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Photosynthesis, leaf area and productivity of 5 poplarclones during their establishment year

Ts Barigah, B Saugier, M Mousseau, J Guittet, R Ceulemans

To cite this version:Ts Barigah, B Saugier, M Mousseau, J Guittet, R Ceulemans. Photosynthesis, leaf area and produc-tivity of 5 poplar clones during their establishment year. Annales des sciences forestières, INRA/EDPSciences, 1994, 51 (6), pp.613-625. �hal-00882974�

Original article

Photosynthesis, leaf area and productivityof 5 poplar clones during their establishment year

TS Barigah B Saugier M Mousseau

J Guittet R Ceulemans 3

1 INRA, Station de Recherches Forestières, BP 709, 97387 Kourou cedex;2 Université de Paris XI, Laboratoire d’Écologie Végétale, Centre d’Orsay,

Bâtiment 362, 91405 Orsay cedex, France;3 Université d’Anvers, Département Biologie, UIA, Universiteitsplein 1, B-2610 Wilrijk, Belgium

(Received 3 November 1993; accepted 24 March 1994)

Summary — The stem volume and biomass (stem + branches) production, net photosynthesis ofmature leaves and leaf area production of 5 poplar (Populus) clones, Populus trichocarpa x deltoides(Raspalje and Beaupré), Populus x euramericana (Robusta) and P trichocarpa (Columbia River andFritzi Pauley), were studied during the first year of growth in an experimental high density plantation(15 600 plants ha-1). Significant differences were found in volume production, woody biomass production,total leaf area and net photosynthesis. Above-ground biomass production was 3.5 times higher inRaspalje than in Robusta. The best performing clones (Raspalje, Beaupré) were those with largeleaves, high leaf area index and high photosynthetic rates. A positive relationship between leaf photo-synthetic capacity and above-ground biomass production was also noted for 4 of the 5 clones. Theeuramerican clone Robusta was an exception, showing high photosynthetic rates, but low biomass pro-duction. This discrepancy was mainly due to the lower leaf area of this clone, and possibly also due toa larger carbon allocation to below-ground biomass (Barigah, 1991). The root/shoot ratios at the endof the first season in the clones Raspalje and Robusta were 1.23 and 1.79, respectively.

net photosynthesis / leaf area / biomass production / Populus

Résumé — Photosynthèse, surface foliaire et productivité de 5 clones de peuplier dans leur pre-mière année. Des plants issus de boutures de 5 clones de peuplier (Populus trichocarpa x deltoides(Raspalje et Beaupré), P x euramericana (Robusta) et P trichocarpa (Columbia River et Fritzi Pauley)ont été cultivés en peuplement dense (15 600 tiges ha-1). Des mesures d’assimilation de CO2 et de crois-sance (surface foliaire, volume de tiges, biomasse aérienne) ont été réalisées sur les jeunes plants. L’ac-cumulation de biomasse du clone le plus performant (Raspalje) représentait 3,5 fois celle observée dansle clone le moins performant (Robusta). Les clones les plus performants (Raspalje, Beaupré) étaientégalement caractérisés par une surface foliaire importante et une assimilation nette foliaire élevée. Lesdifférences de surface foliaire entre clones étaient liées à des différences de surface individuelle desfeuilles et non au nombre de feuilles par arbre, qui était quasi constant. La biomasse aérienne était posi-

tivement corrélée à la capacité photosynthétique foliaire pour 4 clones. Cependant le clone Robusta,de capacité de production faible, présentait une photosynthèse foliaire élevée. Cette faible productionde biomasse aérienne chez Robusta était due à un faible développement foliaire et probablementaussi à un investissement en biomasse racinaire important (Barigah, 1991) ; le rapport de la bio-masse racinaire à la biomasse aérienne était respectivement de 1,23 et de 1,79 pour les clones Ras-palje et Robusta.

photosynthèse foliaire / surface foliaire / production de biomasse / Populus

INTRODUCTION

Plant productivity depends on the interac-tion of light intercepting the leaf area of aplant and the intensity of the CO2 assimila-

tion process taking place in those leaves.The production of forest stands has beenshown to be strongly correlated with totalannual intercepted irradiance (Linder, 1984;Beadle and Long, 1985). Differences in theamount of leaf area displayed or in the inten-sity of the photosynthetic rate will result indifferent biomass productivity rates.

Photosynthetic capacity is known to varywidely among tree species, usually beinghigher in deciduous than in coniferous trees(Ceulemans and Saugier, 1991). In severaltree species, intensive selection for

increased biomass productivity has resultedin hybrids demonstrating heterosis for photo-synthetic performance (Isebrands et al,1988). Moreover, a positive correlationbetween photosynthetic capacity andbiomass productivity has already beendemonstrated for poplar hybrids (Ceule-mans and Impens, 1983; Michael et al,1990), larch hybrids (Matyssek and Schulze,1987) and different provenances of loblollypine (Boltz et al, 1986).

However, in many other cases, net

photosynthesis rate measurements havebeen found to be poorly correlated withgrowth rate and productivity, such as in thecase of Populus grandidentata, P tremu-loides and P smithii (Okafo and Hanover,1978; Reighard and Hanover, 1990). Theseconflicting results are due to the difficulty ofmeasuring the gas exchange rate on com-

parable leaves in different genotypes, tophenological and physiological changes dur-ing the growing season, and to the distri-bution of photosynthates within the tree. Forexample, some poplar clones retain greenleaves late in the fall with a measurable

photosynthetic production even after frosts,thus contributing significantly to a late sea-son stem diameter increment (Nelson et al,1982) and root growth (Isebrands and Nel-son, 1983).

In addition to photosynthetic rate, leafarea is also a very important determinantof biomass productivity. Comparing differ-ent spruce (Picea abies) provenances Grossand Hettesheimer (1983) found a negativecorrelation between leaf area and both

biomass production of the trees and CO2assimilation rate. The relationship betweenbiomass productivity and its determiningfactors may thus be complicated. Never-theless, variability in plant genotypes accord-ing to plant branchiness and leaf distribu-tion, position and orientation within the crowncould strongly influence the efficiency ofconversion of solar energy into biomass pro-duction (Isebrands and Nelson, 1982; Ise-brands and Michael, 1986). However, directlinear relationships between biomass pro-duction and solar radiation intercepted bythe foliage have been demonstrated in agri-cultural crops (Monteith, 1981) as well asin forest stands (Linder, 1984; Leverenz andHinckley, 1990). Although this simple rela-tionship appears robust in young planta-tions, its general and empirical approachhave been criticized (Byrne et al, 1986;Agren et al, 1991).

In this study, photosynthetic capacity,leaf area development, and biomass pro-duction rates of different kinds of poplar(Populus) clones were compared duringtheir first year of growth.

MATERIALS AND METHODS

Five poplar clones were used: 2 fast-growing andhigh-producing interamerican P trichocarpa x Pdeltoides hybrid clones (Raspalje and Beaupré);2 native American clones P trichocarpa (ColumbiaRiver and Fritzi Pauley); and 1 Populus xeuramericana clone (Robusta), which is oftenreferred to as the reference clone. The latter isthe result of a spontaneous hybridization betweenP deltoides and a European P nigra, presumablythe poplar clone Italica. The origin, sex, parentageand provenances (table I) of these clones havepreviously been described (Ceulemans andImpens, 1983; Ceulemans, 1990).

Hardwood cuttings of each of the 5 cloneswere planted on 8 April, 1987 in Orsay (48°50’N,2°20’E) near Paris, France, in monoclonal plots of4 x 4 m on a 0.8 x 0.8 m planting pattern (ie atree density of 1.56 plants per m2). All plots wereirrigated and fertilized. During the first growingseason 4 trees per clone were monitored weekly

for detailed measurements (height, diameter, leafdimensions, number of leaves, photosynthesis,stem height and diameter at 22 cm above theground). Measurements of young stem diameterat 22 cm above the ground was found to be agood compromise between the need for a mea-surement of the diameter close to the ground andthe necessity to eliminate stem distorsion causedby the connection of the roots. These 4 trees werechosen from the 9 interior trees and had oneborder row around them. Stem volume index wascalculated from height (H) and diameter (D) mea-surements as D2H. To estimate total leaf area

per tree (main stem), 80 leaves of surroundingtrees were harvested at different heights to mea-sure their leaf area, using a ΔT leaf area meter(Delta-T Devices, Burwell, Cambridge, UK), andtheir dimensions (length and width). The allometricrelationship between leaf dimensions and leafarea (table II) was then applied to monitor leafarea development of the 4 trees per clone. At theend of the first growing season, all trees includingthe border ones were harvested, because noborder effect was found between the plants in thefirst year for height or for volume index (Van Heckeet al, unpublished data). Leaf biomass and leafarea index (LAI) were estimated using leaf massper area data collected during the growing season.Wood volume (stems and branches) was mea-sured by immersion in water, and wood biomasswas measured at harvest after oven-drying at

80°C for 15 d. Since the dimensions of the plotswere rather small, these biomass values were

only used to compare the performance of thevarious clones and were not representative ofthe biomass production of real stands.

Leaf net photosynthetic rates and incidentphotosynthetic photon flux density (PPFD) weremeasured in the field using an ADC Parkinsonleaf chamber connected to a portable CO2 ana-

lyzer (ADC Company Ltd, Hoddedson, UK) in anopen system arrangement. The leaf chamber wassupplied with an air mixture of a known CO2 con-

centration from a compressed air cylinder, andthe CO2 drop in the chamber was 79 ± 21 vpm.To avoid differences in photosynthetic rates dueto the variation of the CO2 concentration, which

ranged from 360 to 385 vpm in the air containedin different gas cylinders, net photosynthesis at350 vpm (A350) was calculated using the formula:

This formula assumes a linear relationshipbetween net photosynthesis (A) and CO2 con-

centration (C) (Gaastra, 1959), and a constantCO2 compensation point (Γ). This relationshipwas established in the laboratory at 22°C and israther insensitive to variations in r, since a dif-ference of 20 vpm in Γ ronly caused a 2% variationin A350 using Γ equal to 60 vpm.

Only fully expanded leaves having maximumphotosynthetic rates (Barigah, 1991) were usedfor gas exchange measurements and all experi-ments were performed on single attached leaves.

Measurements were made on several sunny daysthroughout the growing season. The data wereplotted in a CO2 assimilation (A) versus PPFDgraph and were fitted using rectangular hyper-bola equation (A = {α•PPFD•Amax/(α•PPFD +Amax)}; where a is the photochemical efficiency,and Amax is the asymptotic value of A at satu-rating irradiance. Leaf photosynthetic capacitywas defined here as the PPFD-saturated net pho-tosynthesis at an atmospheric CO2 concentra-

tion of 350 vpm. Differences among clones in

photosynthetic capacity were assessed using a t-test after comparing confidence intervals at the95% level.

RESULTS

Growth patterns

The total tree height after the first growingseason ranged from 1.8 m for clone Robustato 3.5 m for clone Beaupré (table III). The 2P trichocarpa x P deltoides clones (Beaupréand Raspajle) were superior to the otherclones with regard to tree height, whileclones Columbia River, Fritzi Pauley andRobusta had similar heights around 2.0 m.Stem volume index values (fig 1) increasedfor all clones from the beginning of thegrowing season until mid-October (day 288),except for clone Robusta (Barigah, 1991)which ended extension growth early inSeptember (day 259). At the end of the firstgrowing season, the ranking of the clones interms of stem volume index was in agree-ment with that observed in height growthexcept for clones Columbia River and FritziPauley.

Clone Beaupré had the highest wood vol-ume production (732 cm3, table III), but thehighest biomass (stem + branches) was pro-duced at the end of the first season by cloneRaspalje, a branchy clone (table III). Thefasted growing clone Raspalje produced 3.5times more woody biomass than the slowestgrowing clone Robusta.

The proportion of biomass allocation tothe leaves was nearly the same for allclones, ranging from 28% of total biomassfor clone Beaupré to 36% in clone Robusta(table III). The ratio stem volume

index/actual wood volume almost constant

(0.41) among genotypes, which confirmsthe relevance of using D2H as an index ofwood production.

Photosynthetic characteristics

The relationships between CO2 assimila-

tion rate (A) and PPFD did not show a veryclear saturation level, even at PPFD valuesof 2 000 μmol m-2 s-1 (fig 2). However,

since A increased only slightly between1 300 and 2 000 μmol m-2 s-1, the valuesrecorded over this range were considered as

the maximum net photosynthesis by takingmean value of individual photosynthesis rateof several leaves.

The highest values of photosyntheticcapacity (defined as A at saturating PPFDand 350 vpm CO2) were observed for clonesBeaupré, Raspalje and Robusta (between25.0 and 27.2 μmol m-2 s-1). Significantlylower values of A were found in the 2 P tri-

chocarpa clones, Columbia River and FritziPauley (17.5 and 19.2 μmol m-2 s-1, respec-tively). Differences among clones Beaupré,Raspalje and Robusta were not significant atthe p = 0.05 level.

Leaf area characteristics

Clones Raspalje and Beaupré had the high-est leaf area values per tree at the end of the

growing season (table III); the lowest valueswere observed in Robusta and the values in

Columbia River and Fritzi Pauley were inter-mediate. At mid-August of the first year LAIvalues were 2.75 and 2.95 in clones

Beaupré and Raspalje, respectively, andonly 0.8 for clone Robusta. Significant dif-ferences in the leaf area distribution overmain stem and branches (table III) wereobserved for the studied clones.

The results (table III) showed that in allclones more than half of the total leaf area

was produced on the main stem (the branchleaves were not numerous and were smaller

than the main stem ones). However Bari-gah (1991) observed early in September1989 that the branch leaf area was 3 times

higher than the main stem leaf area in cloneRaspalje and 1.4 times in clone Robusta.

Clone Robusta had the largest number ofleaves on the main stem after the first grow-

ing season (64 leaves), and clone FritziPauley the smallest (48 leaves), but cloneRobusta had the smallest average individual

leaf area with 66 cm2 versus 201 cm2 for

clone Raspalje and 254 cm2 for clone

Beaupré (table III).

DISCUSSION

In terms of woody biomass and stem volumeproductivity, the 2 P trichocarpa x P del-toides clones Beaupré and Raspalje, wereclearly superior to the other 3 clones. Thehigher productivity of these 2 clones can beexplained by both their significantly largerleaf area production (thus, higher LAI) andtheir higher photosynthetic performance.Indeed by ranking the different parametersreported in table III, the correlation betweennet photosynthesis, leaf area and biomass

production becomes evident. The P tri-chocarpa clones, Columbia River and FritziPauley, had the lowest photosynthetic ratesas well as a low leaf area production (thus,low LAI), resulting in a low biomass pro-ductivity (fig 3, table III).

For 4 out of the 5 poplar clones the maxi-mum net photosynthesis was significantlycorrelated with above-ground biomass pro-duction (fig 3). Net photosynthetic rate hasoften been reported not to be correlated withyield (Ledig, 1969; Gifford and Evans, 1981);the reasons for these weak correlations

seems to be inadequate or varying nitrogenand water supply, lack of standardisation ofphotosynthetic measurements (eg, leaf age),plant density, and number of comparablereplications. The high maximum net photo-synthesis values of the P trichocarpa x Pdeltoides clones were of a comparable orderof magnitude to those previously reportedfor similar poplar hybrids (Isebrands et al,1988; Ceulemans, 1990), while the low pho-tosynthetic performance of the 2 P tri-chocarpa clones (Columbia River and FritziPauley) is also in agreement with previousobservations (Ceulemans, 1990).

Clone Robusta was the only clone thatcombined a rather high photosynthetic rate(comparable to clones Beaupré and Ras-palje) with a low volume and a low above-ground biomass production (fig 3). This canbe mainly explained by its low leaf area pro-duction and low LAI, but also by the factthat the clone Robusta had a proportionallylarger allocation to below-ground biomass.For example, at the end of the first growingseason the root/shoot ratio was 1.23 forclone Raspalje and 1.79 for Robusta (Bari-gah, 1991). Similar observations (weak cor-relation between net photosynthetic rateand wood biomass productivity, and signifi-cant differences in root/shoot ratio) havealready been made for the same clones(Impens, 1988) as well as for other poplarclones and species (Okafo and Hanover,1978; Reighard and Hanover, 1990). The

ecological significance of the difference inthe root/shoot ratio is still uncertain as there

is very little knowledge about the specificroles root compounds play in tree survival,growth and development (Loescher et al,1990). Cannell et al (1988) found that, com-pared to willow trees (Salix viminalis), bal-sam poplar (P trichocarpa) stored muchmore biomass in their roots than above

ground (the above-ground biomass andbelow-ground biomass were respectively14 t ha-1 and 3 t ha-1 for the willow, and8 t ha-1 and 4 t ha-1 for the poplar). Cannellet al (1988) stated that the abundance ofbiomass found in the roots of the balsam

poplar was a clonal characteristic, but infact this characteristic is also very common

in the Populus genus (Isebrands, 1982;

Reighard and Hanover, 1990) and in othergenera like Malus, Prunus, Acerand Pinus

(Heim et al, 1979; Kramer, 1986; Loescheret al, 1990). Furthermore, Blake and Raita-nen (1981) and Afocel (1983) consideredthe first growth cycle for cuttings to be poorlyproductive due to greater biomass alloca-tion to root establishment than to above-

ground biomass structures.As the high root/shoot ratio observed in

clone Robusta was not directly reflected in itsabove-ground growth, the abundant reservesstored in the root system of Robusta mightbe the support for the high root respirationrate observed in this clone (Barigah, 1991)and/or for drought adaptation or resistance todiseases. However, these factors were notmonitored in this study.

The best performing clones (Beaupréand Raspalje) seem to be those which notonly develop the largest leaf area and havethe largest LAI, but also those with the high-est individual leaf size (fig 4). The high totalbiomass production of clone Raspalje mightthus mainly be due to its large total and indi-vidual leaf area (Ridge et al, 1986). CloneRaspalje produced not only slightly morebranches and leaves than clone Beaupré,but also a much higher leaf area per tree.However, individual leaf size of clone

Beaupré was slightly larger than that of Ras-palje (table III, fig 4). The larger number ofbranches in clone Raspalje seemed to resultin a larger biomass production, although itsmain stem volume production was slightlyinferior to that of clone Beaupré. It thus

seems that poplar clones with a larger indi-vidual leaf area and a high number of leaveson their branches might have considerableadvantages in developing a high total leafarea per tree early and rapidly during theirfirst growing season, and consequently ahigh LAI.

A striking feature of the fast-growing P tri-chocarpa x P deltoides hybrids remains theirlarge individual leaf size (fig 4B). Earlierexperiments with a variety of these hybridshave already shown that stem volume andstem biomass production were more closelyrelated to individual leaf size than to the

number of leaves produced per tree (Ridgeet al, 1986). The correlation between woodybiomass and individual leaf size (fig 4B)might suggest that the inheritance of fast-growing, large leaves cause the observedincrease in stem biomass (and stem vol-ume) of the P trichocarpa x P deltoideshybrids. However, this relationship needsto be examined over a wide range of F1, F2and backcross material so that the mecha-

nisms associated with it can be understood.

The positive correlation between netphotosynthesis and first year (above-ground)biomass production for 4 of the 5 studyclones, as well as the extended leaf area

duration of some clones due to late leaf

senescence, guarantee high above-groundgrowth in poplar. A significant difference inleaf area duration between the clones

Robusta (568 m2 d m-2) and Beaupré (927m2 d m-2) during their second growing sea-son has been reported previously (Nelsonand Isebrands, 1983; Mau and Impens,1989; Ceulemans et al, 1993).

In breeding and selection programmesfor fast-growing and highly productive poplarclones, attention should be paid to a numberof physiological, morphological and envi-ronmental factors (Magnussen, 1985; Ceule-mans et al, 1987), to soil water regime andnutrient availability (Garbaye, 1979; Gar-baye, 1980; Hinckley et al, 1990) as well asto the inheritance of late retention of greenleaves in the fall with a measurable photo-synthetic production even after frosts (Nel-son et al, 1982).

In conclusion, we believe that high netphotosynthetic rates, in combination withlarge leaf area production and duration, ledto the high biomass production of fast-growing clones Beaupré and Raspalje dur-ing their establishment year.

ACKNOWLEDGMENTS

This research was carried out within the frame-

work of a EEC research project (contract EN3B-0114-B/GDF to I Impens, UIA). The authors thankB Legay, JY Pontailler, J Liebert and JM Dreuil-laux for their help with collection of the experi-mental data. R Ceulemans is a Senior ResearchAssociate of the Belgian National Fund for Scien-tific Research (NFWO, Brussels).

REFERENCES

Afocel (1983) Production de Biomasse : Taillis à CourteRotation. Assoc For Cell, Nangis, France, 214 p

Agren GI, McMurtrie RE, Parton WJ, Pastor J, ShugartHH (1991) State-of-the-art of models of produc-

tion-decomposition linkages in conifer and grass-land ecosystems. Ecol Appl 1, 118-138

Barigah TS (1991) Étude du bilan carboné de 2 clonesde peuplier à croissance contrastée. Thèse de Doc-torat en Sciences, Université Paris-Sud, Orsay,France, 194 p

Beadle CL, Long SP (1985) Photosynthesis- is it limitingto biomass production? Biomass 8, 119-168

Blake TJ, Raitanen WE (1981) A Summary of FactorsInfluencing Coppicing. IEA Rep NE-1981:22. NatSwedish Board for Energy Source Develop, Stock-holm, Sweden, 24 p

Boltz BA, Bongarten BC, Teskey RO (1986) Seasonalpatterns of net photosynthesis of lobolly pine fromdiverse origins. Can J For Res 16, 1063-1068

Byrne GF, Landsberg JJ, Benson ML (1986) The rela-tionship of above-ground dry matter accumulationby Pinus radiata to intercepted solar radiation and soilwater status. Agric For Meteorol 137, 63-73

Cannell MGR, Sheppard LJ, Milne R (1988) Light useefficiency and woody biomass production of poplarand willow. Forestry 61, 125-136

Ceulemans R (1990) Genetic Variation in Functionaland Structural Productivity Determinants in Poplar.Thesis Publishers, Amsterdam, The Netherlands,101 pp

Ceulemans R, Impens I (1983) Net CO2 exchange rateand shoot growth of young poplar (Populus) clones.J Exp Bot 34, 866-870

Ceulemans R, Saugier B (1991) Photosynthesis. In:Physiology of Trees (AS Raghavendra, ed) JohnWiley & Sons, New York, USA, 21-50

Ceulemans R, Impens I, Steenackers V (1987) Varia-tions in photosynthetic, anatomical, and enzymaticleaf traits and correlations with growth in recentlyselected Populus hybrids. Can J For Res 17, 273-283

Ceulemans R, Pontailler JY, Mau F, Guittet J (1993)Leaf allometry in young poplar stands: reliability ofleaf area index estimation, site and clone effects.Biomass Bioenergy 4, 315-321

Gaastra P (1959) Photosynthesis of crop plants as influ-enced by light, CO2 temperature, and stomatal dif-fusion resistance. Meded Landbouwhogesch,Wageningen 59, 1-68

Garbaye J (1979) Sol et productivité des Peupliers ’I214’et ’Robusta’ en populiculture traditionnelle dans leNord du Bassin Parisien. Ann Sci For 36, 39-58

Garbaye J (1980) Nutrition minérale et production despeupliers ’Robusta’ et ’I214’ en populiculture tradi-tionnelle dans le Nord du Bassin Parisien. Ann Sci

For 37, 159-172

Gifford RM, Evans LT (1981) Photosynthesis, carbonpartitioning, and yield. Annu Rev Plant Physiol 32,458-509

Gross K Von, Hettesheimer W (1983) VergleichendeGaswechselmessungen an schnell und langsamwachsenden 18-jährigen Fichten untersschiedlichergeographischer Provenienz. Allg Forst Jagdztg 154,133-139

Heim G, Landsberg JJ, Watson RL, Brain P (1979) Eco-physiology of apple trees: dry matter production andpartitioning by young golden delicious trees in Franceand England. J Appl Ecol 16, 179-194

Hinckley TM, Braatne J, Ceulemans R et al (1993)Growth dynamics and canopy structure. In: Eco-physiology of Short Rotation (CP Mitchell, JB Robert-son, TM Hinckley, L Sennerby-Forsse, eds). Else-vier Science Publishers Ltd, London, UK, 1-34

Impens I (1988) Leaf photosynthesis, foliage canopystructure and resultant biomass production in severalfirst year poplar clones. Proc Euroforum Saarbrüken,24-28 October, New Energies Congress 3, 440-442

Isebrands JG (1982) Toward a physiological basis ofintensive culture of poplar. Proc TAPPI Res DevelDivision Conference. Ashville 29 August-1 st Septem-ber, 81-90

Isebrands JG, Nelson ND (1982) Crown architecture ofshort rotation intensively cultured Populus. II. Branch

morphology and distribution of leaves and specificleaf weight within the crown of Populus ’Tristis’ asrelated to biomass production. Can J For Res 12,853-864

Isebrands JG, Nelson ND (1983) Late-season photo-synthesis and photosynthate distribution in an inten-sively-cultured Populus nigra x P laurifolia clone.Photosynthetica 17, 537-549

Isebrands JG, Michael DA (1986) Effects of leaf mor-phology and orientation on solar radiation intercep-tion and photosynthesis in Populus. In: Crown andCanopy Structure in Relation to Productivity (T Fuji-mori, D Whitehead, eds), Tsuksba, Japan, 359-381

Isebrands JG, Ceulemans R, Wiard BM (1988) Geneticvariation in photosynthetic traits among Populusclones in relation to yield. Plant Physiol Biochem 26,427-437

Kramer PJ (1986) The role of physiology in forestry.Tree Physiol 2, 1-16

Ledig FT (1969) A growth model for tree seedlings basedon the rate of photosynthesis and the distribution ofphotosynthate. Photosynthetica 3, 263-275

Leverenz JW, Hinckley TM (1990) Shoot structure, leafarea index and productivity of evergreen coniferstands. Tree Physiol 6, 135-149

Linder S (1984) Potential and actual production in Aus-tralian forest stands. In: Research for Forest Manage-ment (JJ Landsberg, W Parsons, eds). CSIRO, Mel-bourne, Australia, 11-35

Loescher WH, McCamant T, Keller JD (1990) Carbo-hydrate reserves, translocation, and storage in woodyplant roots. Hort Sci 25, 274-281

Magnussen S (1985) Growth, transpiration, unit leaf rateand water use efficiency of six poplar clones at dif-ferent light and temperature regimes. For Tree Improv18, 1-47

Matyssek R, Schulze ED (1987) Heterosis in hybrid larch(Larix decidua x leptolepis). II. Growth characteristics.Trees 1, 225-231

Mau F, Impens I (1989) Comparative growth analysisof five first year establishment poplar clones (Popu-lus sp) grown under a short-rotation intensive cul-ture system. Ann Sci For 46, 250s-255s

Michael DA, Dickmann DI, Isebrands JG, Nelson ND(1990) Photosynthesis patterns during the establish-ment year within two Populus clones with contrast-ing morphology and phenology. Tree Physiol 6, 11-27

Monteith JL (1981) Does light limit crop production? In:Physiological Processes Limiting Plant Productivity(CB Johnson, ed). Butterworths, London, UK, 23-38

Nelson ND, Dickmann DI, Gottschalk (1982) Autumnalphotosynthesis in short-rotation intensively culturedPopulus clones. Photosynthetica 16, 321-333

Nelson ND, Isebrands JG (1983) Late-season photo-synthesis and photosynthate distribution in an inten-sively cultured Populus nigra x laurifolia clone. Photo-synthetica 17, 537-549

Okafo OA, Hanover JW (1978) Comparative photosyn-thesis and respiration of trembling and bigtoothaspens in relation to growth and development. ForSci 24, 103-109

Reighard GL, Hanover JW (1990) Shoot and root de-velopment and dry matter partitioning in Populusgrandidentata, P tremuloides and P x smithii. CanJ For Res 20, 849-852

Ridge CR, Hinckley TM, Stettler RF, Van Volkenburgh E(1986) Leaf growth characteristics of fast-growingpoplar hybrids Populus trichocarpa x P deltoides.Tree Physiol 1, 209-216