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Pollen of African Spermacoce species
(Rubiaceae) Morphology and evolutionary
aspects
St even Dessein , Suzy Huysmans , Elmar Robbrecht & Erik Smet s
Published online: 05 Nov 2010.
To cite this article: St even Dessein , Suzy Huysmans , Elmar Robbrecht & Erik Smet s (2002) Pollen of
Af rican Spermacoce species (Rubiaceae) Morphology and evolut ionary aspect s, Grana, 41: 2, 69-89, DOI:
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Grana 41: 69±89, 2002
Pollen of African Spermacoce species (Rubiaceae)
Morphology and evolutionary aspects
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STEVEN DESSEIN, SUZY HUYSMANS, ELMAR ROBBRECHT & ERIK SMETS
Dessein, S., Huysmans, S., Robbrecht, E. & Smets, E. 2002. Pollen of African Spermacoce species
(Rubiaceae). Morphology and evolutionary aspects. ± Grana 41: 69±89.
Pollen morphology of 43 African species of the genus Spermacoce has been investigated by scanning
electron and light microscopy. The genus is eurypalynous, which is reected in the remarkable variation
of almost all pollen characters. The average equatorial diameter ( E) ranges from 15.8 mm to 115.5 mm.
Grains are colporate or pororate. The number of apertures varies from 3 up to more than 25. The
majority of species has apertures situated only at the equator (being zonoaperturate), but a few species
have pantoaperturate grains. The endoaperture is generally an endocingulum, often with a secondary
lolongate or lalongate thinning at the ectocolpus; endocolpi and endopores are also observed. The
sexine is usually perforate, but eutectate, foveolate, and (micro)reticulate tecta were also found.
Supratectal elements are present as granules, microspines or spines. The inner nexine surface is granular,
often with irregular grooves (endocracks). Among native African species, nine pollen types are
recognized mainly on the basis of pollen size, aperture morphology and tectum peculiarities. In two of
the pantoaperturate types, apertures are in a conguration not yet recorded for the angiosperms in
general. Some evolutionary trends are proposed that await verication by further systematic study.
Pollen morphological characters have a high taxonomic value in the genus Spermacoce. They provide
almost unique identication marks for the species, which enables sharpening of species boundaries.
Small groups of related species often share the same pollen type. The genus Borreria, previously
separated from Spermacoce on the basis of its fruit morphology only, is not supported by pollen data.
Steven Dessein, Suzy Huysmans & Erik Smets, Laborator y of Plant Systematics, Institute of Botany and
Microbiology, K.U.Leuven, Kasteelpark Arenberg 31, B-3001 Leuven; Belgium: Elmar Robbrecht,
National Botanic Garden of Belgium, Domein van Bouchout, B-1860 Meise; Belgium.
E-mail: steven.dessein@bio.kuleuven.ac.be
(Manuscript received 13 July 2001; accepted 11 April 2002)
The Spermacoce-Borreria alliance (Rubiaceae: Spermacoceae) is a large complex with a worldwide distribution in
the tropics and subtropics. The estimated number of species
varies between 150 and 250 (Verdcourt 1989), depending on
the authors. The plants typically grow in woodlands and
grasslands, and are characterized by a herbaceous habit,
mbriate stipules connected to the petioles, mostly small,
isostylous owers arranged in compact lateral and terminal
inorescences, valvate bud aestivation, uni-ovulate ovary
locules, dry capsular fruits, and presence of raphides. The
group is, along with 18 smaller genera, placed in the tribe
Spermacoceae, subfamily Rubioideae (Robbrecht 1988). A
molecular study of Andersson & Rova (1999) conrmed the
monophyly of the tribe, but the group was nested within
members of the tribe Hedyotideae, which makes the latter
paraphyletic (see also Bremer et al. 1995, Natali et al. 1995,
Bremer 1996, Bremer & Manen 2000). For this reason,
Bremer (1996 ) proposed the Spermacoceae sensu lato, including the former tribes Hedyotideae, Knoxieae and Manettieae.
In the present paper, the term Spermacoceae is used in its
more traditional, narrow sense (cf. Robbrecht 1988).
Generic delimitations within the complex have been
debated for almost two centuries. Spermacoce L. broadly
dened by some authors (e.g., Verdcourt 1975, 1976, 1983,
1989, Deb & Dutta 1984, Sivarajan et al. 1987), is divided
by others (e.g., Bacigalupo 1972, Steyermark 1972, 1974,
Bacigalupo & Cabral 1996) on the basis of peculiarities of
the fruit dehiscence. The segregated genus Borreria G.Mey.
is then characterized by having capsules with a septicidal
opening and both fruit valves dehiscent, and Spermacoce
sensu stricto by its fruits splitting into two valves, one
dehiscent and the other indehiscent (Meyer 1818). These
fruit characters are easy to observe, but no other features
seem to be correlated with it (cf. Verdcourt 1975, 1976, Deb
& Dutta 1984, Sivarajan et al. 1987). In the present article
we accept Verdcourt’s view (1975) and relegate Borreria to
the synonymy of Spermacoce.
Only few, limited studies exist on the pollen of Spermacoce.
The earlier ones were part of broader studies on the phylogeny of Rubiaceae (e.g., Bremekamp 1952, Verdcourt 1958).
All reported that pollen of Spermacoce is multi-aperturate,
but they did not fully survey the morphological variation
within the genus. More recently, pollen studies of the
American representatives of Spermacoceae demonstrated the
systematic value of pollen characters in the tribe. Pollen
characters were used to re-establish the genus Galianthe
(Cabral 1991, Pire & Cabral 1992, Pire 1997a) and to
support a new subgeneric classication for the American
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70
S. Dessein et al.
species of Psyllocarpus ( Kirkbride 1979 ) and Borreria
(Bacigalupo & Cabral 1996, Pire 1996, Cabral & Bacigalupo
1999). Pollen morphology was also used to erect the genus
Phylohydrax for the African and Madagascan Hydrophylax
species (PuV 1986). Until now, pollen of the African
Spermacoce species was never investigated.
The present study aims (1) to survey the pollen morphology of the African representatives of Spermacoce, (2) to
discuss its signicance in the taxonomy of the genus, and (3)
to formulate a hypothesis for the evolution of pollen characters within the genus. The project is part of the ongoing
research of the rst author to document the biodiversity of
Spermacoce in Africa.
MATERIAL AND METHODS
This study is based on herbarium material from BR, K, WAG and
ZT ( Table I ). Pollen of 92 specimens from 43 species were investigated (Table I). For the remaining African species (ca. 25 ) owering
material in the above mentioned herbaria was not suYcient to carry
out palynological research. Due to the problematic delimitation of
several species of Spermacoce, we only selected specimens that fully
correspond with the type specimen (if seen) or with the original
descriptions; additional comments on some problematic species/
specimens are provided ( Table I ). Species introduced to Africa are
marked with an asterisk; the table also indicates the specimens used
for the illustrations.
Mature ower buds were rehydrated in an Ageponâ (Agfa
Gevaert) solution (1:200), and dissected using a stereomicroscope.
Pollen was acetolysed for 9 minutes in a heating block at 90ßC.
Pollen grains for SEM studies were suspended in ethanol (70%),
pipetted onto specimen stubs, air-dried and coated with gold with a
SPI-MODULETM sputter coater. Observations were made under
a Jeol JSM-6400 SEM. Grains for LM studies were mounted in
Kaiser’s glycerin jelly. The slides were observed using a Leitz Dialux
20 with a Ö100 oil immersion or Ö40 objective lens. Equatorial
diameter ( E) was measured under LM in at least ten mature pollen
grains (magnication 1000 ). We were not able to obtain accurate
measurements for the polar axis (P) under LM, since most grains
are suboblate. All other measurements were made on SEM-graphs.
To express the relative length of the colpi, we used the length
colpi/polar axis rate multiplied by 100 (= LC/P). Broken pollen
grains were obtained by shaking a pollen and glass bead suspension
as described by Huysmans et al. (1994 ). Terminology follows Punt
et al. (1999) .
RESULTS
Pollen characters
Pollen morphology of African Spermacoce species is remarkably heterogeneous. In all pollen characters, the group reveals
a variation that is usually only observed at higher systematic
levels. This diversity is described and discussed below for
the diVerent diagnostic pollen characters and is illustrated
by SEM-graphs. Detailed information at species level is
presented in Table II.
Size
Pollen grain size of African Spermacoce species ranges from
small to large, the average equatorial diameter (E ) varying
from 15.8 mm in Spermacoce mauritiana to 115.5 mm in S.
ivorensis. The size variability within a single specimen is
considerable (often exceeding 10%); within a species the
Grana 41 (2002)
variation in E-averages frequently exceeds 20%. Sometimes,
this variation can be explained in terms of intraspecic
variation, as is the case for Spermacoce phyteumoide s: var.
phyteumoides and var. caerulea have smaller pollen grains
than ``var. longituba’’. Verdcourt informally recognized the
latter variety on the herbarium sheets for its longer corolla
tube. In general there is a positive correlation in the study
group between size of the corolla tube and pollen size
(Fig. 1 A; r2 = 0.43; p<0.01): larger owers tend to produce
larger pollen grains. This correlation is also found in many
other groups and may be correlated with diVerences in
nutrition supply (Muller 1979).
In the present study, however, the correlation between
ower and pollen grain size is not strict. Flowers with a
corolla tube smaller than 3 mm have pollen grains ranging
from ca. 15 mm up to 60 mm, while medium sized owers
(tube ca. 7 mm) show pollen grains between 55 mm and
105 mm. Moreover, very variable species, such as Spermacoce
subvulgata, have corolla tubes ranging from 3 to 6 mm, but
no correlated diVerences are observed in the size of their
pollen. Probably, the true correlation lies in the pollen vector
size, rather than in the size of the owers. Although only a
few studies (cf. Muller 1979) have demonstrated that diVerent
pollen vectors prefer diVerent ranges of pollen size, it seems
likely that this partly explains the considerable interspecic
pollen size variation.
Another hypothesis to explain the pollen size variation is
the level of polyploidy. Higher levels of polyploidy may
express itself directly in a larger pollen size (Muller 1979).
Herbaceous Rubiaceae are known to have high levels of
polyploidy (cf. Lewis 1965, Kiehn 1986). Kiehn (1986, 1995 )
surveyed the chromosome numbers of the Rubiaceae; for the
Spermacoceae, the basic chromosome number is predominantly 14, and tetraploidy and hexaploidy originated several
times within the tribe ( Kiehn 1986). Moreover, diVerent
ploidy levels are recorded for specimens of the same species;
hence, giving support for the hypothesis that some of the
intraspecic pollen size variation is caused by diVerences in
ploidy levels.
In many genera of Rubiaceae, diVerences in pollen size
may be explained by heterostyly (Huysmans et al. 1998,
Dessein et al. 2000). In general, the brevistylous form has
larger pollen grains than the longistylous morph (cf. Ganders
1979). African Spermacoce species, however, are invariably
homostylous, hence this hypothesis can not explain the
intraspecic variation observed.
Shape
P/E. ± In equatorial view, pollen shape is described by the
P/E rate. In the study group, subprolate (P/E is 1.14±1.33;
Fig. 10), spheroidal (P/E is 0.88±1.14; Figs. 11±14) as well
as suboblate (P/E is 0.75±0.88; Figs. 15±16 ) and oblate (P/E
is 0.50 ±0.75; Fig. 17 ) pollen is found. The spheroidal condition can be further divided into oblate spheroidal (P/E is
0.88 ±1) and prolate spheroidal (P/E is 1±1.14). There is a
negative correlation between the equatorial diameter and the
P/E rate (Fig. 1 B; r2 = 0.29; p<0.01). The smaller the pollen
grains the higher the P/E value. Spheroidal pollen grains,
however, can be small as well as large.
Pollen of African Spermacoce species (Rubiaceae)
71
Table I. Specimens examined including type- and gure references.
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1
Spermacoce articularis L.f.: treated as a synonym of Spermacoce hispida L. by Verdcourt (1976 ) in FTEA and many others, but recognized
again by Sivarajan et al. (1987). Native to Asia, but introduced in tropical Africa.
2
Cited in FTEA as Spermacoce hispida L. by Verdcourt (1976).
3
Spermacoce assurgens Ruiz & Pav.: There is much confusion about the identity of this species. It was treated under S. laevis Lam. by
Verdcourt (1976 ) in FTEA and many others. Recently, Cabral & Bacigalupo (1999 ) placed S. assurgens in synonymy to Spermacoce remota
Lam., which they transferred to Borreria subgenus Borreria section Borreria, series Laeves. Whether this is correct, needs conrmation; the
pollen grains of the specimen studied here do not correspond with the pollen grains of S. remota (Pire 1996, treated under B. laevis
(Lam.) Griseb.).
4
Spermacoce mauritiana Osia Gideon: the delimitation of this species has been debated for a long time, and it was often confused with
Spermacoce ocymoides Burm.f. Verdcourt (1983 ) ± based on unpublished material of Gideon and Fosberg ± stated that ``the suggestedly
cosmopolitan S. ocymoides is actually a complex of species distinguishable mainly on seed characters and published Gideon’s name
Spermacoce mauritianta (a substitute name for Borreria repens DC.) for the form with two calyx lobes’’. Cabral & Bacigalupo (1996),
however, accept ``Borreria ocymoides as one variable species until more African and Asiatic specimens can be studied’’. The specimens
investigated here are provided with two sepals (as all African species seen by the rst author).
5
The specimen investigated was labeled by Verdcourt as Spermacoce phyteumoides var. longituba . This name, however, is still unpublished.
* Species introduced to Africa.
Taxon
Collection
Country
Herb.
Type
Figure
Spermacoce annua Verdc.
*S. articularis L.f.1 , 2
S. arvensis (Hiern) Good
Mutimushi 3356
Milne-Redhead & Taylor 7522
Bingham 8946
Pope, R-Smith & Goyder 2226
Bidgood, Monasunki & Vollesen 1062
Faulkner 943
Bidgood, Mbago & Vollesen 2528
Richards 12162
Vanden Berghen 6674
Zambia
Tanzania
Zambia
Zambia
Tanzania
Tanzania
Tanzania
Tanzania
Senegal
K
BR
K
K
BR
BR
K
BR
BR
6
15
14
Fig. 25
Vanden Berghen 8522
Thomas 2731
Adam 12589
Berhaut 2933
Leeuwenberg & Beek 10375
Leippert 5071
Lisowski B-1172
Pawek 13957
Skarpe S-444
Bidgood, Mbago & Vollesen 2695
Senegal
Sierra Leone
Guinea
Senegal
Cameroon
Kenya
Tchad
Malawi
Botswana
Tanzania
BR
K
BR
BR
BR
BR
BR
BR
K
BR
15
17
14
Fig. 41
Fig. 44
Figs. 8, 17, 20, 46,
49
Lejeune 197
Chapman 272
Troupin 14994
Pereira, Sarmento & Marques 1829
Lewalle 1694
Saintenoy 162
de Wilde & de Wilde-Duyfjes 3091
D.R. Congo
Malawi
Rwanda
Mozambique
Burundi
Burundi
Cameroon
BR
BR
BR
BR
BR
BR
BR
12
Figs. 51-52
Geerling & Bokdam 984
Dalziel 212
Faulkner 2168
Drummond & Hemsley 3632
Lejoly 85/314
Homble 796
Schaijes 1467
Schaijes 1960
Duvigneaud & Timperman B-2627
Quarre 1957
Hess-Wyss 52/584
Bos, van der Laan & Nzabi 10676
Geerling & Bokdam 1701
Schlechter 12123
Lisowski 56863
Hepper & Maley 7760
Scott s.n.
McClounie 84
Ivory Coast
Nigeria
Tanzania
Tanzania
Burkina Faso
D.R. Congo
D.R. Congo
D.R. Congo
D.R. Congo
D.R. Congo
Angola
Gabon
Ivory Coast
Mozambique
D.R. Congo
Ivory Coast
Malawi
Zambia
BR
K
BR
BR
BR
BR
BR
BR
BR
BR
ZT
WAG
BR
BR
BR
BR
K
K
11
17
Fig. 12
*S. assurgens Ruiz & Pav. 3
S. azurea Verdc.
S. bambusicola (Berhaut)
J.-P.Lebrun & Stork
S. chaetocephala DC.
S. congensis (Bremek.) Verdc.
S. deserti N.E.Br.
S. dibrachiata Oliv.
S. lifolia (Schumach. & Thonn.)
J.-P.Lebrun & Stork
S. liformis Hiern
S. lituba ( K.Schum.) Verdc.
S. hepperana Verdc.
S. hockii (De Wild.) Dessein
S. huillensis (Hiern) Good
S. intricans (Hepper) H.M.Burkill
S. ivorensis Govaerts
S. kirkii (Hiern) Verdc.
*S. latifolia Aubl.
S. latituba ( K.Schum.) Verdc.
Fig. 7
11
14
Figs. 15, 27, 37
16
Fig. 42
11
Figs. 6, 13
11
14
Fig. 43
15
?17
16
15
2
Fig. 21
Figs. 19, 32
15
Figs. 28, 39
Grana 41 (2002)
72
S. Dessein et al.
Table I. (Continued).
Taxon
Collection
Country
Herb.
Type
S. mauritiana Osia Gideon4
Evrard 157
Quarre 7867B
Vanden Berghen 9164
Polhill & Paulo 1419
Thulin & Mhoro 3128
de Wilde 992
Lely 522
Simpson 7325
King 3
D.R. Congo
D.R. Congo
Senegal
Tanzania
Tanzania
Ivory Coast
Nigeria
Sudan
Zambia
BR
BR
BR
BR
WAG
BR
K
K
BR
1
Richards 8431
Tanzania
K
Fig. 38
Carter, Abdullah & Newton 2582
Tanzania
K
Fig. 22
Ngoundai 250
Huxley 84
Malaisse 9691
Schmitz 7228
Homble 930
Troupin 1407
Berhaut 435
Robbrecht & Leman 3377
Vanden Berghen 6197
Leeuwenberg 2323
van den Bossche 3473SerI
Polhill & Paulo 2347
Tanner 659
de Wilde 8518
van Eijnatten 2077
Reekmans 10237
Bredo 1487
Michel 3058
Drake 92
Vanden Berghen 9184
Vanden Berghen 6119
Milne-Redhead 4338
Malaisse & Robbrecht 1996
Bamps, Martins & Maia 4175
Lewalle 5606
Tanzania
Tanzania
D.R. Congo
D.R. Congo
D.R. Congo
D.R. Congo
Senegal
Niger
Senegal
Ivory Coast
Togo
Tanzania
Tanzania
Cameroon
Nigeria
Burundi
D.R. Congo
D.R. Congo
Sudan
Senegal
Senegal
Zambia
R.D. Congo
Angola
Burundi
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
BR
K
BR
BR
BR
15
Fig. 47
Lisowski 10476
Bredo 2262
Lisowski, Malaisse & Symoens 4139
Schlieben 2321
Milne-Redhead & Taylor 8821
D.R. Congo
D.R. Congo
D.R. Congo
Tanzania
Tanzania
BR
BR
BR
BR
BR
15
Fig. 5
Humblot 599
Fay 3445
Gossweiler 2347
Pearson 2772
Hess-Wyss 52/1798
Chevalier 1026
Dessein 24
Madagascar
R.C. Africa
Angola
Angola
Angola
Sudan
Cultivated at BR
K
BR
BR
K
ZT
BR
BR
S. natalensis Hochst.
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S. octodon (Hepper) Hakki
S. phyteuma Schweinf. ex Hiern
S. phyteumoides Verdc. var.
phyteumoides
S. phyteumoides Verdc. var.
caerulea Verdc.
S. phyteumoides Verdc. ``var.
longituba ’’5
S. princeae ( K.Schum.) Verdc.
S. pusilla Wall.
S. quadrisulcata (Bremek.) Verdc.
S. radiata (DC.) Hiern
S. ruelliae DC.
S. senensis ( Klotzsch) Hiern
S. spermacocina ( K.Schum.)
Bridson & PuV
S. sphaerostigma (A.Rich.) Oliv.
S. stachydea DC.
S. stipularis Dessein
S. subvulgata ( K.Schum.)
J.G.Garcia
S. taylorii Verdc.
*S. tenuior L.
S. tenuissima Hiern
S. terminaliora Good.
S. thymoidea (Hiern) Verdc.
*S. verticillata L.
Amb. ± In polar view, the pollen outline is usually circular
and often lobed due to the longer columellae towards the
centers of the mesocolpia or due to the thicker nexine around
the apertures (cf. below). Only Spermacoce natalensis and S.
mauritiana have a triangular or quadrangular polar outline
(Figs. 2±3).
Grana 41 (2002)
1
Figure
Figs. 3, 10, 18, 35
Fig. 2
12
6
14
17
Figs. 23, 36
Figs. 9, 26, 33±34
Figs. 16, 45, 50
Fig. 40
11
11
11
17
15
Fig. 14
?17
17
17
Figs. 29±30
14
1
12
13
13
3
Figs. 48, 53±54
Figs. 57±58
Figs. 24, 55±56
Figs. 4, 11, 31
Apertures
Number. ± The number of colpi ranges from 3±4 in
Spermacoce mauritiana (Figs. 2±3) to 16±21 in S. dibrachiata
(Fig. 8). The pantopororate species have up to 30 pores. The
higher the number of colpi, the higher the intraspecic
variation observed. There is a weak positive correlation
Pollen of African Spermacoce species (Rubiaceae)
73
Table II. Some variable pollen morphologica l characters for each species studied.
Species are arranged by pollen type as discussed in the text. (x): number of specimens studied. Shape as seen in equatorial view: O = oblate; SO = suboblate;
OS= oblate spheroidal; S = spheroidal; PS = prolate-spheroidal; SP = subprolate. Number of apertures: values between brackets were not found in all specimens
investigated . Aperture type: PC = pantocolporate; PP = pantopororate; ZC= zonocolporate. Peculiarities : CM= colpus membrane; EP = equatorial plane. Types
in Endo-column are discussed in the text.
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Apertures
Wall ornamentation
Type Species
Size
Shape
Number
Type Endo Peculiaritie s
Sexine
Nexine
1
S. mauritiana (3)
14-(15.8)-1 8
PS
3-4
ZC
II
1
S. natalensis (2)
14-(16.5)-1 9
SP
3-4
ZC
II
nely granular, endocracks
indistinct
nely granular, endocracks
indistinct or absent
1
S. tenuior (1)*
15-(16.1)-1 7
PS-SP
6-8
ZC
II
perforate, margo of granules/
microspines
eutectat e at apocolpium,
perforate at mesocolpium,
margo of granules
perforate, margo of granules/
microspines
2
S. latifolia (2)*
44-(48.3)-5 0
SO-OS
(7)-9-(11 ) ZC
V
perforate, granulate
granular, broadÔdistinct
endocracks
3
S. verticillata (2)* 23-(28.0)-3 0
OS
(6-9 )
ZC
IV
perforate, granulate
granular, narrowÔdistinct
endocracks
6
S. annua (1)
62-(66.5)-7 4
S
ca. 30
PP
VI
6
S. phyteuma (1)
80-(87.0)-9 0
S
ca. 24
PP
VI
microreticulate to reticulate,
microechinate
perforate-microreticulate ,
microechinate
nely granular, no
endocracks
nely granular, no
endocracks
11
S. assurgens (1)*
35-(36.8)-3 8
SO-OS
8-10
ZC
II
11
38-(44.7)-5 2
SO-OS
(9)-11
ZC
II
11
S. chaetocephala
(4)
S. liformis (1)
30-(32.0)-3 4
S
9-10
ZC
II
11
S. hepperana (1)
42-(46.5)-5 2
SO-OS
9-11
ZC
II
11
11
35-(37.0)-3 9
37-(42.3)-4 5
SO-OS
SO-OS
8-10
(10-13 )
ZC
ZC
II
II
perforate, granulate
perforate, granulate
11
S. pusilla (1)
S. quadrisulcata
(3)
S. radiata (3)
29-(36.2)-4 4
OS
(9)-10(13)
ZC
II
perforate, granulate
12
S. lifolia (2)
50-(56.6)-6 4
S
ca. 15
PC
III
12
S. octodon (2)
37-(40.9)-4 5
S
ca. 14
PC
III
12
S. tenuissima (1)
47-(54.1)-5 7
S
ca. 15
PC
III
13
S. terminaliora
(1)
52-(54.4)-5 7
S
ca. 24
PC
III
13
S. thymoidea (2)
50-(56.9)-6 3
S
24-25
PC
III
14
S. arvensis (3)
75-(81)-8 6
O
(16)-17(18)
ZC
14
S. azurea (2)
62-(69.6)-7 6
O-SO
(13)-15(16)
14
S. dibrachiata (7)
71-(84.8)-9 6
O-SO
14
S. hockii (4)
67-(72.4)-8 2
14
S. phyteumoides
65-(66.7)-6 9
var. phyteumoides
(1)
operculum
present
operculum
present
endocingulum perforate, granulateindistinct
microechinate
perforate, granulate
columellae
slightly
longer in EP
columellae
slightly
longer in EP
colpi
arranged in a
loop
colpi
arranged in a
loop
colpi
arranged in a
loop
perforate, granulate
perforate, granulate
nely granular, endocracks
indistinct or absent
granular, narrowÔdistinct
endocracks
granular, indistinct
endocracks
granular, narrow irregular
endocracks
nely granular, narrow
distinct or obscure
endocracks
?
granular, narrow indistinct
endocracks
granular, narrow indistinct
endocracks
perforate, granulate to
microechinate
granular, narrow indistinct
endocracks
perforate, granulate to
microechinate
granular, narrow distinct or
obscure endocracks
perforate, granulate to
microechinate
granular, narrowÔdistinct
endocracks
colpi
perforate, microechinate
arranged in a
spiral pattern
CM granular, perforate, microechinate
colpi
arranged in a
spiral pattern
granular, numerous irregular
endocracks
I
columellae
distinctly
longer in EP
?
ZC
I
columellae
distinctly
longer in EP
(16-21 )
ZC
I
columellae
distinctly
longer in EP
SO
13-(15 )
ZC
I
columellae
longer in EP
O-SO
14-16
ZC
I
columellae
distinctly
longer in EP
perforate to perforatereticulate in mesocolpia,
microechinate, surface
undulating
perforate to perforatereticulate in mesocolpia,
microechinate, surface
undulating
perforate to perforatereticulate in mesocolpia,
microechinate, surface
undulating
perforate to perforatereticulate in mesocolpia,
microechinate, surface
undulating
perforate to perforatereticulate in mesocolpia,
microechinate, surface
undulating
granular, numerous irregular
endocracks
nely granular, broad
distinct endocracks
nely granular, broadÔdeep
endocracks
nely granular, narrow
distinct endocracks
nely granular, broadÔdeep
endocracks
Grana 41 (2002)
74
S. Dessein et al.
Table II. (Continued).
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Apertures
Wall ornamentation
Type Species
Size
Shape
Number
Type Endo Peculiaritie s
Sexine
Nexine
14
S. phyteumoides
var. caerulea (1)
68-(70.7)-7 3
O-SO
14-15
ZC
I
columellae
distinctly
longer in EP
nely granular, broad
undeep endocracks
14
S. phyteumoides
``var. longituba ’’
(1)
75-(83.2)-9 0
SO
13-14
ZC
I
columellae
somewhat
longer in EP
14
S. stipularis (3)
75-(83.0)-9 2
O-SO
(14)-15(17)
ZC
I
columellae
distinctly
longer in EP
perforate to perforatereticulate in mesocolpia,
microechinate, surface
undulating
perforate to perforatereticulate in mesocolpia,
microechinate, surface
undulating
perforate-microreticulate ,
microechinate
?15
S. articularis (1)* 72-(76.8)-8 2
SO
12-14
ZC
I/II
15
S. congensis (1)
95-(99.0)-10 5
SO
12-14
ZC
II
15
S. huillensis (2)
78-(80.0)-8 2
SO-OS
9-11
ZC
?
15
S. kirkii (1)
88-(97.0)-10 9
SO-OS
10-11
ZC
?
15
S. latituba (2)
88-(99.2)-11 0
SO
(10)-12(13)
ZC
I
15
S. senensis (2)
75-(80.0)-8 4
SO-OS
11
ZC
II
15
S. subvulgata (5)
73-(86.6)-9 4
SO-OS
10-(12 )
ZC
I/II
15
S. taylorii (1)
100-(105.3)-11 0
SO
10-12
ZC
II
CM granular; perforate, microechinate
colpiÔloxocolporate,
nexine
slightly
thicker
around
ectoaperture
microreticulate to reticulate,
microechinate
nexine
perforate, microechinate
slightly
thicker
around
ectoaperture
CM granular; perforate-microreticulate ,
nexine
microechinate to echinate
thicker
around
ectoaperture
CM granular; perforate-microreticulate ,
nexine
microechinate to echinate
thicker
around
ectoaperture
CM granular; perforate-microreticulate ,
nexine
microechinate
thicker
around
ectoaperture
CM granular; perforate-microreticulate ,
nexine
microechinate
thicker
around
ectoaperture
nexine
Microreticulat e to reticulate,
thicker
microechinate
around
ectoaperture
16
S. bambusicola (4) 74-(90.0)-10 5
O-SO
(13)-16
ZC
II
columellae
longer in EP
16
S. ivorensis (1)
105-(115.5)-12 5
OS
16-18
ZC
?
columellae
longer in EP
17
S. deserti (1)
58-(62.0)-6 8
SO
11-13
ZC
II
17
S. lituba (2)
77-(81.2)-8 7
SO-OS
12-(14 )
ZC
?
?17
S. intricans (1)
70-(73.2)-7 6
SO
9-10
ZC
?
17
S. princeae (2)
63-(71.9)-8 7
SO-OS
12-14
ZC
II
17
S. ruelliae (2)
74-(79.1)-9 0
SO-OS
ZC
II
?17
S. spermacocina
(2)
64-(70.1)-7 7
OS
(13)-15(16)
8-9
ZC
II
17
S. sphaerostigma
(4)
S. stachydea (2)
82-(91.0)-10 3
SO
11-(14 )
ZC
II
72-(81.7)-9 1
SO-OS
(12)-13(15)
ZC
II
columellae
longer in EP
columellae
longer in EP
columellae
slightly
longer in EP
columellae
longer in EP
columellae
longer in EP
columellae
slightly
longer in EP
columellae
longer in EP
columellae
longer in EP
17
Grana 41 (2002)
nely granular, broad
undeep endocracks
granular, broad distinct
endocracks
nely granular, indistinct
endocracks
granular, indistinct
endocracks
?
?
granular, narrow deep
endocracks
granular, indistinct
endocracks
granular, narrow indistinct
endocracks
granular, narrow indistinct
endocracks
perforate-foveolate , margins
of perforations bordered,
echinate
perforate, margins of
perforations bordered,
echinate
nely granular, very broad
distinct or obscure
endocracks
?
perforate, granulate to
microechinate
perforate, microechinate to
echinate
perforate, granulate to
microechinate
granular, narrowÔdistinct
endocracks
?
?
perforate-microreticulate ,
granulate to microechinate
perforate-microreticulate ,
(micro)echinate
perforate, granulate to
microechinate
nely granular, narrow deep
endocracks
granular, broad distinct
endocracks
nely granular, indistinct
endocracks
perforate, microechinate to
echinate
perforate, (micro)echinate
granular, no endocracks
granular, narrow distinct
endocracks
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Pollen of African Spermacoce species (Rubiaceae)
75
Fig. 1. Correlation analyzes between diVerent pollen and ower characters. (A) Correlation between corolla tube size and pollen size (r2 =
0.43; p<0.01); S. ivorensis was excluded because of its exceptional long corolla tube. (B) Correlation between P/E index and pollen grain
size (r2 = 0.29; p<0.01) . (C ) Correlation between number of apertures and pollen size (r2 = 0.14; p<0.01) . (D) Correlation between number
of apertures and pollen size with exclusion of the pantoaperturate species (r2 = 0.43; p<0.01).
between pollen size and number of apertures (Fig. 1 C; r2 =
0.14; p<0.01). However, the pantoaperturate species have
many more apertures than can be expected from their size.
This is not surprising if we realize that the surface where the
apertures can originate is much larger than for equally sized
zonoaperturate species. Disregarding the pantoaperturate
species, the positive correlation between number of apertures
and pollen size is strong (Fig. 1 D; r2 = 0.43; p<0.01 ).
This multi-aperturate condition is apomorphic within the
family Rubiaceae, the 3-colporate pollen type being plesiomorphic (cf. Robbrecht 1988). Other genera of the tribe
Spermacoceae also have multi-aperturate grains (Bremekamp
1952, Verdcourt 1958, Kirkbride 1979, Pire & Cabral 1992,
Pire 1997 a, b), but it is rarely found in other Rubiaceae
except in the tribe Rubieae (Bremekamp 1952). In this tribe,
however, the number of colpi is less variable and mostly
xed at 6 to 8 (Huysmans, pers. com.).
Type. ± Apertures of Spermacoce are almost always compound, i.e. built up by two or more components that are
situated in more than one layer of the pollen wall. In the
species studied the apertures usually consist of an ectocolpus
and an endocingulum (e.g., S. dibrachiata). In Spermacoce
verticillata and S. latifolia the endoaperture is a colpus. Both
species, however, are most probably introduced from
America. Spermacoce annua and S. phyteuma are characterized by ecto- and endopores.
Position. ± In most species, the apertures are ordered along
the equator (zonoaperturate; Figs. 10±17), Spermacoce phyteuma and S. annua are pantoaperturate, the ectopores being
evenly spread over the pollen surface (Fig. 9). Pire (1996:
422) noted in some Borreria species ``a tendency of the
apertures to drift away from the equatorial plane; the apertural plane appears as suVering a torsion due to the presence
of one or two pairs of convergent colpi’’. We clearly observed
such loxocolporate colpi in Spermacoce articularis; in other
species, e.g., S. chaetocephala, it was only sporadically
observed.
Two remarkable new colpi arrangements were also
observed. The rst type, with the colpi arranged in a looplike pattern, similar to the line on a tennis ball, is found
in Spermacoce lifolia, S. octodon, and S. tenuissima
(Figs. 51±52 ). The second type, where the short colpi are
arranged in a spiral pattern (Figs. 55±56 ), characterizes
Spermacoce terminaliora and S. thymoidea. To our knowledge these two pollen types have not been previously
observed in angiosperms. The second type can be considered
as an intermediate form between zonoaperturate and pantoporate grains. An in-depth morphological and ontogenetic
study is needed to further clarify these remarkable pollen
types.
Ectoaperture. ± As mentioned above, the ectoaperture is a
colpus in most species (Figs. 18±24). The length of the colpi
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S. Dessein et al.
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76
Figs. 2±9. Polar views of Spermacoce pollen grains.
(2) 3-colporate grain, slightly triangular in outline, tectum eutectate and psilate (S. natalensis).
(3) 4-colporate grain, sub-quadrangular in outline (S. natalensis).
(4) 7-colporate grain, tectum perforate (S. verticillata).
(5) 10-colporate grain, notice the elevation of the sexine around the ectoapertures (arrows), tectum microreticulate (S. taylorii ).
(6) 11-colporate grain, columellae longer in the equatorial plane, tectum perforate (S. lituba).
(7) 13-colporate grain, columellae longer in equatorial plane, tectum perforate-microreticulate (S. arvensis).
(8) 19-colporate grain, columellae longer in equatorial plane, tectum perforate (S. dibrachiata).
(9) pantopororate grain with ca. 24 apertures, tectum perforate-microreticulate and microechinate (S. phyteuma).
Grana 41 (2002)
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Pollen of African Spermacoce species (Rubiaceae)
Figs. 10±17. Equatorial views of Spermacoce pollen grains.
(10) grain subprolate, margo of granules around ectoaperture (S. natalensis).
(11) grain prolate-spheroidal (S. verticillata).
(12) grain spheroidal, columellae in equatorial plane slightly longer (S. liformis).
(13) grain suboblate, columellae longer in equatorial plane (S. lituba).
(14) grain oblate-spheroidal, nexine thickened around ectoapertures forming a distinct margo, colpus membrane beset with large sexine
particles (S. senensis).
(15) grain suboblate, columellae longer in equatorial plane (S. azurea).
(16) grain suboblate, columellae longer in equatorial plane, margins of colpi beset with microspines (S. phyteumoides).
(17) oblate grain, columellae longer in equatorial plane, margins of colpi beset with microspines (S. dibrachiata).
Grana 41 (2002)
S. Dessein et al.
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78
Figs. 18±26. Morphology of ectoapertures of Spermacoce pollen grains.
(18) slit-like colpus with margo of granules (S. natalensis).
(19) slit-like colpus, sexine undiVerentiated (S. latifolia).
(20) slit-like colpus, margins beset with microspines, columellae longer in equatorial plane (S. dibrachiata).
(21) colpus with margo of thickened nexine, colpus membrane beset with sexine particles (S. kirkii ).
(22) slit like apertures with columellae slightly elongated in mesocolpium (S. phyteumoides).
(23) detail of short colpus with margins beset with microspines (S. octodon).
(24) short, spool-shaped aperture, colpus membrane beset with sexine particles (S. thymoidea).
(25) three pores with operculum (S. annua).
(26) pore with operculum of sexine particles (S. phyteuma).
Grana 41 (2002)
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Pollen of African Spermacoce species (Rubiaceae)
compared with the polar axis (LC/P) ranges from 6 in
Spermacoce terminaliora to 62 in S. tenuior. The colpi are
often slit-like (Figs. 18±21), but sometimes more widened
(Fig. 24 ). In the latter case, there is often a gap in the colpus
membrane where the ecto- and endoapertures overlap. If
present, the colpus membrane is beset with large cubicshaped elements. The margins of the ectocolpus are often
beset with microspines (Figs. 20, 23 ). Sometimes, the exine
around the colpi is diVerentiated (Figs. 18, 20±22). Most
commonly, the columellae are longer in the equatorial zone,
but a thicker nexine around the apertures and the presence
of granules around the colpi (Fig. 18 ) were also observed.
These features are further discussed below.
The pantopororate species have pores up to 4 mm in
diameter (Figs. 25±26). An operculum that covers the whole
pore is present. In Spermacoce phyteuma it appears as an
aggregate of angular, sexinous elements intermingled with
smaller particles (Fig. 26); in S. annua it is made up of a
granular aggregate that bears a central spine (Fig. 25).
Endoaperture. ± The endoaperture is mostly an endocingulum, a ring-shaped endoaperture lying at the equatorial plane
(Figs. 27, 29 ). The width of the endocingulum ranges from
1/3 to 2/3 of the length of the ectocolpi and often there are
two triangular extensions (horns) in each mesocolpium. The
inner surface is smooth or nely granular. Within the endocingulum, there is an additional thinning of the nexine at the
ectocolpi. These thinnings are lalongate (Figs. 29±30) or
lolongate (Figs. 27±28 ). In the former case, the thinning is
oval- or diamond-shaped, and in the cut-aways, the surface
is granular; in the latter case, the nexine abruptly declines
near the ectocolpus and the surface becomes rough.
Sometimes, this thinning is bordered by a granular thickening
of the nexine within the endocingulum.
In Spermacoce princeae, the endoaperture is not always
continuous, the structure being disrupted by endocolpi that
are not laterally fused. This transition between endocolpi
and endocingulum has already been observed in other
Rubiaceae (Dessein et al. 2000).
In the species with a loop-like colpus arrangement, a
continuous endoaperture connecting the ectocolpi is observed
(Figs. 53±54 ). It cannot be named an endocingulum, since
it is not situated at the equatorial plane. In each mesocolpium,
two broad extensions are continuous with the pattern of
endocracks. An additional, diamond-shaped thinning within
this endopattern is present at the ectocolpus. In the cutaways a granular layer becomes visible. An equally complex
endopattern is found in Spermacoce thymoidea and S. terminaliora (Figs. 57±58 ), where the ca. 24 colpi are interconnected by an irregular pattern of nexine thinnings: between
two adjacent colpi a V-shaped or straight thinning of the
nexine is present, with a triangular extension on one or both
sides. A second, asymmetrical endocolpus perpendicular to
the rst one can be present, often with branching tips.
Around the ectocolpus, there is an oval thinning, revealing
a perforated, granular layer.
The endopores of Spermacoce phyteuma and S. annua are
not distinct. In Spermacoce annua, it is only visible as a
radiating pattern of ne endocracks within the inner surface
of the nexine surrounding the ectopore; in S. phyteuma
79
(Figs. 33±34 ), the surface of the nexine enclosing the ectopore
is pitted and coarser than the surrounding nexine.
The lalongate endocolpus of Spermacoce verticillata is
bordered by two islands of thickened nexine but the ends
are vaguely delimited and more or less continuous with the
endocracks (Fig. 31). In Spermacoce latifolia, an indistinct
lolongate endocolpus is present (Fig. 32).
In conclusion six types of endoapertures can be
distinguished:
Type I
endocingulum with additional lolongate thinnings
(Figs. 27, 28 )
Type II endocingulum with additional lalongate thinnings
(Figs. 29, 30 )
Type III endopattern comprising an irregular pattern of
nexine thinnings between the ectocolpi (Figs. 53,
54, 57, 58)
Type IV lalongate endocolpus (Fig. 31)
Type V lolongate endocolpus (Fig. 32 )
Type VI endopore (Figs. 33, 34 )
Sexine ornamentation
The variation in sexine patterns within Spermacoce is considerable. The majority of species, however, have a perforated
tectum. Perforation size ranges from 0.1 mm to 1 mm, and
perforation density is species dependent (Figs. 36±40 ). In
some species, small, circular perforations are intermingled
with larger ones. In other species (e.g., S. latituba), there is
a continuous transition into microreticulate tecta (Fig.
40). This character state is indicated as ``perforatemicroreticulate’’ in Table II. A true microreticulate to reticulate tectum (muri narrower than lumina; Fig. 41 ) only occurs
in Spermacoce annua, S. congensis, and S. taylorii. The
tectum of Spermacoce bambusicola tends to be foveolate
(Fig. 42). In this species and in Spermacoce ivorensis the
margins of the perforations are distinctly thickened.
There is often a considerable diVerence between the sexine
pattern observed at the mesocolpium and at the apocolpium.
In Spermacoce natalensis, for example, the tectum is eutectate
at the apocolpium and perforate at the mesocolpium. In
Spermacoce dibrachiata the perforations are more elongated
and much larger at the mesocolpium than at the apocolpium,
the larger perforations being intermingled with smaller ones.
The sexine pattern in which we have large lumina (often
exceeding 1 mm) intermingled with small perforations with
muri broader and smaller than the enclosed lumina is termed
perforate-reticulate in Table II (cf. mesocolpia of Figs.
15±17). We preferred not to use the term heterobrochate
because it refers to a true reticulate pattern (Punt et al.
1999), which is not the case here. In a number of species
(e.g., S. azurea, S. dibrachiata) the tectum is undulating in
the apocolpium (Fig. 38).
The tectum is always beset with supratectal elements,
except for Spermacoce natalensis, S. mauritiana, and S.
tenuior where the apocolpium is smooth or slightly scabrate
(Fig. 35). The supratectal elements can be granules, microspines or spines. They are scattered over the pollen surface,
or more rarely restricted to the zone around the apertures to
form a margo of granules or microspines (Fig. 18).
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80
Figs. 27±34. Endoaperture morphology of Spermacoce pollen grains.
(27) inner view of a broken pollen grain showing endocingulum with additional lolongate thinnings at the ectoapertures (TE ) and in each
mesocolpium an extension of the endocingulum (EE); notice the thickening of the nexine and the elongation of the columellae towards
(arrow) the equatorial plane (S. azurea).
(28) detail of additional lolongate thinning within endocingulum (S. latituba).
(29) inside of pollen fragment with an endocingulum; nexine surface granular with numerous endocracks (S. stachydea).
(30) detail of lalongate thinning within endocingulum (detail of 29).
(31) detail of lalongate endocolpus with two islands of thickened nexine (TN) around endoaperture (S. verticillata).
(32) detail of indistinct lolongate endocolpus (S. latifolia).
(33) inside view at pollen half showing endopori (S. phyteuma).
(34) detail of two endopori (detail of 33).
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Pollen of African Spermacoce species (Rubiaceae)
Figs. 35±42. Ornamentation of the tectum of Spermacoce pollen grains.
(35) detail of apocolpium, eutectate (S. natalensis).
(36) detail of apocolpium, tectum with small perforations, granulate (S. octodon).
(37) detail of apocolpium, tectum with large, elongated perforations, micro-echinate (S. azurea).
(38) detail of apocolpium, tectum surface undulating, perforations large, micro-echinate (S. phyteumoides).
(39) detail of apocolpium, tectum perforate-microreticulate, echinate (S. latituba).
(40) detail of mesocolpium, tectum perforate-microreticulate, small perforations intermingled with larger ones, granulate to micro-echinate
(S. princeae).
(41) detail of mesocolpium, tectum microreticulate to reticulate, micro-echinate (S. congensis).
(42) detail of apocolpium, tectum perforate to foveolate, margins of perforations thickened, (micro-)echinate (S. bambusicola).
Grana 41 (2002)
82
S. Dessein et al.
Columellae
Columellae are always present and well developed
(Figs. 43±46 ). Their length ranges from 0.2 to 2.6 mm at the
apocolpium. In many species, the columellae are longer
towards the centers of the mesocolpia, resulting in a protruding equatorial zone (Fig. 44 ).
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Nexine
The nexine is fairly thick ranging from 0.3 to 1.7 mm at the
apocolpium. The inner surface of the nexine is nely or
coarsely granular. Endocracks are mostly present; they can
be narrow and supercial (Fig. 47 ), narrow and distinct
(Fig. 48 ) or broad and deep (Figs. 49±50 ). Endocracks are
mostly connected to the extensions of the endocingulum, but
are absent in the zones between these extensions. In some
species, the nexine is gradually thickened towards the equatorial plane (Fig. 27), in other species the nexine is distinctly
thickened around the ectoapertures resulting in a protruding
zone around the ectocolpi (Figs. 14, 21 ).
The sexine/nexine rate varies between 0.9 and 2.1 in the
apocolpium, but typically shows a value around 1.5. The
value is strongly inuenced by the position of the measurement (even within the apocolpium) and is thus of minor
importance in the characterization of the pollen grains.
Pollen types
Pollen of Spermacoce is so variable and the variation for
each character so continuous, that it is diYcult to propose a
matching typology without recognizing a large number of
types. However, to make this study more compatible with
the work of Pire (1996), we propose a typology based on
the same characters she used: pollen size, aperture number,
aperture position, relative length of the ectoaperture, and
endoaperture type. In the key below, we also include the
pollen types found among the American representatives of
the Spermacoce/Borreria complex; the type numbers used
correspond with the types of Pire (1996).
Description of pollen types
Only the pollen types found among species present in Africa
are described here. The descriptions are based on the African
material only. For a detailed description of the other pollen
types keyed out below, see Pire (1996).
Type 1 (Figs. 2±3, 10, 18, 35)
Pollen zonocolporate (3±4) or (6±8), mean E 15.8±16.5 mm;
mean P/E rate 1.1±1.2 (prolate-spheroidal, subprolate); polar
outline triangular, quadrangular to almost circular.
Ectocolpus long (LC/P 53±62 ), narrow, slightly sunken.
Endoaperture narrow endocingulum. Tectum perforate to
eutectate at apocolpium; margo of granules or microspines.
Inner nexine surface nely granular.
Species included: 3±4 colporate: S. mauritiana, S. natalensis.
6±8 colporate: S. tenuior.
Remark: Other species with same pollen type listed by
Pire (1996).
Type 2 (Figs. 19, 32)
Pollen zonocolporate (7±11), mean E 48.3 mm; mean P/E
rate 0.88 (suboblate, oblate-spheroidal ); polar outline circular. Ectocolpus long (LC/P 38 ), narrow, slightly sunken.
Endoaperture lolongate. Tectum perforate, uniformly granulate. Inner nexine surface nely granular with very broad,
irregular endocracks.
Species included: S. latifolia.
Remark: Other species with same pollen type listed by
Pire (1996).
Type 3 (Figs. 4, 11, 31)
Pollen zonocolporate (6±9), mean E ca. 28.0 mm; mean P/E
rate 0.95 (oblate-spheroidal ); polar outline circular.
Ectocolpus short (LC/P 20), narrow, slightly sunken.
Endoaperture lalongate. Tectum perforate, uniformly granulate. Inner nexine surface granular with numerous
endocracks.
Species included: S. verticillata.
Remark: Other species with same pollen type listed by
Pire (1996).
Type 6 (Figs. 9, 25±26, 33±34 )
Pollen pantopororate (24±30 ), mean E 66.5±87.0 mm; mean
P/E rate ca. 1 (spheroidal ); polar outline circular. Ectopore
2±5 mm in diameter (LC/P 4.5±5), operculum present.
Endoaperture an indistinct endopore. Tectum perforatemicroreticulate or (micro)reticulate, microspines sparsely
present on whole surface. Inner nexine surface nely granular,
endocracks absent.
Species included: S. annua, S. phyteuma.
Remarks: Other species with same pollen type listed by Pire
(1996). Although included in pollen type 6 of Pire (1996),
Figs. 43±50. Pollen wall stratication and morphology of inner nexine surface of Spermacoce pollen grains.
(43) wall stratication at apocolpium showing nexine, row of short columellae and tectum with microspines; note regular endocracks in
nexine surface (S. hockii ).
(44) broken pollen wall at mesocolpium showing the elongation of the columellae (S. deserti).
(45) cross section of pollen wall in mesocolpium showing from top to bottom: tectum with microspines (T), columellae (C), nexine (N ),
endocingulum (E), lolongate thinning within endocingulum (TE), extensions of endocingulum (EE ) and nexine surface with endocracks
(NE) (S. phyteumoides).
(46) detail of stratication: from top to bottom: perforated tectum with microspines (T ), columellae (C ), and nexine (N ); note granules on
nexine (S. dibrachiata).
(47) inner surface of granular nexine with indistinct endocracks (S. subvulgata ).
(48) inner surface of granular nexine with distinct, narrow endocracks (S. tenuissima).
(49) inner surface of nely granular nexine with broad deep endocracks (S. dibrachiata).
(50) inner surface of nely granular nexine with broad deep endocracks (S. phyteumoides).
Grana 41 (2002)
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Pollen of African Spermacoce species (Rubiaceae)
the pollen described here are larger and the apertures more
numerous.
Type 11 (Fig. 12)
Pollen zonocolporate (8±13 ), mean E 32.0±46.5 mm; mean
P/E rate 0.80±1.00 (suboblate, oblate-spheroidal ); polar outline circular. Ectocolpus short (LC/P 15±25 ), narrow, slightly
sunken. Endoaperture endocingulum with two horns in each
mesocolpium. Tectum perforate, granules (or microspines)
uniformly present. Inner nexine surface nely granular with
numerous narrow endocracks.
Species included: S. assurgens, S. chaetocephala, S. liformis,
S. hepperana, S. pusilla, S. quadrisulcata, S. radiata.
Remark: Other species with same pollen type listed by
Pire (1996).
Type 12 (Figs. 23, 36, 48, 51±54)
Pollen pantocolporate (ca. 15 ), E 40.9±56.6 mm; mean P/E
Grana 41 (2002)
84
S. Dessein et al.
rate ca. 1 (spheroidal ); polar outline circular. Ectocolpus
short (LC/P 6±14 ) and narrow. Endopattern complex,
including an ``endocingulum’’ with horns, an additional
lalongate thinning of the nexine at the ectocolpus, and
numerous, often deep endocracks. Tectum perforate, granules
or microspines uniformly present. Inner nexine surface granular, but smooth within endocracks.
Species included: S. lifolia, S. octodon, S. tenuissima.
Remark: The exact number of apertures is diYcult to
determine.
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Type 13 (Figs. 24, 55±58)
Pollen pantocolporate (ca. 24), mean E 54.4±56.9 mm; mean
P/E rate ca. 1 (spheroidal ); polar outline circular. Ectocolpus
short (LC/P 6±11) and narrow or somewhat widened, colpus
membrane (if present) beset with granules. Endopattern
complex, including an ``endocingulum’’ with horns, an additional lalongate thinning of the nexine at the ectocolpus, and
numerous endocracks. Tectum perforate, small perforations
intermingled with larger ones, microspines uniformly present.
Inner nexine surface granular, numerous endocracks.
Species included: S. terminaliora, S. thymoidea.
Remark: The exact number of apertures is diYcult to
determine.
Type 14 (Figs. 7±8, 15±17, 20, 22, 27, 37±38, 43, 45±46, 49±50)
Pollen zonocolporate (13±21), mean E 66.7±84.8 mm; mean
P/E rate 0.7±0.8 (oblate, suboblate); polar outline circular,
clearly lobed due to longer columellae in the equatorial zone.
Ectocolpus relatively long (LC/P 24±45 ), slit like, margins
beset with microspines. Endoaperture a broad endocingulum
with horns in the mesocolpia and with an additional lolongate
thinning of the nexine at the ectocolpus. Tectum perforate,
often perforate-reticulate at the mesocolpia, large perforations intermingled with smaller ones, surface often undulating; microspines uniformly present. Inner nexine surface
nely granular with broad, undeep or deep, smooth
endocracks.
Species included: S. arvensis, S. azurea, S. dibrachiata, S.
hockii, S. phyteumoides, S. stipularis.
Remark: Pollen of Spermacoce dibrachiata diVers from the
other species included in its high number of colpi.
Type 15 (Figs. 5, 14, 21, 28, 39, 41, 47 )
Pollen zonocolporate (9±14 ), mean E 76.8±105.3 mm; mean
P/E rate 0.82±0.88 (suboblate, rarely oblate-spheroidal );
polar outline circular, slightly or strongly lobed due to
thickened nexine around ectocolpi. Ectocolpus short (LC/P
10±23) and relatively broad, colpus membrane (if present)
beset with large cubic-shaped particles; nexine thickened
around the ectocolpus, forming a distinct margo.
Endoaperture a broad endocingulum with an additional
lalongate or lolongate thinning of the nexine at the ectoaperture. Tectum perforate or perforate-microreticulate, rarely
reticulate; margins of the perforations sometimes slightly
thickened; microspines or spines uniformly present. Inner
nexine surface granular with numerous, often indistinct
endocracks.
Species included: S. congensis, S. huillensis, S. kirkii, S.
latituba, S. senensis, S. subvulgata, S. taylorii.
Tentatively included: S. articularis. We found only one
African collection with suYcient owers to carry out palynological research; the nexine around the ectocolpi is thickened,
but only slightly so.
Remark: In S. congensis, the margo is not distinct, but it ts
very well within this pollen type for all other characters.
Type 16 (Fig. 42 )
Pollen zonocolporate (13±18), mean E 90±115.5 mm; mean
P/E rate 0.7±0.9 (oblate, oblate-spheroidal ); polar outline
circular, lobed due to longer columellae in the equatorial plane. Ectocolpus short (LC/P 14.6±24.6), slit like.
Endoaperture a broad endocingulum with horns in the
mesocolpia and with a rather indistinct lalongate thinning at
the ectocolpus. Tectum perforate or foveolate, margins of
perforations thickened, spines uniformly present. Inner
nexine surface granular with broad, undeep, smooth
endocracks.
Species included: S. bambusicola, S. ivorensis.
Type 17 (Figs. 6, 13, 29±30, 40, 44)
Pollen zonocolporate [(8±10 )±11±16 ], mean E 62.0±91.0 mm;
mean P/E rate 0.8±0.92 (suboblate, rarely oblate-spheroidal );
polar outline circular, often (slightly) lobed due to longer
columellae at the equatorial plane. Ectocolpus relatively
short (LC/P 18±24), slit like. Endoaperture a broad endocingulum with or without horns at the mesocolpia but always
with an additional, lalongate thinning at the ectocolpus.
Tectum perforate or perforate-microreticulate, large perforations often intermingled with smaller ones; microspines or
spines uniformly present. Inner nexine surface granular with
or without distinct endocracks.
Species included: S. deserti, S. lituba, S. princeae, S. ruelliae,
S. sphaerostigma, S. stachydea.
Tentatively included: S. intricans and S. spermacocina. Both
diVer from the other species included in the lower number
Figs. 51±58. Detailed morphology of pollen types 12 & 13 of Spermacoce.
(51) pollen grain of type 12 showing two rows of ectocolpi (S. lifolia).
(52) diVerent view of same pollen grain as in (51 ) showing colpi arranged in a loop.
(53) view of inner side of an half of pollen showing complex endopattern with an ``endocingulum’’ (E ), lalongate thinnings within
endocingulum (TE), extensions of endocingulum (EE), and nexine (NE ) surface with numerous endocracks (S. tenuissima).
(54) Detail of (53).
(55) pollen grain of type 13 showing colpi arranged in a spiral (S. thymoidea).
(56) diVerent view of same pollen grain as in (55 ).
(57) view of inner side of an half of pollen showing complex endopattern with cross-linked endocolpi, lalongate thinnings (TE ) within
endocingulum (E ), extensions of endocingulum (EE), nexine surface (NE) with numerous endocracks (S. thymoidea).
(58) detail of (57) showing the same elements.
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Pollen of African Spermacoce species (Rubiaceae)
85
Grana 41 (2002)
86
S. Dessein et al.
of apertures, the only weak elongation of the columellae in
the EP, and in the granulate to microechinate ornamentation.
They are intermediate between types 11 and type 17.
Key to pollen types
1.
2(1).
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3(1).
4(3).
5(3).
6(5).
7(5).
8(7).
9(8).
10 (9).
11 (8).
12 (11).
13 (7).
14 (13).
15 (14).
16 (15).
Ectoapertures pores ............................................. 2
Ectoapertures colpi .............................................. 3
Pollen zonopo(ro)rate ............. Type 5 (American)
Pollen pantopo(ro)rate ...........................................
.................................. Type 6 (American+ African)
Pollen pantocolporate ......................................... 4
Pollen zonocolporate ........................................... 5
Colpi arranged in a loop ........... Type 12 (African)
Colpi arranged in a spiral ......... Type 13 (African)
E usually smaller than 20 mm; margo of granules ..
.............................................................................. 6
E usually larger than 20 mm; granules evenly scattered over pollen surface ..................................... 7
Endoaperture an endocingulum ..............................
.................................. Type 1 (American+ African)
Endoaperture an endocolpus .. Type 7 (American)
Endoaperture an endocolpus .............................. 8
Endoaperture an endocingulum ......................... 13
Colpi relatively long (L/P>35 ) .......................... 9
Colpi relatively short (L/P<35 ) ........................ 11
E smaller than 30 mm; 6-7-colporate .......................
.................................................. Type 8 (American)
E larger than 30 mm; 8±10-colporate .................. 10
Tectum perforate ..................... Type 2 (American)
Tectum reticulate and heterobrochate .....................
.................................................. Type 9 (American)
Colpi relatively broad ............. Type 4 (American)
Colpi slit-like ...................................................... 12
E smaller than 20 mm ............. Type 10 (American)
E larger than 20 mm ................. Type 3 (American)
E usually smaller than 50 mm ..................................
................................ Type 11 (American+ African)
E larger than 50 mm ........................................... 14
Colpi relatively long (LC/P 24±45 ); number of
apertures mostly more than 14 (rarely 13 ); columellae distinctly longer in equatorial zone; endocingulum with an additional lolongate thinning ..............
.................................................... Type 14 (African)
Colpi shorter; number of apertures usually less than
14; columellae not so distinctly longer in equatorial
zone; endocingulum usually with an additional
lalongate thinning ............................................... 15
Nexine distinctly thicker around the ectoapertures,
visible as a distinct margo, if margo indistinct, colpi
very short (LC/P < 15) and wide; colpus membrane
(if present) beset with cubic-shaped particles .........
.................................................... Type 15 (African)
Margo absent, colpi usually relatively long
(LC/P>15) and slit-like; colpus membrane sometimes beset with cubic-shaped particles .............. 16
Margins of perforations thickened ..........................
.................................................... Type 16 (African)
Margins of perforations not thickened ...................
.................................................... Type 17 (African)
Grana 41 (2002)
DISCUSSION
African vs. American Spermacoce species
In comparing our results with the palynological research of
Pire (1996) on the American representatives of the
Spermacoce-Borreria alliance, some diVerences can be
observed. Pire recognized 11 pollen types, of which only
three are observed among native African species, namely
type 1 with small pollen grains and long colpi, type 6 with
pantopo(ro)rate pollen grains, and type 11 with medium
sized grains with an endocingulum. Six additional pollen
types are described here, which are exclusively found in the
African Spermacoce species. Two of these pollen types have
aperture congurations not previously recorded for the
angiosperms. In general, the following diVerences between
the pollen grains of African and American species are
observed:
1. Sexine patterns are more heterogeneous: perforate to
(micro)reticulate or foveolate in African species, vs.
perforate in most American species;
2. The apertural region is more complex in African than in
American species (presence of margines and multiple
endoapertures), and the pantoaperturate condition is more
diVerentiated in African species;
3. Pollen size range is much larger among African species,
and correlated with this also the variation in the number
of apertures;
4. The number of pantopo(ro)rate pollen grains is lower
among African species (5% vs. 25%);
5. In all but the pantopororate African species, the endocolpi
are laterally joined to form an endocingulum.
These diVerences support the recognition of additional ``patterns of pollen variation’’ for the evolutionary scheme proposed by Pire (1996). These are discussed in the following
paragraph.
Patterns of pollen variation
The pollen variation among the Spermacoce-Borreria alliance
perfectly illustrates Van Campo’s statement that ``amplitude
of pollen variations within a homogenous assemblage pregures, in some cases, the possible pollen types within an
assemblage higher in the classication’’ (Van Campo 1976:
126). Indeed, the diVerent pollen types found in Spermacoce/
Borreria cover to a large extent the pollen variation observed
in Rubiaceae as a whole. Mathew & Philip (1983) surveyed
the pollen morphology of the Indian representatives of the
family and found ve major apertural types: colpate, inaperturate, colporate, porate and pororate. The latter three were
all found in the genus Spermacoce sensu lato.
At this point an evolutionary hypothesis for the
Spermacoce sensu lato species based on molecular and morphological data or even a genus circumscription everyone
agrees on is not available. Hence, a detailed analysis of the
evolution of pollen characters is not possible. Nevertheless,
in the light of the present study of the African taxa, we can
consider the evolutionary sequence of pollen types proposed
for Borreria by Pire (1996). Her evolutionary sequence
postulated four ``tendencies’’:
Pollen of African Spermacoce species (Rubiaceae)
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1. extension of the apertural area; from zonoaperturate
pantoaperturate;
2. reduction of the ectoapertures; from long colpishort
colpipores;
3. narrowing of the endoapertures; from zonorate
lalongatelolongate;
4. increase of the number of apertures; from few apertures
many apertures.
Many authors have previously proposed these trends in
other groups of angiosperms ( Keddam-Malplanche 1985,
Kuprianova 1969, Lewis 1965, Punt 1976, Thanikaimoni
1986, Van Campo-Duplan 1949, Van Campo 1966, 1976),
and they are possibly present in Spermacoce species native
to Africa. However, comparison between Pire’s (1996)
proposed evolutionary sequences and the pollen features
observed in the African Spermacoce species, raises some
additional points. First of all pollen grains of the African
species are signicantly larger on average than those of the
neotropical species. Increase of pollen size is thought to
represent an evolutionary tendency of simple grains ( Van
Campo-Duplan 1949, Keddam-Malplanche 1985). Within
the African Spermacoce species, this tendency is correlated
with an increase of the number of apertures (see above).
Furthermore, at least some tendencies ± or as called by Van
Campo (1976 ) ``patterns of variation’’ ± should be added
here:
1. lumina smalllumina larger;
2. ectocolpi without margoectocolpi with margo;
3. spiralization.
The rst two patterns of variation are illustrated in Figs.
35±42 and Figs. 18±26 respectively, and were inter alia
proposed by Punt (1976). The third one, spiralization, was
introduced by Van Campo (1976) to describe a pattern in
which the line joining the centers of the apertures shows
spiralization. In this pattern, a process that involves
shortening, spiralization of the position, and symmetrization
of the ectoapertures leads to the pantoaperturate condition.
The pattern was observed in Malvaceae ( Van Campo 1976),
and can partly explain the two special pollen types (type 12
& 13 ) observed in Spermacoce.
In conclusion, one can hypothesize that notwithstanding
the supercial resemblance between pollen grains of neotropical and African species, they developed independently. The
ancestral pollen type in Spermacoce is most probably a
3-colporate pollen grain that resembles type 1. Such
3-colporate pollen grains are also found in most members of
the Hedyotideae, and it is thought to be a primitive Rubiaceae
pollen grain type (Mathew & Philip 1983, Robbrecht 1988).
In this context, it is of special interest that the most ubiquitous
(and less specialized) Spermacoce species are characterized
by these 3-colporate pollen grains. Other widespread species,
such as Spermacoce assurgens also have relatively ``primitive’’
pollen grains. Pollen types which are considered more derived
( Types 6, 12, 13 ) often characterize species with a very
narrow distribution.
87
Systematic value
Species delimitation
Pollen of Spermacoce s.l. is very heterogeneous, so that in
many cases species can be determined by their pollen grains
only. As a consequence, pollen characters provide stable and
reliable characters for dening and delimiting species. This
is a rather uncommon situation in Rubiaceae. Except for
other europalynous tribes (e.g., Psychotrieae), pollen grains
have only limited value in species delimitation.
Up to now Spermacoce species were mainly dened on the
basis of general habit, peculiarities of the owers, seed
morphology and type of fruit dehiscence. These characters,
however, can be very variable, hence making the limits of
some species unclear. Pollen grains often provide evidence
to sharpen species boundaries and to place ``diYcult’’ specimens. An example is given by the delimitation of Spermacoce
senensis and S. sphaerostigma (see Verdcourt 1976). The
former is a very variable annual (its height can range from
a few cm to over half a meter), and in its owering state it
is diYcult to separate from Spermacoce sphaerostigma. Pollen
grains, however, clearly separate the two species: Spermacoce
senensis has a margo of thicker nexine, while S. sphaerostigma
has not.
The present study also provides additional support for
taxonomic decisions at the species level made by other
investigators. A clear example is given by ``Borreria bambusicola’’, a species described by Berhaut (1973) based on material
which had been identied as Borreria compressa (correct
name: Spermacoce hepperana). He mainly distinguished
Borreria bambusicola on the basis of its larger owers and
its seeds bearing an elaiosome. Our pollen data give further
support to this view: Spermacoce bambusicola has large
pollen grains with a foveolate tectum and with bordered
perforations, while Spermacoce hepperana has small pollen
grains with a less diVerentiated perforated tectum.
Pollen data sometimes refute taxonomic hypotheses; this
is illustrated by the problematic delimitation of Spermacoce
thymoidea. Verdcourt (1975) relegated ``Borreria hockii’’
(R.D. Congo) to the synonymy of Spermacoce thymoidea
(Angola), and also used the name for some Zambian specimens. His decision was mainly based on habit and ower
morphology, and was at rst sight fairly convincing. After
observing pollen (and seeds), however, we were able to
demonstrate that three distinct species are involved, the two
cited ones and a new one (Dessein et al. in press).
Generic and subgeneric delimitation
Pire & Cabral (1992 ) recognized Galianthe at the generic
level inter alia based on the peculiarities of its pollen grains,
and Pire (1996 ) presented pollen morphological support for
the subgeneric delimitation of Borreria proposed by
Bacigalupo & Cabral (1996). So, at rst sight, pollen has
value in delimiting genera and subgenera within the
Spermacoceae. This consideration, however, should be
handled with care. In our study, we were not able to nd
any correlation between the described types of fruit dehiscence and the pollen morphology observed. This can be an
indication that the fruit typology is not useful, or that the
Grana 41 (2002)
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88
S. Dessein et al.
pollen morphology is too plastic to cluster groups at the
generic level.
The former hypothesis is supported by the observation
that pollen type 1 is found in three species, each with a
diVerent type of fruit dehiscence. Spermacoce mauritiana, a
widespread species in Africa, Asia, as well as the neotropics,
has fruits dehiscing from the apex downwards into four
valves with the remnants of the septum remaining attached
to the valves, which is in agreement with the denition of
Borreria. Spermacoce natalensis has fruits splitting septicidally into tardily dehiscent mericarps, and for this reason it
was once described under Diodia, a genus traditionally
dened as having fruits splitting into indehiscent mericarps,
but recently (Bacigalupo & Cabral 1996, 1999) redened as
having indehiscent fruits. Spermacoce tenuior has fruits splitting into one dehiscent and one indehiscent fruit valve, and
in this corresponds to the strict denition of Spermacoce (cf.
above). In all other morphological characters, however, the
three species are very similar. They all have small owers
(corolla tube usually shorter than 2 mm) grouped in lateral
inorescences, and the anthers are not or only slightly
exserted.
The same pollen type 1 is found in morphologically similar
American ``Borreria’’ species (included by Bacigalupo &
Cabral (1996) in subgenus Borreria subgenus Borreria section
Pseudodiodia). The strong possibility that these species form
a natural group, hence refuting the value of fruit characters
in the delimitation of genera within the tribe, awaits support
from molecular studies. What becomes clear, however, is
that pollen, as well as other morphological characters do not
correlate with the types of fruit dehiscence, an observation
that strongly questions the taxonomic value of this carpological character. Pollen characters on the contrary are rather
well supported by other morphological data.
Pollen type 1 is also found in the neotropical Psyllocarpus
sect. Psyllocarpus ( Kirkbride 1979). The latter genus is
distinguished from the Spermacoce/Borreria group on the
basis of the laterally compressed fruits and seed peculiarities.
In other characters section Psyllocarpus is similar to the
species mentioned above. Kirkbride (1979 ) already remarked
that section Psyllocarpus is probably more closely related to
Borreria by its vegetative structures and is less specialized
than the other section, i.e., sect. Amazonica.
Other groups of morphologically distinctive and similar
species also share pollen types:
1. Type 12 (with the colpi arranged in a loop-like pattern)
is limited to three species. Two of these, namely
Spermacoce octodon and S. lifolia, once formed a genus
on their own, namely Octodon. Its rounded, minute calyx
lobes, the cup-shaped stipules that hold the owers, and
the very slender habit, characterized the genus. The third
species, Spermacoce tenuissima, has never been assigned
to Octodon, but shares the same habit and the minute
calyx lobes. As a consequence, pollen morphology clearly
oVers arguments for resurrecting the (sub)genus Octodon.
2. Type 15 is found in Spermacoce congensis, S. huillensis,
S. kirkii, S. latituba, S. senensis, S. subvulgata, and S.
taylorii. Verdcourt (1976) already pointed to the close
relationship between Spermacoce kirkii and S. subvulgata,
Grana 41 (2002)
but a close relationship between the other species was
never hypothesized. Nevertheless Spermacoce congensis,
S. kirkii, S. subvulgata, and S. taylorii all have a spikelike inorescence, two calyx lobes, and relatively large
owers. Spermacoce huillensis, S. latituba, and S. senensis
mainly diVer in the presence of four calyx lobes. Verdcourt
(1975, 1976), however, described a form of Spermacoce
subvulgata with a four-lobed calyx as variety quadrisepala,
hypothesizing (and thereby suggesting implicitly possible
relationship) that the specimen may well be a hybrid
between S. senensis and S. subvulgata.
3. Another group of related species that share the same
pollen type is formed by Spermacoce azurea, S. hockii,
and S. stipularis. All three have a woody taproot, lanceolate leaves, two calyx lobes, large owers, seeds with an
elaiosome (except the seeds are unknown for S. azurea),
and type 14 pollen grains. All three are conned to high
plateaus of the Zambezian regional center of endemism.
4. Spermacoce thymoidea and S. terminaliora are both
narrow endemics of the Angolan high plateaus. They
share the same habit, but in all other characters they
diVer considerably. Whether the shared pollen type 13 is
an adaptation to the specic environmental conditions or
whether the species are sister taxa needs further study.
In conclusion, pollen characters provide almost unique
markers for many species in this group, enabling sharpening
of species boundaries. Whether this variation is also useful
to identify some groups of related species remains to be
conrmed by incorporation of additional data, but there is
good reason to believe it often is. The groups characterized
by the same pollen type turn out to be in serious conict
with the established generic concepts based on fruit characters only.
ACKNOWLEDGEMENTS
This study was supported by a grant form the Research Council of
the K.U.Leuven (OT/01/25) and by a grant from the F.W.O.Vlaanderen (G.104.01) . Suzy Huysmans is a postdoctoral fellow,
Steven Dessein a research assistant of the F.W.O.
We are indebted to the curators of the herbaria of WAG, K and
ZT for providing pollen material for this investigation. Special
thanks are due to Anja Vandeperre for technical assistance and to
Marcel Verhaegen for kindly taking the scanning electron
micrographs.
Finally, the rst author addresses his sincere thanks to all participants of the Cuba conference for their encouraging comments,
especially to Prof. S. Nilsson, Dr. F. Spieksma, Dr. S. Rodriguez,
and Dr. M. Kedves, and to Drs. P. Schols, B. Harwood, Prof. L.
Andersson, and an anonymous reviewer for critical reading of the
manuscript.
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