Correlations between morphological-anatomical leaf characteristics and environmental traits in Southwest African species oí Androcymbium (Colchicaceae)

              Bot. Macaronésica 24: 73-85 (2003) 73
CORRELATIONS BETWEEN MORPHOLOGICAL-ANATOMICAL LEAF
CHARACTERISTICS AND ENVIRONMENTAL TRAITS IN SOUTHWEST
AFRICAN SPECIES OF ANDROCYMBIUM (COLCHICACEAE)
N. MEMBRIVES\ J. PEDROLA-MONFORT'' & J. CAUJAPE-CASTELLS^
^Estació Internacional de Biología Mediterránia-Jardí Botánic Marimurtra. Passeig Karl Faust, 10. 17300
Blanes. Girona. Apdo. Correos 112. Spain. e-mail: (nuriamem@jazzfree.com and jpedrola@grn.es)
^Jardín Botánico Canario Viera y Clavijo. Apdo 14 de Tafira Alta. 35017. Las Palmas de Gran Canaria.
Spain. e-mail: (julicaujape@granca.step.es)
Recibido: noviembre 2000
Palabras clave: Androcymbium, Colchicaceae, Sudáfrica, morfología, anatomía, aspectos ambientales,
correlaciones.
Key words: Androcymbium, Colchicaceae, South África, morphology, anatomy, environmental traits,
correlations.
SUIVIIVIARY
We studied 32 populations belonging to 17 Southwestern African taxa of the genus Androcymbium in
order to explore the relationships between leaf morphological and anatomical variation and environ­mental
characteristics as measured by distribution in two different type velds (Fynbos and Karoo-Karoid
types) and the valúes of 16 edaphic parameters from 22 soil samples. Our results show that only hydric
disponibility (measured as the amount and distribution of annual rainfall, and the wíater retention capa-city)
correlates significantly with morphological leaf characteristics in Androcymbium. We detected no
significant correlations between pairwise combinations of anatomical traits and climatic or edaphic
parameters. These results conform to the hypothesis that the diversification of Southwestern African
species of Androcymbium, has been mainly influenced by the arid gradient that already exlsted when
these species began to diversify in the Late Miocene. Thus, they seem to agree with the hypothesis of
Stebbins that predicts relatively rapid plant evolution in arid to semiarid regions. Because solely some
combinations between characteristics related to aridity and morphological traits are significantly corre-lated,
our results reflect only partially Axeirod and Raven's suggestion that the specific diversity in South
África is a consequence of climatic and edaphic fragmentation.
RESUiVIEN
Se estudiaron 32 poblaciones pertenecientes a 17 taxones del género Androcymbium distribuidas
en Sudáfrica Occidental con el objetivo de explorar las relaciones entre características morfológicas y
anatómicas foliares y características ambientales medidas según la distribución en dos tipos de vege-
ISSN 0211-7150
74 N. MEMBRIVES, J . PEDROLA-MONFORT & J. CAUJAPE-CASTELLS
tación diferentes (Fynbos y Karoo-tipos karoides) y los valores de 16 parámetros edáficos procedentes
de 22 muestras de suelos. Los resultados obtenidos mostraron que solamente la disponibilidad hidrica
(medida a partir de la cantidad y distribución de las lluvias anuales, y de la capacidad de retención de
agua) se correlaciona significativamente con las características morfológicas de las hojas en Andro-cymbium.
Respecto a los caracteres anatómicos, no se observaron correlaciones significativas con
parámetros climáticos o edáficos. Estos resultados sugieren que la diversificación de las especies de
Androcymbium en Sudáfrica Occidental ha estado condicionada principalmente por el gradiente de
aridez desde el inicio de su especiación a finales del Mioceno. Estos resultados están de acuerdo con
la hipótesis de Stebbins que sostiene una rápida evolución de las especies vegetales en regiones
áridas y semiáridas. Nuestros resultados reflejan sólo parcialmente la hipótesis de Axeirod y Raven que
sugiere que la diversidad específica en Sudáfrica es una consecuencia de la fragmentación climática y
edáfica, debido a que únicamente algunas combinaciones entre características relacionadas con la
aridez y aspectos morfológicos están significativamente correlacionadas.
INTRODUCTION
The species of Androcymbium Willd. (Colchicaceae) are geophytes with an an-nual
vegetative cicle that spend the unfavourable period buried like tunicated
corms. The genus includes about 50 species (ARNOLD & WET, 1993; IVIÜLLER-DOBLIES
& IVIÜLLER-DOBLIES, 1984, 1998; PEDROLA-IVIONFORT et al., 1999a, 1999b,
2000) with a disjunt distribution in arid regions of South Europe and África.
The six species in Northern África distribute all along the IVlediterranean Basin
and in the Canary Islands. The rest of species in the genus (aproximately 45) are
distributed in South África, mainly in the Western región. Southwestern African
species display much higher variability levéis at the morphological (BAKER, 1974;
KRAUSE, 1920; MEMBRIVES, 2000), seminal (MEMBRIVES et al., 2000a), palynologi-cal
(MARTÍN ef al., 1993; MEMBRIVES, 2000), anatomical (MATEU-ANDRÉS eí al.,
1996; MEMBRIVES etal., 2000b), karyological (MARGELI etal., 1998; MONTSERRAT eí
al., in prep.), allozymatic (MEMBRIVES, 2000), and cpDNA levéis (CAUJAPÉ-
CASTELLS eí al., 1999), than their Northern African congeners (PEDROLA-MONFORT,
1993; PEDROLA-MONFORT & CAUJAPÉ-CASTELLS, 1996).
STEBBINS (1952 in AXELROD, 1972) suggested that there are several reasons
why plant evolution would be relatively rapid in arid and semiarid regions. First,
local diversity of soils (and other factors) in áreas where the moisture is limited has
a greater effect on the flora and vegetation than in regions where moisture ¡s ade-quate.
Second, the regional diversity of semi-arid climates promotes the fragmen-tation
of médium to large-sized populations into smaller units which are isolated
from each other but can exchange genes by occasional migration and establish
populations that may give rise to new species. And third, in dry regions, many dif-ferent
specialized vegetative structures (e.g., reduced leaf size, specialized leaf
covering, deciduous habit, deep root system, swollen trunks or bulbs) can evolve
which may enable plants to withstand periods of severe drought. More recent
works argued that the climatic and edaphic fragmentation that characterizes
Southwest África (RICHERSON & LuM, 1980; SHMIDA & WILSON, 1985; BROWN, 1988;
DIAMOND, 1988; WILLIAMSON, 1983; CORNELL, 1993; COWLING eí al., 1997) is the
main cause of the specific diversity of its flora and fauna (AXELROD & RAVEN, 1978).
Thus, climatic and edaphic heterogeneity could be one relevant factor to explain
the observed morphological and anatomical differentiation among the species of
CORRELATIONS BETWEEN MORPHOLOGICAL-ANATOMICAL LEAF CHARACTERISTICS. 75
IRRO-EK6
HUNT-EK3
POEL-NB
I I Fynbos
I I Karoo-Karoid types
CAPE-HO
AUST-WP
AUST-GH
Figure 1.- Geographical distribution of genus Androcymbium according to the veld types (Fynbos and
Karoo-Karoid types). Abbreviations of populations are described in Table 1.
Androcymbium distributed in this área, and between them and their Northern Afri-can
congeners. The main objective of this work is to explore the possible relation-ships
between the morphological and anatomical variation and environmental (cli-matic
and edaphic) parameters in this geographical circumscription of Androcym­bium.
MATERIAL AND METHODS
The material studied connes from 32 populations belonging to 17 Southwestern
African taxa of the genus Androcymbium (Table 1, Fig. 1). These samples are cu-rrently
in cultivation at the greenhouses of the "Estado Internacional de Biología
Mediterránia-Jardí Botánic Marimurtra". Morphological and anatomical characteris-tics
were taken from MEMBRIVES et al. (2000b) and are summarized in Table 2.
Climatic and edapiíic parameters- The studied populations are distributed in two
veld types -Fynbos, and Karoo-Karoid- (Table 1, Fig. 1) according to the dassifi-cation
in ACOCKS (1988). Twenty-two soil samples from these populations oí An­drocymbium
(Table 3) were analyzed following the analytic methods described in
HERRERO-BORGOÑON (1992). The measures of pH were taken from a pH-meter
Beckman H-2 with glass electrodes and calomelans. Water retention capacity
76 N. MEMBRIVES, J . PEDROLA-MONFORT & J. CAUJAPE-CASTELLS
Table 1.- Populations oí Androcymbium analyzed, according to the type veld where inhábil (Fynbos and
Karoo-Karoid types).
Species Code Locality
Taxa i
A. austrocapense U.IVIüll.-Doblies & D
IVIüll.-Doblies
nhabiting the Fynbos
AUST-GH 3418AC (SIIVIONSTOWN) Good Hope Cape
A. capense (L.) K.Krause
A. eghimocymbion U.IVIüll.-Doblies & D. EGHI-GI
Müll.-Doblies
Taxa inhabiting
A. altánense Schónland subsp. clanwi-lliamense
Pedrola, Membrives & J.
M.Monts
A. bellum Schltr. & K. Krause
AUST-WP 3418AD (SIMONSTOWN) Whales Point.
Cape Point Reserve
CAPE-HO 3318AB (CAPE TOWN) Malmesbury to
Hopefield Road, Km 49
3218DB (CLANWILLIAM) Piketberg to Ci-trusdal
Pass
Karoo-Karoid vegetation types
ALBA-PK 3219AA (WUPPERTAL) Clanwilliam to
Wuppertal Road. Km 10
A. burchellii Baker subsp. burchellii
A. burchellii Baker subsp. pulchrum Pe­drola,
Membrives, J. M. Monts & Caujapé
A. circinatum Baker
A. cuspidatum Baker
A. dregei C.PresI
A. eghimocymbion U. Müll.-Doblies & D.
Müll.-Doblies
A. hantamense Schinz
A. henssenianum U. Müll.-Doblies & D.
Müll.-Doblies
A. huntleyi Pedrola, Membrives, J. M.
Monts & Caujapé-Castells
A. irroratum Schltr. & K. Krause
BELL-VI 2817DC (VIOOLSDRIFT) Steinkopf to
Vioolsdrift Road, Km 40
BURC-HX 3319BC (WORCESTER) Worcester to
Towsrivier Road.
PULC-CA 3119DA (CALVINIA) Calvinia to Ceres Road,
7 km turnoff to Kreitzberg
PULC-NI 3118AA (CALVINIA) Wild flower reserve of
Nieuwoudtville
CIRC-NB 2917DB (SPRINGBOK) Springbok to Naba-beep
Road, 100 m
CIRC-SB 2917DB (SPRINGBOK) 3 km W of Spring­bok
CUSP-CA 3119DA (CALVINIA) Calvinia to Ceres Road,
7 km turnoff to Kreitzberg
CUSP-MO 3320CD (MONTAGU) Near Montagu-Bads-kloof.
W of the Gorgo
DREG-PK 3219AA (WUPPERTAL) Clanwilliam to
Wuppertal Road, Km 28
EGHI-PK 3219AA (WUPPERTAL) Clanwilliam to
Wuppertal Road, Km 28
HANT-CA 3119DA (CALVINIA) Calvinia to Ceres Road,
7 km turnoff to Kreitzberg
HENS-EK 2817CC (VIOOLSDRIFT) Eksteenfontein to
Modderfontein Road
HUNT-EK1 2917AD (SPRINGBOK) Springbok to Port
Nolloth Road, 14 km to Eksteenfontein
HUNT-EK3 2917AD (SPRINGBOK) Springbok to Port
Nolloth Road, 20 km to Eksteenfontein
IRRO-EK 2917AD (SPRINGBOK) Sphngbok to Port
Nolloth Road, 6 km to Eksteenfontein
IRR0-EK2 2917AD (SPRINGBOK) Sphngbok to Port
Nolloth, 15 km to Eksteenfontein
IRR0-EK6 2817CC (VIOOLSDRIFT) Eksteenfontein to
Modderfontein Road
IRRO-KA 3018CB (KAMIESBERG) Bitterfontein to
Kliprand Road
IRRO-KW 3118BC (VANRHYNSDORP) Vredental to
Koekenaap Road, 100 m to train station
IRRO-VP 3119AC (CALVINIA) Vanrhynspass
IRRO-VY 3118AD (VANRHYNSDORP) Vrendendal to
CORRELATIONS BETWEEN MORPHOLOGICAL-ANATOMICAL LEAF CHARACTERISTICS... 77
Vanrhynsdorp Road
A. poeltianum U. Müll.-Doblies & D. Müll.- POEL-CO 2917DB (SPRINGBOK) Springbok to Con-
Doblies cordia Road
POEL-NB 2917DB (SPRINGBOK) Springbok to Naba-beep
Road, 100 m
POEL-ST 2917DC (SPRINGBOK) Steinkopf to Spring­bok
Road, 5 km -
A. villosum U. Müll.-Doblies & D. IVIüll.-VILL-EK 2817CC (VIOOLSDRIFT) 1 km 8 of Eks-
Doblies teenfontein
VILL-ST 2917BC (SPRINGBOK) 3 km S of Steinkopf
A. walterí Pedrola, Membrives & J. WALT-ST 2917DC (SPRINGBOK) Steinkopf to Spring-
M.Monts bok Road, 5 km
(WRC) was measured as the percentage of water retained in the soil after the cen-trifugation
of 1000 g of moist sample by capillar ascensión. The total percentage of
carbonate was analyzed with a Bernard calcimeter. The percentage of organic
material was measured following the Jackson method, which is based on the oxi-dation
in cold of the organic matter with Potassium bichromate in acid solution. The
surplus of dicromate was calculated with ferríc sulphate. The quantity of mineral
nitrogen (the only kind assimilable by plants) was determined by distillation of a soil
extract in KCI 2N and collected with a flask containing a mixture of indicators. This
solution was titrated with sulphuric acid 0.001 N. The amount of assimilable phos-phor
was evaluated by the Olsen method, and the colorimetric measures were
made with a Zeiss spectrophotometer using a wavelength of 660 mu. The amount
of assimilable potassium was estimated by atomic absortion spectrophotometry.
Cathionic interchange capacity (CIC) was evaluated by the Bower method, with
little modificatíons. The mechanic analysis consisted of evaluating the soil texture
and the amounts of sand, mud and clay contaíned in samples with the method of
the Bouyoucos densimeter.
Data analysis.- The differences among pairwise combinations of morphological
and anatomical characteristics and veld types were evaluated using a student-t
test. Associations among morphological and anatomical characteristics and
edaphic parameters were calculated with Pearson's correlation. Qualitative cha­racteristics
were coded with numerical valúes (leaf color: 0=green, 1=glaucous;
leaf margin indument: O=smooth or with papillaes, 1=hairy; epidermic cells shápe:
1=rectangular, 2=romboidal, 3=polygonal; mesophyll cells: 0=undifferentiated,
1=differentiated; section: 1=flat, 2=semi-flat, 3=V-shaped; idyoblasts at leaves:
0=unfrequent, 1=frequent; central lamina cells: 0=different in size from the other
cells; 1=similar in size to the other cells). Data analyses were made using the sta-tistic
package SPSS/PC+ versión 6.1.2 (1995).
RESULTS
a) Correlations between morphological-anatomical characteristics and veld
types
Leaf length, leaf section and the central epidermic cells sizes were the only
three characters that differred significantly between the two veld types where the
examined populations occur (Table 4). The four populations from the Fynbos
Taxa
A. albanense subsp.
clanwilliamense
A. austrocapense
A. bellum
A. burche////subsp.
burchellii
A. burchellii subsp.
pulchmm
A. capense
A. circinatum
A. cuspidatum
A. dregei
A. eghimocymbion
A. hantamense
A. Iienssenianuní
A. huntleyi
A. inoratum
A. poeltianum
A. villosum
A. walteri
Shape
L-1J\
L-LA
L
OV-IJV
OV-UV
1 ^
L-LA
OV-LA
A
L-LA
LA
A
L-LA
OV-LA
L-LA
L-LA
L-LA
Leaves
Length
13.3
23.8
13.0
15.9
13.0
15.3
19.3
4.1
7.9
21.6
15.2
15.0
8.1
11.4
12.4
13.4
16.9
C
GR
GR
GL
GR
GR
GR
GL
GR
GL
GR
GL
GL
GL
GR
GL
GL
GL
Shape
DE
DE
E
OR
OV-OR
E
E-DE
DE
A
DE
E-LA
LA
E-DE
E-DE
LA
E-DE
E-DE
Bracts
Length
2.7
3.8
. 3.3
3.9
7.4
4.7
4.5
4.1
4.3
4.1
7.7
5.7
3.1
3.8
4.6
5.5
4.3
C
GR
GR
GL
WH
RD
WH
GL
GR
GR
GR
WH
GL
GL
GR
GL
GL
GL
SECT
V
V
V
F
F
F
F-V
F
V
V
F
F-V
F-V
F
F
F-V
F
Leaf
Margin
Papillae
Papillae
Smooth
Halry{4-6)
Hairy(5-9)
Halry(8-10)
Smooth
Smooth
Papillae
Papillae
Hairy(3-5)
Smooth
Snrooth
Papillae
Papillae
Hairs(l)
Papillae
ECSad
RE
RO
RE
PO
PO
RE
RE
RE
RE
RE
RO
RE
-
RO
RE
RE
RE
STad
35.7
34.1
25.4
25.7
32.7
32.9
29.7
27.6
25.9
39.6
36,7
-
-
36.1
25.5
20.0
31.1
STab
38.6
34.0
18.2
24.5
30.0
32.7
18.6
20.7
28.9
40.0
27.7
-
-
31.6
18.8
20.0
28.4
M
UD
D(2-3)
UD
D(4)
0(2-4)
D(1)
UD
UD
0(1)
UD
0(5-7)
UD
UO
0(2-3)
UD
UD
UD
Id
F
F
FF
F
F
F
F
FF
FF
F
F
FF
F
F
FF
F
FF
CCS
0
S
s
0
0
0
0
s
s
s
0
0
D
0
0
0
0
Table 2. Morphological and anatomical characteristics of genus Androcymbium in Southwest África (from MEMBRIVES eí al., 2000b). Shape: A=Acicular;
DE=Deltoideous; E=Elliptic; L=L¡near; LA=Lanceolate; OR=Orbicular; OV=Ovate. Color (C): WH=White; GL=Glaucous; RD=Reddish; GR=Green. Section
(SECT): F=flat; V=V-shaped. Leaf margin: n' of cells of the hairs in brackets. Epldermic cells siiape in adaxial side (ECS): RE=Rectangular,
00
m
03
71
<
m
c_
•0
m
O
>
1
O
-n
O
Ti
>O c
>
"m0
1 >O
RO=Romboidal, PO=Polygonal. STab and STad=Stofnata indexs in adaxial and abaxial sIde (in %). Mesophyll (M): D=differenciated (n" of layers of paly-sade
parenchyma in bradcets); NO=Undifferenciated. Idyoblasts (Id): F=frequent; FF=few frequent. Central cells size (CCS): D=d¡fferent size; S=similar
size. Long measures are expressed In cm.
Taxa
ALBA-PK
AUST-GH
AUST-WP
AUST-WP
BURC-HX
CAPE-HO
CIRC-SB
CIRC-SB
CUSP-CA
DREG-PK
EGHI-CI
EGHI-PK
HANT-CA
HENS-EK
IRRO-EK
IRRO-KA
IRRO-KW
PULC-CA
PULC-NI
VILL-EK
VILL-ST
WALT-ST{1)
PH
7.06
7.85
7.06
7.09
6.99
7.08
5.05
6.68
6.57
6.32
7.84
6.54
7.19
8.49
7.88
7.69
8.25
7.17
6.57
8.23
6.54
7.28
WRC
4.76
9.65
3.59
6.08
17.40
25.34
6.89
5.12
40.65
5.37
7.73
5.14
62.12
5.96
5.17
6.98
6.59
24.23
36.71
14.10
9.08
6.86
Salinjty
(mmhos)
0.36
0.18
0.09
0.93
0.24
0.95
0.31
0.27
0.51
0.42
0.31
0.44
0.99
1.27
0.33
0.64
1.51
0.78
0.32
0.89
0.48
0.57
C
0.78
6.25
3.51
0.98
3.32
0.87
0.46
0.68
1.09
0.60
1.86
0.71
1.61
1.80
0.42
2.07
1.71
1.23
1.04
6.64
1.15
1.20
o.m.
1.24
1.76
9.50
5.04
1.09
0.59
1.94
1.21
1.64
1.77
1.23
2.40
0.72
0.40
0.26
0.40
0.26
2.11
1.08
0.53
1.08
0.24
N
0.03
0.46
2.07
0.49
0.13
0.06
0.11
0.08
2.24
0.12
0.31
0.16
0.21
0.28
0.48
0.25
0.23
1.62
1.89
0.49
0.10
0.07
P
1.99
3.25
3.08
2.60
1.71
2.84
1.90
1.82
2.73
2.18
2.71
2.81
2.77
1.96
3.97
2.23
2.10
3.12
2.86
4.08
2.07
3.16
K
1.51
0.09
0.74
0.55
0.13
0.41
0.25
1.37
0.68
0.61
0.31
0.42
0.76
0.75
0.82
0.80
1.03
0.39
0.40
0.11
0.19
0.68
CIC
5.14
4.59
19.20
10.99
15.07
12.34
9.55
5.33
21.22
6.42
6.55
6.97
18.82
3.69
1.93
4.42
3.37
18.24
18.03
4.97
10.21
3.36
Sand
90.73
92.65
92.65
83.80
58.96
54.64
71.53
84.61
44.02
82.96
87.57
82.62
54.79
77.94
83.70
80.48
76.97
54.99
40.98
61.88
69.81
78.82
Mud
4.23
5.21
6.95
14.38
15.26
23.03
17.12
9.56
20.10
11.27
4.25
13.04
10.44
16.28
13.47
12.28
17.32
16.97
27.27
30.25
14.11
15.42
Clay
5.04
2.14
0.40
1.82
25.78
22.33
11.35
5.83
35.88
5.77
8.18
4.34
34.77
5.78
2.73
7.24
5.71
28.04
31.75
7.87
16.08
5.76
Texture
AR
AR
AR
AR-F
F-AC-AR
F-AC-AR
F-AR
AR-F
F-AC
AR-F
AR-F
AR-F
F-AC-AR
AR-F
AR-F
AR-F
AR-F
F-AC-AR
F-AC
F-AR
F-AR
AR-F
Thick
41.75
53.57
42.90
30.34
7.43
4.93
18.73
21.87
5.55
16.95
34.63
52.61
11.94
20.19
24.29
39.74
22.25
10.35
4.26
17.00
34.87
45.31
Sand
Middie
36.89
30.37
36.04
47.06
38.13
32.58
43.18
54.42
26.50
49.26
24.66
17.63
33.29
33.90
40.79
23.13
33.18
15.17
15.39
19.86
27.02
21.37
Thin
12.09
8.71
13.71
6.40
13.40
17.13
9.62
8.32
11.97
16.75
28.28
12.38
9.56
23.85
18.62
17.61
21.54
29.47
21.33
25.02
7.92
12.14
O
73
71
m >
—1
O
2
m
m
m
z
O
7¡
"0
I o
O
O >
1 > 2> -H
O s
o >
r->
m
TI
O
X
>>
O
H
m
2
H
W
Table 3.- Results from the edaphic analyses. WRC= water retention capadty (%). C= total carbonates (%). o.m.= organic material (%). N= mineral nitrogen
(mg N/IOOg). P= assimilable phosphor (mg P2 05/IOOg). K= assimilable potassium (meq K/IOOg). CIC= cathionic Interchange capacity (meq/IOOg). The
amounts of sand, mud and day are expressed in %. Texture: F=Franco, AC=Clayey, AR=Sandy.'" same data for population POEL-ST. Abbreviations of
populations are descrit)ed In Table 1.
CD
80 N. MEMBRIVES, J. PEDROLA-MONFORT & J. CAUJAPE-CASTELLS
studied showed leaves significantly longer than those of populations from the Ka-roo,
a V-shaped section and central cells similar in size to the rest. Androcymbium
capense, that exhibited a fíat leaf section and whose central epidermic cells were
larger than the rest was the only exception to this pattern (MEMBRIVES ef al.,
2000b). Conversely, species distributed in the Karoo-Karoid types showed fíat or
semi-flat section (except for A. bellum, A. dregei and A. eghimocymbion), and cen-
• tral cells larger than the rest (except for A. cuspidatum and A. dregei).
b) Correlations between morphological-anatomical characteristics and edaphic
parameters
Table 5 shows that only the edaphic characteristics related to soil textura
showed significant correlations with most morphological variables studied. Leaf
length and shape (lenght/width) were significantly correlated with the percentage of
clay. Soils with a low percentage of clay were associated with long and lanceolate
leaves, while soils with a high percentage of clay were associated with predomi-nantly
short and rounded leaves. Bract length was positively correlated with CIC,
WRC and percentage of mud and clay, and negatively correlated with the percen­tage
of sand. Leaf section was significantly correlated with WRC and percentage of
clay and sand. Fiat leaf sections were associated with soils with high WRC, while
V-shaped sections were observed predominantly in low WRC soils. Leaf color
(green or glaucous) and bract shape did not correlato significantly with any of the
edaphic parameters analyzed.
The morphology of the epidermic cells on the adaxial face of the lamina was
positively correlated with CIÓ, WRC, and with the percentage of clay. Romboidal
and polygonal cell shapes were associated to soils with high CIC, WRC and per­centage
of clay, whereas rectangular cells were associated with more arid condi-tions.
Adaxial side stomatic índices were significantly correlated only with the per­centage
of mud and in abaxial side were significantly correlated with percentage of
sand, mud and clay. Presence of hairs in the leaf margin was positively correlated
with CIC, WRC and the percentage of clay, and negatively correlated with the per­centage
of sand. Mesophyll cell types and the amount of idyoblasts on the leaves
were not significantly correlated with any of the edaphic traits considered.
On the whole, the variability of some morphological and anatómica! structures in
genus Androcymbium was only associated with water disponibility (i.e., with the
edaphic characteristics related to the percentage of clay and WRC). Species that
grow in soils with low WRC and low percentage of clay were characterized by long
and linear or linear-lanceolate leaves, rectangular epidermic cells, smooth or with
papillaes at margin, V-shaped leaf section, and short bracts. By contrast, species
that occur in soils with high WRC and high percentage of clays were characterized
by short and ovate leaves, romboidal or polygonal epidermic cells, pluricellular
hairs at the leaf margin, fíat leaf section and long bracts.
DISCUSSION
Large amounts of variability in morphological and anatomical characteristics
were described for Southwest African species of Androcymbium, reflecting the
large variation detected in other variables (palynoiogical, flower morphology.
CORRELATIONS BETWEEN MORPHOLOGICAL-ANATOMICAL LEAF CHARACTERISTICS. 81
allozymes or cpDNA RFLPs). By contrast, Northern African species of
Androcymbium showed large variation in some anatomical leaf characteristics,
despite the narrow morphological similarity (MATEU-ANDRÉS et al., 1996).
Some morphological leaf characters of Southwestern African Androcymbium
species seem to evolve associated only with the climatic and edaphic factors re-lated
to hydric disponibility (amounts and distribution of annual rainfall, and soil
texture). The two veld types where the studied populations occur are characterized
by different winter rainfall regimes. The Cape Región (dominated by a Fynbos
vegetation) receives more than 250 mm/year (80 % in winter), while the Karoo área
receives less than 300 mm/year (60 % in winter). Androcymbium austrocapense,
A. eghimocymbion, and A. capense occur in the Cape Región and showed bigger
leaf sizes than the rest of species that inhabit in Karoo-Karoid Regions (mean leaf
length valúes are in Table 2). We detected a significant association between leaf
length and veld types. Therefore, a possible explanation for,the bigger leaf size in
Androcymbium species from the Cape Región could be the higher winter rainfall in
this área. The observation that Southeastern African species of Androcymbium
(mainly A. burl<ei, A. decipiens, A. leistneri, A. longipes, and A. natalense) live in a
regime of much higher winter rainfall and show a leaf size similar to species of the
Fynbos Región agrees with our hypothesis.
Although we can rule out a direct relationship between leaf length and winter
rainfall regime in Androcymbium, other leaf characteristics lend themselves to ge-neralization
and fit better theoretical predictions. Species of Androcymbium with a
big leaf surface (ovato-lanceolate shape) inhabit in soils with a high percentage of
cíay, while species with little leaf surface (linear or linear-lanceolate shapes) inhabit
in soils with low percentage of clay. Thus, there seems to be an association bet­ween
leaf surface and soil's texture.
Morphological and anatomical characteristics
Leaf length
Leaf shape (length/width)
Bract length
Bract shape (length/width)
Leaf section
Indument at leaf margin
Epidermic cell shapes
Stomatic Índex at adaxial face
Central cell sizes
Mesophyli cell types
Frequency of leaf idioblasts
t
3.87"
0.38
-0.54
-0.57
2.33*
0.16
-0.10
1.51
2.66*
1.19
-1.33
P
0.001
0.707
0.591
0.574
0.027
0.877
0.918
0.142
0.013
0.242
0.193
Table 4.- Results of Student's t tests to contrast morphological and anatomical characteristics in species
of Androcymbium from the Fynbos and the Karoo-Karoid vegetation types. **, significant at the 0.01
leve!. *, significant at the 0.05 level.
82 N. MEMBRIVES, J. PEDROLA-MONFORT & J. CAUJAPE-CASTELLS
By contrast, bract shape is not significantly correlated with soil texture, and this
might indícate that the characteristics of the bracts could be more influenced by
other factors, probably relatad to pollination effectiveness. There is a cióse relation
between levéis of allozymic diversity and pollination effectiveness in self-incom-patible
species of Androcymbium (MEMBRIVES, 2000; MEMBRIVES eí al., in prep.)-
Previous studies suggested that bract colour and other characteristics related to
the reproductiva system (like néctar production and odour) were important to
estímate the allozymic diversity in Southwest African species of Androcymbium.
For instance, A. burchellii subsp. burchellii (with white bracts) has less allozymic
diversity than A. burchellii subsp. pulchrum (with red bracts), even though they
have the same reproduction system. This could be an important insight to consider
that bract characteristics are more conditioned to pollination effectivity than to
environmental conditions.
V-shaped leaves, glaucous colour, and indument in leaf surface and margin are
argued to represent an adaptive strategy to reduce the transpiration in Mediterra-nean
plants. In cióse agreement, the V-shape of Southwestern African Androcym­bium
leaves was correlated with low WRC. Similarly, semi-flat shapes and leaf
surfaces covered by waxes (glaucous leaf colour) in Androcymbium species from
Namaqualand (Northern Karoo) could also represent an adaptation to the aridity in
this área. Présenes of pluricellular hairs in Androcymbium is associated with soils
that exhibit a high percentage of clay and a high CIC, except for A. cuspidatum
(that Uves in high percentage of clay but shows a smooth margin). The presence of
an indument in the leaf margin dees not seem to be an adaptation to aridity ¡n An­drocymbium,
because species with pluricellular hairs occur in clayey soils, which
exhibit high WRC.
According to these observations, hydric disponibility is associated to some mor-phological
and anatomical characteristics in Androcymbium. Recent allozymic di­versity
studies (MEMBRIVES ef al., in prep.) in these populations found that there is
a significant correlation between the aridity gradation described in this región and
the allozymic diversity levéis. According to these analyses, the reproductivo system
is the variable that most influences allozymic variability in Androcymbium. When
only self-compatible populations were considered, the genetic diversity levéis in
populations distributed in the Northern región of Southwestern África (where aridity
is more severe) are lower than in Southern species. As the different levéis of hydric
disponibility in the diverse habitats of Southwestern África seem to influence the
allozymic diversity levéis, this edaphic trait could determine inter-specific diffe-rences
in terms of evolutionary potential.
Southern African species of Androcymbium show a considerable heterogeneity
in mesophyll cell types, which was also shown for their Northern African congeners
(MATEU-ANDRÉS ef al., 1996). Given the strikingly contrasting climatic and edaphic
characteristics between the arid regions in Northern and Southern África where the
species of Androcymbium inhabit, the mesophyll types do not seem either an
adaptative response to environmental differences or a characteristic of Andro-cymbium's
lineage.
WRC
Sand
Mud'
Clay
M
ID
Margin
L(l)
LÍAO)
L(b)
L/A(b)
Color
ECS
STAd
STAb
Sectlon
CIC
0.710*"
-0.657"
NS
0.770"*
NS
NS
0.621"
NS
NS
0.425*
NS
NS
0.495*
NS
NS
NS
Edaphic parameters
WRC
-0.801**'
NS
0.893***
NS
NS
0.698*"
NS
NS
0.663"
NS
NS
0.476*
NS
NS
-0.525*
sand
t
-0.745*"
-0.922**'
NS
NS
-0.713*"
0.460*
0.436*
-0.659"
NS
NS
NS
NS
0.449*
0.695*"
mud
' 0.428*
NS
NS
' NS
NS
NS
0.504*
NS
NS
NS
-0.465*
-0.456*
-0.547"
clay
NS
NS
0.769*"
-0.424*
-0.455*
0.599"
NS
NS
0.447*
NS
0.584*
-0.623**
M
NS
0.495*
NS
NS
NS
NS
-0.449*
0.753**'
NS
NS
NS
ID
NS
0.425*
-0.530*
NS
-0.506*
NS
' NS
NS
NS
NS
Anatómica! and morphologlcal characteristlcs
Margin L (1)
NS
NS NS
0.576" NS
NS NS
NS NS
0.677** NS
NS NS
NS NS
-0.539* 0.543*'
L/A(l) L(b)
NS
0.594" NS
0.427* NS
-0.441* NS
NS NS
NS NS
' 0.544** NS
L/A(b) Color ECS
NS
NS NS
NS -0.567" NS
NS -0.658" NS
NS NS NS
STAd STAb
0.796*"
NS NS
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m
m
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7¡
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7>3
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V)
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Table 5. Pearson's conrelations for morphologlcal, anatomical, and edaphic characteristlcs. CIC=Cat¡onlc Interchange capacity. WRC= Water retention
capacity. M=Mesophyll types. ID=ldyoblasts. Margin= Presence/absence of pluricellular hairs. L (I) and L/A (!)= length and shape of flrst leaf. L (b) and L/A
(b)= length and shape of flrst bract ECS: Epldermic cells shape at adaxlal face. STAd and STAb=Stomatlc Indexs at adaxiai and abaxlal side. NS=not
slgniflcant. *, slgnification level at 0.05; **, significatlon level at 0.01; ***, slgnlficatlon level at 0.001.
00
84 N. MEMBRIVES, J. PEDROLA-MONFORTS J.CAUJAPE-CASTELLS
CONCLUSIÓN
Because only the characteristics associated with aridity showed a clear rela-tionship
to leaf variability in Androcymbium, our results agree only partially with the
suggestion that the edaphic heterogeneity described in Southwest África is the
main cause to explain the high specific diversity in this región (AXELROD & RAVEN,
1978). Some other morphological and anatomical characteristics are correlated
with veld type or water disponibility. The four populations studied that occur in the
Fynbos showed longer leaves with a V-shaped section, except for A. capense,
which showed a fíat leaf section. Conversely, species that inhabit the Karoo-Karoid
types, showed shorter ieaves, mainly fíat or semi-flat in section, except for A. be-llum,
A. dregei and A. eghimocymbion, with a V-shaped section. Some morpho­logical
and anatomical structures were correlated with soil texture in Androcym­bium.
Species with short ovate leaves, polygonal or rounded epidermic cells, plu-ricellular
hairs at the leaf margin, fíat section, and long bracts occur in soils with
high WRC. On the other side, species with long and linear or linear-lanceolate
leaves, rectangular epidermic cells, smooth or papillae margin, V-shaped section,
and short bracts inhabit soils with low WRC. The hydric gradient correlates to
allozymic variability levéis in Androcymbium in much the same way as it influences
some morphological and anatomical characteristics. Species that occur in the
Northern región of Southwestern África showed lower morphological and genetic
variability valúes than species distributed in the Southern región and this could be
associated with different evolutionary potentials.
ACKNOWLEDGEMENTS
We thank Juanjo Herrero-Borgoñón for the assistance with the analytic methods
and with the interpretation of the edaphic analyses. Josep Maria Montserrat gave
meaningful suggestions on a previous draft of the manuscript. Amparo Ardanuy
provided for the welfare of the material in cultivation. We thank the Karl Faust
Foundation for the economic support of these investigations.
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