Journal of Tropical Forest Science 11(1):132-147 (1999)

EFFECTS OF IRRADIANCE AND SPECTRAL QUALITY ON SEEDLINE TH G DEVELOPMEN JELUTONF TO G (DYERA COSTULATA)

David W. Lee, Steven F. Oberbauer,

Department of Biological Sciences, Florida International University and Fairchild Tropical Garden, Miami, Florida 33199, United States of America

B. Krishnapillay, M. Haris, M. Marzalina & S. K. Yap

Forest Research Institute of Malaysia, Kuala Lumpur 52109, Malaysia

Received September 1997______

, OBERBAUERLEEW. . D , , KRISHNAPILLAYF. . S , , HARISB. , MARZALINA, M. , , M. &YAP, S. K. 1999. Effects of irradiance and spectral quality on the seedling development of jelutong (Dyera costulata). Jelutong [Dyera costulata (Miq.) Hook. f., Apocynaceae] is a long-lived pioneer tree that eventually becomes a giant emergent e raiith nn forest f Peninsulao s r Malaysi d Sumatraan a e conducteW . d trialo t s determine responses of growth, morphology, leaf anatomy, architecture and physi- olog jelutonf o y g seedling differeno t s t irradiances (photon flux density, 400-700 nm, PFD) and spectral qualities (red/far-red quanta, or R:FR). Seedlings were grown in six replicated treatments: (1) direct sunlight and 1.25 R:FR; (2) 40 % solar PFD and 1.25 R:FR; (3) 13 % PFD and 1.25 R:FR; (4) 10 % PFD and 0.25 R:FR; (5) 3 % PFD and 1.25 R:FR; and (6) 3 % PFD and 0.25 R:FR. Based on dry mass increments, final height, collar diameter, architecture, and maximum photosynthe- sis, seedlings grew most rapidly in the 40 % sunlight treatment, and varied little in respons lowo t d emedium-PF -an D environments. Spectral t qualitno d ydi influence growth and development very much, but low R:FR reduced leaf allocation aread reduced an an , d growt mass/days a h . Leaf anatom physiologd an y y were influenced exclusively by PFD. These results are consistent with observations of jelutong seedlings being shade-tolerant, slow growing, stunted in direct sunlight, and dramatically differen theio t t r behaviou laten i r r developmental stage d thaf an so t short-lived pioneers.

Key words: Seedlings - photosynthesis - development - pioneer - rain forest - red/far- red ratio - allocation - shade - Malaysia

LEE, D. W., OVERBAUER, S. F., KRISHNAPILLAY, B., HARIS, M., MARZALINA, M. & YAP, S. K. 1999. Kesan sinaran dan kualiti spektrum terhadap perkembangan anak benih jelutung (Dyera costulata).]elutung [Dyera costulata (Miq.) Hook. f., Apocynaceae] adalah pokok perintis yang panjang hayatny akan ada n menjadi pokok gergasi d i hutan huja Semenanjuni d n g Malaysi n Sumatraada . Kami membuat ujian untuk menentukan tindak balas pertumbuhan, morfologi, anatomi daun, binaan dan fisiologi anak benih jelutung terhadap sinaran yang berbeza (keamatan fluks-foton, 400-700 nm, PFD) dan kualiti spektrum (kuantum "red/far-red," atau R:FR). Anak benih ditana i enamd m rawatan yang diulang cahay) (1 : a matahari secara terun sda

132 Journal of Tropical Forest Science 11(1):132-147 (1999) 133

1.2n da 5 cahay% D D R:FR1.2 10 1.2PF n PF ) 5ada (4 % ;5 R:FR% R:FR40 13 ) ) (2 ;(3 ; n 0.2da 5 D R:FRPF . % n 1.23 ) da 5 (6 D R:FR 0.2n n PF da 5da ; % D R:FR3 PF ) (5 ; Berdasarkan pertambahan biojisim kering, ketinggian akhir, garis pusat kolar, binaan, dan fotosintesis maksimum, anak benih didapati tumbuh paling cepat dalam 40 % rawatan cahaya matahari n sedikida , t berubah-ubah tindak balasnya terhadap persekitaran yang mendapa pertengahanD rendaD PF PF tn hda . Kualiti spektrum tidak begitu mempengaruhi pertumbuha perkembangan nda n pokok, tetapi R:FR rendah akan mengurangkan pengagihan daun dan luas daun, serta mengurangkan pertumbuhan sebagai jisim sehari. Anatomi dan fisiologi daun dipengaruhi oleh PFD. Keputusa i adalanin h tetap dengan cerapan terhadap anak benih jelutung yang toleran-teduhan, lambat tumbuh, terbantut dalam cahaya matahari terusn da , tabiatnya berbeza secara mendadak pada peringkat perkembangan seterusnyn da a juga dalam spesies perintis yang mempunyai hayat yang pendek.

Introduction

In tropical forest succession the first trees to establish after disturbance are pioneers. Such trees typically occu largn ri e gaps light-demandinge ,ar plastie ,ar c in respons ligho et t conditions, photosynthesise rapidlyrelativele ar d an , y short- lived (Bazzaz & Pickett 1979). Their growth and physiology have been contrasted with those of more shade-tolerant mature phase trees (Bazzaz & Pickett 1979, Fetche l 1983a t re , Turne . 1992al t re , Whitmore 1996). However tropican ,i l rain forests some pioneer short-livet no e sar de treesar t ,bu long-lived and eventually attain the canopy in mature forest (Whitmore 1984). Jelutong [Dyera costulata (Miq.) Hk. f.] is such a tree, occuring in tropical rain forests of Peninsular Malaysia and Sumatra. Jelutong grows to heights of 60 m and is among the more common non-dipterocarp emergents (Corner 1988). Its previous value as a latex tree and present exploitation as a non-durable but attractive timber has led to careful observation of its silvicultural characteristics (Watson 1934, Burkill growto 1966t d )an h trial plantatior sfo n forestry (Appanah & Weinland l993). These observations suggest a growth pattern quite different to that of typical early successional trees. Although Jelutong grows rapidl saplina s ya tre d gan e (Appana Weinlanh& d 1993) t appeari , groo t s w e slowlseedlinth t ya g stage, tolerant of shade. It is capable of persistence in a stunted condition and recovery from damage by falling branches (Aminuddin 1982). Yet, seedlings are present in the earliest stages of succession. Whitmore (1973) observed a deficiency in size classes between seedling adultd san naturan si l populations. Aminuddin (1982) grew seedlings in artificial shadehouses at 21,33, 55, 88, and 100% of full sunlight. He observed maximum height and collar diameter in seedlings grown at 33% of sunlight. However, these shading trials only spannee th f e uppeo dth d en r rang f conditioneo s experience seedlingy db naturaa n i s l forest environment (Chazdon et al. 1996). Aminuddin concluded that Jelutong is a relatively light- demanding species that grows best under partial shade. 4 13 Journal of Tropical Forest Science (1)1 1 : 132-147 (1999)

Although soil nutrition and water relations maybe important in determining the relative success of tree seedlings, light is the dominant ecological factor in the rain forest environment (Whitmore 1996). Seedlings growin gradiene th n gi f o t shade microclimates withi forese nth t experience dramatic change irradiancn si e (normally define photosynthetis da c photon flux density, 400-70 PFD)r o , s 0a ,nm well as spectral quality [best described as the ratio of red to far-red quanta, or R:FR (Smith 1994)]. Foliage densit parallea canopd n i yan R F l: y R gap d san alteD rPF manner (Lee 1987, Chazdo 1996). al t ne . Reduced R:FR influences phytochrome equilibria in plant tissues, and induces a variety of developmental responses (Smith 1994). Until recently virtually all research on plant shade responses has manipulate withouD dPF t altering R:FR, thus exposing seedling vere w th y lo o st PFD of rain forest shade and the spectral quality of sunlight. Such research underestimates shade response e naturath n i s l environment (Schmit Wulf& t f 1993). Morga Smitd nan h (1979) demonstrate significanda t increas internodn ei e expansion among shade-intolerant taxa in a systematic survey of European herbs. They postulated that shade-intolerant taxa should generally exhibit a greater response to shifts in R:FR than shade-tolerant taxa. Kwesiga and Grace (1986) concluded that different growth response n seedlingi s f Khayao s senegalensis and Terminalia ivorensis under low R:FR were consistent with this hypothesis. Thus, light-demanding, rapidly-photosynthesising, and fast-growing pioneer species are predicted to be strongly influenced by shifts in R:FR. The evidence concerning this hypothesis is mixed. Lee et al. (1996a) included two early successional species, Endospermum malaccense Parkiad an javanica, thein i r studf yo seedlin gAsia R:Fx d responsesi an y Rnb D raiPF n o sforest t species. Thes taxo eatw varied in developmental responses to light conditions, but only the former species was strongly influenced by R:FR. Most of the research on the influence of PFD and R:F n seedlinRo g functio s examineha n d photosynthetic characteristics, with relatively little influence of R:FR (Turnbull 1991, Kamaluddin & Grace 1992, Kitajima 1994, Tinoco-Ojanguren & Pearcy 1995). Kitajima (1994) detected no effect f reduceo s d R:F plann Ro t growt allocatiod han n pattern thirteen si n taxa. Thre f theso e e were shade-intolerant pioneers, including Ochroma pyramidale. Sasaki and Mori (1981) reported increases in height and internode lengths of seedlings in Shorea ovalis, a shade-tolerant mature forest species. Lee (1988) observed significant developmental response reduceo st d R:F thren Ri e relatively shade-tolerant tropical vines, with specific morphological patterns varyin- gbe tween species. Learning how rain forest tree seedlings respond to the two aspects of shadelight, photon flux densit spectrad yan l quality, will hel understans pu individuaw dho l specie adaptee sar conditiono dt raie th n n sforesti neee studW .o d t y more species, assessing the separate and interactive effects of PFD and R:FR on seedling develop- ment value Th conductinf . eo g researc seedlinge th n ho s of jeluton increases gi d by its unique behaviour: the slow initial growth even in high light conditions, the persistenc understoryn ei rapie th dd growtan , saplina s h a tree d gan . In this researc employee hw e experimentadth l. systeal t e me Le use y db (1996a,b) to study seedling development in other tropical Asian forest species. This Journal o5 f Tropical13 Forest Science 11(1):132-147 (1999)

system manipulate R:F d simpla an n Ri D e sPF factoria l design that permite th s assessmen contributionf to thesf sfactoro o etw plano st t growth, developmend tan physiology. What is the response of jelutong seedlings to shade conditions? How significan R:Fs i t controllinRn i g development anatomicao d w Ho ?morphod lan - logical characters help to explain the observed physiology and growth responses? Ho theswo d e responses correspon actuae th o dt l performanc speciee e th f th e o n si forest? We sought answers to these questions in our study.

Material methodd san s

Seed f Dyeraso costulata were obtained fro mtrea e population establishee th t da Forest Research Institute of Malaysia (FRIM) Arboretum, from seeds collected earlier this century from forest site Malaysian si . Seeds were germinate growd dan n in shallow trays, transferred to poly bags, and grown until 12-15 cm height for approximatel month2 shadey1 % 90 t .sa Extra timneedes ewa d because th f eo delayed germinatio f Jelutonno g seeds. Forest soil, red-yellow ultiso Rengae th f lo m series (a friable sandy loam of good fertility) was used in the initial growth and all shade trials. Seedlings were transferred to plastic pots with 8.3 1 of soil volume. These pots were fertilised with 3g Osmocote 9:14:19 containing 0.2 g MgO at the beginning of the trials. Plants were watered regularly to maintain the soil near fiel analyst d no capacity d edi roote f W adul. o s r tseedling treeou r o s r sfo presence th f mycorrhizae eo speciee t knoth no f wi o s d benefite w ; s fromr o , requires, these fungi. If required, the forest soils may have been adequately inoculate infeco dt rooe th t t system seedlingsf so . We constructed replicates of five shadehouse environments, plus one full sunlight treatment, for a total of 12 treatments. Each shadehouse was 4 X 4 m wit hrooa f line slopin g2.0mo t fro 5 m2. . Externa pulles wa r d lai throug h blind vents inte houseoth s e roowit th n exhaus fa ht a peak e continualln W fa t . y monitored PFD and temperature in the open and in the centre of the houses at heighm 1 t using Li-185s quantum sensors (LI-COR Inc, Lincoln 68504E ,N d )an Campbell thermistor probes attache Campbelo dt l CR-10 dataloggers (Campbell Scientific Inc, Logan 84321)T U , temperaturee Th . housee th n si s were compa- rable, and within 3 °C of ambient on the hottest afternoons (36 °C). Light conditions in the shadehouses were controlled by a combination of shade fabrics and energy films. Energy films reducing PFD to an equivalent extent and absorbing UV-B wavelengths, and altering R:FR differently, were supplied by CorporationM 3 e th . Paul 55144St N , M , . Metal sputter-coated films (RE20) shaded approximatel withouD PF f o t changin% y85 g R:FR dye-impregnated an , d films (NR20) reduced the R:FR to approximately 0.25 with a similar degree of shading. Additional shadin s achievewa g y coverinb d g those enclosures with shade fabric e measureW . d spectral quality wit a Li-180h 0 spectroradiometer (LI-COR Inc, Lincoln 68504)E N , , with R:FR define Smitn i s a dh (1994)d an , spectral quality did not change at the beginning, middle and end of the experi- ments (Tabl . Mea1) e n dail weryD totalPF e f useo s determino dt e lighth e t condition e duratioth r fo sf eac o n h growth triale constructeW . d five shade 136 Journal of Tropical Forest Science 11 (1): 132-147 (1999)

treatments (Table 1): (1) 40% solar PFD and 1.30 R:FR, HRR; (2) 14% PFD and 0.21.30R:FR,MRRd l.3d an 4 an 1 R:FR,MFRD R:FRD PF PF % ,% 0 LRR3 1 ) ) (4 ;;;(3 and (5) 3% PFD and 0.23 R:FR, LFR. We also grew seedlings in direct sunlight at an adjacent site, SRR. Replicates of these six treatments were randomly located on the roofs of two adjacent buildings, for a total of twelve treatments. potten Te d seedling 12-1f so heighm 5c t were placed gri 9 randoml y db 9 a n yo within each shadehouse apartm theid 4 ,0. ,an r initial heights were measured. Five seedlings were dried and weighed just before the growth trials, for comparison to treatments. Seedlings grew in the shadehouses for 429-441 days (12 days were required to complet e harvest)th e e harvesteW . d seedlings whe e talles th nd reache ha t d approximatel heightn i eacr m c Fo .h0 y5 seedlin measuree gw fina) d(1 l height; (2) diamete mast y collara r dr leaf so ) f (3 ;blades , petioles, stems rootsd an ,) (4 ; leaf area internod) (5 ; e distance petiol) (6 ; e length numbe) (7 ; internodef ro n si branches and main axis; (8) and total stem length. These measurements allowed calculatioe th photonf o l f growtno mo sr mass receivedhpe a r so increasy .da r epe We also calculated quantitative indicators of plant structure and architecture: (1) stem robustnes s stea s m mass/length ) tota(2 ; l leaf area/stem length) (3 ; specific leaf mass; (4) mean leaf area; and (5) allocation to seedling organs. The degre f branchino e s estimategwa countiny b d e internodegth l lateraal n i sl branches compared to those in the main axis. We analysed a maximum of ten plant eacr sfo h treatment numbere ;th s were reduce somn di e treatments because of the occasional loss of seedlings (Table 1). A few seedlings failed to grow and a few died. We grew five seedlings in the direct sunlight treatments (SRR) and lost treatmentsiR x seedlingMR e unknowr on fo , n si n reasons.

measuree W d light-saturated photosynthesis (Amax), stomatal conductanced ,an dark respiration (Rdark), usin gLI-COa R LI-6200 photosynthesis system 0.2a d 5 an L cuvette mounte tripoda n chosde o youngesW e . eth t fully mature lea eacf fo h seedlin r thesfo g e measurements removee W . d plants fro shadehousee mth t sa leas e hou on t n advanci r measurementf o e allowed an s d the equilibratmo t e under shade fabric or open sky at light levels near saturation (400-600 umol m-2s -1PFD) .W e constructed preliminary light response curves to determine the level whict a s plante hth s were saturated completee W . finae dth l measurements lateo n r tha afteh n2 r solar noon t 400-100a , 0 umoPFDs l.m LFR LRRd -an - 1 - 2 - treated seedlings were exposed to the lesser intensity and all other treatments at highee th r intensity regulatee addinW y . b D gdPF layer shadf so e fabric. Cars ewa take avoio t n d exposin lighw glo t grown plant minimiso t higo D t s e hPF th e possibilit f photoinhibitionyo measuree W . d photosynthesis depletiowits 0 h1 n times, three periods per measurement. We repeated measurements until steady values were obtained e mixeW . d treatment timed san minimiso st effecy ean f o t time of day on the measurements. We estimated leaf areas by tracing enclosed parts leavee ofth tracinn so g paper, weighing thed an ,n convertin areao gt .

measuree W d R darkenea dar n ki d room, adjacen shadehousese th o t . Plants were equilibrate dare th ko d t condition least completn a i min r 0 d t2 s fo ,an e darknest sa Journal o7 f Tropical13 Forest Science 11(1):132-147 (1999)

prion leas mi measuremento t r5 t r Fo usee . e samW dth . eA r leavefo s a s respiration we used 30 s depletion times repeated three times.

On the same leaves measured for Amax and Rdark , we measured chlorophyll a and b concentrations from 1 cm diameter samples obtained with a cork borer, with the n,n-dimethyl formamide technique of Moran (1982). For the anatomical analysis, 4 mm2 samples of the same leaves used for photosynthesis were fixed in FAA, sampled midway between the midrib and marginhand-sectiont cu e W . s wit hrazoa r blad determino et e leamesophyld fan l thickness (mea f threno e measurement r section)spe maximud an , m palisade length and width (three measurements per section), at 400 X magnification. We also measured stomata lmagnification X densit 0 40 t ya , three timee r leafth spe n i , samples cleared fro chlorophyle mth l extraction. Replicate eacf so h treatment were randomly adjacenlocateo roofe tw th f so n d o t buildings usee W .dtreatmen a t design appropriat physiologicaa r efo l experiment, with sample sizes as the total number of individuals, and not the number of replications. Results were analysed as a stratified random block design using the General Linear Models Procedure of ANOVA (SAS Institute 1985). Initial data were checke r normalitydfo werd an , e rank-transformed when necessary. Post-hoc comparisons were performed from ANOVA using the Fisher's Least Significant Difference test, wit a significanch e threshol p<0.05f do . Comparative contribu- treatmeno t tionD PF f R:F so d t Ran difference s were estimate 2-way db y ANOVA of the low and medium irradiance treatments (LRR, LFR, MRR, and MFR). The relativ developmene eR:Fd th influence an n Ro D PF f f differeno so t t traits were visualise y dcalculatinb g their coefficient f determinatioo s n (Soka Rohl& l f 1981), dividing the sums of squares from 2-way ANOVA, using the simultaneous processin f variablesgo e totath ly b sum, f squaresso alse W o. constructeda Pearson Product Correlation matrix for selected characters, using rank-trans- formed data.

Result discussiod san n

Seedlings generally gre wtreatmene welth n i l t enclosures, free from diseasr eo insect damage, although those growin direcn i g t sunlight appeared stuntey db e exposureth . Shadehouses approximated light environments encountered within the rain forest environment (Table 1, Chazdon et al. 1996). The LFR and LRR treatments wer thasimilaf o t e o raif to D n rPF fores t understory. Small gaps R HR treatments R e werth MR y elargb a d approximatep d an ega ,an R MF e th y db treatment. The spectral quality of LFR and MFR treatments was similar to that understore oth f y (Lee 1987) factoriae Th . l design also meant that certain light environments combined PFD and R:FR in unnatural combinations, as LRR - with the intensity of deep forest shade and the spectral quality of direct sunlight. These treatments affected jelutong seedling growth, architecture and physiol- ogy, but the effects were small compared to previous studies (Lee et al. 1996a,b, 1997). 138 Journal of Tropical Forest Science. 11(1):132-147 (1999)

Table 1. Photosynthetic photons received per day for each of the shade treatments, and for each replication repore W . t dat means aa standars± d deviations. Reported R:FR values were measured mid-way during growth trials, and the % of PFD is the mean of the two replications numbee Th . seedlingf ro s harveste r treatmendpe alss i o) given(N t .

Treatments LFR LRR MFR MRR HRR SRR

Replication 1 0.83 ±0.21 0.84 ±0.24 2.93 + 0.76 3.7 51.3+ 2 10.81+2.73 27.94 ±6.76 9 N= 7 6 10 10 4

Replication 2 0.7 0.14+ 9 0.82 ±0.23 3.18 ±0.82 5.0 1.69+ 4 13.94 ±3.60 33.40 ± 9.25 N = 6 6 6 4 8 4

%PAR 2.6 2.8 10.0 13.4 40.2 -

R:FR 0.25 1.25 0.25 1.25 1.25 1.25

Growth

Rate f growtho s s assessea , finay b d l height, collar diameter (diametet a r transition between masy roo stem)d dr stan d increasan , e (Tabl wer) e2 e smalt a l lomediud wan m PFD. Height increases were less tha other nfo r species grown ni the same treatments (Lee et al. 1996a). Dry mass increase was assessed on a per day basis, because some seedlings gre slightlr wfo y different periods (429-441 days). More importantly, the light levels at low (LRR and LFR) and, especially, medium (MRR and MFR) treatments were not perfectly matched (Table 1), making an f photonassessmeno l mo sr receivedpe t bese th t comparison. Growth ratess a mass/day were not significantly different between LRR and MRR, or LFR and MFR, R:Fw lo R e treatmentth t bu s depressed growth rate t bota s h masPFDy Dr s. increment/mo f photono l significantls wa s y decrease e mediuth t a d m light treatments, and lower (but not significantly) for reduced R:FR. Growth was highest treatmentR HR e significantld th an ,n i y decrease fuln di l sunlight.

Architecture

Plant architecture was not strongly affected by the low and medium light treatments (Table 3). Seedlings produced virtually no branches during the growth period. Internode length was promoted by greater PFD and reduced R:FR, but the effects were not large. Stem robustness, as mass/length, was increase y highedb r PFD slightld an , y decrease R:FRw lo y . db Leaf area/stem length ratio, an indicator of allocation of leaf surface per unit of axis extension, was not strongly affected by PFD, and was slightly reduced by low R:FR, especially t mediua (MFR)D mPF . Journal of Tropical Forest Science 11(1):132-147 (1999) 139

Tabl . Effecte2 lighf o s t treatment plann o s t heigh growthd an t . Treatment abbreviatione ar s described in the methods section and Table 1. Values are means ± standard errors. Values sharing lower case letters are not significantly different from each other.

Treatment Height Collar diameter Dry mass (mg)/ Dry mass (mg)/ (cm) (mm) day mol photons

LFR c la 32. . 1±3 7.14 + 0.56a 14.50 ±4.06a 18.33 ±1.82d LRR 36.0±2.7ace 8.43 ±0.c 5la 23.63 ±3.62bd 28.45 ±1.63e MFR 42.7±3.4bde 8.2 0.60a0± c 17.30±4.34ad 5.67±1.95b MRR 39. 83.4b± c 8.83±0.66ac 33.79 ±4.76be 8.19±2.14c HRR 51.7±2.9d 11.79±0.53b 44.18±3.82ce 3.68±1.72a SRR 32.5 ± 3.9ac 9.55±0.71c 28.05 + 5. 12b 3.29 ± 2.30a

Tabl . Effect3 e f ligho s t treatment n planso t architecture. Treatment abbreviatione ar s described in the methods section and Table 1. Values are means ± standard errors. Values sharing lower case letters are not significantly different from each other.

Treatment Internode Stem mass (mg) Leaf area (cm2)/ length (cm) /length (cm) stem length (cm)

LFR 2.7 ± 0.6a 47.3 ± 10.9a 11.40±1.51be LRR 3.7±0.5ac 55.8 ± 9.7ab 15.98 ±1.39d MFR 4.7±0.7bce 67.7±11.7bc 6.16±1.67a MRR 6.0±0.6b 101. 912.2cd± 14.48 + 1.81cde HRR 7.7±0.6d 103. 810.9± d 11.41±1.56bc SRR 3.5±0.7ae 133.2 + 15.4d 10.81 ±4.39abd

Allocation

Relative allocation plano st t organs represent strategie exploratioe th r sfo r nfo r exploitatioo resourcef no s (Grime 1979, Tilman 1988). Percentag masy dr sf eo allocation to leaves, stems and roots varied among the treatments (Figure 1). Allocation to leaves was reduced with increasing PFD, and was also reduced at low R:FR. Leaf allocation was extremely small in the stunted seedlings grown in direct sunlight (SRR). Stem mass allocation varied little with treatment. However, root mass allocation increased with light intensity significantlt no s ,wa y affecte R:FRy db , and was 42 % of total dry mass in plants grown in direct sunlight.

Leaf morphology

Mean lea t stronglf no ares awa y affecte treatmentse th reducey s db wa t y dbu ,b low R:FR and full sunlight (Table 4). Petiole length and leaf shape (as width/ length) changed very little. Leaf specific mass increased only in the HRR and SRR treatments. Leaf morphology was not strongly affected by these treatments, except stuntine foth r fuln gi l sunlight (SRR). 140 Journal of Tropical Forest Science 11 (1): 132-147 (1999)

100 Q| Leaves ae be 0 Stems S Roots 80-

1 0)

20-

R SR R HR R MR R MF R LR R LF

Figur . Allocatioe1 masy dr leaveso st f no , stem rootd s an seedling n si jelutongf so . Treatment symbol e describear s methode th n di s sectio Tabld an n . Verticae1 l bars indicate standard errors, and identical letters between treatments indicate that they are not significantly different from each other.

Tabl . e4 Effect lighf o s t treatment lean so f morpholog anatomyd yan . Treatment abbreviations are described in the methods section and Table 1. Values are means ± standard errors. Values sharing lower case t significantl letterno e sar y different from each other.

Area Specific mass Petiole Width/length Palisade Treatment (cm2) (mg cm2) (mm) widtm h(u

LFR 46.1+5.3b 3.58 + 0.33a 23.7±1.5bc 0.2 3O.Ol± a 19.8±0.5b LRR 62.6±4.0cd 3.94±0.16a 25.4±1.3c 0.26±0.01b 20.3 + 0.5b MFR 41.0 + 4.9ab 4.14±0.22a 20.6±2.1ab 0.26±0.01b 17.9±0.6ac MRR 61.6±9.3bd 4.09±0.22a 22.2±1.7abc 0.27±0.01c 19.3±0.5bc HRR b 1 48.. 6 9± 6.33±0.24a 24.7±1.3bc 0.2 0.0l7+ b 17.6±0.5a SRR 28.1+3.9a 6.54±1.13b 17.9±1.4a 0.2 0.0l6+ b 16.7±0.7a

Leaf anatomy

Leaf thickness did not vary among the low- and medium-intensity treatments, but did increase in the SRR and HRR treatments (Figure 2). These effects were paralleled in measurements of mesophyll thickness and palisade length. Palisade width increased at low light levels, and stomatal density increased from the lowest PFD to direct sunlight (Tables 4 & 5). R:FR contributed little to leaf anatomy characteristics. Journal of Tropical Forest Science 11(1):132-147 (1999) 141

Total thickness 200- Mesophyll thickness 200 Palisade length

ec o E c 'w 100 100 CO 0> .n: o

LFR LRR MFR MRR HRR SRR

Figure 2. Leaf and mesophyll thickness, and palisade cell length, among the different shade treatments. Tallest bartotae ar s l leaf thickness. Treatment symbols are described in the methods section and Table 1. Vertical bars indicate standard errors, and identical letters between treatments indicate that they t significantlno e ar y different from each other.

Physiology

Pigment composition, both per area and a/b, varied little among all of the

treatments (Table 5). Maximum photosynthesis (Amax )dark respiration (Rdark) and stomatal conductance wer middld e littlan w ee lo affecte intensite th y b d y treat- ments (Figure 3). These processes all increased significantly in plants grown at

40% and direct sunlight, and Amax was highest in plants grown in the former

condition thesn I . e treatment experimentad san l conditions comparabls wa , A e x

to that of Hopea odorata, a relatively shade-toleranma t Malesian dipterocarp species (Lee et al. 1997). These maximum rates were similar to those of late successional tropical forest Moraceae (Strauss-Debenett Bazzai& z 1991 shade-tolerand an ) t neotropical forest species (Kitajima 1994). The effects of PFD and R:FR on seedling growth, architecture and physiology e assesseb n ca compariny db e coefficientgth f determinatioo s r eacnfo h trait resulting fro factoriae mth l analysimediud an w variancf mslo o e treatmentth f eo s (Table 6). The coefficients are not absolute values, their range limited by the treatment conditions for the factorial design (LFR, LRR, MFR, MRR) and the genetic variation within the seedlings - independent of treatment effects. These coefficient indicato d s relative eth e contribution spectrad an D lPF qualitf so o yt each of the traits, and the total variation of each trait to the range of shade conditions (plasticity). 142 Journal of Tropical Forest Science 11(1):132-147 (1999)

6- MaximuJ [ m photosynthesis Oar0 k respiration c 5- 1 c

7co 4- CM i 1 E i j - cy i b b a O a "5

1- c, d. / / b b /'/f / n- 77*77 7/Z1 ?y/5 TfrA /y/v Y//, LFR LRR MFR MRR HRR SRR

Figur . Maximue3 m photosynthesis (A dard maxan )k respiration (Rdark leaven i ) s from seedlings differene oth f t shade treatments. Treatment symbol describee ar s methode th n di s section and Table 1. Vertical bars indicate standard errors, and identical letters between treatments indicate that they are not significantly different from each other.

Tabl . Effecte5 lighf o s t treatment stomatan so l densit conductanced yan pigmend an , t composition. Treatment abbreviations are described in the methods section Tabld an . Valuee1 e meanar s standars± d errors. Values sharing lower case letters are not significantly different from each other.

Treatment Stomatal density Stomatal conductance Chlorophyll (104 cm-2) (mol m-2s-1) (ug cm-2) (a/b)

LFR 1.47±0.07b 0.055 ±0.006a 28.45 ±1.43ac 2.38±0.04a LRR 1.32 + 0.07a 0.047 ±0.006a 31.65 ±1.32bc 2.33±0.04a MFR 1.89±0.07d 0.059 ±0.006a 29.18±1.57bcd 2.37±0.04a MRR 1.70±0.07c 0.050 ±0.006a 30.04 ± 1.39bce 2.38 ± 0.04a HRR 2.39±0.07e 0.089 ± 0.006b 27.1 1.39ad5+ e 2.3 0.048+ a SRR 3.32±0.09f 0.094 ±0.008b 24.08 ±1.86a 2.40±0.05a

Limited variation in light treatments

In general range th , flexibilitf eo thesf yo e traits, compare thoso dt other efo r species unde e samth r e experimental conditions (Le. 1996a,bal t ee , 1997s )wa rather small. Since the treatment variation was most likely contributed by different genotypes, plasticity may only explain part of these responses (Nicotra et al 1997). These results suggest that jelutong seedlings were somewhat indifferene th o t t shade conditions e greatesTh . t response charactere th r sfo s were among plants grown at 40% full sunlight. Limited response to varying shade may be characteristic Journal of Tropical Forest Science 11(1):132-147 (1999)

of plants tha e toleranar t f shadeo t intolerand an , f direco t t sunlight (Bazzaz& Pickett 1979). Seedlings of jelutong thus do not seem adapted to the full sun conditions of early succession, but grow more slowly under partial shade condi- tions. These results are consistent with the growth trials of Aminuddin (1982), and also demonstrat limiteea d acclimation perhapr o , s persistence deeo t , p shade.

Table 6. Coefficients of determination for the treatment effects of irradiance (PFD) and spectral quality (R:FR),as well as interactions, on the characters reported in Tables 2-5

Character R:FR PFD Interactions

Height 0.001 0.112* 0.023 Collar diameter 0.048 0.029 0.008 Growth mass/day 0.202 *** 0.023 0.002 Growth mass/mol 0.056 * 0.41* 8** 0.024 Internode length 0.057 * 0.20* 9** 0.000 Stem mass/length 0.039 0.126** 0.001 Leaf area/stem length 0.242 *** 0.069 * 0.024 % Leaf allocation 0.092 ** 0.386 *** 0.003 % Stem allocation 0.070 * 0.028 0.000 % Root allocation 0.021 0.414*** 0.007 Leaf area 0.138** 0.005 0.001 Specific leaf mass 0.013 0.055 0.016 Petiole length 0.008 0.059 0.001 Leaf width/length 0.157** 0.052 0.000 Stomatal density 0.062 * 0.37* 1** 0.001 Leaf thickness 0.003 0.030 0.014 Mesophyll thickness 0.001 0.040 0.019 Palisade cell length 0.089 * 0.076 * 0.005 Palisade cell width 0.036 0.092 * 0.009 Maximum photosynthesis 0.002 0.068 * 0.001 Maximum respiration 0.006 0.29* 7** 0.036 Stomatal conductance 0.079 * 0.008 0.000 Chlorophyll/cm2 0.029 0.001 0.011 Chlorophylb a/ l 0.008 0.020 0.000

*Denotes treatment effec two-wan i t 0.0005< s a y * ANOV 0.005.< ** s 0.05d a < an * A,s a * ,

Small contribution of spectral quality treatmentto effects

Reduction in R:FR is generally not very important in controlling the develop- men jelutonf o t g seedlings, about halcontributioe th f f intensitno y (Tabl. e6) Effect R:Ff so R were only importan controllinn ti growt) g(1 mass/days ha lea) (2 ;f area/stem lengthleafd an shap) (3 ;aread ean . Reduced leaf allocation (Figur) e1 may be related to the slightly smaller area per leaf, and the reduced leaf area/stem length. A correlation matrix for these characters (Table 7) shows strong positive relationships between growth as mass/day and leaf area/stem length. Reduced leaf area may limit total capacity for carbon assimilation, thereby reducing growth rates. Such effects were probably more important in the low R:FR treatments. These pattern consistene sar t wit growte hth h dat Kitajimf ao a (1994) photosynthesid ,an s 144 Journal of Tropical Forest Science 11 (1): 132-147 (1999)

was als t show significantle ono b o nt y influence r researchR:Fy dhe b Rn i r thao , t of others (Kwesiga & Grace 1986, Turnbull 1991, Tinoco-Ojanguren & Pearcy 1995).

Table 7. Pearson product correlations of growth and photosynthesis with plant architecture lead an f structure.

A MD T FH MMO SML LAS LF% PHO CON LTH STM

Heigh - 0.57t 7 -0.038 0.384 0.045 - 0.074 0.358 0.137 0.096 0.160 (FHT) *** *** ** ** Mass/day - 0.060 0.667 0.464 0.117 0.490.237 8 0.258 0.299 (MDA) *** *** *** * * ** Mass/mol - - 0.266 0.551 0.740 -0.440 - 0.372 -0.491 - 0.756 (MMO) * *** *** *** *** *** *** Stem mass/ 0.109 -0.340 0.430 0.280 0.287 0.477 length (SML) ** *** * * *** Leaf area/ 0.729 -0.064 -0.211 -0.147 - 0.253 ste m(LASL. ) *#* * %Leaf -0.245 -0.,237 - 0.298 - 0.587 (LF%) * * * *** Photosyn- - 0.598 0.412 0.540 thesis (PHO) *** *** *#* Conductance - 0.293 0.478 (CON) ** *** Leaf thick- - 0.546 ness (LTH) *** Stomatal density (STM)

Levels of significance of correlations are depicted as * = < 0.05, ** = < 0.005, *** = < 0.0005.

Predictors of seedling growth

Measure seedlinf so g growth (mass/da y- MDA , final heigh collad an t r diam- eter) were strongly correlated with each other and further comparisons of growth with other characters used onl mass/dae yth y data mas y (TablDr s . incremene7) t r molpe f photoneo s received (MM O Tabln realls i i ) indicaton e7 ya e th f o r efficiency of growth with the amount of radiation received. Since such efficiency is reduced at higher fluxes, MMO is not positively correlated with measurements of growth (Tabl . However7) e , such characters that document capacitr fo y assimilation—as percentage leaf allocation and leaf area per stem length—were significantly correlated with growth efficiency. Growth efficienc jelutonf o y g seedling taxx . (1996a si averagflus a al w e t reportexlo e wa th d t r e sa an ) e fo Le y db the lowest—the most suppressed—at 40 % full sunlight (HRR) compared to these taxa. Growth, as MDA, was correlated with two architectural characters, stem mass per length (SML) and leaf area per stem length (LAS). Greater leaf area would allow for more total carbon fixation and more growth. Growth was also

strongly correlated with Amax and other characters associated with gas exchange: conductivity, leaf thickness and stomatal density. Journal of Tropical Forest Science 11 (1):132-147 (1999) 145

Photosynthesi strongls wa ) y correlateA s( d with leaf anatomy, with increases

lean i f thickness, stomatal conductanc stomatad ean l density. Conductivit Ad max yan were measure same th t eda time botd strongle an ,h ar y dependen stomatan o t l density. Photosynthesi t correlateno s swa d with chlorophyll/are r chlorophylao l a/b; neither of these varied much among the treatments and they were not included in Table 7. The increase in air-cell contacts associated with the thicker leaf and mesophyll may contribute to gas exchange (Sharkey 1985, Nobel 1991, Parkhurst 1994), but the main effect is likely to be stomatal conductance (Wong et al. 1979). Clearl seedline yth g leaves of jeluton relativele gar y thic durabled kan , markedly different fro thie expendabld mth nan e leave short-livef so d pioneers whice har also capabl mucf eo h higher rate photosynthesif so s (Strauss-Debenedett Berlyi& n 1994).

Seedling functional ecology

seedlinge Th s of jeluton limitee variatioge ar th n di theif no r response ligho st t climates during their establishment. Even thoug presene h b seee they th dyma n ti bank and establish as early pioneers, they are stunted by direct sunlight and grow most rapidly under partial shade. Their plasticity of root allocation to light conditions suggests that they may possess adaptations to water stress to which early successional environments may be exposed. They are capable of continued but slow growth under conditions approaching forest understory, and thus may persist for long periods under deep shade. They may encounter such shade when overtoppe faster-growiny db g short-lived pioneers. They persist, continu growo et , and eventually become established as fast growing saplings. This change in growth rates suggests that ther likele e age b size-related ear o y-an t d physiologicad an l anatomical correlates. Such ontogenetic flexibilit e shiftth n i s lighf yo t responses have been documented in other tropical trees (Clark & Clark 1992, Farnsworth & Ellison 1996). These changes wer t observeeno d durin limitee gth d duratiof no these trials t Appanabu , Weinland han d (1993) noted that leavetree e th ear f so thicker and tougher than those of seedlings.

Conclusion

Jelutong (Dyera costulata) is a long-lived pioneer which eventually becomes a gigantic rain forest emergent. In early succession its seedlings grow slowly, are shade tolerant, and stunted by direct sunlight. These seedlings vary little in a range of light conditions, and are little affected by shifts in spectral quality. Yet, as saplings aduld an t trees the capable yar verf eo y rapid growth resulte Th . seedlinf so g trials jelutonn o g contrast strongly with thos f Endospermumo e malaccense (Le. al et e 1996a), which may be present in the seed bank in the same forests, establishes early, and attains a height of 40 m in mature forest. Its seedlings grow rapidly at low PFD, var overaln yi l response strongle lightar o st d an ,y affecte reducey db d R:FRo N . clear factors emerge which constrain growth rate thesn i s e plants (Lamber& s 146 Journal of Tropical Forest Science 11(1):132-147 (1999)

Poorter 1992). These results demonstrat complexite eth seedlinf yo g growtd han establishmen n i tropicat l rain forests, emphasisin dangee gth f generalisino r g about species response members a s guildsf so , whether the e associateyar d with gap f differenso t size r noto s . Additional researc varieta n h o f specie yo s will certainly help us understand the complexity of seedling ecology and establish- ment in tropical rain forests.

Acknowledgements woule W d lik thano et k Salleh Mohd. Nor formee th , r Director Genera f FRIMo l , fos encouragemenrhi supportd tan receivee W . d technical support from Rosli Alias, K. C. Ang, Zaini Bahari, Siti Asha Abu Bakar, Hamsinah Hashim, Christian Herrera, Noraida Idaris, Akoh Jin, Fazale Mahmud, Birgith Phillips, Zaiton Salleh and Juntak So. We also benefitted from technical advice by S. Appanah, Paulette Johnson.Joel Trexler, Tom Turner and T.C. Whitmore. The German GTZ mission at FRIM provided lodging for the U.S. authors. The research was supported by NSF grant DEB-9020137 and a donation of materials from the 3M Corporation.

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