmoore et al. 1995). However, surprisingly little bi-France. In spite of its importance, relatively little is known ological information is available for most hardwood treeabout red oak growth strategies and carbon allocation pat- species. If more basic biological information were availableterns, about carbon assimilation and allocation, shoot and root

growth patterns, basic nutritional requirements, and flower-ing processes, scientists and forest managers could develop

Received June 25, 1999. Accepted March 6, 2000. better natural and artificial regeneration systems.

R.E. Diekson _ and J.G. lsebrands. USDA Forest Service, Shoot-growth patterns of forest tree seedlings can be clas-Forestry Sciences Laboratory, 5985 Highway K, Rhinelander, sifted as determinate, semideterminate, or indeterminateWI 54501, U.S.A. (Dickson 1994). Northern red oak is a good example of aP.T. Tomlinson. Department of Biology, College of species with semideterminate or episodic growth whereCharleston, 66 George Street, Charleston, SC 29424, U.S.A. shoot growth occurs as distinct flushes (Hanson et al. 1986;_Corresponding author, e-mail: rdickson/nc rh@fs.fed.us Dickson 1994). During a flush, stem and leaves of the new

Can. J. For. Res. 30:1296--1307 t2000"_ © 2000 NRC Canada

Dickson et at.: I 1297

Fig. 1. Schematic diagram of the Quercus morphological index (QMI) showing the different growth stages, the source leaves treated ateach growth stage, and the within-flush leaf numbering system.

QMI Staqes Definition

1 Lag _k. Leavesfullyexpanded ==_ _ 3- 12

2 SL ZF Linearstemgrowth2LL =='-m IHm _ "_ 3-9

2 Lag _ Linearteafgrowth m.t,, D m _3 Bud IlK TreatedLeaf _" 4= m

3 SL _ Non-treatedLeaf "== m==='-u In-3 LL ==v

3Lag 141 '=='= _ 3-1

_ ,---,_ _ _ 2-8

.i::t5, _ mm-D-_,.._-,l,_ ..2 _ 2.1, :!: "1- mm" "

1 Lag 2 Bud 2 SL 2 LL 2 Lag 3 Bud 3 SL 3 LL 3 Lag

Quercus Morphlogical Index (QMI)

flush expand concurrently, creating a strong sink. When determine how the allocation of photosynthate from differ-leaves of the new flush are fully expanded, they no longer ent leaves in different flushes changes with plant age andimport photosynthate as sinks but export photosynthate as plant size.sources. This cycling of sink demand and source regions in Information obtained from studies of carbon allocation in

oak seedlings is associated with changes in photosynthetic red oak is highly significant, because it has broad applica-rates and carbon-allocation patterns (Hanson et al. 1988a, tion, not only for other oak species, but also for both temper-1988b; Dickson 1991) and in carbon metabolic patterns of ate and tropical species with flushing growth habit.leaves, stems, and roots (Dickson et al. 2000) If active leafgrowth is not present in red oak seedlings, stem and rootgrowth and carbon storage pools may not provide enough Materials and methodssink strength to maintain rapid carbon fixation rates. Such

Plant material

sink-limited plants might confound response to imposed en- Seedlings were grown from acorns collected from a single par-vironmental stresses, ent tree in the Rhinelander area and stored according to Teclaw and

Increasing vegetative growth rates or increasing sink de- Isebrands (t987). Stratified and pregerminated seed was sown in 6-mand increases carbon-exchange rates (CER) of preexisting L (15 cm diameter by 35 cm high) pots filled with a I:1 (v/v) mix-or new leaves of many plant species (see Hanson et al. ture of sphagnum peat and sand, and maintained in controlled envi-(1988a) and reviews by Dickson (1991) and Dickson and ronmental growth chambers (27°C, 16 h light : 21°C, 8 h dark)

Isebrands (1991)). Increases in sink demand may result from with an average light intensity of 300--400 Ixmol.m-2.s -lnatural growth cycles (Sleigh et al. 1984), defoliation or photosynthetically active radiation (PAR) (95% fluorescent, 5% in-pruning (Tschaplinski and Blake 1989), or any factor that in- candescent lighting). Plants were watered two or three timescreases sink to source ratios (Geiger 1987). With favorable weekly with complete nutrient solution and flushed with tap wateronce every 2 weeks. The nutrient solution was a modified Johnsonenvironmental conditions, red oak leaves of the first or sec- solution (Johnson et al. 1957) containing urea and additional KC1ond flush continue to mature during the next flush and CER to provide a balanced nitrogen source (8 mM NO 3, 8 mM NH4)continues to increase well after full expansion (Hanson et al. and a N:P:K ratio of 16:3:9 more suitable for oak growth. These1988a). In addition, CER of first- and second-flush leaves cultural methods were adequate to maintain rapid growth throughinitially decreased, then increased during the next flush of at least four flushes. Physiological age of the seedlings used in the

shoot growth, showing a strong response to changing sink experiments was defined by the Quercus morphological indexdemand (Hanson et al. 1988a). These studies (Hanson et al. (QMI) (Hanson et al. 1986; Isebrands et al. 1994), which divides

1988a, 1988b) showed the importance of plant growth stage each flush of shoot growth into four developmental stages: budand total leaf area for carbon fixation of the plant but pro- swell (Bud), linear stem growth (SL), linear leaf growth (LL), andvided no information on the relative contribution of leaf co- apparent rest (Lag) (Fig. 1).

horts within each of the flushes to growth of various plant Plant treatment with 14CO2organs. Such information requires laco2-1abeling studies toPlant leaves were labeled with 14CO2 in a treatment chamber

determine the ultimate sink of carbon from individual leaves, containing an overhead Sunbrella high-intensity light fixture (Envi-Therefore, we conducted a study to determine basic carbon ronmentat Growth Chambers, Chagrin Falls, Ohio) with high-allocation patterns within northern red oak seedlings during pressure sodium and metal-halide lamps (400 W each), a closed-episodic growth, to determine where photosynthate from loop _4CO2 generating and circulating system, and a Plexiglas,particular source leaves was utilized within the plant, and to water-cooled exposure cuvette (Isebrands and Dickson 1991).

© 2000 NRC Canada

1298 Can, J. For. Res. Vol. 30, 2000

Light intensities at the level of the labeled leaf ranged from 300 to leaves and a standard photosynthetic rate (6.0 ktmol CO2-m-Ls-J)800 ).tmol.m-2.s -I. Plants were taken from the growth chambers 4- based on previously determined light saturated photosynthetic rates6 h after the beginning of the light period and preconditioned in for growth-chamber grown red oak (Hanson et al. 1988a, 1988b).the treatment chamber for at least 1 h before exposure to 14COz. An average rate over a broad range of plant ages, source leaf posi-

For each 14CO2 treatment, a single leaf was enclosed in the tious, and QMI growth stages was chosen to avoid further con-cuvette and exposed to 0.9 MBq _4CO2 for 30 rain. After the founding allocation-related changes and for simplicity. The30 min exposure, two punches (5.5 mm diameter) were taken from 6.0/amol CO2.m-Z-s-I was adjusted for a 16-h day, 34.6gmol.cm -2,the treated leaf to estimate 14C fixation; plants were then removed then scaled by the average size and number of leaves in a cohort ofto a different growth room for a 48-h transport period. The 48-h leaves in a flush. Average leaf size for each cohort was estimatedtransport period was necessary to allow stabilization of allocation by the average area of all J4CO2-treated leaves in that cohort. Totalpatterns and chemical pools with rapid turnover rates and to mini- millimoles CO, fixed per leaf cohort per 16-h day was furthermize plant growth after treatment (Dickson et al. 1990). After the scaled based on the percentage of total 14C exported from the leaf48-h transport period, plants were separated into treated (source) and the percentage of J4C translocated up or down from the indi-leaf, other leaves and stems (by flush), taproot, and lateral roots, vidual leaf.Plant tissues were oven-dried (70°C), weighed, ground to 40 mesh,

and subsampled for t4C. The leaf punches were dried and weighed, Statistical analysesand the 14C content was determined on the intact punches after Three individual plants were treated for each leaf position atsolubilization with BTS-450 and suspension in Ready-Organic each QMI growth stage. Means and standard error of the meansscintillation cocktail (both Beckman Instruments Inc., Fullerton, were calculated for the percentage of 14C translocated, leaf area,Calif.) to estimate initial photosynthetic 14Cfixation (Dickson et al. dry mass, mass ratios, and days from epicotyl emergence to each1990). Content of 14C in the harvested tissues was determined by QMI growth stage. Standard errors for relative growth rates wereliquid scintillation spectrometry of tissue subsamples (5-20 rag), the mathematical sum of the errors associated with mass and days.hydrated and suspended in Ready-Gel scintillation cocktail(Beckman Instruments Inc., Fullerton, Calif.).

Results

Allocation of 14C within the plantTo determine JnC allocation within the plants, three series of Carbon export from source leaves during seedling

plants were treated. In the first series, a subapical first-flush (up- developmentper) leaf (leaves 1-3 or 1-4 on this typically four- or five-leaf flush) Total carbon fixed and exported from source leaves dif-

was treated at each QMI growth stage from 1 Lag to 4 Bud feted during seedling development. Fully expanded but(Fig. 1). Additional suprabasal (lower) leaves (I-2) were also physiologically young leaves at 1 Lag retained most of the

treated at selected QMI growth stages. In the second series, a me- 14C fixed in the source leaf (Fig. 2A). Only abotit 20--25% ofdian second-flush leaf (2-4) was treated at each QMI growth stage the 14C was exported from these source leaves at 1 Lag. Ex-from 2 Lag to 4 La_. Additional upper, subapical leaves (2-7) andlower, suprabasal leaves (2-2) were also treated at selected QMI port from upper first-flush leaves increased during the sec-growth stages. In the third series, a median third-flush leaf (3-5 or ond flush to greater than 70% of the _4C recovered,3-6) was treated at each QMI growth stage from 3 Lag to 4 Lag. decreased to 56% at 2 Lag, increased again to 72% duringAdditional upper and lower leaves were treated as in the second se- the third flush, then decreased to about 20% at 4 Bud.ties. Three individual plants were treated for each leaf position at Export patterns of second-flush leaves were similar toeach QMI growth stage. Allocation of 14C within the plants was those found for first-flush leaves (Fig. 2B). About 30% ofexpressed as percentage of 14C found in each plant tissue compared the fixed 14C was exported from the second-flush medianto total _4C recovered in the plant or total _4Ctranslocated from the leaf at 2 Lag. Export from median leaves increased to 80%source leaf. Allocation was expressed as percent rather than an ab- early in the third flush, then decreased to about 55% at 3solute amount because the amount of 14C initially fixed and trans-ported differed considerably among plants, but the percent Lag and remained at that percentage during the fourth flush.allocated to different tissue within a plant was quite consistent. Carbon export patterns of third-flush leaves at 3 Lag and

during the fourth flush were similar to those found for first-

Plant growth and aliometric relationships and second-flush leaves (Fig. 2C).Leaf area and dry mass data from all three series of plants de- The translocation of photosynthate upwards or downwards

scribed above were combined to examine plant growth patterns and in the plant changed during the flush reflecting changes inother aUometric relationships. Although the data set created by relative sink strength of developing shoots and roots. At 1merging data from across allocation experiments was potentially Lag, 80-90% of the exported lnc was translocated down tobiased as regards sampling, it did provide evidence of growth rela- lower stem and roots (Fig. 3A). During second-flush devel-tionships parallel to those observed in allocation. Leaf areas were opment, most current photosynthate from first-flush leavesdetermined at harvest with a LI-COR leaf area meter (LI-3000A, was allocated upward to developing stem and leaves of theLI-COR, Lincoln, Neb.). Relative growth rates (g.kg-Lday-l), both new flush. This cycle repeated during the third flush; how-instantaneous and modeled (Hunt 1990), were based on the average

ever, only about 20-30% of current photosynthate from first-number of days from epicotyl emergence to each QMI growthstage and the average dry mass at each QMI growth stage. Mass ra- flush leaves was allocated upward for third-flush develop-tios of leaves, shoots, and roots of individual trees were calculated ment, while 70-80% was allocated downward to stem andfrom the mass of the various organs divided by the mass of the roots. The pattern of transport from second-flush sourcewhole plant, leaves was similar to that for first-flush leaves except essen-

tially no current photosynthate from second-flush leaves was

Calculations scaling up allocation data for individual allocated to fourth-flush development (Fig. 3B). Third-flushleaves to the flush level leaves, with the same up and down transport pattern as first-

Total upward or downward carbon allocation from different and second-flush leaves, supplied essentially all current pho-leaves within a flush was calculated from the areas of individual tosynthate required for fourth-flush development (Fig. 3C).

© 2000 NRC Canada

_) Dickson et al.: I 1299

i) Fig. 2. Percentage of the total 14Ctranslocated from first-, Fig. 3. Percentage of total 14C translocated upward from first-,:s second-, and third-flush source leaves at different QMI stages, second-, and third-flush source leaves at different QMI growth!" (A) First-flush source leaves, upper, subapical leaf treated, stages. (A) First-flush source leaves, upper leaf treated.t- (B) Second-flush source leaves, median leaf treated. (C) Third- (B) Second-flush source leaves, median leaf treated. (C) Third-L- flush source leaves, median leaf treated. Retained lac in the flush source leaves, median leaf treated. Percentage of trans-e, source leaves is the reciprocal plot of the translocated 14C.Re- located n4Cbelow the source leaves is the reciprocal plot of that

suits are from a 48-h chase period after treatment with 14CO2. translocated upward. Open circles show the percentage of naCt Lag stages are indicated by the dotted lines. Error bars are SEMs. translocated upward from a lower treated leaf (A) or from an up-I , ............ per treated leaf (B and C) from the flushes. Lag stages are indi-

_st Flus'.71 cated bY the d°tted lines" Err°r bars are SEMs" i

f 75 100 ...........60 _ A !First Flush

8O45

._. 6030 O

40O 15 : : : "O

,_ O: : _ I _ I I I I i I ', ', _, Q.--" 20

o i ii i ; I i i I i75 c)ofj_ • .

I-- 60 r- 100ww..-

o _ B Second Flush"45 I-- 80 It:.

30 v 60• . (--

15 B Second Flush .o 40(_ 0: : _ I _ : : _ ' _ ' ' ' ; ' (_13.. ' ' ' ' _ ' " ¢o

75 C Third Flu_h- oo) 20r- 0 ; : I : , , , , , ,

60 -r/_ _ 100 C Third Flush

45 _/_ -" _ 80 (?30 Q. 60

15 40

t I I I I ' I a I | n ! I

o_._,_ c_._,_,_v o_._c_r.ff o_ 20

QMI Growth Stage -_ -_--'' " o, __...,.., ___. e__ ,v ,_,_ ,_'o_,_ _ _'

When upper, median, and lower leaves of the same flush QMI Growth Stagewere treated with L4C, different allocation patterns werefound for leaves at different positions in the flush. Even with for total carbon translocated upward or downward fromfirst-flush leaves that often appear whorled on the stem with these leaves).no large differences in leaf insertion position, the lower leavestranslocated only 40% of 14C upwards during 2LL (Fig. 3A, Carbon transloeation to different plant parts2LL, open circle), while upper leaves translocated 90% of The percentage of current photosynthate translocated tonZC upwards. During early development of the third flush, other leaves, stems, or roots differed during a flush. Whenmedian leaves of the second flush allocated 70-80% of cur- upper first-flush leaves were treated with X4CO2at 1 Lag,rent photosynthate to third-flush development, while lower about 10% of the exported _4C was translocated to otherleaves allocated less than 20% upward to the third flush leaves of the first flush (Fig. 4A), and the remaining 90%(Fig. 3B, 3LL, open circle). Similar allocation patterns were was translocated to lower stem and roots (Figs. 4B and 4C,found for third-flush leaves during the fourth flush. Upper respectively). During the development of the second flush,leaves of the third flush translocated 80% of current most translocated ]4C was allocated to second-flush leaves

photosynthate upwards to the fourth flush (Fig. 3, 4LL, open and stem (62-74% leaves and 20-25% stems, respectively)circle), while median and lower leaves translocated only (Figs. 4A and 4B). During 2 Lag, most u4C was again allo-about 40% upwards. Thus, upper and median second-flush cated to lower stem and roots (Figs. 4B and 4C). During de-source leaf cohorts had similar translocation patterns, and velopment of the third flush, only about 30% of the ]4Cthese differed from the lower cohort of second-flush source translocated from first-flush leaves was allocated to third-leaves. In contrast, median and lower third-flush source flush leaves and stem; the remaining t4C was translocatedleaves had similar translocation patterns, and these differed upward to second-flush stems and downward to first-flushfrom the upper cohort of the third flush (see Table 2 below stems or roots (Figs. 4B and 4C). Transport of L4Cfrom

© 2000NRC Canada

1300 Can. J. For.Res. Vol. 30, 2000

Fig. 4. Percentage of J4C translocated from upper first-flush Fig. 5. Percentage of 14Ctranslocated from median second-flushsource leaves found in leaves, stems, or roots at different QMI source leaves found in leaves, stems, or roots at different QMIgrowth stages. (A) 14Cfound in the first-, second-, and third- growth stages. (A) 14Cfound in the leaves of the differentflush leaves. (B) 14Cfound in stems. (C) 14Cfound in roots, flushes. (B) 14Cfound in stems. (C) t4C found in roots. DataData show distribution within the plant of 14Cexported by first- show distribution within the plant of 14Cexported by second-flush leaves in Fig. 3A. Lag stages are indicated by the dotted flush leaves in Fig. 3B. Lag stages are indicated by the dottedlines. Error bars are SEMs. lines. Error bars are SEMs.

t80 /t_ i A Leaves 75 [ ..... ! -i _" \ i Flush ! 60 A Leaves

60 i \ i • First i Flushi \i @ Secor_:l 45 "_ • First

O" 40 _.. 0 .rThirdl / _" -- @ Second= , ,0 . oo 0 o 0o ....... o f TTT TTTT T-- 13 ' ' ' -- 75o_ 80 Stems,-- r- B Stems

_ 60I-- 60 I---

_ 45

"o_ 40 i_ "_

,-- E 30

20 _ 15O Oo o o•',-" "*" 0

,-- 80 ,'- 75 _ r" p,4_,t,

._o (2_ _'_

60 _ 60 _I_0 0

_:_ 40 _ 453O

2015

0 0 1 I 1 | i I i t t

___'_ _---,., __ _ _ _ .-, _ _ _ ,-, .,_

QMI Growth Stage QMI Growth Stage

median second-flush leaves followed the same patterns as area (Hanson et al. 1988b). Individual leaf areas of ourdescribed for first-flush leaves (Figs. 5A, 5B, and 5C): up- three-flush seedlings varied from 70 to 163 cm 2 correspond-ward to developing leaves and stem during development of ing to 2.4 to 5.6 mmol carbon fixed per leaf per 16-h daythe third flush and downward to lower stem and roots during (Table 1). Scaling this to the number of leaves in each leaflag. In contrast to upper first-flush leaf allocation to the third cohort (upper, median, lower) yielded estimates of 4.8 toflush, median second-flush leaves allocated little 22.4 mmol total carbon fixed per cohort per day and 14.8 tophotosynthate to the developing fourth flush (data not 51.6 mmol per day total carbon fixed per flush (Table 1).shown). Essentially all current photosynthate required for Estimates of total carbon fixed, exported, and translocatedfourth-flush development apparently came from the third- upward or downward from different leaf cohorts within aflush leaves or was fixed in situ by the developing leaves of flush show a large gradient in the direction of translocationthe fourth flush. Allocation patterns of third-flush leaves (to the developing flush or to lower stem and roots) depend-during the fourth flush (3 Lag to 4 Lag) were similar to ing on the position of the leaf within the flush (Table 2).those found for first- and second-flush leaves (data not Even in the first flush where little difference in allocationshown), patterns among leaves was expected, upper leaves

translocated 6.2 mmol of current photosynthate upward toScaling allocation data up to the flush level the developing shoot and 0.7 mmol downward at 2LL, while

The relative contribution of leaves from different positions lower leaves translocated only 1.5 mrnol upward andwithin a flush to seedling development can be estimated 2.2 mmol downward to lower stem and roots (Table 2). At 2from their respective leaf areas, photosynthetic rates, and al- Lag and 3LL (6.7 and 7.8 rnmol, respectively), essentiallylocation coefficients. Photosynthetic rates per unit area for all current photosynthate from first-flush leaves was allo-fully expanded leaves within a flush are similar; therefore, cated to lower stem and roots (Table 2). Similar up andtotal leaf carbon fixation rates are closely related to total leaf down changes in allocation were found for second- and

© 2000NRC Canada

Dickson et al.: I 1301

Table 1. Leaf area and carbon fixation rates for three flushes of leaves on northern red oak

seedlings.lit t i

Leaf carbon No. of Total carbon

Leaf Individual leaf fixation per day leaves per fixation per daycohort area (cm2)a (mmol/lea(') flush cohort (retool/cohort c)

First-flush leaves

Upper 94 (n = 15) 3.2 3 9.6Lower 74 (n = 35) 2.6 2 5.2Flush total 430a 5 14.8

Second-flush leaves

Upper 122 (n = 12) 4.2 3 12.6Median 93 (n = 17) 3.2 3 9.6

Lower 70 (n = 12) 2.4 2 4.8Flush total 785 8 27.0

Third-flush leaves

Upper 140 (n = I0) 4.8 4 19.2Median 163 (n = 15) 5.6 4 22.4

Lower 72 (n = 9) 2.5 4 10.0Flush total 1500 12 51.6

|

Note: A standard photosynthetic rate for these seedlings (6.0 gmol.m-2.s4) was scaled to a 16-h dayand by leaf area and number of leaves in cohorts within each flush.

"Leaf areas are average values for all treated leaves of that cohort (n = number of plants averaged).bLeaf carbon fixation rates are calculated from 6.0 lamol CO,-m4.sq (Hanson et al. 1988a, 1988b)

scaled to a 16-h day and for the average area of treated leaves in that cohort (6.0 gmol COz.m--'-s-t per16-h day = 34.6 lamol.cm-2 x 94 cm2 = 3.2 mmol/teaf per 16-h day).

_Total carbon fixation equals leaf carbon fixation × the number of leaves in each leaf cohort.aFlush total leaf area was calculated by multiplying individual leaf areas by the number of leaves in

that cohort and summing cohorts within a flush.

third-flush leaf cohorts. As more leaves (and leaf area) were (Fig. 6). Plant total dry mass accumulation was approxi-added to the seedlings, the median leaf cohort shifted alloca- mately exponential as indicated by the linear response oftion from mostly upward (second-flush leaves 67% or log-transformed average dry mass at each QMI growth stage4.8 mmol up and 33% or 2.2 mmol down at 3LL) to mostly when plotted against the average days after emergence

downward (third-flush leaves 37% or 4.9 mmol up and 63% (Fig. 7A). Similarly, log-transformed average dry mass ofor 8.3 mmol down at 4LL) during the next flush (Table 2). shoots and roots at each QMI growth stage were essentially

Although different leaf cohorts allocated different linear (Fig. 7B). Modeling these data provide estimates ofamounts of carbon upward and downward, when transport relative growth rates (Rm) for shoots (R m = 42.5 g.kg-l-day -1,was summed for all leaf cohorts, upward and downward re = 0.97), for roots (R m = 50.1 g.kg-l.day -1, re = 0.97), andtransport during flush development was about equal in larger for intact seedlings (R m = 44.6 g.kg-Lday -I, re = 0.97).plants (Table 3). At 3LL, when the developing third flush is However, there is some deviation from linearity even though

a major sink, total transport from first- and second-flush the re values for the entire data set indicate a strong linear fitleaves was 14.2 mmol/day upward and 15.6 mmol/day of the data. Further, deviations from the linear fit appear

downward (Table 3). Similarly, at 4LL, transport was systemati c, especially for root and shoot data (Fig. 7B). If17.2 mmol/day upward and 17.8 mmol/day downward. Con- these same log-transformed data are used to calculate instan-versely, during Lag stages of at least the first four flushes of taneous relative growth rates (Ri), these changes are accentu-growth, most transport was downward, ated (Fig. 7C). Shoot R i was greatest at the lag stages (based

on the growth from LL to lag), while root R i was greatest at

Plant growth and allometric relationships the Bud and SL stages. Cyclic growth was also indicated byTo understand allocation patterns in the context of seed- changes in shoot/root ratios (Fig. 8A). Shoot/root ratios

ling growth, we analyzed biomass and leaf area data pooled show large fluctuations associated with flushes: high at lag

across the harvested plants in all three allocation experi- and low during flushing. In addition to this within-flush cy-ments. Northern red oak growth is quite rapid in our growth clic pattern, shoot/root ratios gradually decrease with plantchamber environment and fertilizer regime. Three-flush (3 age as shoot growth decreases relative to root growth.Lag) and four-flush (4 Lag) seedlings can be produced in 60 Mass ratios of the different plant components are also cy-and 95 days, respectively, after epicotyl emergence from the clic with maxima and minima ratios associated with differ-soil (Table 4). These 3 Lag and 4 Lag seedlings had a total ent QMI growth stages (Figs. 8B and 8C). Shoot mass ratiosleaf area of 0.195 and 0.409 m z and a total plant dry mass of (Fig. 8B), leaf mass ratios, and leaf area ratios (Fig. 8C) all18 and 62 g, respectively. Leaf mass per unit area initially peaked at or slightly before the lag growth stage. The patterndecreased from SL to LL as the leaves expanded, then in- of root mass ratios was essentially a mirror image of shootcreased to about 60 g/m 2 for leaves of the first three flushes and leaf ratio patterns with minima at the lag growth stages

© 2000 NRC Canada

1302 Can. J. For. Res. Vol. 30, 2000

Table 3. Total carbon translocated upward or downward

.-=_° _ _ (mmol/day per flush) from leaves of each flush at selected QMI_ growth stages of northern red oak seedlings.

_ r-_. _ , , ,_, o_ _ r-- oo e_ ,o _. _: c-i _ _ _ First-flush Second-flush Third-flush

o ._ o QMI leaves leaves leaves Total

2 _ _ stage Up Down Up Down Up Down Up Down

o _=_ 2LL 7.7 2.9 .... 7.7 2.9m oo 2Lag 0.9 6.7 0.7 6.6 _ -- 1.6 13.3

d r-: d ,-4 c5 d ,--, -: _ ,, ,..Z - 3LL 1.9 7.8 12.3 7.8 -- -- 14.2 15.6

o-_ 3Lag 0.6 6.2 1.6 14.2 1.6 12.7 3.8 33.1o_

_ 4LL -- -- 0.4 4.4 16.8 13.4 17.2 17.8o o 4Lag _ -- 0.3 3.7 1.5 28.9 1.8 32.6.u_

=-_0_,

_0 _ c,i e-i _ ei ,--: ¢-i ¢,i ¢,i e6 _: _ ,6 Table 4. Plant age, total leaf area, and dry mass of northern red,_ _ " oak seedlings at each Quercus morphological index (QMI)-¢cq

O' ¢, r-= . growth stage.

_x_ ....._ = QMI growth Age (days after Seedling dry

_ ._ sta,,e emergence) Leaf area (m2) mass (g)"_ d .--: d d 6 c_do d_dl -_ ',o"_

i l _ _ ILag 15±0.61 0.0315±0.0031 1.68±0.18

2Bud 20±1.31 0.0279+0.0032 2.21±0.18,. o, _ _ 2SL 22+0.00 0.0542±0.0019 4.16±0.56

_ _ 2LL 26±0.33 0.0651±0.0053 4.36±0.56

- _ _ ,_- _ ,-: ¢4 e,i c4 u_ _ _ _ 2Lag 36+1.04 0.0906±0.0071 6.80±0.54"6 3Bud 45±2.64 0.0876±0.0111 9.86-* 1.69

_ _ 3SL 52-*2.97 0.1149±0.0126 13.03..1.41= - 3LL 55±2.13 0.1511±0.0139 13.82±1.15

,.OO

"_ _ = 3Lag 59.*0.69 0.1949..0.0072 18.30±1.00

-= ] ] I I e,i e,i_r"_ o_ ,,6 o6--°°m _: , _-_ 4Bud 64-.1.76 0.2449-.0.0184 26.46±2.08-_ _: 4SL 75±1.33 0.2737±0.0151 37.92..1.46

"_ _ = 4LL 89±3.47 0.3767±0.0289 51.73-.4.06

"_ [.- _ 4Lag 96-.1.85 0.4092+0.0270 62.20-_:4.93

"" -- Note: Values are means + SEM of 3-19 plants depending on the

_ number of plants treated with '4C at each QMI growth stage.

_' I I I I o,*o -,*o_ (Fig. 8B). In addition to cycling within a flush, shoot and

_ _ _ leaf ratios decreased and root ratios increased with plant age." '_ 'q. _ All of these cyclic allometric ratios are consistent with largeO ¢q _ ¢q

o o -_ _ ,,4 _: ,e changes in allocation of carbon within the plant both during"_ [ I ] [ _ r-: _ 06 - ,-, _ flushing and with plant size.

= _o_ Discussiono

-= 8 _ _ Shoot growth patterns of forest trees are genetically_ ,= _ r- _ _ - _ r_ _ _ o ¢5 _ _ programed but may be modified by environmental changes........ t_ _:

= Such inherent growth patterns (e.g., determinate,

.= _-_ semideterminate, or indeterminate) significantly influence._ _ carbon fixation rates of individual leaves and carbon alloca-_O

=o _._- tion within the plant (Hanson 1988a; Dickson 1991). With-_ out detailed information about growth patterns and the

..... ,_ ,- application of such information in the design of research& studies, much misinformation may be generated or rather

_ _ _ large changes in morphological development and physiologi-_ _" _ cal processes missed when results are averaged from plants

_. _#'_''_r-_.=_--_o_ _. ._- ,5 _ _ ,n: _ e,i o_ r; _ _: : : _ = in different ontogenetic stages. To control for differences inm _ -8 _ ontogenetic development, the QMI was developed based one,i _ = _ _ simple stem and leaf measurements that allow the treating

_ _ _ _ ,_ _ _ _ _ _ # _ { and sampling of oak seedlings at specific stages of develop-ment (Hanson et al. 1986). The QMI defines four distinct

© 2000 NRC Canada

Dicksonet al.: I 1303

Fig. 6. Changes in leaf mass per unit area of first-, second-, and Fig. 7. Increase in average dry mass of northern red oak seed-third-flush source leaves of northern red oak seedlings at differ- lings plotted against average days after emergence. (A) Log-ent QMI growth stages. Lag stages are indicated by the dotted transformed seedling total dry mass increase with plant age afterlines. Error bars are SEMs. epicotyl emergence from the soil. (B) Log-transformed shoot and

root dry mass increase with plant age. (C) Instantaneous relative70 ' ............ growth rates (Ri) of shoots and roots. Ri is based on log-

__h transformed mass changes at each QMI interval (e.g., LL to Lag,

< 60

.-. Lag to Bud, or Bud to SL stages). Lag stages are indicated by_, 50 the dotted lines. Error bars are SEMs.co Et_ 5.0 ,'-' ........

,._ 4.0 i"30 " o Sect,.... , , , , i O ,Th,ir6, 3.0-J 0_

r0' ,_v to _.,_/ r0' _..,_' to _',.4 q;t _-,.7tO 2.4 _O'

_--,_,"V ,v_,_o ,'_ "_ v _'_' 2.0

° ;QMI Growth Stage ,- 1.o _0.0 ;'1 I " I i I I "O3

4.5i_ • iRoot

growth stages within each flush (Fig. 1) and provides a basis _ : zx ::Shoot iI:1

for associating a specific developmental stage with physio- _" 3.0 _,a ::

logical or morphological response to treatments. Carbon a .__Jtransport patterns, shoot and root growth, and other r-_j 1.5allometric relationships all change during a growth flush and ._"- __.,r- "_these changes are accentuated when related to a specific 0.0

QMI growth stage. -1.5 . __',-i ! • I I I ! "

Carbon export from source leaves and allocation within 5 30 45 60 75 90

the plant Days after EmergenceThe rate of carbon fixation within and transport out of a

fully expanded leaf depends on species, leaf age, sink de- , ..... _ , , ,mand, plant developmental stage, and many other factors i C(Geiger 1987; Hanson et al. 1988a; Dickson et al. 1990; _ 100 :_ _rk, i'_.

Dickson 1991). Many of these factors interact in episodic t_ 75flushing species such as red oak to produce widely varying "7 50patterns of carbon fixation and transport. Any factor that in- 25creases sink strength relative to existing source strength usu- t:nally increases photosynthetic rates. Because the stem and "-"

new leaves of a flush are expanding and developing at the r/'- 0 _same time, the new flush is a major sink that strongly influ- -25ences the existing leaves, particularly in small seedlings. ^_^--,_ _-_ _'-_ _-_ _ _"J_•v ,v_,_ _ ,o_,_ _ _,_,Photosynthetic rates of first-flush red oak leaves increasedduring flush expansion and decreased during lag for both the QMI Growth Stagesecond and third flush, indicating a strong feedback responseto changing sink strength (Hanson et al. 1988a). Similarchanges in photosynthetic rates were found with cocoa Dickson and Shive 1982). We found this same age-related(Theobroma cacao L.), another species with episodic growth incorporation and transport pattern in red oak leaves of this(Sleigh et al. 1984). Carbon transport or retention in source study (Fig. 2) and in a previous study (Dickson et al. 1990),leaves is also cyclic and is related to both leaf age and sink where only about 25% of the t4C-photosynthate wasdemand. Young leaves at the lag phase (both first- or translocated out of first-or second-flush source leaves at 1second-flush leaves) are fully expanded but physiologically Lag and 2 Lag, respectively. Transport out of source leavesimmature, because photosynthetic rates (Hanson et al. increased to 70-80% of the _4Crecovered in the plant during1988a), protein, and structural carbohydrates (Dickson et al. the next flush and cycled in subsequent flushes. The large2000) continue to increase throughout the next flush. In ad- increase in _4Cretained by first-flush source leaves at 3 Lagdition, maturation gradients are found both within leaves and 4 Bud probably indicates senescence of these older(Tomlinson et al. 1991) and within a flush (Dickson et al. leaves (Tobias et al. 1995). Retention of recently fixed car-1990). bon in senescing leaves is common, because transport pro-

As cottonwood (Populus deltoides Bartr. ex Marsh.) cesses seem to decline more rapidly than carbon fixation,leaves expand and mature physiologically, less carbon fixed indicating a loss of phloem activity (Dickson and Nelsonby the leaf is incorporated into in situ chemical fractions, 1982; Nelson and Isebrands 1983).and more carbon is exported (Dickson and Larson 1981; Interesting transport gradients were found among different

© 2000 NRCCanada

117,.__,__ - " ................................................... - ......... :_-

1304 Can. J. For.Res. Vol. 30, 2000

Fig. 8. Changing allometric relationships of northern red oak to the third flush at 3LL but essentially no photosynthate up-leaves, shoots, and roots at different QMI growth stages, ward to the fourth flush (Fig. 3B).

(A) Seedling shoot/root ratio at each growth stage. (B) Root As more flushes are produced by oak seedlings, the num-mass ratio (RMR) and shoot mass ratio (SMR) (root or shoot bet of leaves and leaf area increases significantly. Northernmass/whole plant mass). (C) Leaf mass ratio (LMR) (leaf red oak seedlings grown under our experimental conditionsmass/whole plant mass) and leaf area ratio (LAR) at each QMI usually have about 4, 8, and 12 leaves in the first-, second-,growth stage. Lag stages are indicated by the dotted lines. Error and third-flushes, respectively. The larger number of leavesbars are SEMs. and larger leaf area per leaf (Table 1) increases total leaf

5.0 ........ , , , , area and photosynthetic capacity; 3 Lag seedlings may haveo /_ more than six times as much total leaf area as 1 Lag seed-

IZ_ 4.0 lings (Table 4). The larger number of leaves and larger leaf._ area result in within-plant transport patterns more like inde-oo 3.0 terminate growing plants such as cottonwood. In cotton-

wood, the upper, recently mature leaves provide most of the

2.0 photosynthate necessary for new leaf and shoot develop-.c: ment, the middle leaf cohort translocates both 'upwards to

1.0 _ developing leaves and downward to lower stem and roots,0.0 : I _ _ : " " : _ : " _ ; o and the lower leaf cohort translocates largely to lower stem

",,,_

._ 0.40 SMR B 0.85 _ and roots (Dickson 1986, 1991). Similar differential alloca-0.35 _ T 1_ _t--_ 0.80 IZ -'-'- tion patterns of upper or lower leaves of a flush were found

2,_ 0.30 0.75 _ _. in 14Ctransport studies with cocoa (Sleigh et al. 1984). Sucht_

.__ 0.25 0.70 _; _ pattems are probably common with many episodic flushing.,-, -_ .._.. species.o "-" 0.20 0.65 o The importance of these within-plant allocation patternso r-rV 0.15 RMR 0.60 03 and the contribution of individual leaves within and among

0.00 _ I I I ', : : I I I I I } 0.00 flushes was clarified when these allocation patterns werequantified using percent ]4C exported, percent 14C

.o 0.7 0x LMR r 32 ._ translocated up or down, leaf area, and a standardt_

_Z" 0.6 28 _" _ photosynthetic rate (Tables 1-3). Although the upper, me-

_ 0.5 24 _ 't_ dian, and lower leaves allocated different amounts of 14C-,-- " photosynthate upward or downward, the total carbon allo-

_ 0.4 20 < "_ cated upward or downward, when summed for second- and"-" third- flush leaves, was essentially equal during the leaf-

.j 0.3 ; .d linear stage of the third and fourth flushes (Table 3). During0.0 ........... _ ' 0 a lag phase (2 Lag, 3Lag, 4 Lag; Tables 2 and 3),90%of

•.,.t_ "tO^"'J c0' 50_,/ _cr--.._ tO "4 ,o,.. _ ff ,v_,_o o_ _.,_ _, v_, current photosynthate from all leaves is allocated to lowerstem and roots. The 10% found above the treated leaves is

QMI Growth Stage probably recycled through the root system as amino and or-ganic acids (Dickson 1989; Dickson et al. 1990).

leaves of a flush. During the development of a new flush, The allocation of current photosynthate to the root sys-the upper leaves of both the first and second flushes ex- terns of larger oak plants is significant, because it providesported a greater amount of 14C than the lower leaves (Ta- carbon for continual root growth as well as water and nutri-

ent uptake during the flush. In addition, the allocation ofble 2), perhaps reflecting their proximity to the rapidlyexpanding sink of the new flush and the physiological influ- current photosynthate to roots and the resulting root growthence of this new sink on source leaf metabolism. In addition, may increase the production and translocation of variousthe lower leaves of the first flush retained more 14Cthan the growth hormones and essential nutrients (cytokinins, amino

upper leaves during the later stages of the third flush (e.g., 3 acids, etc.; see Dickson 1994) thus increasing the number ofLag), perhaps reflecting senescence in these older leaves, leaves in each subsequent flush and stimulating occasional

Because of the episodic growth pattern of oak seedlings, plants to change to indeterminate growth in the third orfourth flush.relative sink strength of developing leaves, stems, and rootschanges during the flush cycle, and this change in sinkstrength initiates an extreme shift in the direction of trans- Plant growth and allometrie relationshipsport within the plant (Fig. 3). This cycling is greatest in Allometric relationships are frequently considered in stud-small plants with relatively small leaf area but becomes ies of plant response to environmental changes, because themodulated as more flushes and more leaves are added to the differential carbon allocation to leaves, stems, or roots andplant. For example, upper first-flush leaves translocated to growth or storage may significantly affect how differentabout 90% of current J4C-photosynthate upward to the sec- species respond to environmental changes. To determine andond flush at 2LL and about 25-30% upward to the third correctly interpret allometric changes, however, careful con-flush (Fig. 3A). In contrast, upper second-flush leaves sideration must be given to growth rates, plant size, andtranslocated about 70% of current J4C-photosynthate upward ontogenetic stage. Much recent discussion has been devoted

© 2000 NRCCanada

Dickson et al.: I 1305

to ontogenetic drift in allometric relationships and how this out of phase (Fig. 7C). The fluctuation in shoot/root ratios

drift might influence the interpretation of research data could result from either constant root growth and episodic(Coleman and McConnaughay 1995; den Hertog et al. 1996; shoot growth or episodic root and shoot growth.Gedroc et al. 1996). Few allometric relationships vary con- Both episodic root growth and constant root growth havesistently among species except in general terms but differ been found for trees with episodic shoot growth (Dicksonfor individual plant species, depending on growth strategy 1994). Taproot growth may stop completely or simply slowand response to varying environments (Schulze 1983). Leaf down during shoot growth (Reich et al. 1980; Thaler andmass per unit area was the most consistent allometric mea- Pages 1996a). In contrast, taproot growth may be constantsurement found with our seedlings and followed the ex- during shoot growth (Belgrand et al. 1987; Harmer 1990;pected pattern associated with leaf age, decreasing as the Pages and Serra 1994). These differences may result fromleaves expanded, then increasing to about 60 g/m2 as the differences in available current photosynthate or stored car-leaves aged (Fig. 6). Leaf mass of a particular flush in- bohydrates. Reserves in the acorn cotyledons may maintaincreased well into the next flush because northern red oak taproot growth during flushing (Belgrand et al. 1987; Dick-leaves continue to develop both photosynthetically and son 1994), and root reserves may be utilized in some spe-structurally for several QMI growth stages after full expan- cies. Root reserves, however, may not be available for newsion (Tomlinson et al. 1989). An increase in leaf mass per root growth in many species (Wargo 1979; Philipson 1988;unit area with time is a common feature of many plants Dickson 1991).(Kloeppel et al. 1993) and may result from the deposition of Much evidence indicates that current photosynthate is re-structural carbohydrates and other organic compounds or the quired for new root growth in many species (Aquirrezabal etcontinued import of inorganic products such as calcium. The al. 1994; Horwath et al. 1994). This is particularly importantleaf mass per unit area (60 g/m 2) of our seedlings is greater in flushing species when most current photosynthate is allo-than expected based on the relatively low light intensity of cated to the shoot system during flush development. Whenthe growth rooms and is similar to that found for sun leaves photosynthate is limited, different parts of the root systemof several oak species (Abrams and Kubiske 1990; Reich et may respond differently because of varying sink strengthal. 1995). Leaf weight per unit area is quite variable and re- within the root. In work with Hevea, taproot growth rate de-sponds to different growth environments, particularly light, creased during leaf expansion but did not stop completely,decreasing as light intensity decreases (Takahara 1986; growth rates of secondary roots cycled more than taproots,Ellsworth and Reich 1992, 1996). and tertiary root growth stopped completely (Thaler and

Other allometric relationships such as leaf mass ratio (leaf Pages 1996a). These fluctuations in root growth were greatermass/total plant dry mass), root mass ratio, and shoot/root in shaded plants that had limited current photosynthate (Tha2ratio usually change in a consistent fashion depending on the ler and Pages 1996b). Similar results were found withinherent developmental pattern of a particular species. Theobroma (Kummerow et al. 1982). Data presented by bothShoot/root ratios often show a curvilinear relationship dur- Belgrand et al. (1987) and Harmer (1990) showed cycling ining early plant development, either increasing or decreasing lateral root growth while taproot growth was constant. In ad-rapidly to some constant ratio (Coleman and McConnaughay dition, Belgrand et al. (1987) showed cycles of total number1995; Gedroc et al. 1996). A rapid increase in shoot/root ra- of laterals, growth rates of laterals, and frequency distribu-tio to some constant value is a common pattern for annual tion along the taproot that were probably related to flush cy-plants that initially allocate carbon to root growth, then to cle, but this was not considered in their paper. The aboveleaf and stem growth (Schulze 1983). Herbaceous information indicates that root systems are extremely dy-perennials, in contrast, have cyclic shoot/root ratios because namic, that different parts of the root system may respondof cyclic shoot and root growth during the growing season, differently, and that small changes in experimental environ-Woody perennials with large amounts of secondary growth ments that affect levels of current photosynthate may influ-increase stem mass compared with root and leaf mass ence root growth and apparent cycling during flushing.(McMurtrie and Wolf 1983). Total leaf mass becomes con- Nevertheless, total carbon allocated to root systems wasstant after some period of development, so the leaf/mass ra- three to four times greater at lag than at LL (Table 3). There-tio decreases with age. In contrast, the shoot/root ratio fore, the cycling of shoot/root ratios associated with differ-generally increases to some constant value with age. How- ent QMI growth stages seems reasonable.ever, the conservative growth strategy of oaks that favorsroot growth during early plant development, particularly inresponse to stress, may result in decreasing shoot/root ratios Conclusions

until conditions change to favor top growth (Kolb and Research in this study was conducted with one- to four-Steiner 1990). flush red oak seedlings, and the results probably do not ap-

During early stages of growth, whole plants and their dif- ply directly to large trees that typically have only one flushferent parts usually have an exponential or a log-linear early in the growing season. However, large trees have cyclicgrowth curve. Our seedlings were no exception for total dry shoot and root growth and current photosynthate is probablymass (Fig. 7). However, growth of shoots and roots was important for fine root growth during the summer. Oak seed-strongly cyclic, and the cycles were associated with QMI ling growth and carbon-allocation patterns may have consid-growth stages (Fig. 7). These cycles were accentuated when erable implications for management of red oak. Managementshoot/root ratios, root mass ratios, or leaf mass ratios practices can be designed to favor shoot or root growth. For(Fig. 8) were plotted, because shoot and root growth were example, if three-flush seedlings could be rapidly produced

© 2000 NRC Canada

1306 Can. J. For. Res. Vol. 30, 2000

in nursery beds, then further flushing inhibited, the large leaf Dickson, R.E. 1986. Carbon fixation and distribution in youngarea produced would provide current photosynthate for allo- Populus trees. In Proceedings: Crown and Canopy Structure incation to stem growth, root growth, and storage producing a Relation to Productivity. Edited by T. Fujimori and D. White-

higher quality seedling (Schultz and Thompson 1991). In ad- head. Forestry and Forest Products Research Institute; Ibaraki,dition, northern red oak with its flushing growth habit, pro- Japan. pp. 409-426.rides an ideal experimental system for the study of Dickson, R.E. 1989. Carbon and nitrogen allocation in trees. Ann.photosynthetic and carbon transport changes in response to Sci. For. 46(Suppl.): 631s-647s.changing sink strength because changing sink strength is a Dickson, R.E. 1991. Assimilate distribution and storage. Ch. 3. Innatural response to the flush cycle and requires no artificial Physiology of trees. Edited by A.S. Raghavendra. John Wiley &plant manipulation. Sons, New York. pp. 51-85.

Allocation patterns are also useful in mechanistic process Dickson, R.E. 1994. Height growth and episodic flushing in north-ern red oak. In Biology and silviculture of northern red oak in

modeling work. Allocation coefficients were used to develop the North Central Region: a synopsis. Compiled by J.G.the ECOPHYS process-based poplar growth model (Host et Isebrands and R.E. Dickson. USDA For. Serv. Gen. Tech. Rep.al. 1996), and allometric relationships such as plant NC-173. pp. 1-9.

growth/total leaf area, leaf mass/plant mass, and shoot/root Dickson, R.E., and Isebrands, J.G. 1991. Leaves as regulators ofratios are very consistent at a particular stage of plant stress response. In Response of plants to multiple stresses.growth and commonly have r2 values of 0.9 or better. This Edited by H.A. Mooney, W.E. Winner, and E.J. Pell. Academicstudy also provides considerable basic biological informa- Press, New York. pp. 3-34.tion about carbon allocation and shoot and root growth pat- Dickson, R.E., and Larson, P.R. 1981. _4C fixation, metabolic la-

terns of northern red oak grown with optimal experimental beling patterns, and translocation profiles during leaf develop-conditions. Such information would be useful for future ment in Populus deltoides. Planta, 152: 461-470.studies of red oak growth responses to environmental Dickson, R.E., and Nelson, E.A. 1982. Fixation and distribution of

stresses such as increasing CO 2 concentrations, temperature, JaC in Populus deltoides during dormancy induction. Physiol.and drought stresses associated with predicted global climate Plant. 54: 393-401.change. Dickson, R.E., and Shive, J.B., Jr. 1982. _4CO2 fixation,

translocation, and carbon metabolism in rapidly expandingleaves of Populus dehoides. Ann. Bot. (London), 50: 37-47.

Acknowledgments Dickson, R.E., Isebrands, J.G., and Tomlinson, P.T. 1990. Distribu-

tion and metabolism of current photosynthate by. single-flushWe gratefully acknowledge the technical assistance given northern red oak seedlings. Tree Physiol. 7: 65-77.

by Gary Buchschacher for greenhouse and growth room Dickson, R.E., Tomlinson, P.T., and Isebrands, J.G. 2000. Parti-plant culture, Gary Garton and Beth Hair for laboratory tioning of current photosynthate to different chemical fractionsanalysis, and Ed Bauer for graphics design. In addition, in leaves, stems, and roots of northern red oak seedlings duringhelpful suggestions by four reviewers considerably improved episodic growth. Can. J. For. Res. 30: 1308-1317.the manuscript. Funding was provided by USDA-CRGO Ellsworth, D.S., and Reich, P.B. 1992. Leaf mass per area, nitrogengrant 86-FSTY-9-0214, and the USDA Forest Service, North content and photosynthetic carbon gain in Acer saccharum seed-Central Research Station. lings in contrasting forest light environments. Funct. Ecol. 6:

423--435.

Ellsworth, D.S:, and Reich, P.B. 1996. Photosynthesis and leaf hi-References trogen in five Amazonian tree species during secondary succes-

sion. Ecology, 77: 581-594.Abrams, M.D., and Kubiske, M.E. 1990. Leaf structural character- Gedroc, J.J., McConnaughay, K.D.M., and Coleman, J.S. 1996.

istics of 31 hardwood and conifer tree species in central Wiscon- Plasticity in root/shoot partitioning: optional, ontogenetic, orsin: influence of light regime and shade-tolerance rank. For. both? Funct. Ecol. 10: 44-50.

Ecol. Manage. 31: 245-253. Geiger, D.R. 1987. Understanding interactions of source and sinkAquirrezabal, L.A.N., Deleens, E., and Tardieu, E 1994. Root regions of plants. Plant Physiol. Biochem. 25: 659--666.

elongation rate is accounted for by intercepted PPFD and Gifford, R.M., and Evans, L.T. 1981. Photosynthesis, carbon patti-source-sink relations in field and laboratory-grown sunflower, tioning, and yield. Annu. Rev. Plant Physiol. 32: 485-509.Plant Cell Environ. 17: 443-450. Gower, S.T., Isebrands, J.G., and Sheriff, D.W. 1995. Carbon allo-

Belgrand, M., Dreyer, E., Joannes, H., Velter, C., and Scuiller, I. cation and accumulation in conifers. Chap. 7. In Resource phys-1987. A semi-automated data processing system for root growth iology of conifers: acquisition, allocation, and utilization. Editedanalysis: application to a growing oak seedling. Tree Physiol. 3: by W.K. Smith and T.M. Hinckley. Academic Press, New York.393--404. pp. 217-254.

Chapin, ES., III. 1991. Integrated responses of plants to stress. Hanson, P.J., Dickson, R.E., lsebrands, J.G., Crow, T.R., andBioScience, 44: 29-36. Dixon, R.K. 1986. A morphological index of Quercus seedling

Coleman, J.S., and McConnaughay, K.D.M. 1995. A non- ontogeny for use in studies of physiology and growth. Treefunctional interpretation of a classical optimal-partitioning ex- Physiol. 2: 273-281.ample. Funct. Ecol. 9: 951-954. Hanson, P.J., Isebrands, J.G., Dickson, R.E., and Dixon, R.K.

den Hertog, J., Stulen, I., Fonseca, E, and Delea, P. 1996. Modula- 1988a. Ontogenetic patterns of CO 2 exchange of Quercustion of carbon and nitrogen allocation in Urtica dioica and rubra L. leaves during three flushes of shoot growth. I. MedianPlantago major by elevated CO2: impact of accumulation of flush leaves. For. Sci. 34: 55-68.

nonstructural carbohydrates and ontogenetic drift. Physiol. Hanson, P.J., Isebrands, J.G., Dickson, R.E., and Dixon, R.K.

Plant. 98: 77-88. 1988b. Ontogenetic patterns of CO 2 exchange of Quercus

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Harmer, R. 1990. Relation of shoot growth phases in seedling oak Populus nigra x laurifolia clone. Photosynthetica, 17: 537-549.to development of the tap root, lateral roots and fine root tips. Pages, L., and Serra, V. 1994. Growth and branching of the taprootNew Phytol. 115: 23-27. of young oak trees--a dynamic study. J. Exp. Bot. 45: 1327-

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