Systematic relationships of some species of the genus Androcymbium Willd. (Colchicaceae) in western South África

              Bot. Macaronésica 24: 107-126 (2003) 107
SYSTEMATIC RELATIONSHIPS OF SOME SPECIES OF THE GENUS
ANDROCYMBIUM WILLD. (COLCHICACEAE) IN WESTERN SOUTH
ÁFRICA
J. PEDROLA-MONFORT\ N. MEMBRIVES\ J. M. MONTSERRAT^ AND J. CAUJAPÉ-
CASTELLS^
' Estado Internacional de Biología Mediterránia - Jardí Botánic Marimurtra. Passeig Karl Faust, 10.
17300 - Blanes. Girona. Apdo. Correos 112. Spain. (jpedrola@grn.es; nuriamem@jazzfree.com)
^ Instituí Botánic de Barcelona-CSIC. Avda. Muntanyans s/n, Montjuíc. Barcelona. Spain.
(jmmontserrat@ibb.csic.es).
Jardín Botánico Canario «Viera y Clavijo». Apdo. 14 de Tarifa Alta. 35017 Las Palmas de Gran Cana­ria.
Spain. (julicaujape@grancanaria.com)
Palabras clave: Androcymbium, Colchicaceae, similaridad, filogenia, taxonomía, África.
Key words: Androcymbium, Colchicaceae, similarity, phylogeny, taxonomy, África.
SUMMARY
Recent morphological and allozymic studies are discussed in five taxa of genus Androcymbium from
the western región of the Cape province (South África) in the context of the systematic implications of
phylogenetic analysis based on cpDNA and morphologic data. Based on this synthesis, we modify the
taxonomic category of A. latifolium, that is included as a subspecies of A. burchellii. These five taxa {A.
burcliellii subsp. burctiellii, A. burctiellii subsp. pulchrum, A. egliimocymbion, A. huntleyi and A. walteri)
are described and illustrated.
RESUMEN
Recientes estudios de similaridad aloenzímática y filogenia (en base a caracteres morfología y
RFLPs del cpDNA) permiten la discusión de sus implicaciones sistemáticas en cinco especies del gé­nero
Androcymbium. Con los datos obtenidos reestructuramos la categoría taxonómica de la especie A.
latifolium incluyéndola como subespecie de A. burchellii. Estos cinco táxones (A. burchellii subsp. bur­chellii,
A. burchellii subsp. pulchrum, A. eghimocymbion, A. huntleyi y A. walteri) son descritos e ilustra­dos.
ISSN 0211-7150
108 J. PEDROLA-MONFORT, N. MEMBRIVES, J. M. MONTSERRATS J . CAUJAPE-CASTELLS
INTRODUCTION
Androcymbium Willd. (Colchicaceae) consists of about 50 species (ARNOLD &
WET, 1993; MüLLER-DoBLiES & MüLLER-DOBLiES, 1998; PEDROLA-MONFORT ef al.
1999a, 1999b) with a disjunct distribution in África (Figure 1). Most of them (about
40) occur in the western región of South África, only seven in eastern South África
and six in North África (four in the IVIediterranean basin and two in the Canary Is-lands).
WILLDENOW (1808) segregated the species of genus Melanthium L. with
tepals differenced in lannina and claw and grouped them into the genus Androcym­bium.
Species of genus Androcymbium are herbaceous plants with a tunicated corm,
that show cataphylls of papery texture at senescence. Leaves dispose alternately,
distically, tristically or spirally in the stem. The bracts are usually shorter and wider
than leaves and differ fronn these in texture and color. As a rule, the third leaf
shows an intermedíate morphology. The flowers have six tepals differentiated into
lamina and claw, each with a stamen inserted at the base of the tepal's lamina.
The nectarios are situated at the base of the filament. Some species show the
nectary in the dorsal side of the filament (opposite the lamina), while others show a
cylindrical nectary around the filament. The ovary is tricarpelar and trilocular, and
the fruit is a capsule, either indehiscent or dehiscent with a septicide aperture,
coriaceous or papery in texture. Most of species show idioblasts in the leaves,
tepals and capsules that are easily identified by densely distributed red spots.
20 10 o 10 20 30 40 50
Figure 1.- Geographic distribution of tlie genus Androcymbium.
SYSTEMATIC RELATIONSHIPS OF SOME SPECIES OF THE GENUS ANDROCYMBIUM 1 09
During the past ten years, detailed morphological and allozymic studies in 61
populations that represent 24 species of Androcymbium have been carried out by
our group (PEDROLA-MONFORT & CAUJAPÉ-CASTELLS 1994, 1995, 1996, 1998;
MEMBRIVES, 2000) using a collection of more than 4000 individuáis from northern
and soutiiern África maintained in culture in the greenhouses of the "Estació Inter­nacional
de Biología Mediterránia-Jardí Botánic Marimurtra". Recently, our group
has produced works on the phylogeny based on morphological (MEMBRIVES, 2000)
and cpDNA RFLPs data (CAUJAPÉ-CASTELLS eí a/., 1999b), and dispersal dynamics
of the genus (CAUJAPÉ-CASTELLS & PEDROLA-IVIONFORT, 1997; CAUJAPÉ-CASTELLS
eí a/., 1999a). This diverse Information spectrum regarding similarity and phylogo-netic
relatedness in the genus allowed us to establish compíete comparisons at tne
population and species levéis. In this study, we will consider five taxa {A. burchellii
Baker subsp. burchellii, A. burchellii Baker subsp. pulchrum Pedrola, Membrives,
J. M. Monts. & Caujapé, A. eghimocymbion U. Müll.-Doblies & D. Müll.-Doblies, A.
huntleyi Pedrola, Membrives, J. M. Monts. & Caujapé, and A. walteri Pedrola,
Membrives & J. M. Monts.) which are paradigmatic examples of systematic agree-ments
and discrepancies among the available datasets. Given the generalizad lack
of Information for the species of the genus, we include the description and illustra-tions
of the five species analysed.
MATERIAL AWD METHODS
Morphological characterizations of the material induded in this survey are
based on both cultured and herbarium specimens (see Appendix). Morphological
and allozymic similarity data are from MEMBRIVES (2000). The morphological simi­larity
tree was built from 56 characters (both biometric and qualitative) appiying the
taxonomic distance option in NTSYS-pc (ROHLF, 1992). The allozymic similarity
tree was generated from NEI's (1978) genetic distance based on frequency data of
16 loci in BIOSYS-1 versión 1.7 (SWOFFORD & SELANDER, 1981). The morphologi­cal
phylogeny (MEMBRIVES, 2000) was constructed based on 44 morphological and
reproductivo traits using the option mult*1000 in NONA 2.0 (GOLOBOFF, 1993). One
of the 27 most parsimonious trees was used as a phylogenetic hypothesis of inter-species
relationships. The cpDNA RFLP phylogeny (CAUJAPÉ-CASTELLS et al.,
1999b), was obtained by random addition sequence (100 replicatos) and the TBR
algorithm within the option branch swapping in PAUP* versión 4d64 (D. SWOFFORD,
with permission) with MULPARS and ACCTRAN character optimization.
RESULTS AND DISCUSSION
1. The previously known species Androcymbium burchellii Baker and A.
latifolium Schinz: a new proposal to include A. latifolium as a subspecies
of A. burchellii (figures 2-5)
Androcymbium burchellii is morphologically very similar to A. latifolium Schinz.
Both of them have ovate, thick leaves with scarce short multi-cellular hairs along
110 J. PEDROLA-MONFORT, N. MEMBRIVES, J. M. MONTSERRATS J. CAUJAPE-CASTELLS
the edge, tepal's claw more than twice the length of the lamina, anthers noticeably
exserted and the filament thickened at the base (Figs. 3-5). Reproduction system is
preferentially self-incompatible and the néctar gives off a strong disagreeable
smell. According to the information available they have different chromosome
number: 2n=22 in A. burchellii and population CA of A. latifolium (from Calvinia),
and 2n=20 in population NI of/A. latifolium (from Nieuwoudtville) (Montserrat et al.,
in prep.). Most of the floral characters studied do not differ substantially between
them (Table 1). Nevertheless, a remarkable difference is the purple abaxial face of
the leaves and the white bracts with a green reticulation in A. burchellii, whereas
A. latifolium shows a green abaxial face and purple bracts. Floral biometric
measurements are superior in population NI oí A. latifolium those in population CA
of >A. latifolium or in A. burchellii. Accordingly, the morphological similarity tree (Fig.
2A) sepárales both populations of A. latifolium (NI) and joins A. latifolium (CA) to
A. burchellii. In contrast, both populations of A. latifolium appear in the same
cluster in the allozyme tree (Fig 2B). Genetic identity between A. burchellii and
A. latifolium (CA) is 0.894, and that between A. burchellii and A. latifolium (NI) is
0.898 (MEMBRIVES, 2000). These valúes are similar to the genetic identities
between subespecies or between conspecific populations (CRAWFORD, 1990).
These pieces of evidences and the considerable morphological similarity between
them do not support the separation of these. The morphological (MEMBRIVES, 2000)
and cpDNA RFLP (CAUJAPÉ-CASTELLS et al., 1999b) hypotheses of phylogenetic
relationships coincide in grouping these two taxa in the same clade (Fig. 2C,D).
Recent crossability experiments realized between A. burchellii and A. latifolium
produced a small percentage of viable seeds (MEMBRIVES eí al., in prep.) which
indícate a substantial degree of reproductive isolation between both taxa. In addi-tion,
their geographic distribution is well delimited. Androcymbium burchellii occurs
in the Great Karoo around Sutherland, from top of Botterkiof Pass in the west to
the Nuweveldberge in the east and Bloutouring near Montagu in the south.
Androcymbium latifolium is distributed in the Great Karoo NW of the A. burchellii
área, from Nieuwoudtville to Sutherland (in MÜLLER-DOBLIES & MÜLLER-DOBLIES,
1998). Therefore, is no evidence of sympatric overlapping between both taxa.
Thus, following STUESSY (1990) we consider it justified to propose their separation
into two subspecies of A. burchellii using the priority criterion.' A. burchellii subsp.
burchelli and A. burchellii subsp. pulchrum.
Species n LL LF AA* LE*
A. burchellii 22 6.37±0.94 10.19±1.25 2.71±0.25 14.69+1.70
A. latifolium 29 6.16±1.46 10.73±2.95 2.99±0.71 16.10±2.72
Table 1.- Mean and standard deviation for the most important characters in the differentiation of A.
burchellii and A. latifolium. n: number of individuáis studied. LL: tepal's lamina length, LF: filament
length, AA: anther width, and LE: style length. The characters were measured in mm. Asterisks after
variable codes signal significant differences between the two species at the 0.05 level.
SYSTEMATIC RELATIONSHIPS OF SOME SPECIES OF THE GENUS ANDROCYMBIUM 111
A. burchellii
A. latifolium (CA)
A. latifolium (NI)
A. burcheüii
A. latifolium (CA)
A. latifolium (NI)
A
A. burclieilii
A. latifolium
D
A. burciiellii
A. latifolium
Figure 2.- Similarity relationships between A. burchellii and A. latifolium in terms of (A) morphological
and (B) allozymic data and phylogenetic relationships according to (C) morphological and (D) cpDNA
RFLPs. CA: Calvinia, NI: Nieuwoudtville.
Keys of determination for the subespecies of A. burchellii:
- Leaves green at the adaxial face and purple at the abaxial face, margin with a
purple line in the outer part. Bracts white with green longitudinal and transversal
nerviations forming a reticulate pattern A. burchellii subsp. burchellii
- Leaves green at both faces, margin without a purple line. Bracts reddish.
A. burchellii subsp. pulchrum
Androcymbium burchellii Baker subsp. burchellii
Typus: A. burchellii Baker in J. Bot. 12 (1874) 246. Herbarium Burchell 1401 ex
Baker.
Corm ovoid, (9)14(20) mm in diameter, with a narrow basal crest; tunics brown-reddish,
dark, coriaceous and smooth. Cataphyll white and striped purple, up to 5
mm, papery in texture at senescence. Leaves distichous, ovate-lanceolate, fleshy,
(125)159(210) X (16)23(37) mm, amplexicaule, green at the adaxial face and pur­ple
at the abaxial face, apex acute; margin with a white wing with multi-cellular
short hairs (formed by 4-6 cells), more frequently near the apex, and a purple line
in the outer part due to the abundancy of idioblasts. Bracts different in shape and
texture to leaves, white with green longitudinal and transversal nerviations forming
112 J. PEDROLA-MONFORT, N. MEMBRIVES, J. M. MONTSERRATS J. CAUJAPE-CASTELLS
a reticulate pattern, margin without indument. The first bract orbicular, (30)39(60) x
(30)43(52) mm, apex rounded; the others bracts ovate-lanceolate, (40)49(60) x
(15)18(25) mm, apex acute. Flowers sessile, 1-6 per corm, pestilent scented;
perlanth 15-28 mm; tepal's lamina deltoideous, recurved, apex acute, (4.7)6.4(9) x
(5.3)6.6(8.5) mm, green, with semi-transparent auricules few developed; claw
(10.5) 13.6 (18) mm long, white striped purple. Stamens noticeably exserted; fiia-ments
cylindrical, (8)10.2(13) mm long, purple; anthers lanceolate, (5.7)6.7(8) x
(2.2)2.7(3.2) mm, purple; nectary cylindrical, purple, 4 times wider than the fila-ment.
Ovary subglobose, (6)7.4(10) mm long; style (11)14.7(18) mm long; stigma
papilose, punctiform, purple. Capsule globose, dehiscent, (13)15(18) x
(13)15.5(17) mm. Seeds globose, (1.8)2(2.6) mm in diameter, testa dark brown
and rough, without a developed raphe. Abundant idioblasts present on leaves, le­páis
and capsule. Rollen diaperturate with microrreticulate surface sculpturing,
11.2x19.8x12.6 pm. Species preferently self-incompatible. Low levéis of vegetative
reproduction in cultivation. 2n=22.
Flowering in August-Setember (December-January in J.B. Marimurtra).
Distribution: Great Karoo around Sutherland, from top of Botterkiof Pass in the
west to the Nuweveldberge in the east and Bloutouring near Montagu in the south.
Figure 3.- Androcymbium burchellii Baker subsp. burchellii a: plant general view. b: tepal. c: capsule
¡mmature. (Measures of b-c are expressed in mm).
SYSTEMATIC RELATIONSHIPS OF SOME SPECIES OF THE GENUS ANDROCYMBIUM 113
Androcymbium burchellii Baker subsp. pulchrum (Baker) Pedrola, Membrives,
J.M.Monts. & Caujapé comb. et stat. nov.
=A. latifolium Schinz. In Bull. Herb. Boissier IV (1894): 415. Typus: Süd-Africa,
Hamtam-Geb. 1869, Dr. Meyer {comm. Purcell) Herbarium de Zürich (Z) holo!
=A. pulchrum Schltr. & K. Krause. In Notizbl. Bol Gart. Berlin-Dahiem 7: 522
(1920). Typus : Northern Cape.- (Calvinia): Onder-Bokkeveld, Oorgskioof, 21-08-
1897. Schiechter 10953. Herbarium Berlín (B) holo!
Corm ovoid (10.7)12.8(16) mm in diameter, with a narrow basa! crest; tunics
brown-reddish, dark, coriaceous and smooth. Cataphyll white and striped purpie,
up to 5 mm, papery in texture at senescence. Leaves distichous, ovate-lanceolate,
fleshy, (70)130(230) x (14)29(56) mm, amplexicaule, green, apex acute; margin
with a white wing with multi-cellular short hairs (formed by 4-6 cells), more fre-quently
near the apex. Bracts different in shape and texture to leaves, red, margin
without indument. The first bract ovate-orbicular, apex rounded; the others bracts
ovate-lanceolate, (40)74(125) x (45)63(90) mm, apex acute. Flowers sessüe, 1-5
per corm, pestilent scented; perianth 17-28 mm; tepal's lamina deltoideous, re-curved,
apex acute, (7)8(9) x (3)4.2(5) mm, green, with semi-transparent auricules
few developed; claw (10)14.1(18.5) mm, white striped purpie. Stamens noticeably
exserted; füaments cyündrical, (13)14.6(16) mm, green or purpie; anthers lanceo-late,
(5.7) 6.8 (7.5) x (2.7) 3 (3.4) mm, pink-purpiish; nectary cylindrica!, purpie, 4
times wider than the filament. Ovary subglobose; style (17)19.3(21) mm; stigma
papiloso, punctiform, purpie. Capsule globose, dehiscent (13)15(18) x (14)15.5
(17) mm. Seeds globose, (1.9) 2.6 (3.5) mm in diameter, testa dark brown and
rough, without a developed raphe. Abundant idioblasts present on leaves, tepals
and capsule. Rollen diaperturate with microrreticulate surface sculpturing,
12.1x22.5x13.3 pm. Species preferently self-incompatible. Low levéis of vegetative
reproduction in cultivation. 2n=20, 22.
Flowering in August-Setember (December-January in J.B. Marimurtra).
Distribution: Great Karoo NW of the A. burchellii área, from Nieuwoudtville to
Sutherland.
Figures 4-5.- Androcymbium burchellii subsp. burchellii, from cultivation (4). Androcymbium burchellii
subsp. pulchrum, from cultivation (5).
114 J. PEDROLA-MONFORT, N. MEMBRIVES, J. M. MONTSERRATS J. CAUJAPE-CASTELLS
2. Androcymbium eghimocymbion U.Müll.-Doblies & D.Müll.-Doblies (Figures 6-
9).
Corm globose (4.1)6.2(10.5) mm in diameter, the basai crest as wide as the
corm; tunics brown, coriaceous and smooth. Cataphyll membranous and white,
papery in texture at senescence. Leaves disticlious, linear-lanceolate, 75-120 (270
mm in cultivation) x (5)10(16) mm, amplexicaule, green, apex acute, margin
densely toothed. Bracts deltoideous, similar in texture to leaves, (25)41(80) x
(17)28(40) mm, green, apex rounded, margin densely toothed. Flowers subsessile
(10 mm long), 1-5 per corm, odourless; perianth 7-13 mm; tepal's lamina deltoid,
conspicuously concave, recurved, apex mucronate, (3.2)4.7(6) x (5)6.9(9.8) mm,
green, with transparent auricules; claw (3.5)4.9(6.8) mm long, white and purple
striped. Stamens exserted; fiíament (3.5)5.7(7.2) mm long, green; anthers oval,
(2.6)3.5(4.2) X (1.2)1.7(2) mm, red; nectary cylindrical, purple, slightiy wider than
the fiíament. Ovary subglobose; style (2.5)3.2(4) mm long; stigma papilose, capi-tate,
purple. Capsule oblong, dehiscent, (9)12.6(17) x (6)8.4(11) mm. Seeds globo­se,
(1.2)1.5(1.7) mm in diameter, testa dark brown, rough and without developed
raphe. Abundant idioblasts present on leaves, tepals and capsule. Rollen triapertu-rate
with perfórate surface sculpturing, de 16.2x27.2x17.2 pm. Species self-com-patible,
sometimes cleistogamous. Vegetativo reproduction absent in cultivation.
Flowering in August (January in J.B. Marimurtra).
Distribution: Cape Province, in the mountain regions of the Karoo, between
Wuppertal and Cape Town.
Figure 6.- Androcymbium eghimocymbion U.Müll.-Doblies & D.Müll.-Doblies. a: plant general view. b:
tepal. c: immature capsule, d: tepal from A. austrocapense. (Measures of b-d are expressed in mm).
SYSTEMATIC RELATIONSHIPS OF SOME SPECIES OF THE GENUS ANDROCYMBIUM 115
Androcymbium eghimocymbion differs morphologically from A. austrocapense
U.Müll.-Doblies & D.Müll.-Doblies in showing a shorter tepal, a lamina more conca­ve
and exserted anthers (Figs. 6-9, tabla 2). Furthermore, the seed testa in
A. austrocapense is fleshy, which is a unique feature among the specíes of
Androcymbium studied. Both species are self-compatible and have odourless
néctar. Both species have three pore aperturas.They occur in the vegetation type
known as Fynbos: A. austrocapense is found in litoral dunes whereas A. eghimo­cymbion
prefers montainous áreas. The studied populations in each species
appear consistently grouped in the morphological and allozymic similarity trees, but
the genetic identity between them is very low (0.356 in MEMBRIVES, 2000), corres-ponding
to valúes reported for species belonging to different genera (GOTTLIEB,
1981). The morphological phylogenetic hypothesis places A. eghimocymbion at the
base of a clade (MEMBRIVES, 2000), with A. austrocapense and A. eucomoides as
the closer derived species. In contrast, the cpDNA RFLP phylogenetic hypothesis
separates these species into two ciadas. On the one hand, A. autrocapense is
basal in the dada containing the North African species. On the othar hand, A.
eghimocymbion is basal in the ciada with the South African species (Fig. 7). This
example illustrates a discrapancy between different sourcas of data. At the mor­phological
level, both similarity and phylogeny group A. eghimocymbion and A.
austrocapense. Instead, allozymes raveal a very low identity between them, and
cpDNA RFLPs sepárate them in two different, well-supported clades. This contras-ting
topological positioning of the two species under morphological or molecular
data seems supportive of a fast evolution of molecular traits respect to morphologi­cal
features in these two species.
Species n LL* LU* LA* LE*
A. eghimocymbion 25 4.73±0.7 4.87+0.7 3.51 ±0.4 3.22±0.3
A. austrocapense 63 9.26±1.4 9.24±1.0 3.92±0.6 6.78±0.9
Table 2.- Mean and standard deviation for the most important characters in the differentiation of A.
eghimocymbion and A. austrocapense. n: number of individuáis studied. LL: tepal's lamina length,
LU; tepal's claw length, LA; anther length, and LE: style length. The characters were measured in
mm. Asterisks after variable codes signal significant differences between the two species at the 0.05
level.
116 J. PEDROLA-MONFORT, N. MEMBRIVES, J . M. MONTSERRAT&J. CAUJAPE-CASTELLS
A. eghimocymbion (Cl)
A. eghimocymbion (PK)
A. austrocapense (GH)
A. eghimocymbion (Cl)
A. eghimocymbion (PK)
A. austrocapense (GH)
A. austrocapense (WP)
A B
A. eghimocymbion
A. austrocapense
A. eucomoides i-T
A. austrocapense (WP)
North African species
A. austrocapense
A. eghimocymbion
Figure 7.- Similarity relationships between A. eghimocymbion and A. austrocapense in terms of (A)
morphological and (B) allozymatic data and phylogenetic relationships according to (C) morptiological
data and (D) cpDNA RFLPs. Cl: Citrusdal, PK: Pal<huispas, GH: Good Hope, WP: Whale's Point.
Figures 8-9.- Androcymbium eghimocymbion, from the field (8). Androcymbium austrocapense, from
cultivation (9).
3. Androcymbium huntleyi Pedrola, Membrives, J.M.Monts.
Fontquería (1999) 53: 1 (BC 834977; NBG) (Figures 10-13)
& Caujapé. In
Corm globose (7.6)10.2(13) mm wide, the basal crest as wide as tire corm;
tunics brown, coriaceous and smootln. Cataphyll membranous and wliite, papery in
texture at senescence. Leaves distichous, lanceolate (55)81(92) x (8)12(18) mm,
amplexicaule, glaucous, apex apiculate, margin witlrout indument. Bracts elliptic-deltoideous
with similar texture to the leaves, (15)17(20) (40 mm in cultivation) x
(16)18(21) mm, glaucous, margin winged with a very few papilles. Flowers sessile.
SYSTEMATIC RELATIONSHIPS OF SOME SPECIES OF THE GENUS ANDROCYMBIUM 117
1-2 per corm; perianth 7-10 mm long; tepal's lamina deltoideous, recurved, apex
acute, (2.5)3.4(4.7) x (2)2.8(4.5) mm, white, semi-transparent, auricules scarcely
developed; claw (2.5)3.5(4.2) mm long, white-greenish. Stamens exserted;
filaments cylindrical (3)4.5(5.5) mm long, iight green; anthers oval (1.2)1.6(2) x
(0.8)1.2(1.5) mm, yellow; nectary cylindrical, yellow and orange in its maturity, 3-4
times wider than the fílament. Ovary subglobose; style (2.5)2.8(3) mm long; stigma
papillose, subpunctiform, green. Capsule globoso, dehiscent, (12)13(15) x
(9)10.2(13.5) mm. Seeds globoso, (1.3)1.4(1.6) mm in diameter; testa dark brown,
rough and without developed raphe. Abundant idioblasts present on leaves, tepals
and capsule. Rollen diaperturate with microrugulate-perforate-reticulate surface
sculpturing, 19.3x26.4x19.6 |jm. Species self-compatible. Vegetativa reproduction
observed in cultivation. 2n=18.
Fiowering in August (November-December in J.B. Marimurtra).
Distribution: Cape Province. Namaquaíand, near Eksteenfontein.
Androcymbium huntleyi is similar to A. henssenianum U.Müll.-Doblies & D.Müll.-
Doblies (Figs. 12-13) in the yellow colour of the anthers and the linear or
subpunctiform stigma, never punctiform. However, A. huntleyi presents an
exserted stamen, a short style and leaves and bracts morphologically
differentiated, whereas A. henssenianum features semi-exserted stamen, a style
twice as long as the style of A. huntleyi and leaves and bracts that differentiate
gradually (Fig. 10, Table 3). Morphological similarity data group the populations of
both species, thereby indicating that they are very closely related under phenetic
tenets (Fig. 11 A). Both of them appear in the same clade at the morphological
phylogeny and therefore they share a recent common ancestor (Fig. 11C).
However, these species are considerably distant in the UPGMA tree with allozymic
data (Fig. 118) and show a genetic identity of 0.203 (MEMBRIVES, 2000), which is a
very low valué that corresponds to species belonging to different genera according
a
50mm
Figure 10.- Androcymbium huntleyi Pedrola, Membrives, J.M.Monts. & Caujapé. a: plant general view.
b: tepal. c: capsule immature. d: tepal of A. henssenianum. e: capsule Immature of A. henssenianum
(Measures of b-e are expressed in mm).
118 J. PEDROLA-MONFORT, N. MEMBRIVES, J. M. MONTSERRATS J. CAUJAPE-CASTELLS
to GOTTLIEB (1981). In the allozyme tree, A. henssenianum groups with A. burchellii
and A. latifolium, whereas A. huntleyi is cióse to A. dregei. Data bearing on cpDNA
RFLPs are not available for these two species. This example illustrates a
coincidence between morphological similarity and phylogeny (that implies a cióse
relationship between these species) which is not supported at the level of allozymic
similarity.This result also suggests a faster evolution of allozymic traits than of
morphological features.
Species LU* LA* LE* LC*
A. henssenianum
A. huntleyi
33
6
5.87±1.7
3.55±0.6
1.21±0.2
1.64±0.3
6.64±0.7 6.72±1.0
2.76±0.2 13.00±1.1
Table 3.- Mean and standard deviation for the most important characters in the differentiation of A.
huntleyi and A. henssenianum. n: number of individuáis studied. LU: tepal's claw length, LA: anther
length, LE: style length, and LC: Capsule length. The characters were measured in mm. Asterisks
after variable codes signal signlficant differences between the two species at the 0.05 level.
A. henssenianum
A. huntleyi (EK1)
A. huntleyi (EK3)
A. henssenianum
A. huntleyi
A. henssenianum
— A. burchellii
_ A. latifolium
A. dregei
A. huntleyi
Figure 11.- Similarity relationship between A. burchellii and A. latifolium in terms of (A) morphological
and (B) allozymic data. C: phylogenetic relationships according to morphological data. EK1: 14 km to
Eksteenfontein, EK3: 20 km to Eksteenfontein.
SYSTEMATIC RELATIONSHIPS OF SOME SPECIES OF THE GENUS ANDROCYMBIUM 119
Figures 12-13.- Androcymbium huntleyi, from cultivation (12). Androcymbium henssenianum, from
cultivation (13).
4. Androcymbium walterí Pedrola, Membrives & J.M.Monts. In Fontqueria (1999)
54(2): 7-9 (BC 834975; Herb. Jardí Botánic Marimurtra; MA; NBG) (Figures 14-
18)
Corm laterally compressed, (7)9.5(14) mm in diameter, with a basa! crest
ascending by both sides of the corm; tunics brown, coriaceous, witln marl<ed nerves
descending down tine tunics to tine renovation bud. Cataphyll membranous, white,
papery in texture at senescence. Leaves distichous, ovate-lanceolate, 40-60 (200
in cultivation) x (5)15(25) mm, amplexicaule, glaucous, apex acute, margin witii
papillaes more frequently near the apex. Bracts elliptic with similar texture to
leaves, (25)42(55) x (15)22(26) mm, glaucous, apex acute, margin with a narrow
white wing. Flowers subsessile, 1-2 per corm, disagreeably scented; perianth 20-
25 mm long; tepal's lamina lanceolate, recurvad, apex obtuse, (10)13.4(17) x
(7)8.3(12) mm, green, with auricules semi-transparent embrancing only the
filament's sides; claw (4.5)7.3(10) mm long, white with purple nerviations. Stamens
semi-exserted; filaments (6)8.6(11.5) mm long, purple; anthers lanceolate,
(5)7.3(10) X (2)2.5(3.5) mm, bluish-purple; nectary cylindrical, purple, twofold wider
than the filament. Ovary oblong (6)7.1(8) mm long; style (7)8(9) mm long; stigma
papilose, capitate, purplish. Capsule globose, dehiscent, (9)11.9(16) x (7)11.1(17)
mm. Seeds globose, (1) 1.4 (1.7) mm in diameter, testa black and rough, without a
developed raphe. Few idioblasts on leaves, but abundant in tepals and capsule,
identifiable in the senescence as densely distributed red dots. Rollen diaperturate
with microrugulate-perforate-reticulate surface sculpturing, 10.4x18.7x11.9 pm.
Species with preferential self-incompatible reproduction. Annual vegetative
reproduction ends up with the formation of a little daughter corm situated near the
apical bud of the mother corm. 2n=20.
Flowering in August (December-January in J.B. Marimurtra).
Distribution: Cape Province. In Namaqualand Región, near Springbok.
Androcymbium walterí and A. poeltianum U.Müll.-Doblies & D.Müll.-Doblies
share several morphological traits: fíat corm with decurrent foldings on the surface
120 J. PEDROLA-MONFORT, N. MEMBRIVES, J. M. MONTSERRATS J. CAUJAPE-CASTELLS
and a crest ascending along its sides. The tepal's length and the proportion
between lamina and claw are statisticall indistinguishable. In turn, the anther in A.
walteri is semi-exsert and more than twice as long as A. poeltianum's (Fig. 14,
Table 4). Both species share with A. bellum the same vegetative propagation mode
(i.e. a tiny corm that remains stuck to the mother corm under the coriaceous tunic
during several years). However, they differ in other features related to sexual
reproduction. Androcymbium poeltianum is self-compatible and has inodorous
néctar, while A. walteri and A. bellum are preferentially self-incompatible and have
odoriferous néctar (pestilent in the former and aromatic in the latter). Morphological
similarity indicates a closer relationship oí A. poeltianum with A. walteri tUan with A.
bellum (Fig. 15A). On the contrary, allozymic similarity (Fig. 15B) suggests a closer
relationship of A. walteri with A. bellum than with A. poeltianum. Allozymic identity
between A. walteri and A. poeltianum is 0.808, and that between A. walteri and A.
bellum is 0.875. The morphological phylogeny (Fig. 15C) groups these three
species in the same clade, but allows for the possibility that A. bellum and A.
poeltianum bear a closer relationship than either of them to A. walteri. A very
different picture emerges from the cpDNA RFLP phylogeny (Fig. 15D), with
A.waiteri and A. poeltianum closely related phylogenetically and A. bellum in a
distant clade. This example is illustrative of a coincidence between morphological
and allozyme relationships which is not paralleled by the cpDNA RFLP phylogeny.
Species n LL LF* LA* LE*
A.waiteri 9 13.39±1.9 8.59±1.6 7.33±1.3 8.00±0.5
A. poeltianum 7 12.80±1.9 6.10±1.0 3.41±0.5 6.22±0.8
Table 4.- Mean and standard deviation for the most important characters in the differentiation of A.
walteri and A. poeltianum. n: number of individuáis studied. LL: tepal's lamina length, LF: fllament
length, LA: anther length, and LE: style length. The characters were measured in mm. Asterisks
after variable codes signal significant differences betw/een the two species at the 0.05 level.
Under a phenetic perspective, the morphological identification of all these
Androcymbium species and subspecies is not always supported on allozymic
grounds, and this is a first conflicting área between morphological and molecular
data. However, the phenetic species concept underlies the assumption that a
greater similarity indicates a closer phylogenetic (and therefore taxonomic) affinity.
From this standpoint, species' description and justification obbeys to purely
mechanistic species concepts, which are untestable because of lack of universality
in the criteria used.
The historical species concept is, for some authors, currently preferred on the
grounds that it can be applied and tested consistently (LUCKOW, 1995). Henee,
recent phylogenetic studies using parsimony methods in morphological and cpDNA
RFLP databases embracing a consistent populational representation of
SYSTEMATIC RELATIONSHIPS OF SOME SPECIES OF THE GENUS ANDROCYMBIUM 121
50 mm
12,8
6,1
Figure 14.- Androcymbium walteri Pedrola, Membrives & J.M.Monts. a: Plant general view. b: tepal. c:
capsule immature. d: tepal of/A. poeltianum (measurements of b-d are expressed in mm).
A. bellum
A. walteri
A. poeltianum (CO)
A. poeltianum (NB)
A. poeltianum (ST)
A. bellum
A. walteri
A. poeltianum (CO)
A. poeltianum (NB)
A. poeltianum (ST)
A. walteri
A. bellum
A. poeltianum ks A. bellum
A. walteri
A. poeltianum
A. cuspidatum
Figure 15.- Slmilarlty relationships between A. eghimocymbion and A. austrocapense in terms of (A)
morphological and (B) allozymatic data and phylogenetic relationships according to (C) morphological
data and (D) cpDNA RFLPs. CO: Concordia, NB: Nababeep, ST: Steinl<opf.
122 J. PEDROLA-MONFORT, N. MEMBRIVES, J . M. MONTSERRATS J . CAUJAPE-CASTELLS
Figures 16-18.- Androcymbium walterí, from field (16). Androcymbium poeltianum, from cultivation
(17). Androcymbium bellum, from cultivation (18).
Androcymbium (CAUJAPÉ-CASTELLS ef al., 1999b; MEMBRIVES, 2000) set the stage
to test the species concept in this genus from an evolutionary standpoint. The
major drawback under this scheme is that support for (phenetic) species
description comes from phylogenetic hypotheses. Because of their different
phylosophical contexts and purposes, conclusions reached at each of these two
analytical levéis might conflict.
If we consider that the topologies tracking the changos in the chioroplast
genome and in morphological traits are reflecting true genealogical relationships,
the probiem lies in deciding whether we can assert that these species are different
entities phylogenetically. Stated in other terms, would they be within the smaller
diagnosable units (CRACRAFT, 1983; NIXON & WHEELER, 1990) ? It is difficult at this
point to be precise at distinguishing the species as a mínimum diagnosable unit,
and this has implications at the sampling (a comprehensivo populational sampling
is required) and analytical (we need to survey several different molecular markers)
levéis.
The analysis of a comprehensivo sampling of populations under different
morphological and molecular markers to obtain the smaller diagnosable units is not
always possible. Bearing this in mind, we can compare this difficulty with that
deriving from the application of other generally used species concepts (i. e. the
biological species concept) where experimental work is also arduous often times.
SYSTEMATIC RELATIONSHIPS OF SOME SPECIES OF THE GENUS ANDROCYMBIUM 123
ACKNOWLEDGEMENTS
Amparo Ardanuy provided for the well being and conservation of the cultured
material. Jordi Gibert gave insightful suggestions to an earlier versión of the
manuscript. The expeditions of sampíing of the material in culture and the studies
of conservation genetics developed at the "Estació Internacional de Biología
Mediterránia-Jardí Botánic Marimurtra" have been supported and fundad by the
Karl Faust Foundation. The cpDNA RFLP study was funded by Juli Caujapé-
Castells whíle he was a recipient of the post-doctoral grant 1996BEAI300012 from
the Generalitat de Catalunya.
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SYSTEMATIC RELATIONSHIPS OF SOME SPECIES OF THE GENUS ANDROCYMBIUM 125
Appendix. Examined material (Abbreviations óf the herbariums according to HOLMGREN etal., 1990).
A. austrocapense- SOUTHAFRICA.- Western Cape: Caledon, Kleinimond (3419AB), 15-X-1949, A.F.
969 (NBG); Caledon, Kogel Bay (3419CA), 2-VIII-1946, W.F. Parker 4088 (NBG); Caledon, Hangklip
(3419CA), 6-IX-1942, R.H. Compton 13574 (NBG); Wilderness dunes, George C.P., 16-VIII-1944, R. H.
Compton 15755 (NBG); Simonstown, Red Hill (3418AB), 18-VII-1903, E.P. Phillips 349 (NBG);
Simonstown (3418AB), 1-VII-1993, C. Martins 18892 (J); Simonstown, Good Hope (3418AC), 17-VII-
1994, Pedrola-Monfort & Caujapé-Castells (NBG 153704), (Jardí Botánic Marimurtra 1371), in culta
(Jardi Botánic Marimurtra); Simonstown, Whale's Point (3418AD), 17-VII-1.994, Pedrola-Morifort &
Caujapé-Castells (Jardí Botánic Marimurtra 1370), in culta (Jardí Botánic Marimurtra); Wilderness
(3422BA), 16-VIII-1944, R.H. Corripton 74303 (NBG).- Eastern Cape: SW of Port Elizabeth (3425AB),
30-VIII-1981, D. Snijman 123278 (NBG); Cape Recite Natural Reserve, VIII-1983, M. C. Oliver (UO
3157944).
A. burchellii.- SOUTHAFRICA. - Northern Cape: Anysberg Nature Reserve, Farm Kleinspreuwfontein
177 (3320BC), 3000 ft. 27-VIII-1987, J.W. Lloyd 1056 (NBG); Laingsburg C.P., Whitehill (3320BB), 17-
VIII-1942, R.H. Compton 13399 (NBG); Nieuwoudtville, farm Matjesfontein (3119AC), 23-VIII-1993, P.
Goldblatt & J. Manning 9641 (NBG); Sutherland, Houthoek (3220CA), 31-VIII-1971, W.J. Hanekon 1550
(NBG); Tangua Karoo (3220DA), 31-VIII-1921, R. Marlotti 10374 (NBG); Tangua Karoo (3220DA), IX-
1921, R. Marlotti 10374 (B); Houthoek (3220CA), 31-VIII-1971, W.J.Hanekom 1550 (K); Sutherland,
Koedoes Mountains (3220CC), 21-IX-1981, P. Goldblatt 6307 (MO); Worcester (3319BC), 24-VII-1994,
Pedrola-Monfort & Caujapé-Castells (Jardí Botánic Marimurtra 1368), in culta (Jardi Botánic
Marimurtra).
A. eghimocymbion- SOUTHAFRICA. - Western Cape: Cape Town, Paarl Mountain (3318DB), 500 ft.
28-VII-1961, /. Kruger m9 (NBG); Helderberg, Stellenbosch C.P. (3418BB), 240 m., 6-VIII-1944, R.H.
Parker 3897 (NBG); Cape Península. Botlaryberg, on farm Koopmanskioof (3318DD), 1500 ft. 13-IX-
1988, J. Beyers 71 (NBG); Wuppertal, Pakhuíspass, 10 km from Clanwilliam (3219AA), 8-VIII-1994,
Pedrola-Monfort & Caujapé-Castells (NBG 153709); Simonstown, Somerset West (3418 BB), 13-VIII-
1995, P. Runnalls 813 (NBG); Cape Península. VIII-1950, Pillans 10570 (MO); Citrusdal (3218DB), 8-
\/lll-1994, Pedrola-Monfort & Caujapé-Castells (Jardí Botánic Marimurtra 1395), in culta (Jardí Botánic
Marimurtra); Wuppertal (3219AA), 8-VIII-1994, Pedrola-Monfort & Caujapé-Castells in culta (Jardí
Botánic Marimurtra).
A. henssenianum.- SOUTHAFRICA. - Northern Cape: Vioolsdhft, 2 km N of Eksteenfontein, before the
turn off to Modderfontein (2817CD), 10-VIII-1979, U.Müll.-Doblies & D.Müll.-Doblies 79177a (B);
Vioolsdhft (2817CC), 4-VIII-1994, Pedrola-Monfort & Caujapé-Castells in culta (Jardi Botánic
Mahmurtra).
A. huntleyi- SOUTHAFRICA.- Northern Cape: Vioolsdhft, Road to Eksteenfontein (2917CD), 24-VIII-
1992, P. Goldblatt & J. Manning 9313 (MO); 20 km S of Eksteenfontein (2917AD), 4-VIII-1994, Pedrola-
Monfort & Caujapé-Castells (BC 834977), in culta (Jardí Botánic Mahmurtra).
A. latifolium- SOUTHAFRICA.- Northern Cape: Calvinia (3119BD), 25-VIII-1968, F. Stayner (NBG
87514); Nieuwoudtville, Farm Oohogskioof near Nieuwoudtville (3118BB), 10-VIII-1983, C.M. van Wyk
1418 (NBG); Klip Koppies, Nieuwoudtville (3118BB), 9-VIII-1961, S.G. Lenis 5863 (NBG); 5 miles S of
Calvinia (3119BC), 21-VII-1961, W.F. Barker 9303 (NBG); Nieuwoudtville (3118BB), undated,
C.L./,e/fo/díH 1425/98-67 (K); Oohgoskioof, 21-VIII-1897, Schiechter ^0953 (B,COI,MO); Nieuwoudtville
(3119AA), 27-VII-1994, Pedrola-Monfort & Caujapé-Castells (Jardí Botánic Mahmurtra 1384), in culta
(Jardí Botánic Mahmurtra); Calvinia (3119DA), 27-VII-1994, Pedrola-Monfort & Caujapé-Castells (Jardí
Botánic Mahmurtra 1385), in culta (Jardí Botánic Marimurtra),- Western Cape: Rusoord, N de
Sutheriand (3220AD), 2-IX-1973, /W.F. Thompson, 1795 (NH).
A. poeltianum- SOUTHAFRICA. - Northern Cape: Concordia. NE of the settiement (2917DB), Alt.
1050 m. 15-VIII-1980, U.Müll-Doblies & D.Müll.-Doblies 80102J (B); Sphngbok to Nababeep Road
(2917DB), 6-VIII-1994, Pedrola-Monfort & Caujapé-Castells (Jardí Botánic Mahmurtra 1376), in culta
(Jardí Botánic Mahmurtra.); Sphngbok to Concordia Road (2917DB), 6-VIII-1994, Pedrola-Monfort &
Caujapé-Castells (Jardí Botánic Mahmurtra 1377), in culta (Jardí Botánic Mahmurtra); 5 km from
Steinkopf to Sphngbok (2917DC), 3-VIII-1994, Pedrola-Monfort & Caujapé-Castells in culta (Jardí
126 J. PEDROLA-MONFORT, N. MEMBRIVES, J . M. MONTSERRATS J . CAUJAPE-CASTELLS
Botánic Marimurtra).
A. walteri- SOUTHAFRICA.- Northern Cape: Steinkopf (2917DC), 3-VIII-1994, Pedrola-Monfort &
Caujapé-Castells (BC 834975); Steinkopf {2917DC), 3-VIII-1994, Pedrola-Monfort & Caujapé-Castells
(Jardí Botánic IVIarimurtra 1380), in culta (Jardí Botánic IVIarimurtra).
-. NAIVIIBIA: Witputz, across 21 km top of Inill, Down 9,36 km (2716DA), 12-VII-1983, N.J. van Berkel
498 (NBG).