Comparative growth of four Syzygium species within simulated shade environments of a Sri Lankan rain forest

Forest Ecology and Management 174 (2003) 511–520

Comparative growth of four Syzygium species within simulated shade environments of a Sri Lankan rain forest B.M.P. Singhakumaraa, Harshi K. Gamagea,1, Mark S. Ashtonb,* a

Department of Forestry and Environmental Science, University of Sri Jayawardenapura, Nugegoda, Sri Lanka b School of Forestry and Environmental Studies, Yale University, New Haven, CT 06511, USA Received 10 September 2001; accepted 18 February 2002

Abstract In this study we tested the hypothesis that related tree species within the timber tree genus Syzygium differ in their shadetolerance. We propose that difference in tolerance relate to the successional status and site affinities of each species found within the rain forests of southwest Sri Lanka. Seedlings of each of the four Syzygium species were grown for 24 months in replicated environmental treatments that simulated six different shade quality and quantities recorded from a Sri Lankan rain forest. Treatments were: (i) a deep uniform shade (DS) environment that comprised only 1% of photosynthetic photon flux density (PFD) as compared to that of the full open; (ii) a medium uniform shade (MS) environment receiving 14% of PFD as compared to the full open; (iii) a light uniform shade (LS) environment receiving 50% of PFD; (iv) the center environment of a small 200 m2 opening (SD), receiving 18% of PFD; (v) the center environment of a large 400 m2 canopy opening (LD), receiving 54% of PFD; and (vi) full sun (FS) receiving 100% of PFD. All species increased both above- and below-ground growth with increasing amounts of PFD. Seedling height, root collar diameter and dry mass gain were greatest in the brighter shade treatments with little discrimination shown among LD, LS, and FS. Significant differences in growth also occurred among the four species. Comparisons among species in the full sun (FS) treatment revealed S. rubicundum and S. operculatum to have greater height increments than S. makul and S. firmum. The low leaf mass ratio of S. operculatum, in particular, and S. rubicundum, suggests both to be prone to wilt during periods of desiccation. S. rubicundum also had greatest leaf and branch numbers and smallest leaves compared to the other three species. S. firmum in particular, but also S. makul, had larger, thicker leaves, with greater total dry mass in the FS treatment compared to the other two species. In the deep shade treatment (DS) S. firmum had greatest total dry mass and S. operculatum had the least. Taken together these findings reveal S. rubicundum and S. operculatum to be the most shade-intolerant of the four Syzygium species. Both appear prone to desiccation and water loss, though we speculate the small, numerous leaves and fine branches of S. rubicundum (characteristics of more drought-tolerant species) make this species less so. Both S. firmum and S. makul do best in the brighter shade treatments. Compared to the other two Syzygium spp., both are less susceptible to desiccation in high light environments because of their larger, thicker leaves and greater bulk. S. firmum appears to be the most shade-tolerant of the four Syzygium species. Findings have direct implications for forest management. To secure regeneration establishment and release or to create suitable planting environments Syzygium spp. require silvicultural treatments that account for species specific limitations of site (water availability) and shade (canopy opening size). # 2002 Elsevier Science B.V. All rights reserved. Keywords: Biomass allocation; Desiccation; Leaf morphology; Red:far red ratio; Seedling growth; Shade-tolerance; Syzygium spp. * Corresponding author. E-mail addresses: [email protected] (B.M.P. Singhakumara), [email protected] (H.K. Gamage), [email protected] (M.S. Ashton). 1 Present address: Department of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington, New Zealand.

0378-1127/02/$ – see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 0 2 ) 0 0 0 7 1 - 3

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1. Introduction Tree seedling response to shade has long been the subject of forest research because of importance in predicting establishment of natural regeneration for forest management. Plants that are able to survive and grow in the shade of a forest understory are categorized as shade-tolerant (Lee et al., 1996). Shadeintolerant species require high irradiance regimes for establishment and growth (Whitmore, 1989; Veneklaas and Poorter, 1998). Above- and belowground response of seedlings to variation in light availability is a central area of study in plant ecology (McConnaughay and Coleman, 1999). Understanding tree species shade-tolerance in a forest is one of the underlying principles to the development of silvicultural regeneration techniques for forest management. Shade-tolerant plants have evolved various adaptations to utilize low levels of light in the rain forest understory. The high leaf area per unit leaf mass, low shoot to root ratio and smaller leaf mass per unit area, are some of the measures that have been used to infer shade-tolerance (DeLucia et al., 1998; Osunkoya et al., 1994; Kitajima, 1994). Shade-tolerant plants allocate most of their photosynthate to leaves in order to increase the area available for interception of light. Studies have therefore revealed that the shade-tolerance of a species is influenced by the way biomass is partitioned between plant parts (King, 1994). Such abilities to partition and re-allocate structural attributes of root, stem and leaf tissues to maximize growth and survival in light-limited habitats is therefore a good indicator of shade-tolerance (DeLucia et al., 1998). This study assessed the performance of four Syzygium spp. grown over a 2-year period in shade treatments that provided different light qualities and quantities. The objective of this study was to gain an understanding of how related species differ in shade-tolerance with one another and to contribute toward an autoecological information base that can be used to develop techniques for the sustainable management of Sri Lanka’s rain forests. We hypothesized that the more shade-intolerant Syzygium spp. would have higher growth, leaf number and number of branches, higher dry mass and lower leaf area than the more shade-tolerant species in

the brighter shade treatments; while the more shade-tolerant Syzygium species would exhibit more water-use efficient growth morphologies and would have higher growth and leaf area, higher dry mass and lower numbers of branches and leaf numbers in the shade as compared to the shade-intolerant species.

2. Site and species descriptions The experiment was done at the Sinharaja World Heritage site. The region is classified as a mixeddipterocarp forest (Gunatilleke and Ashton, 1987). The study site comprises upland hills that range in altitude between 300 and 700 m with a mean annual rain fall of 5000 mm and a mean daily temperature of 27 8C (Ashton et al., 1995). The four species selected for this study were Syzygium firmum Thw., S. makul Gaertn., S. rubicundum Wight and Arn. and S. operculatum (Roxb.) Niedz. All belong to the family Myrtaceae and are very common in the southwest rain forest region of Sri Lanka. S. firmum and S. makul are endemic species to the island. All four species are dominants of the forest canopy (S. firmum and S. rubicundum) and subcanopy (S. makul and S. operculatum) of late-successional forest. They are important timber sources and have edible fruits. Demographic data obtained from a 20 ha plot shows that at least three of the species appear to have different site affinities across the rain forest topography. S. operculatum occurs in lower slopes and valleys of the rain forest topography, where small rivers and perennial streams are found. S. makul occupies deep soils of valleys and midslopes. S. rubicundum occurs on mid-slopes that have different aspects to those upon which S. makul is found (see Fig. 1) (Ashton, 1981). The remaining species, S. firmum, is found at lower elevations within the rain forest and has therefore not been recorded in the demographic plot. All four of these species have wildlife value because their fruit provides a considerable resource to a variety of forest birds. Fruit from S. operculatum also provides an important source of vitamin C for children in rural areas. S. rubicundum, S. firmum and S. makul are important plywood and framing timbers for house construction.

Fig. 1. Demographic stem maps of a 25 ha plot in Sinharaja for juveniles (all individuals
1 and <10 cm dbh; small black squares) intermediate size trees (all individuals
10 and <30 cm dbh; large black square squares) and mature trees (all individuals
30 cm dbh; large black circles): (A) S. makul; (B) S. operculatum; (C) S. rubicundum. The plot is aligned N–S and ranges in elevation between 400 and 560 m. The topography of the plot comprises two slopes; one with a generally eastern and southern aspect and the other with a western and northern aspect. The slopes are bisected approximately down the middle of the plot by a stream that runs from the northeast toward the southwest.

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Fig. 1. (Continued ).

3. Methods and materials 3.1. Experimental design Twenty-four well-ventilated environmental shelters were constructed in a large opening at the Sinharaja field station. The shelters were designed to create shade treatments that represented a range of photosynthetic photon flux densities (PFDs) and red:far red (R:FR) ratios found within the Sinharaja forest (Ashton, 1992). Six combinations of irradiance and spectral quality were created, each represented by four environmental

shelters as replicates ð4  6 ¼ 24Þ (see Table 1 for details). Treatments comprised: (i) a deep uniform shade (DS) environment that comprised only 1% of photosynthetic PFD as compared to that of the full open; (ii) a medium shade (MS) environment that simulated the inside forest edge adjacent to a 400 m2 canopy opening, receiving 14% of PFD as compared to the full open; (iii) a light uniform shade (LS) environment that simulated an outside edge of a 400 m2 canopy opening, receiving 50% of PFD; (iv) the center environment of a small 200 m2 opening (SD), receiving 18% of PFD most of which occurred daily as direct sunlight over a short period (2 h) of

Table 1 The various measures of light quantity and quality in the six shade treatmentsa

2 1

Maximum PFD recorded on clear sunny days (mmol m s ) Total daily PFD recorded on clear sunny days (mol m2 day) R:FR ratio Periods of direct sunlight on clear sunny days (h/day)

DS

MS

LS

SD

LD

FS

50 1.2 0.23 –

350 6.0 0.97 –

700 16.3 1.05 –

1600 7.4 1.27 2.5

1600 13.2 1.27 5.5

1600 38.1 1.27 12

a DS: deep uniform shade; MS: medium uniform shade; LS: light uniform shade; SD: small opening (short duration of direct light); LD: large opening (long duration of direct light); FS: full sun.

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time; (v) the center environment of a large 400 m2 canopy opening (LD), receiving 54% of PFD most of which occurred daily as direct sunlight over a long period (6 h) of time; and (vi) FS receiving 100% of PFD. For the uniform shade treatments the quality and quantity of irradiance were altered by spraying a particular ratio of paint pigments within a clear varnish base onto a clear plastic film (Lee, 1985; Ashton, 1995). A photo-spectro-radiometer (LI-1800, Li-Cor, Lincoln, NB) verified the shade quality treatments. Light treatments altering the duration of direct PFD (small opening (SD) and large (LD) opening), were created by constructing a series of parallel vertical slats aligned north–south, horizontally placed 2 m above the ground and across the complete interior of a shelter. All shelters allowed for adequate ventilation through a system of louvers without using electrical power. Seed was collected from different parent trees located in Sinharaja region. Seeds were mixed together for each species and germinated on a nursery bed in 50% shade. Two-month-old seedlings were taken bare-rooted from the nursery and individually planted in plastic bags in January 1996. Twenty-four seedlings of each species were used in four replicates (six seedlings per each replicate) for each shade treatment. The total number of seedlings that were established for the experiment was 576 (6 shade treatments  4 species  24 seedlings/species). Each seedling was planted in forest topsoil obtained from one valley bottom location and mixed with sand to improve drainage. Details on the soil nutrition of this soil mixture have been reported by Gunatilleke et al. (1996). The soil (3 kg) was packed into black circular plastic bags 30 cm deep and 15 cm in diameter. Bags were placed at regular intervals at 30  30 cm spacing between bag centers. Watering

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was done on a daily basis to insure soils approached saturation. A black plastic lining beneath the bags prevented root contact with the ground. Any water that collected on the floor was allowed to drain away through strategically placed holes in the plastic. 3.2. Seedling growth measurements Seedling height (from the top of apical shoot to the ground), number of leaves, and number of branches on the dominant apical shoot were measured every 6 months over a 2-year period from January 1996 to 1998. At the end of the 2-year period seedlings were destructively sampled and measured for dry weight and weight allocation to fine root, tap root, leaf and stem tissue. Twelve seedlings per species were selected (three per shelter) for each shade treatment. Sample seedlings were oven dried for 48 h at 80 8C for dry mass measurements. Dry mass allocation to leaves (LMR) was calculated by dividing the dry leaf mass with the total dry mass of the whole seedling. Stem mass ratio (SMR: dry mass of both main shoot and the branches), and root mass ratio (RMR: dry mass of both taproot and fine roots) were calculated similarly. Before oven drying leaf areas were estimated for each seedling by randomly selecting three mature leaves per seedling. This was done using a CID-202 leaf area meter (CID, Vancouver, WA). Area measurements were used to calculate mean area for single leaves. 3.3. Data analysis Height increment was calculated by subtracting the measurements taken at the initiation of the experiment from the measurements taken at the end of the experiment. A two-way ANOVA test (general linear model)

Table 2 Variance ratios following two-way ANOVA on height increment (cm), leaf number and branches, leaf size (cm2), root length (cm), root collar diameter (cm), LMR, SMR and RMR using data from the six shade treatments (DS, MS, LS, FS, SD, LD) (*: P < 0:05; **: P < 0:01)

Shade Species Block Shade  species ***

Height increment (cm)

Number of leaves

Number of branches

Leaf size (cm2)

Root Root collar Total dry length (cm) diameter (cm) mass (g)

LMR

SMR

RMR

198.12**** 8.53**** ns 3.38***

92.93**** 871.53**** ns 31.27****

59.47**** 171.40**** ns 7.60****

728.23**** 3358.36**** ns 83.01****

1016.13**** 50.14**** ns 24.24****

110.33**** 228.50**** ns 12.05****

152.59**** 53.59**** ns 6.20****

111.57**** 277.65**** ns 5.18***

P < 0:001. P < 0:0001.

****

849.76**** 106.71**** ns 11.64****

2666.99**** 180.90**** ns 26.09****

Table 3 (a) Means of growth performance measures: height increment (cm), root collar diameter (cm) and total dry mass (g). (b) Means of morphology measures: leaf number/seedling, branch number/seedling, leaf size (cm2). (c) Mass ratios: leaves (LMR), stems (SMR) and roots (RMR)a DS

MS

(a) Shade treatments: growth performance Height increment (cm) S. firmum 2.75 (0.53) b S. makul 1.00 (0.84) c S. operculatum 2.71 (0.43) b S. rubicundum 4.00 (1.12) a

SD

14.79 18.00 24.65 25.11

(1.50) (2.68) (1.65) (2.16)

0.35 0.26 0.45 0.30

(0.014) (0.015) (0.021) (0.018)

6.66 3.17 8.19 3.50

(0.49) (0.28) (0.95) (0.38)

(b) Shade treatments: morphological measures Leaf number S. firmum 4.43 (0.50) a 11.58 S. makul 4.83 (0.70) a 15.46 S. operculatum 8.17 (1.15) a 24.50 S. rubicundum 8.20 (4.26) a 96.63

Root collar diameter (cm) S. firmum 0.19 S. makul 0.11 S. operculatum 0.11 S. rubicundum 0.12

(0.014) (0.017) (0.022) (0.013)

Total dry mass (g) S. firmum S. makul S. operculatum S. rubicundum

(0.10) (0.02) (0.07) (0.06)

Branch number S. firmum S. makul S. operculatum S. rubicundum Leaf size (cm2) S. firmum S. makul S. operculatum S. rubicundum

0.84 0.14 0.26 0.12

(1.13) (0.08) (0.46) (0.04)

FS

(2.85) (2.91) (2.61) (2.29)

0.60 0.52 0.64 0.53

(0.023) (0.029) (0.024) (0.021)

a b a b

23.70 14.90 15.55 13.82

(2.24) (1.75) (1.18) (1.33)

(0.77) (1.18) (2.07) (9.50)

b b b a

18.54 25.24 28.74 172.74

0.54 0.41 0.90 4.53

(0.17) (0.14) (0.31) (0.63)

b b b a

1.21 1.71 0.78 9.13

(0.24) (0.27) (0.21) (1.01)

b b b a

1.13 2.82 1.33 9.09

(0.22) (0.35) (0.25) (0.95)

b b b a

1.00 1.73 0.58 9.05

(0.18) (0.19) (0.20) (0.79)

b b b a

0.79 2.48 1.13 11.05

(0.17) (0.32) (0.29) (1.00)

b b b a

44.26 26.68 37.67 4.05

(2.31) (1.77) (1.96) (0.20)

a ab b c

62.90 42.03 43.53 7.04

(2.46) (1.82) (1.58) (0.20)

a b b c

53.14 41.66 35.31 6.03

(1.77) (1.38) (1.53) (0.19)

a b c d

63.75 35.88 37.41 6.58

(3.44) (1.90) (1.71) (0.25)

a b b c

54.21 36.57 27.03 5.82

(3.54) (1.31) (1.50) (0.21)

a b c d

a c b d

0.59 0.53 0.42 0.53

(0.025) (0.037) (0.026) (0.013)

a b c b

0.57 0.47 0.40 0.43

(0.015) (0.021) (0.019) (0.021)

a b c bc

0.50 0.45 0.33 0.46

(0.023) (0.024) (0.023) (0.026)

a b c ab

0.58 0.46 0.39 0.43

(0.020) (0.018) (0.010) (0.020)

a b c bc

0.51 (0.022) a 0.42 (0.028) b 0.32 (0.016) c 0.38 (0.025) bc

a b b b

a b c b

a b b b

(c) Shade treatments: mass ratios LMR S. firmum 0.55 (0.031) S. makul 0.35 (0.025) S. operculatum 0.46 (0.067) S. rubicundum 0.25 (0.087)

LD

38.13 34.10 40.43 43.04

0.08 (0) 0 0 0 13.06 1.34 2.39 0.19

LS

measures b ab a a b c a bc

ab b a a ab b a b

a b b b

(1.22) b (1.58) b (1.77) b (12.50) a

26.54 32.00 41.79 40.45

(3.95) (1.89) (3.09) (3.12)

0.58 0.55 0.68 0.45

(0.035) (0.019) (0.029) (0.032)

20.24 23.01 18.47 11.60

(2.42) (1.70) (1.22) (1.88)

16.67 33.73 32.21 164.00

b ab a a

33.39 33.77 41.25 44.86

(3.49) (3.60) (2.67) (3.45)

0.56 0.59 0.65 0.58

(0.027) (0.033) (0.036) (0.026)

a a ab b

18.36 18.59 16.31 17.43

(1.75) (1.78) (1.68) (1.39)

(1.56) b (2.30) b (2.09) b (16.85) a

16.78 26.23 29.08 161.73

ab ab a b

b b a a a a a a

a a a a

27.33 28.87 36.68 42.35

b b ab a

0.58 (0.032) ab 0.62 (0.038) ab 0.67 (0.029) a 0.53 (0.029) b 21.93 25.32 19.70 15.81

(1.06) b (2.06) b (1.80) b (10.43) a

(2.41) (2.47) (3.66) (3.40)

14.42 26.78 31.78 136.84

(1.92) (2.90) (0.94) (1.38)

ab a ab b

(0.89) b (2.01) b (1.98) b (14.85) a

Shoot mass ratio S. firmum S. makul S. operculatum S. rubicundum

0.27 0.45 0.20 0.46

(0.022) (0.037) (0.042) (0.073)

b a b a

0.19 0.15 0.17 0.24

(0.020) (0.019) (0.013) (0.016)

b b b a

0.23 0.22 0.23 0.30

(0.014) (0.013) (0.007) (0.018)

b b b a

0.21 0.19 0.22 0.25

(0.016) (0.010) (0.013) (0.011)

ab b ab a

0.21 0.25 0.24 0.31

(0.009) (0.016) (0.015) (0.010)

b b b a

0.20 (0.015) ab 0.18 (0.019) b 0.24 (0.018) a 0.24 (0.015) a

RMR S. firmum S. makul S. operculatum S. rubicundum

0.18 0.20 0.33 0.29

(0.012) (0.016) (0.078) (0.040)

c c a b

0.21 0.32 0.41 0.24

(0.027) (0.048) (0.037) (0.023)

c b a c

0.20 0.30 0.37 0.27

(0.018) (0.024) (0.023) (0.033)

c b a ab

0.29 0.36 0.45 0.30

(0.018) (0.031) (0.031) (0.029)

c b a c

0.21 0.29 0.37 0.26

(0.021) (0.026) (0.023) (0.023)

c b a b

0.30 (0.017) b 0.40 (0.032) a 0.44 (0.026) a 0.38 (0.037) ab

a Means are given for the four species across six different shade treatments (DS: deep shade; MS: medium shade; SD: small opening; LS: light shade; LD: large opening; FS: full sun). Means across species for each shade treatment sharing the same letter are not significantly different at P < 0:05% level. Data in parentheses are standard errors of the mean.

B.M.P. Singhakumara et al. / Forest Ecology and Management 174 (2003) 511–520

was performed for all measures using Statistica, Version 5. One-way ANOVA tests were performed for each variable to test replication effect. All data were log transformed prior to analysis. Analyses tested each variable for differences among species, among shade treatments and in their interactions. The differences among species and among shade treatments that were significant were evaluated at the 5% level of significance using Tukey’s Studentized range.

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S. rubicundum. In the DS treatment S. firmum had greatest dry mass gain and S. operculatum had the least. 4.2. Morphological measurements Treatment differences: Overall there were greater numbers of branches and leaves, and larger leaf sizes in the brighter shade treatments (SD, LD, LS, FS) as compared to medium uniform shade (MS) (Table 3b and Table 4). Measurements of leaf number and size

4. Results Variance ratios of all measurements for two-way ANOVAs showed significant differences among shade treatments, among species, and in interactions between shade treatments and species (Table 2). Growth performance measures (height increment, root collar diameter, total dry mass) all exhibited greater levels of significance across shade treatments irrespective of species. Alternatively, morphological measures (leaf number, leaf size, branch number) all showed greater levels of significance among species irrespective of shade treatment. 4.1. Growth performance measurements Treatment differences: All species except S. firmum exhibited greatest height increments across all the brighter shade treatments (SD, LD, LS, FS) (Table 3a and Table 4). S. firmum was the only species that appeared to show some discrimination by growing better in SD and LD shade treatments as compared to FS and LS. Root collar diameters showed similar trends as for height among the brighter shade treatments with largest dimensions for all brighter environments (SD, LD, LS, FS) irrespective of shade treatment. Except for S. firmum species showed greater amounts of discrimination in regard to the brighter shade treatments for total dry mass. S. rubucundum had greatest total dry mass in the LD treatment; S. operculataum and S. makul had greatest total dry mass in the FS treatment. Species differences: Differences among species were also evident with S. rubicundum and S. operculatum exhibiting greater height increments across the treatments than S. firmum and S. makul (Table 3a). For dry mass trends were reversed with S. firmum exhibiting greater dry mass gains than S. operculatum and

Table 4 Differences in the various growth performance and morphological measures between shade treatments for each speciesa DS

MS

SD

LS

LD

FS

Height increment S. firmum S. makul S. operculatum S. rubicundum

d c c c

c b b b

a a a a

b a a a

ab a a a

b ab ab a

Root collar diameter S. firmum S. makul S. operculatum S. rubicundum

c d c d

b c b c

a b a ab

a ab a b

a a a a

a a a ab

Total dry mass S. firmum S. makul S. operculatum S. rubicundum

c d d d

b c c c

a b b b

a ab ab b

a ab b a

a a a ab

Leaf number S. firmum S. makul S. operculatum S. rubicundum

d c c c

c b b b

a a a a

b a a a

ab a a a

b ab ab a

Branch number S. firmum S. makul S. operculatum S. rubicundum

c d c d

b c ab c

a b b b

a a a b

ab b b b

b ab ab a

Leaf size S. firmum S. makul S. operculatum S. rubicundum

c c d d

b b ab c

a a a a

ab a b ab

a a ab a

ab a c b

a

The six different shade treatments are: DS: deep shade; MS: medium shade; SD: small opening; LS: light shade; LD: large opening; FS: full sun. Letters qualitatively indicate significant differences among treatments ða > b > cÞ according to Tukey’s Studentized range test ðP < 0:05%Þ.

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were least in the DS treatment. For S. firmum, S. operculatum and S. rubicundum greatest leaf size was attained in the SD shade treatment. S. firmum also attained the highest leaf numbers in the SD treatment. Species differences: S. rubicundum had the greatest number of leaves and branches across all treatments except the DS treatment (Table 3b). Differences in branch and leaf number among the other species were negligible. S. firmum exhibited the largest leaf size followed by S. makul and S. operculatum, with S. rubicundum having the smallest leaves. 4.3. Mass ratios Trends among species remained consistent across the shade treatments. S. operculatum had greatest RMR, followed by S. makul and S. rubicundum, with S. firmum having the least (Table 3c). Leaf mass ratio (LMR) was reverse with S. firmum having greatest proportion allocated to leaf tissue and S. operculatum having the least. S. rubicundum had greatest SMR as compared to the other species especially in the brighter shade treatments.

5. Discussion Results clearly define the breadth of shade treatments under which each of the four Syzygium spp. attained their greatest height growth, leaf area, and dry mass gain. Dry mass gain as a measure of performance would suggest that S. makul and S. firmum were superior competitors as compared to the other two species. Both S. makul and S. firmum are similar, putting on greater structural bulk (as demonstrated by their larger root collar diameters, larger leaf size, low numbers of fine branches, and high dry mass gains) as compared to S. operculatum and S. rubicundum. Their similarity in growth and morphology may be one reason for why S. makul appears to be restricted to higher elevations in the forest than S. firmum—the two are rarely found to co-exist within the same forest landscape. Both may be considered slow-growing in height increment, tolerant of understory shade, and presumably with their thick, large leaves—less desiccation prone in bright, hot environments than S. operculatum and S. rubicundum.

Of the two we suggest S. firmum to have leaves that are more adapted to the rain forest climates of lower elevations. S. firmum’s larger leaves and greater LMR in the brighter environments would make it better adapted to the higher levels of heat and humidity of wet tropical climates at lower elevations. This is corroborated by leaf anatomical measures of S. firmum which indicate it also has thicker leaves and cuticle (Gamage et al., unpublished data). Growth in height is often a useful indicator of fitness because it is usually correlated with increases in biomass. In this study this is not the case: height increment and dry mass gain change rank among species. Height increment, however, is also a good measure of seedling response to competition for light (Fetcher et al., 1983). Clearly, S. rubicundum and S. operculatum are superior in height growth as compared to S. makul and S. firmum. This, together with greater branching, smaller and more numerous leaves (especially S. rubicundum) and more slender structure, make S. operculatum and S. rubicundum fast-growing and pioneer-like. This is corroborated by their known distribution within the rain forest. Both are associated with forest disturbance. With a larger leaf size than S. rubicundum, we speculate S. operculatum to be the most prone to desiccation—this fits well with its restricted distribution along disturbed areas of rivers and streams. S. rubicundum can be found on mid-slope sites, often with other fast-growing, but long-lived tree species, such as Shorea trapezifolia (Ashton et al., 1995, 2001). The dramatically smaller leaf size of S. rubicundum could be related to a trade-off between higher photosynthetic rates per unit leaf area and increased evaporative demands arising in high light (Nobel, 1977; Givinish, 1988), making this species shade-intolerant adapted to drier or more stressed environments. This kind of pioneer-like growth morphology supports our contention that the sites where S. rubicundum occurs with S. trapezifolia are actually legacies of disturbance perhaps caused by forest clearance for swidden agriculture or from multiple blowdowns by wind (De Zoysa et al., 1991; Ashton et al., 2001). In this study there is some evidence to suggest that some of the Syzygium spp. are able to maintain high rates of height growth and dry mass gains in partial shade (i.e. equal to or better than in the FS treatment)

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by increasing leaf size (S. operculatum, S. rubicundum) or leaf number (S. firmum). Interestingly, the SD treatment which allowed only 18% PFD of FS, still had equal or better growth than the LS treatment with 50% PFD of FS. This may demonstrate the poorer light quality effect (lower R:FR ratio) of the LS treatment though the evidence for this is only suggestive. All this adds to a growing body of literature that suggests many seedlings of rain forest canopy trees actually do better under partial shade conditions than in the FS. Most of this work has been done on canopy tree species in mixed-dipterocarp forest of the Asian tropics (Sasaki and Mori, 1981; Turner, 1989, 1990; Ashton and Berlyn, 1992; Ashton, 1995). These results are contrary to work done particularly in the neotropics where seedlings of canopy tree species do best in FS conditions (Popma and Bongers, 1988, 1991; Kitajima, 1994; Pattison et al., 1998). In summary this study demonstrates the differential degrees of shade-tolerance and growth of the four Syzygium spp. examined. The study also demonstrates that differences among species are best elucidated by using several measures of growth performance with Syzygium spp. changing rank when measures of height growth and dry mass gain are compared with each other. This has implications for forest management and rain forest restoration planting. Syzygium species are site specific with some that are shadetolerant and others that are clearly not. Care must be taken to plant Syzygium spp. on appropriate site and shade environments. To apply the findings in this study to forest management applications further experimental plantings under field conditions needs to be done within the forest and on abandoned agricultural lands as a next step in testing the findings in this study.

Acknowledgements We would like to thank Chaminda Kumarasingha and B.W. Gunasoma for helping to set the experiment up and for measuring the seedlings. We also acknowledge logistic support and help from the Forest Department of Sri Lanka, and financial support from the MacArthur Foundation, USA.

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