Morphologicai seed studies of southwest african Androcymbium (Colchicaceae)

              Bot. Macaronésica 24: 87-106 (2003) 87
MORPHOLOGICAL SEED STUDIES OF SOUTHWEST AFRICAN
ANDROCYMBIUM (COLCHICACEAE)
NURIA MEMBRIVES\ JOAN PEDROLA -MONFORT^ & JULI CAUJAPÉ-CASTELLS^
' Estado Internacional de Biología Mediterránia-Jardi Botánic Marimurtra. Passeig Karl Faust, 10.
17300 - Blanes. Girona. Apdo. Correos 112. España (nuriamem@jazzfree.com; jpedrola@grn.es).
^ Jardín Botánico Canario «Viera y Clavijo». Apdo. 14 de Tarifa Alta. 35017 Las Palmas de Gran Cana­ria,
islas Canarias. España (julicaujape@granca.step.es).
Recibido: Agosto 2000.
Paiabras clave: Androcymbium, Colchicaceae, morfología seminal, filogenia, África.
Key words: Androcymbium, Colchicaceae, seed morphology, phylogeny, África.
SUMIVIARY
Macromorphological and micromorphological seed characteristics are described in 32 populations
belonging to 19 taxa of the genus Androcymbium distributed in Southwest África. The heterogeneity
shown in the seed characteristics in Southwest African species is compared with the uniformity des­cribed
previously in the Northern African congeners. The principal seed characteristics are evaluated in
the taxonomic classification of the genus, and their evolution is considered under a recent cladistic
analysis from morphological data. According to this phylogeny, all seed characters studied show com-plex
patterns of parallelisms and reversáis in the evolution of the genus.
RESUMEN
Se describen las características macromorfológicas y micromorfológicas de las semillas de 32 po­blaciones
pertenecientes a 19 taxones del género Androcymbium distribuidas en Sudáfrica Occidental.
La heterogeneidad observada en las características seminales en las especies sudafricanas se com­para
con la uniformidad descrita previamente en los congéneres norteafricanos. Las principales carac­terísticas
seminales se evalúan en la clasificación taxonómica del género y la evolución de estos ca­racteres
se analiza en un reciente análisis dadista a partir de datos morfológicos. Según esta filogenia,
todos los caracteres seminales estudiados presentan complejos patrones de paralelismos y reversiones
en la evolución del género.
ISSN 0211-7150
88 NURIA MEMBRIVES, JOAN PEDROLA -MONFORT & JULI CAUJAPÉ-CASTELLS
INTRODUCTION
The genus Androcymbium Willd. (Colchicaceae) is represented by about 50
species (ARNOLD & WET, 1993; MÜLLER-DOBLIES & MÜLLER-DOBLIES, 1998;
PEDROLA-MONFORT et al., 1999a, 1999b, 2000) with a disjunct distribution in África
(Fig. 1A). The genus has been historically divided into three sections: Androcym­bium,
Erythrostictus, and Dregeocymbium (KRAUSE, 1920). Most of the species
belong to section Androcymbium and are distributed in South África, either in the
western (about 40 species) and in the eastern (seven species) región. Only two
species are ascribed to section Dregeocymbium {A. dregei and A. exiguum). These
distribute in Southwest África and Namibia. Seven species belong to section Ery­throstictus
and occur mainly in Northern África (four in the IVlediterranean basin
and two in the Canary Islands), and only one of them {A. roseum), occurs in
Southern África. MÜLLER-DOBLIES & MÜLLER-DOBLIES (1998) published a new su-praspecific
classification of section Androcymbium where they propose its segre-gation
into two subsections with eight series and four subseries. Recently,
MEMBRIVES (2000) proposes a new generic classification under phylogenetic tenets
based on the cladistic analysis of morphological and reproductive traits.
Given that seed morphology has been shown to be a conservative character in
many plant species (DAVIS & HEYWOOD, 1963), it is generally inferred that it bears
taxonomic valué (STEBBINS, 1974; STUESSY, 1990). Within the Colchicaceae, varia-bility
in seed size, colour, carúncula presence and in the microstructure of the ex-ternal
layer has been reported in some genera (BUXBAUM, 1936; NORDERSTAM,
1982; PEDROLA-MONFORT, 1993). In Ornitlioglossum, the microstructure of the ex-ternal
layer is of proven taxonomic usefulness (NORDERSTAM, 1982). Previous sur-veys
in the genus Androcymbium allowed species differentiation based on seed
size alone (GREUTER, 1967; ROESSLER, 1974; SANTOS, 1977; REIFERBERGER, 1990;
PEDROLA-MONFORT, 1993). Within section Erythrostictus, the shape of the cells of
the infernal layer showed inter-specific variability, with the Northern African A. wys-sianum
and the Southern African A. roseum displaying rectangular cells, and the
rest of species showing quadrangular cells (PEDROLA-MONFORT, 1993).
Our objectives are, first, to describe seed morphology and biometry in a broad
.representation o\ Androcymbium species distributed in Southwest África (Fig. IB)
in order to assess their valué for taxonomic classification within the genus. And
second, to assess the evolution of these traits in the frame of a recent cladistic
analysis based on morphological data.
MATERIALS AND METHODS
We sampled 32 populations representing 19 taxa of genus Androcymbium dis­tributed
in Southwest África (Appendix 1; Fig. IB), and the six species from
Northern África already studied by PEDROLA-MONFORT (1993). Seeds were ob-tained
from plants grown in culture except from those belonging to A. cruciatum
and A. volutare which correspond to herbarium specimens (U. Müll-Doblies & D.
Müll.-Doblies 80099n -Botanischer Garten und Botanisches Museum Berlín-
MORPHOLOGICAL SEED STUDIES OF SOUTHWEST AFRICAN ANDROCYMBIUM 89
Dahiem- for A. cruciatum, and P. Goldblatt 6238 -Royal Botanic Carden, Kew- for
A. volutare).
Figure 1.- A. Geographic distribution of genus Androcymbium. The numbers show the distribution of
Northern African species (1: A. hiérrense; 2: A. psammophilum; 3: A. gramineum; 4: A. wyssianum; 5:
A. rechingerii; 6: A. palaestinum). B. 'Geographic distribution of the Southwest African populations
studied. The abbreviations of the Southwest African populations are described in Appendix 1.
90 NURIA MEMBRIVES, JOAN PEDROLA -MONFORT & JULI CAUJAPÉ-CASTELLS
Macromorphological traits.- Following previous studies within the Colchicaceae
(NORDERSTAM, 1982; PEDROLA-MONFORT, 1993), we studied seed shape, diameter,
colour, and carúncula presence/absence. Morphological observations and biome-trical
measurements were carried out in a binocular lens. Seed diameter was ob-tained
by pooling 50 measurements of each of five individuáis per population.
Micromorphological traits.- The seeds of the species of genus Androcymbium
show two different layers that wrap the endosperm and form the testa (PEDROLA-MONFORT,
1993). Accordingly, the micromorphological descriptions of the seeds
considered both the external and the infernal layers. To observe the infernal layer,
the seeds were boiled during 10-15' and then the external cell layer was removed
using a nail. Then, seeds were subjected to ultrasonic waves to remove cellular
remains of the external layer. The studied traits were the shape of the cells in both
layers. Observations were carried out using the Scanning Electron Microscope
(SEM) at the University of Valencia (Spain).
RESULTS
The irregularities due to the pressure within the capsula notwithstanding, the
seeds of genus Androcymbium are always globoso (Figs. 4-8) except in A. cuspi-datum
(Fig. 7C), where they show a slightly eiliptical shape. Seed diameter was
mostly around 1.5 mm (Table 1, Fig. 2) and varied between 0.7 mm in A. dregei
and 3.5 mm in A. burchellii subsp. pulchrum. The seed colour varied among light
brown, brown, brown-reddish and black (Table 1).
Diameter (mm)
Figure 2- Seed diameter in Androcymbium. The boxes show the median, the quartiles and the
extreme valúes. In all cases, the ñames of species are coded with the first four letters.
MORPHOLOGICAL SEED STUDIES OF SOUTHWEST AFRICAN ANDROCYMBIUM 91
Population Seed color Seed diameter CAR EXT INT
Section Androcymbium
ALBA-PK
AUST-GH
AUST-WP
BELL-VI
BURC-HX
CAPE-HO
CIRC-SB
CUSP-CA
CUSP-MO
EGHI-CI
EGHI-PK
HANT-CA
HENS-EK
HUNT-EK3
IRRO-EK
IRR0-EK2
IRR0-EK6
IRRO-KA
IRRO-KW
IRRO-VP
IRRO-VY
POEL-GO
POEL-NB
POEL-ST
PULC-GA
PULC-NI
VILL-EK
VILL-ST
VOLU-ST
WALT-ST
CRUC-CA
DREG-PK
Brown-reddish
Brown-reddish
Brown-reddish
Black
Brown
Brown
Black
Brown
Brown
Brown
Brown
Brown-reddish
Brown-reddish
Black
Black
Black
Black
Black
Black
Brown-reddish
Black
Black
Black
Black
Brown
Brown
Black
Black
?
Black
?
Light brown
(1.20
(1.50
(1.30
(1.00
(1.80
(1.35
(1.70
(1.50
(1.20
(1.30
(1.20
(1.90
(1.30
(1.30
(1.20
(1.50
(1.50
(1.20
(1.10
(1.30
(1.20
(1.00
(1.20
(1.20
(1.90
(2.20
(1.40
(1.60
)1.52
)1.92
)1.79
)1.07
)2.07
)1.49
)1.84
)1.62
)1.45
)1.51
)1.41
)2.14
)1.52
) 1.44
)1.43
)1.74
)1.69
)1.49
)1.33
)1.49
)1.39
)1.25
)1.42
)1.26
)2.30
)2.76
)1.58
)1.83
(1.80)
(2.50)
(2.40)
(1.20)
(2.60)
(1.50)
(1.90)
(1.90)
(1.70)
(1.70)
(1.60)
(2.40)
(1.65)
(1.60)
(1.60)
(1.90)
(1.90)
(1.80)
(1.60)
(1.70)
(1.60)
(1.50)
(1.60)
(1.40)
(2.80)
(3.50)
(1.80)
(2.00)
P
A
A
A
A
P
P
A
A
A
A
P
P
A
P
P
P
P
P
P
P
A
A
A
A
A
P
P
A
A
(1.00)1.35(1.70)
Section Erythrostictus
? A
Section Dregeocymbium
(0.70)0.94(1.20) A
Retícula
Mosaic
Mosaic
Mosaic
Rough
Retícula
Mosaic
Retícula'
Retícula'
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Mosaic
Rough
Rough
Mosaic
Mosaic
Mosaic
Mosaic
Rough
Reticulate (I)
:e(ll)
IV)
IV)
III)
;e(ll)
III)
:e(l)
:e(l)
IV)
IV)
II)
I)
III)
III)
Quadrangular
Rectangular
Rectangular
Indifferenced
Quadrangular
Quadrangular
Rectangular
Quadrangular
Quadrangular
Rectangular
Rectangular
Quadrangular
Quadrangular
Indifferenced
Variable
Variable
Variable
Variable
Variable
Variable
Variable
Rectangular
Rectangular
Rectangular
Quadrangular
Quadrangular
Rectangular
Rectangular
Quadrangular
Quadrangular
Quadrangular
Quadrangular
Tablel.- Macromorphological seed characteristics of genus Androcymbium. CAR: carúncula
(P=present; A=absent). Seeds are measured in mm. EXT: Microstructure of the external layer; INT: Gell
morphology of the interna! layer. The abbreviations of the populations are described in Appendix 1.
92 NURIA MEMBRIVES, JOAN PEDROLA -MONFORT & JULI CAUJAPÉ-CASTELLS
In species A. albanense subsp. clanwHIiamense, A. capense, A. circinatum, A.
hantamense, A. henssenianum, A. irroratum, and A. villosum, the raphe develops
in a carúncula (Table 1; Figs. 4A,E; 5C; 6A,C; 7E,G), a phenomenon that has also
been reported in other genera of the Liliales like Erythronium, Gagea, Uvularia,
Colchicum, Hermodactylus, and Patersonia (DAHLGREN, 1985). The width of this
caruncula-like raphe is never higherthan 1 mm.
The external layer is rough in A. austrocapense, A. bellum, A. burchellii subsp.
burcheijii, A. burchellii subsp. pulchrum, A. circinatum, A. cruciatum, A. dregei, A.
eghimocymbion, A. gramineum, and A. villosum (Figs. 5G; 6; 7A; 8) and smooth in
the rest of species studied. Cell shape and disposition as analyzed in the SEM
revealed three distinct patterns of microstructure in the external layer (Table 1):
a) Type mosaic. It features cells with walls within the cell surface. It is observed
in most species studied and four subtypes can be distinguished. Mosaic I is cha-racterized
by a smooth pavement with regular, polygonal cells with 5-6 faces of
different size that have sharp edges and a thin cell wall (Figures 4; 5B). It was
observed in A. henssenianum, A. huntleyi, A. irroratum (populations IRRO-KA,
IRRO-KW, IRRO-VP and IRRO-VY), A. poeltianum, and A. walteri. Mosaic II is
characterized by a smooth pavement with regular cells, blunt edges and a thick cell
wall (Fig. 5D,F). It was observed in A. iiantamense, A. volutare, and A. irroratum
(populations IRRO- EK2 and IRR0-EK6). Mosaic III is characterized by an irregular
rough pavement with differently sized polygonal cells with 5-6 faces arranged in
different levéis, sharp edge and a thin cell wall (Figs. 5H; 6B,D). It was observed in
A. bellum, A. circinatum, A. irroratum (population IRRO-EK), and A. villosum.
Mosaic IV is characterized by a smooth pavement with irregular cells with rounded
or ellipticai edges and undifferentiated cell walls (Fig. 9F,H). It was observed in A.
austrocapense and A. eghimocymbion.
b) Type reticulate. It features an external layer micromorphology with walls
overtaking the cell surface. Two subtypes were observed among the studied spe­cies.
Reticulate I is characterized by irregular polygonal cells (Fig. 4B,D) and was
observed in A. cuspidatum and A. dregei. Reticulate II corresponds to a su-prareticulate
structure with a thin reticle on top of the thick reticle unerneath (Fig.
7F,H) and was observed in A. albanense subsp. clanwHIiamense, and A. capense.
c) Type rough. It features irregular pavement without clear cell edges (Fig. 8)
and was described in A. burchellii subsp. burchellii, A. burchellii subsp. pulchrum,
A. cruciatum, and in all the Northern African species of the genus.
The surface of the internal layer showed a rough surface in A. bellum and A.
huntleyi, where the cell edges cannot be precisely delimited (Fig. 9A, table 1). In
contrast, the rest of species showed a smooth or almost smooth wall (Fig. 9B,C,D),
where the edges of the cells in the internal layer are well delimited and group the
species in three general types: 1) quadrangular cells in A. albanense subsp.
ClanwHIiamense, A. burchellii subsp. burchellii, A. burchellii subsp. pulchrum, A.
capense, A. cruciatum, A. cuspidatum, A. dregei, A. gramineum, A. hantamense,
A. henssenianum, A. rechingerii, A. volutare and A. walteri (Fig. 9B); 2) rectangular
cells in A. eghimocymbion, A. austrocapense, A. circinatum, A. poeltianum, A.
villosum, and A. wyssianum (Figs. 9C); and 3) irregular cells (generally quadran­gular
tending to rectangular) in A. hiérrense, A. irroratum, A. palaestinum, and A.
psammophilum (Fig. 9D).
MORPHOLOGICAL SEED STUDIES OF SOUTHWEST AFRICAN ANDROCYMBIUM 93
DISCUSSION
Seed morphology in the species of Androcymbium shows a remarkable inter-specific
heterogeneity, while it behaves quite uniformly at the intra-specific level
except for the seven studied populations of A. irroratum. On the one hand, popula-tion
IRRO-EK shows a rough extemal layer, whereas the rest show a smooth ex-ternal
layer. On the other hand, seeds of population IRRO-VP are brown-reddish,
and the rest of conspecific populations are black (Table 1).
Seed size in the South African taxa (Table 1) is similar to that of the North Afri-can
congeners (Table 2) and, of which A. palaestinum and A. rechingerii show the
smallest seeds (averaging 1.6 mm), and A. hiérrense shows the biggest seeds,
with an average of 2.3 mm (ARDANUY, 1997). Remarkably, seed size in genus An­drocymbium
is small as compared with other genera of the Colchicaceae like Col-chicum,
Merendera, Bulbocodium, Ornitlioglossum, and Gloriosa (NORDERSTAM,
1982; GiBERT, unpubl.).
laxa
A. gramineum
A. hiérrense
A. palaestinum
A. psammoptiiium
A. rectiingerii
A. wyssianum
Seed diameter
1.75 ±0.20
2.26 ± 0.29
1.60 + 0.12
1.75 ±0.23
1.60±0.15
1.93 ±0.26
CAR
A
A
A
A
A
A
EXT
Rugóse
Rugóse
Rugosa
Rugóse
Rugóse
Rugóse
INT
Quadrangular
Irregular
Irregular
Irregular
Quadrangular
Rectangular
Table 2.- Macromorphological seed characteristics of Northern African species of genus
Androcymbium (from PEDROLA-MONFORT, 1993). CAR: carúncula (P=present; A=absent). EXT:
Microstructure of the external layer; INT: Cell morphology of the infernal layer. The diameter of the
seeds are measured in mm.
The carúncula might act as a nourishing reward and, therefore, it could be re-lated
to seed dispersal mechanisms. All South African species studied show dehis-cent
capsule. Henee, seed dispersal can be carried out individually, indicating that
dispersal agents could be influencing the distribution of individuáis in populational
space. In contrast, some of the species distributed in North África feature a dehis-cent
capsule and, consequently, the dispersal unit is the whole stock of seeds per
individual. A study in a stand of A. gramineum revealed that this is a paramount
factor in determining the spatial distribution of individuáis in neighbourhoods of
genetically related individuáis (CAUJAPÉ-CASTELLS & PEDROLA-MONFORT, 1997).
A cióse relationship between A. wyssianum (distributed in Northern África) and
A. roseum (distributed in Southern África) was inferred by PEDROLA-MONFORT
(1993) from the observation of rectangular cells in the infernal layer of the seeds in
both species. This fact led to the consideration that A. wyssianum and A. roseum
might be the same species or were closely related. This also indicated that A.
roseum, distributed in South África, could be of paramount importance to under-
94 NURIA MEMBRIVES, JOAN PEDROLA -MONFORT & JULI CAUJAPÉ-CASTELLS
stand the dispersal path of the genus into North África. Recent studies allowed us
to observe additional seed material and indicate that the cells in the interna! layer
of A. hiérrense, A. palaestinum, and A. psammophilum (which were defined as
quadrangular in PEDROLA-IVIONFORT, 1993) show variable morphologies (Tabla 2).
A recent phylogeny based on cpDNA RFLPs (CAUJAPÉ-CASTELLS eí al., 1999)
groups A. gramineum, A. palaestinum, and A. rechingerii, and the species A. hié­rrense,
A. psammophilum, and A. wyssianum in diferent clades. This topology is
well supported and hints at the possibility that the present distribution of the North
African species might be accounted for by the existence of two different dispersal
Unes starting in South África (CAUJAPÉ-CASTELLS eí al., in mss.). The shape of the
cells in the infernal layer might support this hypothesis under the consideration that
the species that exhibit rectangular cells (A. roseum and A. wyssianum, and with
variability A. hiérrense, A. psammophilum, and A. palaestinum) could be more
primitiva than A. gramineum and A. rechingerii, whose cells tend to be quadrangu­lar.
The morphological variability observed in the cells of the infernal layer of South
African species makes it difficult to substantiate this hypothesis.
Taxonomic implications
None of the seed characters allows to support the classification of the genus in
three sections {Androcymbium, Dregeocymbium and Erythrostictus). All of the seed
characters examinad (size, shape, colour, presence/absance of carúncula, typa of
externa! and interna! layer) show variability in the 17 taxa of section Androcymbium
included in this study. Therefore, seed characters cannot be used as an indicator
of sectional taxonomic category in the genus Androcymbium.
The only representative studied of section Dregeocymbium {A. dregei) shows
two seed traits that differantiate it from the rest of species: a small seed size (al-most
always < 1 mm) and the brown light colour of the external cover. This species
had been included in section Erythrostictus by previous authors (MÜLLER-DOBLIES
& MÜLLER-DOBLIES, 1990). The seed traits exclusive of A. dregei in the genus ara
not shared by the rest of species within section Erythrostictus (PEDROLA-MONFORT,
1993; ARDANUY, 1997), which have biggar and darker seeds. From the studied
species, only A. bellum and some individuáis of popuiations IRRO-KW and POEL-CO,
present a seed diameter that overlaps only partially with the range observad in
A. dregei. However, their seeds are black.
Androcymbium cruciatum has been included historicaily within section Erythros­tictus
(Appendix 1). This species shares the absence of carúncula with the North
African species (belonging to this section), and differst from them in the external
layer type. MEMBRIVES (2000) argües for the inclusión of A. cruciatum in a new
monotypic section based on morphological traits.
The species A. bellum was segregata from section Erythrostictus and include it
in section Androcymbium by MÜLLER-DOBLIES & MÜLLER-DOBLIES (1998). This spe­cies
shares with other species in section Erythrostictus the absence of carúncula
and the roughnass of the testa's external layer. However, the seeds of A. bellum
show a smaller size and a rougher infernal layer than the othars (PEDROLA-MONFORT,
1993). According to seed traits, A. bellum is most similar to A. huntleyi
(that belongs to section Androcymbium) than the other species of section Erythros-
MORPHOLOGICAL SEED STUDIES OF SOUTHWEST AFRICAN ANDROCYMBIUM 95
tictus. Both of them share seed colour and diameter, the absence of carúncula,
mosaic external layer and rough internal layer, and they only differ in the size and
shape of the cells in the external layer.
Only 15 of the 34 taxa classified within section Androcymbium (Appendix 2) by
MüLLER DoBLiES & MüLLER DOBLiES (1998) wsre jncluded in our study. The two
subsections of these authors are not supported by any of the studied characters.
Subsection Gradatocymbium includes the species A. albanense, A. poeltianum, A.
henssenianum, and A. cuspidatum, that differ in most of the studied tralts (seed
shape, colour, caruncula's presence, type of external layer and shape of the cells
of the internal layer). Neither does subsection Androcymbium share any of the
studied seed traits. For instance, A. irroratum and A. eghimocymbium (series
Eghimocymbia) differ in seed colour, presence/absence of carúncula, type of mo­saic
and the shape of the internal layer cells (Table 1).
A cladistic analysis of genus Androcymbium based on morphological and re-productive
data (MEMBRIVES, 2000) concludes that none of the seed traits analysed
is monophyletic (Fig. 3) and shows that carúncula presence appeared three times
in the evolution of the genus. First in A. henssenianum, then in A. hantamense and
A. capense, and finally in A. irroratum, A. albanense subsp. cianwilliamense, A.
vilíosum, and A. circinatum. Furthermore, this character would have undergone a
reversal in A. volutare, A. walterí, A. bellum, and A. poeltianum. When the evolution
of the microstructural patterns of the external layer is analysed, the result is that
none of the four types behaves as a monophyletic trait either. Rough forms appear
at the base of the morphological phylogenetic tree as primitive external layer
microstructures, and then again in the terminal clade formed by A. burchellii subsp.
burchellii and A. burchellii subsp. pulchrum. Reticulate types appear three times in
that phylogeny: in the clade made up by A. dregei and A exiguum, in A.
cuspidatum and in A. crispum. Suprareticulate types appear independently in
species from two distinct clades {A. capense and A. albanense subsp.
cianwilliamense). Mosaic types appear three times also: in A. henssenianum and
A. huntleyi, in A. melanthioides and A. hantamense, and in the clade that groups A.
eghimocymbion, A. austrocapense, A. irroratum, A. vilíosum, A. circinatum, A. vo­lutare,
A. walterí, A. bellum, and A. poeltianum.
Given that none of the seed traits analysed in the genus Androcymbium are
good indicators of phylogenetic relatedness (MEMBRIVES, 2000), they have no
usefulness as taxonomic descriptors of supra-specific classification under a phy­logenetic
perspective. Therefore, we can conclude that the seed characters con-sidered
do not indícate either phylogenetic taxonomic assemblages, or morpho­logical
groupings like the historical classification in three sections (KRAUSE, 1920),
or the MüLLER-DoBLiES & MÜLLER-DOBLIES (1998) proposal.
96 NURIA MEMBRIVES, JOAN PEDROLA -MONFORT & JULI CAUJAPÉ-CASTELLS
Outgroup
gromineum
crudafum
dregei
exiguum
henssenianum \ ^Cj
huntleyi
longipes
hughocymbion
cuspidafum
críspum
burchellii subsp. burchellH
burchellil subsp. pulchrum
melanthioides
hanfomense
capense
eghimocymbhn
ausfrocapense
irroratum
]-^Q
albanense
villosum
circinafum
volufare
walferi
bellum
poelfianum
V Q
Figure 3.- Phylogenetic tree of genus Androcymbium from morphologic and reproductive data
(MEMBRIVES, 2000). The species with seminal data unknown have been excluded. The evolution of
the extemal layar seed microstructure (squares at the end of the branches) and the
presence/absence of carúncula (where the presence of carúncula is representad by a pictura of the
seed with a developed raphe) is representad in the trea. Types of microstructure: R=rough;
Re=reticulate; S=suprareticulata; M=mosaic; ?=unknown data.
MORPHOLOGICAL SEED STUDIES OF SOUTHWEST AFRICAN ANDROCYMBIUM 97
ACKNOWLEDGEMENTS
We thank Isabel Mateu-Andrés for the facilities given to undertake this study
and for her suggestions in the classification of cell patterns. Amparo Ardanuy pro-vided
for the welfare of the material in cultivation. The Karl Faust Foundation gave
financial support for both the expedition to South África that allowed us to collect
the analysed samples and the subsequent investigations in conservation genetics
oí Androcymbium carried out in the "Estació Internacional de Biología Mediterránia-
Jardí Botánic Marimurtra".
REFERENCES
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del genere Androcymbium Willd. Trebail fi de carrera. Universitat de Glrona.
ARNOLD, T.H. & B.C. DE WETT, 1993.- Plants of southern África: Ñames and Distribution. Memoirs ofthe
botanical survey of South África No. 62. pp. 131.
BuxBAUM, F., 1936.- Die Entwickiungslinien der Lilioideae. I. DIe Wurmbaeoideae. Bot. Archiv 38: 213-
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CAUJAPE-CASTELLS, J . & J. PEDROLA-MONFORT, 1997.- Space-time patterns of genetic structure within a
stand of Androcymbium gramineum (Cav.) McBride (Colchicaceae) l-leredity 79: 341-349.
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Phylogeny of the Genus Androcymbium (Colchicaceae) Syst. Bot. 24(4): 581-597.
DAHLGREN, R., H.T. CLIFFORD & P.F. YEO, 1985.- Tfie families ofthe Monocotyiedons: Structure, Evolu-tion,
and Taxonomy. Springer-Verlag. Berlin.
DAVIS, P.H. & V.H. HEYWOOD, 1963.- Principies ofAngiosperm Taxonomy. Ed. Olivier. Edinburg.
GREUTER, W., 1967.- Contributiones floristicae Austro-Aegeae. Candoiiea 22(2): 233-253.
KRAUSE, K., 1920.- Revisión der Gattung Androcymbium Willd. Notizbl. Bot. Gart. Berlin 7: 512-526.
MEMBRIVES, N., 2000.- Biología evolutiva del genere Androcymbium (Colchicaceae) a Sudáfrica Occi­dental.
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MÜLLER-DOBLIES, U. & D. MüLLER-DoBLiES, 1990.- Zur Kenntnis der Gattung Androcymbium (Colchica­ceae)
mi südlichen Afrika: 2. Androcymbium exiguurn hal doch Artv\íert. Wiildenowia 19:453-470.
- & D. MüLLER-DoBLiES, 1998.- De Liliifloris Notulae. 6. De decuria prima specierum novarum generis
Androcymbium sect. Androcymbium (Colchicaceae) in África Australi s.l. Praeterea novitates de
huius sectionis nonnullarum specierum --distributione (praesertim aucta speciminibus
STEIIenbosensibus i.a. collectis a botánico vero E. G. H. OLIVERO) Fedd. Reper. 109 (7-8): 551-
572.
NoRDERSTAM, B., 1982.- A monograph of the genus Ornithogiossum (Liliaceae). Opera Botánica 64: 1-
51.
PEDROLA-MONFORT, J., 1993.- Bioiogia pobiacionai dei compiexe Androcymbium gramineum (Cav.)
McBride (Coichicaceae). Tesis Doctoral. Universitat de Valencia.
- N. MEMBRIVES, J.M. MONTSERRAT & J. CAUJAPE-CASTELLS, 1999a.- A new/ species from the Western of
South África: Androcymbium huntieyi (Colchicaceae) Fontqueria 53: 1-2.
- N. MEMBRIVES & J.M. MONTSERRAT, 1999b.- Two new Androcymbia (Colchicaceae) from Western
South África. Fontqueria 54(2): 7-9.
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Macaronésica, 24: 107-126.
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MORPHOLOGICAL SEED STUDIES OF SOUTHWEST AFRICAN ANDROCYMBIUM 99
Appendix 1.- Sampled populations and localities of genus Androcymbium studied in Southwest África.
Abb: abbreviations of the population and locality.
Population Abb. Locality
Section Androcymbium
A. albanense subsp.
clanwilliamense
A. austrocapense
A. austrocapense
A. bellum
A. burchellii subsp.
burchellii
A. burchellii subsp.
pulchrum
A. burchellii subsp.
pulchrum
A. capense
A. circinatum
A. cuspidatum
A. cuspidatum
A. eghimocymbion
A. eghimocymbion
A. hantamense
A. henssenianum
A. huntleyi
A. irroratum
A. irroratum
A. irroratum
A. irroratum
A. irroratum
A. irroratum
A. irroratum
A. poeltianum
A. poeltianum
A. poeltianum
A. villosum
A. villosum
A. volutare
A. walteri
Section Erythrostictus
A. cruciatum
ALBA-PK
AUST-GH
AUST-WP
BELL-VI
. BURC-HX
PULC-CA
PULC-NI
CAPE-HO
CIRC-SB
CUSP-CA
CUSP-MO
EGHI-CI
EGHI-PK
HANT-CA
HENS-EK
HUNT-EK3
IRRO-EK
IRR0-EK2
IRR0-EK6
IRRO-KA
IRRO-KW
IRRO-VP
IRRO-VY
POEL-CO
POEL-NB
POEL-ST
VILL-EK
VILL-ST
VOLU-CA
WALT-ST
CRUC-ST
Section Dregeocymbium
A. dregei DREG-PK
3219AA (WUPPERTAL) Clanwilliam-Wuppertal Road. Km 10
3418AC (SIIVIONSTOWN) Road to the Cape of Good Hope
3418AD (SIMONSTOWN) Wheal's Point. Cape Point Reserve
2817DC (VIOOLSDRIFT) Steinkopf to Vioolsdhft Road. Km 40
3319BC (WORCESTER) Worcester to Towsrivier Road. Near
Hexrivierpass
3119DA (CALVINIA) Calvinia to Ceres Road, 7 l<m from the
deviation to Kreitzberg
3118AA (CALVINIA) Wild Flowers Reserve of Nieuwoudtville
3318AB (CAPE TOWN) Malmesbury to Hopefield Road. Km 49
2917DB (SPRINGBOK) 3 l<m W of Springbol<
3119DA (CALVINIA) Calvinia to Ceres Road, 7 l<m from the
deviation to Kreitzberg
3320CD (MONTAGU) Near Montagu-Badskioof. W side of the
gorge.
3218DB (CLANWILLIAM) N-7 Road in the Piketberg Pass to
Citrusdal
3219AA (WUPPERTAL) Clanwilliam to Wuppertal Road. Km 28
3119DA (CALVINIA) Calvinia to Ceres Road, 7 km from the
deviation to Kreitzberg
2817CC (VIOOLSDRIFT) Eksteenfontein to Modderfontein Road
2917AD (SPRINGBOK) Springbok to Port Nolloth Road, 20 km
from the first entry to Eksteenfontein
2917AD (SPRINGBOK) Springbok to Port Nolloth Road, 6 km
from the first entry to Eksteenfontein
2917AD (SPRINGBOK) Springbok to Port Nolloth Road, 15 km
from the first entry to Eksteenfontein
2817CC (VIOOLSDRIFT) Eksteenfontein to Modderfontein
Road, first turn
3018CB (KAMIESBERG) Bitterfontein to Kliprand Road.
3118BC (VANRHYNSDORP) Vredental to Koekenaap Road,
100 from the train station
3119AC (CALVINIA) Vanrhynspass
3118AD (VANRHYNSDORP) Vrendendal to Vanrhynsdorp
Road.
2917DB (SPRINGBOK) Springbok to Concordia Road.
2917DB (SPRINGBOK) Springbok to Nababeep Road.
2917DC (SPRINGBOK) Road from Steinkopf to Springbok, 5 km
2817CC (VIOOLSDRIFT) 1 km S of Eksteenfontein
2917BC (SPRINGBOK) 3 km S of Steinkopf, parallel to N7.
3119BC (CALVINIA) Perdekraal Farm
2917DC (SPRINGBOK) Road from Steinkopf to Springbok. Km 5
2917BC (SPRINGBOK) 5 km SSW of Steinkopf, parallel to N7.
3219AA (WUPPERTAL) Clanwilliam to Wuppertal Road. Km 28
100 NURIA MEMBRIVES, JOAN PEDROLA -MONFORT & JULI CAUJAPÉ-CASTELLS
Appendix 2.- Taxonomic classification for section Androcymbium proposed by MÜLLER-DOBLIES &
MÜLLER-DOBLIES(1998).
Section Androcymbium
Subsection Gradatocymbium U.Müll.-Doblies & D.Müll.-Doblies
Serie Gradatocymbia U.Müll.-Doblies & D.Müll.-Doblies
Subserie Gradatocymbia
A. longipes, A. natalense, A. decipiens
Subserie Swazicymbia U.Müll.-Doblies & D.Müll.-Doblies
A. swazicum, A. burkei
Subserie Leistnerocymbia U.Müll.-Doblies & D.Müll.-Doblies
A. leistneri, A. albanense subsp. albanense, A. poeltianum
Subserie Pachystyla U.Müll.-Doblies & D.Müll.-Doblies
A. henssenianum
Serie Trifoliata U.Müll.-Doblies & D.Müll.-Doblies
A. cuspidatum, A. kunkelianum, A. worsonense, A. hughocymbium
Subsection Aridrocymbium
Serie Eghimocymbia U.Müll.-Doblies & D.Müll.-Doblies
A. eucomoides, A. undulatum, A. albomarginatum, A. vanjaarsveldii, A. scabromar-giriatum,
A. irroratum, A. eghimocymbion
Serie Myiocymbia U.Müll.-Doblies & D.Müll.-Doblies
A. circinatum, A. villosum, A. volutare
Serie Therocymbia U.Müll.-Doblies & D.Müll.-Doblies
A. burchellü, A. ¡atifolium
Serie Meliitocymbia U.Müll.-Doblies & D.Müll.-Doblies
A. capense, A. ciliolatum, A. hantamense, A. austrocapertse, A. crispum
Serie Androcymbium
A. melanthioides, A. orienticapense, A. striatum
Serie Schiechterocymbia U.Müll.-Doblies & D.Müll.-Doblies
A. bellum
MORPHOLOGICAL SEED STUDIES OF SOUTHWEST AFRICAN ANDROCYMBIUM 101
Figure 4.- Microstructure of seed external layer in Androcymbium. Type mosaic \ AB A
henssenianum. C,D. A. huntleyi. E,F. A. irroratum (IRRO-KW). G,H. A. poeltianum. AC EG Seed'
The white Unes indícate 500 ^m. B,D,F,H. Detail of the microstructure of the external layer The white
102 NURIA MEMBRIVES, JOAN PEDROLA -MONFORT & JULI CAUJAPÉ-CASTELLS
Figure 5.- Microstructure of seed external layer in Androcymbium. Type mosaic I. A,B. A. walteri.
Type mosaic II. C,D. A. hantamense. E,F. A. volutare. Type mosaic III. G,H. A. bellum. A,C,E,G.
Seed. The white lines indícate 500 pm. B,D,F,H. Detall of the microstructure of the external layer. The
white linpíí inriinate 100 iim
MORPHOLOGICAL SEED STUDIES OF SOUTHWEST AFRICAN ANDROCYMBIUM 103
Figure 6.- Microstructure of seed external layer in Androcymbium. Type mosaic III. A,B. A. circinatum.
C,D. A. villosum. Type mosaic VI. E,F. A. austrocapense. G,H. A. eghimocymbion. A,C,E,G. Seed. The
white lines indícate 500 pm. B,D,F,H. Detall of the microstructure of the external layer. The white Unes
indícate 100 pm.
104
NURIA MEMBRIVES, JOAN PEDROLA -MONFORT & JULI CAUJAPÉ-CASTELLS
Figure 7.- Microstmctürorseed externa, layer in ^nf^'^^¡;^^;;^¡^^¡^Zwi^¡nJ^se%^
the external layer. The white linas indícate 100 tjm.
MORPHOLOGICAL SEED STUDIES OF SOUTHWEST AFRICAN ANDROCYMBIUM 105
Figure 8.- Microstructure of seed external layer in Androcymbium. Type rough. A B. A burchelhi subsp.
burchellii CD A cruciatum. E,F. A. gramineum. G,H. A. burchelln subsp. pulchrum A,C,e^. Seed.
S e white línes indícate 500 pm. B,D,F,H. Detall of the microstructure of the exterr^al layer. The white
linea indícate 100 pm.
106 NURIA MEMBRIVES, JOAN PEDROLA -MONFORT & JULI CAUJAPÉ-CASTELLS
Figure 9.- Shape of the ¡nternal layer cells. A. Rough (A. bellum). B. Quadrangular polygonal {A.
henssenianum). C. Rectangular polygonal {A. austrocapense). D. Irregular polygonal {A. irroratum).
The white lines indínate fiO um.