Photosynthesis of Nine Pioneer Macaranga Species from Borneo in Relation to Life History

Ecology, 79(7), 1998, pp. 2292±2308 ᭧ 1998 by the Ecological Society of America

PHOTOSYNTHESIS OF NINE PIONEER MACARANGA SPECIES FROM BORNEO IN RELATION TO LIFE HISTORY

STUART JAMES DAVIES1 Harvard University Herbaria, 22 Divinity Avenue, Cambridge, Massachusetts 02138 USA and Biology Department, Universiti Brunei Darussalam, Bandar Seri Begawan 2028 Brunei

Abstract. Early successional (pioneer) tropical tree species are characterized by a suite of ecophysiological and life history traits; however, little is known of the relationships between these groups of traits, and their consequences for species' distribution patterns in diverse tropical forests. This study investigated leaf-level ecophysiological variation in seedlings of nine sympatric, pioneer tree species of Macaranga (Euphorbiaceae) from Borneo, grown at three light levels (high: ϳ19 mol/d; medium: ϳ7 mol/d; low: ϳ3.6 mol/ d). A multivariate analysis of traits associated with species' successional status was used to rank species according to life history variation, and then to investigate patterns of covariation in seedling ecophysiological and life history traits. Ecophysiological traits varied signi®cantly among the nine species. On a leaf area basis, Ϫ2 Ϫ1 dark respiration (Rd-area) in high-light seedlings ranged from 0.51 to 0.90 ␮mol CO2´m ´s , Ϫ2 Ϫ1 and light saturated net photosynthesis (Amax-area) ranged from 7 to 13 ␮mol CO2´m ´s . Amax-mass and Rd-mass were strongly negatively correlated with leaf mass per unit area (LMA). Among species, Amax-mass and Rd-mass were strongly positively correlated for high-light grown seedlings, re¯ecting a trade-off between high assimilation rates and respiratory costs.

Within species, Amax-area, Rd-area, gs, LMA, and photosynthetic light compensation point were signi®cantly greater in high-light grown plants for all species. Due to the high plasticity

of LMA, Amax-mass and Rd-mass were only weakly in¯uenced by light growth conditions, suggesting that resource allocation patterns that maximize photosynthetic ability are critical to survival and growth in low light for these species. Principal components analysis (PCA) of ecophysiological traits for the nine species

revealed a continuum of variation from species with relatively low Amax, low gs, and high LMA to species with the opposite traits. The primary axis of the PCA of life history traits was strongly related to variation in shade tolerance and seed mass. The second life history axis distinguished among the more shade-intolerant species. The PCAs of ecophysiological and life history traits were not completely concordant due to variation in life history traits

among high Amax species. Amax-mass and LMA, were correlated with a successional ranking of the species. The study shows how a suite of inter-related ecophysiological and life history traits can result in a diversity of pioneer tree ecologies. Key words: ecophysiology; growth rates; life history; Macaranga; photosynthesis; pioneer trees; rain forest; seed size; shade tolerance; Southeast Asia; secondary succession; tree seedlings.

INTRODUCTION simply determined by photosynthetic capacity (Field Leaves of tropical pioneer trees typically photosyn- 1988), but involves the interaction among a suite of thesize and respire at higher rates than later succes- ecophysiological, morphological, and demographic sional canopy or understory species (Bazzaz and Pick- traits in relation to ¯uctuations in available resources ett 1980). Numerous studies have veri®ed this pattern (Mulkey et al. 1993). Pioneer trees, for example, are (e.g., Reich 1995); however a recent review of variation typically characterized by light-induced seed germi- in photosynthetic characteristics among tropical trees nation, high growth and mortality rates, short leaf life revealed considerable variation in photosynthetic ca- spans, high tissue nitrogen and phosphorus concentra- pacity within early- and late-successional species tions, low wood density, early reproductive maturation, groups (Strauss-Debenedetti and Bazzaz 1996). This is and high fecundity, as well as high rates and plasticities not surprising as successional status of species is not of photosynthesis and respiration (Swaine and Whit- more 1988, Raaimakers et al. 1995, Reich et al. 1995, Manuscript received 27 February 1997; revised 17 Sep- Ackerly 1996). A combination of some or all of these tember 1997; accepted 8 October 1997; ®nal version received traits may enable a species to successfully colonize 31 October 1997. open microsites, but at the same time may limit their 1 Present address: Institute of Biodiversity and Environ- mental Conservation, Universiti Malaysia Sarawak, 94300 ability to persist in low-light environments. Under- Kota Samarahan, Sarawak, Malaysia. standing the relationships among physiology, whole- 2292 October 1998 PHOTOSYNTHESIS IN MACARANGA 2293 plant allocational patterns, and demographic charac- the species can be found growing in the same forest teristics of different species is central to understanding gaps or large-scale disturbances (Davies 1996). The the distribution patterns of tropical trees. species do however, vary in their degree of gap de- Many studies of tropical tree ecophysiology have pendence, and in a wide range of life history charac- emphasized comparisons among species of different teristics. The ®rst goal of the study was to examine successional status (e.g., Riddoch et al. 1991b, Strauss- among- and within-species patterns of leaf-level vari- Debenedetti and Bazzaz 1991, Thompson et al. 1992), ation in photosynthetic traits for seedlings of the nine resulting in a great deal of information on ecophysi- species when grown under a range of experimental light ological and allocational differences between the ex- levels. I assess whether Macaranga species differ in tremes of the tree life history spectrum. In most cases the magnitude and plasticity of ecophysiological traits, the successional status of the species involved has been and how the ecophysiological traits are interrelated. based on anecdotal natural history information, making The second goal of the study was to investigate how the link between ecophysiological attributes and spe- leaf-level ecophysiological traits vary in relation to cies' distributions in the forest tenuous (but see Kita- known variation in Macaranga life histories. A detailed jima 1994, and Walters and Reich 1996 for temperate analysis of attributes that are usually linked to species' trees). Only recently have studies addressed the ques- successional status, including growth and mortality tion of how species with similar ecologies or succes- rates, shade tolerance, seed size, fecundity, and tree sional positions differ in their patterns of assimilation stature, is used to rank the species according to life and allocation (Hogan 1988, Ashton 1992, Moad 1992, history variation. Patterns of covariation between seed- Newell et al. 1993; see also Sipe 1994 for temperate ling leaf-level photosynthetic traits and the species' life trees). Fine-scale differences in physiology and allo- history ranking are then investigated. Finally, the con- cation have been found to be important in in¯uencing sequences of ecophysiological and life history varia- the distribution of some more shade-tolerant plant spe- tion for the distribution patterns and coexistence of cies. For example, Chazdon (1986) demonstrated that these sympatric pioneer species are discussed. differences in biomass allocation and architecture METHODS among palm species enabled them to survive under Study species and life history characteristics different irradiance minima in the forest. Similarly, Mulkey et al. (1993) demonstrated compensating dif- Macaranga Thou. (Euphorbiaceae) is a genus of ferences in ecophysiology, tissue turnover, and allo- ϳ300 species of rain forest trees distributed between cation among three shade-tolerant Psychotria species west Africa and the south Paci®c Islands, with a center that enabled them all to tolerate low irradiances. of diversity in Malesia (Whitmore 1981). There are Among pioneer species, differences in ecophysiologi- about 50 species in Borneo, the majority of which are cal characteristics have been reported in numerous high-light demanding pioneers. From 1991 to 1994, a studies (Strauss-Debenedetti and Bazzaz 1996). Reich study of life history variation among 11 species of et al. (1995) showed considerable variation in maxi- Macaranga was conducted in Lambir Hills National mum photosynthetic rates in early successional tierra Park, Sarawak, Malaysia (4Њ20Ј N, 113Њ50Ј E; Davies ®rme species in Venezuela. Tan et al. (1994) found 1996). This involved monitoring mapped and tagged higher leaf mass-based maximum photosynthetic rates trees in a 52-ha long-term ecological research plot, and in pioneer species of fertile soils than pioneer species in seven smaller secondary forest plots. The 52-ha plot of infertile soils in Singapore. Furthermore, numerous was established following the methods used for similar studies, which have included more than one early suc- plots in Panama (Hubbell and Foster 1983) and pen- cessional species, have reported differences in eco- insular Malaysia (Manokaran et al. 1990). In all plots, physiological traits for pioneer trees (e.g., Riddoch et individuals Ն1 cm diameter at breast height (dbh) were al. 1991a, Kitajima 1994); however, the degree to tagged in 1991±1992 and their diameters and heights which these differences relate to differences in spatial measured (in the seven secondary forest plots seedlings distribution or life history characteristics of the species Ͻ1 cm dbh were included). Plants were remeasured or is not known. Pioneer species have been shown to per- recorded dead in 1994, ϳ2.5 yr after the initial mea- form differentially with respect to gap size (Brokaw surements. Diameter growth rate was assessed based 1987, Popma et al. 1988), and to differ in maximum on these measurements. Annual mortality rates were tree size and longevity (SarukhaÂn et al. 1985, Swaine calculated following Sheil et al. (1995). For analysis, and Whitmore 1988). The degree to which this varia- trees of each species were divided into four life-stage tion is re¯ected in species' ecophysiological charac- classes: seedling/sapling, prereproductive, reproduc- teristics has rarely been addressed. tive, and mature. The seedling/sapling life-stage class In this study, I investigated leaf-level ecophysiolog- corresponded to individuals Ͻ2 cm dbh for all species; ical variation among nine sympatric species of Ma- otherwise, life-stage classes represented different dbh caranga (Euphorbiaceae). The species are all relatively classes for different species due to their differing re- early successional trees and form a major component productive ontogenies (Davies 1996). An index of the of the secondary forest ¯ora of Borneo; up to seven of shade tolerance for each species was inferred from the 2294 STUART JAMES DAVIES Ecology, Vol. 79, No. 7

TABLE 1. Macaranga species included in the ecophysiological study with a summary of life history traits derived from a two and half year study of trees of all size classes in Sarawak, Malaysia (see Methods: Study species and life history characteristics and Davies 1996).

Diameter growth (mm/yr) Mortality (%/yr)

Species I II III IV n I II III IV n M. hosei 0.29 0.35 0.36 0.25 159 0.30 0.07 0.15 0.09 327 M. winkleri 0.86 1.25 0.41 0.12 100 0.20 0.10 0.13 0.25 168 M. gigantea 0.22 0.37 0.74 0.39 46 0.19 0.02 0.05 0.00 364 M. hypoleuca 0.17 0.41 0.17 0.45 57 0.23 0.04 0.13 0.03 73 M. beccariana 0.24 0.33 0.24 0.14 398 0.26 0.16 0.11 0.15 728 M. triloba 0.15 0.30 0.37 0.14 225 0.39 0.06 0.04 0.03 419 M. trachyphylla 0.22 0.25 0.23 0.17 693 0.14 0.06 0.03 0.08 903 M. hullettii 0.17 0.08 0.08 0.11 366 0.02 0.02 0.03 0.05 405 M. lamellata 0.13 0.09 0.08 0.08 329 0.01 0.01 0.00 0.02 348 Notes: Growth rate is median diameter growth rate. Mortality is annual percentage mortality. Shade tolerance is mean crown illumination (CI) index of trees in the forest, using a scale of 1 ϭ shade tolerant to 5 ϭ very shade intolerant. Tree height is estimated asymptotic height. Fecundity is mean annual reproductive output. Growth and mortality rates are given for four life-stage classes: I, seedling/sapling; II, prereproductive; III, reproductive; and IV, mature. Sample sizes (n) used to estimate each of the life history traits are listed. Species are arranged in order of successional ranking, from shade intolerant to tolerant as in Fig. 4. distribution of large numbers of individuals in the for- for the experiment, with the three light levels on two est with respect to light availability, following Clark benches each. and Clark (1992). This involved assigning a crown il- The three experimental light levels were: high light lumination (CI) index, on a scale of 1±5, to each in- (plants grown in full sun on open benches), medium dividual based on a visual assessment of the degree of light, and low light. Medium- and low-light treatments crown exposure to light (5, completely exposed; 1, were created with neutral density shade cloth. Shade- completely shaded). Mean CI index was used as the cloth shelters were built on four of the six benches, estimate of each species' shade tolerance. Hemispher- ensuring air circulation around the plants. The medium- ical ®sh-eye photographs demonstrated that the ®ve CI light treatment was created by excising 10-cm wide values represented on average signi®cantly different strips (50 cm apart, oriented north±south) out of the levels of canopy openness (Davies et al., 1998). Dif- shade cloth such that any point on the bench received ferences in stand establishment history, spatial hetero- short periods of sunlight (``sun¯ecks'') during the day. geneity in recruitment, and species-speci®c height The low-light treatment had 1-cm wide strips excised growth patterns may all bias CI index as an estimate in a similar way, providing very brief sun¯eck periods of species' shade tolerance. However, large numbers in a typical day; this treatment represents somewhat of individuals distributed across Ͼ52 ha of forest were higher light levels than the understory of a tropical used to account for some of this variation. Furthermore, forest (Chazdon and Fetcher 1984). the ranking of mean CI indices for each species re- Average photon ¯ux densities (PFD; measured with mained consistent through ontogeny and was consistent quantum sensors and data logger, LI-COR Incorporated, with overall mean CI indices, suggesting that CI index Lincoln, Nebraska, USA) for the three light treatments was indicative of light environment preferences among were: high light, 18.93 mol´mϪ2´dϪ1 (n ϭ 57 d); medium the species (Davies et al. 1998). Tree height was es- light, 7.08 mol´mϪ2´dϪ1 (n ϭ 5 d); and low light, 3.61 timated as asymptotic maximum height, following Tho- mol´mϪ2´dϪ1 (n ϭ 21 d). Typical diurnal curves of PFD mas (1995). Estimates of mean staminate and pistillate for the three light treatments are shown in Fig. 1. fecundity were based on monitoring individuals over Plants and soil three reproductive seasons. Life history traits for the Seeds were collected from numerous mother trees of nine species included in the comparative ecophysio- each species, except for M. lamellata, M. hypoleuca, logical study are summarized in Table 1, see Davies and M. hosei where only one mother tree was found. (1996) for further details. The species are dioecious so genetic diversity is likely Experimental design to be reasonably high among seedlings for all species Seedlings of the nine Macaranga species were grown used. In July 1993, seeds were sown in nursery beds. in the Brunei Forestry Department glasshouse in Sun- Germination was synchronous among the nine species gai Liang, Brunei (4Њ39Ј N, 114Њ31Ј E). The experiment after ϳ3 wk. In August 1993, seedlings with 2±4 leaves involved three light levels, with two blocks and 20 (ϳ2±4 cm tall) were transplanted individually into ϳ4- replicate plants per treatment±block combination, a to- L black plastic polybags in the glasshouse. Seedling tal of 1080 plants. Six glasshouse benches were used positions were assigned randomly within each block of October 1998 PHOTOSYNTHESIS IN MACARANGA 2295

TABLE 1. Extended. twice during the experiment. At the time of gas exchange measurements, plants were growing vigorously and there was no evidence of root restriction by the Shade pots. Fecundity tolerance After 1 mo all pots received 200 mL (1.67 g/L) of Seed Tree height (male CI mass Fecundity ¯owers/ 15:30:15 NPK water-soluble fertilizer. Each pot sub- index n (mg) (m) n (seeds/yr) yr) sequently received 100 mL of the same concentration 4.0 115 5.1 31.3 159 5.3 ϫ 105 8.4 ϫ 106 fertilizer each month during the experiment. At each 4.0 103 1.7 21.5 135 6.0 ϫ 104 1.9 ϫ 106 fertilizer application a general purpose water-soluble 5 7 4.2 42 13.7 29.3 129 1.9 ϫ 10 1.1 ϫ 10 fungicide±algicide, Triconsan 20 (Tri-Products, Pro- 3.6 35 22.4 22.5 42 ´´´ 3.0 ϫ 106 3.4 222 15.2 17.2 355 2.1 ϫ 104 2.8 ϫ 105 prietary Limited, Singapore), was also applied. 3.4 215 17.0 22.4 336 1.3 ϫ 104 1.6 ϫ 106 3.2 226 22.7 21.5 421 1.4 ϫ 104 1.2 ϫ 106 Gas exchange measurements 2.6 229 28.3 17.9 82 2.1 ϫ 103 5.7 ϫ 105 2.1 255 64.0 15.0 109 2.2 ϫ 102 1.4 ϫ 105 Gas exchange was measured on the youngest or second youngest fully expanded leaf on plants of all species grown in the three light levels, between 28 January and 9 April 1994. In the late afternoon 24 randomly selected plants (8 per light level) were moved from their benches to a separate bench in the glasshouse and watered to ®eld capacity. That night, dark respiration was measured, and the following morning photosyn- the experiment. Seedling survivorship was very high; thetic light response curves were quanti®ed. the few seedlings that died were immediately replaced. Dark respiration and photosynthesis were measured Seedlings were potted in sieved forest topsoil, col- with a portable, closed gas exchange system (Model lected from secondary forest in Andulau Forest Re- 6200, LI-COR Incorporated, Lincoln, Nebraska, USA) serve. This soil is a sandstone-derived sandy haplic with a 1-L cuvette. Before every set of gas exchange acrisol (or udult ultisol, see Davies and Becker 1996), measurements (respiration and photosynthesis), the in- with a high sand content, and is generally nutrient poor frared gas analyzer calibration was checked against a

(Baillie et al. 1987, Ashton and Hall 1992). Pot posi- CO2 standard. The humidity sensor was calibrated sev- tions were randomly rearranged within each block, eral times during the measurement period using a LI-

FIG. 1. Representative diurnal time courses of average PFD in three experimental light treatments measured with LI- COR quantum sensors on predominantly cloudless days. Logging was at 5-min intervals for high and low light treatments and at 30-min intervals for the medium light treatment. Total PFD per day is listed in each graph. 2296 STUART JAMES DAVIES Ecology, Vol. 79, No. 7

COR portable dew point generator (Model LI-610). The clusion of these sources of variation is necessary if quantum sensor was checked against LI-COR quantum broader evolutionary trends in the light response of sensors. photosynthesis are to be investigated. At most ®ve pho- Leaf-level dark respiration was measured at night tosynthesis measurements were made on any one leaf (2000±2300) on plants in complete darkness. One spe- so individual leaf light response curves could not be cies was measured per night and all species were mea- analyzed. The light response of photosynthesis was sured on two different nights. Nighttime temperature modeled with the nonrectangular hyperbola (Ramos in the glasshouse during the respiration measurements and Grace 1990, Sims and Pearcy 1991, Evans et al. ranged from 27Њ to 29ЊC, humidity was Ն70%, and 1993, Ogren and Evans 1993): cuvette CO2 concentration was maintained between 330 2 and 370 mg/kg. One estimate of respiration rate was ͙{␣Q ϩ AmaxϪ [(␣Q ϩ A max) Ϫ 4⌰␣QA max]} P ϭ R ϩ made per plant, based on the mean of three consecutive d 2⌰ measurements in which cuvette CO2 concentration was increased by 0.7 mg/kg (ϳ2±4 min per leaf). where Rd is the dark respiration rate (␮mol Ϫ2 Ϫ1 Light response curves were quanti®ed in the morning CO2´m ´s ), P is the photosynthetic rate (␮mol Ϫ2 Ϫ1 (0700±1200) on the day after the dark respiration mea- CO2´m ´s ), ␣ is the apparent quantum yield, Q is surements. Across all photosynthesis measurements photosynthetically active radiation (␮mol´mϪ2´sϪ1), A is the asymptotic light-saturated photosynthetic CO2 concentration was 330 Ϯ 20 mg/kg, ambient tem- max perature was 33ЊϮ2ЊC, relative humidity was 63 Ϯ rate, and ⌰ is the convexity of the curve. Parameters 8%, and vapor pressure de®cit was 20 Ϯ 5 mbars. All of the light response models were estimated with non- plants to be measured were housed under numerous linear least-squares regression using the NONLIN pro- layers of neutral density shade cloth, and a range of cedure in SYSTAT 5.2 (Wilkinson 1990), which pro- PFD levels were produced by successively removing vides asymptotic 95% con®dence intervals for each layers of shade cloth. Initial measurements were at low parameter. This modeling resulted in one light response PFD levels 0±50 ␮mol´mϪ2´sϪ1 and were then gradually curve for each species and light level. Due to the dif- increased to 1500±1800 ␮mol´mϪ2´sϪ1. At least 20 min ®culty of statistically comparing nonlinear regression acclimation time at each PFD level was allowed before parameters among light levels and species (Ross 1981), photosynthesis measurements were made; there was no comparisons were made in a number of ways. First, evidence that plants were not fully acclimated within overlap of 95% con®dence intervals of parameter es- the 20 min (see also Poorter and Oberbauer 1993). One timates were inspected for signi®cant differences. In species was measured per day, and all species were addition, the apparent quantum yield, ␣, was estimated measured on at least two different days; in total, 8±12 by least squares linear regression of the light response different individuals were used for each species and curves between 0 and 50 ␮mol´mϪ2´sϪ1 PFD. Compar- light treatment. Photosynthesis measurements were isons among species were then made with tests for made at 3±5 light levels for each plant, but not all plants homogeneity of slopes (Sokal and Rohlf 1981). Light were measured at the same light levels. Macaranga compensation points were estimated as the x-intercept species, like a number of other tropical pioneer tree of the light response curve. Amax and stomatal conduc- species (Chiariello et al. 1987, Huc et al. 1994), can tance, gs, were compared with two-factor ANOVAs have strong midday depressions in photosynthesis (S. (light ϫ species) for measured rates above light satu- J. Davies, unpublished data); individual plants that un- ration (estimated visually from light response curves). derwent an obvious midday depression in photosyn- Patterns of covariation in leaf-level ecophysiological thetic rate (usually associated with stomatal closure) traits and life history traits among the nine species were were excluded from light response modeling. investigated with principal components analyses (PCA) Respiration and photosynthetic rates are presented of correlation matrices using SYSTAT 5.2 (Wilkinson on both leaf area and mass bases. Fresh leaf area was 1990). Thirteen traits were included in the analysis of determined with an automatic leaf area meter (Hayashi- life history variation: estimated maximum tree height, Denkoh AAM-8, Tokyo, Japan), and leaf mass was staminate and pistillate fecundity, seed mass, estimated determined following drying to constant mass at 60ЊC. shade tolerance (CI index), and growth and mortality rates for four life-stage classes (as in Table 1). The Analysis analysis of ecophysiological traits included mean val- To assess species-level differences in light response ues of: light-saturated photosynthesis and dark respi- characteristics, gas exchange measurements of all in- ration on leaf-area bases, maximum stomatal conduc- dividuals of a species from a light treatment were tance, apparent quantum yield, and leaf mass per unit pooled for light response curve estimation (see also area, for seedlings grown in all three light environments Hogan 1988, Tinoco-Ojanguren and Pearcy 1995). This (Table 2, Fig. 2). Parallel analysis was used to deter- approach includes much individual, temporal, leaf age, mine the signi®cance of each principal component and local environmental variation in light response (Franklin et al. 1995). In both analyses, only the ®rst curves. However, for species-level comparisons the in- two components were signi®cant (P Ͻ 0.05) and are October 1998 PHOTOSYNTHESIS IN MACARANGA 2297

TABLE 2. Ecophysiological traits for seedlings of nine species of Macaranga grown in three light environments (high, medium, and low as described in Fig. 1).

Light environment Light compari- Species High Medium Low son

Ϫ2 Ϫ1 Rd-area (␮mol CO2´m ´s ) M. hosei Ϫ0.55b (0.04) Ϫ0.41ab (0.04) Ϫ0.34b (0.03) a/b/b M. winkleri Ϫ0.66ab (0.05) Ϫ0.38b (0.02) Ϫ0.42ab (0.03) a/b/b M. gigantea Ϫ0.90a (0.08) Ϫ0.63a (0.06) Ϫ0.66a (0.07) a/b/ab M. hypoleuca Ϫ0.57b (0.03) Ϫ0.47ab (0.04) Ϫ0.43ab (0.03) a/ab/b M. beccariana Ϫ0.68ab (0.03) Ϫ0.45ab (0.02) Ϫ0.49ab (0.04) a/b/b M. triloba Ϫ0.58b (0.03) Ϫ0.37b (0.02) Ϫ0.42ab (0.02) a/b/b M. trachyphylla Ϫ0.84a (0.06) Ϫ0.63a (0.08) Ϫ0.62a (0.07) a/a/a M. hullettii Ϫ0.51b (0.03) Ϫ0.30b (0.02) Ϫ0.34b (0.02) a/b/b M. lamellata Ϫ0.53b (0.03) Ϫ0.35b (0.02) Ϫ0.35b (0.02) a/b/b

Ϫ1 Ϫ1 Rd-mass (nmol CO2´g ´s ) M. hosei Ϫ10.09c (0.61) Ϫ11.12bcd (1.10) Ϫ10.44b (1.36) a/a/a M. winkleri Ϫ19.89a (1.76) Ϫ13.64abc (0.98) Ϫ15.43ab (0.98) a/b/ab M. gigantea Ϫ18.29a (1.55) Ϫ16.86a (1.67) Ϫ19.01a (2.34) a/a/a M. hypoleuca Ϫ9.64c (0.56) Ϫ12.35abcd (1.07) Ϫ11.87ab (0.91) a/a/a M. beccariana Ϫ11.26bc (0.75) Ϫ12.25abcd (0.83) Ϫ14.39ab (1.26) a/a/a M. triloba Ϫ10.37bc (0.56) Ϫ9.32cd (0.50) Ϫ12.04ab (0.59) ab/b/a M. trachyphylla Ϫ16.76ab (2.34) Ϫ15.99ab (1.51) Ϫ18.70a (2.00) a/a/a M. hullettii Ϫ7.96c (0.52) Ϫ7.53d (0.46) Ϫ8.99b (0.54) a/a/a M. lamellata Ϫ8.17c (0.49) Ϫ8.14d (0.39) Ϫ8.96b (0.53) a/a/a LMA (g/m2) M. hosei 51.6cd (1.29) 36.9b (0.76) 34.4c (0.54) a/b/b M. winkleri 36.0e (0.92) 28.1c (0.75) 26.3d (0.52) a/b/b M. gigantea 48.7d (1.07) 36.9b (0.64) 35.1bc (0.54) a/b/b M. hypoleuca 59.6ab (0.91) 39.4b (0.92) 39.1ab (0.83) a/b/b M. beccariana 56.6bc (1.21) 36.7b (1.16) 36.9abc (1.18) a/b/b M. triloba 54.3bcd (1.12) 38.7b (0.72) 35.2bc (0.51) a/b/c M. trachyphylla 49.8d (1.79) 37.5b (0.83) 34.1c (0.99) a/b/b M. hullettii 61.0ab (1.17) 40.1ab (0.63) 37.3abc (0.76) a/b/b M. lamellata 63.3a (1.13) 44.1a (0.74) 41.0a (0.59) a/b/c

Ϫ2 Ϫ1 Maximum gs (mol H2O´m ´s ) M. hosei 0.37b (0.014) 0.29a (0.008) 0.26a (0.008) a/b/b M. winkleri 0.33bc (0.016) 0.19b (0.011) 0.19b (0.010) a/b/b M. gigantea 0.18d (0.004) 0.22b (0.014) 0.18bc (0.011) a/a/a M. hypoleuca 0.28bcd (0.010) 0.17b (0.012) 0.27a (0.009) a/b/a M. beccariana 0.55a (0.036) 0.33a (0.013) 0.29a (0.013) a/b/b M. triloba 0.26cd (0.014) 0.19b (0.009) 0.13cd (0.005) a/b/c M. trachyphylla 0.22d (0.009) 0.19b (0.012) 0.20b (0.008) a/a/a M. hullettii 0.24cd (0.013) 0.20b (0.008) 0.19b (0.006) a/b/b M. lamellata 0.20d (0.007) 0.11c (0.003) 0.11d (0.004) a/b/b

Apparent quantum yield (mol CO2/photon) M. hosei 0.032c (0.004) 0.038c (0.003) 0.034f (0.003) b/a/ab M. winkleri 0.039b (0.003) 0.047b (0.003) 0.046cd (0.004) b/a/a M. gigantea 0.045a (0.006) 0.039c (0.004) 0.038ef (0.003) a/b/b M. hypoleuca 0.029c (0.004) 0.047b (0.007) 0.052b (0.003) b/a/a M. beccariana 0.032c (0.003) 0.038c (0.003) 0.042de (0.004) b/a/a M. triloba 0.043ab (0.004) 0.043b (0.003) 0.049bc (0.004) a/a/a M. trachyphylla 0.041ab (0.005) 0.045b (0.005) 0.046bcd (0.005) a/a/a M. hullettii 0.030c (0.004) 0.039c (0.003) 0.036f (0.004) b/a/a M. lamellata 0.046a (0.004) 0.059a (0.003) 0.063a (0.003) b/a/a

Notes: Rd is dark respiration rate on leaf area (Rd-area) and mass (Rd-mass) bases (sample size per light level for each species, n ϭ 11±19, mean sample size ϭ 16). LMA is leaf mass per unit area (n ϭ 33±40, mean sample size ϭ 39). Maximum gs is stomatal conductance at light saturation (n ϭ 14±105, mean sample size ϭ 45). Apparent quantum yield was calculated using linear regression for PFD Ͻ 50 ␮mol´mϪ2´sϪ1. For each trait, mean values are given with standard error in parentheses, except for apparent quantum yield where 95% con®dence intervals are given in parentheses. Mean values were compared among species for each light level (letters beside means) and among light levels for each species (right column, with letters in same order as means). Values represented by the same letter are not signi®cantly different (P Ͼ 0.05, ScheffeÂ's test for all traits except for apparent quantum yield where slopes were compared with pairwise homogeneity of slopes tests). Species are listed by successional ranking, from shade intolerant to tolerant as in Table 1. 2298 STUART JAMES DAVIES Ecology, Vol. 79, No. 7

FIG. 2. Measured mean (Ϯ1 SE) photosynthetic rates at light saturation in nine species of Macaranga grown in three light environments (high, medium, and low as described in Fig. 1). (A) Amax-area, and (B) Amax-mass. Sample size ϭ 14±105 (mean ϭ 45) measurements per species for each light level. Different letters indicate signi®cantly different rates among light levels within species (P Ͼ 0.05; ScheffeÂ's tests). Species are listed by the ®rst three letters of their names, and by successional ranking, from shade intolerant to tolerant as in Table 1. Tests of among-species differences in Amax are presented in Table 3. presented. Other statistical methods follow Sokal and small and not signi®cant. Leaf mass per unit area

Rohlf (1981), and rs is used to refer to Spearman rank (LMA) was on average 37±64% greater in high-light correlation coef®cients. plants than low-light grown plants for all species (P Ͻ 0.05 in all species, Table 2). The differences in LMA RESULTS between medium- and low-light grown plants were Dark respiration much smaller (range: 0±10%) and signi®cant in only two species. In part, due to the plasticity of LMA Rates of dark respiration on leaf area (Rd-area) and among light levels, R -mass was much less affected by mass (Rd-mass) bases varied signi®cantly among both d seedling light environment than R -area. With the ex- species and light levels (Table 2). Average Rd-area rates d in high-light grown plants varied from 0.51 ␮mol ception of M. winkleri, Rd-mass was highest in either Ϫ2 Ϫ1 Ϫ2 Ϫ1 low- or medium-light environments for all species, but CO2´m ´s in M. hullettii to 0.90 ␮mol CO2´m ´s most of these differences were not statistically signif- in M. gigantea. Rd-mass was highest in M. trachyphylla Ϫ1 Ϫ1 and M. gigantea with rates Ͼ15 nmol CO2´g ´s in icant (Table 2). all light environments, and more than twice the Rd- The absolute plasticity in Rd, measured for each spe- mass rates of M. lamellata and M. hullettii at the other cies as the difference between highest and lowest mean extreme. rates in the three light environments, was positively

Eight Macaranga species had signi®cantly higher correlated with Rd in high light (Rd-area: rs ϭ 0.67, P

Rd-area for high-light grown seedlings than medium- ϭ 0.06; Rd-mass: rs ϭ 0.72, P ϭ 0.04). However, rel- or low-light seedlings (Table 2). Differences in Rd-area ative plasticity in Rd (the relative difference between between medium- and low-light grown plants were highest and lowest rates) was not signi®cantly corre- October 1998 PHOTOSYNTHESIS IN MACARANGA 2299

Ϫ2 Ϫ1 TABLE 3. Asymptotic light-saturated photosynthetic rate (Amax, ␮mol CO2´m ´s ) and light compensation point (LCP, ␮mol´mϪ2´sϪ1) derived from the modeled light response of photosynthesis, for nine Macaranga species grown in three PFD environments (high, medium, and low).

High Medium Low

2 2 2 Species Amax LCP r n Amax LCP r n Amax LCP r n hosei 10.95 (0.47) 17.5 0.96 265a 8.13 (0.44) 11.2 0.95 282b 6.88 (0.24) 6.9 0.95 253b winkleri 11.44 (0.54) 16.0 0.99 142a 7.27 (0.46) 8.4 0.95 146bc 7.16 (0.44) 8.0 0.96 139bc gigantea 9.18 (1.41) 20.0 0.95 213bcd 8.39 (0.97) 12.4 0.93 197c 6.81 (0.59) 11.6 0.95 189de hypoleuca 10.08 (0.82) 17.8 0.97 143b 7.73 (0.51) 10.5 0.94 147bc 7.85 (0.29) 8.4 0.97 151a beccariana 13.46 (1.64) 21.7 0.95 171a 10.39 (0.14) 11.6 0.91 211a 8.23 (0.64) 10.3 0.96 189b triloba 9.06 (0.47) 16.4 0.97 242bc 9.62 (1.42) 6.9 0.96 144bc 6.81 (0.71) 10.0 0.93 180e trachyphylla 9.74 (0.86) 18.0 0.98 133c 7.85 (0.58) 12.3 0.96 123bc 6.98 (0.45) 11.4 0.96 133cd hullettii 7.48 (0.37) 17.8 0.96 187c 6.80 (0.51) 6.3 0.95 185c 6.22 (0.25) 7.2 0.97 182cde lamellata 7.17 (0.58) 8.1 0.96 169d 4.62 (0.15) 6.5 0.97 184d 5.35 (0.43) 3.7 0.93 176f Notes: For the model, r2 is the coef®cient of determination, and n is the sample size. Values in parentheses are 95% con®dence intervals for parameter estimates. Different letters within each light treatment indicate signi®cantly different (P Ͻ 0.05) Amax-area rates among species, based on ScheffeÂ's tests of measured values at light saturation as presented in Fig. 2. Species are listed by successional ranking, from shade intolerant to tolerant as in Table 1.

lated with Rd in high light (Rd-area: rs ϭϪ0.45, P ϭ of Amax on a leaf-mass basis (Fig. 2). In only one spe-

0.20; Rd-mass: rs ϭ 0.47, P ϭ 0.19). cies, M. winkleri, was Amax-mass signi®cantly greater

For both Rd-area and Rd-mass there was evidence that in high-light grown plants than low-light plants; this dark respiration rates vary temporally within species. species also exhibited the least plasticity in LMA (Ta- Dark respiration was measured on two nights for all ble 2). Four species, including the three with lowest nine species. Four of the nine species showed a sig- Amax, had signi®cantly lower Amax-mass in high light ni®cant difference in Rd-mass or Rd-area between the than in low- and medium-light grown seedlings. Oth- two nights (P Ͻ 0.05, data not shown). Overall, how- erwise, Amax-mass was rather similar among light levels ever, the trends in Rd among species and light envi- (Fig. 2). ronments were similar between nights. Among species, absolute plasticity (as for Rd above) of A was signi®cantly positively correlated with A Comparative light response of photosynthesis max max in high-light grown plants on an area basis (rs ϭ 0.88, The nonrectangular hyperbola model described a P ϭ 0.01), but not on a mass basis (P ϭ 0.8). Relative high proportion of the variation in the response of pho- plasticity of Amax-area was weakly positively correlated tosynthesis to increasing light levels, as indicated by with Amax-area in high light (rs ϭ 0.67, P ϭ 0.06), while coef®cients of determination ranging from 0.91 to 0.99 relative plasticity of Amax-mass was weakly negatively

(Table 3). Modeled Amax values tended to be slightly correlated with Amax-mass in high light (rs ϭϪ0.57, P higher than mean values based on analyses of Amax mea- ϭ 0.11). surements at light saturation (Fig. 2); however the gen- Mean stomatal conductance at light saturation, gs, Ϫ2 Ϫ1 eral patterns were similar. Amax on both leaf area and varied from Ͼ0.25 mol H2O´m ´s in all three light mass bases varied signi®cantly among species. Amax- environments in M. beccariana and M. hosei, to near Ϫ2 Ϫ1 area in high-light grown plants ranged from 11±13 0.10 mol H2O´m ´s in M. lamellata (Table 2). High- Ϫ2 Ϫ1 ␮mol CO2´m ´s in species such as M. beccariana to light grown plants had signi®cantly higher gs than me- Ϫ2 Ϫ1 7±8 ␮mol CO2´m ´s in M. lamellata (Table 3). Amax- dium- or low-light seedlings in most species, but there mass also varied signi®cantly among species (P Ͻ were few signi®cant differences in gs between medium- 0.001), with the highest species' means being more and low-light grown plants (Table 2). Stomatal con- than twice the lowest means (Fig. 2). Macaranga wink- ductance was strongly positively correlated with pho- leri, with the lowest overall LMA, had the highest Amax- tosynthetic rate in all species and light environments Ϫ2 Ϫ1 mass (Ͼ230 nmol CO2´m ´s ) in all light environ- (Pearson r ϭ 0.67±0.92, mean r ϭ 0.84, for nine species ments. As with Amax-area, M. beccariana and M. hosei and three light levels). had very high mass-based rates of photosynthesis, and Apparent quantum yield, ␣, and light compensation

M. lamellata had signi®cantly lower Amax-mass rates point (LCP) also differed among species and light lev- than all other species in all light levels. els (Table 2). Among-species differences in ␣ showed

Amax-area was affected by light environment in all no obvious relationship to other ecophysiological traits, species (Fig. 2). Amax-area was signi®cantly greater in although M. lamellata had the highest values and M. high-light grown plants than medium- or low-light hosei and M. hullettii had the lowest values. Most spe- plants in eight species, and medium-light plants had cies tended to have higher ␣ in low-light grown plants; signi®cantly greater Amax-area than low-light grown ®ve of the differences were signi®cant (Table 2). Ma- plants in six species. As with dark respiration, the dra- caranga lamellata, with the lowest Amax rates, had the matic plasticity of LMA led to very different patterns lowest LCPs (Table 3). High-light plants of all species 2300 STUART JAMES DAVIES Ecology, Vol. 79, No. 7

FIG. 3. Relationships between seedling ecophysiological traits among nine Macaranga species grown in three light environments (high, medium, and low as described in Fig. 1). Data points are species' means at each of the three light levels. Ϫ2 Ϫ1 Regression relationships are listed below. (A) Leaf area-based net photosynthesis (Amax-area, ␮mol CO2´m ´s ) vs. stomatal Ϫ2 Ϫ1 2 conductance (gs, mol H2O´m ´s ) at light saturation. High light: Amax-area ϭ 5.47 ϩ 15.04gs, r ϭ 0.75, P ϭ 0.002; medium 2 2 light: Amax-area ϭ 3.88 ϩ 19.03gs, r ϭ 0.55, P ϭ 0.021; low light: Amax-area ϭ 4.71 ϩ 11.01gs, r ϭ 0.67, P ϭ 0.007. (B) Ϫ1 Ϫ1 Leaf mass-based net photosynthesis at light saturation (Amax-mass, nmol CO2´g ´s ) vs. mass-based dark respiration (Rd- Ϫ1 Ϫ1 2 mass, nmol CO2´g ´s ). High-light grown plants: Amax-mass ϭ 71.2 ϩ 9.63Rd-mass, r ϭ 0.50, P ϭ 0.033; medium light: 2 2 Amax-mass ϭ 121.1 ϩ 7.72Rd-mass, r ϭ 0.23, P ϭ 0.19; low light: Amax-mass ϭ 127.1 ϩ 5.36Rd-mass, r ϭ 0.28, P ϭ 0.14. 2 (C) Leaf mass-based net photosynthesis at light saturation vs. leaf mass per unit area (LMA, g/m ). High light: Amax-mass ϭ 2 2 539 Ϫ 6.50LMA, r ϭ 0.75, P ϭ 0.002; medium light: Amax-mass ϭ 555 Ϫ 9.10LMA, r ϭ 0.54, P ϭ 0.025; low light: Amax- mass ϭ 479 Ϫ 7.89LMA, r2 ϭ 0.72, P ϭ 0.004. (D) Leaf mass-based dark respiration vs. leaf mass per unit area. High light: 2 2 Rd-mass ϭ 38.68 Ϫ 0.49LMA, r ϭ 0.79, P ϭ 0.001; medium light: Rd-mass ϭ 27.35 Ϫ 0.41LMA, r ϭ 0.28, P ϭ 0.14; 2 low light: Rd-mass ϭ 29.23 Ϫ 0.45LMA, r ϭ 0.26, P ϭ 0.19. had higher LCPs than low- and medium-light grown not strongly correlated (P Ͼ 0.05 for all three light plants. levels), and on a leaf-mass basis Amax and Rd were correlated for high-light grown plants only (Fig. 3B). Ma- Relationships between leaf-level caranga gigantea and M. trachyphylla, with interme- ecophysiological traits diate photosynthetic rates, had the highest respiration

Relationships between ecophysiological traits among rates (Table 2). Rates of both Amax and Rd were nega- the nine Macaranga species were assessed for plants tively correlated with LMA when these traits were con- grown in each of the three light levels. Among species, sidered on a leaf-mass basis (Fig. 3C, D), but not on light-saturated net photosynthesis (Amax) was strongly a leaf-area basis. That is, ``thicker''-leaved species (as- positively correlated with maximum stomatal conduc- suming similar leaf densities) had intrinsically lower tance in all three light levels (Fig. 3A), as was the case Amax-mass and Rd-mass than ``thinner''-leaved species. within species. On a leaf-area basis, Amax and Rd were This pattern is different from the ®ndings within spe- October 1998 PHOTOSYNTHESIS IN MACARANGA 2301 cies, where LMA was signi®cantly greater in high-light grown plants, but Amax-mass and Rd-mass were typically not different among seedling light environments. Ap- parent quantum yield, ␣, and LCP, were not strongly correlated with other ecophysiological traits, although

LCP was positively related to Rd-area as might be ex- pected (data not shown). Relationships between photosynthetic and life history traits Life history traits vary considerably among the nine Macaranga species (Table 1). The PCA of life history traits revealed two signi®cant components (P Ͻ 0.05). No distinct groupings of the species can be recognized, rather the axes describe continua of life history variation (Fig. 4A). The ®rst PC of the analysis was strongly negatively related to shade tolerance and seed mass (Table 4), where shade tolerance was inferred from the distribution of individuals in the forest with respect to light levels (mean CI index). Macaranga lamellata, with the largest seeds, was also the most shade-tolerant species (Table 1), and M. winkleri, M. hosei, and M. gigantea, with considerably smaller seeds, were the most shade intolerant. The second PC of the life history analysis distinguished among the more shade-intolerant species: M. beccariana, M. winkleri, M. gigantea, and M. hosei (Fig. 4A). The former pair of species are smaller trees at maturity than the latter pair (Table 1). In addition, M. beccariana and M. winkleri have signi®cant size-dependent declines in diameter growth rates, and size-dependent increases in mortality rates, neither of which are found in M. gigantea and M. hosei (Table 1; Davies 1996). These traits were correlated with the second PC of the FIG. 4. Plots of the ®rst two components from the prin- life history analysis (Table 4). cipal components analyses of life history and ecophysiolog- The ®rst PC of the ecophysiological analysis was ical traits in nine species of Macaranga. (A) Analysis of life strongly positively related to photosynthetic potential, history traits as presented in Table 1. Percentage of variation with M. lamellata at the low extreme and M. beccariana explained by the ®rst two components: 1, 48%; 2, 27%. (B) Analysis of ecophysiological traits derived from the experi- at the high extreme (Fig. 4B, and Table 4). The second ment presented in this study. Traits were included for seed- PC of the ecophysiological analysis was negatively re- lings of all species grown in each of the three light environ- lated to respiration rates in all three light environments, ments: light-saturated photosynthetic rate on a leaf area basis M. gigantea and M. trachyphylla having particularly (Amax-area), maximum stomatal conductance (gs), dark respiration on a leaf area basis (Rd-area), apparent quantum yield high respiration rates. (␣), and leaf mass per unit area (LMA). Percentage of vari- The position of some of the more shade-intolerant ation explained by the ®rst two components: 1, 44%; 2, 24%. species differed between the ecophysiological and life See Table 4 for component loadings for traits strongly as- history analyses. Macaranga beccariana was more sociated with the ®rst two components of each analysis. Spe- similar to M. hosei in ecophysiological traits, but more cies indicated by letters: A, M. trachyphylla;B,M. beccariana;E,M. gigantea;L,M. triloba;M,M. lamellata;O,M. similar to M. winkleri in life history traits. Macaranga hosei;U,M. hullettii;W,M. winkleri; and Y, M. hypoleuca. hosei is a large high-light demanding tree similar in life history to M. gigantea, but these species differ considerably in seedling ecophysiology (Table 2). Ma- the only traits measured that were strongly related to caranga gigantea and M. trachyphylla share seedling the ®rst PC of the life history analysis (P Ͻ 0.05). Amax- ecophysiological similarities, but M. trachyphylla is a mass, for seedlings grown in all three light levels, was more shade-tolerant and smaller tree than M. gigantea positively correlated with CI index and negatively cor- (Table 1). related with seed mass (Fig. 5A, B). LMA was signif- The ®rst PC of the life history analysis provides a icantly negatively correlated with CI index and posi- quantitative ranking of the species along a successional tively correlated with seed mass (Fig. 5C, D). These continuum, against which to compare changes in leaf- relationships re¯ect higher Amax-mass and lower LMA level ecophysiological traits. Amax-mass and LMA were in the more shade-intolerant species. The plasticity of 2302 STUART JAMES DAVIES Ecology, Vol. 79, No. 7

TABLE 4. Component loadings for traits strongly associated with the ®rst two axes of the principal components analyses presented in Fig. 4. The ®ve traits with the highest component loadings are listed for each analysis: (a) analysis of life history traits and (b) analysis of ecophysiological traits.

Component I Component 2 a) Life history traits Shade tolerance Ϫ0.975 Mortality, IV Ϫ0.867 Seed mass Ϫ0.905 Staminate fecundity 0.683 Maximum height 0.792 Growth rate, I Ϫ0.672 Mortality, III 0.786 Mortality, II Ϫ0.662 Growth rate, III 0.728 Growth rate, IV 0.627 b) Ecophysiological traits

Amax-area, H 0.885 Rd-area, H Ϫ0.840 gs,M 0.866 Rd-area, L Ϫ0.793 Amax-area, L 0.853 ␣,H Ϫ0.753 Amax-area, M 0.808 Rd-area, M Ϫ0.691 gs,L 0.787 LMA, H 0.607 Notes: Life history traits for each of the nine species were based on two and a half years of surveys of tree populations growing in Lambir Hills National Park, Sarawak, Malaysia. Growth rate is median diameter growth rate, mortality rate is annual percentage mortality, shade tolerance is based on the mean crown illumination index, seed mass is on a dry mass basis, tree height is estimated maximum height, and fecundity is average annual ¯ower (staminate) or seed (pistillate) production. Growth and mortality rates were included in the analysis for trees in the four life-stage classes: I, seedling/sapling; II, prereproductive; III, reproductive; and IV, mature. See Methods for further details. Ecophysiological traits are derived from seedlings grown in either high (H), medium (M), or low (L) light levels (as described in Figs. 1 and 4).

Amax-mass was weakly positively correlated with the DISCUSSION successional ranking (r ϭ 0.62, P ϭ 0.08). R -mass s d Leaf-level ecophysiological variation in Macaranga and Rd-area were not signi®cantly related to the successional ranking of the species (P Ͼ 0.1 in all three This study demonstrated signi®cant variation in eco- light levels). As noted above, M. gigantea and M. tra- physiological responses to seedling light growth con- chyphylla differ in life history traits, yet have similarly ditions among nine Macaranga species. The light re- high Rd (Table 2), and Amax was only weakly correlated sponse of photosynthesis spanned a wide range, from M. beccariana with high rates of light saturated pho- with Rd in these species (Fig. 3). Growth and mortality were not strongly linked to the tosynthesis and stomatal conductance (Amax-area ϳ 13 Ϫ2 Ϫ1 Ϫ2 Ϫ1 primary successional ranking of the species (Table 4). ␮mol CO2´m ´s , and gs ϳ 0.60 mol´m ´s ), to M. However, variation in the size dependence of growth lamellata with relatively low rates of gas exchange Ϫ2 Ϫ1 and mortality rates distinguished among the more (Amax-area ϳ 7 ␮mol CO2´m ´s , and gs ϳ 0.10 Ϫ2 Ϫ1 shade-intolerant species (PC 2). To assess the extent to mol´m ´s ). This range is typical for seedlings of trop- which survival and growth re¯ect the seedling leaf- ical pioneer species grown in high-light environments (Strauss-Debenedetti and Bazzaz 1996). However, con- level ecophysiological traits that were associated with siderably higher rates of gas exchange have been re- the successional ranking, relationships between growth ported for seedlings (Oberbauer and Strain 1984) and and mortality and A -mass and LMA were examined max mature trees (Zotz and Winter 1994, Zotz et al. 1995) across the four life-stage classes (Fig. 6). There were of some pioneer species. Similar A rates have been size-dependent shifts in the A -mass vs. growth and max max reported for saplings of Macaranga species elsewhere the Amax-mass vs. mortality relationships. Seedling Amax- in Asia (e.g., Tan et al. 1994). Amax of mature trees of mass was strongly positively correlated with diameter Macaranga species are somewhat higher than the val- growth rates in the seedling/sapling life stage, but was ues reported here; preliminary data from ®eld studies not signi®cantly correlated with diameter growth rates in Brunei suggest that some of the study species have at larger tree sizes. In contrast, mortality rates were rates of up to 20 ␮mol´mϪ2´sϪ1 (S. J. Davies and W. least well correlated with Amax-mass at the seedling/ Booth, unpublished data; see also Koyama 1981). Dark sapling size class, but were strongly correlated with respiration rates, apparent quantum yield, and PFD at Amax-mass in larger size classes. LMA was strongly light compensation of Macaranga species in this study negatively correlated with growth rate in the ®rst three were also similar to values reported for other pioneer life-stage classes, but not for mature trees. LMA was trees and shrubs (Fredeen and Field 1991, Thompson not signi®cantly correlated with mortality rates across et al. 1992, Kamaluddin and Grace 1993). all tree sizes. All species exhibited substantial variation in gas ex- October 1998 PHOTOSYNTHESIS IN MACARANGA 2303

Ϫ1 Ϫ1 FIG. 5. Relationships between net photosynthesis (Amax-mass, nmol CO2´g ´s ) and leaf mass per unit area (LMA, g/m2) (vertical axes) and shade tolerance (CI index) and seed mass (mg) (horizontal axes) for nine species of Macaranga. Ecophysiological traits are derived from seedlings grown in three light levels: high (H), medium (M), and low (L) (see Fig.

1). Life history traits are as presented in Table 1. (A) Amax-mass vs. CI index, H: rs ϭ 0.61, P ϭ 0.08; M: rs ϭ 0.56, P ϭ 0.11; L: rs ϭ 0.46, P ϭ 0.19. (B) Amax-mass vs. seed mass, H: rs ϭϪ0.82, P ϭ 0.02; M: rs ϭϪ0.78, P ϭ 0.03; L: rs ϭ Ϫ0.62, P ϭ 0.08 (C) LMA vs. CI-index, H: rs ϭϪ0.74, P ϭ 0.04; M: rs ϭϪ0.71, P ϭ 0.05; L: rs ϭϪ0.55, P ϭ 0.12. (D) LMA vs. seed mass, H: rs ϭ 0.78, P ϭ 0.03; M: rs ϭ 0.90, P ϭ 0.01; L: rs ϭ 0.70, P ϭ 0.05. change characteristics among the three light levels in cessional or pioneer species have high plasticity in this experiment. Qualitatively, these responses were these traits (Bazzaz and Pickett 1980, see below). largely consistent with patterns observed for tropical Due to the high levels of plasticity in LMA in all trees from all successional stages (Langenheim et al. Macaranga species, Rd-mass and Amax-mass differences 1984, Kwesiga et al. 1986, Ramos and Grace 1990, among light treatments were much less than for area- Strauss-Debenedetti and Bazzaz 1991, Thompson et al. based comparisons. This trend has also been observed 1992, Newell et al. 1993). High-light grown seedlings in other tropical tree species (Kitajima 1994). The more produced leaves with a higher LMA than low- or me- ef®cient distribution of photosynthetic tissue with re- dium-light grown plants, and they also had higher rates spect to incident PFD, the lower ratio of structural to of Rd-area, Amax-area, gs, and higher irradiance at light photosynthetic tissues (Strauss-Debenedetti and Berlyn saturation and compensation. Apparent quantum yield, 1994), and/or the greater leaf surface area available for

␣, was mostly lower in high-light plants, consistent CO2 diffusion may result in equivalent or often higher with some studies (e.g., Langenheim et al. 1984, Ob- Amax on a mass basis in leaves of shade-grown seedlings erbauer and Strain 1985), but contrary to others (e.g., (Field and Mooney 1986, Reich and Walters 1994). Rd- Kwesiga et al. 1986, Wiebel et al. 1993). Furthermore, mass was more or less equivalent among light treat- the large quantitative differences in ecophysiological ments for most species; the corollary of this is that and morphological responses between light levels for survival and growth in low-light environments in these all species are consistent with the view that early suc- species may largely depend on shifts in the allocation 2304 STUART JAMES DAVIES Ecology, Vol. 79, No. 7

Consequently, single-leaf estimates of Rd may not be a good indicator of whole plant respiration rates and compensation points (Givnish 1988, Lehto and Grace

1994). The temporal variation in Rd remains unex- plained, although for some species there was variation in ambient temperatures between the different measurement nights.

The differences in Amax among Macaranga species were greatest in high-light grown seedlings; however

the rank order of species for Amax (on both area and mass bases) was very similar among light treatments.

Whereas within-species Amax-mass tended to be very similar among light treatments, among-species differ-

ences in Amax-mass were greater than Amax-area differences. This was due to the different patterns of LMA variation within and among Macaranga species. Within species, LMA was higher in plants grown at high PFD levels, yet among species the more high-light demand-

ing species (higher Amax) tended to have lower LMA. Kitajima (1994) reported a similar result for 13 tropical tree species spanning a wide range of successional positions, and suggested that within-species responses to light gradients ran counter to among-species evolutionary trends. The tendency for LMA to increase in later successional species has been reported for other tropical trees, and is often correlated with lower nitrogen concentration per unit leaf mass (Reich et al. 1991, Raaimakers et al. 1995), increased leaf longevity (Reich et al. 1992), and the importance of maintaining leaves that are resistant to herbivores and pathogens (Kitajima 1994). The plasticity of ecophysiological responses to light environments, also varied signi®cantly among the nine Macaranga species. Plasticity was assessed as the absolute difference in response between high and low light, and as the relative difference in response between high and low light. The degree of plasticity, of course, depends in part on the range of experimental treatment FIG. 6. Size dependence of the relationships between of the plants (Strauss-Debenedetti and Bazzaz 1996). seedling leaf-level ecophysiological traits and tree growth and The light levels used for this study were selected to mortality rates of forest growing trees for nine species of mimic a large-scale canopy opening, a medium-sized Macaranga. (A) Light saturated photosynthetic rate (Amax- mass) vs. growth and mortality. (B) Leaf mass per unit area forest gap, and a relatively bright understory. The low- (LMA) vs. growth and mortality. Ecophysiological traits are light treatment (ϳ3.6 mol´mϪ2´dϪ1) represents ϳ10% of for high-light grown plants, and growth and mortality rates full sun in north Borneo. All nine species grew suc- are given in Table 1. The four tree life-stage classes are: I, cessfully in the low-light treatment, and coupled with seedling/sapling; II, prereproductive; III, reproductive; and IV, mature. Values are Spearman rank correlation coef®cients the low LCPs measured for the species, it appears that for each variable among the nine species. Note negative cor- they would all have survived and grown at somewhat relations in (B). The dashed line refers to the P ϭ 0.05 sig- lower light levels. Nevertheless, the absolute plasticity ni®cance level in each graph. of Amax-area, Rd-area, and Rd-mass (but not Amax-mass) was positively correlated with the maximum performance of each of these traits in high-light grown seed- of plant biomass that maximize photosynthetic ability lings, indicating a trend toward greater plasticity in (Kitajima 1994). It is important to note, however, that Macaranga species with higher respiration or photo- signi®cant differences in Rd were observed for some synthetic rates, as has been found in numerous studies species on different nights, indicating that Rd-mass may (Bazzaz and Carlson 1982, Oberbauer and Strain 1984, vary in the short term in response to factors such as Chazdon 1992). Relative plasticity of Amax and Rd was carbohydrate status (Sims and Pearcy 1991), average not correlated or was only weakly correlated (for Amax- daily PFD, and leaf life span (Fredeen and Field 1991). area) with maximum performance in each trait. October 1998 PHOTOSYNTHESIS IN MACARANGA 2305

Dark respiration and Amax were positively correlated and Williamson 1989), may indicate greater suscepti- on a mass basis among species in high-light grown bility to herbivores or pathogens. Consequently, sur- seedlings, although the relationship was weaker on an vival ability in low light may depend on both low res- area basis. The substantially higher Rd-mass rates in piration rates and allocation patterns. Whilst Rd was species with higher Amax-mass suggests a trade-off be- signi®cantly lower in the more shade-tolerant species tween photosynthetic capacity and respiratory cost (M. lamellata and M. hullettii), Rd varied signi®cantly among these species. This relationship may be an im- among the more shade-intolerant species; overall there- portant determinant of the degree of shade that the fore, Rd was not strongly linked to the successional different Macaranga species can tolerate (Walters and ranking of the species. Whether the differences in leaf- Field 1987, Sims and Pearcy 1989), such as in small level dark respiration rates among some of the more gaps or following canopy closure of a gap. Macaranga shade-intolerant species re¯ect differences in whole- lamellata and M. hullettii, the species with the lowest plant respiration rates, and consequently differences in

Rd rates and LCPs, can inhabit considerably more shady the minimum forest light levels inhabitable requires forest microsites than the other species (Davies 1996). further study. Mortality rates of seedling/saplings were

The relatively high Rd rates in M. gigantea and M. not correlated with leaf-level ecophysiological traits trachyphylla cannot be easily explained; however, it is (Fig. 6); however, this life-stage class included plants interesting to note that these species have the largest of up to 2 cm dbh, and the links between ecophysio- seedling leaves and enormous sapling leaves (Whit- logical processes and survival may function at very more 1969). early developmental stages that could not be detected in this study. Leaf-level ecophysiological and life history variation Both Amax and LMA were signi®cantly correlated A suite of ecophysiological and life history traits are with growth rates in the seedling/sapling life-stage typically associated with the plants that appear early (Fig. 6). However, due to variation among the more in tropical forest succession (Bazzaz 1979). However, shade-intolerant species, growth rates were not strongly rarely have studies attempted to directly assess the links linked to the successional ranking. Higher Amax-mass between leaf-level processes and broader ®eld-based and lower LMA have been consistently found in species life history phenomena (although see Kitajima 1994). with faster seedling growth rates (e.g., Reich et al.

In this study, I conducted a multivariate analysis of a 1992, Walters et al. 1993). Amax and LMA were much suite of life history traits to rank species along a suc- less well correlated with the growth rates of trees in cessional gradient, and then used this ranking to assess later life stages. Whilst the species with the lowest Amax patterns of variation in leaf-level ecophysiological rates had the lowest growth rates at all life stages, the traits. Whilst this approach is nonmechanistic in as- more shade-intolerant species varied signi®cantly in sessing correlations between different levels of plant the ontogeny of growth rates (Davies 1996). Whether organization, it does provide insight into the inherent the size-dependent changes in growth rates of some of functional interdependencies of the numerous traits that the more shade-intolerant species (e.g., M. winkleri) characterize early successional species. are correlated with changes in mature-tree, leaf-level The ®rst axis of the multivariate analysis of life his- ecophysiology requires further study. tory traits was strongly associated with variation in Seed mass was strongly positively related to the axis shade tolerance and seed mass. The distribution of trees of successional ranking (shade tolerance) among the of all size classes with respect to light levels in the nine Macaranga species. Amax was signi®cantly lower forest was used as an index of shade tolerance (see and LMA signi®cantly higher in the larger seeded spe- Methods). Other researchers have de®ned shade tol- cies. Seed mass has been found to be related to shade erance based on light requirements for germination and tolerance in some studies (Metcalfe and Grubb 1995) establishment (Swaine and Whitmore 1988), or growth but not in others (Kelly and Purvis 1993, Osunkoya et or survival rates in low light (Augspurger 1984, Popma al. 1994), and Grubb and Metcalfe (1996) argue that and Bongers 1988, Kitajima 1994), and clearly shade traits other than seed mass are probably more important tolerance is the result of a combination of traits (Wal- in conferring shade tolerance. Further comparative ters and Reich 1996). Among the ecophysiological studies with the ϳ300 pioneer and nonpioneer Macar- traits measured, only Amax-mass and LMA were strongly anga species may help clarify the relative importance correlated with the primary axis of life history varia- of seed size in contributing to shade tolerance in this tion. Therefore, both photosynthetic and morphological group. However, the results of this study stress that a attributes change along the species' successional rank- suite of traits potentially contribute to variation in ing, as has been found in other studies (e.g., Reich et shade tolerance. al. 1995, Ellsworth and Reich 1996). Amax was nega- Leaf-level ecophysiological variation was not tively, and LMA positively, correlated with shade tol- strongly related to estimated maximum tree height, erance (see also Kitajima 1994). The species with high- even though tree height is an important axis of life er Amax having signi®cantly ``thinner'' leaves (lower history variation among Macaranga species (Davies LMA), and probably lower wood density (Weimann 1996). This ®nding is in direct contrast with a study 2306 STUART JAMES DAVIES Ecology, Vol. 79, No. 7 of shade-tolerant rain forest trees in Malaysia (Thomas Department helped with many aspects of the experimental 1993), in which photosynthetic capacity was positively work. David Ackerly, Peter Ashton, Fakhri Bazzaz, Jaime Cavalier, Robin Chazdon, Elizabeth Farnsworth, Peter correlated with maximum tree height. It was argued Wayne, and two anonymous reviewers improved the manu- that the vertical gradient in light availability under a script greatly with their comments and suggestions. closed forest canopy results in species of different sizes LITERATURE CITED intercepting different light levels with their intrinsic Ackerly, D. D. 1996. Canopy structure and dynamics: In- physiologies re¯ecting this (Thomas 1993). In early tegration of growth processes in tropical pioneer trees. successional environments, consistent vertical light Pages 619±658 in S. S. Mulkey, R. L. Chazdon, and A. P. gradients are probably much less distinct, so PFD levels Smith, editors. Tropical forest plant ecophysiology. Chap- through ontogeny may be independent of species' size. man and Hall, New York, New York, USA. Ashton, P. M. S. 1992. Leaf adaptations of some Shorea Indeed, in this study, among the species with the higher species to sun and shade. New Phytologist 121:587±596. assimilation rates Macaranga hosei grows to 30 m in Ashton, P. S., and P. Hall. 1992. Comparisons of structure height and M. beccariana is a small tree of ϳ17 m. among mixed dipterocarp forests of north-western Borneo. The nine Macaranga species studied here vary dra- Journal of Ecology 80:459±481. matically in leaf-level ecophysiological and life history Augspurger, C. K. 1984. Light requirements of neotropical tree seedlings: a comparative study of growth and survival. attributes, supporting the notion that pioneer species Journal of Ecology 72:777±796. (Swaine and Whitmore 1988, Bazzaz 1991) encompass Baillie, I. C., P. S. Ashton, M. N. Court, J. A. R. Anderson, a considerable diversity of characteristics, including E. A. Fitzpatrick, and J. Tinsley. 1987. Site characteristics ecophysiological, demographic, and architectural fea- and the distribution of tree species in mixed dipterocarp forest on Tertiary sediments in central Sarawak, Malaysia. tures, and that different functional interactions between Journal of Tropical Ecology 3:201±220. these traits lead to different pioneer life histories. To Bazzaz, F. A. 1979. Physiological ecology of plant succes- what extent does the variation in photosynthetic light sion. Annual Review of Ecology and Systematics 10:351± response determine the distribution of species in the 371. forest? All nine species are common gap specialists . 1991. Regeneration of tropical forests: Physiological responses of pioneer and secondary species. Pages 91±118 (see note above on M. lamellata) in Borneo; indeed, in A. Gomez-Pompa, T. C. Whitmore, and M. Hadley, ed- many of the species are sympatric on small spatial itors. Rain forest regeneration and management. The Par- scales (Davies et al. 1998). It seems likely that the thenon Publishing Group, Parkridge, New Jersey, USA. limitations imposed by high respiration rates at low Bazzaz, F. A., and R. W. Carlson. 1982. Photosynthetic acclimation to variability in the light environment of early PFD levels, coupled with allocational limitations, may and late successional plants. Oecologia 54:313±316. be an important determinant of species' spatial distri- Bazzaz, F. A., and S. T. A. Pickett. 1980. The physiological butions in the forest. This situation is analogous to ecology of tropical succession: a comparative review. An- relatively high-light demanding Piper species that dif- nual Review of Ecology and Systematics 11:287±310. fer in dark respiration rates (Walters and Field 1987). Brokaw, N. V. L. 1987. Gap-phase regeneration of three pioneer tree species in a tropical forest. Journal of Ecology Among the higher Amax-species of Macaranga, mortal- 75:9±19. ity rates were signi®cantly increased in low-light forest Chazdon, R. L. 1986. Physiological and morphological basis environments (Davies 1996), but whether this was due of shade tolerance in rain forest understory palms. Principes to high respiration rates and LCPs or the lower LMA 30:92±99. . 1992. Photosynthetic plasticity of rain forest shrubs and less durable leaves is not known. Ultimately, the across natural gap transects. Oecologia 92:586±595. extent to which the rather subtle differences in assim- Chazdon, R. L., and N. Fetcher. 1984. Photosynthetic light ilation rates among the more high-light demanding of environments in a lowland tropical rainforest in Costa Rica. the Macaranga species in¯uences their ecological pref- Journal of Ecology 72:553±564. erences, remains to be explored in concert with the Chiariello, N. R., C. B. Field, and H. A. Mooney. 1987. Midday wilting in a tropical pioneer tree. Functional Ecol- importance of other limiting resources such as water ogy 1:3±11. and soil nutrients. Clark, D. A., and D. B. Clark. 1992. Life history diversity of canopy and emergent trees in a neotropical rain forest. ACKNOWLEDGMENTS Ecological Monographs 62:315±344. The experiment described in this paper was carried out Davies, S. J. 1996. The comparative ecology of Macaranga during a research fellowship at the University of Brunei Da- (Euphorbiaceae). Dissertation. Harvard University, Cam- russalam. I am extremely grateful to the University and Gov- bridge, Massachussetts, USA. ernment of Brunei for their ®nancial and logistical support. Davies, S. J., and P. Becker. 1996. Floristic composition and I thank the Government and Forestry Department of Sarawak, stand structure of mixed dipterocarp and heath forests in Malaysia, for permission to work in Lambir Hills National Brunei Darussalam. Journal of Tropical Forest Science 8: Park. The 52-ha Long Term Ecological Research plot is run 542±569. by the Sarawak Forest Department in collaboration with Har- Davies, S. J., P. A. Palmiotto, P. S. Ashton, H. S. Lee, and vard University (NSF award DEB 9107247 to P. S. Ashton) J. V. LaFrankie. 1998. Comparative ecology of 11 sym- and Osaka City University, Japan. The research was also patric species of Macaranga in Borneo: tree distribution in funded by a student grant from the Department of Organismic relation to horizontal and vertical resource heterogeneity. and Evolutionary Biology at Harvard University. The per- Journal of Ecology 86, in press. mission of the Brunei Forestry Department to use their nurs- Ellsworth, D. S., and P. B. Reich. 1996. Photosynthesis and ery facilities is gratefully acknowledged. Peter Becker, Web- leaf nitrogen in ®ve Amazonian tree species during early ber Booth, Martin Barker, and the staff of the Brunei Forestry secondary succession. Ecology 77:581±594. October 1998 PHOTOSYNTHESIS IN MACARANGA 2307

Evans, J. R., I. Jakobsen, and E. Ogren. 1993. Photosynthetic requirements for regeneration in southeast Asian rain for- light-response curves 2. Gradients of light absorption and est. Canadian Journal of Botany 73:817±826. photosynthetic capacity. Planta 189:191±200. Moad, A. S. 1992. Dipterocarp juvenile growth and under- Field, C., and H. A. Mooney. 1986. The photosynthesis± storey light availability in Malaysian tropical forest. Dis- nitrogen relationship in wild plants. Pages 25±55 in T. J . sertation. Harvard University, Cambridge, Massachusetts, Givnish, editor. On the economy of plant form and function. USA. Cambridge University Press, Cambridge, UK. Mulkey, S. S., S. J. Wright, and A. P. Smith. 1993. Com- Field, C. B. 1988. On the role of photosynthetic responses parative physiology and demography of three Neotropical in constraining the distribution of rainforest plants. Aus- forest shrubs: alternative shade-adaptive character syn- tralian Journal of Plant Physiology 15:343±358. dromes. Oecologia 96:526±536. Franklin, S. B., D. J. Gibson, P. A. Robertson, J. T. Pohlmann, Newell, E. A., E. P. McDonald, B. R. Strain, and J. S. Dens- and J. S. Fralish. 1995. Parallel analysis: a method for low. 1993. Photosynthetic responses of Miconia species determining signi®cant principal components. Journal of to canopy openings in a lowland tropical rainforest. Oec- Vegetation Science 6:99±106. ologia 94:49±56. Fredeen, A. L., and C. B. Field. 1991. Leaf respiration in Oberbauer, S. F., and B. R. Strain. 1984. Photosynthesis and Piper species native to a Mexican forest. Physiologia Plan- successional status of Costa Rican rain forest species. Pho- tarum 82:85±92. tosynthesis Research 5:227±232. Givnish, T. J. 1988. Adaptation to sun and shade: A whole Oberbauer, S. F., and B. R. Strain. 1985. Effects of light plant perspective. Australian Journal of Plant Physiology regime on the growth and physiology of Pentaclethra ma- 15:63±92. croloba (Mimosaceae) in Costa Rica. Journal of Tropical Grubb, P. J., and D. J. Metcalfe. 1996. Adaptation and inertia Ecology 1:303±320. in the Australian tropical lowland rainforest ¯ora: contra- Ogren, E., and J. R. Evans. 1993. Photosynthetic light-re-

dictory trends in intergeneric and intrageneric comparisons sponse curves I. The in¯uence of CO2 partial pressure and of seed size in relation to light demand. Functional Ecology leaf inversion. Planta 189:182±190. 10:512±520. Osunkoya, O. O., J. E. Ash, M. S. Hopkins, and A. W. Gra- Hogan, K. P. 1988. Photosynthesis in two neotropical palm ham. 1994. In¯uence of seed size and seedling ecological species. Functional Ecology 2:371±377. attributes on shade-tolerance of rain forest tree species in Hubbell, S. P., and R. B. Foster. 1983. Diversity of canopy northern Queensland. Journal of Ecology 82:149±163. trees in a neotropical forest and implications for conser- Poorter, L., and S. F. Oberbauer. 1993. Photosynthetic in- vation. Pages 25±41 in S. L. Sutton, T. C. Whitmore, and duction responses of two rainforest tree species in relation C. Chadwick, editors. Tropical rain forest: ecology and to light environment. Oecologia 96:193±199. management. Serial Publication Number 2 of the British Popma, J., and F. Bongers. 1988. The effect of canopy gaps Ecological Society. Blackwell Scienti®c, Oxford, UK. on growth and morphology of seedlings of rain forest spe- Huc, R., A. Ferhi, and J. M. Guehl. 1994. Pioneer and late cies. Oecologia 75:625±632. stage tropical rain forest tree species (French Guiana) grow- Popma, J., F.Bongers, M. MartõÂnez-Ramos, and E. Veneklaas. ing under common conditions differ in leaf gas exchange 1988. Pioneer species distribution in treefall gaps in Neo- regulation, carbon isotope discrimination and leaf water tropical rainforest; a gap de®nition and its consequences. potential. Oecologia 99:297±305. Journal of Tropical Ecology 4:77±88. Kamaluddin, M., and J. Grace. 1993. Growth and photo- Raaimakers, D., R. G. A. Boot, P. Dijkstra, S. Pot, and T. synthesis of tropical forest tree seedlings (Bischo®a javan- Pons. 1995. Photosynthetic rates in relation to leaf phos- ica Blume) as in¯uenced by a change in light availability. phorus content in pioneer versus climax tropical rain forest Tree Physiology 13:189±201. trees. Oecologia 102:120±125. Kelly, C. K., and A. Purvis. 1993. Seed size and establish- Ramos, J., and J. Grace. 1990. The effects of shade on the ment conditions in tropical trees. On the use of taxonomic gas exchange of seedlings of four tropical trees from Mex- relatedness in determining ecological patterns. Oecologia ico. Functional Ecology 4:667±677. 94:356±360. Reich, P. B. 1995. Phenology of tropical forests: patterns, Kitajima, K. 1994. Relative importance of photosynthetic causes, and consequences. Canadian Journal of Botany 73: traits and allocation patterns as correlates of seedling shade 164±174. tolerance of 13 tropical trees. Oecologia 98:419±428. Reich, P. B., D. S. Ellsworth, and C. Uhl. 1995. Leaf carbon Koyama, H. 1981. Photosynthetic rates in lowland rain forest and nutrient assimilation and conservation in species of trees of Peninsular Malaysia. Japanese Journal of Ecology differing successional status in an oligotrophic Amazonian 31:361±369. forest. Functional Ecology 9:65±76. Kwesiga, F. R., J. Grace, and A. P. Sandford. 1986. Some Reich, P. B., C. Uhl, M. B. Walters, and D. S. Ellsworth. photosynthetic characteristics of tropical timber trees as 1991. Leaf lifespan as a determinant of leaf structure and affected by the light regime during growth. Annals of Bot- function among 23 amazonian tree species. Oecologia 86: any 58:23±32. 16±24. Langenheim, J. H., C. B. Osmond, A. Brooks, and P. J. Ferrar. Reich, P. B., and M. B. Walters. 1994. Photosynthesis±ni- 1984. Photosynthetic responses to light in seedlings of se- trogen relations in Amazonian tree species. II. Variation in lected Amazonian and Australian rainforest tree species. nitrogen vis-a-vis speci®c leaf area in¯uences mass- and Oecologia 63:215±224. area-based expressions. Oecologia 97:73±81. Lehto, T., and J. Grace. 1994. Carbon balance of tropical Reich, P. B., M. B. Walters, and D. S. Ellsworth. 1992. Leaf tree seedlings: a comparison of two species. New Phytol- life-span in relation to leaf, plant, and stand characteristics ogist 127:455±463. among diverse ecosystems. Ecological Monographs 62: Manokaran, N., J. V. LaFrankie, K. M. Kochummen, E. S. 365±392. Quah, J. E. Klahn, P. S. Ashton, and S. P. Hubbell. 1990. Riddoch, I., J. Grace, F. E. Fasehun, B. Riddoch, and D. O. Methodology for the ®fty hectare research plot at Pasoh Lapido. 1991a. Photosynthesis and successional status of Forest Reserve. Forest Research Institute Malaysia, Ke- seedlings in a tropical semi-deciduous rain forest in Ni- pong, Malaysia. geria. Journal of Ecology 79:491±503. Metcalfe, D. J., and P. J. Grubb. 1995. Seed mass and light Riddoch, I., T. Lehto, and J. Grace. 1991b. Photosynthesis 2308 STUART JAMES DAVIES Ecology, Vol. 79, No. 7

of tropical tree seedlings in relation to light and nutrient Thomas, S. C. 1993. Interspeci®c allometry in Malaysian supply. New Phytologist 119:137±147. rain forest trees. Dissertation. Harvard University, Cam- Ross, G. J. S. 1981. The use of non-linear regression methods bridge, Massachusetts, USA. in crop modelling. Pages 269±282 in D. A. Rose and D. . 1995. Asymptotic height as a predictor of growth A. Charles-Edwards, editors. Mathematics and plant phys- and allometric characteristics in Malaysian rain forest trees. iology. Academic Press, London, UK. American Journal of Botany 83:556±566. SarukhaÂn, J., D. Pinero, and M. Martinez-Ramos. 1985. Plant Thompson, W. A., L.-K. Huang, and P. E. Kriedeman. 1992. demography: A community-level interpretation. Pages 17± Photosynthetic response to light and nutrients in sun-tol- 31 in J. White, editors. Studies on plant demography: a erant and shade-tolerant rainforest trees. II. Leaf gas ex- festschrift for John L. Harper. Academic Press, London, change and component processes of photosynthesis. Aus- UK. tralian Journal of Plant Physiology 19:19±42. Sheil, D., D. F. R. P. Burslem, and D. Alder. 1995. The Tinoco-Ojanguren, C., and R. W. Pearcy. 1995. A compar- interpretation and misinterpretation of mortality rate mea- ison of light quality and quantity effects on the growth and sures. Journal of Ecology 83:331±333. steady-state and dynamic photosynthetic characteristics of Sims, D. A., and R. W. Pearcy. 1989. Photosynthetic char- three tropical tree species. Functional Ecology 9:222±230. acteristics of a tropical forest understorey herb, Alocasia Walters, M. B., and C. B. Field. 1987. Photosynthetic light macrorrhiza, and a related crop species, Colocasia escu- acclimation in two rainforest Piper species with different lenta, grown in contrasting light environments. Oecologia ecological amplitudes. Oecologia 72:449±456. 79:53±59. Walters, M. B., E. L. Kruger, and P. B. Reich. 1993. Relative Sims, D. A., and R. W. Pearcy. 1991. Photosynthesis and growth rate in relation to physiological and morphological respiration in Alocasia macrorrhiza following transfers to traits for northern hardwood tree seedlings: species, light environment and ontogenetic considerations. Oecologia 96: high and low light. Oecologia 86:447±453. 219±231. Sipe, T. W. 1994. Gap partitioning among maples (Acer)in Walters, M. B., and P. B. Reich. 1996. Are shade tolerance, central New England: shoot architecture and photosynthe- survival, and growth linked? Low light and nitrogen effects sis. Ecology 75:2318±2332. on hardwood seedlings. Ecology 77:841±853. Sokal, R. R., and F. J. Rohlf. 1981. Biometry. Freeman, New Weimann, M. C., and G. B. Williamson. 1989. Wood speci®c York, New York, USA. gravity gradients in tropical dry and montane rain forest Strauss-Debenedetti, S., and F. A. Bazzaz. 1991. Plasticity trees. American Journal of Botany 76:924±928. and acclimation to light in tropical Moraceae of different Whitmore, T. C. 1969. First thoughts on species evolution successional positions. Oecologia 87:377±387. in Malayan Macaranga (Studies in Macaranga III). Bio- Strauss-Debenedetti, S., and F. A. Bazzaz. 1996. Photosyn- logical Journal of the Linnean Society 1:223±231. thetic characteristics of tropical trees along successional . 1981. Macaranga in New Guinea and the Bismarck gradients. Pages 162±186 in S. Mulkey, R. L. Chazdon, Archipelago. Kew Bulletin 34:599±606. and A. P. Smith, editors. Tropical forest ecophysiology. Wiebel, J., D. Eamus, E. K. Chacko, W. J. S. Downton, and Chapman and Hall, New York, New York, USA. P. Ludders. 1993. Gas exchange characteristics of man- Strauss-Debenedetti, S., and G. P. Berlyn. 1994. Leaf ana- gosteen (Garcinia mangostana L.) leaves. Tree Physiology tomical responses to light in ®ve tropical Moraceae of dif- 13:55±69. ferent successional status. American Journal of Botany 81: Wilkinson, L. 1990. SYSTAT: The system for statistics. 1582±1591. SYSTAT, Evanston, Illinois, USA. Swaine, M. D., and T. C. Whitmore. 1988. On the de®nition Zotz, G., G. Harris, M. Koniger, and K. Winter. 1995. High of ecological species groups in tropical rainforests. Vege- rates of photosynthesis in the tropical pioneer tree, Ficus tatio 75:81±86. insipida Willd. Flora 190:265±272. Tan, G. C.-H., B.-L. Ong, and I. M. Turner. 1994. The pho- Zotz, G., and K. Winter. 1994. Photosynthesis of a tropical tosynthetic performance of six early successional tropical tree, Ceiba pentandra, in a lowland forest in Panama. Tree tree species. Photosynthetica 30:201±206. Physiology 14:1291±1301.