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Pollen and reproductive morphology of Rhigiophyllum and Siphocodon
(Campanulaceae): two unique genera of the fynbos vegetation of
South Africa
W.M.M. EDDIE*, C.N. CUPIDO** and J.J. SKVARLA***
Keywords: Campanulaceae, Campanuloideae, Cape fl ora, carpels, fl oral evolution, fynbos, pollen, Rhigiophylleae, seed pockets, tribus nov.,
Wahlenbergioideae
ABSTRACT
Pollen grains of Rhigiophyllum squarrosum Hochst., Siphocodon spartioides Turcz. and S. debilis Schltr., are fl attened
and triangular with pores at the angles. This morphology is radically different from known pollen of the Campanulaceae s.str.:
the Campanulaceae are treated here as a family separate from the Lobeliaceae, Cyphiaceae, Nemacladaceae, Pentaphrag-
mataceae and Sphenocleaceae (Lammers 1992). As traditionally conceived, the Campanulaceae is very heterogeneous and,
in many classifi cations, these families were treated as subfamilies of a much-enlarged Campanulaceae. The consistently dif-
ferent fl oral morphology, biochemistry and pollen structure of the Lobeliaceae favours the recognition of this predominantly
tropical group as a separate family.
The pollen grains of these species are described in comparison with other members of the Campanulaceae. Based on
surface characteristics of their pollen grains, we conclude that they represent an early offshoot of the wahlenbergioid line-
age in southern Africa. We suggest that this unique pollen may also be the result of a highly selective regime in the fynbos,
associated with specialized pollinators, and base-poor soils, in addition to possible adaptations for ant dispersal and fi re.
Rhigiophyllum Hochst. and Siphocodon Turcz. are also unique in having free carpel-like structures within the ovary. These
shrink to form seed pockets around the seeds and disperse as units when the capsule matures. Data from molecular studies
support the contention that these taxa form a sister group to all other wahlenbergioids and that this should be formally recog-
nized in a classifi cation system. We treat Rhigiophyllum and Siphocodon within the Campanulaceae: Wahlenbergioideae, as a
separate tribe, the Rhigiophylleae tribus nov., the species of which are distinguishable from other wahlenbergioids by unique
angulaperturate pollen, epipetalous stamens, free carpel-like structures and seed pockets.
INTRODUCTION
During the course of a palynological re-investigation
of the Campanulaceae1 s.str., a number of pollen samples
were obtained from material in the herbarium of the Royal
Botanic Garden Edinburgh and sent to the third author
for scanning electron micrograph imaging (SEM). Subse-
quently, samples representing Rhigiophyllum squarrosum
Hochst. and Siphocodon spartioides Turcz., were found
to have fl attened, angular (triangular) pollen grains with
pores at the angles. This morphology is radically differ-
ent from all known pollen of the Campanulaceae, although
it was reported for both genera in the landmark paper (in
Russian) by Avetisian in 1967, which we had inadvertently
overlooked. Initially, we suspected that the samples were
contaminated, possibly due to alien pollen on the stigmas
of the herbarium material. However, an examination of
material at the Compton Herbarium at Kirstenbosch by the
second author using light microscopy, confi rmed that both
of these species indeed had radically different pollen mor-
phology. A third species, S. debilis Schltr., was also exam-
ined by the second author and found to have pollen similar
to its congener but was not included in the SEM analyses.
This report describes the pollen shape and surface fea-
tures of the exine of the two principal species and genera
involved. We also discuss other features of these two gen-
era such as fl oral morphology and the unique seed pock-
ets, particularly with respect to their possible ecological
signifi cance. Finally, we discuss the systematic usefulness
of these fi ndings for a revised classifi cation of the wahlen-
bergioid genera and describe a new tribe, the Rhigiophyl-
leae, to accommodate Rhigiophyllum and Siphocodon.
MATERIALS AND METHODS
Pollen (Table 1) was examined with a JEOL model 880
scanning electron microscope after cleaning with acetoly-
sis (Erdtman 1960) and made electrically conductive with
gold/palladium (Chissoe & Skvarla 1996). For the light
microscope (LM) examination, pollen of the respective
species was removed from alcohol-preserved fl owers. The
pollen was placed on a microscope slide in a drop of water
and examined. The gynoecium of Rhigio phyllum was
exposed by a longitudinal free-hand section through the
hypanthium wall and the removal of tissue with forceps.
* Offi ce of Lifelong Learning, University of Edinburgh, 11 Buccleuch
Place, Edinburgh EH8 9LW, Scotland, UK. E-mail: weddie1@staff-
mail.ed.ac.uk.
** Compton Herbarium, South African National Biodiversity Institute,
Private Bag X7, 7735 Claremont, Cape Town. E-mail: C.Cupido@
sanbi.org.za.
*** Oklahoma Biological Survey & Department of Biology and
Microbiology, University of Oklahoma, 770 Van Vleet Oval, Norman,
Oklahoma, 73019-6131, USA. E-mail: jskvarla@ou.edu.
MS. received: 2009-03-30.
1 The Campanulaceae is treated here as a family separate from the Lo-
beliaceae, Cyphiaceae, Nemacladaceae, Pentaphragmataceae and Sphe-
nocleaceae (Lammers 1992). As traditionally conceived, the Campanu-
laceae is very heterogeneous and, in many classifi cations, these families
were treated as subfamilies of a much-enlarged Campanulaceae. The
consistently different fl oral morphology, biochemistry and pollen struc-
ture of the Lobeliaceae favours the recognition of this predominantly
tropical group as a separate family. Welman (2000) treats the Campanu-
laceae separately from Lobeliaceae, within which she included the ge-
nus Cyphia P.J.Bergius.
Bothalia 40,1: 103–115 (2010)
104 Bothalia 40,1 (2010)
Brief history of original description of Rhigiophyllum
and Siphocodon
Hochstetter (1842) established the genus Rhigiophyl-
lum for the sole species R. squarrosum, which was fi rst
collected near Elim, Bredasdorp. Siphocodon was estab-
lished a decade later by Turczaninow (1852) for S. spar-
tioides, based on collections from Klein Houwhoek, east
of Grabouw, and from Swartberg, Caledon. Forty-fi ve
years later, Schlechter (1897) described a second spe-
cies, Siphocodon debilis from Elim.
Ecology, distribution and morphology
Rhigiophyllum squarrosum and both species of
Siphocodon occur on nutrient-poor soils associated
with sandstone slopes of the southwestern Cape and are
typical, but highly localized, fynbos plants. Rhigiophyl-
lum occurs from Akkedisberg, northeast of Stanford to
Napier and Bredasdorp, whereas S. spartioides occurs
from Sir Lowry’s Pass near Somerset West to the Lange-
berg in Riversdale and S. debilis occurs from the Hotten-
tots Holland Mountains near Stellenbosch to Bredasdorp
and inland to Riviersonderend (Figure 1).
Rhigiophyllum squarrosum is a rigid, sparsely
branched subshrub, ± 0.30–0.45 m tall with the habit of
species of Roella L. Its broadly ovate, coriaceous leaves
are imbricate, squarrose, entire and in four ranks. Lan-
ceolate bract-like leaves subtend the azure-violet fl ow-
ers, which are aggregated in a terminal head. The corolla
is elongated and consists of a long narrow tube termi-
nated by fi ve spreading obtuse lobes. The style is fi li-
form, exserted, and terminates into three short stigmatic
lobes (Figure 2A, B).
The two species of Siphocodon are radically differ-
ent in appearance from Rhigiophyllum. They are gla-
brous, wiry subshrubs (S. spartioides is 0.3–0.6 m tall,
S. debilis somewhat smaller) with sparse, minute, scale-
like, appressed leaves. The fl owers are solitary, termi-
nal and axillary, mostly towards the apices of the stems
in a loose, few-fl owered infl orescence. The fl owers of
Siphocodon spartioides are bluish purple, whereas those
of S. debilis are violet or whitish with pinkish brown
honey-guides on the corolla tube. The corolla is nar-
rowly tubular-campanulate with fi ve spreading obtuse
lobes incised to about one-third the length of the tube.
The style is fi
liform, included and terminates into three
short stigmatic lobes in S. spartioides, whereas in S.
debilis the stigma is capitate (Figure 2C–E).
On closer inspection of the corolla and capsule of
both genera, a number of common features are found.
For example, both have rather long, tubular corollas
with the stamens adnate via the fi laments to the corolla
tube, the latter feature being unique among the Cam-
panulaceae. The stamens of Rhigiophyllum squarro-
sum, which are almost exserted, are attached below the
apex of the corolla tube but the fi laments are decurrent
nearly to the base. In Siphocodon debilis, the stamens
are included and are attached at the middle of the corolla
tube, whereas in S. spartioides, they are attached in the
upper part of the tube.
The capsule dehiscence is by means of a plug in Rhigio-
phyllum (Figure 3C) or circumscissile by means of an
operculum in Siphocodon (Figure 3E). In both genera,
these structures comprise the upper part of the ovary and
the style, surrounded by the persistent corolla. In Rhigio-
phyllum, the line of dehiscence is above the calyx lobes
and the seeds (within seed pockets) are dispersed through
a narrow hole, whereas in Siphocodon it is below, so
that, when the operculum detaches, the remaining lower
TABLE 1.—Species of Campanulaceae and Lobeliaceae for which pollen samples were examined in this study
Species Collector/No. Herbarium
Burmeistera vulgaris E.Wimm. R. Lent 526 Bebb
Campanumoea javanica Blume A. Henry 9634 RBGE
Codonopsis convolvulacea Kurz Chungtien-Liang-Dali Expedition 648 RBGE
Craterocapsa montana (A.DC.) Hilliard & B.L.Burtt O.Hilliard & B.L. Burtt 13221 RBGE
Cyclocodon lancifolius (Roxb.) Kurz Collector unknown 1563 RBGE
Jasione montana L. F.J. Hermann 4405 Bebb
Leptocodon gracilis (Hook.f.) Lem. Sinclair & Long 4980 RBGE
Merciera brevifolia A.DC. Schlechter 7211 RBGE
Microcodon hispidulus (L.f.) Sond. Collector unknown 1993 RBGE
Prismatocarpus fruticosus (L.) L’Hér. C.M. van Wyk 3420 RBGE
Rhigiophyllum squarrosum Hochst. Schlechter 9616 RBGE
Roella prostrata E.Mey. ex A.DC. R. Dümmer 938 RBGE
Siphocodon spartioides Turcz. E. Esterhuysen 35770 RBGE
Wahlenbergia marginata (Thunb. ex Murray) A.DC. J. & C. Taylor 16613 Bebb
RBGE, Royal Botanic Garden, Edinburgh.
FIGURE 1.—Known distribution of Rhigiophyllum squarrosum (dotted
line); Siphocodon spartioides (solid line) and S. debilis (dashed
line).
Bothalia 40,1 (2010) 105
part of the capsule is a neat, open, cup-like structure.
In Rhigiophyllum, the remainder of the capsule easily
detaches from the pedicel and disperses, probably with
some seeds remaining inside. Since the line of dehiscence
in the capsule of Rhigiophyllum is above the calyx lobes,
it resembles that of Roella and therefore differs in posi-
tional homology from the mechanism in Siphocodon.
Unlike other wahlenbergioids, these two genera have
(2)3 free carpel-like structures within the inferior ovary,
each of which has two to several pendulous ovules
attached near the top (Figure 4B7). It is diffi cult to decide
if the seed pockets separate from the wall of the infe-
rior ovary of adult fl owers or if they are formations sui
generis (proliferations of the placentae) (Erbar & Leins
pers. comm.)*. Some ovules appear to abort before matu-
rity leaving just one or two seeds per structure (Figure
FIGURE 2.—A, B, Rhigiophyllum squarrosum: A, habit; B, details of infl orescence. C, D, Siphocodon spartioides: C, details of fl ower and remains
of capsule; D, slender wiry stems. S. debilis: E, details of fl ower showing honey-guides and the twisted, entwined stems. Photographs: A,
W.M.M. Eddie; B–E, C.N. Cupido.
A B
C D E
* Profs Claudia Erbar and Peter Leins conducted a preliminary investi-
gation of the ovary of Rhigiophyllum from material supplied by the sec-
ond author. They report that the inferior ovary develops as in all other
cases [of Campanulaceae] due to an intercalary growth in the fl oral axis
and that the seed pocket is a special form of an endocarp. The epider-
mis (and eventually a few cells of deeper layers) of the ovary locules
separates from the wall of the inferior ovary to form the seed pockets. A
complete ontogenetical study (including histology and SEM-investiga-
tion) is planned and the results will be published in due course.
106 Bothalia 40,1 (2010)
4E11). The walls of these carpel-like structures shrink
to enclose the seed at maturity, forming a carunculated
pocket (Figure 4D10), which is released entire from the
mature capsule. This structure was apparently overlooked
by Botting Hemsley in Hooker’s Icones plantarum (1897)
where he described the ovary simply as: ‘Ovarium 3-locu-
lare, loculis pluriovulatis, ovulis pendulis’. In Sonder
(1865: 596), this seed pocket is apparently misidenti-
fi ed as a ‘very loose, rugose testa’. The protuberances on
the surface of the seed pocket are similar in both genera
although in Siphocodon they are more round and regular.
There are also slight differences in seed shape. Siphoco-
don seeds are slightly diamond-shaped in comparison
with the oval seeds of Rhigiophyllum. In both genera the
seeds have a strong electrostatic charge and ‘jump’ to
about 0.1 m when manually extracted from the pockets.
The function of the seed pocket is unknown, but it may
perform a role in dispersal, for example by ants. The
seeds of these three taxa are large and few in number
and this may be correlated with the establishment of the
seedling in nutrient-poor environments (Eddie & Cupido
2001). The shiny testa of the seed would suggest that
dormancy and nutrient release by fi re may be important
components in their ecology. Shiny testae are a feature
of many annual species of the Campanulaceae where
seed dormancy is the norm (Eddie 1997).
Description of pollen grains of Rhigiophyllum
squarrosum and Siphocodon spartioides
Figures 5 and 6 show the radical differences in pol-
len morphology between Rhigiophyllum squarrosum and
Siphocodon spartioides and other wahlenbergioid genera
such as Wahlenbergia Schrad. ex Roth, Crateroca psa Hil-
liard & B.L.Burtt, Prismatocarpus L’Hér., Roella, Mer-
ciera A.DC. and Microcodon A.DC. and between platy-
codonoid genera such as Leptocodon (Hook.f.) Lem.,
Campanumoea Blume, Cyclocodon Griff. ex Hook.f. &
Thomson and Codonopsis subgen. Pseudocodonopsis
Kom.
Pollen grains disperse as monads and they are superfi -
cially like Alnus Miller/Betula L./Corylus L. (Betulaceae)
or Rhamnus L. (Rhamnaceae), but very unlike the pollen
of Pentaphragma Wall. ex G.Don (Pentaphragmataceae),
which was formerly considered to be close to the Cam-
panulaceae, and which has trilobate pollen with the pores
between the lobes (Dunbar 1978, 1979, 1981). Their
shape in polar view is reminiscent of species of Acarpha
Griseb. (Calyceraceae) (De Vore et al. 2007) or species of
Lopezia Cav. (Onagraceae) (third author). They are angu-
lar (triangular and obtuse or straight to slightly convex)
in polar view; non-angular (elliptic and obtuse) in equa-
torial view; trizonoporate (rarely tetrazonoporate) (steph-
anoporate of Faegri & Iversen 1975) in equatorial zone;
pori circular, situated at the angles (angulaperturate) and
non-vestibulate; large, ± 50 m diameter (R. squarrosum,
Figure 5A) or ± 40 m diameter (Siphocodon spartioides,
Figure 5B); sculpturing is verrucate in S. spartioides, or
psilate in R. squarrosum.
Palynological investigations of the Campanulaceae
Studies of the pollen of the Campanulaceae are exten-
sive and the family is comparatively well known paly-
nologically, but there are gaps in our knowledge of the
wahlenbergioid taxa of the southern hemisphere, and of
many endemic campanuloid taxa of central Asia. A brief,
if diverse, survey of Campanulaceae pollen was pro-
vided by Erdtman (1952), followed by a similar survey
of 21 genera by Chapman (1967). Avetisian (1967) pro-
vided a fi rm foundation for a systematic re-appraisal of
the family using palynological characters, but the most
thorough examination of the family using scanning elec-
tron microscopy was conducted by Dunbar (1973a–c,
FIGURE 3.—A–C, Rhigiophyllum
squarrosum, Cupido s.n.: A,
fruiting head showing aggre-
gation of mature capsules; B,
individual mature capsules
removed from head and show-
ing spreading calyx lobes; C,
withered corollas enclos-
ing styles with attached plug
(ovary top). D, E, Siphoco-
don spartioides, Eddie 1017:
D, branched stem showing
remains of dehisced capsules;
E, corolla enclosing style and
attached to upper calyx and
calyx lobes (circumscissile
lid or operculum). Scale bars:
A–C, 10 mm; D, E, 10 mm.
Artist: W.M.M. Eddie.
A
B
C
D
E
Bothalia 40,1 (2010) 107
1975a, b, 1978, 1979, 1981, 1984), who also studied
ontogeny, and by Dunbar & Wallentinus (1976) using
phenetic methods. The pollen of the Campanulaceae can
be divided into two broad groups as follows:
1. The platycodonoid taxa of Asia and Africa (e.g.
Platycodon A.DC., Cyananthus Wall. ex Benth., Codo-
nopsis Wall., Cyclocodon, Campanumoea, and Canarina
L.) have pollen that is either 6–10-colpate, 3-colporate,
or 5- or 6-colporate (Figure 6). They have in common
an oblate-spheroidal shape, a relatively high number of
colpi and an exine sculpturing that consists of spinules,
verruca-like spinules, or verrucae, between which are
small pits of uniform diameter, or a reticulum in low
relief with very small lumina. The ektexine structure
consists of a tectum perforated by mostly narrow chan-
nels, medium to high bacula that are closely adpressed
in some species, and a reduced or absent foot layer. The
endexine is almost undivided.
2. The campanuloid and wahlenbergioid taxa have
pollen that is 3- or 4-porate, 6-porate, or 12-porate (Fig-
ure 5). The porate taxa are mostly zonotreme or rarely
pantoporate. The pantoporate condition is approached in
those species that have an increased number of pores and
where the position of the pores becomes irregular and
not strictly zonotreme. The shape of the pollen is sphe-
roidal or oblate-spheroidal, rarely suboblate or prolate-
spheroidal. The exine sculpture consists of spinules of
different number, shape and size. Between the spinules
there are ridges, protrusions or a low-relief reticulum,
fi nger-like structures, or ridges with the top end bent
upwards (Dunbar 1975a). The ektexine structure (and
sculpture) varies from simple to complex. Complex
ektexine consists of a surface covered by spinules, dis-
tinctly divided basally, short ridges/protrusions between
spinules, a sponge-like tectum, stubble-like bacula con-
tinuous with an undivided foot layer, and connections
to the tectum may be thin. Less complex ektexine con-
FIGURE 4.—LM photographs of Rhigiophyllum squarrosum. A, gynoecium and corolla showing: A1, calyx lobes; A2, corolla; A3,
peduncle. B, detail of gynoecium showing: B4, corolla; B5, calyx lobe; B6, ovary wall; B8, separate carpel-like structures;
enclosing B7, pendulous ovules. C9, central veins of ovary; D10, carunculated seed pockets formed by shrinking carpel-like
structures; E11, seed pocket showing a mature seed. Photographer: C.N.Cupido.
A B C
D E
1
2
3
4
6
7
5
8
9
10
11
108 Bothalia 40,1 (2010)
sists of a surface covered by spinules, which, in some
species, divide basally, together with protrusions, low-
relief reticula, a thin, distinctly outlined tectum perfor-
ated by channels, high bacula that are continuous with
the tectum and an undivided foot layer. Simple ektexine
consists of a surface covered by discrete spinules, less
distinctly divided than the complex type, and low pro-
trusions. The uniformly outlined tectum is perforated by
narrow channels and has the same thickness as the undi-
vided foot layer. The bacula are medium/high, and are
continuous with the tectum and foot layer. The endexine,
which varies in thickness, is lamellated, except in the
simple ektexine type.
Knowledge of pollen morphology in the wahlen-
bergioid genera is patchy and mostly concentrated on
the genus Wahlenbergia (Thulin 1974; Dunbar 1975a,
b), although a detailed study of the pollen of Hetero-
chaenia A.DC. was undertaken by Badré et al. (1972),
and by Straka & Simon (1969). Wahlenbergioid gen-
era such as Prismatocarpus, Roella, and Wahlenber-
gia are all in Dunbar’s Group 1, i.e. pollen grains that
are mostly radially symmetrical, isopolar, zonotreme,
3–5-porate, spheroidal and tectate. Spinules are evenly
distributed over the non-apertural surface of the pollen
grains. These three genera did not show any particular
clustering with each other with respect to the other taxa
(Dunbar 1975a, b). Apparently Von Brehmer (1915)
considered the pollen morphology to be of no value
as a taxonomic character in Wahlenbergia. However,
Erdtman (1952) placed Wahlenbergia, Roella and Pris-
matocarpus in a group of genera with (2)3–(5)-porate,
suboblate to oblate spheroidal pollen with spinulifer-
ous sexine, which is thinner than the nexine. Avetisian
(1967) studied fi ve species of Wahlenbergia (including
W. hederacea (L.) Rchb.), seven species of Lightfoo-
FIGURE 5.—SEM micrographs of pollen of wahlenbergioid genera of Campanulaceae plus Jasione (all polar view except C). A,
Rhigiophyllum squarrosum Hochst.; B, Siphocodon spartioides Turcz.; C, Prismatocarpus fruticosus (L.) L’Hér. (equatorial
view); D, Wahlenbergia marginata (Thunb. ex Murray) A.DC.; E, Craterocapsa montana (A.DC.) Hilliard & B.L.Burtt; F,
Microcodon hispidulus (L.f.) Sond.; G. Roella prostrata E.Mey. ex A.DC.; H, Merciera brevifolia A.DC.; I, Jasione montana
L. Scale bars: A–C, E–G, 10 m; D, H, I, 5 m. SEM micrographs by J.J. Skvarla.
A B C
D E F
G H I
Bothalia 40,1 (2010) 109
tia L’Hér. nom. illeg. and Cephalostigma A.DC., and
claimed to be able to differentiate between these three
taxa. Straka & Simon (1969) distinguished two types
of wahlenbergioid pollen in the Madagascan fl ora. The
Cephalostigma-type is characteristic of C. hirsutum
Edgew. and is 4–6-pantoporate, whereas the Wahlen-
bergia-type, which is 3-zonoporate is characteristic of
W. perrieri Thulin and W. madagascariensis A.DC.,
in addition to the Mascarene endemic genera Berenice
Tul. and Heterochaenia (Thulin 1975).
The species studied by Thulin (1975) and formerly
placed in Cephalostigma included: Wahlenbergia erecta
(Roth ex Schult.) Tuyn; W. fl exuosa (Hook.f. & Thom-
son) Thulin; W. hirsuta (Edgew.) Tuyn; W. hookeri
(C.B.Clarke) Tuyn; W. ramosissima (Hemsl.) Thulin;
and W. perrottettii (A.DC.) Thulin. He concluded that
Wahlenbergia, Cephalostigma and Lightfootia could not
be distinguished on pollen characters, although W. hir-
suta has an increased numbers of pores that could be
of taxonomic value. According to Thulin, with increas-
ing number of pores, the position of the pores becomes
irregular and not strictly zonotreme. Several differences
in spinule size and density exist between different groups
of the genus Wahlenbergia. For example, the W. undu-
lata (L.f.) A.DC. group has longer spinules than other
groups, and the area of the exine between the spinules in
the W. undulata and W. madagascariensis groups is dis-
tinctly granular or with short ridges. Thulin (1974) also
reported that the pollen of Namacodon Thulin disperses
in tetrads, unlike the pollen grains of all other taxa in the
family, which disperse as monads—tetrads have been
recorded in Legousia falcata (Ten.) Fritsch ex Janch.
(fi rst author, unpublished data).
Molecular studies
Recent molecular studies using trnL-F and ITS gene
sequences (Cupido 2008) and combined chloroplast
DNA datasets (rbcL, atpB and matK) (Haberle et al.
2009) have shown quite conclusively that the strongest
molecular affi nities of Rhigiophyllum are with the two
species of Siphocodon (Figures 7; 8). Merciera, Roella
and Prismatocarpus form a well-supported clade, but
the relationships within this clade are largely unresolved.
Merciera however, forms a weakly supported subclade.
Roella, Prismatocarpus and Wahlenbergia were also
found to be paraphyletic, the latter massively so. Theil-
era E.Phillips was found to be closest to several species
of Wahlenbergia, all of which were formerly treated as
Lightfootia, and in a clade comprising Craterocapsa
and Wahlenbergia procumbens (L.f.) A.DC., W. huttonii
(Sond.) Thulin, and W. stellarioides Cham.
Another surprising result of the molecular studies has
shown that Rhigiophyllum and Siphocodon form a sister
group to all the other southern hemisphere wahlenber-
gioids, including taxa from the Mascarene Islands and St
Helena (Haberle et al. 2009). This has profound impli-
cations, for it suggests that this split in lineages was a
very ancient one. Previous molecular studies (Eddie et
al. 2003) using ITS nrDNA found a clear dichotomy
between the colpate/colporate platycodonoid taxa and
the porate wahlenbergioid and campanuloid taxa. This
major split in the Campanulaceae is hypothesized to
be a consequence of the isolation engendered by tec-
tonic activity in a fragmenting Early Tertiary Gondwana
(Eddie et al. 2003). Subsequent evolution of these two
lineages was independent, with the bulk of the platyco-
A B C
D E F
FIGURE 6.—A–F, SEM micrographs of pollen of platycodonoid genera of Campanulaceae and Lobeliaceae (all polar view except E
and F): A, Codonopsis (subgen. Pseudocodonopsis Kom.) convolvulacea Kurz.; B, Cyclocodon lancifolius (Roxb.) Kurz; C,
Campanumoea javanica Blume; D, E, Leptocodon gracilis (Hook.f.) Lem.; F, Burmeistera vulgaris E.Wimm. (Lobeliaceae).
Scale bars: A–C, 10 m; D–F, 5 m. SEM micrographs by J.J. Skvarla.
110 Bothalia 40,1 (2010)
donoids in eastern Asia, the wahlenbergioids in Africa,
and the campanuloids differentiating primarily in north-
ern Africa and the evolving Mediterranean region.
DISCUSSION AND CONCLUSIONS
Pollen morphology of Rhigiophyllum and Siphocodon
The triangular pollen of Rhigiophyllum and Siphoco-
don is so unlike the known pollen of the Campanulaceae
that it throws their relationship with that family into
question. Kolakovsky (1987: 1573) excluded both genera
from the Campanulaceae, yet, from molecular data (Eddie
et al. 2002; Haberle et al. 2009) and their possession of
porate pollen, it would appear that these genera are cor-
rectly placed close to typical wahlenbergioid, porate taxa.
From a biogeographical viewpoint, one would favour a
relationship with the wahlenbergioid taxa so character-
istic of southern Africa, and with which they have tradi-
tionally been associated. The surface sculpturing of the
pollen is more simplifi ed, lacks the dense spinuliferous
condition, and recalls the surface features of the pollen
found in the platycodonoid genera. This suggests that
these two genera may represent an older lineage of the
Campanulaceae in southern Africa that is somewhat inter-
mediate between platycodonoids and wahlenbergioids, or
it may be that the pollen morphology is convergent with
that of the platycodonoids (perhaps the result of paedo-
morphosis and/or neoteny). However, some porate pol-
len in the Campanulaceae is simpler in structure than the
dense spinuliferous type. Avetisian (1967) suggested that
tropical colpate/colporate pollen is the most primitive
type within the Campanulaceae, whereas porate pollen
from temperate zones, including pantoporate pollen, is
considered an advanced type (Van Campo 1966; Muller
1970; Punt 1976). Dunbar’s (1984) results agree partially
with this view with respect to complex exine. Perhaps the
unique triangular pollen represents a highly specialized
adaptation either to conditions pertaining to their pol-
linators or to some, yet unknown, biological component
FIGURE 7.—Strict consensus of 165
equally parsimonious trees
(length = 859, CI = 0.511,
RI = 0.739) found after heu-
ristic search of the ITS data
set for 75 taxa of the South
African Campanulaceae and
four Lobeliaceae/Cyphiaceae
(outgroup). Bootstrap val-
ues 50 % indicated above
branches. Numbers below
branches indicate posterior
probability values expressed
as percentages (from Cupido
2008). , clades common to
all analyses.
Bothalia 40,1 (2010) 111
of the fynbos vegetation. This explanation seems highly
plausible, but no other members of the Campanulaceae
have this type of pollen, so the functional signifi cance of
the triangular pollen remains unresolved.
General morphology and ecology of the fynbos
wahlenbergioids
Rhigiophyllum and Siphocodon share a number of
morphological features with other fynbos taxa such as
Merciera, Theilera, Roella, Prismatocarpus and many
fynbos species of the group formerly included in the
illegitimate genus Lightfootia. They all show radical
departures in a whole suite of morphological characters
from the temperate Campanulaceae bauplan, although
most can loosely be described as ericoid. All are dwarf
undershrubs or shrublets, somewhat rigid or wiry, and
frequently with ericoid leaves in fascicles (e.g. Merciera
and Theilera), or imbricate, as in Rhigiophyllum.
Many of them have long tubular fl owers (Merciera,
Theilera, Rhigiophyllum, and Siphocodon) and indehis-
cent capsules (Merciera) or at least an unusual capsule
dehiscence mechanism (Prismatocarpus, Roella, Rhigio-
phyllum, and Siphocodon). Several of these genera (e.g.
Merciera, Theilera, and Prismatocarpus, subgen. Afro-
trachelium Adamson) even show a remarkable, if super-
fi cial, resemblance to the Lobeliaceae and Stylidiaceae,
and the fl owers of Rhigiophyllum look similar to those
of Calycera Cav. (Calyceraceae). The fl owers are either
solitary and more or less sessile (Roella, Prismatocarpus,
Theilera and Merciera), in loose terminal infl orescences
(Prismatocarpus, Siphocodon), or rarely in dense heads
(Rhigiophyllum). These features suggest a general con-
vergence in morphologies that may correlate with similar
ecologies. However, as shown by the molecular studies,
these subgroups are not part of the same phylogenetic
sublineages and their similarities are probably superfi cial.
They may be best considered as parallel ecotypes.
FIGURE 8.—Strict consensus of 415
equally parsimonious trees
(length = 945, CI = 0.684, RI
= 0.872) found after heuris-
tic search of the trnL-F data
set for 90 taxa of the South
African Campanulaceae and
six Lobeliaceae/Cyphiaceae
(outgroup). Bootstrap val-
ues 50 % indicated above
branches. Numbers below
branches indicate posterior
probability values expressed
as percentages (from Cupido
2008). , clades common to
all analyses;, clades com-
mon between trnL-F and the
combined analysis.
112 Bothalia 40,1 (2010)
Rhigiophyllum is so dissimilar morphologically from
both species of Siphocodon that, on fi rst inspection, a
close relationship between these two genera is not obvi-
ous. Furthermore, Siphocodon spartioides is very unlike
S. debilis, yet, the infrageneric disparity in morphology
between Siphocodon spartioides and S. debilis offers a
possible clue to the evolutionary history of all three taxa,
in addition to that of the fynbos wahlenbergioids in gen-
eral. This disparity suggests that divergent selection pres-
sure has been intense, driving three closely related spe-
cies towards radically different morphologies. A similar
situation is seen in the two species of Musschia Dumort.
(Campanulaceae) on Madeira (Eddie et al. 2003).
The evolutionary divergence of Rhigiophyllum and
Siphocodon probably occurred early, in concert with the
progressive aridity of the Cape Region (Cupido 2008).
From the similarity of their fl oral morphology with other
fynbos plants, we can infer that these taxa have highly
specialized pollination syndromes, probably with long-
proboscid fl ies (including horse fl ies, tangle-wing fl ies
and bee fl ies) as the principal pollen vectors (Goldblatt et
al. 1995). However, until further studies are completed,
we simply do not know what adaptive advantages, if
any, are conferred by the unique pollen morphology, and
ontogenetic studies are required to determine the signifi -
cance of the triangular shape before and after tetrad for-
mation.
It is clear that these three species display a highly
integrated complex of adaptations to the fynbos vegeta-
tion and that nuances in ecological requirements prob-
ably account for the differences between them, but the
functional aspects of these adaptations remain unclear.
This argument applies also to all the other wahlenber-
gioid genera in the fynbos, and therefore the merging of
genera such as Theilera and the illegitimate Lightfootia
in Wahlenbergia is surely premature (Lammers 1995;
Goldblatt & Manning 2000), although Lammers (2007:
382) acknowledged that some species, currently included
in Wahlenbergia, could be given separate generic recog-
nition. From this perspective, the recognition of Rhigio-
phyllum and Siphocodon should be upheld.
From the pollen studies, and the work of Dunbar, it
would appear that there are more similarities between
the pollen of the Campanulaceae and the Cyphiaceae
s.lat. than the Lobeliaceae. The unique stylar morphol-
ogy of the Cyphiaceae suggests that this family may be
the most ancient lineage of Campanulales in Africa and
possibly derived from ancestors, which, themselves,
eventually diversifi ed in Australia as the Goodeniaceae
and Stylidiaceae. This hypothesis requires further inves-
tigation. The Cyphiaceae have unicellular stylar hairs,
which resemble those of the Campanulaceae more than
those of Lobeliaceae (Leins & Erbar 2005), and it would
be interesting to survey this character as well as second-
ary pollen presentation mechanisms in all South African
genera of the Campanulales.
The major dichotomy between the pollen of the
platycodonoids (represented in Africa and the Canary
Islands by the relict Canarina) and the wahlenbergioids/
campanu loids, suggests that this split is an ancient one
(Eddie et al. 2003) dating from the early Tertiary. Yet,
we do not know what the ancestral morphology of these
ancient African progenitors was like, but from them the
wahlenbergioids diversifi ed into several morphological
types such as herbs or shrubs. Perhaps the Mascarene
genera such as Nesocodon Thulin and Heterochaenia,
both of which recall the platycodonoids in their fl oral
morphology, most resemble the ancient forms. In south-
ern Africa, the onset of aridity, beginning in the Oli-
gocene, probably is the ultimate cause of evolutionary
diversifi cation within the wahlenbergioids, with addi-
tional factors such as geographic and ecological isolation
(especially soil types and pollinators). Shrubby types
such as Roella are particularly associated with the Medi-
terranean climate of the Cape region, whereas herba-
ceous, rosette types such as Craterocapsa would appear
to be restricted to areas with a greater moisture regime.
The relictual disjunct distribution of Craterocapsa from
eastern South Africa to the Chimanimani Mountains of
Zimbabwe may be highly signifi cant.
Taxonomic implications
One can of course attempt to analyse it, to fi t it into this system of
thought or that, but by its very nature it is bound to cause a diversion
in the neatly-fi tted jigsaw. In the end the diversion becomes the devia-
tion that wrecks the system. No wonder those who create systems fear
it like the devil.
Neil Gunn 1956 (The Atom of Delight)
Since their original discovery and description, Rhigio-
phyllum and Siphocodon were classifi ed by all southern
African workers as being close to other wahlenbergioid
genera. We now know that the two genera are more
divergent from all other wahlenbergioid taxa than was
previously thought, yet, from molecular analyses, they
are obviously still part of that nexus of southern African
Campanulaceae. However, they represent a sister lineage
separate from other South African taxa, which suggests
that they are an old, albeit highly adapted group ( 28
million years, Cupido 2008). The current classifi cation
of South African wahlenbergioids is not adequate for the
recognition of these taxa and should therefore be modi-
fi ed accordingly.
Kolakovsky (1987, 1994) recognized four subfamilies
within the Campanulaceae based largely on the nature of
carpel dehiscence and the presence or absence of an axi-
corn: Prismatocarpoideae Kolak.; Canarinoideae Kolak.;
Wahlenbergioideae (Endl.) Kolak.; and Campanuloideae.
In this treatment, the South African genera were divided
between his Prismatocarpoideae (Craterocapsa, Nama-
codon, Prismatocarpus, Roella and Treichelia Vatke)
and his Wahlenbergioideae (Heterochaenia, Microcodon,
Theilera and Wahlenbergia, plus a number of typically
platycodonoid and campanuloid genera).
Takhtajan (1997) also divided the Campanulaceae
into four subfamilies: (Cyananthoideae nom. inval.? ;
Ostrowskioideae (Fed.) Takht.; Canarinoideae Kolak.; and
Campanuloideae, giving great weight to the type of pollen
grains. He subdivided the Campanuloideae into about thir-
teen tribes, including four South African tribes: the Wahl-
enbergieae (Wahlenbergia, Berenice, Theilera, Gunillaea
Thulin, Nesocodon, Heterochaenia, and Microcodon);
Prismatocarpeae (Prismatocarpus, Namacodon, Roella,
Craterocapsa, and Treichelia); Siphocodoneae (Siphoco-
don and Rhigiophyllum); and Merciereae (Merciera). The
Bothalia 40,1 (2010) 113
problem with both of these systems is that there are too
many tribes, that each tribe is almost the equivalent of a
genus, and that it is diffi cult to get a perspective of the
major lineages within the subfamilies. Kolakovsky’s sys-
tem places far too much emphasis on the axicorn, which
is probably more useful in delimiting campanuloid taxa.
Takhtajan’s treatment of the South African genera comes
closest to our thinking but the number and boundaries of
his tribes may have to be revised.
Sonder (1865) included the four tribes Lobelieae,
Campanuleae, Cyphieae and Goodenovieae in the Cam-
panulaceae. He subsequently divided the Campanuleae
into three subtribes: Wahlenbergieae (capsule opening at
the apex; ovules many); Merciereae (stamens free; ovary
one-celled, with an incomplete septum; 4 basal ovules);
and Siphocodeae (stamens epipetalous; ovary 3-celled,
each cell with 2 ovules). Note that Sonder used the same
suffi x ‘-eae’ for his subtribal names instead of ‘-inae’. He
considered Rhigiophyllum to be a ‘doubtful genus’ and
we think he simply tagged it on at the end of his account
of the Campanuleae immediately after Siphocodon. He
probably never intended to include it in his ‘Siphoco-
deae’ but there is some ambiguity to his account (p.
597) and it would have been clearer if he had placed it
sequentially after Roella. Rhigiophyllum is certainly very
distinct from Siphocodon and, if he had meant to include
it in his Siphocodeae, he would surely not have consid-
ered it to be of doubtful status. Takhtajan (1997) placed
these two genera in his tribe Siphocodoneae Takht.,
which he recognized along with 12 other tribes in his
subfamily Campanuloideae. As far as we can determine,
Takhtajan’s Siphocodoneae was not formally validated.
Was Takhtajan swayed by Sonder’s rather ambiguous
account? Lammers (2007: 671) lists the Siphocodoninae
Sond. as a subtribe of the Wahlenbergieae Endl.
It would be tempting, given the highly divergent pol-
len morphology, to give subfamily status to Rhigiophyl-
lum and Siphocodon. However, there are a number of
other taxa that are also somewhat anomalous and do not
fi t comfortably into either the Wahlenbergioideae or the
Campanuloideae, e.g. Wahlenbergia hederacea, Feeria
Buser, Jasione L., Musschia and Campanula L. sect.
Pterophyllum Damboldt. Wahlenbergia hederacea, which
is a unique component of western European Atlantic
regions, is remote from all other wahlenbergioids. Feeria
is closer in its morphology to the wahlenbergioids,
whereas Jasione is closer to the campanuloids (Eddie et
al. 2003; Eddie unpubl.). Molecular studies also support
the closer association between Jasione and the campanu-
loids (Cosner et al. 2004). These taxa probably stem from
ancestral taxa common to both groups, what Eddie et al.
(2003) referred to as ‘transitional groups’. In the world of
classifi cation, there are always taxa that do not fi t neatly
into man-made schemes. Given the uniqueness of Rhigio-
phyllum and Siphocodon, we hereby include them in a
new tribe of the Campanulaceae as follows:
Rhigiophylleae Eddie & Cupido, tribus nov. Type:
Rhigiophyllum Hochst.
Siphocodoninae Sond. in Harv. & Sond., Flora cap-
ensis 3: 531 (1865) (as ‘Siphocodeae’). Siphocodoneae
Takht.: 409 (1997).
Fruticuli habitu et affi nitate Roellae vel Prismato-
carpi, a quibus praecipue pollinis granis applanatis et tri-
angularibus, uno poro in quoque angulo praeditis, differ-
unt; corolla longe tubulosa, staminibus inclusis, ad tubi
medium vel infra corollae orem insertis; structuris mem-
branaceis liberis intra ovarium carpella simulantibus, in
tempore maturitatis se contrahentibus, seminum marsu-
pia rugosa vel carunculata formantibus et semina conti-
nentibus dispersis; capsula dehiscente aut obturamento
supra calycis lobos amoto (Rhigiophyllum) aut operculo
infra calycis lobos circumscissili (Siphocodon).
Shrublets with the appearance of, and affi nity with,
Roella or Prismatocarpus, principally differing from
them by pollen grains that are fl attened horizontally and
triangular, with one pore at each angle; with corolla long-
tubular, with stamens included and inserted at the mid-
dle of the tube or below the mouth of the corolla; with
free membranous structures within the ovary resembling
carpels, shrinking at maturity, forming rugose or carun-
culated seed pockets and dispersed containing the seeds;
with the capsule dehiscing either by removal of a plug
above the calyx lobes (Rhigiophyllum) or by a circum-
scissile operculum below the calyx lobes (Siphocodon).
This also necessitates that we clarify the placement of
this new tribe within a suggested overall classifi cation
system of the Campanulaceae. To date, the reclassifi cation
of the Campanulaceae is still fl uid and a presentation of a
new system is inappropriate in this paper. However, we
recommend the recognition of three subfamilies within
the Campanulaceae to embrace the platycodonoids,
wahlenbergioids and campanuloids, based principally
on pollen morphology, but also supported by biogeog-
raphy. Thus, the tribe Rhigiophylleae would be included
in subfamily Wahlenbergioideae Kolak. (1987)—includ-
ing Prismatocarpoideae Kolak. (1987), comprising Wahl-
enbergia, Prismatocarpus and allied genera possessing
spherical or triangular, porate pollen and capsule dehis-
cence that is predominantly apical by valves. Their dis-
tribution primarily in the southern hemisphere, extending
marginally into the northern hemisphere in Eurasia but
poorly represented in South America.
This study has shown that what at fi rst sight appears
as novel, morphological divergences are integrated with
many other features of a plant’s morphology, ecology
and evolution, and that no single aspect can ultimately be
divorced from the plant as a whole. Because these unique
plants are so fi nely tuned to their unique environment, they
are highly vulnerable to disturbance, habitat degradation
and climate change. We still know very little about them
but we hope that their protection is assured and that further
studies of such intriguing plants will be forthcoming.
ACKNOWLEDGEMENTS
We thank the Regius Keeper and the librarians of the
Royal Botanic Garden, Edinburgh, for access to the her-
barium collections and for their help in locating numer-
ous obscure references. We are indebted to Prof. R.K.
Jansen and the University of Texas at Austin for fund-
ing that enabled us to collect many of the taxa in the
fi eld, and for facilities available to W.M.M. Eddie dur-
ing the tenure of a NSF postdoctoral scholarship. The
114 Bothalia 40,1 (2010)
Curator of the Compton Herbarium is also thanked for
facilities during the course of this study and the Western
Cape Nature Conservation Board for granting permis-
sion to collect plants. Thanks also to W.F. Chissoe of the
Samuel Roberts Noble Electron Microscopy Laboratory,
University of Oklahoma, for meticulous help with pollen
preparation and use of the scanning electron microscope.
Ian Hedge (Royal Botanic Garden, Edinburgh), Dr Mar-
tin Ingrouille (University of London) and Assoc. Prof.
Tom Lammers (University of Wisconsin, Oshkosh) com-
mented on an earlier draft and made many helpful sug-
gestions for improvement. In particular we are grateful
to Tom for helping to extract us from the nomenclatu-
ral quagmire of the Campanulaceae. Philip Oswald and
Dr Ted Oliver kindly corrected and greatly improved
our initial attempt at the Latin diagnosis, for which
Peter Bostock’s software program TRANSLAT proved
extremely helpful. We are also grateful to Dr Geoffrey
Harper (Royal Botanic Garden, Edinburgh) for his excel-
lent translations of Kolakovsky’s papers from the Rus-
sian. We would also like to thank Profs Claudia Erbar
and Peter Leins (University of Heidelberg) for their very
informative and helpful comments and for elucidating
the nature of the seed pockets.
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