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Ecology |
2Department of Botany, University of Florida, Gainesville, Florida 32611 USA; 3Smithsonian Tropical Research Institute, Box 2072, Balboa, Ancon, Panama
Received for publication February 12, 2002. Accepted for publication June 27, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: leaf age • leaf longevity • leaf nitrogen content • leaf position • photosynthetic capacity • self-shading • tropical trees
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Zotz and Winter, 1994
; Ackerly and Bazzaz, 1995
; Kitajima, Mulkey, and Wright, 1997a
). This decline is not an uncontrolled physiological deterioration, but is caused by a redistribution of resources, especially nitrogen, to younger leaves for optimization of whole-shoot photosynthetic income (Field and Mooney, 1983
; Hikosaka, Terashima, and Katoh, 1994
; Ackerly, 1996
). Consideration of the effect of leaf age on photosynthetic capacity (A) is necessary to estimate the long-term carbon budget of a leaf and of the whole crown. The effect of leaf age on photosynthetic capacity is also critical in cost-benefit theories of optimal leaf longevity (Kikuzawa, 1991
) in which total daily photosynthetic income, not photosynthetic capacity, is modeled. However, the former can be estimated as a linear function of the latter (Zotz and Winter, 1994
). Thus, if we can approximate the functional form of the decrease in photosynthetic capacity with leaf age, it will be possible to model long-term carbon budgets for whole crowns.
A linear decrease of photosynthetic capacity (At) with time after full leaf expansion (t) may be expressed in a following equation (Kikuzawa, 1991
):
 | (1) |
; Makino, Mae, and Ohira, 1984
; Ackerly and Bazzaz, 1995
). However, in tropical tree species with greater leaf lifetimes of 174–315 d, b was significantly greater than actual leaf longevity (Kitajima, Mulkey, and Wright, 1997a
).
A cost-benefit analysis incorporating this function suggests that leaf longevity is expected to be short when the initial net photosynthetic rate of the leaf (a) is high and/or the decline rate (a/b) is fast (Kikuzawa, 1991
). A negative correlation between mean leaf longevity and initial photosynthetic capacity (model parameter a, or y intercept of regression) has been demonstrated across a variety of plant species both locally and globally (Koike, 1988
; Reich et al., 1991
; Reich, Walters, and Ellsworth, 1992
; Mulkey, Kitajima, and Wright, 1995
). In contrast, data for the interspecific relationship between leaf longevity and the slope of the A–leaf age relationship (parameter a/b) are scarce, but our earlier study (Kitajima, Mulkey, and Wright, 1997a
) supported Kikuzawa's prediction.
Two sampling schemes are commonly employed for determining the A–leaf age relationship: repeated measurements of the same individual leaves (Scheme 1) and measurements of leaves with contrasting ages and positions within a branch on a given sampling day (Scheme 2, possible only for species with successive leaf production). These two methods, however, may yield different results because leaves produced in different seasons may differ in initial photosynthetic capacity and rates of decline (Field and Mooney, 1983
; Kitajima, Mulkey, and Wright, 1997a
, b
). Even if all sampled leaves are produced within the same season, Scheme 2 may underestimate the decline rate, because leaf lifetime varies within branches, trees, and populations, and rapidly aging leaves that die young are underrepresented in Scheme 2. This bias has not been evaluated in most studies that have examined A–leaf age relationships.
In a species with successive leaf production, the slope of the A–leaf age relationship should be a function of rates of leaf production and of the development of within-branch self-shading (Kikuzawa, 1995
; Ackerly, 1996
), which in turn is a function of light and nitrogen availabilities experienced by the leaves (Hikosaka, Terashima, and Katoh, 1994
; Ackerly and Bazzaz, 1995
). Within a single architectural type (e.g., orthotropic branch with successive leaf production), functional leaf traits that affect self-shading, such as leaf size, leaf mass per area, and leaf production rates, vary greatly among tropical tree species. In addition, the consequences of heterogeneity in light and nitrogen availability among branches and individuals on the A–leaf age relationship and leaf longevity have not been adequately addressed for adult canopy trees.
Here, we report the rate of decline of photosynthetic capacity with leaf age for two tropical canopy tree species whose leaf longevity (74–94 d) is much shorter than the five tree species studied earlier at the same site (Kitajima, Mulkey, and Wright, 1997a
) but longer than Heliocarpus appendiculatus studied by Ackerly and Bazzaz (1995)
. Leaf age from the time of leaf full expansion was determined more precisely with weekly censuses than in our earlier study with monthly censuses. The objectives of our current study are: (1) to fill a gap in empirical data of a/b parameter in the A–leaf age relationship for tropical species with intermediate leaf longevity; (2) to evaluate the difference between the two sampling schemes; (3) to examine whether among-leaf variation in the A–leaf age relationship is related to leaf production rates among branches; (4) to compare two species that are similar in leaf longevity and overall architecture (orthotropic branches and successive leaf production) but differ in the maximum leaf number per shoot and range of light environments experienced by the leaves; (5) to explore the functional basis for the A–leaf age relationship by examining relationships among leaf age, leaf position, light microenvironment, leaf mass per area, nitrogen contents, and photosynthetic capacity in greater detail than in our earlier study.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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).
Species, leaf census, and sampling
Cecropia longipes Pitt. (Cecropiaceae, mature height 10–15 m) and Urera caracasana (Jacq) Griseb (Urticaceae, mature height 5–10 m) are common pioneer trees at the study site (nomenclature following D'Arcy, 1987
). They are deciduous during the dry season and start producing leaves in mid-April. Both species successively produce leaves throughout the rainy season on orthotropic branches in whirls. None of the marked terminal branches developed a secondary branch during the study. The total number of leaves per branch increased in both species between the first census (13 May 1996) and the last census in which we marked new leaves (19 August 1996) (Table 1). From the monthly census data of all leaves produced during 1993, 56% and 68% of annual leaf production takes place during this period in Cecropia and Urera, respectively. The total crown leaf area of these two tree species reach their maximum values in mid- to late rainy season (S. J. Wright, unpublished data).
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In each marked branch, 1–2 leaves that became fully expanded between 6 May and 3 June were selected for repeated in situ measurements of light saturated photosynthetic rates (Scheme 1). In the second sampling scheme (Scheme 2), leaves of known ages within a branch, encompassing the full range of leaf age and position gradient, were measured on a given sampling date between late June and early August. A total of three and four branches (one branch per tree plus a second branch in one of the trees) were sampled with Scheme 2 for Cecropia and Urera, respectively.
Measurement of photosynthesis and light in the field
We measured the light-saturated net CO2 assimilation rate per unit leaf area (= photosynthetic capacity, A) and stomatal conductance to water (Gs) with a portable infra-red gas analyzer (LI-6400, Li-COR, Lincoln, Nebraska, USA). Light with the photon flux density (PFD) at 1500 µmol · m–2 · s–1 was supplied with red light emitting diodes (LI-6400-02). The CO2 concentration of the reference air entering the leaf chamber was adjusted with a CO2 mixer control unit such that the "sample" air exiting the chamber contained 350 ppm of CO2. This resulted in CO2 concentration of the reference air to be in the range of 360–388 ppm and most typically close to 370 ppm. All gas exchange data were collected in the mornings between 0800 and 1200. The chamber temperature was controlled by maintaining the Peltier block temperature at 28°C. The relative humidity of the reference air was kept as close to ambient (usually 70–85%) as possible. The air flow rate was 500 mL/min. We also measured A for a smaller number of leaves during their expansion; the increase of A was sharp during expansion and continued for an additional 1–2 wk after leaves reached their full sizes. These gas exchange data during leaf expansion, including estimated intercellular CO2 concentration, have been reported elsewhere (Terwilliger et al., 2001
). In this paper, we report only the results of photosynthesis after leaves reached their full sizes.
Light availability (daily total PFD) at the leaf surface was measured continuously for 5 d for a subset of leaves sampled with Scheme 2, immediately before or after the field gas exchange measurements (5–6 leaves per branch). A calibrated GaAsP sensor (Hamamatsu, Japan) was attached to the adaxial surface of each sampled leaf and hourly means for PFD sampled every 5 s were recorded with LI-1000 data loggers (LI-COR). The results were expressed as %PFD (the mean percentage of the total daily PFD above the canopy) for each leaf.
Laboratory measurements
Photosynthetic light response curves were determined for incident PFD between 0 and 1900 µmol photons·m–2·s–1 with a leaf-disk oxygen electrode and data acquisition software (Hansatech, Norfolk, UK) for one arbitrarily selected branch of each species (Scheme 2). The leaf disks (10 cm2 each) were sampled just after dawn on the day of measurement and kept in dark aerated plastic containers lined with moist filter paper until measured. Light provided by a Björkman-type lamp (Hansatech) was increased in steps by combinations of neutral density glass filters after oxygen evolution rate reached quasi-steady state at each light level. The electrode chamber was supplied with humidified air with 10% CO2 and cooled by circulating 28°C water. Quantum yield (initial slope) and dark respiration rate were calculated from regression analysis of the linear region of the photosynthetic light response curve of each leaf. The age effects on photosynthetic light-response curves were summarized by fitting non-rectangular hyperbola (Lieth and Reynolds, 1987
) for mean values for 2–3 leaves of each age group.
We determined leaf mass per area (LMA, in grams per square meter) from 3.43 cm2 leaf disks for leaves sampled for Scheme 2 field gas exchange and all disks used for oxygen electrode measurements after drying them at 60°C for 
5 d. Nitrogen contents per unit mass (Nm) and per unit area (Na) were determined for the same leaf disks from leaves used in the Scheme 2 field gas exchange with a Perkin-Elmer CHNO/S Model II elemental analyzer (Perkin-Elmer, Shelton, Conneticut, USA). Leaf disks used for the oxygen electrode measurements were used for determination of mineral ash contents (as a percentage of dry mass) after ashing at 500°C in a muffle furnace for 6 h.
Statistical analyses, including leaf survival analysis and regression and correlation analyses among leaf traits, were done with JMP V.3.0 (SAS, 1994
). Species difference in initial photosynthetic capacity was tested with a t test for estimated y intercepts for individual leaves sampled with Scheme 1 (N = 10 leaves per species). Species difference in slopes of the A–leaf age relationships was tested as a significant species-by-age interaction in ANCOVA with pooled data with species as the main factor and leaf age as covariate.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Within each species, there was a substantial variation in the slopes and intercepts of the A–leaf age relationships among leaves sampled with Scheme 1, such that the range of values overlapped considerably between the two species (Table 2). This variation was largely explained by leaf production rates; the slope was steeper for leaves on branches that had higher leaf production rates (Fig. 2; P = 0.05 for Cecropia). On average, Cecropia had a higher initial photosynthetic capacity (y intercept, t test P < 0.003) and steeper negative slope (significant species–by–leaf age interaction in ANCOVA, P < 0.02), which was expected from its shorter leaf longevity. However, estimated x intercepts (= leaf age at which A would reach zero in a linear extrapolation) did not differ significantly between the two species. In both species, x intercepts were greater than the mean leaf lifetime, but less than the 90th percentile leaf lifetime.
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Leaf mass per area increased significantly with leaf age in both species (Fig. 5C, D). Cecropia leaves exhibited greater proportional increase of LMA than Urera. Consequently, photosynthetic capacity per mass (Amass = A divided by LMA) exhibited even steeper declines than A, especially in Cecropia (Table 3). Leaves of both species accumulated very high amounts of ash; up to 16% of leaf dry mass in Cecropia and 30% in Urera, increasing linearly with leaf age (Fig. 7). Ash-free mass increased with leaf age in Cecropia, but was independent of leaf age in Urera. Ash-free mass per leaf area was estimated for all leaves for which LMA was calculated, using the linear regression of percentage of ash on leaf age. Photosynthetic capacity per ash-free mass (Aash-free) declined less steeply with leaf age than Amass (r = –0.70 vs. r = –0.82 in both species). Nitrogen content per unit leaf area did not change with leaf age, position, and light availability in Cecropia, but it decreased in Urera (Fig. 5E, F, Table 3). However, because of the steep increase of LMA, nitrogen per unit mass declined in Cecropia as well as in Urera (Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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along with our earlier study (Kitajima, Mulkey, and Wright, 1997a
). Species with shorter leaf longevity exhibit (1) a higher initial photosynthetic capacity and (2) a steeper rate of decline of photosynthetic capacity with leaf age (parameter a/b in Kikuzawa's model). The slopes for the two tropical pioneers with mean leaf lifetime of 74–93 d were between –0.2 and –0.25 µmol CO2 · m–2 · s–1 per day. In contrast, five other tree species at the same site with mean leaf lifetimes of 174–315 d had shallower slopes of –0.032 to –0.018. Between the two species reported here, on average, Ceropia, with slightly shorter leaf longevity, had steeper slopes than Urera when leaves were sampled with Scheme 1. Cecropia also had a higher peak photosynthetic capacity than Urera as predicted by theoretical and empirical models (Kikuzawa, 1991
; Reich, Walters, and Ellsworth, 1992
).
The link between parameters a and b and optimal leaf longevity (t*) is more explicitly predicted by the following relationship (Kikuzawa and Ackerly, 1999
):
 | (2) |
). The data reported here fit well to this general relationship, along with five other species at the same site (K. Kitajima and K. Kikuzawa, unpublished data). The good fit of observed data to the cost-benefit model suggests that leaf longevity is primarily a function of "payback time" for the cost of construction and maintenance of leaves (Chabot and Hicks, 1982
; Williams, Field, and Mooney, 1989
) and leaf-support tissues (Kikuzawa and Ackerly, 1999
).
The x intercept of the A–leaf age relationship is an extrapolation of the leaf age at which photosynthetic capacity would reach zero. Because total daily net photosynthetic income should reach zero before photosynthetic capacity reaches zero, the x intercept should be greater than the actual leaf lifetime for a given species. Interestingly, the discrepancy between the x intercept and the mean leaf lifetime is smaller for species with shorter leaf lifetime. The x intercepts were approximately the same as the mean leaf lifetime of 28–37 d in Heliocarpus appendiculatus (Ackerly and Bazzaz, 1995
). The x intercepts were similar for Cecropia and Urera; greater than the mean leaf lifetime but shorter than the 90th percentile of leaf lifetime in both species (this study). In contrast, the x intercepts for five species with longer leaf lifetime were much greater than the 90th percentile of leaf lifetime (Kitajima, Mulkey, and Wright, 1997a
).
Sampling schemes and variation among individual leaves
Overall, the two contrasting sampling regimes produced similar A–leaf age relationships. In this study, Scheme 1 with a larger sample size (N = 10 leaves, spread among nine branches on three trees) should produce better estimates for the population than Scheme 2 (N = 3–4 branches). Repeated measurements of individual leaves (Scheme 1) resulted in a steeper relationship than did measurements of a chronosequence on a single day (Scheme 2) in Urera. This was expected because leaves that exhibit faster physiological decline and die early would be underrepresented in Scheme 2. Yet, in Cecropia, the mean did not differ between the two schemes.
There was large variance among individual leaves in lifetime and rate of decline of photosynthetic rates. A part of the within-species variance appears to be explained by different leaf production rates among branches. All else equal, branches with higher leaf production rates should develop self-shading more rapidly, and consequently, leaves should exhibit more rapid declines of photosynthetic capacity (Fig. 2), as predicted by the theories of optimal nitrogen allocation from old, shaded leaves to young leaves (Field and Mooney, 1983
; Hirose and Werger, 1987a
; Ackerly, 1992
; Hikosaka, Terashima, and Katoh, 1994
; Ackerly and Bazzaz, 1995
).
Leaf age, nitrogen reallocation, and photosynthetic capacity
In both species, the decrease in photosynthetic nitrogen use efficiency (A/Na) contributed to the decline of photosynthetic capacity with leaf age. Such decreases in A/Na with leaf age have been observed commonly (Hirose and Werger, 1987b
; Reich, Walters, and Ellsworth, 1991
; Sobrado, 1992
; Witkowski et al., 1992
; Reich et al., 1994
; but see Mooney et al., 1981
; Field and Mooney, 1983
). In Urera, decreasing Na with leaf age, presumably due to nitrogen reallocation from old to new leaves, also contributed to the decline of photosynthetic capacity. However, in Cecropia, Na did not change with leaf age.
While the pattern found for Urera was consistent with theories of optimal resource allocation, the lack of nitrogen reallocation in Cecropia was surprising. The equilibrium number of leaves for Cecropia was only six per branch. These leaves were displayed in a manner that minimized self-shading within the orthotropic branches. Although the estimated leaf area index of a mature Cecropia crown was only ca. 1 (S. Mulkey, unpublished data), there was a sharp decline of light availability with leaf age within each branch (Fig. 5A, B). Based on photosynthetic light-curve characteristics and ambient light measurements, Cecropia leaves senesced and abscised before self-shading caused midday light levels to drop below saturating PFD. In contrast, orthotropic terminal branches of Urera held more than twice as many leaves, which experienced a lower and narrower range of light than Cecropia. Although Urera experienced lower light availability than Cecropia leaves, Urera maintained higher A/Na (Fig. 6C, D) through acclimation and redistribution of nitrogen. The significant decrease of dark respiration in Urera, but not in Cecropia, also suggests a greater acclimation potential of Urera leaves (Table 3).
The increase in LMA with leaf age contributed to the decrease of Nm and Amass in both Cecropia (which did not change Na) and Urera (which reallocated nitrogen to younger leaves). Leaf mass per area also increased with leaf age in the five other tree species we studied at the same site. These ubiquitous increases in LMA with leaf age were at least partly due to accumulation of mineral ash, especially silicon and calcium, in leaves of these species (K. Kitajima, unpublished data). In particular, the observed LMA increase was entirely due to ash accumulation in Urera and due to both ash and carbon accumulation in Cecropia. The ratio of structural and nonstructural carbon, however, did not change consistently with leaf age in either species (Terwilliger et al., 2001
).
The decline in mesophyll conductance with leaf age (Loreto et al., 1994
) may be another reason for lowered nitrogen use efficiency. Lower stomatal conductance (Gs) and water use efficiency (or ratio of A to Gs) are often, but not always, observed with leaf aging (Field and Mooney, 1983
; Sobrado, 1992
; Witkowski et al., 1992
; Dawson and Bliss, 1993
). In our study, only Urera exhibited lower Gs with leaf age (Fig. 5F), while only Cecropia exhibited a decline in water use efficiency (Fig. 4 of Terwilliger et al., 2001
).
Summary
The effect of leaf age on photosynthetic capacity per unit leaf area was similar for the two species, but differed slightly in the direction expected by cost-benefit theory. Urera, with a longer leaf lifetime, exhibited a slightly shallower slope in A–leaf age relationship. Repeated measurements of the same leaf demonstrated variation within species, apparently reflecting differences among branches in rates of leaf production and self-shading. Measurements of leaf age sequences in 3–4 branches produced A–leaf age slopes roughly similar to those from repeated measurements of individual leaves. We conclude that either method is acceptable for species with successive leaf production, as long as the sample size is adequate for sampling heterogeneity among branches and leaves. Interestingly, leaf age and position were more reliable predictors of photosynthetic rate than variables that are considered to be the physiological bases of the A–leaf age relationship, such as %PAR, LMA, Na, and Gs. This suggests that the economic trade-off between leaf longevity and photosynthetic rate is the main determinant of A–leaf age relationship.
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FOOTNOTES |
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4 Author for correspondence (kitajima{at}botany.ufl.edu
; FAX: 352-392-3993)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Ackerly D. D. 1996 Canopy structure and dynamics: integration of growth processes in tropical pioneer trees. In S. S. Mulkey, R. L. Chazdon, and A. P. Smith [eds.], Tropical forest plant ecophysiology, 619–658. Chapman and Hall, New York, New York, USA
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