Effects of shade on seedling growth, morphology and leaf photosynthesis in six subtropical thicket species from the eastern Cape, South Africa

Forest Ecology and Management, 61 ( 1993 ) 199-220

199

Elsevier Science Publishers B.V., Amsterdam

Effects of shade on seedling growth, morphology and leaf photosynthesis in six subtropical thicket species from the eastern Cape, South Africa P.M. Holmes*, R.M. Cowling Institute for Plant Conservation, Botany Department, Universityof Cape Town, Rondebosch 7700, South Africa (Accepted 4 May 1993 )

Abstract We investigated the plasticity of seedlings to shade in six shrub species common in subtropical thicket, in order to assess their microhabitat preferences for regeneration. Cassineperagua and Sideroxylon inerme, which also occur in adjacent forests, were the most shade tolerant and would be unlikely to require canopy gaps for recruitment: their relative reduction in growth in dense shade was slight, as was their increase in leaf weight ratio (LWR); leaf inclination was adjusted to near horizontal in dense shade and maximum net photosynthetic rate (A,,~) remained fairly low in sun-acclimated plants. Rhus glauca, which also occurs on forest margins, demonstrated the highest growth rates, especially in the open, and together with its high potential A,,u is well-equipped as a pioneer, and would benefit from canopy gaps for establishment. Cassine aethiopica, which is also common in coastal forests, was slower growing than Rhus, but less shade tolerant than C. peragua and Sideroxylon and would probably benefit from canopy gaps for establishment. Pappea capensis and Schotia afra, which also occur in open savanna vegetation, demonstrated a growth and morphological pattern indicative of species adapted to periodic drought, in having a high ratio of woody conductive tissue to leaf tissue with accompanying slow growth. Their relatively poor performance in deep shade suggests that canopy gaps would benefit their recruitment. We concluded that canopy gaps may be essential for recruitment of the full species complement in sub-tropical thickets.

Introduction

In southern Africa, the subtropical forests and savannas of northeastern regions grade into subtropical thickets in the eastern Cape, which in turn grade into mediterranean-climate shrublands in the southwest Cape. These transitions parallel a gradient in rainfall seasonality from predominantly summer rainfall through all-year rainfall to predominantly winter rainfall. In this paper we focus on subtropical thicket of the eastern Cape. The overstorey corn"Corresponding author: telefax (SA)-021-6503726.

© 1993 Elsevier Science Publishers B.V. All rights reserved 0378-1127/93/$06.00

200

P.M. Holmes, R.,~ Cowling~ForestEcology and Management 61 (1993) 199-220

ponent of thicket includes a mix of subtropical forest and savanna species. Further details of the biogeography and complex phytochorology of this region are provided in Werger (1978), Gibbs-Russell and Robinson ( 1981 ) and Cowling (1983). The eastern Cape has a warm temperate climate with a midsummer moisture deficit (Cowling, 1984). Monthly coefficients of variation in rainfall are high, and extremely prolonged droughts are not uncommon (Cowling, 1984). Thicket occurs in areas receiving 300-800 mm annual rainfall (Cowling, 1984; Everard, 1987). Its conservation status is poor with under 2% preserved (Lubke et al., 1986). Large tracts have been converted to wheatlands and much of the remainder is utilised for stock farming, particularly goats, the region contributing substantially to South Africa's mohair industry (StuartHill, 1992). Thicket communities are stable but non-resilient (Cowling, 1984), being very slow to recover following high levels of disturbance, such as that caused by overstocking (Aucamp and Barnard, 1980). Such features are indicative of communities dominated by stress-tolerant species (sensu Grime, 1987). Seedling recruitment is seldom observed (Hoffman and Everard, 1987; Midgley and Von Maltitz, 1991; Stuart-Hill, 1992; Midgley and Cowling, 1993 ), causing concern both to conservationists and stock farmers. This has led to speculation that the natural disturbance regime has changed from one of low disturbance in precolonial times to one of high disturbance (Hoffman and Everard, 1987). The large herbivores (e.g. elephant, buffalo, kudu), whose numbers were greatly reduced by the early hunters and settlers in the 1800s (Skead, 1987) would have created a mosaic of small gaps through browsing and path formation (Stuart-Hill, 1992), which might be important for the regeneration of shade-intolerant species. Removal of indigenous herbivores results in dense impenetrable thicket with no regeneration niche for shadeintolerant seedlings, while stocking with an equivalent biomass of goats results in excessive shrub death and opening of the canopy (Stuart-Hill, 1992). Alternative explanations for the observed lack of seedlings are that the climate has changed, becoming drier over the last few millennia (Deacon and Lancaster, 1988 ), or that recruitment is episodic or infrequent, requiring an unusual sequence of environmental conditions for success. The objective of this study is to investigate the responses of thicket seedlings to shade, to ascertain whether canopy gaps might play a role in thicket recruitment dynamics. We adopted an empirical, mechanistic approach (Givnish, 1988) to compare the growth, morphological and physiological plasticity to shade of seedlings of six shrub species common in subtropical thickets. As many dominant species in Cape subtropical thickets derive from forests and savannas (Cowling, 1983 ) we refer to tropical forest recruitment dynamics as a comparative model. Thicket differs from forest in being of lower stature and hence having low susceptibility to windthrow as the major distur-

P M. Holmes, R.M. Cowling~ForestEcology and Management 61 (I 993) 199-220

201

bance force. The only potential gap-forming factor in thicket is large-herbivore damage (Stuart-Hill, 1992). Methods

The species chosen for study are evergreen sclerophyll shrubs, which differ in their core distributions and habitats, and which may form trees in other formations, such as evergreen forest (Table 1 ). In March 1990, seedlings 13 months old, grown from native seed were obtained from a nursery. Except for C. peragua and Sideroxylon, which were collected in the southwest Cape, seeds of all species were collected in the eastern Cape. Pappea comprised two batches: one about 6 months old and the other 12 months old. At the Kirstenbosch Nursery (33°58'S, 18°26'E) in the southwest Cape, seedlings were repotted into 6-1 propagation bags containing potting mixture (one part estate loam (granitic), two parts Phillippi sand, two parts compost, 1 kg m -3 superphosphate, l kg m-3 bonemeal). The experimental design was a splitplot, with three levels of shading-open (no shade), and shade-cloth enclosures intercepting 40 and 80% of irradiancewreplicated twice. Each treatment plot contained six seedlings each of the six species, positioned randomly. Every month, bags were rotated by 180 ° and repositioned within the plots. Within species there were no initial differences in plant size and leaf number among treatment plots (ANOVA, P< 0.05). Plants were watered to field capacity several times per week during the dry summer months and weekly during the wet winter months. No additional fertilizer was applied during the trial.

The light environment Irradiance measurements (using a PAR meter: Skye SKP200, Skye Instruments Ltd., UK) taken half-hourly throughout a late summer (February 1991 ) day gave integrated results of 68.03 tool m - 2 day- ~, 34.16 ( 50.2% ) tool m - 2 day-i and 10.12 (15.0%) mol m -2 day- ~for open, 40% and 80% shade-cloth treatments respectively. Respective maximum photon flux densities were 2390 /zmol m -2 s -~, 1425/~mol m -2 s -~ and 415/zmol m -2 s -~. In closed subtropical thickets instantaneous irradiance measurements in the understorey averaged about 3% of those measured above canopy (R.M. Cowling, unpublished data, 1990).

Growth and morphological responses Plant height and basal stem diameter were measured in early April 1990 and at monthly intervals, ending in April 1991. Leaves were counted and additional new leaves were monitored by labelling the earlier growth. However,

Fabaceae: Caesalpinoideae Sapotaceae

Anaeardiaeeae

Sapindaceae

Shrub to small tree, 3-5 m tall Shrub to small tree, up to 11 m tall

Shrub, rarely small tree, u p t o $ mtall

Small tree, 3-9 m tall

Shrub to tree, up to 12 m tall

Shrub to tree, up to 12 m tall

Growth form

Bird

Mammal

Bird

Bird

Bird

Bird

Dispersal mode

qnformation from Palmer and Pitman (1972) and Coates-Palgrave (1977).

L.

Sideroxylon inerme

L. var afra

Schotia a f r a

Thunb.

Rhus glauca

Edd. & Zeyh.

Pappea capensis

L.

Cassine peragua

Celastraceae

Celastraceae

Cassine aethiopica

Thunb.

Family

Species

Table 1 Eecologieal characteristics and distributions of study species z

Forest margins, riverine fringes, dune scrub Karroid scrub, dry watercourses Littoral forest, coastal woodland, evergreen forest

Evergreen forest, riverine fringes, open woodland Evergreen forest, riverine fringes, dune scrub Open woodland, riverine fringes

Vegetation types

Widespread: Ethiopia to southern Cape Swaziland to SW Cape along coastal areas Zimbabwe to SE Cape; Karoo to S Namibia Coastal areas from Transkei to SW Cape S Namibia to SE Cape Kenya along coast to SW Cape

Distribution

300-1500 mm, strong summerall year 300-1750 mm, strong summerstrong winter 200-800 mm, strong summerall year 500-1500 mm, summer-strong winter 200-800 mm, summer-all year 300-1500 mm, strong summerstrong winter

Rainfall mean and season

q~

P

O~

...¢

vo

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after 2 months this method had to be abandoned because of the high incidence of lateral growth. Complete leaf counts were repeated in January and April 1991. In order to estimate initial leaf area non-destructively, leaf length was measured in random subsamples of at least 15 leaves per plant, so that leaf areas could be calculated from regression equations of leaf length against leaf area (Van Laar, 1983) obtained at the end of the trial. During the week before harvesting, the number of main branches from the leading stem were counted as an indication of canopy architecture, and the inclination from horizontal of the topmost fully expanded leaf was measured. Abaxial stomatal density was estimated (stomata are universally absent on the adaxial leaf surface ) using nail varnish leaf imprints, on the topmost fully expanded leaf in a random subsample of three plants per species and treatment. Five fields of view of known area were counted per leaf and the mean of these counts converted to stomatal density. Plants were harvested in April 1991 and the roots, stems and leaves separated. Roots were carefully washed to remove adhering soil and organic particles, and leaves were passed through a leaf area meter (LI-3000 planimeter, LICOR, Lincoln, NB) before the three components were oven dried at 80°C to constant mass. Primary data were used to calculate the following additional variables: relative growth rates in height (RGRH), basal diameter (RGRD), leaf number (RGRLN) and leaf area (RGRLA), calculated as the difference between final and initial values divided by initial value and averaged over the 52 week trial; shoot to root ratio (S/R), leaf area ratio (LAR, cm 2 g-i ), leaf weight ratio (LWR) and specific leaf area (SLA, c m 2 g - i ). Subsamples of dried leaf material (three plants per species and treatment) 28

280

24

240

2O

-200

® 16

~160

i 12

-120

~

g

- 80 4

40

0

w A M 1990

J

J

A

S

0 0

Month

N

D

J

F

M

1991

Fig. 1. Mean daily m a x i m u m (squares) and m i n i m u m (triangles) temperature ( ° C ) and total rainfall (circles; ram) during intervals between growth measurements at the Kirstenbosch nursely. (April corresponds to the interval between the first two measurements etc.)

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were analysed for total leaf nitrogen using the standard micro-Kjeldahl technique. Those few plants dying or becoming severely stunted during the year were excluded from the analysis. The design was balanced by including only five of the six seedlings of each species per treatment plot, if necessary by excluding one at random. Plot means for each species were calculated before the data were analysed by two-way split-plot ANOVA (BMDP program 2V; Dixon, 1990). Leaf nitrogen variables and leaf stomatal density were analysed by two-way ANOVA (BMDP program 7D; Dixon, 1990) and multiple range tests (Student-Newman-Keuls). Climate data were obtained from the Kirstenbosch Weather Station (Fig. 1 ) and correlations between mean maximum and minimum daily temperature and relative growth rates in height and basal diameter were calculated.

Leafphotosynthetic responses As an indication of physiological plasticity, leaf photosynthetic gas exchange was measured in the nursery under natural light in early summer (November 1990) once plants had acclimated to the different shade treatments and were actively growing again following the winter months. The uppermost fully expanded leaf (generally third to fifth from the apex) was selected on each plant used for measurements. We used a portable infrared gas analyser (IRGA; Model LCA-2) in the open system and differential mode, with a single leaf enclosed in a Parkinson leaf chamber (Model PLC-N) (both Analytical Development Corporation, Hoddesdon, UK). The cuvette was held horizontally during measurements. The enclosed projected leaf areas were measured for subsequent incorporation into the calculations. Input air was supplied from 5 m above ground, and the IRGA set up to pass air at 0% relative humidity over the leaf. Air temperature and humidity inside the cuvette and incident photosynthetic photon flux density (PPFD) were measured by the chamber and recorded on the data logger. Net photosynthesis was determined from the flow rate (300 ml min- ~) and the concentration differences of CO2 and H20 between inlet and outlet air using the equations of Von Caemmerer and Farquhar ( 1981 ). Data were downloaded via RS232 interface to a microcomputer for processing. Diurnal patterns of leaf photosynthesis were measured, using three plants per species and treatment, to indicate periods of maximum activity. Leaves were each measured five different times during direct sunlight hours, except in the 80% shade-cloth treatment where leaves were measured only four times. Spot readings from three replicates per species and treatment were then taken during periods of maximum photosynthesis. In April 1991, three replicate plants per species and treatment were moved into a phytotron chamber delivering 2000/~mol m -2 s-t irradiance, in order

P.M. Holmes, R.M. Cowling~ForestEcology and Management 61 (1993) 199-220

205

to generate light response curves in a controlled environment. Plants were given 48 h to equilibrate to the 12 h photoperiod with ambient temperatures of 25°C alternating with 20°C in the dark and with 50% and 65% relative humidity respectively. Shade cloth was used to progressively reduce the irradiance, and at least 20 rain allowed for equilibration to each new irradiance level. Calculations of photosynthetic parameters follow the methods of Thompson et al. ( 1988 ). Maximum net photosynthetic rate (Am~), and dark respiration (Rdark), were calculated as the mean CO2 exchange rate under high light conditions and dark conditions, respectively. Apparent quantum yield of photosynthesis (or) was calculated as the slope of the initial portion of the light response curve. Light compensation point (Q0) was calculated as Q0 -" Rdark/O~

To estimate the light saturation point (Qt), a truncated rectangular hyperbola was fitted to the light response data using non-linear regression

A=min{a(Q-Qo)A*/[a(Q-Qo)+A], Am,x} where min means take the minimum value, Q is the incident PPFD and A* is a curvature parameter. The light saturation point (Qt) was then calculated as

Qt =A*Am~x/ [Ot(A*-Amax) l + Qo Results

Growth responses Height growth (mean RGRH) in C. aethiopica, Pappea, Schotia and Sideroxylon was significantly correlated with mean maximum daily temperature, and less significantly with mean minimum daily temperature (Table 2), but there was no correlation between diameter growth (mean RGRD) and temperature. There was a highly significant species effect for all growth variables, but only one variable (dry weight) had a significant shading effect, partly because of the low number of degrees of freedom (Table 3 ).

Shading effects Final height was greatest under 80% shade in all species except C. aethiopica and Pappea, which grew tallest under 40% shade (Table 3). Maximum RGRH was also recorded under 80% shade except in Pappea and Rhus, which peaked under 40% shade. Diameter growth and RGRD were highest in the open for all species, except C. aethiopica and Pappea, which again peaked

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Table 2 Correlations between RGRN and mean maximum and minimum daily temperatures (n = 12 ) Species

Cassine aethiopica Cassine peragua Pappea capensis

Percent shade

0 40 80

0 40 80

0 40 80

Max.

Min.

Species

0.844"* 0.633" 0.597*

0.746" 0.569 0.409

Rhus glauca

0.039 0.121 0.362

0.050 0.048 0.187

Schotia afra

0.653* 0.881"* 0.614"

0.712" 0.754** 0.525

Sideroxylon inerme

Percent shade

0 40 80

0 40 80

0 40 80

Max.

Min.

0.335 0.339 0.513

0.324 0.411 0.572

0.447 0.616" 0.511

0.365 0.529 0.472

0.632* 0.762** 0.468

0.614" 0.791"* 0.498

*0.01
under 40% shade. Final plant dry weight was similar in the open and under 40% shade, but much lower under 80% shade in all species.

Species effects The data indicate three groupings: Pappea and Schotia with slower growth than the other species; C. peragua and Rhus generally with the fastest growth; C. aethiopica and Sideroxylon usually intermediate between these two groups (Table 3). The largest relative increase in height under 80% shade compared with the open was in Schotia followed by C. peragua, and the lowest was in Rhus. The largest relative decrease in stem diameter under 80% shade compared with the open was in C. aethiopica, with Sideroxylon and Pappea showing least difference. Similarly, final dry weight differed most in C. aethiopica and least in Pappea and Sideroxylon between open and 80% shade treatments.

Morphological responses There was a highly significant species effect for all variables except leaf inclination, but significant shading effects only for S/R, LAR and SLA (Tables 3-6). There were significant species-shading interactions for LWR, SLA, leaf inclination, leaf nitrogen concentration and stomatal density, suggesting a different magnitude of response among species.

Shading effects With the exception of Pappea, all species responded to shading by increasing the S/R (Table 3). The number of lateral branches produced was similar in open and 40% shade treatments and, with the exception of Pappea, was greatly reduced under 80% shade. Rhus had a far more branched architecture

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207

Table 3 (a) Mean growth response of subtropical thicket species to different shade treatments in a nursery (n = 2 ) Species

Percent shade

Height (mm)

RGRn t

Cassine aethiopica

0 40 80

325.0 474.7 439.1

0.018 0.022 0.024

Cassine perugua

0 40 80

581.2 783.7 824.0

Pappea capensis

0 40 80

Rhus glauca

Diam. (mm)

RGRD 2

Dry wt. (g)

S/R 3

Branch No:

8.45 8.55 6.15

0.018 0.020 0.013

21.24 23.98 9.28

2.60 3.35 4.27

3.60 3.70 2.00

0.024 0.030 0.032

14.05 13.00 10.50

0.028 0.025 0.022

57.28 59.74 31.38

2.23 2.58 3.82

6.90 7.70 5.00

154.8 213.5 188.3

0.006 0.011 0.006

6.75 7.55 5.85

0.008 0.009 0.004

5.53 6.90 3.70

i.42 1.78 1.70

3.20 2.90 2.80

0 40 80

546.5 606.4 660.7

0.033 0.040 0.035

I 1.85 10.75 8.70

0.042 0.040 0.033

48.13 36.46 22.47

3.02 3.63 4.66

20.30 19.70 10.40

Schotia afra

0 40 80

146.0 227.3 280.5

0.010 0.017 0.022

7.60 6.95 5.70

0.013 0.011 0.005

6.94 6.94 4.27

1.65 2.54 3.24

2.50 1.40 0.90

Sideroxylon inerme

0 40 80

324.6 399.4 426.1

0.018 0.021 0.022

9.75 9.50 8.45

0.022 0.020 0.018

24.07 21.73 15.29

1.97 2.44 2.52

3.00 1.50 0.30

(b) F-values from split-plot ANOVA Factor

Species (SP) Shading (SH) SPXSH

d.f.

5, 15 2, 2 10, 15

F-values Height

RGRN

Diam.

RGRD

Dry wt.

S/R

Branch No.

40.9"" 17.3 0.5

65.3"" 15.0 i.2

75.5"" 6.0 1.6

69.7"" 11.6 0.4

51.2"" 226.7" 2.3

12.4"" 232.6" 0.9

30.6"" 19.5 1.2

2Relative growth in height (mm m m - t week- t ). 2Relative growth in diameter at base of stem (mm m m - t week- ~). JShoot to root ratio. 4Number of main branches from central stem. "~P< 0.001; "0.001 < P< 0.01; "0.01
than the other species. Final leaf number and RGRLr~ peaked in the open or 40% shade (Table 4). In all species, open and 40% shade treatments yielded similar results, with fewest leaves being produced under 80% shade. Final leaf area peaked under 80% shade in Rhus and Schotia, and under 40% shade in

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Table 4 (a) Leaf characteristics of subtropical thicket species grown under different shade treatments in a nursery (n=2) Species

Cassine aethiopica

Cassine peragua

Percent Leaf

RGR~'

Leaf area R G R ~ 2 LAR J

shade

No.

0 40 80

149.0 0.029 142.3 0.029 102.7 0.019

492.2 630.3 501.9

0.028 0.032 0.033

23.1 26.8 57.3

143.0 0.033

1592.0

0.043

172.8 0.040 82.9 0.026

1803.6 1469.6

0.046 0.045

0 40 80

'

(cm 2)

LWR 4 SLA s

(cm2g -')

Leaf incl.

(cm~g -') class~ 0.406 0.443 0.526

56.6 60.1 108.2

4.50 2.60 2.30

27.7

0.412

67.1

4.80

30.2 47.5

0.408 0.430

73.8 109.9

3.30 1.00

Pappea capensis

0 40 80

60.9 0.010 54.5 0.006 34.3 0.003

68.9 Ii8.7 82.9

-0.004 0.013 -0.003

14.9 22.7 27.8

0.221 0.270 0.199

72.5 88.3 135.9

4.20 3.00 2.60

Rhus glauca

0 40 80

404.9 0.057 276.2 0.053 201.1 0.042

1133.2 1153.7 1339.4

0.064 0.070 0.058

23.7 34.6 62.6

0.326 0.362 0.397

72.7 94.3 157.1

5.00 3.20 2.00

Schotia afra

0 40 80

49.1 0.018 49.0 0.020 40.7 0.015

115.4 166.6 202.9

0.018 0.026 0.031

16.4 23.6 47.8

0.298 0.357 0.455

54.4 66.0 104.3

4.10 2.50 2.70

Sideroxylon inerme

0 40 80

81.5 0.033 61.7 0.024 41.7 0.017

592.2 692.0 648.3

0.036 0.040 0.035

24.5 31.4 43.1

0.420 0.444 0.454

57.9 70.8 94.6

4.90 3.40 1.40

(b) F-values from split-plot ANOVA Factor

d.f.

F-values Leaf No. RGRu~

Species (SP) Shading (SH) SPXSH

5, 15 29.4*-2, 2 5.4 10, 15 1.7

59.1"" 13.7 1.0

Leafarea RGRt.,~

LAR

LWR

SLA

Leaf incl.

100.8'** 9.3 0.7

7.4" 44.6* 2.2

45.9*8.9 3.2"

18.7" 267.7" 2.6"

0.8 32.8 5.3"

48.3*" 13.0 0.7

IRelative growth rate in leaf number (no. n o . - ' week-'). ZRelative growth rate in leaf area (cm 2 cm-2 week- t ). 3Leaf area ratio. 4Leaf weight ratio. SSpecific leaf area. elnclination of leaf from the horizontal (nine classes: l, 0-10°; 2, I !-20 ° etc.). " P < 0 . 0 0 1 ; "0.001
the other species. RGRLA also peaked under either 40 or 80% shade. In all species, LAR peaked under 80% shade as did LWR, except for Pappea, which peaked under 40% shade. SLA was significantly higher under 80% shade in all species compared with the other two treatments. All species responded to

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209

Table 5 (a) Leaf nitrogen content in subtropical thicket species grown under different shade treatments in a nursery (X_+SD, n = 3 ) Variable

mgNg -t

Percent shade 0 40 80

g N m -2

0 40 80

Cassine aethiopica

Cassine peragua

Pappea capensis

Rhus glauca

Schotia afra

Sideroxylon inerme

10.08 _+ 1.14 10.76 _+0.50 12.11 +0.91

9.12 _+ 1.56 8.64" +0.77 12.51 b _+0.79

15.69 _+0.28 13.59 -+0.48 13.99 _+ 1.47

11.54 _+ 1.92 12.53 -+0.93 12.67 +0.67

12.17 ° _+ 1.44 15.36 _+ 1.50 19.22 b _+2.38

12.73 _+ 1.38 13.51 _+0.72 15.07 _+ 1.86

1.87" +0.37 1.96" +0.34 1.18 b +0.21

1.36 +0.44 1.31 +0.12 1.12 +0.07

2.66" +0.38 1.58 b +0.28 1.09b +0.26

1.58" +0.18 !.38" +0.16 0.72 b +0.02

2.39 +0.36 2.40 +0.12 1.89 +0.07

1.89 +0.24 1.88 +0.14 1.72 _+0.31

( b ) F-values from two-way ANOVA

Factor

Species Shading Interaction

d.f.

5, 36 2, 36 10, 36

F-values m g N g -l

g N m -2

24.5 "°° 17.2 °°° 4.3"

19.6"** 32.8*** 3.9"

°**P< 0.00 !; " 0 . 0 0 i < P<0.01.

Within a species, values with a different superscript are significantly different (Student-NewmanKeuls test, 95% confidence limits).

shading by reducing their leaf inclination from horizontal, In all species except Pappea, leaf nitrogen content on a dry weight basis peaked under 80% shade, but this was significant only for C. peragua and Schotia (Table 5 ). On a leaf area basis, leaf nitrogen content peaked in the open, except for C. aethiopica and Schotia in which it peaked at 40% shade. Stomatal density was highest in the open and lowest under 80% shade, with the exception of Schotia in which it was lowest under 40% shade (Table 6).

Species effects There was broad overlap in S/R among species, but in all shade treatments Pappea performed at the lower end and Rhus at the upper end. Compared with the open treatment, Schotia had the greatest relative increase in S/R under 80% shade and Pappea the least. Rhus and C. peragua had the highest

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Table 6 Leaf stomatal density (stomata m m - 2 ; X_+ SD, n = 3 plants t ) in subtropical thicket species grown under different shade treatments in a nursery Percent shade 0 40 80

Cassine aethiopica

Cassine peragua

275.6 + 56.4 238.6 +30.0 229.4 _+20.8

307.2 + 41.6 311.8 +22.9 228.7 _+ 17.6

Pappea capensis 243.2' + 14.8 221.8" + 12.2 143.2 b _+71.6

Rhus glauca 272.6" + 40.0 180.2" + 12.2 98.6 b + 14.1

Schotia afra 246.5" + 28.0 152.5 b + 12.2 173.9 + 16.2

Sideroxylon inerme 281.8" + 56.8 251.1 +23.8 170.9 b +4.6

tMean of five counts on one leaf per plant. Within a species, values with a different superscript are significantly different ( S t u d e n t - N e w m a n Keuls test, 95% confidence limits).

F-values from two-way ANOVA (log stomata) Factor Species Treatment Interaction

d.f. 5, 36 2, 36 10, 36

F 12.7 *° 41.9"" 4.1 **

***P< 0.001; *°0.001
incidence of lateral branching. Sideroxylon showed the greatest relative reduction in branching under 80% shade and Pappea the least change. Rhus had the highest values for leaf number and RGRLN. There was overlap among the other species, with C. peragua and C. aethiopica usually grouped above the remaining species, and Pappea at the lower end. Relative to the open treatment, Rhus plants under 80% shade had the greatest reduction in leaf number, and Schotia the least. Those three species with the greatest relative reduction in leaf number under 80% shade (Rhus, Sideroxylon, Pappea) also had the biggest relative increase in average leaf size between these two treatments. Three groupings were evident for leaf area and RGR~, in ascending order: Pappea and Schotia, C. aethiopica and Sideroxylon, C. peragua and Rhus. However, Schotia had the greatest relative increase in total leaf area under 80% shade compared with the open. In the open, Pappea and Schotia had a lower LAR than the other species, but in the other treatments there was broad overlap among species. Pappea had the lowest values for LWR, with the other species overlapping. Compared with the other species, C. peragua and Sideroxylon had very little increase in LWR between open and 80% shade treatments, and similarly recorded the lowest increase in SLA. For SLA there was broad overlap among species, with Pappea and Rhus grouped at the highest end. SLA and average leaf size both increased most in Rhus under 80% shade relative to the open. Cassineperagua and Sideroxylon were the most

P,M. Holmes. R.M. Cowling~ForestEcologyand Management61 (1993) 199-220

211

responsive to shading in terms of reducing leaf inclination: in both species leaves were held horizontally under 80% shade. Leaf nitrogen content on an area basis overlapped among species, but under 80% shade Rhus recorded lower and Sideroxylon and Schotia higher contents than the other species. There was also overlap among species for leaf nitrogen on a dry weight basis, except under 80% shade in which Schotia recorded the highest value. Although there was broad overlap among species, C. peragua had highest stomatal density under all treatments. Rhus had the lowest stomatal density under 80% shade.

Leafphotosynthetic responses There was a slight midday ( 11:00-15:00 h) depression in COz assimilation rate, with a dramatic increase in the later afternoon for C. aethiopica and Pappea. Except for measurements taken before 09:00 h, diurnal variation in PPFD did not exceed inter-plant variation in PPFD (within each shade treatment). Thus, the observed diurnal patterns may reflect responses to changes in vapour pressure deficit (VPD). In most species there was a good correlation between net COz assimilation and stomatal conductance (Gs), especially at lower conductance values. However, only C. peragua and Sideroxylon had a negative correlation between Gs and VPD (for plants grown in the open: C. Table 7 Mean maximum net CO2 assimilation rates ( X + SD, n= 3;/zmol CO2 m -2 s - ~) for plants exposed to different shade regimes Species

Cassine aethiopica

Cassine peragua Pappea capensis Rhus glauca

Schotia afra Sideroxflon inerme

Percent shade 0

40

! 7.90 + 5.90" 4.75 + 1.94 26.34 + 5.12" i 8.43 + 5.61 ! 1.54 + 9.25 5.83 + 0.60

6.52 6.70 8.34 13.55 4.18 4.39

80 + 0.20 + 2.79 + 3.27 b + 4.90 + 3.27 + 1.40

4.38 4.84 6.79 7.74 4.75 3.53

+ 1.76 b + 1.24 + 2.53 b + 0.92 + 3.03 + 0.82

Within a species, values with a different superscript are significantly different (Studcnt-NewmanKeuls test, 95% confidence limits). F-values.from two-way ANOVA

Factor Specics Treatment Interaction "**P< 0.001 ; **0.001 < P< 0.01.

d.f. 5, 36 2, 36 1O, 36

F 9.5"** 27.0"* 3.7"

2 !2

P.M. Holmes. R.M. Cowling/ForestEcologyand Management 61 (I 993) 199-220

Table 8 Photosynthetic parameters calculated from irradiance response curves for six subtropical thicket species subjected to different shade treatments. Data were gathered in the phytotron and methods of calculation follow Thompson et al. ( 1988 ). Standard deviations are given in parentheses (n = 3 ) Species

Percent A" shade

Rdark

a

(20

A,,~,

Q~

12.8 1.43(0.84) 9.1 0.77(0.21) 5.7 1.43(0.16)

0.0180(0.0076) 0.0159(0.0025) 0.0178(0.0028)

76.6(11.9) 48.0 (9.8) 80.7 (3.7)

8.06(0.47) 5.12(1.43) 5.01(2.04)

1286 784 736

40 80

16.6 1.49(0.10) 7.5 1.75(0.45) 5.4 1.19(0.34)

0.0197(0.0077) 0.0282(0.0030) 0.0196(0.0032)

81.7(23.5) 61.5 (9.2) 60.2(11.4)

9.53(1.31) 6.40(0.91) 4.38(1.06)

1217 1610 1243

0 40 80

25.5 1.92(0.97) 19.1 1.55(0.40) 5.7 0.95(0.26)

0.0177(0.0031) 0.0204(0.0061) 0.0191(0.0093)

92.3(50.8) 81.9(39.7) 56.6(22.3)

8.52(2.11) 12.09(3.76) 3.73(!.70)

815 1697 622

Rhusglauca 0 40 80

27.8 2.24(1.01) 16.9 2.11(0.54) 5.7 1.30(0.71)

0.0287(0.0054) 0.0266(0.0112) 0.0226(0.0115)

75.3(23.3) 84.8(27.3) 59.7(16.1)

14.75(1.91) 11.24(0.66) 3.72(0.75)

i170 1332 792

0 40 80

40.6 1.28(0.09) 21.5 0.75(0.15) 10.5 1.89(0.14)

0.017710.0095) 0.0185q0.0090) 0.0267q0.0091)

99.2(76.3) 50.4(30.0) 75.2(20.6)

12.9 (4.09) 10.3 (2.01) 7.09(0.67)

1165 1113 893

0

14.7 1.36(0.24) 8.7 2.10(0.16) 5.6 1.83(0.20)

0.0147(0.0017) 0.0206(0.0035) 0.0268(0.0035)

92.0(10.2) 103.7(16.8) 69.4(13.2)

8.45(2.45) 7.45(0.63) 4.83(0.65)

1444 2626 1382

Cassine aeth@ica

Cassine peragua

Pappea capens~

Schotia afra

Sideroxylon inerme

0

40 80 0

40 80

A*, dimensionless curvature parameter; R,~rk, dark respiration (#tool CO2 m -2 s -~); a, apparent quantum yield (tool CO. tool- *quanta); Qo, light compensation point (/zmol quanta m - ' s- i ); A.,~, maximum net CO2 assimilation rate (/zmol COs m -2 s-I); Qt, light saturation point (/zmol quanta

m-2s-I).

peragua, r=0.722, d.f.=13, P<0.005; Sideroxylon, r=0.794, d.f.=7, P<0.01). Spot readings taken during periods of highest photosynthetic activity yielded estimates of the mean maximum CO2 assimilation rate under the shade regime to which the plants were acclimated (Table 7). All species except C. peragua recorded highest rates in the open. Cassine peragua and Sideroxylon recorded low rates in all treatments. Irradiance levels vary within the phytotron and as the cuvette was moved to each plant, curves for some of the species-shading combinations are unfortunately lacking in data for higher irradiance levels, which has led to some spurious calculations of photosynthetic parameters (e.g. Pappea, open; Sideroxylon, 40% shade; Table 8 ). The phytotron environment was cooler and more humid than the nursery

P.M. Holmes, R.M. Cowling~ForestEcology and Management 61 (1993) 199-220

2 13

environment on a summer day, with air temperature not exceeding 25°C whilst relative humidity was maintained at 50%. This resulted in higher Am~ values in the phytotron for plants of C. peragua and Sideroxylon acclimated to the open. Cassine aethiopica, Pappea and Rhus recorded highest Am~ for plants acclimated to open and 40% shade treatments (excepting the spurious result for Pappea in the open). Am~ values for plants acclimated to 80% shade was similar in all species. There was little difference in R~rk among species and treatments, with only Pappea and Rhus showing the expected reduction with acclimation to increased shading. In all species except C. aethiopica, however, the light compensation point was lower in plants acclimated to 80% shade compared with those in the open. Only Schotia and Sideroxylon had a marked increase in apparent quantum yield with shading. Discussion

Although the shade-cloth treatments did not provide identical light environments to those found in a small gap or thicket understorey, they enabled us to assess the relative responses of the six species to shading and may point to the species' habitat preferences in the establishment phase. Light flecks which are important in maintaining the positive carbon balance in understorey species (Pearcy, 1983; Pearcy and Calkin, 1983 ) were precluded, and the red]far-red ratio, although not measured, was probably not reduced as much by shade cloth as by a thicket canopy. The latter may have altered the growth responses to shade, especially in the less shade-tolerant species (Hart, 1988). The response to shade treatment was compounded in some species by response to air temperature. In particular, growth in Pappea was strongly correlated with mean maximum daily temperature: it suffered considerable dieback during the cool winter months, with a high incidence of leaf-shedding. Three species (Pappea, C. aethiopica and Schotia) do not naturally occur in the southwest Cape, and it is possible that they may have responded differently tO shading had the trial been conducted in the warmer, drier climate of the eastern Cape. Slow height growth rates in C. aethiopica and Pappea were associated with low winter temperatures, whereas in C. peragua and Rhus there was no such relationship. Because of the severe die-back and generally poor growth in Pappea, especially under shade, and the greater initial age of its seedlings, its growth and some morphological responses to shading cannot be compared with those of the other species.

Growth responses Rhus had by far the fastest growth rates in height and stem diameter in all treatments, but produced relatively little biomass under 80% shade, as did C. aethiopica. Low relative biomass production in shade indicates shade intol-

2 14

P,II. Holmes, R.M. Cowhng/Forest EcologyandManagement 61 (1993) 199-220

erance (Popma and Bongers, 1988). The remaining species (C. peragua, Schotia, Sideroxylon, Pappea) had progressively higher relative biomass production under 80% shade. Pappea and Schotia were the slowest growing species.

Morphological responses The relative increase in allocation of dry mass to shoots is a well-documented response to shading (Popma and Bongers, 1988; Bongers et al., 1988). The relative decrease in branching under 80% shade was particularly high in Sideroxylon and is consistent with a strategy for maximising height growth in shaded environments. Relative growth in leaf number was generally highest in the open and sometimes under 40% shade, which is similar to findings for tropical forest species (Bongers and Popma, 1990). Rhus produced the most leaves and had the highest RGRLN and RGRLA in all shade treatments. Pappea and Schotia produced the fewest leaves and both the lowest leaf area and leaf weight relative to plant weight (excepting Schotia in deep shade). Cassineperagua and Sideroxylon had the lowest increase in LWR under 80% shade relative to the open, suggesting shade tolerance (McClendon and McMillen, 1982). Schotia had a large relative increase in LWR under 80% shade, suggesting shade intolerance, and Rhus and C. aethiopica were intermediate in their responses. The change in leaf inclination to near horizontal under 80% shade in C. peragua and Sideroxylon would enable them to trap relatively more irradiance under heavy shade than the other species. All species showed the typical pattern of lower stomatal density with increased shading, although this was not so marked in the two Cassine species which had the smallest increase in individual leaf area with shading. Reduction in stomatal density generally reflected the change in individual leaf area with shading. The pattern of nitrogen investment in subtropical thicket leaves is consistent with those from some other studies (e.g. Evans, 1989; Hollinger, 1989; Midgley et al., 1992): slightly elevated leaf nitrogen levels on a leaf weight basis with increased shading, converting to reduced leaf nitrogen on a leaf area basis, owing to the structural changes in the leaf induced by shading. Ramos and Grace (1990) found a trend for higher leaf nitrogen on a dry weight basis in shade-intolerant secondary species compared with shade-tolerant species, but there was no obvious trend in our data. The leaf nitrogen levels recorded for Rhus are lower than those measured in another study (Midgley et al., 1992) in which the nitrogen status of the soil had been raised by inputs from alien acacia litter (Witkowski, 1991 ). This comparison suggests that the potting soil used in this trial is representative of a fairly low nutrient system.

P M. Holmes, R.M. Cowling~Forest Ecology and Management 61 (1993) 199-220

215

Leaf photosynthetic responses Although the photosynthetic capacities of plants are poor predictors of their growth rates (Poorter, 1989; Denslow et al., 1990; Korner, 1991; this study), they enable comparisons to be made of the species' physiological plasticity under different shade regimes. Gas exchange measurements in the nursery environment indicate that C. peragua and Sideroxylon have low rates of CO2 assimilation in all light environments, whereas the other four species have much higher potential rates of CO2 assimilation when grown in the open. Estimates of photos)'nthetic parameters from light response curves in the phytotron indicate large values for Rda~k, (2O and QI in plants acclimated to the shade compared with those in studies of tropical tree seedlings (Thompson et al., 1988; Ramos and Grace, 1990). Values for those photosynthetic parameters for Rhus grown in the shade are also high compared with those measured for the same species in another study (Midgley et al., 1992). This suggests that the observed discrepancies may in part be due to an insufficient number of irradiance levels being recorded in our light response curves. A second problem may be that Rda~ was not measured with sufficient precision by the open gas exchange system (Ramos and Grace, 1990). A common pattern of response to shading is a reduction in Am,x and light compensation and saturation points, together with the maintenance of a (Midgley et al., 1992). Of our six thicket species, only Pappea and Rhus demonstrated this pattern. Sclerophyllous trees and shrubs have a relatively low potential photosynthetic nitrogen-use efficiency (Field and Mooney, 1986) and those of mediterranean regions may reach light-saturated rates of photosynthesis at less than one-third of the maximum irradiance, apparently owing to low photosynthetic enzyme content (Mooney, 1981 ). In plants acclimated to the open, light saturation generally occurred at about half the maximum irradiance. This may relate to the higher leaf nitrogen content and possibly higher photosynthetic enzyme content of the subtropical thicket leaves compared with those measured for mediterranean shrubs (Mooney, 1981 ). The observed diurnal CO2 assimilation pattern with a midday depression, has also been recorded for some mediterranean shrubland species in the southwest Cape during summer (Van der Heyden and Lewis, 1990) and in mediterranean sclerophyllous shrubs in response to seasonal drought (Mooney, 198 l; Harley et al., 1987). As our plants were well-watered, CO2 assimilation may have been limited either by high leaf temperature, or by stomatal closure in response to an increased vapour pressure difference between leaves and air: the so-called 'feed-forward response mode' (Chaves, 1991 ). The ability of C. peragua and Sideroxylon to respond to increasing VPD suggests that they are drought-avoiders of the saving type (Chaves, 1991 ). Such an adaptation may be appropriate for understorey or forest species which would ex-

2 16

P..t£ Holmes. R.M. Cowling/ForestEcology and Management 61 (1993) 199-220

perience a moister microclimate than that of open thicket. The other species may rather respond to a decrease in plant water potential: the so-called hydraulic 'feed-back response' (Chaves, 1991 ) and high leaf temperature, rather than stomatal closure, probably limited their CO2 assimilation at midday. General discussion With the exception of Pappea, which performed very poorly, all species were able to accumulate biomass in all three shade environments. Many long-lived perennials, inci!uding most trees, experience a wide range of environments during their life-span and as a result have evolved high acclimation potential and phenotypic plasticity to compensate for immobility (Bazzaz, 1991). Thicket species also demonstrate phenological plasticity: Pierce and Cowling (1984) found no obvious patterns of growth, flowering or fruiting, indicating a generalist strategy, in which plants respond to suitable conditions when they arise. On a relative basis, however, C. peragua and Sideroxylon are the most shade tolerant: reduction of growth in the shade was relatively slight, as was the increase in LWR; leaf inclination was adjusted to near horizontal in the shade and A,,a~ remained fairly low in sun-acclimated plants. These two species also occur in evergreen forest (Coates-Palgrave, 1977 ) and may resemble shade-tolerant primary species of tropical forests in not requiring canopy gaps for seedling establishment (Denslow, 1980; Augspurger, 1984; Brokaw, 1987; Denslow, 1987; Uhl et al., 1988). The rapid growth in Rhus and its high potential rates of photosynthesis indicate its similarity to tropical forest pioneers (Uhl et. al., 1988; Ramos and Grace, 1990) and suggest it would benefit from canopy gaps for colonisation. However, it has a very broad irradiance tolerance and may even be able to establish in the shade. A high degree of lateral canopy spread has also been noted in the seedling stage of many tropical forest pioneer trees (Grime, 1987 ). Although C. aethiopica has a slower growth rate than Rhus and could not be classed as a pioneer, it would probably benefit from canopy gaps for establishment because of its relatively high biomass production in the open and high potential rates of photosynthesis. Pappea and Schotia deviated in their responses to shade from the tropical forest model, because of their combination of slow growth yet high potential rates of photosynthesis in sun-acclimated plants. They naturally occur in open semi-arid habitats as well as in thicket (Coates-Palgrave, 1977). Adaptation to adverse environments (e.g. those with periodic drought) may have resulted in genetic constraints to rapid growth (Poorter, 1989). Evergreen plants subjected to drought have evolved a structural system which generally has a low leaf area index (and hence low potential production) and a high ratio of woody conductive tissue to leaf tissue (Mooney, 1981 ). Pappea and Schotia have both the smallest leaf area and leaf weight relative to plant weight of all

P.M. Holmes, R.M. Cowling/ForestEcology and Managemem 61 (1993) 199-220

2 17

species tested (excepting Schotia in deep shade). Their relatively poor performance in the shade suggests that they may require canopy gaps for successful seedling establishment. Preliminary germination studies are consistent with this prediction: fewer germinants were recorded in the shade than in open or lightly shaded environments in both species (P. M. Holmes, unpublished data, 1990). The results suggest that recruitment in eastern Cape subtropical thickets could be improved with the presence of canopy gaps for less shade-tolerant species and shaded sites for shade-tolerant species. Superimposed on the gap dynamics is the unpredictability of the rainfall ofthe region (Cowling, 1984 ). Thicket-forming shrubs and trees in mediterranean-climate regions where moisture may be limiting require a temporal pattern of high precipitation to produce a large seed crop (Keeley, 1986 ), followed by above-average precipitation for seedling establishment (Keeley, 1986; Hastings et al., 1989). It is highly probable that recruitment of the full species complement in eastern Cape subtropical thickets also requires an unusual temporal sequence of rainfall events in addition to the presence of suitable canopy gaps. This will be difficult to test in the field because of the long time scales involved. A possible approach may be a demographic study linked to climatic records. Other factors which might affect recruitment and which require investigation are seed dispersal and viability. Many of the species present in subtropical thickets, especially those also occurring in evergreen forests or riverine thickets, are at the arid end of their distribution range. Although seedling establishment may occur episodically or infrequently, once established, they persist as a significant component of the vegetation.

Acknowledgements We thank the staff at the Kirstenbosch National Botanical Gardens for accommodating the trial in their nursery and for their assistance in moving bags and watering plants. We also thank Graham La Cock for providing half the Pappea seedlings. Wendy Paisley helped to monitor plant growth and Sue Ganse van Rensburg, Robert Tshivandekanu, Fana Mokoena and Marijke Honig assisted with the harvest. Willy Stock undertook the leaf nitrogen determinations. We are also grateful to Mike Cramer and Niki Phillips for advice and assistance in using infra-red gas analysis equipment. We thank Guy Midgley, Jeremy Midgley, Tony Rebelo and an anonymous referee for their comments on earlier manuscripts. Pat Holmes' research was funded by the Foundation for Research Development and the University of Cape Town.

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