141, 365–377. With 3 figures 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003



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Figure 2. Mean net photosynthesis and stomatal conduc-

tivity for the four Syzygium  species in different shade

treatments. Bars indicate one standard error of mean. Spe-

cies not sharing the same letter within a shade treatment

differ significantly at P < 0.05.

Table 1. Variance ratios following two-way analysis of variance on seedling photosynthesis (mmol m

-2

  s



-1

), stomatal

conductivity (mmol m

-2

  s



-1

), leaf number and leaf area (cm

2

). Degree of significance: **** P  <  0.0001; *** P  <  0.001;



** P < 0.01; * P < 0.05

Photosynthesis

Stomatal

conductivity

Number of leaves

Single leaf area

Total leaf

area/seedling

Shade treatment

46.13****

8.65****

92.93****

728.23****

2019.82****

Species

10.10**


1.01 ns

871.53****

3358.36****

53.07****

Block

ns

ns



ns

ns

ns



Shade ¥ Species

4.49***


4.84***

31.27****

83.01****

27.29****



Syzygium firmum  and  S. operculatum  had the

greatest areas of their individual leaves in the partial

shade treatments as compared to the DS (99%) and FS

(0%) treatments (Fig. 3). Syzygium firmum  had the

largest individual leaf area in the SO (82%) and LO

(65%) shade treatments. Syzygium makul and S. rubi-



cundum had the largest individual leaf areas in all the

brightest treatments (SO, LO, LS, FS).



Syzygium firmum  had the greatest total leaf area

per seedling in the SO (82%) shade treatment (Fig. 3,

Table 3). Syzygium makul  had the greatest total leaf

area in the LS (58%) shade treatment; and



S. operculatum  and  S. rubicundum  had the greatest

total leaf areas per seedling in all the brightest shade

treatments (SO, LS, LO, FS).

Trends among species

In all shade treatments S. rubicundum had the high-

est leaf numbers with S.  firmum  having the least

(Fig. 3).  Syzygium rubicundum  differed most in leaf

number among shade treatments. Syzygium firmum

and S. operculatum differed the least (Table 2).

Across all shade treatments S. firmum  had the

largest individual leaf areas followed in order by S.



makul  and  S. operculatum,  and then S. rubicundum.

Comparisons of total leaf areas per seedling were

more variable. Greatest total leaf area in the DS (99%)

was exhibited by S. firmum. The least total leaf areas

in the DS treatment were in S. makul  and

S. rubicundum.  Compared to other species, S. makul

had the greatest total leaf area in the LS (58%) and FS

(0%) treatments. In the LO (65%) shade treatment all

species had about the same total leaf area (Fig. 3).



Syzygium rubicundum  showed the greatest differ-

ences in both individual leaf area and total leaf area

change across the different shade treatments as com-

pared to the other species, followed in decreasing

order by S. makul and S. operculatum, with S. firmum

showing the least change (Table 2).

L

EAF


 

ANATOMY


Species trends across treatments

Anatomical measures of leaf structure differed signif-

icantly among shade treatments, between species and

in interactions between both shade treatments and

species (Table 4). All species produced thicker leaves


LEAF STRUCTURE OF SYZYGIUM SPECIES

371


© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 141, 365–377

T

able 2.

Plasticity values (highest/lowest) across the shade treatments for various physiological,

 morphological and anatomical leaf mea

sures


. (Plasticity 

=

 x/X;



where 

is the deep shade value and X is the optimum value among shade treatments).



 Species followed by the same letter within 

a treatment are not signifi

cantly

different at the 5% level



Net

photosynthesis

Conductivity

Leaf


number

Leaf


size

T

otal



leaf area

Blade


thickness

Cuticle


Upper

epidermis

P

alisade


mesophyll

Lower


epidermis

Stomatal


density

S.

 firmum

3.92b


1.09d

3.78c


4.88d

16.35d


2.14a,b

2.31a,b


1.66a

1.76a


1.73a

1.73a,b


S.

 makul

3.17bc


6.30b

6.98b


31.36a

153.01b


1.70b

2.48a


1.45a

1.33b


1.88a

1.88a


S.

 operculatum

2.51c


10.80a

3.94c


18.21c

56.14c


2.21a

1.27c


1.61a

1.56a,b


1.16b

1.83a


S.

 rubicundum

8.08a


2.91c

21.00a


37.05a

780.97a


1.52b

1.72b


,c

1.81a


1.30b

1.25b


1.55b

and cuticles, deeper palisade mesophyll and epidermal

layers with increase in light (Table 5). All species

increased epidermal cell thickness from DS (99%) to FS

(0%) (Table 5), but these trends were less marked for

lower epidermal than the upper epidermal dimensions.

Stomata were predictably found only on the lower

leaf surface of all Syzygium spp. and increased in den-

sity with decrease in shade (Table 5).

Trends among species

Syzygium firmum  had most plasticity for palisade

mesophyll dimensions, S. firmum  and  S. makul  had

most plasticity for cuticle and lower epidermis thick-

ness (Table 2). Syzygium rubicundum  and  S. makul

had least plasticity for leaf blade and palisade thick-

ness.  Syzygium operculatum  had least plasticity for

cuticle and lower epidermis thickness (Table 2).

In general S. firmum  had the thickest leaves, cuti-

cles and largest palisade mesophyll in all the brighter

shade treatments followed in order by S. makul, then



S. operculatum and S. rubicundum together (Table 5).

However, for the same above leaf attributes, except

cuticle thickness, S makul had the largest and thick-

est leaves of the four species in the deepest shade (DS,

99%), followed in declining order by S. firmum,

S. rubicundum and S. operculatumSyzygium firmum

had the thickest cuticle in the DS (99%) treatment

(Table 5).

In most shade treatments, S.  firmum  and  S.  rubi-



cundum  had thicker upper epidermal dimensions

than  S.  makul  and  S.  operculatum.  Generally,



S. operculatum and S. makul  had the thinnest lower

epidermal dimensions (Table 5). However, it must be

noted that though S. makul  had thinner cell dimen-

sions, it was the only species to have several lower epi-

dermal layers. Comparing all the anatomical

measures made on leaves, plasticity across shade

treatments was usually least for lower epidermal

thickness, except for S. makul (Table 2).



Syzygium operculatum had significantly higher sto-

matal densities than the other species in all shade

treatments.  Syzygium rubicundum  had significantly

lower stomatal densities and smallest stomatal plas-

ticity among the treatments as compared to the other

species (Table 2).

DISCUSSION

S

PECIES



 

LEAF


 

STRUCTURE

 

IN

 



RELATION

 

TO



 

SERAL


 

STATUS


 

AND


 

KNOWN


 

TOPOGRAPHIC

 

POSITION


Our results show that comparative analysis of leaf

structure and physiology among related species can

give clues as to particular species site affinity within a

forest. Syzygium firmum has optimum photosynthesis



372

H. K. GAMAGE ET AL.

© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 141, 365–377

in the brighter partial shade treatments (MS, 85%; LS,

58%). Syzygium firmum also has relatively high plas-

ticity in dimensions of leaf structure across the shade

treatments as compared to the other Syzygium  spp.

Compared to its relatives, S. firmum had the highest

total leaf area per seedling in the DS (99%). All this

suggests  S. firmum  to be shade-tolerant but a gener-

alist capable of growing in a range of shade environ-

ments. The thicker leaves and cuticles of S. firmum, its



Figure 3. Morphological measurements of leaf number, area of individual leaves, and total leaf area for Syzygium species

across the shade treatments. Bars indicate one standard error of mean. Species not sharing the same letter within a shade

treatment differ significantly at P < 0.05.

relatively lower stomatal density and stomatal con-

ductivity, and its larger individual leaf size than the

other species also make it conservative in water-use.

These leaf structure and physiological characteristics

conform to its known growth habit, that of a late suc-

cessional tree that grows on a wide range of topo-

graphic sites within mature lowland forest and within

tree-fall canopy openings at elevations between 50 and

300 m a.s.l.



LEAF STRUCTURE OF SYZYGIUM SPECIES

373


© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 141, 365–377

Syzygium makul had its highest photosynthetic rate

in the LS treatment (58% shade). Its relatively thick

leaf dimensions, and low stomatal conductivity makes

this species similar in leaf structure to S. firmum.

Compared to the other species, S. makul was the only

one to have multiple layers of lower epidermal cells,

making the lower epidermal cell layer thicker than

any of the other Syzygium  spp. Multiple-layering of

the lower epidermis may promote greater water-use

efficiency.

The distribution and growth habit of S. makul

clearly appear to have the same late-successional

wide-ranging topographic affinities as S. firmum, but

its core range is the hill rain forest of the Sinharaja

(300–700 m a.s.l.). The relatively thicker and bigger

leaf attributes of S. firmum  as compared with



S. makul  may make S. firmum  better adapted to the

hotter and more dessicating climate found at lower

elevations.

Table 3. Summary of morphological variables for the four Syzygium spp.in different shade treatments (DS, deep shade;

MS, medium shade; SO, small opening; LO, large opening; LS, light shade; FS, full sun). Shade treatments have been

arranged from highest to lowest amounts of shade. Treatments followed by the same letter for a given species are not

significantly different at the 5% level

DS (99%)

MS (85%)


SO (82%)

LO (65%)


LS (58%)

FS (0%)


Leaf number

S. firmum

c

b



a

ab

ab



b

S. makul

c

b



a

a

a



a

S. operculatum

c

b



a

a

a



a

S. rubicundum

c

b



a

a

a



a

Leaf size



S. firmum

d

c



a

a

b



b

S. makul

c

b



a

a

a



a

S. operculatum

c

a



a

a

a



b

S. rubicundum

c

b



a

a

a



a

Total leaf area



S. firmum

d

c



a

b

b



b,c

S. makul

d

c



b

b

a



b

S. operculatum

b

a



a

a

a



a

S. rubicundum

c

b



a

a

a



a

Table 4. Variance ratios following two-way analysis of variance on thickness of cuticle (CT), leaf blade (LB), upper

epidermis (UE), palisade mesophyll (PM), lower epidermis (LE) (all mm) and stomatal frequency (SF) (mm

-2

) using data



from the six shade treatments. Degree of significance: **** P < 0.0001; *** P < 0.001; ** P < 0.01; * P < 0.05

Cuticle


Leaf blade

Upper


epidermis

Lower


epidermis

Palisade


mesophyll

Stomatal


density

Shade treatment

100.38****

566.80****

192.71****

9.02***


94.05****

265.52****

Species

2101.41****



4324.82****

86.92****

219.49****

1170.18****

316.24****

Block


ns

ns

ns



ns

ns

ns



Shade ¥ species

37.22****

95.12****

7.47***


11.47****

37.24****

5.13***

Leaf physiological and structural attributes suggest



S. operculatum  to be shade-intolerant and water-

wasteful. This species attained optimum rates of net

photosynthesis in the LS (58%) treatment, with a pal-

isade mesophyll that was the thinnest of the Syzygium

species in DS (99%), an incapacity to add more than

one layer of palisade mesophyll in the brighter shade

treatments, and relatively low plasticities in leaf area,

leaf production and P

N

.  Syzygium operculatum  had



the highest stomatal conductivity and stomatal densi-

ties of all the Syzygium species but the thinnest leaves

and cuticle (especially in the brighter shade treat-

ments), suggesting a proneness to dessication. These

characteristics match its distribution along waterways

(seasonal streams, seepages, rivers) in second growth

or disturbed forest areas of the Sinharaja forest.

Highest photosynthetic rates for S. rubicundum

were in FS (0%) treatment. Syzygium rubicundum

also had greatest photosynthetic plasticity among the



374

H. K. GAMAGE ET AL.

© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 141, 365–377

T

able 5.

Summary of anatomical variables for the four 



Syzygium

 species in different shade treatments (DS,

 deep shade;

 MS


, medium shade;

 SO


, small opening;

LO

, large opening;



 LS

, light shade;

 FS

, full sun).



 Shade treatments ha

ve been arranged from highest to lowest amounts of shade

Data are means with standard



errors in parentheses.

 Species followed by the same letter within a treatment are not signifi

cantly different at the 5% level

DS (99%)


MS (85%)

SO (82%)


LO (65%)

LS (58%)


FS (0%)

Leaf blade thic

kness (

m

m)



S.

 firmum

189.17 (3.53)b

295.17 (2.13)a

371.00 (3.81)a

384.67 (2.64a

363.17 (4.87)a

404.50 (5.98)a

S.

 makul

218.50 (5.15)a

179.83 (1.89)b

236.17 (3.04)b

257.00 (2.05)b

248.83 (4.61)b

305.67 (4.33)b

S.

 operculatum

87.67 (1.10)c

136.00 (3.47)c

157.50 (2.12)c

167.50 (2.47)c

164.33 (2.08)c

193.67 (2.69)c

S.

 rubicundum

191.50 (1.67)b

125.67 (1.39)d

158.83 (1.75)c

164.17 (2.89)c

159.50 (1.95)c

186.83 (1.75)c

Cuticle thickness (

m

m)

S.



 firmum

2.89 (0.084)a

4.13 (0.086)a

5.48 (0.138)a

6.06 (0.139)a

6.58 (0.123)a

6.69 (0.175)a

S.

 makul

1.60 (0.087)b

1.54 (0.054)b

2.64 (0.091)b

3.47(0.073)b

3.19 (0.096)b

3.82 (0.104)b

S.

 operculatum

1.26 (0.043)bc

1.29 (0.048)c

1.01 (0.043)d

1.107(0.038)c

1.18 (0.049)c

1.20 (0.048)d

S.

 rubicundum

1.16 (0.054)c

1.28 (0.054)c

1.71 (0.057)c

1.31 (0.065)c

1.39 (0.051)c

2.00 (0.077)c

Upper epidermal thic

kness (

m

m)



S.

 firmum

11.98 (0.275)a

15.76 (0.212)a

17.72 (0.302)a

16.64 (0.241)a

19.36 (0.332)a

19.88 (0.307)b

S.

 makul

13.20 (0.508)a

12.56 (0.209)c

14.44 (0.299)b

14.68 (0.280)b

15.76 (0.412)b

18.20 (0.424)c

S.

 operculatum

10.78 (0.172)b

13.48 (0.311)bc

14.52 (0.388)b

14.88 (0.266)b

15.00 (0.451)b

17.32 (0.411)c

S.

 rubicundum

11.82 (0.176)ab

13.52 (0.286)b

17.60 (0.321)a

16.44 (0.367)a

18.20 (0.324)a

21.44 (0.284)a

P

alisade mesophyll thic



kness (

m

m)



S.

 firmum

46.30 (1.051)b

63.72 (0.913)a

67.72 (0.861)a

79.74 (2.291)a

80.80 (1.302)a

81.64 (1.193)a

S.

 makul

49.64 (0.926)a

48.52 (0.894)b

57.04 (0.965)b

55.16 (0.908)b

52.44 (0.971)b

64.56 (0.897)b

S.

 operculatum

30.04 (0.530)c

38.44 (0.950)c

39.48 (0.866)d

40.04 (0.654)d

42.68 (0.484)c

46.92 (0.762)c

S.

 rubicundum

48.48 (0.540)ab

37.32 (0.344)c

45.24 (0.528)c

45.56 (0.987)c

45.16 (0.577)c

42.56 (0.642)d

Lower epidermal thic

kness (

m

m)



S.

 firmum

8.64 (0.184)a

10.42 (0.181)a

10.00 (0.182)a

10.14 (0.232)a

12.00 (0.278)a

10.84 (0.166)a

S.

 makul

7.44 (0.344)b

8.28 (0.218)c

8.08 (0.180)b

8.38 (0.170)b

8.18 (0.207)c

9.04 (0.233)b

S.

 operculatum

8.02 (0.157)ab

7.40 (0.189)d

8.04 (0.204)b

7.48 (0.202)c

6.94 (0.203)d

7.04 (0.203)c

S.

 rubicundum

8.34 (0.282)ab

9.42 (0.197)b

10.40 (0.218)a

8.92 (0.214)b

9.28 (0.224)b

10.32 (0.200)a

Stomatal density (mm

-

2

)



S.

 firmum

279.20 (8.55)bc

349.87 (4.79)b

472.27 (10.26)a

455.73 (15.39)c

473.60 (10.40)c

482.93 (9.23)c

S.

 makul

287.20 (6.10)b

363.73 (5.69)b

491.73 ((8.78)a

526.13 (11.66)b

529.87 (7.29)b

541.07 (7.72)b

S.

 operculatum

342.13 (7.79)a

393.33 (8.22)a

499.20 (14.09)a

626.40 (23.51)a

567.47 (7.66)a

597.60 (9.34)a

S.

 rubicundum

248.80 (17.20)c

281.87 (4.13)c

347.73 (6.98)b

342.40 (10.04)d

353.07 (5.52)d

386.93 (11.71)d


LEAF STRUCTURE OF SYZYGIUM SPECIES

375


© 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 141, 365–377

species. Both attributes suggest S. rubicundum  to be

the most shade-intolerant of the Syzygium  spp. As

compared with the other speciesS. rubicundum  had

the lowest stomatal densities and smallest leaves,

with thin cuticles and leaf thickness, but highest

numbers of leaves. Smaller leaf size and associated

attributes of leaf structure suggest a trade-off between

higher photosynthetic rates per unit leaf area and

increased evaporative demands of high light environ-

ments (Nobel, 1977; Givinish, 1988; Strauss-

Debenedetti & Berlyn, 1994). Taken together, the

leaf physiological and structural attributes of

S. rubicundum match its known early-  to mid-succes-

sional habitat on midslope sites in the Sinharaja for-

est that are thought to have originated from swidden

cultivation (De Zoysa et al., 1991).

C

HANGES


 

IN

 



LEAF

 

STRUCTURE



 

AND


 

MORPHOLOGY

 

IN

 



RELATION

 

TO



 

SHADE


 

QUALITY


Comparison among shade treatments that received

the same total amount of PFD (MS, 85% vs. SO, 82%)

reveal that the more uniform but poorer light quality

of the MS (85%) treatment produced significantly

lower and thinner leaf anatomical dimensions than

the SO (82%) treatment. The short periods of direct

sunlight provided in the SO treatment appears to

have a much stronger influence on increasing leaf

structural dimensions than the uniform diffuse shade

of MS. Comparison between shade treatments at

brighter levels of PFD – between uniformly brighter

but poorer quality shade and longer periods of direct

light (LS, 58% vs. LO, 65%) – reveal that there is vir-

tually no difference between treatments across almost

all anatomical measures. This suggests that the

nature of light quality and uniformity may play more

important roles in leaf development in more shady

environments than brighter ones. Evidence for differ-

ences in overall growth performance of tropical rain

forest tree species in relation to changes in light qual-

ity has been weak (Ashton, 1995; Lee et al., 1996).

Strongest response differences have been shown to be

from changes in amount of shade (Jurik et al.  1982;

Chazdon & Kaufmann, 1993; Strauss-Debenedetti &

Berlyn, 1994). This study demonstrates that shade

quality may play a significant role in promoting seed-

ling establishment in environments with high

amounts of shade. This also lends credence to claims

by foresters that the most favourable environments

for seedling establishment of advance regeneration

species (sensu  Smith  et al., 1997) is within environ-

ments that provide intermittent direct light (a.k.a.

shelterwood, Smith et al., 1997) at the forest ground-

storey rather than brighter but more uniform shade

conditions.

Evidence from this study also supports the conten-

tion that seedlings of many slower-growing rain forest

canopy tree species perform best under various condi-

tions of partial shade as compared with full sun in the

mixed-dipterocarp forest types of Asia (Sasaki & Mori,

1981; Turner, 1989; Ashton, 1995). This does not

appear to be the case with most species of canopy tree

from the neotropics, where studies show seedlings

grow best in full sun (Fetcher et al., 1983; Popma &

Bongers, 1988, 1991; King, 1994; Kitajima, 1994).

Reasons for differences in performance of canopy tree

seedlings between the two realms may relate to the

fact that these bioregions have evolved over long per-

iods of time within very different climates and distur-

bance histories.

In summary, leaf structure and physiological mea-

sures, when taken together, can provide useful inter-

pretations of species site affinity. This study supports

others on different genera within rain forests (Ashton

& Berlyn, 1992; Strauss-Debenedetti & Berlyn, 1994;

Lee  et al., 1996). Findings strongly support hypothe-

ses that species assemblages within Sri Lankan for-

ests have evolved strong predictable morphological,

anatomical and physiological adaptation and response

in relation to environmental gradients. This is in con-

trast to other studies that suggest many rain forest

species are site generalists with similar suites of adap-

tations and plasticities that are largely overlapping.

On the practical side, our results suggest that these

rain forest trees need careful site and shade environ-

ment selection for restoration plantings and species

conservation planning.

ACKNOWLEDGEMENTS

This study was made possible with funding from the

MacArthur Foundation and a scholarship from the Sri

Lanka National Science Foundation. We gratefully

thank the Sri Lanka Forest Department for use of

their research facilities and for accommodating us at

the Sinharaja Field Station. We also thank our tech-

nicians Chaminda Kumara and B.W. Gunasoma. Both

were responsible for helping to establish and maintain

the experiment. Lastly, we would like to thank Camp-

bell Webb, Jefferson Hall and Graeme Berlyn for com-

ments and ideas on the draft manuscript.

REFERENCES


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