Olivier Maurin Philosophiae Doctor Botany Faculty of

Transcription

A PHYLOGENETIC STUDY OF THE FAMILY
COMBRETACEAE WITH EMPHASIS ON THE GENUS
COMBRETUM IN AFRICA
by
Olivier Maurin
Dissertation submitted in fulfillment of the
requirements for the degree
Philosophiae Doctor
In
Botany
in the
Faculty of Science
at the
University of Johannesburg
Supervisor: Prof. M. van der Bank
Co-supervisor: Prof. M. W. Chase
December 2009
I declare that this dissertation has been composed by me and the work contained within,
unless otherwise stated, is my own.
_________________________
O. Maurin (December 2009)
Table of contents
TABLE OF CONTENTS
INDEX TO TABLES ......................................................................................................................7
INDEX TO APPENDICES ..............................................................................................................9
INDEX TO FIGURES ..................................................................................................................11
ABSTRACT ................................................................................................................................21
FOREWORD ..............................................................................................................................25
ACKNOWLEDGMENTS ..............................................................................................................29
LIST OF ABBREVIATIONS .........................................................................................................33
CHAPTER 1: GENERAL INTRODUCTION AND OBJECTIVES......................................................41
1.1 GENERAL INTRODUCTION .................................................................................................41
1.2 PLACEMENT OF COMBRETACEAE WITHIN MYRTALES ....................................................44
1.3 TAXONOMIC HISTORY OF COMBRETACEAE (TABLE 1.3).................................................46
1.4 OBJECTIVES OF THE STUDY ...............................................................................................50
CHAPTER 2: PHYLOGENETIC RELATIONSHIPS OF COMBRETACEAE INFERRED FROM
NUCLEAR AND PLASTID DNA SEQUENCE DATA: IMPLICATIONS FOR GENERIC
CLASSIFICATION .................................................................................................................73
2.1 INTRODUCTION ..................................................................................................................73
2.2 MATERIALS AND METHODS ...............................................................................................76
2.2.1 Taxon sampling ........................................................................................................76
2.2.2 Outgroup and loci selection .....................................................................................77
2.2.3 DNA extraction, PCR and sequencing .....................................................................78
2.2.4 Sequencing and alignment .......................................................................................79
2.3 RESULTS .............................................................................................................................81
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2.3.1 Molecular evolution .................................................................................................81
2.3.2 rbcL analysis with a broad outgroup sampling (analysis 1)...................................82
2.3.3 Combined plastid analysis (analysis 2)....................................................................83
2.3.4 ITS analysis (analysis 3)..........................................................................................83
2.3.5 Combined molecular analysis (analysis 4) ..............................................................84
2.4 DISCUSSION ........................................................................................................................85
2.4.1 Relationships within tribe Laguncularieae...............................................................86
2.4.2 Subtribal relationships within tribe Combreteae .....................................................86
2.4.4 Relationships within subtribe Combretinae .............................................................90
2.4.5 Relationships within Combretum subgenus Combretum including Meiostemon....93
2.4.6 Relationships within Combretum subgenus Cacoucia including Quisqualis and
Calopyxis...........................................................................................................................97
2.5 CONCLUSIONS ..................................................................................................................100
2.6 TAXONOMIC CHANGES ....................................................................................................101
CHAPTER 3: NOTES ON THE PHYLOGENY, CLASSIFICATION AND BIOGEOGRAPHY OF
COMBRETUM SECTIONS ANGUSTIMARGINATA, SPATHULIPETALA AND MACROSTIGMATEA
S.S. (COMBRETACEAE), WITH THE DESCRIPTION OF A NEW SPECIES FROM SOUTH
AFRICA..............................................................................................................................115
3.1 INTRODUCTION ................................................................................................................115
3.2 MATERIALS AND METHODS .............................................................................................116
3.2.1 Plant material.........................................................................................................116
3.2.2 Scale morphology...................................................................................................117
3.2.3 Phylogenetic analyses ............................................................................................117
3.2.4 Evaluation of morphological and biogeographical data .......................................119
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3.2.5 Species description and identification key .............................................................119
3.3 PHYLOGENETICS, CLASSIFICATION AND BIOGEOGRAPHY OF SECTION
ANGUSTIMARGINATA, MACROSTIGMATEA S.S.
AND SPATHULIPETALA .................................119
3.3.1 Distribution, habitat and habit...............................................................................119
3.3.2 Phylogenetic data...................................................................................................125
3.3.3 Morphological characters......................................................................................126
3.3.4 Leaf scales anatomy ...............................................................................................127
3.4 DISCUSSION ......................................................................................................................127
3.5 DESCRIPTION OF NEW SPECIES........................................................................................132
3.5.1 Diagnostic characters ............................................................................................134
3.5.2 Distribution and habitat.........................................................................................134
3.5.3 Conservation status................................................................................................135
3.5.4 Further collection..................................................................................................135
3.6 KEY TO SPECIES OF COMBRETUM SECTION ANGUSTIMARGINATA AND
MACROSTIGMATEA S.L. ..........................................................................................................136
CHAPTER 4: NOTES ON PHYLOGENETICS, MORPHOLOGY AND BIOGEOGRAPHY OF
COMBRETUM SECTION CILIATIPETALA (COMBRETACEAE), WITH THE DESCRIPTION OF
A NEW SPECIES FROM SOUTH AFRICA .............................................................................153
4.1 INTRODUCTION ................................................................................................................153
4.2 MATERIALS AND METHODS .............................................................................................156
4.2.1 Plant material.........................................................................................................156
4.2.2 Scale morphology...................................................................................................156
4.2.3 Phylogenetic analyses ............................................................................................157
4.2.4 Evaluation of morphological and biogeographical data .......................................158
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4.2.5 Species description and identification key .............................................................159
4.3 PHYLOGENETICS, CLASSIFICATION AND BIOGEOGRAPHY OF SECTION CILIATIPETALA 159
4.3.1 Distribution, habitat and habit...............................................................................159
4.3.2 Phylogenetic data...................................................................................................164
4.3.3 Morphological characters......................................................................................164
4.3.4 Leaf scale anatomy.................................................................................................165
4.4 DISCUSSION ......................................................................................................................165
4.5 DESCRIPTION OF NEW SPECIES........................................................................................168
4.5.1 Diagnostic characters ............................................................................................170
4.5.2 Distribution and habitat.........................................................................................171
4.5.3 Eponymy .................................................................................................................171
4.5.4 Conservation status................................................................................................171
4.5.5 Further collections .................................................................................................172
4.6 KEY TO SPECIES OF COMBRETUM SECTION CILIATIPETALA ...........................................172
CHAPTER 5: THE EVOLUTIONARY HISTORY AND BIOGEOGRAPHY OF COMBRETACEAE ....189
5.1 INTRODUCTION ................................................................................................................189
5.2 MATERIAL AND METHODS ...............................................................................................190
5.2.1 Sampling.................................................................................................................190
5.2.2 DNA extraction, amplification, sequencing & alignment ......................................191
5.2.3 Divergence time estimation (using Beast)..............................................................193
5.2.4 Optimisation of habitat, climate, and morphological characters ..........................194
5.3 RESULTS ...........................................................................................................................195
5.3.1 rbcL analysis with a broad outgroup sampling (analysis 1; Figure 5.1) ..............195
5.3.2 Combined plastid and nuclear analysis (analysis 2; Figure 5.2) ..........................195
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5.4 DISCUSSION ......................................................................................................................197
5.4.1 Origin of Combretaceae.........................................................................................197
5.4.3 Tribe Laguncularieae and the evolution of mangroves .........................................200
5.4.4 Split between Combretinae and Terminaliinae......................................................202
5.4.5 Subtribe Terminaliinae...........................................................................................202
5.4.6 Subtribe Combretinae ............................................................................................203
5.5 CONCLUSIONS ..................................................................................................................207
CHAPTER 7: REFERENCES.....................................................................................................235
APPENDICES ...........................................................................................................................257
ANNEXES ................................................................................................................................281
ANNEXE 1: TAXONOMY AND DISTRIBUTION OF QUISQUALIS PARVIFLORA ..........................281
ANNEXE 2: A CONSPECTUS OF COMBRETUM (COMBRETACEAE) IN SOUTHERN AFRICA,
WITH TAXONOMIC AND NOMENCLATURAL NOTES ON SPECIES AND SECTIONS ...................293
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6
Index to Tables
INDEX TO TABLES
CHAPTER 1
TABLE 1.1 The 17 genera of Combretaceae recognised in this study. Number of species
included for each genus from Mabberley (2008). The two genera in brackets are recent
changes ............................................................................................................................ 51
TABLE 1.2 Proposed families within Myrtales from 1981 to 2009...................................... 53
TABLE 1.3 History of genera recognised within Combretaceae from 1810 to 2007 ........... 54
TABLE 1.4 History of classification within Combretaceae. ................................................. 59
TABLE 1.5 Subgeneric and sectional classification of Combretum and closely related
genera. ............................................................................................................................. 61
CHAPTER 2
TABLE 2.1 Genera studied, including subfamily, tribal and sectional classification. Sections,
classification and number of species included within each genus Combretum are from
Stace (1980a, 1980b), Van Wyk (1984) and Mabberley (2008). Number of species
included in this study is indicated in parentheses. Sectional classification of Terminalia
from Griffiths (1959)..................................................................................................... 103
TABLE 2.2 Maximum parsimony statistics from the analyses of the separate and combined
data sets. ........................................................................................................................ 105
CHAPTER 5
TABLE 5.1 Circumscription of Myrtales according to different authors............................ 209
TABLE 5.2 Biogeography and classification of Combretaceae according to Mabberley
(2008), Exell & Stace (1966), and Stace (1968, 1980a, 1980b). Geographical range: Am
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Index to Tables
= America; Af = Africa; As = Asia; Au = Australasia. In brackets is the total; under
genus total number of species worldwide; under continent total number of species per
geographic area. ............................................................................................................ 210
TABLE 5.3 Node ages in millions of years (mya). For each node, the estimated age, along
with the 95% high posterior density interval (95%HPD), are presented. Node numbers
correspond to those in Figure 5.2. ................................................................................. 212
Table 5.4 Node ages in millions of years (mya). For each node, the estimated age along
with the 95% high posterior density interval (95%HPD) are presented. Node numbers
correspond to those in Figure 5.3. ................................................................................. 213
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Index to Appendices
INDEX TO APPENDICES
CHAPTER 2
APPENDIX 2.1 Voucher information and GenBank accession numbers for taxa used in this
study. A dash indicates DNA regions not sampled and DNA sequences obtained from
GenBank are underlined. Voucher specimens are deposited in the following herbaria:
BISH = Bishop Museum, Honolulu, U.S.A.; JRAU = University of Johannesburg (UJ),
Johannesburg, South Africa; K = Royal Botanic Gardens, Kew, Richmond, United
Kingdom; PRE = South African National Botanical Institute, Pretoria, South Africa;
MO = Missouri Botanical Garden, St. Louis, U.S.A. ................................................... 257
CHAPTER 3
study. Voucher specimens are deposited in the following herbaria: JRAU = University
of Johannesburg (UJ), Johannesburg, South Africa...................................................... 263
APPENDIX 3.2 Characters, character states, and explanatory notes on characters used in the
cladistic analyses of the morphological data matrix ..................................................... 264
APPENDIX 3.3 Character states for the 32 morphological characters scored for accessions
included in the molecular analyses. See appendix 3.2. for character definition. .......... 266
CHAPTER 4
JRAU = University of Johannesburg (UJ), Johannesburg, South Africa; PRE = South
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Index to Appendices
African National Botanical Institute, Pretoria, South Africa; MO = Missouri Botanical
Garden, St. Louis, U.S.A............................................................................................... 267
APPENDIX 4.2 Characters, character states, and explanatory notes on characters used in the
cladistic analyses of the morphological data matrix. .................................................... 269
APPENDIX 4.3 Character states for 28 morphological characters scored for accessions
included in the molecular analyses. See appendix 4.2. for character definitions.......... 271
CHAPTER 5
BISH = Bishop Museum, Honolulu, U.S.A.; JRAU = University of Johannesburg (UJ),
Johannesburg, South Africa; K = Royal Botanic Gardens, Kew Richmond, United
Kingdom; PRE = South African National Botanical Institute, Pretoria, South Africa;
MO = Missouri Botanical Garden, St. Louis, U.S.A; Taxa distribution is mentioned, and
for voucher use as for the large rbcL analysis, distribution is for the genus................. 272
10
Index to Figures
INDEX TO FIGURES
CHAPTER 1
FIGURE 1.1 Distribution of the Combretaceae (from Heywood et al., 2007). ..................... 64
FIGURE 1.2 Specimen of Combretum apiculatum subsp. apiculatum in northern Botswana.
......................................................................................................................................... 64
FIGURE 1.3 Large specimen of Combretum imberbe along the Okavango river (Botswana).
......................................................................................................................................... 64
FIGURE 1.4 Specimen of Terminalia sericea in northern Botswana.................................... 65
FIGURE 1.5 Combretum platypetalum, young flowering shoot from underground rootstock.
Specimen collected in the Haka game reserve, Harare, Zimbabwe. ............................... 65
FIGURE 1.6 Combretacous hair. ........................................................................................... 65
FIGURE 1.7 Leaf scale of Combretum collinum subsp. suluense, observed under microscope
after staining.................................................................................................................... 66
FIGURE 1.8 Leaf glandular hair of Quisqualis indica observed under scanning electron
microscope (SEM). Photograph: P.M. Tilney................................................................. 66
FIGURE 1.9 Leaf scale of Combretum hereroense observed under scanning electron
microscope (SEM). ......................................................................................................... 66
FIGURE 1.10 Extrafloral nectaries (EFN) on petiole of Terminalia arjuna. ........................ 67
FIGURE 1.11 Axillary and simple inflorescence of Combretum imberbe. ........................... 67
FIGURE 1.12 Terminal and ramified inflorescences on Combretum collinum subsp. gazense.
......................................................................................................................................... 67
FIGURE 1.13 Globular inflorescences on Combretum mkuzense. ........................................ 68
FIGURE 1.14 Elongated inflorescences on Combretum celastroides subsp. orientale........ 68
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Index to Figures
FIGURE 1.15 Inflorescence of Terminalia trichopoda with apetalous flowers. ................... 68
FIGURE 1.16 Flowers with petals of Lumnitzera racemosa. ................................................ 69
FIGURE 1.17 Flowers of Quisqualis indica, the upper hypanthium is developed into a
narrow and elongated attractive structure. ...................................................................... 69
FIGURE 1.18 Flowers with nectariferous disk of Combretum celastroides subsp. orientale.
......................................................................................................................................... 69
FIGURE 1.19 Inflorescences of Combretum fruticosum, with scentless flowers and elongate
stamens. Photograph: M. Garcia. .................................................................................... 70
FIGURE 1.20 Four-winged fruits of Combretum microphyllum. .......................................... 70
FIGURE 1.21 Round fruit of Combretum bracteosum. ......................................................... 70
FIGURE 1.22 Summary tree of relationships within Myrtales. General topology is from
Soltis et al. (2000) with modifications from Savolainen et al. (2000b) and Clausing &
Renner (2001).................................................................................................................. 71
CHAPTER 2
FIGURE 2.1 A single randomly selected (of the 6 340) equally most parsimonious tree based
on the combined plastid data (TL = 1 148 steps, CI = 0.48 and RI = 0.76). Numbers
above the branches are Fitch branch lengths (DELTRAN optimisation), and those below
the branches are bootstrap percentages above 50%. Arrows indicate groups not present
in the strict consensus tree............................................................................................. 106
FIGURE 2.2 One of the 3 910 equally parsimonious trees based on the combined plastid data
(TL = 1,037 steps, CI = 0.72 and RI = 0.88). Numbers above the branches are Fitch
lengths (DELTRAN optimisation), and those below the branches are bootstrap
percentages above 50%/Bayesian PPs > 0.5. Arrows indicate clades not present in the
12
Index to Figures
strict consensus tree. Current subtribal (Vollesen, 1981) and sectional (Stace, 1980a)
classification is indicated on the right. .......................................................................... 108
FIGURE 2.3 One of the 2 500 Fitch trees obtained from the analysis of ITS. Numbers above
the branches are Fitch lengths (DELTRAN optimisation), and those below the branches
are bootstrap percentages above 50%/Bayesian PPs > 0.5. Arrows indicate clades not
present in the strict consensus tree. (TL = 1,744 steps, CI = 0.41 and RI = 0.78). Current
subtribal (Vollesen, 1981) and sectional (Stace, 1980a) classification is indicated on the
right. .............................................................................................................................. 110
FIGURE 2.4 One of the 184 most parsimonious trees (3 163 steps, CI = 0.46, RI = 0.76)
from the combined plastid and nuclear ITS data set. Numbers above the branches are
Fitch lengths (DELTRAN optimisation), and those below the branches are bootstrap
percentages above 50%/Bayesian PPs > 0.5. Arrows indicate clades that collapse in the
strict consensus tree. Current subtribal (Vollesen, 1981) and sectional (Stace, 1980a)
CHAPTER 3
FIGURE 3.1 Distribution maps for members of Combretum sections Angustimarginata,
Spathulipetala and Macrostigmatea s.s.: (a) Combretum caffrum, (b) Combretum
engleri, (c) Combretum erythrophyllum, (d) Combretum gillettianum (e) Combretum
kirkii, (f) Combretum kraussii, (g) Combretum mkuzense, (h) Combretum nelsonii, (i)
Combretum nwambiyana, (j) Combretum schumanni, (k) Combretum vendae, (l)
Combretum woodii, (m) Combretum zeyheri. Thick black line demarcates potential
geographical range. ....................................................................................................... 139
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Index to Figures
FIGURE 3.2 One of the six most parsimonious trees (364 steps, CI = 0.83, RI = 0.85) of
section Ciliatipetala from the combined plastid and nuclear ITS data. Branch lengths
(DELTRAN optimisation) are indicated above the branches, and bootstrap percentages
above 50%/Bayesian posterior probabilities below. Current sectional (Stace, 1980a)
FIGURE 3.3 Habit, habitat, climate, bark and stem morphological characters plotted on the
most parsimonious tree (Figure 3.2). Legends are described under the figure. ............ 142
FIGURE 3.4 Leaf anatomical characters plotted on one of the most parsimonious trees
(Figure 3.2). Legends are described under the figure. .................................................. 143
FIGURE 3.5 Leaf scales characters plotted on one of the most parsimonious trees (Figure
3.2). Legends are described under the figure. ............................................................... 144
FIGURE 3.6 Inflorescence and flower characters plotted on one of the most parsimonious
trees (Figure 3.2). Legends are described under the figure........................................... 145
FIGURE 3.7 Fruits and germination characters plotted on one of the most parsimonious trees
(Figure 3.2). Legends are described under the figure. .................................................. 146
FIGURE 3.8 Combretum kraussii: scale from leaf............................................................... 147
FIGURE 3.9 Combretum mkuzense: scale from leaf. ........................................................... 147
FIGURE 3.10 Scale details of Combretum nwambiyana. .................................................... 147
FIGURE 3.11 Herbarium specimen of Combretum nwambiyana (Bryden 154), with fruit
details. ........................................................................................................................... 148
FIGURE 3.12 Combretum nwambiyana: habitat and slender habit. .................................... 149
FIGURE 3.13 Combretum nwambiyana: a multi-stem low branching tree with young
branches showing a slender habit.................................................................................. 149
14
Index to Figures
FIGURE 3.14 Combretum nwambiyana: yellowish pale bark largely covered with lichens.
....................................................................................................................................... 150
FIGURE 3.15 Combretum nwambiyana: branchlet with large sized fruits. ......................... 150
FIGURE 3.16 Combretum nwambiyana: germinating seed. ................................................ 150
FIGURE 3.17 Herbarium specimen of Combretum nwambiyana (Brynard & Pienaar 4259),
with inflorescence and flower details............................................................................ 151
CHAPTER 4
FIGURE 4.1 Distribution maps for members of Combretum section Ciliatipetala: (a)
Combretum acutifolium, (b) Combretum albopunctatum, (c) Combretum apiculatum
subsp. apiculatum, (d) Combretum apiculatum subsp. leutweinii (e) Combretum
edwardsii, (f) Combretum moggii, (g) Combretum molle, (h) Combretum nigricans, (i)
Combretum petrophilum, (j) Combretum psidioides (all subspecies), (k) Combretum
stylesii, (l) Combretum viscosum, (m) Combretum sp. nov. A, (n) Combretum sp. nov.
C., (o) Combretum sp. nov. D. Thick black line demarcates potential geographical range.
....................................................................................................................................... 175
FIGURE 4.2 The most parsimonious tree (466 steps, CI = 0.72, RI = 0.60) of Combretum
section Ciliatipetala from the combined plastid and nuclear ITS data. Branch lengths
(DELTRAN optimisation) are indicated above the branches, and bootstrap percentages
above 50%/Bayesian PPs > 0.5 below. Arrows indicate branches that collapse in the
strict consensus tree. Current sectional classification (Stace, 1980a) is indicated on the
right. .............................................................................................................................. 177
FIGURE 4.3 Habit, habitat, climate, bark and stem morphological characters plotted on the
most parsimonious tree (Figure 4.2). Legends are described under the figure. ............ 178
15
Index to Figures
FIGURE 4.4 Leaf anatomical characters plotted on the most parsimonious tree (Figure 4.2).
Legends are described under the figure. ....................................................................... 179
FIGURE 4.5 Leaf scale characters plotted on the most parsimonious tree (Figure 4.2).
Legends are described under the figure. ....................................................................... 180
FIGURE 4.6 Inflorescence and fruit characters plotted on the most parsimonious tree (Figure
4.2). Legends are described under the figure. ............................................................... 181
FIGURE 4.7 Combretum stylesii: scale structure. Photograph. A.E. van Wyk.................... 182
FIGURE 4.8 Combretum edwardsii: scale from leaf. .......................................................... 182
FIGURE 4.9 Combretum molle: scale from leaf. ................................................................. 182
FIGURE 4.10 Combretum stylesii, Herbarium specimen (Styles 2489) showing flower (Styles
3309) and fruit details (Styles 2489). ............................................................................ 183
FIGURE 4.11 Combretum stylesii: climbing habit showing stem strangling Euphorbia
tirucalii.......................................................................................................................... 184
FIGURE 4.12 Combretum stylesii, branch with fruits. Photograph. D. Styles. ................... 184
FIGURE 4.13 Combretum stylesii, flower details. Photograph. D. Styles. .......................... 184
FIGURE 4.14 Combretum stylesii: fruit details. Photograph. D. Styles. ............................. 185
FIGURE 4.15 Combretum stylesii: germinating seed. Photograph. D. Styles. .................... 185
FIGURE 4.16 Tugela Valley, KwaZulu-Natal; habitat of Combretum stylesii. Photograph.
D. Styles. ....................................................................................................................... 185
FIGURE 4.17 Tugela Valley, KwaZulu-Natal; habitat of Combretum stylesii. Photograph. D.
Styles. ............................................................................................................................ 186
16
Index to Figures
CHAPTER 5
FIGURE 5.1 Chronogram obtained based on rbcL for the order Myrtales. Abbreviations:
Memec = Memecylaceae; CAROP = Crypteroniaceae, Alzateaceae, Rhynchocalycaceae,
Oliniaceae and Penaeaceae; Vochys = Vochysiaceae; PsiHet = Psiloxylaceae and
Heteropyxidaceae. Values at nodes are age estimates, and numbers underneath branches
refer to the text. ............................................................................................................. 216
FIGURE 5.2 Chronogram of Combretaceae obtained from the combined analysis of rbcL,
ITS, trnH-psbA and psaA-ycf3. Abbreviations: Glabrip.= Glabripetala; Mic.=
Micrantha; Brev. = Breviramea; Cam.= Campbestria, Imberb.= Plumbea; Haplos.=
Haplostemon; Trichopetal.= Trichopetala; Calopyx.= Calopyxis; Gra. = Grandiflora;
Poiv.= Poivrea; Ox.= Oxystachia; Meg.= Megalanthara. Values at nodes are age
estimates, and numbers underneath branches refer to the text...................................... 218
FIGURE 5.3 Habitat mapped onto the phylogenetic tree for subtribe Combretinae. .......... 219
FIGURE 5.4 Climate mapped on phylogenetic tree for subtribe Combretinae. .................. 220
FIGURE 5.5 Shape of the upper hypanthium mapped on phylogenetic tree for subtribe
Combretinae. ................................................................................................................. 221
FIGURE 5.6 Type of trichomes mapped on phylogenetic tree for subtribe Combretinae... 222
FIGURE 5.7 Number of cells per leaf scale mapped on phylogenetic tree for subtribe
Combretinae. ................................................................................................................. 223
FIGURE 5.8 Mangrove distribution, where Geomorphic and climatic barriers explain the
Eurafrican gap. Illustration from Plaziat et al., 2001. ................................................... 224
FIGURE 5.9 Flowers of Combretum celastroides. The Upper hypanthium is flat shaped and
such characters is viewed as possible ancestral state within Combretum. .................... 224
17
Index to Figures
FIGURE 5.10 Flowers of Combretum imberbe, previously part of section Hypocrateropsis,
which is now transferred into its own section, Plumbea. The species also present an
upper receptacle almost flat. Petals are almost inexistent............................................. 224
FIGURE 5.11 Inflorescences and flowers of Combretum apiculatum. The upper receptacle
is conical, petals are absent. .......................................................................................... 225
FIGURE 5.12 Inflorescence and flowers of Combretum kraussii. The shape of the upper
hypanthium is cupuliform to infudibuliform. Petals are smalls but the upper hypanthium
is colourfull. .................................................................................................................. 225
FIGURE 5.13 Inflorescence and flowers of Combretum elaeagnoides. .............................. 225
FIGURE 5.14 Flower of Combretum platypetalum. The species belongs to section
Conniventia (subgen. Cacoucia) and is closely related to C. paniculatum and C.
microphyllum. The red colour is also observed on other species such as C. bracteosum,
which belong to section Trichopetala. .......................................................................... 226
FIGURE 5.15 Inflorescence and flowers of Combretum paniculatum (section Conniventia).
....................................................................................................................................... 226
FIGURE 5.16 Flower of Combretum indica (syn. Quisqualis indica). The floral structure in
section Quisqualis (subgen. Cacoucia) present the extreme form in term of upper
hypanthium shape where it is long and tubular. Petals are well developed and colourfull.
....................................................................................................................................... 226
FIGURE 5.17 Inflorescence and flowers of Combretum grandiflorum (section Grandiflora).
....................................................................................................................................... 227
FIGURE 5.18 Inflorescence and flowers of Combretum coccineum (section Poivrea).
Illustration from http://www.mobot.org, voucher Andrianjafy 1618 CB...................... 227
18
Index to Figures
FIGURE 5.19 Flower of Combretum mossambicense (section Trichopetala). The upper
hypanthium is comical to campanulate. The flowers show a tendency to the elongation
of the upper receptacle and petals are well developed. ................................................. 227
19
20
Abstract
ABSTRACT
The complexity of Combretaceae and lack of information on phylogenetic relationships
within the family led me to explore relationships between and within genera of
Combretaceae by means of combined analyses of plastid (rbcL, psaA-ycf3 spacer, and
psbA-trnH spacer) and nuclear ribosomal ITS sequences for all but three of the 17 genera in
Combretaceae. The current classification of the family into two subfamilies,
Strephonematoideae and Combretoideae, is corroborated. Within Combretoideae, division
into two tribes, Laguncularieae and Combreteae, is strongly supported. Within Combreteae
subtribe Terminaliinae relationships between genera are largely unresolved. Terminalia is
not supported as monophyletic, and two groups were identified, one containing mainly
African species and another of mostly Asian species. Pteleopsis, Buchenavia and
Anogeissus are embedded within Terminalia, and I suggest that all genera of Terminialiinae
with the exception of Conocarpus should be included into an expanded Terminalia. Within
subtribe Combretinae, a clade formed by the two monotypic genera Guiera and
Calycopteris is sister to the rest of the subtribe. Within Combretinae, groupings are
consistent with recent results based on morphological data. Combretum is currently divided
into three subgenera: Apethalanthum, Cacoucia and Combretum. The two last were
included in this study and supported as monophyletic. Meiostemon is sister to subgenus
Combretum, and Quisqualis is embedded within subgenus Cacoucia. I recommend that
subgenus Combretum should be expanded to include Meiostemon and subgenus Cacoucia
to include Quisqualis. The sectional classification within Combretum proposed in earlier
morphological studies is confirmed except for the exclusion of Combretum imberbe from
section Hypocrateropsis into a separate and monotypic section and the inclusion of
21
Abstract
Combretum zeyheri (section Spathulipetala) within section Macrostigmatea. In order to
accommodate Combretum imberbe a new section is suggested which is formally described
in Maurin et al. (2010). The reinstatement of previously recognised sections Grandiflora
and Trichopetala, both of which had been sunk into subgenus Cacoucia section Poivrea, is
also suggested. In this study two new species from South Africa are presented: Combretum
nwambiyana O.Maurin, M.Jordaan & A.E.van Wyk and Combretum stylesii Maurin,
Jordaan & A.E.van Wyk. The formal description of these two new species will be done in
regular journals.
Divergence time estimates using a Bayesian MCMC approach implemented in
BEAST suggested a crown date for Combretaceae around 82.6 mya with the two subtribes
Combretinae and Terminaliinae splitting at the end of the Late Cretaceous during a period
marked by a number of mass extinctions both in plants and animals. The Miocene and
Pliocene are characterised by constant speciation with many clades within Combretaceae
succesfully adapting to savanna vegetation and diversifying within it.
22
23
24
Foreword
FOREWORD
This thesis is presented in five chapters. The research topics (Chapters 2 to 5) are
preceeded by an introduction (Chapter 1) describing the motivation for the study. Chapter 2
is the first of three chapters dealing with the taxonomy of Combretaceae and in particular
southern African Combretum. The factual content of Chapters 2 to 4 is as published,
although the format has been standardised to provide uniformity throughout the thesis. The
papers are as follows:
(1) “Phylogenetic relationships of Combretaceae inferred from nuclear and plastid DNA
sequence data: implications for generic classification”, Botanical Journal of the Linnean
Society, accepted November 2009 (Chapter 2).
(2) “Notes on the phylogeny, classification and biogeography of Combretum section
Ciliatipetala (Combretaceae), with the description of a new species from South Africa”,
submitted September 2009 (Chapter 4).
(3) Chapter 3 focuses on sections Angustimarginata, Macrostigmatea and Spathulipetala
with a description of a new species from the Kruger National Park. In the chapter the floral
descriptions are based on relatively old herbarium material. During December 2009 I will
collect flowering material, which will enable me to complete the species description.
(4) Chapter 5 deals with the evolutionary history and biogeography of Combretaceae. The
paper is in preparation and will be submitted for publication in 2010.
The research papers are followed by a summary (Chapter 6). The two manuscripts
presented in Annexes 1 and 2 are added as supplementary information and are not a formal
part of the thesis. This work resulted from collaborative research with Braam van Wyk and
Marie Jordaan and have been submitted for publication in Bothalia.
25
Foreword
All pictures in the documents (with the exception of annexes 1 and 2), unless
stated, are from the author of the dissertation.
26
27
28
Acknoledgments
ACKNOWLEDGMENTS
I am grateful to Prof. Michelle van der Bank, associate professor at the University of
Johannesburg, for her supervision, support of my work, and confidence in my abilities. I
shall also praise her patience over the last four years for supporting me at all time in
pursuing and submitting the thesis.
I am very grateful to Prof. Mark W. Chase, Keeper of the Jodrell Laboratory at The Royal
Botanic Gardens Kew (UK), for his support, time and advise in the set-up of the project
and follow up and as my co-supervisor.
I am very thankful to Prof. Abraham E. van Wyk from H.G.W.J. Schweickerdt Herbarium
at Department of Plant Science from University of Pretoria, for our collaborative work, his
suggestions and advise on several chapters of this thesis.
My sincere thanks to Marie Jordaan from the National Herbarium at Pretoria (SANBI), for
our collaborative work on the family Combretaceae for the past four years.
Chapter 5 devoted to Biogeography in the thesis involved the help, suggestions and
corrections of several people who I wish to thanks gratefully: Prof. Vincent Savolainen
from Imperial College (UK) for giving me the opportunity to visit his facility at Silwood
Park and develop my knowledge in the field of Biogeography; Dr. Felix Forest Head of the
Molecular Systematics Laboratory at the Royal Botanic Gardens Kew (UK), for advice,
sharing ideas and correcting the final draft; Dr. Jan Schnitzler for his patience in training
29
Acknoledgments
me to the use of biogeography software while at Imperial College; Dr. James Richardson
for helping me with the biogeographical analysis and for advise; and Prof. Nina Rønsted
for her advice and suggestions.
Dr Martyn Powell for proofreading most of the chapters of the thesis.
I must also thank many people that were involved or with whom I interacted during the last
four years: Robert Archer, Herman van der Bank, Roy Bengis, Patricia Berjak, Yanis
Bouchenak-Khelladi , Christien Bredenkamp, Laslo Csiba, Meg Coates-Palgrave, Aaron
Davis, Mike Fay, Tinus Fourie, Tim Fulcher, Hugh Glen, Johan Hurter, Clyde Imada, Ernst
van Jaarsveld, Edith Kapinos, Eve Lucas, Gillian Maggs-Kölling, Desiree Marimuthoo,
Bongizwe Mgenge, Jacob Mlangeni, Stephen Midzi, Annah Moteetee, Alpheus Mothapo,
Lebo Cynthia Motsi, Magda Nel, Velly Nlovo, Bosa Okoli, Thomas Rikombe, Joshlyn
Sand, Yashica Sing, Clive Stace, Hester Steyn, David Styles, Patrica Tilney, Pieter Winter,
Elsa van Wyk and Guin Zambatis.
I also need to thank the following institution for their financial help and plant collecting
permits, or for providing or processing plant material: The National Botanical Research
Institute Namibia (NBRI), Ministry of Tourism Namibia, The Millennium Seed Bank, The
Missouri Botanical Garden , University of Johannesburg, The Royal Botanic Gardens Kew,
The South African National Biodiversity Institute (SANBI) and The National Research
Foundation (NRF; South Africa.
30
Acknoledgments
I am very grateful to my family mostly to Guy, Michèle and Laurence for their constant
support, to Edouard for all his advice and Annaelle and Matteo my favourite niece and
nephew. I also want to thanks my good friends, several whom have their names mentioned
above.
31
32
List of abbreviations
LIST OF ABBREVIATIONS
°C = Degrees Celsius
µm = micrometer
A.Chev. = Chevalier, A.
AIC = Akaike Information Criterion
a.s.l. = above sea level
Abh. Königl. Akad. Wiss. = Abhandlungen der Königl. Akademie der Wissenschaften zu
Berlin
ABI = Applied Biosystems, Inc
ACCTRAN = Accelerated transformation optimisation
Afzel. = Afzelius, A.
APG = Angiosperm Phylogeny Group
Aubrév. = Aubréville, A.
BEAST = Bayesian Evolutionary Analysis Sampling Trees
Benth. = Bentham, G.
BI = Bayesian inference
BISH = Herbaria of the Bishop Museum, Honolulu, U.S.A.
Boj. = Bojer, W.
Bol. Soc. Brot. sér. = Boletim da Sociedade Broteriana
bp = base pair
BP = Bootstrap Percentage (support)
ca. = approximately
CAROP = Crypteroniaceae, Alzateaceae, Rhynchocalycaceae, Oliniaceae and Penaeaceae
33
CI = Consistency Index
Cogn. = Cognieux, C.A.
Comm. = Commerson, P.
Corp. = Corporation
CTAB = Hexadecyltrimethylammonium bromide
Cult. = Cultivated
DC. = De candolle A.-P.
DELTRAN = Delayed transformation optimisation.
DMSO = Dimethyl Sulfoxide
DNA = Deoxyribonucleic acid
DRC = Democratic Republic of Congo
Dumort. = Dumortier, B.C.J.
e.g. = exempli gratia (for example)
Eckl. = Ecklon, C.F.
Edinb. Phil. Journ. = The Edinburgh New Philosophical Journal
EFN = Extrafloral nectaries
Engl. = Engler, H.G.A.
EtOH = Ethanol
F = Forward primer
FAA = Formaldehyde – Acetic acid – Ethanol, a preservative of plant material
F.Hoffm. = Hoffmann, F.
F.Muell. = von Mueller, F.J.H.
g = gram
G.Forst. = Forster, J.G.A.
34
Gaertn. = von Gaertner, C.F.
Gagnep. = Gagnepain, F.
GenBank = National Center for Biotechnology Information
Gerr. = Gerrard, W.T.
GTR+I+G = General Time Reversible + Gamma + Proportion Invariant
Guill. = Guillemin, J.B.A
Harv. = Harvey, W.H.
Hochst. = Hochstetter, C.F.F.
holo. = holotype
Hook.f. = Hooker, J.D.
i.e. = id est (that is)
ILD = Incongruence length test
Inc. = Incorporated
iso. = Isotype
ITS = Internal Transcribed Spacer
J.R.Forst. = Forster, J.R.
J.St.-Hil. = Saint-Hilaire, J.H.J.
JRAU = Herbarium of the University of Johannesburg (UJ), Johannesburg, South Africa
Juss. = de Jussieu, A.L.
K = Herbarium of the Royal Botanic Gardens, Kew, Richmond, United Kingdom
KNP = Kruger National Park
KZN = KwaZulu-Natal province
L. = Linnaeus (von Linné), Carl (1707-1778)
L.f. = Linnaeus (von Linné), Carl (1742-1783)
35
Lam. = de Lamarck, J.P.A.P. de M.
Lindl. = Lindley, J.
LTT = Lineage through time plot
m = meter
Marc.-Berti = Marcano-Berti, L.
Mart. = von Martius, C.F.P.
MCMC = (Bayesian) Markov Chain Monte Carlo
Mildbr. = Mildbraed, G.W.J.
min = Minutes
min. = Minimum
mm = millimeter
MO = Herbarium of the Missouri Botanical Garden, St. Louis, U.S.A.
MP = Maximum Parsimony
MRCA = Most recent common ancestor
Müll.Arg. = Müller of Aargau
MulTrees = Multiple equally parsimonious trees
Mya = Millions years ago
N.E. Br. = Brown, N.E.
NaCl = Sodium Chloride
NBRI = National Botanical Research Institute Namibia
NH = Natal Herbarium
No. = Number
nom. cons. = nomen conservandum
nom. cons. emend. prop. = nomen conservandum emendatus propositus
36
nom. rej. prop. = nomen rejiciendum propositus
nrDNA = nuclear ribosomal deoxyribonucleic acid
NRF = National Research Foundation (South Africa)
PAUP = Phylogenetic Analysis Using Parsimony software program
PCR = Polymerase chain reaction
Perr. = Perrottet, G.S.
Pers. = Persoon, C.H.
Pflanzenw. Ost-Afrikas C = Die pflanzenwelt Ost-Afrikas und der nachbargebiete
PHMV = Psiloxylaceae/Heteropyxidaceae/Myrtaceae/Vochysiaceae
PP = Posterior probabilities
PRE= Herbarium of South African National Botanical Institute, Pretoria, South Africa
PRU = HGWJ Schweickerdt Herbarium, University of Pretoria.
psaA-ycf3 = intergenic spacer between the psaA and ycf3 genes
PVP = Polyvinyl pyrolidone
R = Reverse primer
R.Br. = Brown, R.
rbcL = ribulose-bisphosphate carboxylase gene
RBG Kew = the Royal Botanic Gardens Kew
RI = Retention Index
Roxb. = Roxburgh, W.
Ruíz & Pav. = Ruíz Lopez, H and
SANBI = South African National Botanical Institute
sect. nov. = section novis
SEM = Scanning Electron Microscope
37
s.l. = sensu lato
s.s. = sensu stricto
Sitzungsber. Acad. Wien, Math. -Nat. = Sitzungsber. der Kaiserlichen Akademie der
Wissenschaften Wien, Math.-Naturwiss
Sond. = Sonder, O.W.
Sonn. = Sonnerat, P.
sp. nov. = species novis (new species)
Suess. = Suessenguth, K.
Schweick. = Schweickerdt, H.G.W.J
Swynn. = Swynnerton, C.F.M.
Syn = Synonymous
Taub. = Taubert, P.H.W.
TBR = Tree-bisection-reconnection
TIM + G = Transitionnal Model + Gamma
TL = Tree length
trnH-psbA = spacer between trnH and psbA genes
Tul. = Tulasne, R.L.
UCLN = Uncorrelated lognormal
UK = United Kingdom
USA = United States of America
UV = Ultraviolet
Verdc. = Vercourt, B.
Wall. = Wallich, N.
Warm. = Warming, J.E.B
38
Willd. = von Willdenow, C.L.
Zeyh. = Zeyher, C.L.P.
39
40
Chapter 1: General introduction and objectives
CHAPTER 1: GENERAL INTRODUCTION AND OBJECTIVES
1.1 GENERAL INTRODUCTION
Combretaceae R. Br. consist of trees, shrubs and lianas with up to 23 genera currently
recognised (Stace, 2007). The list of genera recognised in this study, intrafamilial
classification, number of species and distribution are listed in Table 1.1. They occur
worldwide in tropical and subtropical ecosystems, particularly forests, open dry savannas
and mangroves (Figure 1.1). In forests and their margins, large trees, often with a typical
flat-topped shape (Terminalia L.), or lianas (Combretum Loefl. subgenus Cacoucia Exell
& Stace, Quisqualis L.) are usually found. In drier environments, such as open savannas,
Combretaceae are mainly represented by medium to large shrubs (Figures 1.2 to 1.4).
Some species in these dry environments are adapted to frequent fires, and they produce
small flowering shoots from an underground trunk (Combretum platypetalum Welw.;
Figure 1.5). In drier habitats lianas are also present (Combretum microphyllum Klotzsch)
as well as trees and shrubs that possess scandent shoots, resembling climbers (Combretum
mossambicense Engl. and Combretum kraussii Hochst.).
Combretaceous hairs, unicellular, slender, with thick walls and a distinctive basal
compartment on the epidermis of leaves, are one of the defining features of Combretaceae
(Heiden, 1893; Stace, 1965; Tilney, 2002; Figure 1.6). These hairs can vary in form and
shape and are useful for species identification. Leaves in the family are generally opposite
to whorled, simple, entire and evergreen or deciduous. The leaves of Combretum and
Terminalia species may have domatia at the axis of main and lateral veins, but these are
marginal in Strephonema Hook.F. Combretaceae are also characterised by scales or
41
stalked glands. These multicellular structures are generally more abundant on the lower
surfaces of the leaf blade, but they can also occur on inflorescences and fruit. Scales
generally occur in Combretum subgenus Combretum Loefl. (Combretinae Exell & Stace),
as well as Guiera Adans. and Calycopteris Lam. (Stace, 1965, 2007; Figures 1.7 and 1.9),
whereas stalked glands are found in Combretum subgenus Cacoucia, including Quisqualis
and Calopyxis Tul. (Stace, 1965; Figure 1.8). Extra floral nectaries have been recorded in
some members of Combretaceae: some species of Terminalia (Figure 1.10), Laguncularia
racemosa C.F. Gaeertn, Meisotemon Exell & Stace, Pteleopsis Engl., and Quisqualis
(Bielbl & Kinzel, 1965; Belin-Depoux, 1978; Tilney & Van Wyk, 2004).
Inflorescences are axillary or terminal in Combretaceae and can be simple to
ramified or globular to elongate (Figures 1.11 to 1.15). Flowers are generally bisexual,
rarely dioecious, 4-5-merous, largely actinomorphic and sometimes slightly zygomorphic.
The hypanthium surrounding the ovary (or lower hypanthium) is extended and tubular
(upper hypanthium). The sepals (4-5) are inserted on the tip of the upper hypanthium. The
four to five petals are often small (in some cases well developed) to inconspicuous or even
absent (Figures 1.16 to 1.19). Stamens are usually as many as sepals, generally in two
whorls, free and rarely adnate, with the exception of Meiostemon and Terminaliopsis
Danguy, in which a single whorl of stamens is found; anthers are tetralocular. A
nectariferous disc is often present at the base of the lower hypanthium (Figure 1.18). Two
types of pollen are found in Combretaceae, the first being tricoporate as in Strephonema,
Laguncularia C.F.Gaertn. and Dansiea Byrnes, and the second, in the remaining genera, is
heterocolpate (Stace, 2007). A unilocular ovary with 2-7 ovules and a simple style is
typical for the family.
42
Stace (2007) distinguished three main specialisations for pollination in the family,
namely (1) loss of petals, (2) enlargement of the upper hypanthium (Figure 1.17), and (3)
clustering of flowers into groups (Figure 1.19). Only a few taxa exhibit large, welldeveloped petals, as in Quisqualis and some Combretum, which appear to be pollinated by
hawkmoths. Taxa with inconspicuous to no petals employ different strategies to attract
pollinators; for example, in Combretum section Calopyxis the upper hypanthium is colorful
but not fragrant (possible sunbird pollination). Small, scented and nectariferous flowers
pollinated by a wide range of insects are common in the family, and unscented,
nectariferous flowers in large numbers without petals but with elongated stamens forming
large colorful spicate inflorescences are found in some of the American taxa, e.g.
Combretum fruticosum Stuntz (Figure 1.19).
Fruits of Combretaceae contain a single, mostly indehiscent seed with two to five
wings (Figure 1.20). Dispersal of seeds is variable and the papery wings are found in the
seeds of taxa occurring in open vegetation suggesting wind dispersal. Taxa with bigger
fruits without wings are mostly found in forests or close to water (e.g. Combretum
bracteosum Engl & Diels; Figure 1.21). Mangrove taxa have fruit that contain air pockets
allowing them to float. Two cotyledons are generally found, but in some cases there can be
up to five that are fused to form a circular cotyledon. Germination is for most species
typical, with shoots rising from between the cotyledons. In Combretum zeyheri Sond.,
stems and leaves are born on a shoot appearing underneath the fused cotyledon, whereas in
Combretum viscosum Exell the shoot originates below the cotyledon and emerges from the
ground a few centimeters away. This is in contrast with most other species in which the
shoot appears above the fused cotyledons.
43
The number of chromosomes generally varies between 2n = 24 and 26 (x = 12 and
13) with polyploids reaching up to 2n = 96 and 104 (Stace, 2007). Some DNA C-values
were reported for Terminalia, varying from 3.6 to 12.8 picograms (pg) (Bennet & Leitch,
1995; Ohri, 1996), and Anogeissus Wall., 2.0 to 2.8 pg (Orhi & Kumar, 1986; Bennet &
Leitch, 1997).
Fossil records of the family are numerous; however, their affiliation to
Combretaceae is not always certain because of the type of material observed, i.e. leaves
(Stace, 2007). Cretaceous fossils are mostly composed of leaves, and their identities are
unclear since it is difficult to confirm their taxonomic link to Combretaceae.
Terminalioxylon Schönfeld is the oldest known Combretaceae fossil and dates from the
Upper Cretaceous (Mädel-Angeliewa & Müller-Stoll, 1973). Friis et al. (1992) described
an extinct genus Esgueiria from flowers dating from the Late Cretaceous. Two species
were described from Portugal, Esgueria adenocarpa and E. miraensis (Friis et al., 1992),
and one from Japan, E. futabensis (Takahashi et al., 1999). Anogeissoxylon was reported
by Ahmed et al. (2007) to have an age of 65-54 mya. Recent fossils of Terminalia have
also been reported from the Late Oligocene/Miocene (De Franscheschi et al., 2008).
1.2 PLACEMENT OF COMBRETACEAE WITHIN MYRTALES
The order Myrtales Lindl.represent one of the best-studied orders of angiosperms, but
disagreements regarding composition of and relationships within the order still exist
(Dahlgren & Thorne, 1984; Conti et al., 1996; APG II, 2003; APG III, 2009). Myrtales
families are listed in Table 1.2. Currently Combretaceae are included in Myrtales (rosids)
with 10 other families: Alzateaceae S.A. Graham, Crypteroniaceae A. DC.,
44
Heteropyxidaceae Engl. & Gilg., Psiloxylaceae Croizat, Lythraceae J.St.-Hil. (including
Punicaceae Bercht. & J.Presl and Trapaceae Dumort.), Melastomataceae Juss. (including
Memecylaceae DC.), Myrtaceae Juss., Onagraceae Juss., Rhynchocalycaceae L.A.S.
Johnson & B.G.Briggs, and Vochysiaceae A.St.-Hil. (APG II, 2003). The small South
African families Oliniaceae Harv. & Sond. and Penaeaceae Sweet. are also sometimes
recognised within Myrtales (Soltis et al., 2005). APG III (2009) expanded Penaeaceae to
include Oliniaceae and Rhynchocalycaceae. Cronquist (1981, 1988) and Heywood et al.
(2007) placed Thymelaeaceae Juss., Lecythidaceae A. Rich, Rhizophoraceae Pers.,
Haloragaceae R.Br., and Gunneraceae Meisn. within Myrtales, but several recent
molecular studies clearly exclude them (Conti et al., 1993; Savolainen et al., 2000a, b;
Soltis et al., 2000.). According to these studies Myrtales are composed of two major clades
(Conti et al., 1993, 1996, 1997; Savolainen et al., 2000b; Soltis et al., 2000; Clausing &
Renner, 2001; Figure 1.22). Clade 1 consists of Combretaceae sister to Onagraceae +
Lythraceae, the last enlarged to include Trapa L.and Punica L., which were sometimes
placed in families of their own. Several molecular studies have focused on Onagraceae and
Lythraceae (Raven, 1979; Conti et al., 1993; Levin et al., 2003, 2004; Graham et al.,
2005). Although Combretaceae have been intensively studied using morphological
approaches (Engler & Diels, 1899, 1900; Exell, 1931, 1953, 1978; Stace, 1965, 1969,
1980a, 1980b; Exell & Stace, 1966; Alwan, 1983; El Ghazali et al., 1998; Tilney, 2002;
Tilney & van Wyk, 2004), there has been a lack of results regarding phylogenetic
relationships within the family (Tan et al., 2002). Clade 2 consists of two subclades. In
subclade one, Myrtaceae + Vochysiaceae are sister to Heteropyxidaceae Engl. & Diels +
Psiloxylaceae. Subclade two consists of Melastomataceae sister to Crypteroniaceae,
Alzateaceae and Rhynchocalycaceae, as successive sisters to Oliniaceae + Penaeaceae
45
(Conti et al., 1997; Savolainen et al., 2000b; Soltis et al., 2000; Clausing & Renner, 2001;
Figure 1.22).
1.3 TAXONOMIC HISTORY OF COMBRETACEAE (TABLE 1.3)
In 1810, Brown established Combretaceae and included nine genera: Terminalia,
Chunchoa Pav. (= Terminalia), Bucida L., Combretum, Cacoucia Aubl., Quisqualis,
Getonia Roxb. (= Calycopteris), Laguncularia C.F.Gaertn, and Conocarpus L. Brown’s
concept of the family was similar to the current classification although he did not include
two important genera described at the time, Lumnitzera Willd. and Guiera Adans. These
two genera were only incorporated into the family in 1828 by De Candolle (1828a), who
also added Pentaptera Roxb. (= Terminalia), Poivrea Comm. (= Combretum subgenus
Cacoucia section Poivrea), and Ramatuela Kunth (= Terminalia section Ramatuella),
which were described after 1810. The latter author also suggested the first internal
classification for the family based on cotyledon morphology. De Candolle (1828a)
described two tribes, Combreteae and Terminalieae. Combreteae consisted of Combretum,
Cacoucia, Quisqualis, Lumnitzera, and Ceratostachys Blume (the last now in Nyssaceae
Juss./Cornaceae Bercht. & J.Presl), which De Candolle (1828b) later removed from
Combreteae without being able to place it elsewhere. Terminalieae included Terminalia,
Chuncoa, Bucida, Getonia, Laguncularia, Conocarpus and Agathisantes Blume (= Nyssa
L., Nyssaceae/Cornaceae). De Candolle (1828b) excluded Bruguiera Sav. (now included in
the mangrove family Rhyzophoraceae) and Bobua DC. (= Bobu, = Symplocos,
Symplocaceae). He also subdivided Terminalieae in two groups based on petal
46
presence/absence; Laguncularia, Guiera and Poivrea were included in the group
possessing petals.
Don (1832) revised the classification proposed by De Candolle (1928a) and divided
Combretaceae into two tribes, Combreteae and Terminalieae, transferring Laguncularia,
Guiera and Poivrea from Terminaliées to Combreteae and excluding Ceratostachys from
Combretaceae. Eichler (1867) suggested a similar classification with two tribes,
Terminalieae and Combreteae, characterised respectively by presence/absence of petals. In
1880, Koehne suggested transfer into Combretaceae of Strephonema Hook.f, a new genus
from tropical West Africa that had previously been included in Lythraceae.
In 1899-1900, Engler & Diels proposed a classification of Combretaceae that has
provided a sound framework for further investigations into this group. They supported
inclusion of Strephonema in Combretum, but kept it separate from the remaining taxa by
creating the subfamily Strephonematoideae. All remaining genera were included in the
subfamily Combretoideae, which were divided into four tribes: Combreteae, Terminalieae,
Calycopterideae, and Laguncularieae. They transferred Cacoucia from Terminalieae to
Combreteae. Sectional classifications for Combretum and Terminalia, the two largest
genera in the family, were also proposed. Several years later, Exell (1931) also followed
the classification of Engler & Diels (1899, 1900) with the following exceptions: (1)
Laguncularieae differ considerably from the other three tribes Combreteae, Terminalieae,
and Calycopterideae so they were separated from them, and (2) re-circumscription of
Quisqualis by transferring to it several species previously included in Combretum.
In 1966, Exell & Stace again redefined the classification based on the observations
of Exell (1931) and proposed that within Combretaeae only two tribes should be
recognised: Laguncularieae and Combreteae. The latter was divided into three subtribes:
47
Combretinae, Terminaliinae and Pteleopsidinae (the last comprising only Pteleopsis).
Pteleopsis has long been considered as an intermediate between Combretum and
Terminalia (Exell, 1931; Exell & Stace, 1966), but in 1981 Vollesen concluded that
Pteleopsis is more closely related to Terminalia than it is to Combretum. Exell & Stace
(1966) also segregated Meiostemon and Terminaliopsis from Combretum and Terminalia,
respectively, as they are the only representatives in Combretaceae that have a single row of
stamens. In 1981 an Australian endemic genus Dansiea Byrnes was described and included
in Laguncularieae (Byrnes, 1981; Stace, 2007). A summary of the taxonomic history of
Combretaceae is provided in Tables 1.2 and 1.3.
The current classification of Combretaceae remains similar to that proposed by
Engler & Diels (1899) and later updated by Exell & Stace (1966). The infrageneric
classifications of the two largest genera (Combretum and Terminalia) of the family have
not received similar attention. Combretum is divided into three subgenera, Combretum,
Cacoucia and the monotypic Apethalantum Exell & Stace. Combretum is characterised by
scales, Cacoucia by glandular hairs, and Apethalantum by both. The sectional
classification within Combretum as first suggested by Engler & Diels (1899, 1900) was
updated through the years by various authors and today comprises 46 sections. Sectional
classification within Combretum and closely related genera is listed in Table 1.5. However,
a complete infrageneric treatment for Terminalia is still lacking.
In the present study, representatives of 17 genera were included (Table 1.1)
namely: (1) Combretum (~255 spp.) the largest genus in the family with its center of
distribution in Africa with around 224 species, (2) Terminalia (~190 spp.) the second
largest genus that is more equally distributed, although more species are present in Asia
and Africa, (3) Buchenavia Eichler the third largest genus of the family with ~24 species in
48
tropical America, (4) Strephonema Hook f. with three to four species of trees restricted to
tropical West Africa, (5) Laguncularia C.F.Gaertn a monotypic mangrove tree sometimes
with pneumatophores occurring on the eastern and western coasts of tropical America and
western coast of tropical Africa, (6) Lumnitzera Willd. with two mangrove species,
Lumnitzera racemosa Willd. occuring from the eastern coast of African (with the border
between Mozambique and South Africa as the southern most distribution), Madagascar,
and tropical Asia to the Pacific and Lumnitzera littorea (Jack.) Voigt distributed from
tropical Asia to northern Australia, (7) Macropteranthes F.Muell. with five species
endemic to northern Australia, (8) Dansiea Byrnes with two species of trees endemic to
northern Australia, (9) Pteleopsis Engl. with ~10 species of trees endemic to Africa, (10)
Anogeissus (DC.) Wall with five species of trees and shrubs from tropical West Africa to
Southeast Asia, (11) Finetia Gagnep. with a single species from Southeast Asia (Thailand,
Laos), (12) Conocarpus L. with two species, the first occurring in mangroves in the New
World and tropical West Africa tropics and the second restricted to the Horn of Africa and
southern Yemen, (13) Quisqualis L. with 16 species of lianas restricted to the Old World
tropics, (14) Meiostemon Exell & Stace, with two species and two subspecies of shrubs
namely, M. tetrandrus (Exell) Exell & Stace (Mozambique, Zambia and Zimbabwe) and
M. humbertii (Perrier) Exell & Stace (Madagascar), (15) Thiloa (Eichler) with three
species of small trees, shrubs or lianas endemic to northern South America, (16)
Calycopteris Lam. (= Getonia Roxb.) a monospecific genus of scrambling shrubs from
Southeast Asia, and (17) Guiera Adans. also a monospecific genus of shrubs occurring in
tropical West Africa. Calopyxis Tul. from Madagascar and Bucida L. from Central
America and Florida have been formally transferred to Combretum (Jongkind, 1995) and
Terminalia (Stace, 2002).
49
1.4 OBJECTIVES OF THE STUDY
This project was aimed at re-evaluating previous morphological hypotheses on generic
circumscriptions and affinities among the 17 genera of Combretaceae using molecular
(DNA) sequence data. The specific objectives of the study were to:
1. Reconstruct a phylogeny for Combretaceae (14 genera and 101 taxa) using DNA
sequences from the internal transcribed spacers (ITS) of nuclear ribosomal DNA and three
plastid regions (rbcL, trnH-psbA and psaA-ycf3), from which the major lineages and
generic relationships can be assessed. These were compared to the current taxonomy in
order to provide a better understanding of taxonomy and evolutionary relationships within
the group.
2. Determine the systematic placement of Meiostemon, Thiloa (Combretum subgenus
Combretum) and Quisqualis (Combretum subgenus Cacoucia) within Combretaceae.
3. Determine the possible inclusion of Pteleopsis, Buchenavia and Anogeissus in
Terminalia.
4. Examine the scale structures on the abaxial side of the leaf in Combretum subgenus
Combretum using microscopic techniques. These characters will be mapped onto a
phylogenetic tree to test the usefulness of scale structure for generic and sectional
circumscriptions and the use for the identification of sterile material.
5. Determine a date for the root node of Combretaceae using BEAST to establish when the
major radiation of the family took place and to understand issues relating to the dispersal of
the group and also biogeographical patterns.
50
Chapter 1: General Introduction of Objectives
TABLE 1.1 The 17 genera of Combretaceae recognised in this study. Number of species included for each genus from Mabberley (2008). The two genera in brackets
are recent changes
Subfamily
Tribe
Sub-tribe
Genus
No.
Geographical distribution
species
Strephonematoideae
Strephonema Hook.f. (1867)
3-4
Tropical West Africa
Engl. & Diels (1899)
Combretoideae Engl. &
Laguncularieae Engl. &
Laguncularia C.F.Gaertn
1
Eastern and Western Tropical America, tropical West Africa
Diels (1899)
Diels (1899)
(1807)
Lumnitzera Willd. (1803)
2
East Africa to Pacific
Macropteranthes F. Muell.
5
Australia
Dansiea Byrnes (1981)
2
Australia
Terminaliinae (DC.) Exell &
Anogeissus (DC.)Wall
8
Old World tropics
Stace (1966)
(1831)
Buchenavia Eichler (1866)
24
Tropical America
Conocarpus L. (1753)
2
Tropical American and African mangroves
Bucida L. (1759) (=
4
Florida, Central America, West Indies
(1863)
Combreteae DC. (1828)
Terminalia L.)
51
Pteleopsis Engl. (1894)
Terminalia L. (1767)
Combretinae
9
190
Tropical and Southern Africa
Tropics and subtropics
Finetia Gangnep. (1917)
1
Thailand, Laos
Calycopteris Lam. (1793)
1
Southeast Asia
23
Madagascar
255
Tropics and subtropics
(syn: Getonia Roxb.)
Calopyxis Tul. (1856) (=
Combretum)
Combretum Loefl. (1758)
Guiera Adans (1789)
1
North tropical Africa
Meiostemon Exell & Stace
2
Zambia, Zimbabwe and Madagascar
Quisqualis L. (1762)
16
Old World tropics
Thiloa Eichler (1866)
3
Tropical South America
(1966)
52
TABLE 1.2 Proposed families within Myrtales from 1981 to 2009.
Cronquist, 1981,
Soltis et al., 2005
Mabberley, 2008
APG, 2003
APG, 2009
1988
New classification (Mabberley,
2008; APG, 2009)
Alzateaceae
Alzateaceae
Crypteroniaceae
Alzateaceae
Alzateaceae
Combretaceae
Combretaceae
Combretaceae
Combretaceae
Combretaceae
Crypteroniaceae
Crypteroniaceae
Crypteroniaceae
Crypteroniaceae
Crypteroniaceae
Gunneraceae
-
-
-
-
Gunnerales
Haloragaceae
-
-
-
-
Saxifragales
Heteropyxidaceae
Heteropyxidaceae
Myrtaceae
Heteropyxidaceae
Myrtaceae
Lecythidaceae
-
-
-
-
Lythraceae
Lythraceae
Lythraceae
Lythraceae
Lythraceae
Melastomataceae
Melastomataceae
Melastomataceae
Melastomataceae
Melastomataceae
Memecylaceae
Memecilaceae
Melastomataceae
Melastomataceae
Melastomataceae
Myrtaceae
Myrtaceae
Myrtaceae
Myrtaceae
Myrtaceae
Oliniaceae
Oliniaceae
Crypteroniaceae
Oliniaceae
Penaeaceae
Onagraceae
Onagraceae
Onagraceae
Onagraceae
Onagraceae
Penaeaceae
Penaeaceae
Crypteroniaceae
Penaeaceae
Penaeaceae
Psiloxylaceae
Psiloxylaceae
Myrtaceae
Psiloxylaceae
Myrtaceae
Punicaeeae
Punicaceae
Lythraceae
Lythraceae
Lythraceae
Rhynchocalycaceae
Rhynchocalycaceae
Rhynchocalycacea
Penaeaceae
Crypteroniaceae
Ericales
e
Rhizophoraceae
-
-
-
-
Sonneratiaceae
Sonneratiaceae
Lythraceae
Lythraceae
Lythraceae
Thymelaeaceae
-
-
-
Trapaceae
Trapaceae
Lythraceae
Lythraceae
Lythraceae
Vochysiaceae
Vochysiaceae
Vochysiaceae
Vochysiaceae
Vochysiaceae
Malphigiales
Malvales
53
TABLE 1.3 History of genera recognised within Combretaceae from 1810 to 2007
Brown, 1810
De Candolle, 1828a
De Candolle, 1828b
Chunchoa Pers. (1805)
Bucida L. (1759)
Cacoucia Aubl. (1775)
Getonia Roxb. (1798)
Laguncularia C.F.Gaertn (1807)
Bucida L. (1759)
Guiera Adans. (ex Juss) (1789)
Pentaptera Roxb. (1832)
Poivrea Comm. (ex Thouars) (1811)
Ramatuella Kunth (1825)
Agathisanthes Blume (1826) (= Cornaceae)
Ceratostachys Blume (1826)(= Cornaceae)
Bruiguera (= Rhizophoraceae)
Bobua DC (1828) (= Symplocaceae)
-
Bucida L. (1759)
Agathisanthes Blume (1826)
Ceratostachys Blume (1826)
= Rhizophoraceae
Bobua DC (1828)
-
-
54
Don, 1832
Endlicher, 1840
Bentham & Hooker, 1865
Bucida L. (1759)
Agathisanthes Blume (1826)
= Cornaceae
Bobua DC (1828)
-
Bucida L. (1759)
= Cornaceae
= Symplocaceae
Anogeissus (DC.)Wall (1831)
Sphalanthus Jack (1822)
-
Bucida L. (1759)
Illigera Blume (1826) (= Hernandiaceae)
Gyrocarpus Jacq. (1763) (= Hernandiaceae)
Sparattanthelium Sparattanthelium
-
55
Eichler, 1867
Koehne, 1880
Brandis, 1893
Bucida L. (1759)
Illigera Blume (1826)
Gyrocarpus Jacq. (1763)
Sparattanthelium Mart.(1841)
-
Bucida L. (1759)
Illigera Blume (1826)
Gyrocarpus Jacq. (1763)
Sparattanthelium Mart.(1841)
Strephonema Hook f. (1867) (ex Lythraceae)
-
Bucida L. (1759)
Calycopteris Lam (1793) (= Getonia Roxb.
= Terminalia L.(1767)
= Hernandiaceae
= Hernandiaceae
= Hernandiaceae
Strephonema Hook f. (1867)
Macropteranthes F.Muell. (1863)
Calopyxis Tul. (1866)
-
56
Engler & Diels, 1899, 1900
Exell, 1931
Exell & Stace, 1966
Bucida L. (1759)
= Combretum Loefl. (1758)
Calycopteris Lam (1793)
= Ramatuella Kunth (1825)
-
Bucida L. (1759)
= Terminalia L. (1767)
= Quisqualis L. (1762)
Finetia Gagnep. (1816)
Terminaliopsis Danguy (1923)
-
Terminalia L. (1767) (= Chunchoa )
Bucida L. (1759)
Terminalia L. (1767) (= Pentaptera)
Combretum Loefl. (1758) (= Poivrea)
Meiostemon Exell & Stace (1966)
-
57
Jongking, 1995
Stace, 2002
Stace, 2007
Bucida L. (1759)
Combretum Loefl. (1758) (=Calopyxis)
-
Terminalia L.(1767) (= Bucida)
-
Combretum Loefl. (1758) (= Quisqualis)
Combretum Loefl. (1758) (= Thiloa)
Combretum Loefl. (1758) (= Meiostemon)
Terminalia L. (1767) (= Terminaliopsis)
Dansiea Byrnes (1981)
58
TABLE 1.4 History of classification within Combretaceae.
De Candolle, 1828a,1828b
Don, 1832
Combretées
Combreteae
Ceratostachys Blume (1826)(=
Cornaceae)
Poivrea Comm. (ex Thouars)
(1811)
Group 1
Guiera Adans.(ex Juss) (1789)
Poivrea Comm.(ex Thouars)
(1811)
Group2
Agathisanthes Blume (1826) (=
Cornaceae)
Bobua DC (1828) (=
Symplocaceae)
Bucida L. (1759)
Combreteae
Terminaliées
Endlicher, 1840
Terminalieae
Poivrea Comm. (ex Thouars)
(1811)
Terminalieae
Bobua DC (1828) (=
Symplocaceae)
Agathisanthes Blume (1826) (=
Cornaceae)
Bucida L. (1759)
Bucida L. (1759)
59
Bentham & Hooker, 1865
Eichler, 1867
Combreteae
Combreteae
Group1
Group2
Bucida L. (1759)
Gyrocarpeae
Terminalieae
Engler & Diels, 1899, 1900
Bucida L. (1759)
(1807)
Strephonematoideae
Combretoideae
Calycopterideae
Combreteae
Guiera Adans.(ex Juss) (1789)
Laguncularieae
Macropteranthes F. Muell.
(1863)
Terminalieae
Bucida L. (1759)
Illigera Blume 1826 (= Hernandiaceae)
Gyrocarpus Jacq. (1763) (=
Hernandiaceae)
Sparattanthelium Mart. (1841)(=
Hernandiaceae)
60
TABLE 1.5 Subgeneric and sectional classification of Combretum and closely related genera.
Genus
Subgenus
Section
No. of
species
recognised
Calycopteris
1(1)
Southeast Asia
Lam
Calopyxis Tul.
23 (1)
Combretum
Combretum Loefl.
Hypocrateropsis Engler &
Loefl.
(1758)
Diels (1899)
Madagascar
6
Africa
2
West Africa
4
Africa
11
Asia
6
West Africa
(1899)
1
South America
Discoloria Engler & Diels
2
South America
3
South America
1
South America
14
Africa and Madagascar
Polyneuron Exell (1937
1
Gabon
Combretastrum Eichler
11
Africa and America
1
Brazil
1
Asia
6
Asia
11
Africa
Micrantha Exell & Stace
(1969)
Campestria Engler & Diels
(1899)
Tetragonocarpus
C.B.Clarke (1878)
Tomentosa Engler & Diels
(1899)
Parviflora Engler & Diels
(1899)
Monetaria Engler & Diels
(1899)
Elegantia Engler & Diels
(1899)
Chionanthoidea Engler &
Diels (1899)
(1867)
Terminaliopsis Ridley
(1890)
Acuminata Engler & Diels
(1899)
Quisqualoidea C.B.Clarke
(1878)
Paucinervia Engler & Diels
(1899)
61
Paradoxa Engler & Diels
1
Congo, Gabon and Angola
3
America
12
America
Mettalicum Exell & Stace
4
Africa
1
Zambia and Angola
5
Africa
(1899)
Leprosa Engler & Diels
(1899)
(1968)
Aureonitentia Exell & Stace
(1969)
Breviramea Engler & Diels
(1899)
Ciliatipetala Engler & Diels
13+
Africa and Arabia
(1899)
Angustimarginata Engler &
6
Southern Africa
1
Africa
8
Africa
4
Africa
1
Congo and Gabon
10
Africa
Acuta Keay (1950)
1
West Africa
Paraquisqualis Exell &
1
Congo
1
India to Burma
1
Africa
2
Asia
Kaloedron Miq. (1856)
3
Asia
Capituliformaia Engler &
1
West Africa
Diels (1899)
Spathulipetala Engler &
Diels (1899)
Glabripetala Engler &
Diels (1899)
Macrostigmatea Engler &
Diels (1899)
Longipilosa Engler & Diels
(1899)
Fusca Engler & Diels
(1899)
Stace (1969)
Apetalanthum Exell &
Apetala Engler & Diels
Stace (1966)
(1899)
Cacoucia Exell &
Mucronata Engler & Diels
Stace (1966)
(1899)
Glandulosa Engler & Diels
(1899)
Diels (1899)
Lasiopetala Engler & Diels
2/3
Africa
62
(1899)
Conniventia Engler & Diels
20
Africa
4
Africa
Spinosa Exell (1953)
4
America
Oxystachia Exell (1968)
1
Namibia and Angola
(1899)
Racemosa Engler & Diels
(1899)
Poivrea G.Don (1832)
31 (6)
Africa, Madagascar and
Asia
Megalantherum Exell
1
Namibia and Angola
1
Congo
6
Africa and America
23
Madagascar
(1968)
Pseudoquisqualis Exell
(1968)
Cacoucia Exell & Stace
(1966)
Calopyxis Tul. (1856) (=
Calopyxis)
Guiera Adans
Meiostemon
(= subgenus Combretum
Exell & Stace
section Haplostemon Exell
1(1)
Northern tropical Africa
2 (2)
Zambia, Zimbabwe and
Madagascar
Quisqualis L.
16 (3)
Old World tropics
Thiloa Eichler
3 (1)
63
FIGURE 1.1 Distribution of the Combretaceae (from Heywood et al., 2007).
FIGURE 1.2 Specimen of Combretum
apiculatum subsp. apiculatum in northern
Botswana.
FIGURE 1.3 Large specimen of Combretum
imberbe along the Okavango river (Botswana).
.
64
FIGURE 1.4 Specimen of Terminalia sericea in northern Botswana.
FIGURE 1.5 Combretum platypetalum, young
flowering shoot from underground rootstock.
Specimen collected in the Haka game reserve,
Harare, Zimbabwe.
FIGURE 1.6 Combretacous hair.
65
FIGURE 1.7 Leaf scale of Combretum collinum subsp.
suluense, observed under microscope after staining
FIGURE 1.8 Leaf glandular hair of Quisqualis indica
observed under scanning electron microscope (SEM).
Photograph: P.M. Tilney
FIGURE 1.9 Leaf scale of Combretum hereroense observed under scanning electron microscope (SEM).
66
FIGURE 1.10 Extrafloral nectaries (EFN) on petiole of Terminalia arjuna.
FIGURE 1.11 Axillary and simple inflorescence of Combretum imberbe.
FIGURE 1.12 Terminal and ramified inflorescences on Combretum collinum subsp. gazense.
67
FIGURE 1.13 Globular inflorescences on Combretum mkuzense.
.
FIGURE 1.14 Elongated inflorescences on Combretum celastroides subsp. orientale.
FIGURE 1.15 Inflorescence of Terminalia trichopoda with apetalous flowers.
68
FIGURE 1.16 Flowers with petals of Lumnitzera racemosa.
FIGURE 1.17 Flowers of Quisqualis indica, the upper hypanthium is developed into a narrow and elongated
attractive structure.
FIGURE 1.18 Flowers with nectariferous disk of Combretum celastroides subsp. orientale.
69
FIGURE 1.19 Inflorescences of Combretum fruticosum, with scentless flowers and elongate stamens. Photograph: M.
Garcia.
FIGURE 1.20 Four-winged fruits of Combretum microphyllum.
FIGURE 1.21 Round fruit of Combretum bracteosum.
70
FIGURE 1.22 Summary tree of relationships within Myrtales. General topology is from Soltis et al. (2000) with
modifications from Savolainen et al. (2000b) and Clausing & Renner (2001).
71
72
Chapter 2: Phylogenetic relationships of Combretaceae
CHAPTER 2: PHYLOGENETIC RELATIONSHIPS OF COMBRETACEAE INFERRED FROM NUCLEAR
AND PLASTID DNA SEQUENCE DATA: IMPLICATIONS FOR GENERIC CLASSIFICATION
2.1 INTRODUCTION
Combretaceae R. Br. comprise 17 genera and approximately 525 species of trees, shrubs, lianas
and mangroves distributed mainly in tropical and subtropical Africa, but also in Central and
South America, southern Asia and northern Australia (Mabberley, 2008). The presence of
combretaceous hairs, unicellular with slender thick walls and a distinctive basal compartment on
the epidermis of the leaves is one of the defining features of Combretaceae (Stace, 1965; Tilney,
2002). These can vary in form and shape and are useful for species identification. Combretaceae
are also characterised by scales or stalked glands, which are multicellular structures that are
generally more abundant on the lower surfaces of the leaf blade and can also occur on
inflorescences and fruits. Scales generally occur in Combretum Loefl. subgenus Combretum
Exell & Stace, Guiera Adans. ex Juss. and Calycopteris Lam. (Stace, 1965, 2007), whereas
stalked glands are found in Combretum subgenus Cacoucia (Aublet) Exell & Stace, including
Quisqualis L. and Calopyxis Tul. (Stace, 1965).
The family is currently divided into two subfamilies, Combretoideae Engl. & Diels and
Strephonematoideae Engl. & Diels, the latter comprised of a single genus, Strephonema Hook.f.,
with three species of trees restricted to western tropical Africa. Strephonematoideae differ from
those of Combretoideae in possessing a semi-inferior ovary, whereas it is inferior for all taxa of
Combretoideae. Combretoideae are divided into two tribes, Laguncularieae Engl. & Diels and
Combreteae DC., based on adnate prophylls on the hypanthium of Languncularieae (Stace,
2007), whereas these are unfused in members of Combretoideae. Laguncularieae comprise four
73
genera of trees, shrubs and mangroves: Laguncularia C.F.Gaertn., a monotypic mangrove genus
of tropical America and western tropical Africa; Lumnitzera Willd. with two species of mangrove
shrubs and trees distributed from eastern tropical Africa to Australia including India and some
islands in the Indian and Pacific Oceans; Macropteranthes F.Muell. (five species) and Dansiea
Byrnes (two species), which both are trees and shrubs endemic to Australia.
Combreteae are divided into two subtribes, Terminaliinae (DC.) Exell & Stace and
Combretinae Exell & Stace. Terminaliinae include pantropical Terminalia L., the largest genus
of the subtribe comprising around 150 species of trees (often used as timber) and shrubs. The
name Bucida L. (1759) predates Terminalia (1767), and according to Stace (2002) its adoption to
cover species of Terminalia would require around 200 new combinations and is therefore highly
undesirable. Bucida, s.s. with three species all from Central America differs from all other
American species of Terminalia and from nearly all other Terminalia in possessing small fruits
that retain the upper portion of the hypanthium. However, according to Stace (2002) Terminalia
tetrandra (Danguy) Capuron, Terminalia mantaly H. Perrier and Terminalia mantaliopsis
Capuron from Madagascar also have fruits like those of Bucida. Stace (2002) concluded that
obviously the retained upper hypanthium is not unique to Bucida, and it should therefore be
amalgamated with Terminalia. Other genera in Terminaliinae are: Pteleopsis Engl., an African
tree genus of about ten species; Buchenavia Eichler, 20 species of trees and shrubs from tropical
America; Anogeissus (DC.) Wall., seven species of trees and shrubs distributed from western
tropical Africa to Southeast Asia including India; monotypic Finetia Gagnep., a tree endemic to
Thailand and Laos; and Conocarpus L., with two species of trees and shrubs growing in
mangroves from tropical America to tropical Africa including islands in the Atlantic Ocean to
Yemen in the Arabian Peninsula.
74
Combretinae contain the largest genus of the family, Combretum, with approximately 250
species of trees, shrubs, scandent shrubs and lianas occurring in tropical and subtropical regions
except in the Pacific and most of Australia. The most recent infrageneric classification (Stace,
1980b) divided Combretum into three subgenera: Combretum, Cacoucia and Apetalanthum Exell
& Stace. The first two subgenera include most of the species and are distinguished by scales
located mainly on the lower surface of the leaf in subgenus Combretum and by microscopic
stalked glands in subgenus Cacoucia (Engler & Diels, 1899; Exell, 1953, 1968, 1970, 1978;
Stace, 1969, 1980a, 1980b; Wickens, 1973; Tilney, 2002). Subgenus Apetalanthum comprises a
single species from Southeast Asia and possess both scales and glandular hairs. Africa is the
centre of diversity for the genus with 163 species (Klopper et al., 2006) compared to the
Americas with 33, Asia with 27 and Australia with one (Stace, 1980b; Pedley, 1990). According
to Stace (2007), Combretum currently includes Quisqualis, Calopyxis, Thiloa Eichler and
Meiostemon Exell & Stace, but not all these taxonomic changes have been formally published.
Jongking (1990) questioned the delimitation of Combretum versus Quisqualis. Quisqualis
comprises 16 species of lianas restricted to the Old World tropics and shares the morphological
characters of Combretum subgenus Cacoucia (i.e., absence of scales, presence of stalked glands).
Jongking (1995) also transferred Calopyxis to Combretum, including around 23 species endemic
to Madagascar. Thiloa, three species from the Neotropics, and Meiostemon, with two species
from southern Africa and Madagascar, have been often seen as close relatives of Combretum
subgenus Combretum. The two monotypic genera Calycopteris and Guiera are restricted to
Southeast Asia and western tropical Africa, respectively.
Since no comprehensive phylogenetic framework currently exists for Combretaceae,
exept for the study of Tan et al. (2002) with limited sampling, it is impossible to evaluate any of
the abovementioned taxonomic hypotheses. Thus, in this study, I have conducted a phylogenetic
75
analysis of Combretaceae using DNA sequence data from three plastid regions (rbcL, trnH-psbA
spacer and psaA-ycf3 spacer) and the internal transcribed spacers (ITS) of nuclear ribosomal
DNA. The main objectives were, firstly, to compare results of this study to the current
infrageneric taxonomy to determine if classification changes are needed and, secondly, to
evaluate the sectional classification within Combretum.
2.2 MATERIALS AND METHODS
2.2.1 Taxon sampling
Representatives of 14 of the 17 genera accepted in Combretaceae (including 101 species and
subspecies) were analysed in this study. Samples were chosen to represent the full range of floral
diversity and habits within the family (Table 2.1). Samples were collected during fieldwork in
Limpopo, Mpumalanga, Gauteng, KwaZulu-Natal (all provinces of South Africa) and Botswana,
Mozambique, Namibia and Zimbabwe. Samples from cultivated species from the Lowveld
National Botanical Garden (Nelspruit, South Africa), Pretoria National Botanical Garden
(Pretoria, South Africa), Kirstenbosch National Botanical Garden (Cape Town, South Africa),
National Botanic Garden, Harare (Zimbabwe) and the Honolulu Botanical Gardens (USA) were
also included, as well as material grown from seed collected in the wild, DNA banks and
herbarium specimens from the collections of the Missouri Botanical Garden (MO) and the Royal
Botanic Gardens, Kew (K). Four undescribed species from South Africa were also included and
will be described jointly with the South African National Biodiversity Institute (SANBI, South
Africa). Voucher specimen information and GenBank accession numbers for the taxa used in the
study are listed in the Appendix 2.1. I was unable to obtain fresh material for Dansiea,
Macropterantes, Finetia and Combretum apetalum, and PCR was unsuccessful from DNA
76
extracted from herbarium material, which prevents us from assessing relationships of the two
Australian genera and between the Combretum subgenus Apetalanthum with subgenera
Combretum and Cacoucia.
2.2.2 Outgroup and loci selection
The psaA and ycf3 spacer, rbcL and ITS regions were chosen because a recent study used these
genes (Tan et al., 2002), which enabled us to add to this pre-existing dataset. The trnH-psbA
spacer was also sequenced since it has proven to be useful at the species level in several families
of angiosperms (Sang et al., 1997; Lahaye et al., 2008). To select an appropriate outgroup for my
analyses, a broadly sampled rbcL dataset was analysed; it included 20 representatives of Myrtales
Lindl. and a representative of each of the following families: Annonaceae Juss., Escalloniaceae
R.Br. ex.Dumort., Geraniaceae Juss., Lamiaceae Martynov, Lauraceae Juss., Malvaceae Juss. and
Zygophyllaceae R. Br. (Figure 2.1). Previous studies did not reach a well-supported topology for
relationships among the various families of Myrtales, so I wished to re-confirm outgroup
relationships in this study using my own data. My results confirmed that the pair Strephonema
mannii Hook.f. and Strephonema pseudocola A.Chev. were sister to Combretoideae, and thus I
used the genus as outgroup in the single region analyses. For the combined molecular analysis of
Combretaceae I added three members of Myrtales (Galpinia transvaalica N.E. Br., Lythraceae
J.St.-Hil.; Ludwigia peploides (Kunth) P.H.Raven, Onagraceae Juss.; Eugenia uniflora L.,
Myrtaceae Juss.) as outgroups because my rbcL study and previous studies indicated that
Lythraceae, Onagraceae and Myrtaceae are the closest relatives of Combretaceae (Conti et al.,
1997; Systma et al., 2004).
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2.2.3 DNA extraction, PCR and sequencing
DNA was extracted from 0.3 g of silica-gel dried leaf material (Chase & Hills, 1991) or
herbarium material using the 2X CTAB method described by Doyle & Doyle (1987), with the
addition of 2% polyvinyl pyrolidone (PVP) to help reduce the effects of high polysaccharide
concentration in the samples. To avoid problems of PCR inhibition, all samples were purified
using QIAquick purification columns (QIAgen, Inc., Hilden, Germany) according to the
manufacturer’s protocol.
Amplification of rbcL was carried out in two overlapping fragments using the following
primer combinations: 1F-724R and 636F-1426R (Olmstead et al., 1992; Fay et al., 1997). The
trnH-psbA spacer was sequenced using primers 1F and 2R (Sang et al., 1997). The psaA-ycf3
spacer was amplified using the PG1f and PG2r primers (Huang & Shi, 2002). Additional
Combretum-specific internal primers were designed to overcome regions of micro-satellites
located within the psaA-ycf3 spacer: psaA-ycf3 IR 5-CTA GGA ACT TCT AAT TGA GA-3 was
used to sequence past a poly-T region located around 350bp from the beginning in several taxa;
psaA-ycf3 IF 5-CAT GTA TTT CGA GTC TGT TT-3 was used to sequence past a similar region
located at the 3’ end of the fragment. ITS was amplified in two non-overlapping pieces using two
internal primers with a pair of external primers: 17SE-ITS2 and ITS3-26SE (White et al., 1990;
Sun et al., 1994).
All reactions were performed using Ready Master mix (Advanced Biotechnologies,
Epsom, Surrey, UK), with addition of 4.5% of dimethyl sulfoxide (DMSO) to ITS amplification
reactions to reduce secondary structure problems common in ribosomal DNA (Álvarez &
Wendel, 2003). PCR amplification was performed using the following programs: for rbcL and
trnH-psbA spacer 3 min at 94°C followed by 28 cycles of 1 min 94°C, 1 min at 48°C, and 1 min
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at 72°C, with a final extension at 72°C for 7 min; for psaA-ycf3 spacer and ITS 1 min at 94°C
followed by 26 cycles of 1 min at 94°C, 1 min at 48°C and 3 min at 72°C followed by a final 7
min extension (72°C). Amplified products were purified using QIAquick columns (QIAgen,
Germany) following the manufacturer’s protocol. Cycle sequencing reactions were carried out
using BigDye© V3.1 Terminator Mix (Applied Biosystems, Inc., ABI, Warrington, Cheshire,
UK) and cleaned using the EtOH-NaCl method provided by ABI; they were then sequenced on
an ABI 3130xl genetic analyser.
2.2.4 Sequencing and alignment
Complementary strands were assembled and edited using Sequencher version 4.6 (Gene Codes
Corp., Ann Arbor, Michigan, USA) and sequences were aligned manually in PAUP* (version
4.0b1; Swofford, 2002) without difficulty due to low levels of insertions/deletions (indels) except
for the trnH-psbA spacer for which large regions were excluded from analyses due to alignment
difficulties. Nineteen indels were included for the plastid DNA analyses as presence/absence
characters. The aligned matrices are available from the author (olive.maurin@gmail.com).
2.2.5 Phylogenetic analyses of molecular data
Maximum parsimony (MP) using PAUP* version 4.0b1 (Swofford, 2002) was implemented to
analyse (1) the rbcL data including representative of Myrtales and several phylogenetically
distantly related families to identify the appropriate outgroup for Combretaceae, (2) the
combined plastid data of Combretaceae, (3) the ITS data of Combretaceae, and (4) the combined
sequence data of Combretaceae. Tree searches were conducted using 1,000 replicates of random
taxon addition, retaining 10 trees at each step, with tree-bisection-reconnection (TBR) branch
swapping and MulTrees in effect (saving multiple equally parsimonious trees). The trees
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collected in the 1000 replicates were then used as starting trees for another search without a tree
limit. Support for clades in all analyses was estimated using bootstrap analysis (Felsenstein,
1985) with 1000 replicates, simple sequence addition, TBR swapping, with MulTrees in effect
but saving a maximum of 10 trees per replicate. Bootstrap support (BP) was classified as high
(85–100%), moderate (75–84%) or low (50–74%). All data sets were analysed separately, and
the individual bootstrap consensus trees examined by eye to identify topological conflicts, i.e.
moderate to high support for different placement of taxa. 'Congruence tests' such as the
incongruence length test (ILD) can be unreliable (Reeves et al., 2001; Yoder et al., 2001) and
therefore were not used in this study. Delayed transformation character optimisation
(DELTRAN) was used to calculate branch lengths, due to reported errors
(http://paup.csit.fsu.edu/problems.html) with accelerated transformation optimisation
(ACCTRAN) in PAUP v.4.0b1.
I could not amplify all taxa for rbcL, psaA-ycf3, and ITS, and thus the three matrices do
not contain identical sets of taxa (Appendix 2.1). I investigated the effects of these missing
sequences on patterns of relationships as well as support in the combined analysis by performing
two combined analyses: (1) all taxa with all data, and (2) all taxa for which at least some data
were present. I found that missing data did not affect the second analysis and thus illustrate the
combined results with all taxa (analysis 4).
Bayesian analysis (BI; Huelsenbeck & Ronquist, 2001; Ronquist & Huelsenbeck, 2003)
was performed using MRBAYES v. 3.1.2. For each matrix ITS, rbcL, psaA-ycf3, trnH-psbA, the
most appropriate model was selected using MODELTEST v. 3.06 (Posada & Crandall, 1998).
For ITS, rbcL and psaA-ycf3, the model GTR+I+G was selected, and for trnH-psbA, TIM + G in
which the two resulting models share the same number of substitutions = 6 and rates = gamma,
base frequency = empirical, clock = unconstrained, and I used 2,000,000 generations with trees
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sampled every 200. Three analyses were perfomerd: (1) all plastid loci combined (2) ITS
nrDNA; (3) combined plastid and nuclear regions. Partitioned analyses were run for (1) and (3)
since different models were selected. The resulting trees were plotted against their likelihoods to
determine the point where likelihoods converged on a maximum value, and all the trees before
the convergence were discarded as ‘burn-in’ (1000 trees). All remaining trees were imported into
PAUP 4.0b10, and a majority-rule consensus tree was produced showing frequencies (i.e.
posterior probabilities or PP) of all observed bi-partitions. PP values are shown on the MP trees
because the topologies are identical. The following scale was used to evaluate the PPs: below
0.95, weakly supported; 0.95–1.0, well supported.
2.3 RESULTS
2.3.1 Molecular evolution
Statistics for MP analyses for the three plastid partitions and the combined 3-region data set are
shown in Table 2.2. Of the plastid regions used, trnH-psbA (excluding unalignable regions) had a
significantly higher number of variable sites (31.0%; Table 2.2) than psaA-ycf3 (24.2%) or rbcL
(15.2%). The number of potentially parsimony informative characters for rbcL within
Combretaceae (8.67%) is much lower than for the two other plastid regions, trnH-psbA and
psaA-ycf3 (17.39% and 16.04%, respectively). The variable sites evolve at a similar rate for
trnH-psbA (1.65 changes per variable site) and rbcL (1.70 changes per variable site) and
performed equally well (as measured by retention index; RI). One insertion of about +/- 300 base
pairs (bp) was identified in the trnH-psbA data matrix that was cladistically informative, with
Meiostemon and all species of Combretum subgenus Combretum sharing this character. The ITS
region had more than twice the number of variable sites (45.3%) and potentially parsimony
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informative characters (54.3%) of any of the plastid regions (Table 2.2). It evolves at a much
faster rate than the plastid genes (4.35 changes per variable site) with a lower consistency index
(CI) and RI.
Results from four analyses are presented: the large rbcL dataset with a broad outgroup
sampling (Figure 2.1), combined plastid regions (rbcL + psaA-ycf3 + trnH-psbA; Figure 2.2), ITS
(Figure 2.3), and combined plastid and ITS (rbcL + psaA-ycf3+ trnH-psbA + ITS; Figure 2.4).
2.3.2 rbcL analysis with a broad outgroup sampling (analysis 1)
Parsimony analysis yielded 6,340 most parsimonious trees of 1148 steps with a CI of 0.48 and a
RI of 0.76 (Table 2.2). One of the most parsimonious trees with branches collapsing in strict
consensus tree marked is illustrated in Figure 2.1. Monophyly of Combretaceae and the two
subfamilies, Strephonematoideae and Combretoideae, is moderately to weakly supported (82 and
68 BP, respectively). Relationships within Combretoideae were unresolved resulting in a large
polytomy in the strict consensus tree with only a few supported clades.
I initially included two sequences obtained from GenBank in the analysis namely,
AF281477 (Conocarpus erectus L.) and AF281478 (Calycopteris floribunda Lam.) from the
study of Tan et al. (2002). This analysis of rbcL sequences placed C. erectus sister to Abroma
Jacq. and Theobroma L. (Malvaceae) and C. floribunda grouped with Teucridium (Lamiaceae).
This is in contrast with the results of Tan et al. (2002) where C. erectus was placed as sister
group to Terminaliinae and C. floribunda sister to Combretinae. I thus exclude these two
accessions from the combined analysis (analysis 4) since this discrepancy may represent a case of
misidentification or deposition of the wrong rbcL sequences in GenBank.
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2.3.3 Combined plastid analysis (analysis 2)
Individual plastid sequence analyses (results not shown) were topologically consistent (negligible
to zero incongruence), and for the purpose of the results and discussion were combined and
treated as a single analysis. The parsimony analysis yielded 3,910 most parsimonious trees of
1,037 steps with a CI of 0.72 and a RI of 0.88 (Table 2.2). One of the most parsimonious trees is
illustrated in Figure 2.2. Results support monophyly of Combretaceae (98 BP/1.0 PP).
Subfamilies Strephonematoideae and Combretoideae are strongly supported (96 BP/1.0 PP and
87 BP/1.0 PP). Within Combretoideae, there was weak support for monophyly of tribes
Laguncularieae, Terminaliinae and Combretinae excluding Calycopteris (52 BP/0.9 PP, 66
BP/1.0 PP and 57 BP/1.0 PP, respectively). Within Terminaliinae, Terminalia comprises at least
four major clades.
Within the weakly supported Combretinae, the positions of Calycopteris and Guiera are
unresolved. With the exception of Calycopteris and Guiera, two main clades can be
distinguished: clade 1 is weakly (54 BP/1.0 PP) supported and includes all species of Combretum
subgenus Combretum and Meiostemon and clade 2 although supported in the strict consensus
tree, received support less than 50 BP in the bootstrap analysis. This last clade includes all
representatives of Combretum subgenus Cacoucia as well as Quisqualis and Calopyxis.
2.3.4 ITS analysis (analysis 3)
Analysis resulted in 2,500 equally most parsimonious trees with TL = 1,744, CI = 0.41 and RI =
0.78 (Table 2.2). One of the most parsimonious trees is illustrated in Figure 2.3. Tribe
Laguncularieae are strongly supported (100 BP/1.0 PP) as sister to the rest of Combretaceae.
Within Combretoideae, two subclades are identified, namely Terminaliinae excluding
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Conocarpus (74 BP/1.0 PP) and Combretinae excluding Calycopteris and Guiera (91 BP/0.94
PP). The positions of Conocarpus (Terminaliinae), Calycopteris (Combretinae) and Guiera
(Combretinae) are unresolved within tribe Combretaceae. Within the Terminaliinae clade,
groupings comparable to the combined plastid analysis can be observed: Terminalia is
polyphyletic with at least four clades. Although weakly supported, two main groups in
Combretinae are observed; these correspond to Combretum subgenus Cacoucia (64 BP/0.99) and
Combretum subgenus Combretum (53 BP/0.98 PP). Species of section Hypocrateropsis are wellsupported clade (99 BP/1.0 PP) as sister to the rest of Combretum subgenus Combretum with a
support less than 50 BP. As in the combined plastid analysis Meiostemon, Combretum inberbe
and Thiloa are included in Combretinae, but their positions are unresolved.
2.3.5 Combined molecular analysis (analysis 4)
Results of the combined plastid analysis are largely congruent with those of the ITS analysis, and
all data were therefore combined (3,683 characters; Table 2.2). Parsimony analysis produced 184
trees (TL = 3163; CI = 0.46; RI = 0.76). One of the most parsimonious trees is shown in Figure
2.4. Combretaceae are strongly supported as monophyletic (96 BP/1.0 PP) with
Strephonematoideae (just Strephonema) sister to Combretoideae. Although there is no MP
bootstrap support for monophyly of Laguncularieae, BI supports their monophyly (0.95 PP). BI
also supports the sister relationship of Langunculariae with Combreteae (77 BP/1.0 PP).
Monophyly of Combreteae is weakly supported in the MP analysis (68 BP) and strongly
supported in the BP analysis (0.96 PP). Within Combreteae, both subtribes are well supported,
Terminaliinae with 72 BP/1.0 PP and Combretinae with 64 BP/1.0 PP. Relationships within
Terminaliinae are unresolved in the MP analysis and well resolved in the BI analysis. Two main
clades are observed, with Conocarpus sister (79 BP/0.98 PP) to the remaining genera of this
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subtribe. Clade 1 (1.0 PP) contains representatives of Terminalia from Africa, Asia, Australia
and the Pacific islands. Buchenavia, Bucida and Pteleopsis are embedded within them. The
second clade (1.0 PP) consists of Asian Terminalia taxa. Anogeissus is embedded within this
second Terminalia clade.
In the clade representing Combretinae, Calycopteris and Guiera are together sister to the
remaining taxa (96 BP/1.0 PP). Bayesian analysis produced a more resolved topology than the
MP analysis with two well-supported clades. Clade 1 includes all representatives of Combretum
subgenus Combretum (0.99 PP) and Meiostemon, whereas clade 2 contains all taxa belonging to
Combretum subgenus Cacoucia as well as Quisqualis and Calopyxis (81 BP/1.0 PP). The
position of Thiloa is unresolved in both the MP and BI analyses. Within subgenus Combretum,
two main groups are found. The first group (59 BP/1.0 PP) includes sections Hypocrateropsis
(excluding Combretum imberbe; 100 BP/1.0 PP), Ciliatipetala (99 BP/1.0 PP),
Macrostigmatea/Spathulipetala (100 BP/1.0 PP) and Angustimaginata (100 BP/1.0 PP).
Meiostemon is supported as sister to subgenus Combretum in the BI analysis (1.0 PP), but its
position is unresolved in the MP analysis. Group 2 (1.0 PP) includes sections Glabripetala,
Mettalicum, Breviramea, Campestria as well as Combretum imberbe from section
Hypocrateropsis.
2.4 DISCUSSION
Because the results of the plastid and ITS matrices are highly congruent, I will restrict the
discussion to results obtained from the combined data set (Figure 2.4). The results confirm
monophyly of Combretaceae with Strephonematoideae distinct from the remaining genera of the
family (96 BP/1.0 PP). Strephonema (Strephonematoideae) was initially placed within
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Lythraceae (Bentham & Hooker, 1865), but Engler & Diels (1900) recognised
Strephonematoideae within Combretaceae because the genus also possesses combretaceous
segmented hairs. Strephonema is easily distinguished from the other genera in the family by its
revolute domatia, characteristic pattern of epidermal cells, paracytic subsidiary cells and twoarmed hairs (Stace, 1965). Furthermore, according to Jongkind (1995), Strephonema exhibits
more putatively plesiomorphic characters than any other genus in the family. It possesses semiinferior ovaries and fruits without wings or other obvious adaptations for dispersal (Jongkind,
1995), whereas the remainder of the family possess inferior ovaries and fruits with wings.
2.4.1 Relationships within tribe Laguncularieae
Engler & Diels (1899) first considered Languncularieae as one of four tribes within
Combretoideae. It was distinguished from the other three tribes by a pair of bracteoles adnate to
the lower receptacle and lack of obvious venation on the adaxial epidermis in the leaf surface
(Stace, 1965). The three remaining tribes were lumped into a single tribe: Combreteae (Stace,
1965) that included Laguncularia, Lumnitzera and Macropteranthes. Dansiea was described in
1981 and included in Laguncularieae (Stace, 2007). In the MP analysis, monophyly of tribe
Laguncularieae did not receive BP >50, whereas it was strongly supported in the BI analysis
(0.95 PP).
2.4.2 Subtribal relationships within tribe Combreteae
In the current sampling of Combreteae, I was able to include all genera with the exception of
Finetia. Subdivision of Combreteae by Vollesen (1981) into two subtribes, Terminaliinae (72
BP/1.0 PP) and Combretinae (64 BP/1.0 PP), is well supported in the MP and BI analyses. The
two monotypic genera Guiera and Calycopteris are together sister to the rest of Combretinae.
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Although only moderately supported in the MP analysis, Conocarpus is strongly supported as
sister to the remaining genera and included in Terminaliinae in the BI analysis (79 BP/0.98 PP).
2.4.3 Relationships within subtribe Terminaliinae
Six genera are currently recognised within Terminaliinae: (1) Anogeissus (tropical West Africa to
Southeast Asia); (2) Buchenavia (tropical America); (3) Conocarpus (tropical America,
northeastern Africa and southern Yemen); (4) Finetia (Thailand and Laos); (5) Pteleopsis
(Africa); and (6) Terminalia (America, Africa, Madagascar and Asia to Australia; Stace, 2007).
The results from the current study confirm that Terminalia is not monophyletic and
contains two distinct groups, a mainly African group with a few taxa from the New World and
the Pacific islands and a second mostly Asian group including some New World taxa. Although
my sampling of Terminalia species is relatively small compared to the number of species in the
genus I am suggesting several taxonomical changes. These are based on (1) my phylogenetic
results, (2) a recent proposal to transfer Bucida to Terminalia (Stace, 2002), and (3) the existing
doubt regarding the relationship between Pteleopsis and Terminalia (Vollesen, 1981). I therefore
propose that with the exception of Conocarpus, which can easily be distinguished from all other
genera of Terminaliinae by its stalked glands (Stace, 1965) and glandular trichomes (Stace,
1980b), all other genera of Terminaliinae should be transferred to Terminalia. I am following this
option of merging these genera of Terminaliinae within Terminalia since the genus predates the
others. Much greater sampling will be necessary to assess relationships and develop a modern
classification for the tribe.
Pteleopsis species are shrubs to small trees without scales or stalked glands, but they
often have conspicuous small, pink, conical buds in the axis of the leaf or leaf scars (Coates
Palgrave, 2002). The genus has 12 species in tropical Africa (Klopper et al., 2006), of which two
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species occurs south of the Zambezi River. Pteleopsis was considered distinct from Terminalia
due to its male flowers only at the base of the inflorescence and not at the apex, as is the case for
Terminalia (Stace, 2007). This character, however, proved to be unreliable for the separation of
these genera since there are species of Terminalia with only basal male flowers (section
Ramatuellea Kunth.; Stace, 2007). On the other hand, according to Exell & Stace (1966) and
Wickens (1973), Pteleopsis represents an intermediate between Combretum and Terminalia
based on several characters, namely it shares character-states with Combretum in having petals
(petals are completely absent in Terminalia) and opposite leaves. However, it seems to be closely
related to Terminalia based on character such as spirally convolute cotyledons, flattened fruits,
andromonoecious flowers and lack of scales and stalked glands. Tilney & Van Wyk (2004)
reported the occurrence of extrafloral nectaries on leaves of Pteleopsis and Terminalia, but these
are absent in Combretum. Pteleopsis fruits possess 2-5 wings, whereas those of Terminalia
generally possess 2 wings and Combretum 4-5 wings. In the current study, I retrieved high
support for an embedded position of Pteleopsis in Terminalia. I thus propose that Pteleopsis to be
united with Terminalia, the latter having priority.
Buchenavia comprises 24 species (Mabberley, 2008) from tropical and subtropical
Central and South America (Stace, 1965). Analysis for the current study suggests Terminalia
bellirica (Gaertn.) Roxb. is sister to Buchenavia, and the latter included in the clade containing
mainly African species of Terminalia. According to Stace (1965), Terminalia and Buchenavia
have only one or two minor floral characters distinguishing them. Molecular data here strongly
support Buchenavia as embedded within Terminalia and I therefore propose Buchenavia be
transferred to Terminalia.
Anogeissus is a genus of eight species distributed from the Old World tropics including
the Arabian Peninsula (Mabberley, 2008). It is difficult to distinguish from Terminalia based on
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epidermal and leaf morphological features and shares some similarities with Conocarpus in
possessing numerous stomata on the upper epidermis as the primary difference from Terminalia
(Stace, 1965). Anogeissus was once included in Conocarpus as section Anogeissus DC (1828),
but Guillemin & Perrotet (1833) raised it to genus. Fruit characters are diagnostic for the two
genera, with Anogeissus having cone-like heads with wings or ribs and an apical beak
representing the persistent calyx-stalk (lower receptacle above the ovary) and Conocarpus with a
4-ribbed, slightly flattened and achene-like fruit (Stace, 2007) with the calyx stalk deciduous
(Scott, 1979). Molecular data from the current study do not indicate a close relationship between
Conocarpus and Anogeissus, but rather that Anogeissus is embedded in the mainly Asian clade of
Terminalia. I propose to unite also Anogeissus and Terminalia.
Bucida, when accepted as a separate genus, comprises three species (Mabberley, 1997)
from Central America, the Caribbean and North America (Florida). In 2002, Stace transferred
Bucida to Terminalia. Bucida differs consistently from other American Terminalia and nearly all
other Terminaliinae in having a small, nut-like fruit that retains the withered crown-like upper
portion of the hypanthium (Stace, 2002), whereas Terminalia fruits are generally hard and woody
with two wings (Stace, 1965).
African species of Terminalia are relatively well studied and a sectional classification has
been suggested (Griffiths, 1959). For the remainder of the genus, there is an insufficient or only
localised sectional classification (Capuron, 1967; Clarke, 1878; Exell, 1954; Griffiths, 1959;
Pedley, 1990). In the current study, the genus is polyphyletic and has the closely related genera
of Terminaliinae imbedded, with the exception of Conocarpus. BI revealed two main clades
within Terminalia, as discussed above. I thus formally propose the transfer of Pteleopsis,
Buchenavia and Anogeissus to Terminalia, Bucida having been already transferred (Stace, 2002).
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2.4.4 Relationships within subtribe Combretinae
In the MP analysis, the subfamily is weakly supported (64 BP), whereas in the BI analysis it
receives strong support (1.0 PP). Currently five genera are recognised within Combretinae
(Stace, 2007): (1) Combretum (pantropical) (2); Calycopteris (Southeast Asia); (3) Meiostemon
(tropical southern Africa, Madagascar); (4) Thiloa (Central America) and (5) Guiera (northern
tropical Africa). Stace (2007) suggested transferring Meiostemon to Combretum, but this was
never formally published. Delimitation of Quisqualis and Combretum has been discussed
(Jongkind, 1990), and the molecular results for the current study support the transfer of
Quisqualis to Combretum. I was unable to sequence Combretum apetalum Wall. in this study due
to the difficulty of obtaining fresh material, and PCR was unsuccessful from herbarium DNA.
This species is important because it is the only representative of one of the three subgenera
within Combretum, C. subgenus Apetalanthum. It shares morphological characters with the other
two subgenera: the stalked glands of subgenus Cacoucia and scales of subgenus Combretum
(Stace, 1980a, 2007).
The two monotypic genera, Calycopteris and Guiera, are together sister to the rest of
Combretinae. According to Stace (1980b), Calycopteris and Guiera are morphologically distinct,
although the upper and lower epidermis of these two genera is similar (Stace, 1965). The
relationship of Calycopteris with other genera within the subtribe has never been fully
investigated, even though it resembles Guiera, Thiloa and Combretum in possessesing scales
(Stace, 1965). Guiera is easily distinguishable by its epidermal cells and numerous shortly
segmented hairs (Stace, 1965). The position of Thiloa within Combretinae is unresolved. Eichler
(1866) separated Thiloa from Combretum by floral structure (lack of petals and a single row of
stamens), whereas Stace (2007) included the genus in Combretum subgenus Combretum. These
floral characters are not unique to Thiloa but are also present in other taxa within Combretum
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(absence of petals in Combretum apetalum and a single row of stamens in Meiostemon). Thiloa
needs to be sampled more densely to assess its relationship with subgenus Combretum.
In the BI analysis, two main clades are found in Combretinae, one (0.99 PP) including all
representatives with scales and the other in which they are absent (81 BP/1.0 PP). The first
represents Combretum subgenus Combretum with Meiostemon, a small genus with two species,
as their sister. Exell & Stace (1966) erected Meiostemon as a new genus based on the suppression
of one whorl of stamens, which is different from Combretum. These authors also concluded that
Meiostemon shows no affinity to any other section within Combretum, although both species
possess scales like all species currently in subgenus Combretum. According to Exell (1978), the
distribution of Meiostemon in Mozambique, Zambia, Zimbabwe and Madagascar could indicate a
relatively ancient origin and could also have resulted from recent, long-distance dispersal. I
propose its reinstatement as Combretum section Haplostemon as described by Exell (1939).
The second clade includes representatives of subgenus Cacoucia and consists of two main
subgroups, each moderately supported. There is strong support (86 BP/1.0 PP) for Quisqualis,
Combretum coccineum (Sonn.) Lam. (syn: Poivrea Comm. ex DC.; now a section within
Combretum subgenus Cacoucia), and Calopyxis as imbedded within subgenus Cacoucia.
Jongkind (1990, 1995) argued for the inclusion of Quisqualis and Calopyxis in Combretum, just
as Engler & Diels (1899, 1900) had done for Poivrea. Calopyxis, with 18 out of the 19 species
endemic to Madagascar, has flowers in which petals are absent as in the case of Terminalia,
whereas Quisqualis has flowers with five petals. According to Stace (2007), these putative
differences are not consistent. Quisqualis is a small genus comprising 16 species of lianas
distributed in the Old World tropics (Mabberley, 1997). Morphologically they share important
similarities with the climbing species of Combretum subgenus Cacoucia (Exell & Stace, 1966).
Quisqualis species have microscopic stalked glands similar to those found in subgenus Cacoucia,
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whereas the scales characteristic of the subgenus Combretum are absent (Exell & Stace, 1966;
Wickens, 1973). Fruits of subgenus Cacoucia are 4-5-winged, whereas in Quisqualis they are
generally 5-winged. In addition to this, Quisqualis species have long, tubular upper receptacles
that are absent in Combretum (Hooker, 1867; Lawson, 1871) and stamens not exserted or shortly
exserted beyond the petals; in the case of Combretum, the species have long, protruding stamens.
These characters have proven to be unreliable for the separation of Quisqualis and Combretum.
Exell (1931) proposed a new generic classification system in which Quisqualis was separated
from Combretum on account of the style being adnate to the upper receptacle for about half the
length. In 1964, Exell & Stace reorganised the delimitation of these two genera, but this
separation was found to be unreliable by Jongkind (1990). Jongkind (1990) stated that since no
character has been identified that would allow for the reliable and unambiguous separation of
Quisqualis and Combretum, they must be united with the name Combretum having priority. An
additional character of Quisqualis species as well as most representatives within subgenus
Cacoucia is the presence of attractive pink-reddish flowers, which are not found in the rest of the
family. In the case of Quisqualis, the elongated calyx might represent a modification for moth
pollination (Stace, 2007).
A revision of the generic classification within the subtribe Combretinae seems necessary
to make them conform to the criteria of monophyly. Apart from the primary principle of
monophyly, Backlund & Bremer (1998) also proposed as secondary principles that a
classification should maximise stability, phylogenetic information, support for monophyly and
ease of classification. Based on this, I propose that Combretum subgenus Combretum should be
expanded to include Meiostemon and that Combretum subgenus Cacoucia should include
Quisqualis. My study confirmed the recent treatment of Calopyxis as members of Combretum
subgenus Cacoucia (Jongkind, 1995)
92
2.4.5 Relationships within Combretum subgenus Combretum including Meiostemon
2.4.5.1 Section Angustimarginata
This section was described by Engler & Diels (1899) and includes the following South African
species: C. erythrophyllum (Burch.) Sond., C. caffrum (Eckl. & Zeyh.) Kuntze, C. kraussii
Hochst., C. nelsonii Dümmer, C. vendae A.E.van Wyk and C. woodii Dümmer. It is restricted to
southern Africa and has been well studied and amended with the work of Van Wyk (1984), who
reinstated four species, C. caffrum, C. nelsonii, C. kraussii and C. woodii, and described a new
species, C. vendae. Section Angustimarginata Engl. & Diels is a natural group, which is easily
distinguished by inconspicuous scales, often obscured by the indumentum and/or glutinous
secretions (Exell, 1970, 1978). Other characters for this section are: bark smooth or flaking in
small papery pieces, young leaves that are white or creamy without chlorophyll (some turning
red in autumn), reddish calyx lobes and mature fruit usually partially or completely tinted pink to
dark red (Van Wyk, 1984). In this study, section Angustimarginata is strongly supported (100
BP/1.0 PP) with C. kraussii and C. vendae grouping together with strong support (87 BP/1.0 PP).
According to Van Wyk (1984), C. kraussii is morphologically the most primitive species of the
group, a hypothesis that a molecular study cannot refute. The current molecular study
corroborates the hypothesis that C. woodii and C. nelsonii are distinct species from C. kraussii as
Exell (1970, 1978) suggested.
2.4.5.2 Section Ciliatipetala
According to the latest revision of the sectional classification (Stace, 1980b), section
Ciliatipetala Engl. & Diels comprises 10 species from Africa and Yemen in the Arabian
Peninsula. In this study, six described and three undescribed species from Africa were included),
93
and these members of section Ciliatipetala form a strongly supported clade (99 BP/1.0 PP) that is
characterised by flowers with small ciliate petals generally produced in large numbers. Fruits are
generally small, and scales variable in size from 40–120 µm; they have 7–12 radial walls often
with additional tangential walls (Exell, 1978). Although this group seems natural in the current
results and one of the largest sections within Combretum subgenus Combretum, Stace (1969)
considered it as one of the most problematic with most of the species falling into two major
groups centred around C. molle R. Br. and C. apiculatum Sond. Stace (1969) also hypothesised
about the existence of species complexes or aggregates around C. psidioides Welw., C. moggii
Exell and C. albopunctatum Suesseng. Stace (1969) proposed that further characters should be
studied and suggested that some of these taxa might even need to be separated into different
groups. Although my sampling does not include many representatives of each aggregate as
recognised by Stace (1969), my results indicate that section Ciliatipetala comprises two main
clades. The first includes C. albopunctatum, C. apiculatum and C. molle, and the second C.
moggii, C. petrophilum Retief and C. edwardsii Exell (88 BP/1.0 PP and 99 BP/1.0 PP,
respectively). It would be imperative to add representatives of the aggregates around C. nigricans
Lepr. mentioned by Stace (1969), as well as more representatives of each aggregate (for example,
the different forms or ecotypes of C. molle and subspecies of C. psidioides) to have a better
understanding of this section and its subsectional groupings.
2.4.5.3 Sections Macrostigmatea and Spathulipetala
Results for the current study support inclusion of section Spathulipetala Engl. & Diels in section
Macrostigmatea Engl. & Diels (100 BP/1.0 PP). According to Stace (1980b), section
Macrostigmatea comprises four species from Africa and section Spathulipetala only one, C.
zeyheri Sond. that is widespread throughout southern Africa. The division of the group into two
94
sections is questionable. Exell (1978) reported on relationships between the two sections and
stated that they share similarities such as scale size, scale fragmentation into walls and fruit size.
Results from the current study strongly support lumping C. zeyheri in section Macrostigmatea.
Combretum zeyheri shows a close relationship to C. mkuzense J.D.Carr & Retief from the sand
forests in KwaZulu-Natal (70 BP/1.0 PP). This result is not unexpected since both species have
large fruits, up to 50 x 50 mm and even larger in some specimens. A second specimen supposed
to be C. mkuzenze (voucher RBN 154) was included in the analysis following suggestions that the
localised species from the sand forest of KwaZulu Natal might extend to similar vegetation in the
northwest of the country. The molecular data do not suggest that these two accessions are
members of the same species and this second taxa is now treated as a new species that will be
described jointly with authors from South Africa National Biodiversity Institute (SANBI) in a
forthcoming publication. Exell (1978) suggested that C. kirkii M.A.Lawson and C. gilletianum
Liben could be segregated from C. schumanii into a separate section based on the floral disk
being glabrous or not. The current study however supports C. kirkii as sister to the rest of section
Macrostigmatea, but before any conclusions can be made C. gillettianum Liben should be
included in the analysis.
2.4.5.4 Sections Hypocrateropsis (excluding Combretum imberbe)
Section Hypocrateropsis Engl. & Diels is characterised mainly by petals that are linear-elliptic
and glabrous with large leaf scales (50-150 µm in diameter); it comprises six species from Africa
(Stace, 1980b). Until now, C. imberbe Wawra was accepted as a member of this group, a
placement that my study, however, does not support. To confirm this result I included two
specimens of C. imberbe from different localities (Namibia and South Africa) in the analysis. As
mentioned previously, scale size and shape are consistent character in this section (scales are
95
generally <100um with primary and secondary radial and tangential walls); however, scale
density is a character that distinguishes C. imberbe from the rest of the section. In C. imberbe,
scales are mostly contiguous to overlapping, which differs from C. celastroides Welw. ex
M.A.Lawson and C. padoides Engl. & Diels in that they are rarely contiguous (Exell, 1978). In
this case, scale density in addition to shape and construction might be an important taxonomic
character to investigate at both species and sectional level. Stace (1969) also mentioned the
epidermis with a well-developed venule reticulum, sparse to frequent hairs and usually undulatewalled areolar cells without papillae in the six species he studied; these are absent in C. imberbe.
This is in contrast with the other species in which there are only obvious major laterals veins and
midribs, no hairs, and straight-walled cells, those beneath the scales with conspicuous, rounded
papillae.
2.4.5.5 Sections Glabripetala and Mettalicum
Engler & Diels (1899) grouped C. adenogonium Steud. ex A.Rich (= C. fragrans F.Hoffm.) and
the subspecies of C. collinum Fresen under Glabripetala Engl & Diels, but this section was later
dismembered, with a new section for C. collinum (section Mettalicum Exell & Stace) based on
differences in scale structure (Stace, 1969). Results from the current study support the distinction
of these taxa and their separation in sections Glabripetala and Mettalicum. The phylogenetic
results support Glabripetala as sister to the southern African sections Angustimargina,
Macrostigmatea and Spathutipetala, and Mettalicum as more closely related to sections
Campestria Engl. & Diels, Breviramea Engl. & Diels and C. imberbe (the last previously
included in section Hypocrateropsis).
96
2.4.5.6 Sections Campestria and Breviramea
Stace (1980b) considered section Elaegnoidea Engl. & Diels a synonym of section Campestria.
Sections Campestria and Breviramea are each represented by four species in Africa, and only
one representative of each is included in the current study: C. elaeagnoides Klotzsch
(Campestria) and C. hereroense Schinz (Breviramea). To have a more comprehensive overview
of these two sections and their relationships with the apparently closely related sections
Mettalicum and Glabripetala, more species of each section should be included in future.
2.4.6 Relationships within Combretum subgenus Cacoucia including Quisqualis and Calopyxis
As previously discussed, subgenus Cacoucia is unique in its glandular, compartmented hairs and
absence of scales (Stace, 1980a). Flowers of this subgenus exhibit better developed petals than in
subgenus Combretum and they are often colourful with nectariferous disks, probably linked to
adaptation for pollination by birds and moths. This becomes even more obvious in Quisqualis,
which according to my results is closely related to subgenus Cacoucia. In this analysis, subgenus
Cacoucia is well supported (81 BP/1.0 PP) and divided into two low to moderately supported
clades in the MP analysis, but both of these are strongly supported in the BI analysis (1.0 PP,
0.97 PP, respectively). The first comprises two subclades, one with species belonging to
Quisqualis (0.95 PP) and the second with several species of Combretum subgenus Cacoucia
section Poivrea and members of former Calopyxis now considered to be in Combretum (100
BP/1.0 PP). However, the three taxa, C. holstii Engl., C. mossambicense (Klotzsch) Engl., and C.
bracteosum (Hochst.) Brandis (previously section Trichopetaleae Engl. & Diels) did not group
with other representatives of section Poivrea. Combretum grandiflorum G.Don is unresolved and
was previously included in section Grandiflora Engl. & Diels. I therefore suggest that the two
97
sections Trichopetaleae and Grandiflora be reinstated to accommodate the paraphyletic section
Poivrea.
Following the suggestion of Capuron (1967), Stace (1980a) elevated Poivrea grandidieri
to Calopyxis grandidieri; however, according to Jongking (1995), if this species is placed in
Calopyxis the most important character that previously separated this genus from the related
Combretum subgen. Cacoucia is no longer present in all species (i.e. the absence of petals). In
1995, Jongkind transferred Calopyxis back into Combretum within subgenus Cacoucia section
Calopyxis Jongkind, which my results support.
The second clade is supported by 76 BP (MP) and 1.0 PP (BI). With BI, the clade is
enlarged to include C. oxystachyum Welw. ex M.A.Lawson, C. watti Exell, and C. goldieanum
F.Muell (0.97 PP). This clade also includes section Conniventia Engl. & Diels, two taxa of
section Poivrea as well as two monotypic sections from southern Africa: Megalantherum Exell
(C. wattii) and Oxystachia Exell (C. oxystachyum).
Subgenus Cacoucia contains 13 sections in total with around 78 species (Stace, 1980b),
most of them occurring in Africa and Madagascar with distributions mainly north of the Zambezi
River. The current study included only ten species representing four sections and therefore it is
necessary to have more sampling of this subgenus to create a better understanding of
relationships within and between sections.
2.4.6.1 Section Poivrea
Engler & Diels (1899, 1900) included Poivrea in subgenus Cacoucia, and according to Stace
(1980b) the section comprises 31 species from Africa, Madagascar and Asia. The current study
includes the widespread species C. mossambicense and an atypical species with round wingless
fruit, C. bracteosum, from the eastern coastal forests of KwaZulu-Natal and Eastern Cape (South
98
Africa). Combretum holstii is morphologically similar to C. mossambicense, a relationship
confirmed by the analysis (100 BP/1.0 PP). These three species do not group with C. coccineum
(also section Poivrea). They represent a group of morphologically similar species that were
previously included in section Trichopetala. Reinstatment of the section sunk by Stace (1980a) in
section Poivrea would be appropriate according to the results. However, these three species do
not group with C. goldieanum F.Muell., an Asian species also previously considered a member of
section Trichopetala. Combretum goldieanum seems more closely related to C. oxystachyum of
section Oxystachia, although they form a clade with weak support (0.69 PP).
2.4.6.2 Section Conniventia
Section Conniventia Engl. & Diels occurs in Africa and is represented in my sampling by four
out of the 20 species (Stace, 1980b). Combretum platypetalum Welw. ex M.A.Lawson comprises
four subspecies based on hairy receptacles and leaves (Exell, 1968). It is a perplexing group that
warrants further study with more individuals from each subspecies. In the current analysis, I
included two specimens of C. platypetalum, one from the Caprivi Strip (Namibia) and the other
collected close to Harare (Zimbabwe). The relationship between C. platypetalum, C. paniculatum
Vent. and C. microphyllum Klotzsch (Exell, 1978) is equally unclear, which makes this group
even more confusing. An investigation of C. platypetalum and its relationship to C. paniculatum
and C. microphyllum is required.
Wickens (1973) considered C. microphyllum and C. paniculatum to be one species and C.
microphyllum to be a subspecies of C. paniculatum; however Exell (1978) preferred to treat these
as two separate species. The current study supports the opinion of Exell (1978), and this is also
confirmed by the distribution and differences in drought tolerance of C. microphyllum and C.
paniculatum. The latter is a mesic forest species from tropical Africa with a southern distribution
99
in the Soutpansberg (RSA). In contrast to this, C. microphyllum is more resistant to drought and
found along riverbanks in savanna vegetation.
2.5 CONCLUSIONS
The well-resolved and supported results presented here allow a discussion of the classification
and relationships between the genera of Combretaceae, with some suggestions for improving
their classification. The analyses generally support the current classification, particularly the
transfer of genera that were solely based on equivocal morphological data, namely: (1)
Terminalia (nom. cons.) for Bucida; and (2) Combretum (nom. cons.) for Calopyxis as well as
the sectional classification proposed progressively by Engler & Diels (1899), Exell (1939, 1953,
1968) and Stace (1980b), except for inclusion of C. imberbe within section sect.
Hypocrateropsis. From the results, I propose the following: (1) combination of Terminalia,
Buchenavia, Anogeissus and Pteleopsis with the name Terminalia having priority; (2) transfer of
the two species of Meiostemon (Exell, 1939) to Combretum; (3) reinstatement of subgenus
Combretum section Haplostemon for which both species were previously placed in subgenus
Combretum, (4) transfer of Quisqualis to Combretum, as suggested by Jongking (1995) and Stace
(2007); (5) reinstatement of sections Grandiflora and Trichopetala, which had previously been
sunk in section Poivrea; and (6) establishment of a new section for C. imberbe.
Taxonomic decisions to adjust the generic limits will be better evaluated by inclusion of
more species sampling. Adding the two Australian genera, Dansiea and Macropteranthes, would
be necessary to assess relationships within tribe Laguncularieae. In order to have a better
understanding of the generic and subgeneric relationships with the tribe Combreteae, addition of
species from Buchenavia, Finetia, Pteleopsis, Thiloa and Combretum subgenus Combretum
100
section Calopyxis would be necessary. It will also be imperative to add the third and monotypic
subgenus Apetalanthum as well as representatives of all sections of Combretum and Terminalia.
2.6 TAXONOMIC CHANGES
The taxonomic changes and new section presented in this section are suggested in this thesis but
are formally describe in Maurin et al. (2010).
Combretum Loefl., Iter Hispanicum App.: 308 (1758) [Combret.], nom. cons. emend. prop.
Type: Combretum fruticosum (Loefl.) Stuntz.
(=)
Quisqualis L., Species Plantarum ed. 2, 1 (1762) [Combret.], nom. rej. prop. Type:
Quisqualis indica L.
(=)
Meiostemon Exell & Stace, Bol. Soc. Brot. sér. 2, 40: 18, in adnot. (1966), nom. rej. prop.
Type: Meiostemon tetrandrum Exell.
Combretum Loefl., subgenus Combretum, section Haplostemon Exell
Combretum Loefl. subgenus Combretum section Plumbea O.Maurin, Jordaan & A.E.van Wyk
Sectioni Hypocrateropsidi valde affinis sed habitu arboris unicaulis discretae, juventute ramis
decussatis, ramulis brevibus lateralibus apice spinescente; foliis perdense lepidotis, squamis
plerumque contiguis vel superpositis, magnis 120--300µm diametro, cellulis permultis parvis,
solum costa nervisque primariis lateralibus conspicuis, margine disci dense tomentoso, stylo cum
squamis stipitatis, cotyledonibus infra planum humi orientibus, differt.
Type: C. imberbe Wawra in Sitzungsber. Acad. Wien, Math. -Nat., 38: 556 (1860)
101
This section is named Plumbea, derived from the Latin word plumbum which mean lead,
referring to the heartwood of C. imberbe which is extremely hard, heavy and durable; hence the
common name leadwood.
Combretum Loefl. subgenus Cacoucia (Aublet) Exell & Stace section Grandiflora Engler &
Diels
Type: C. grandiflorum G. Don in Edinb. Phil. Journ. (1824) 346
Combretum Loefl. subgenus Cacoucia (Aublet) Exell & Stace section Trichopetala Engler &
Diels
Type: C. trichopetalum Engler = C. mossambicense (Klotsch) Engler in Pflanzenw. Ost-Afrikas
C (1895) 292
Terminalia L., Syst. Nat., ed. 12, 2: 674. (15-31 Oct 1767) [Combret.], nom. cons. emend. prop.
Type: Terminalia catappa L.
(=)
Pteleopsis Engl., Abh. Königl. Akad. Wiss. Berlin, 25. 1894, nom. rej. prop.
Type: Pteleopsis variifolia Engl.
(=)
Anogeissus (DC) Wall., Florae Senegambiae Tentamen 1:279. 1832, nom. rej. prop.
Type: Anogeissus acuminata
(=)
Buchenavia Eichler., Flora 49(11): 1866, nom. rej. prop.
Type: Buchenavia capitata (Vahl.) Eichler.
102
TABLE 2.1 Genera studied, including subfamily, tribal and sectional classification. Sections, classification and number of species included within each genus Combretum are
from Stace (1980a, 1980b), Van Wyk (1984) and Mabberley (2008). Number of species included in this study is indicated in parentheses. Sectional classification of
Terminalia from Griffiths (1959).
Subfamily
Tribe
Subtribe
Strephonematoideae
Engl. & Diels
Combretoideae Engl. & Laguncularieae
Diels
Engl. & Diels
Combreteae DC.
Genus
Subgenus
Section
Strephonema Hook.f.
Terminaliinae (DC)
Exell & Stace
Combretinae Exell &
Stace
No. of
species
3-4 (2)
1 (1)
Lumnitzera Willd.
2 (2)
Anogeissus (DC.)Wall
8 (2)
Buchenavia Eichler
Conocarpus L.
24 (2)
2(2)
Bucida L.
(= Terminalia L.)
Pteleopsis Engl.
Terminalia L.
4 (1)
West Tropical Africa
Tropical America, Western
Tropical Africa
Eastern tropical Africa to
Australia including India and
some islands in the Indian and
Pacific Oceans
Old world tropics
Calycopteris Lam.
9 (2)
(2)
(1)
(1)
(1)
(1)
(2)
(1)
(1)
(11)
1(1)
Tropical America
Tropical America and Africa,
northeast Africa to southern
Yemen
Florida, Central America, West
Indies
Tropical and Southern Africa
—
—
—
Africa
—
Africa
—
Africa
—
South East Asia
Calopyxis Tul.
23 (1)
Madagascar
Abreviatae
Catappa
Mantaly
Myrobalanus
Pentaptera
Platycarpae
Psidioides
Stenocarpae
Unknown
103
Combretum Loefl.
Cacoucia (Aubl.) Conniventia
Exell & Stace
Megalantherum
Oxystachia
Poivrea
Combretum
Loefl.
Guiera Adans
Quisqualis L.
Thiloa Eichler
20 (3)
Africa
1 (1)
1 (1)
31 (6)
Namibia, Angola
Namibia
Africa, Madagascar and Southeast
Asia.
Southern Africa
Angustimarginata
6 (6)
Breviramea
Campestria
Ciliatipetala
Glabripetala
Hypocrateropsis
Macrostigmatea
Mettalicum
Micrantha
Spathulipetala
5(1)
4 (1)
10 (9+3)
8 (3)
6 (5)
4 (3+1)
4 (1)
2 (1)
1 (1)
1(1)
2 (2)
16 (3)
3 (1)
Africa
Africa
Africa and Arabic Peninsula
Africa
Africa
Africa
Africa
West Africa
Africa
North Tropical Africa
Zambia, Zimbabwe and
Madagascar
Old World tropics
104
TABLE 2.2 Maximum parsimony statistics from the analyses of the separate and combined data sets.
rbcL
rbcL
trnH-psbA
psaA-ycf3
Myrtales
Combretaceae
No. of taxa
126
100
85
96
Combined
plastid
103
ITS
93
Combined plastid
+ ITS
103
No. of included characters ( = aligned length)
1349
1349
667
929
2945
738
3683
No. of constant characters
924
1144
460
704
2308
337
2645
No. of variable sites
425
205
207
225
637
401
1038
(31.5%)
(15.19%)
(31.03%)
(24.22%)
(21.63%)
(54.34%)
(28.18%)
282
117
116
149
382
334
716
(20.9%)
(8.67%)
(17.39%)
(16.04%)
(12.97%)
(45.26%)
(19.44%)
No. of most parsimonious trees
6340
463
4
1426
3910
2500
184
Tree Length
1148
347
341
314
1037
1744
3163
CI
0.48
0.67
0.75
0.82
0.72
0.41
0.46
RI
0.76
0.87
0.91
0.92
0.88
0.78
0.76
Average number of changes per variable site
2.70
1.70
1.65
1.39
1.63
4.35
3.05
No. of parsimony informative sites
(number of steps/number of variable sites)
105
12
69
Combretoideae
Combretaceae
6
78
10
18
15
7
36
4
7
15
2
3
4
32 51
10
11 99
17
72
16
79
12
85
4
16
65
13
4
6
16 79
6
98 12
99
2
10
3
3 75 11
7
69
4
61
22
28
3
99
17
73
44
100
29
54
44
56
.
24
21
5
6
15
12
83 7
29
11
7
79
90
30
59
41
33
Strephonema mannii
Strephonema pseudocola
Lythrum salicaria
Cuphea llavea
Galpinia transvaalica
Punica granatum
Camissonia boothii
Oenothera macrocarpa
Clarkia xantiana
Ludwigia peploides
Erisma floribunda
Vochysia tucanorum
Qualea sp.
Ruizterania albiflora
Leptospermum scoparium
Melaleuca alternifolia
Eugenia uniflora
Heteropyxis natalensis
Psiloxylon mauritianum
Alzatea verticillila
Olinia vanguerioides
Melastoma beccarianum
Abroma angusta
Theobroma cacao
Erodium gruinum
Zygophyllum cordifolium
Escallonia pulverulenta
Teucridium parvifolium
Xylopia hypolampra
Laurus nobilis
Lythraceae
Onagraceae
Vochysiaceae
Myrtaceae
Crypteroniaceae
Melastomataceae
Malvaceae
Geraniaceae
Zygophyllaceae
Escalloniaceae
Lamiaceae
Annonaceae
Lauraceae
FIGURE 2.1 A single randomly selected (of the 6 340) equally most parsimonious tree based on the combined plastid
data (TL = 1 148 steps, CI = 0.48 and RI = 0.76). Numbers above the branches are Fitch branch lengths (DELTRAN
optimisation), and those below the branches are bootstrap percentages above 50%. Arrows indicate groups not
present in the strict consensus tree.
106
Combretum erythrophyllum
1
62/1.0
1
2
84/1.0
9
93/1.0
Combretum woodii
Combretum kraussii
1
1
Combretum nelsonii
Angustimarginata
Combretum caffrum
Combretum vendae
4
-/0.98
Combretum sp. nov. E
6
99/1.0
2
Combretum mkuzense
Spathulipetala
Combretum zeyheri
15
100/1.0
1
1
6
-/0.85
12
1
-/0.57
Combretum engleri
Macrostigmatea
Combretum kirkii
Combretum glutinosum
Glabripetala
Combretum fragrans
6
Combretum apiculatum subsp. leutweinii
1
-/0.95
Combretum molle (RSA 1)
1
1
Combretum psidioides subsp. dinteri
2
11
90/1.0
2
85/1.0
Combretum sp. nov. A
2
4
5
-/1.0
2
72/1.0
1
2
5
1
5
2
20
100/1.0
3
95/0.1
5
1
7
20
54/1.0
1
1
63/0.95
5
91/1.0
1
7
1
62/0.99
9
97/1.0
4
69/1.0
1
11
13
3
60/1.0
10
100/1.0
1
1
-/0.52
12
20
3
52/1.0
7
4
97/0.99
4
88/0.95
19
57/1.0
1
3
93/1.0
2
2
4
2
5
2
96/0.87
1
2
53/0.96
3
8
6
3
1
3
96/1.0
1
1
3
93/1.0
7
3
14
5
55/0.65
Combretum petrophyllum
Combretum sp. nov. B
Combretum sp. nov. C
Combretum celastroides subsp.orientale
Combretum padoides
Combretum celastroides subsp.celastroides
Hypocrateropsis
Combretum tenuipes
Combretum collinum
Combretum collinum subsp. gazense
Combretum collinum subsp. suluense
Mettalicum
Combretum collinum subsp. taborense
Combretum collinum subsp. hypopilinum
Combretum hereroense
Breviramea
Combretum imberbe (Nam)
Combretum imberbe (RSA)
Combretum elaeagnoides
Hypocrateropsis
Campestria
Meiostemon tetrandrus
Meiostemon humbertii
Combretum platypetalum (Nam)
Combretum platypetalum (Zim)
Combretum microphyllum
Conniventia
Combretum coccineum
Poivrea
Thiloa glaucocarpa
Combretum wattii
Megalantherum
Quisqualis caudata (=Combretum)
Quisqualis indica (=Combretum)
Quisqualis parviflora (=Combretum)
Combretum grandiflorum
Poivrea
Calopyxis grandidieri (=Combretum)
Combretum holstii
1
1
1
Combretum moggii
Combretum paniculatum
7
1
-/0.63
Ciliatipetala
Combretum edwardsii
Subgenus Combretum
3
Tribe Combreteae Subtribe Combretinae
Combretum apiculatum subsp. apiculatum
5
97/1.0
3
-/1.0
Micrantha
Subgenus Cacoucia
2
-/0.93
Combretum micranthum
Combretum albopunctatum
1
62/0.98
11
Combretum mossambicense
Poivrea
Combretum bracteosum
Quisqualis littorea (=Combretum)
Combretum goldieanum
Poivrea
Combretum oxystachium
Oxystachia
107
Terminalia brachystemma
3
4
81/0.97
Terminalia molle
Terminalia sericea
Terminalia trichopoda
1
1
10
-/1.0
3
Terminalia catappa
19
1
-/0.65
4
89/1.0
4
10
4
5
12
99/1.0
2
2
8
4
94/1.0
2
10
66/1.0
1
5
11
100/1.0
6
99/1.0
4
87/1.0
12
100/1.0
4
54/0.98
1
4
5
16
11
97/1.0
3
52/0.9
19
45
96/1.0
25
21
12
Terminalia muelleri
Pteleopsis myrtifolia (Form 2)
Pteleopsis anisoptera
Terminalia tomentosa
Terminalia arjuna
Terminalia myriocarpa
Anogeissus leiocarpa
Terminalia chebula
Terminalia hainanensis
Conocarpus sericeus
Conocarpus erectus
Calycopteris floribunda
Guiera senegalensis
1
Laguncularia racemosa
9
5
22
100/1.0
Bucida buceras (=Terminalia)
Anogeissus acuminata var lanceolata
2
18
2
-/0.78
1
3
4
73/1.0
Terminalia stuhlmanii
Terminalia bellirica
11
1
-/0.65
Terminalia pruniuoides
Buchenavia tetraphylla
8
1
28
98/1.0
Terminalia sambesiaca
9
1
2
80/1.0
7
-/1.0
Terminalia stenostachya
Buchenavia reticulata
1
77
87/1.0
Terminalia phanerophlebia
1
3
21
66 / 1.0
Terminalia ivorensis
Terminalia mantaly
9
4
89/1.0
3
Terminalia litoralis
Tribe Combreteae Subtribe Terminaliinae
5
85/1.0
2
Terminalia kaernbachii
11
3
27
13
12
Lumnitzera littorea
Lumnitzera racemosa
Strephonema mannii
Eugenia uniflora
Ludwigia peploides
Tribe Laguncularieae
3
-/0.6
Subfamily
Strephonematoideae
16
FIGURE 2.2 One of the 3 910 equally parsimonious trees based on the combined plastid data (TL = 1,037 steps, CI =
0.72 and RI = 0.88). Numbers above the branches are Fitch lengths (DELTRAN optimisation), and those below the
branches are bootstrap percentages above 50%/Bayesian PPs > 0.5. Arrows indicate clades not present in the strict
consensus tree. Current subtribal (Vollesen, 1981) and sectional (Stace, 1980a) classification is indicated on the
right.
108
11
3
96/1.0
6
83/0.99
3
21
1
9
94/1.0
1
63/0.94
2
2
1
3
7
13
100/1.0
6
-/0.53
2
11
3
6
98/0.99
8
-/0.68
27
100/1.0
3
91/1.0
1
4
2
7
100/1.0
1
1
33
100/1.0
7
-/0.72
6
4
5
-/0.9
4
7
9
93/1.0
12
16
20
100/1.0
8
44
Combretum molle (RSA1)
Combretum molle (RSA2)
Ciliatipetala
Combretum moggii
Combretum edwardsii
Combretum nelsonii
Combretum caffrum
Combretum woodii
Combretum kraussii
Angustimarginata
Combretum vendae
Combretum fragrans
Glabripetala
Combretum mkuzense
Combretum zeyheri
Macrostigmatea
Spathulipetala
Combretum engleri
Combretum kirkii
Micrantha
7
53/0.98
22
38
8
8
14
100/1.0
5
13
100/1.0
19
99/1.0
1
23
4
4
81/0.93
4
85/1.0
9
100/1.0
4
70/0.99
5
1
4
15
100/1.0
7
6
89/0.99
1
9
6
5
-/0.96
12
100/1.0
5
17
7
64/0.99
14
100/1.0
6
86/0.99
7
100/1.0
2
5
10
18
19
Breviramea
Combretum celastroides subsp. celastroides
Combretum padoides
Hypocrateropsis
Combretum tenuipes
Combretum holstii
Poivrea
Quisqualis littorea (=Combretum)
Quisqualis parviflora (=Combretum)
Quisqualis caudata (=Combretum)
Quisqualis indica (=Combretum)
Poivrea
Combretum coccineum
Conniventia
Poivrea
1
Hypocrateropsis
1
Thiloa glaucocarpa
15
24
15
96/1.0
Campestria
Combretum wattii
17
14
100/1.0
Oxystachia
Megalantherum
Poivrea
1
25
2
2
90/1.0
2
7
57/0.94
Mettalicum
Combretum collinum
9
52/1.0
4
Subgenus Cacoucia
21
100/1.0
1
64/0.82
24
100/1.0
48
Subgenus Subgenus Subgenus
Combretum Cacoucia Combretum
6
5
-/0.73
34
91/0.94
4
77/0.99
8
11
Subgenus Combretum
5
9
88/1.0
7
92/1.0
Guiera senegalensis
109
14
-/0.69
9
54
100/1.0
4
Conocarpus sericeus
Conocarpus erectus
7
100/1.0
3
63/0.99
3
20
Terminalia molle
4
5
3
9
100/1.0
16
100/1.0
18
44
5
53/0.98
7
20
14
31
100
7
7
14
98/1.0
64
100/1.0
8
15
99/1.0
6
15
74/1.0
12
50/1.0
4
14
100/1.0
29
100/1.0
Terminalia mantaly
Terminalia prunioides
Terminalia chebula
15
1
18
1
1
Terminalia arjuna
22
4
.
7
31
6
53
1
14
2
26
95/0.99
Terminalia muelleri
6
6
-/0.8
2
13
5
-/1.0
Terminalia sericea
Lumnitzera littorea
Strephonema mannii
Tribe
Laguncularieae
1
1
53/0.98
2
2
Subfamily
Strephonematoideae
10
-/1.0
FIGURE 2.3 One of the 2 500 Fitch trees obtained from the analysis of ITS. Numbers above the branches are Fitch
lengths (DELTRAN optimisation), and those below the branches are bootstrap percentages above 50%/Bayesian PPs
> 0.5. Arrows indicate clades not present in the strict consensus tree. (TL = 1,744 steps, CI = 0.41 and RI = 0.78).
Current subtribal (Vollesen, 1981) and sectional (Stace, 1980a) classification is indicated on the right.
110
.
8
14
7
9
97/1.0
4
21
22
99/1.0
2
-/1.0
3
-/0.78
4
5
14
1
7
2
-/0.99
12 -/0.62
99/1.0
5
10
12
1
36
100/1.0
12
4
-/0.98
15
67/1.0
37
100/1.0
13
55/0.91
12
59/1.0
16
100/1.0
2
6
1
24
-/0.99
12
78/1.0
7
100/1.0
34
100/1.0
1
-/0.99
Combretum engleri
Combretum kirkii
Macrostigmatea
Micrantha
Combretum padoides
Hypocrateropsis
3
5
1
7
1
2
28
54/1.0
2
34
48
27
7
-/1.0
25
100 / 0.1
1
27
19
98/1.0
13
4
5
81/0.99
46
15
100/1.0
5
-/0.96
2
12
12
100/1.0
1
8
77/1.0
7
97/1.0
8
78/0.88
3
11
81/1.0
18
100/1.0
6
76/1.0
15
10
2
6
5
100/1.0
Combretum collinum
Mettalicum
Campestria
Breviramea
Hypocrateropsis
Combretum holstii
Poivrea
Calopyxis grandidieri (= Combretum)
Quisqualis parviflora (= Combretum)
Quisqualis caudata (= Combretum)
Quisqualis indica (= Combretum)
Poivrea
Conniventia
18
3
21
64/1.0
11
100/1.0
Calopyxis grandidieri (= Combretum)
13
Quisqualis littorea (= Combretum)
23
21
98/1.0
Combretum celastroides subsp.celastroides
Combretum tenuipes
2
10
13
100/1.0
Combretum vendae
Spathulipetala
29
8
Angustimarginata
Combretum woodii
Combretum kraussii
Combretum zeyheri
46
-/0.86
Glabripetala
Combretum mkuzense
16
22
100/1.0
Combretum fragrans
10
17
3
97/1.0
33
100/1.0
10
7
33
100/1.0
Combretum moggii
Combretum caffrum
Combretum nelsonii
1
Ciliatipetala
Combretum edwardsii
5
5
61/0.98
2
4
6
87/1.0
4
3
7
64/1.0
11
Subgenus Combretum
7
88/1.0
5
Subgenus Cacoucia
9
11 97/1.0
98/1.0
Combretum coccineum
Poivrea
45
6
-/0.97
5
-/0.69
27
20
17
23
96/1.0
29
67
Combretum wattii
Oxystachia
Megalantherum
Thiloa glaucocarpa
Guiera senegalensis
111
1
1
5
-/0.51
15
9
14
-/1.0
39
3
2
3
98/1.0
11
-/0.97
5
3
1
8
25
9
-/1.0
4
78/1.0
5
52
3
81/1.0
11
65/1.0
15
-/1.0
1
29
2
41
22 100/1.0
100/1.0
2
19
4
31
100/1.0
31
79/0.98
115
77/1.0
10
9
14
7
-/0.68
28
72/1.0
43
100/1.0
8
23
17
99/1.0
6
-/1.0
17
2
21
98/1.0
181
96/1.0
34
100/1.0
2
29
24
62
99/1.0
7
31
11
- /1.0
19
10
- / 0.95
80
88/1.0
21
12
8
52
23
-/1.0
25
Terminalia mantaly
35
15
15
Terminalia sericea
Terminalia molle
Terminalia pruniuoides
Terminalia stuhlmanii
Buchenavia tetraphylla
2
6
94/1.0
7
86
Terminalia chebula
Terminalia arjuna
Conocarpus sericeus
Conocarpus erectus
Lumnitzera littorea
Lumnitzera racemosa
Strephonema mannii
Eugenia uniflora
Ludwigia peploides
Tribe Laguncularieae
21
75/1.0
Terminalia muelleri
1
33
Terminalia stenostachya
17
16
71/1.0
68/0.96
Terminalia kaernbachii
Subfamily
Strephonematoideae
5
-/0.9
Terminalia catappa
FIGURE 2.4 One of the 184 most parsimonious trees (3 163 steps, CI = 0.46, RI = 0.76) from the combined plastid and
nuclear ITS data set. Numbers above the branches are Fitch lengths (DELTRAN optimisation), and those below the
branches are bootstrap percentages above 50%/Bayesian PPs > 0.5. Arrows indicate clades that collapse in the strict
consensus tree. Current subtribal (Vollesen, 1981) and sectional (Stace, 1980a) classification is indicated on the right.
112
113
114
Chapter 3: Notes on Combretum section Angustimarginata, Spathulipetala and Macrostigmatea and C.
nwambiyana
CHAPTER 3: NOTES ON THE PHYLOGENY, CLASSIFICATION AND BIOGEOGRAPHY OF
COMBRETUM SECTIONS ANGUSTIMARGINATA, SPATHULIPETALA AND MACROSTIGMATEA S.S.
(COMBRETACEAE), WITH THE DESCRIPTION OF A NEW SPECIES FROM SOUTH AFRICA
3.1 INTRODUCTION
The well-resolved proposed phylogenetic tree resulting from a recent molecular study on the
family Combretaceae R.Br. (Maurin et al., 2010; Chapter 2) enabled a review of relationships
within Combretum Loefl. subgenus Combretum. Results suggested a close relationship between
sections Angustimarginata Engl. & Diels and Macrostigmatea Engl. & Diels sensu stricto with
the inclusion (if strict monophyly is followed) of Combretum zeyheri Sond. (section
Spathulipetala Engl. & Diels) within section Macrostigmatea sensu lato.
Section Angustimarginata includes six species (Combretum caffrum (Eckl. & Zeyh.)
Kuntze, C. erythrophyllum (Burch.) Sond., C. kraussii Hochst., C. nelsonii Dummer, C. vendae
A.E.van Wyk and C. woodii Dummer), all restricted to southern Africa. According to Exell
(1970, 1978) the inconspicuous scales, often obscured by an indumentum of combretaceous
hairs and/or glutinous secretions (the latter more noticeable in herbarium material), distinguish
this section from the rest of Combretum. Van Wyk (1984) considered the section to be a
homogenous and natural taxon, and also supplied additional diagnostic characters. Section
Macrostigmatea s.s., as previously defined, comprises four species (Combretum engleri Schinz,
C. schumannii Engl., C. kirkii M.A.Lawson, C. gillettianum Liben) from eastern and southern
Africa. Up to now section Spathulipetala has been considered monotypic, with C. zeyheri Sond.
the sole representative; this species is widespread throughout southern Africa. The recently
described Combretum mkuzense J.D.Carr & Retief from northeastern KwaZulu-Natal
(Maputaland) was not formerly included in any section and molecular data provided by Maurin
115
nwambiyana
et al. (2010; Chapter 2), suggests its placement either within section Macrostigmatea s.s. or
Spathulipetala.
The primary aim of this chapter is to reassess delimitation of the African Combretum
sections Angustimarginata, Macrostigmatea s.s. and Spathulipetala, by evaluating phylogenetic
relationships based on molecular and morphological evidence. The morphological characters
used to distinguish these three sections within Combretum are discussed. The geographical
range of each species is related to the African phytochoria of White (1983). A new species from
the Kruger National Park, South Africa, is presented; its position within section Macrostigmatea
s.s. is evaluated and an identification key for this section is presented.
3.2.1 Plant material
Material of most species currently recognised within sections Angustimarginata,
Macrostigmatea s.s. and Spathulipetala was available for the study, except for C. schumannii
Engl. and C. gillettianum Liben (both section Macrostigmatea). Combretum mkuzense and the
new species from Kruger National Park, two species that molecular data have shown to be
closely related to section Macrostigmatea s.s. and Spathulipetala (Maurin et al., 2010; Chapter
2), were also included in the sampling. Two representatives of section Ciliatipetala Engl. &
Diels. as well as C. imberbe Wawra (section Plumbea O.Maurin, M.Jordaan & A.E.van Wyk)
and C. celastroides subsp. celastroides (section Hypocrateropsis Engl. & Diels.) were selected
as outgroups based on results from Maurin et al. (2010; Chapter 2). In total 15 taxa were
included, and their voucher information is presented in Appendix 3.1.
116
nwambiyana
3.2.2 Scale morphology
Leaf and fruit material (from herbarium specimens) was used to obtain scales for light
microscopic study. Intact leaves or fruit were partly rehydrated in boiling water and stained for
one hour in a 1% aqueous solution of toluidine blue. After washing with water to remove excess
stain, the material was dehydrated in an ethanol series, transferred through two changes of
absolute ethanol:xilene (50:50) and finally two changes of xilene. A drop of the mountant
entellan (Product 7961, E. Merck, Darmastadt), diluted with xylene, was deposited onto the
material. The surface of the leaf/fruit below the drop of entellan was then gently scraped with a
scalpel to loosen the scales. This is best done under a dissecting microscope, which allows for
the mostly darkly stained scales to be viewed. A drop of entellan with suspended scales was
removed from the plant surface with a Pasteur pipette and mounted on a microscope slide with a
cover slip. Slides were observed under a Zeiss Axioplan 2 compound microscope, and images
were captured on an Axiovision 4.7 light microscope. The Z-option of the image capture
software was used to produce a sequence of digital pictures of the same scale at different
focusing levels. These images were then stacked using the Combine ZM free software
(http://www.hadleyweb.pwp.blueyonder.co.uk/CZM/Manual/Install.htm).
3.2.3 Phylogenetic analyses
analyse the combined sequence data of the taxa included in this analysis. Tree searches were
conducted using 1,000 replicates of random taxon addition, retaining 10 trees at each step, with
tree-bisection-reconnection (TBR) branch swapping and MulTrees in effect (saving multiple
equally parsimonious trees). The trees collected in the 1000 replicates were then used as starting
trees for another search without a tree limit. Support for clades in all analyses was estimated
using bootstrap analysis (Felsenstein, 1985) with 1000 replicates, simple sequence addition and
117
nwambiyana
TBR swapping with MulTrees in effect but saving a maximum of 10 trees per replicate.
Bootstrap percentages (BP) were classified as high (85–100), moderate (75–84) or low (50–74).
All data sets were analysed separately, and the individual bootstrap consensus trees examined by
eye to identify topological conflicts, i.e. moderate to high support for different placement of
taxa. 'Congruence tests' such as the incongruence length test (ILD) can be unreliable (Reeves et
al., 2001; Yoder et al., 2001) and therefore were not used in this study. Delayed transformation
character optimisation (DELTRAN) was used to calculate branch lengths, due to reported errors
was performed using MRBAYES v. 3.1.2 only on the combined data set. For each matrix, ITS,
rbcL, psaA-ycf3, trnH-psbA, the most appropriate model was selected using MODELTEST v.
3.06 (Posada & Crandall, 1998). For ITS, rbcL and psaA-ycf3, GTR+I+G was selected, and for
trnH-psbA, TIM + G, in which the two resulting models share the same number of substitutions
= 6 and rates = gamma, base frequency = empirical and clock = unconstrained; 2,000,000
generations were used with trees sampled every 200. The resulting trees were plotted against
their likelihoods to determine the point where likelihoods converged on a maximum value, and
all the trees before the convergence were discarded as ‘burn-in’ (1000 trees). All remaining trees
were imported into PAUP 4.0b10, and a majority-rule consensus tree was produced showing
frequencies (i.e. posterior probabilities or PP) of all observed bi-partitions. PPs are shown on the
MP trees because the topologies are identical. The following scale was used to evaluate PPs:
below 0.95, weakly supported; 0.95–1.0, well supported.
118
nwambiyana
3.2.4 Evaluation of morphological and biogeographical data
Morphological data were recorded from field observations, herbarium specimens and literature,
especially Carr (1988). Scale structure was compared with data from Stace (1969). Species
distributions are based on new collections made for this study and existing information from
Klopper et al. (2006), www.tropicos.org, Missouri Botanical Garden (2009), and the
International Plant Name Index (2008). Distribution maps are presented in Figure 3.9, and
ecological data (climate and habitat) for all species are presented in the results. The map
template was obtained from Hester Steyn (SANBI) and is based on Van Wyk & Smith (2001;
map 3). Morphological characters used are presented in Appendix 3.2 and characters states in
Appendix 3.3. Characters states in extant taxa were investigated and plotted by hand on one of
the most parsimonious trees.
3.2.5 Species description and identification key
A description for a new species from Kruger National Park is presented. To formally describe
this new species more flowering material will be needed. An identification key for all species of
sections Angustimarginata, Spathulipetala and Macrostigmatea, including the species not
present in the molecular sampling is provided.
3.3 PHYLOGENETICS, CLASSIFICATION AND BIOGEOGRAPHY OF SECTION ANGUSTIMARGINATA,
MACROSTIGMATEA S.S.
AND SPATHULIPETALA
3.3.1 Distribution, habitat and habit
Distribution maps are presented in Figure 3.1. The majority of the taxa occur in savannas
(woodland) and thickets, usually in relatively arid areas. Two species differ from the rest
119
nwambiyana
however: Combretum caffrum occurrs mostly in gallery forest/riverine bush in the Eastern Cape
and C. kraussii in temperate Afromontane and subtropical coastal forest in the eastern and
northeastern parts of South Africa. In most cases the distribution of the taxa presented is
relatively restricted, some being extremely localised; C. zeyheri has the most extensive
distribution in southern and eastern Africa. Here, for each species, I first review distribution and
habitat, followed by the habit. Species are related to the African phytochoria of White (1983), as
modified by Huxley et al. (1998), and the more local centres of endemism as demarcated in Van
Wyk & Smith (2001).
Combretum caffrum (Eckl. & Zeyh.) Kuntze. — The species is endemic to the Eastern Cape
Province of South Africa (Figure 3.1a), where it is near-endemic to the Albany centre of
endemism (Van Wyk & Smith, 2001). It occurs in the Afromontane archipelago-like centre of
endemism, and in the Maputaland-Pondoland regional mosaics where it is usually associated
with gallery forest/bush along the banks of watercourses. It favours proximity to water but can
also be found on hills and mountains up to 1 100 m a.s.l. (above sea level). Combretum caffrum
can be confused with C. erythrophyllum (section Angustimarginata), which has a much wider
distribution in southern Africa but does not overlap the range of C. caffrum.
Combretum engleri Schinz — The species occurs in northern Namibia including the Caprivi
Strip, and southern Angola (Figure 3.1b), mainly associated with the Zambesian regional centre
of endemism and Kalahari-Highveld regional transition zone. It generally grows in savanna and
mixed woodland, under relatively arid conditions and on deep Kalahari sand at elevations
between 1 500 and 2 000 m a.s.l. It is rarely abundant and generally found as widely scattered
plants in its range. Combretum engleri and C. schumannii share several morphological
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characters, and some authors (Exell, 1970, 1978; Wickens, 1973) have sunk C. engleri into C.
schumannii.
Combretum erythrophyllum (Burch.) Sond. —Found in Botswana, Mozambique, Namibia,
South Africa and Zimbabwe. In Namibia it occurs only along the Orange River on the border
with South Africa (Figure 3.1c). The distribution covers several phytogeographical regions,
namely the Zambesian regional centres of endemism, the Afromontane archipelago-like centre
of endemism, the Swahilan-Maputaland regional transition zones and the MaputalandPondoland regional mosaics. Like C. caffrum, it favours proximity to water, usually growing
along watercourses, but it can also occur some distance from water, with the ability to seemingly
tolerate dry periods. It is found from sea level up to 1 600 m a.s.l.
Combretum gillettianum Liben. (provisional) — A species with a restricted distribution from
Zambia to the Democratic Republic of Congo (Figure 3.1d). It is associated with the Zambesian
regional centres of endemism in Brachystegia woodland at elevations of around 900 m a.s.l.
Combretum kirkii M.A.Lawson —The species has a scattered distribution and is sometimes
locally abundant in Mozambique, Malawi, Zambia and Zimbabwe (Figure 3.1e). It is present in
the Zambesian regional centres of endemism and can be found in a wide range of vegetation
types such as grassland, woodland and along rivers.
Combretum kraussii Hochst. — The species occurs on the eastern side of South Africa, southern
Mozambique and Swaziland (Figure 3.1f). It is present in the Zambesian regional centres of
endemism, the Afromontane archipelago-like centre of endemism and the MaputalandPondoland regional mosaic. It is generally associated with mostly evergreen forests, their
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margins, and relatively high-rainfall mountain slopes, rocky outcrops and in ravines from sea
level up to 1 200 m a.s.l. Combretum kraussii was considered by Exell (1970, 1978) to be a
synonym of C. woodii and C. nelsonii, a view not followed here.
Combretum mkuzense J.D.Carr & Retief — The species is restricted to the northern part of
KwaZulu-Natal (Figure 3.1g) where it occurs in the Maputaland-Pondoland regional mosaics
region, in mixed woodland on deep sand. It is endemic to the Maputaland centre of endemism
(Van Wyk & Smith, 2001).
Combretum nelsonii Dummer — The species is endemic to South Africa, mainly occurring in
the Limpopo Province and in the northwestern part of Mpumalanga (Figure 3.1h). It is found in
the Zambesian regional centre of endemism, in open vegetation such as savanna woodland,
mostly in rocky places on sandy soils around 1 000 and 1 200 m a.s.l.
Combretum nwambiyana O.Maurin, M.Jordaan & A.E.van Wyk. —An apparently rare species,
known at present only from the northern part of the Kruger National Park (Figure 3.1i), the
Nwambiya Sandveld, an outlier area of deep Kalahari sand that forms part of the Zambesian
regional centre of endemism. This particular sandveld is relatively small in South Africa, but
covers a much larger area in adjacent parts of Mozambique where the distribution of the species
remains to be assessed. It is associated with a dry and floristically diverse form of thicket, a
vegetation type often containing highly localised species. The elevation of the sandveld varies
between 400 and 600 m a.s.l.
Combretum schumannii Engl. (provisional) —The distribution of the species is centred in
eastern African with records from Somalia, Kenya, Tanzania, Mozambique, Malawi, Zambia,
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and the Caprivi Strip in Namibia and northern Botswana (Figure 3.1j). However, the fact that C.
schumannii is sometimes treated as a synonym of C. engleri could cause some confusion in
maps attempting to depict distributions of the two species. The distribution of C. schumannii is
distinct (Carr, 1988), and therefore records of C. schumannii in southeastern Zambia, northern
Botswana and Namibia might actually be of C. engleri. It is present in the Somali-Masai and
Zambesian regional centre of endemism and Swahilan-Maputaland regional transition zone. The
species is found in a wide range of vegetation types, from lowland rainforest to Brachystegia
woodland.
Combretum vendae A.E.van Wyk — Endemic to South Africa, where it is restricted to the
Soutpansberg mountain range in Limpopo Province, an area that forms part of the Soutpansberg
centre of endemism (Van Wyk & Smith, 2001; Figure 3.1k). It occurs in the Zambesian regional
centre of endemism and Afromontane archipelago-like centre of endemism. It is found in
savanna woody vegetation that is relatively low, hot and arid. Two forms of C. vendae
(distinctively glabrous and pubescent) have been reported in the region.
Combretum woodii Dummer — The species is often associated with C. kraussii with the
distribution of the latter overlapping that of C. woodii. It occurs in northern KwaZulu-Natal,
Mpumalanga and Swaziland. In Mpumalanga it is relatively rare and can only be found in the
vicinity of the Strydom Tunnel, Barberton and on Ship Mountain southeast of Pretoriuskup in
the Kruger National Park (Figure 3.1l). It is associated with the Afromontane archipelago-like
centre of endemism and in the Maputaland-Pondoland regional mosaic. It is generally found in
open woodland or forest, mostly on rocky slopes but also on sand, in riverine thickets and
wooded gorges up to 1 200 m a.s.l.
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Combretum zeyheri Sond. — This is a species with a wide distribution in southern and eastern
Africa occurring from the northern part of KwaZulu-Natal and present in Mpumalanga and
Limpopo provinces in South Africa, Swaziland, Mozambique, northern Botswana, Namibia
(including the Caprivi strip), Angola, Zambia, Malawi, the southern part of the Democratic
Republic of Congo, Tanzania, and parts of Kenya (Figure 3.1m). Its range covers several
phytogeographical regions, namely the Somali-Masai and Zambesian regional Centre of
endemism, the Afromontane archipelago-like centres of endemism, the GuineoCongolian/Sudanian and Swahilan-Maputaland regional transition zone, and the MaputalandPondoland regional mosaic. Due to its extensive range it is found in many kinds of vegetation
such as grassland, savanna, thicket and woodland from 50 m up to 1,500 m. It can be found in
dry conditions but also close to water; it is tolerant of a variety of soil types.
Most species in the three sections included in the study are trees and shrubs, with no real
climbers with the exception of C. kirkii and under certain conditions C. woodii. Several species
such as C. kraussii, C. woodii, C. mkuzense and C. nwambiyana can present typical
“combretaceous scandent habit” on new and vigorous shoots.
The habitat is variable within the three sections. Species can occur in: (a) forest or along
forest edges, for example C. kraussi (section Angustimarginata) and in some cases C. woodii
(section Angustimarginata); (b) dry sand forests, for example C. mkuzense and C. nwambiyana
(both included within section Spathulipetala); (c) along rivers or in proximity of water, for
example C. erythrophyllum, C. caffrum (both from section Angustimarginata), and C. kirkii
(section Macrostigmatea); and (d) savanna or open woodland, for example C. engleri (section
Macrostigmatea), C. nelsonii (section Angustimarginata), C. vendae (section Angustimarginata)
and C. zeyheri (section Spathulipetala).
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Most species studied in these sections are subjected to frequent fire but present relatively
thin and smooth back that surprisingly seems to provide relatively efficient protection against
fire. Several of these species are capable of overcoming the passage of fire, most probably
because they have the ability to develop woody parts underground that enable them to re-sprout;
growing among rocks (as in C. nelsonii) may provide additional protection. The position of the
cotyledons is located for most taxa above the level of the soil. As mentioned by Exell & Stace
(1972) the rather unusual germination observed in C. zeyheri with an independent shoot rising
from below the fused cotyledons (Carr, 1988) has never been recorded in rainforest species and
therefore may well be an adaptation to fire. Combretum zeyheri is the only member of the
sections discussed here that exhibits such an unusual type of germination. All others have the
new shoot rising from between the two cotyledons, which are above soil level. Combretum
zeyheri has obviously been successful in adapting to fire, which may explain its extensive range
in fire-prone vegetation.
3.3.2 Phylogenetic data
Maximum parsimony analysis of the combined matrix provided the following statistics: number
of included characters = 3683; number of constant characters = 3420; number of variable sites =
263 (7.14%); number of parsimony informative sites = 139 (3.77%); number of trees (Fitch) =
6; number of steps (tree length) = 364; CI = 0.83; and RI = 0.85. One of the most parsimonious
trees is presented in Figure 3.2.
Section Angustimarginata is weakly supported as sister to sections Macrostigmatea and
Spathulipetala (52% BP) in maximum parsimony analyses, but Bayesian analysis resulted in
0.91 PP, which is still weakly supported. Section Angustimarginata is strongly supported (100
BP/1.0 PP) with two well-supported subclades. In the first subclade, although relationships were
unresolved, there was moderate (MP) to high (PP) support for the grouping C. erythrophyllum,
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C. nelsonii and C. caffrum (70 BP/0.98 PP) with C.woodii sister to it (99 BP/1.0 PP). In the
second subclade, C. kraussii and C. vendae group together with strong support (99 BP/1.0 PP).
Section Spathulipetala (C. zeyheri) is strongly supported (100 BP/1.0 PP) and embedded within
section Macrostigmatea. Within this clade, and considering that I was unable to include two
species (C. schumannii Engl., C. gillettianum Liben) previously associated with section
Macrostigmatea, C. engleri and C. kirkii are successively sister (61 BP/1.0 PP; 100 BP/1.0 PP,
respectively) to C. nwambiyana, C. mkuzense and C. zeyheri (99 BP/1.0 PP).
3.3.3 Morphological characters
Coded characters were mapped by hand in the most parsimonious way onto one of the most
parsimonious trees and presented in Figures 3.3 to 3.7 (Appendices 3.2 and 3.3).
Several morphological characters, such as the bark structure, position of cotyledons, and
scale density on the lamina, support a close relationship between the three sections. Several
characters can also be used to distinguish the three sections from each other. Species within
section Angustimargina share leaves that are cream-coloured in spring, turning reddish purple in
autumn. Size and the colour (when mature) of fruits are also useful for delimiting the sections;
representatives within section Angustimarginata possess relatively small fruits of about 20 x 20
mm that are generally yellowish tinged or uniformly pink to red, whereas in sections
Spathulipetala and Macrostigmatea s.s. fruit are mostly large and greenish to yellowish.
Overall, fruits within sections Macrostigmatea and Spathulipetala are relatively large compared
to section Angustimarginata with C. zeyheri possessing the largest fruits in the genus. These
large fruits also have a “pod part” with a tough pericarp that possibly plays a role as fire
protection for seeds. Scale morphology can also be used to separate the three sections, as
discussed in the following paragraph.
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3.3.4 Leaf scales anatomy
Scale anatomy is best assessed in scales obtained from young developing leaves that are freshly
fixed and preserved in FAA; this allows for the preservation of complete and turgid scales. I
found that in rehydrated herbarium material or leaves collected at a late stage, most of the scales
are somewhat shrivelled and damaged due to the release of secretions that often form a glutinous
layer on cuticle.
Results from the present study were compared with the description of scales in Stace
(1969) and Van Wyk (1984). Section Angustimarginata has the simplest scale cell structure
within subgenus Combretum: scales are rounded, slightly scalloped along the margin and
composed of 8–16 cells with only primary radial walls presents. Scales of C. kraussii are
depicted in Figure 3.8. Sections Macrostigmatea s.s. and Spathulipetala possess slightly more
complex scales with a range of variation from simple scales as in section Angustimarginata to
scales composed of up to 25 cells, which including primary and secondary tangential walls. The
“most complex scale type” is found in C. kirkii. Scales of C. mkuzense (Figure 3.9), C.
nwambiyana (Figure 3.10), and C. zeyheri are similar and cannot be used to distinguish among
these species, especially the first two mentioned. In section Angustimarginata scales are
generally glistening, which is not the case in the other two sections.
3.4 DISCUSSION
From a morphological perspective, sections Angustimarginata, Macrostigmatea s.s. and
Spathulipetala have been well studied; however, molecular results add a new dimension to our
understanding of their relationships.
Stace (1969) characterised section Angustimarginata by the presence of scales on all
parts (leaf, fruits, and inflorescence), often hidden by copious glutinous secretion and sparse to
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dense combretaceous hairs on all parts. He suggested that morphological characters in this
section, with the exception of the absence of hairs on petals and the congested inflorescences,
are similar to those of section Ciliatipetala. Exell (1970, 1978) described section
Angustimarginata as being characterised by the upper receptacle being cupuliform to
campanulate, petals glabrous and variable in shape (subcircular, obovate to spathulate and
elliptic), stamens inserted shortly above the margin of the disk, which is glabrous with the
margin shortly free and pilose. Scales are composed of 8–16 cells, more abundant on the upper
surface of the leaf blade, inconspicuous, generally small (50–75 um in diam.) and often
obscured by an indumentum of combretaceous hairs and/or glutinous secretions. Van Wyk
(1984) added to the characters defined by Exell (1970, 1978), specifically: bark more or less
smooth or flaking in small pieces, juvenile leaves partly or completely cream-coloured, autumn
leaves bright red, exterior calyx lobes usually tinged reddish purple, mature fruits partly to
completely tinged pink to dark red, and secondary xylem of older stems with islands of
interxylary phloem.
Section Macrostigmatea s.s. was characterised by Exell (1970, 1978) as possessing
glutinous flowers arranged in subcapitate spikes, with an upper receptacle cupuliform to
infundibuliform, petals obovate and circular and glabrous, and the disk glabrous or pilose with a
short free margin. Leaf scales are generally small (45–85 µm in diameter) and 8-16-celled. Stace
(1968) also mentioned that scales are present, and all parts have glutinous secretion and hairs
mostly sparse on leaves and fruits and sparse to abundant on the flowers.
Section Spathulipetala comprises a single species, C. zeyheri, and is viewed by Exell
(1970, 1978) as a section evidently linked to section Macrostigmatea s.s. He described the
section as having the upper receptacle infundibuliform, petals obovate to spathulate, glabrous,
disc pilose with a free margin, leaf scales rather small (40–75 µm in diameter), circular to
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slightly convexly scalloped delimited by 7–9 cells tangential walls. Scales in this section are
frequent on all young above-ground parts.
The observations and results from the current study support the close relationships of the
three sections and the distinction of Angustimarginata from Macrostigmatea s.s./Spathulipetala.
Section Angustimarginata, described by Van Wyk (1984) as a natural group, is well supported
(Maurin et al., 2010; Chapter 2); however, the distinction between Macrostigmatea
s.s./Spathulipetala is slightly more difficult to assess since C. zeyheri (section Spathulipetala) is
embedded within section Macrostigmatea s.s. Although the two missing taxa of section
Macrostigmatea (C. schumanii and C. gillettianum) should be included in the analysis to
confirm the decision to transfer C. zeyheri to section Macrostigmatea s.s., current
morphological and molecular results are sufficient to warrant a partial solution. I present two
options: (a) enlarge section Spathulipetala to incorporate the two new species; or (b) transfer C.
zeyheri (section Spathulipetala) to section Macrostigmatea. The first option of enlarging
Spathulipetala to include the two obviously closely related species is well supported (99 BP/1.0
PP). The three species share the characteristic of having large 4-winged fruits, most certainly the
largest within the genus. This character is however also shared with C. kirkii, C. engleri, C.
schumannii and C. gillettianum from section Macrostigmatea s.s. The second option, for an
enlarged section Macrostigmatea is tempting as molecular results show strong support (100
BP/1.0 PP) for the clade Macrostigmatea s.s./Spathulipetala. There are numerous morphological
characters that have been identified and seem useful to distinguish section Angustimarginata
from Macrostigmatea s.l. As mentioned previously, spring and autumn leaves are characteristic
of section Angustimarginata and not observed in Macrostigmatea s.l. Leaf scales also present an
obvious distinction between Angustimarginata and Macrostigmatea s.l.: the former is
characterised by a small number of cells per leaf scales (<16), absence of primary and secondary
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radial and tangential walls, and scales that are often glistening; the other section does not have
such characters.
According to Exell & Stace (1972), four types of cotyledons are known for
Combretaceae, namely: (a) below ground; (b) arising from the hypocotyls above ground on
short petioles; (c) arising below ground but emerging above ground on long petioles; and (d)
arising below ground but emerging and being fused above ground to form an unusual peltate
structure on a single long stalk formed by the connate petioles. The last type of seedling is rare
in the genus and has only been reported in C. zeyheri (section Macrostigmatea s.l.), C. collinum
(section Glabripetala), and C. fragrans (section Glabripetala) (Exell & Stace, 1972), all of
which are successful species in savannas prone to fire. It is thus not a character unique to C.
zeyheri, although it could still be considered an autapomorphy for this particular clade and
therefore used to separate sections Macrostigmatea s.s. and Spathulipetala. I did not consider
this feature significant enough to separate the two sections.
Unfortunately few germination records (and seedling descriptions) are available for
members of Combretum, and I would recommend that more evidence on germination be
gathered for the genus and experiments be initiated. These traits would be informative to
investigate as they could show a correlation for the species occurring in fire-prone vegetation:
for example thin or rough bark, underground woody structures that would allow the plant to
resprout (when not possessing thick and protective bark), adjustment in the germination process
(epigeal or hypogeal), and young plants to regenerate shoots from lateral buds located on the
hypocotyle.
I here propose, giving due consideration to the fact that two taxa from section
Macrostigmatea are absent from the study and that there are no obvious morphological
synapomorphies separating the two sections, that section Spathulipetala be provisionally
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subsumed into section Macrostigmatea s.l., classifying de facto all species discussed above
within the same section.
The situation regarding Combretum scales and their evolutionary development remains
unclear (Stace, 1969). The largest and most complex scales within Combretum are found in
section Hypocrateropsis, and this section is also viewed as one of the most primitive (or least
advanced) of the genus because of the shape of the almost flat upper hypanthium (Stace, 1969).
A study by Van Wyk (1984) on section Angustimarginata considered the scales of C. kraussii to
be the simplest (eight cells) and most primitive within the section, with all other species of
section Angustimarginata derived from it. Combretum kraussii has a cupuliform to flat upper
hypanthium suggesting a primitive character for this particular section. In the three sections
studied here, section Angustimarginata possesses simple scales with 8–10 (–16) cells and
primary radial walls only, whereas in Spatulipetala and Macrostignatea scales are more
complex with a greater number of cells and primary and secondary radial and/or tangential walls.
In section Angustimarginata, the shape of the upper hypanthium is conspicuously variable, C.
kraussii being clearly distinct with the most open upper hypanthium, whereas in the remaining
species it is more campanulate to elongate (Van Wyk, 1984). Exell (1970, 1978) and Wickens
(1973) characterised sections Macrostigmatea s.s. and Spathulipetala by their cupuliform to
infundibuliform upper hypanthium. In section Hypocrateropsis I did not observe an association
between a flat upper hypanthium and large and complex scales, a pattern previously noted by
Stace (1969).
Although I can offer no conclusive evidence for the evolution of scales within
Combretum, a way to elucidate this phenomenon might be to use molecular dating methods.
Results from phylogenetic studies (Chapter 5) indicated that section Macrostigmatea s.l.
diverged at an earlier stage, around 11 mya (middle Miocene), whereas the Angustimarginata
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clade diverged at a later point, at 7 mya (Late Miocene). This could support the hypothesis that
complex scales have a more ancient origin, but this possibility needs to be investigated further.
3.5 DESCRIPTION OF NEW SPECIES
Combretum nwambiyana O.Maurin, M.Jordaan & A.E.van Wyk.
a. Molecular data confirm a close relationship between C. mkuzense and C. zeyheri with C.
nwambiyana sister to this pair.
b. Combretum nwambiyana is distributed locally in northeastern South Africa in Limpopo
province, whereas C. mkuzense is restricted to the Maputaland centre of endemism in
northeastern KwaZulu-Natal and southern Mozambique. There is no record of C. mkuzense
outside the Maputaland centre with the exception of the one collected in the Nwawbiya sandveld
(KNP), which is here described as a separate species. Distance between the two sites is more or
less 500 km.
TYPE – Bryden 154 (Figure 3.11), 2231CB. Kruger National Park, Nwambiya Sandveld, on the
border with Mozambique, Vlakteplaas section, Nxanatseni Region, Limpopo, South Africa
(PRE)
Scrambling, spreading multi-stem shrub to small tree up to 4 m high, also scrambling on
surrounding vegetation and on the ground (Figure 3.12–3.13), occurring in dense woodland but
generally found in more opene vegetation, in deep Kalahari sands, associated with a rich
diversity of trees and shrubs in the Nwambiya sandveld. Vegetation deciduous or semideciduous, bark ± smooth, flaking in some parts on large specimens, yellowish-light brown to
greyish (Figure 3.14). Young branches light greyish brown, sometimes darker, finely tomentose
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on young branches, with sparse whitish to translucid indumentum. Second year branches
brownish with first bark showing some longitudinal peeling. Leaves opposite, sometimes
whorled in 3s on vigorous shoots; lamina elliptic to broadly elliptic, (15)20 – 55(85) mm long,
(10)15 – 25(30) mm wide, base tapering to round and in some case slightly cuneate, sometime
with tiny lobes, apex acute, sometimes apiculate, sparsely hairy on both sides when young,
becoming almost glabrous except for hair tufts along the midrib on the abaxial side; midrib
slightly sunken above, especially near the petiole where hairs remain more abundant, abaxial
venation is strongly raised; lateral veins opposite to subopposite, 5 – 8 pairs; petiole (2)3 – 4(5)
mm long, covered with whitish hair and rarely becoming almost glabrous. Inflorescences
axillary, simple or ramified (x3) spikes, (15)17 – 22(25) mm long, peduncle and rachis brownish
covered with scales and glutinous, almost glabrous, bracts no longer than 1 – 2 mm, ±linear,
caducous. Flowers regularly distributed along the spikes from 0.5 – 0.8 mm of the base. Flowers
tetramerous, greyish-yellowish. Lower receptacle ca. 2 – 3 mm long, 2 mm wide, glabrous and
glutinous. Upper receptacle ± 2 mm long, 3 mm wide, cupuliform to infundibuliform, scales
glutinous, visible, rarely with hairs. Sepals ca. 1 mm long ± deltate. Petals yellowish, ± 2.0 – 2.5
mm long, 1 – 2 mm wide, obovate-spathulate. Stamens 8, ± uniseriate, inserted shortly above the
margin of the disk; filaments ca. 2-4 mm long; anthers ca. 0.7 – 0.9 mm long. Style ca. 5 mm
long. Fruit 4-winged, green when young turning yellowish to pale brown, ca. 20 – 25 mm long,
25 – 38 mm wide, broadly elliptic, circular to subcircular in outline, apical peg absent, wings
15-19 mm wide, the “pod part” of the fruit is covered with a lustrous shine due to glutinous
secretion, stipe 8 – 10 mm long (Figure 3.15). Cotyledons 2, epigeal (Figure 3.16). Scales
present on inflorescences and flowers, conspicuous on both surfaces of leaves, more abundantly
distributed on the abaxial surface, often concealed by glutinous secretions, ca. 75 – 80(100) µm
diam., ± circular with a scalloped margin, constituted by 16+ cells delimited by 8 primary
radials walls and secondary radial and tangential walls. Flowering has been recorded in October
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and almost certainly lasts until the end of November; ripe fruits were observed at the end of
January. These times might vary depending on spring rainfall, which generally marks the
beginning of the vegetative growth.
3.5.1 Diagnostic characters
Combretum nwambiyana is morphologically closely related to C. zeyheri and C. mkuzenze. The
first collections of C. nwambiyana were often identified as C. zeyheri. However with the
description of C. mkuzense in 1989, plant material of Combretum nwambiyana was re-identified
as C. mkuzense. Molecular data suggest the two species to be closely related but distinct.
Combretum nwambiyana differ from C. zeyheri in possessing smaller fruits, a multi-stem habit
and long trailing and vigorous branches. The distinction between C. nwambiyana and C.
mkuzense is less obvious. Observations suggest that leaves are slightly larger in C. mkuzense and
cotyledons tends to be obovate in C. nwambiyana whereas they are narrower in C. mkuzense.
3.5.2 Distribution and habitat
The first collection of C. nwambiyana dates back to 1954. Schmidt et al. (2002) reported it
under C. mkuzense, and recently (2006) it was collected in KNP. An accurate account of its
distribution remains to be assessed; collections known so far are restricted to the KNP in the
Nwambiya Sandveld that borders Mozambique. The Sandveld extends into Mozambique in the
Parque Nacional do Limpopo, and thus the possibility exists that the species also occurs in
Mozambique, near the border with the KNP. Wind-blown deposits with deeper fine red sands
characterise the Nwambiya Sandveld. The vegetation type is a dense low forest with a high
diversity of trees and shrubs compared to surrounding areas, which includes mainly Xeroderris
stuhlmanii — Combretum apiculatum and Terminalia sericea — Pogonarthria squarrosa tree
savanna vegetation type as characterised by Van Rooyen (1978). Combretum nwambiyana is
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associated with other Combretaceae for example: Combretum celastroides Welw. ex Lawson
subsp orientale Exell, C. imberbe Wawra, C. collinum Fresen., C. apiculatum Sond subsp.
apiculatum, C. mossambicense (Klotzsch) Engl., C. padoides Engl. & Diels, C. zeyheri Sond.,
Pteleopsis myrtifolia (C. Lawson) Engl. & Diels, Terminalia prunioides C. Lawson and T.
sericea Burch. ex DC. Other species also associated with C. nwambiyana are: Baphia
massaiensis Taub., Croton steenkampianus Gerstner, Erythroxylum emarginatum Thonn.,
Heinsia crinita (Afzel.) G.Taylor, Hugonia orientalis Engl., Hyperacanthus amoenus (Sims)
Bridson, Monodora junodii Engl. & Diels, Salvadora australis Schweick., S. persica L.,
Strychnos spinosa Lam., Thilachium africanum Lour., Tinnea rhodesiana S.Moore, Uvaria
caffra E.Mey. ex Harv. & Sond., Vitex ferruginea Boj. ex Schauer subsp. amboniensis (Gürke)
Verdc., Xeroderris stuhlmannii (Taubert) Mendonca & E.P.de Sousa, and Zanthoxylum
leprieurii Guill. & Perr. The climate is characterised by summer rainfall from December to
February, with dry winters (annual mean = 545 mm), generally frost free and a mean
temperature varying between 4°C in June and 28°C in December.
3.5.3 Conservation status
Combretum nwambiyana does not face any particular threat since it occurs in a protected area.
Fire and browsers are the main threats to the rich vegetation of the sandveld, which has to some
extent adapted to these conditions.
3.5.4 Further collection
KNP, Vlakteplaas section, Nwambiya Sandveld, 2231CB, 22°41’09.9”S, 31°23’ 41.6”E, 27
April 1954 ; Van der Schillft 3694 (PRE, KNP); 2231CB, 22°41’09.9”S, 31°23’ 41.6”E, 20 Oct.
1958, Brynard & Pienaar 4259 (PRE, KNP, Figure 3.17); 2231CB, 22°41’09.9”S, 31°23’
135
nwambiyana
41.6”E, 23 Oct. 1958, Brynard & Pienaar 4265 (PRE, KNP); 2231CB, 22°41’09.9”S, 31°23’
41.6”E, 28 Jan.2006, Bryden 154 (PRE, KNP, JRAU).
3.6 KEY TO SPECIES OF COMBRETUM SECTION ANGUSTIMARGINATA AND MACROSTIGMATEA S.L.
Molecular data were not available for Combretum gilletianum and C. schumannii. Inclusion of
these two species within section Macrostigmatea s.l. is provisional pending confirmation of
their taxonomic position.
1a First leaves in spring on the adaxial side partly or completely cream coloured turning bright
red in autumn. Fruit generally smaller than 2 cm in diameter:
2a Leaves glabrous beneath when mature (except for scales), often with hair-tuft domatia:
3a Flowers in elongate, laxly flowered spikes (25)35–60(85) mm long; plants occurring both in
forest and savanna regions:
4a Leaf lower surface with secondary veins raised but intersecondary veins ± flat; scales
composed of 8(- 10) radial cells; trees; nearly always occurring in or near forests; widespread
C. kraussii
4b Leaf lower surface with both secondary and intersecondary veins conspicuously raised (often
yellowish in dried specimens); scales composed of (10-) 16 radials cells; trees, shrubs or
climbers(?); occurring in forests and savannas; recorded from the southeastern Mpumalanga,
Swaziland and northern Natal widespread
C. woodii
3b Flowers in congested subcapitate spikes, (10)15-20(35) mm long; plants associated with
savanna or if in forest regions then confined to gallery bush:
4a Leaves elliptic, obovate-elliptic or obovate; flowers with the upper receptacle obviously
divided into a lower ± campanulate part containing the disk and an expanded ± cupuliform
136
nwambiyana
upper part; usually shrubs; recorded from savanna and rocky terrain in southern Limpopo
widespread widespread
C. nelsonii
4b Leaves narrowly elliptic or lanceolate; flowers with the upper receptacle ± cupuliform, not
obviously divided into a lower and upper part; usually trees; recorded from the banks of
watercourses in the Eastern Cape, and southwestern KwaZulu Natal
C. caffrum
2b Leaves distinctly abaxially hairy when mature, at least on the midrib and secondary veins.
5a Flowers with the upper receptacle visibly divided into a lower ± campanulate part containing
the disk and an expanded ± cupuliform upper part; reticulation of abaxial surface of the lamina
conspicuously raised; recorded only from northern Limpopo (Venda)
C. vendae
5b Flowers with the upper receptacle ± campanulate, not obviously divided into two parts;
reticulation of abaxial surface of lamina flat or slightly raised; widespread along watercourses in
southern Africa
C. erythrophyllum
1b Juvenile leaves not showing any cream colour, and generally yellowish in autumn; fruit
generally larger than 2 cm in diameter; petals obovate to spathulate generally larger than 1 mm
and as large as wide:
6a Inflorescences of short subcapitate to glomeruliform spikes, fruits generally larger than 2.5 x
2.5 cm :
7a Disk glabrous with only a short free margin, anthers 0.6 x 0.5 mm; fruits 2.5 to 3.5 cm long:
8a Leaves usually not longer than 40 mm long, sparsely hairy to glabrous excepts for scales and
tufts in the main axils; spike up to 30 mm long and lepidote, occasionally glutinous; multistemmed spreading shrubs, with rather smooth bark, occurring in mixed woodland or savanna,
often in semi-arid regions and on Kalahari sands in Naminia and Botswana widespread
C. engleri
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nwambiyana
8b Leaves usually up to 10 cm long, glabrous except for scales, inflorescences short spikes up to
7 mm, glutinous, trees up to 18 m with flaky bark, occurring in coastal forest to savanna
woodland
C. schumannii
7b Disk with a pilose free margin for c. 1 mm; anthers 1.0-1.2 x 0.8-1.0 mm; fruit up to 5 cm in
diameter, liana:
9a Leaves opposite or in whorls of 3 to 4; fruit not decurrent at the base, stipe up to 2.5(3) cm,
liana up to 15 m with bark grey to silvery, rough and flaky; in grasslands, savanna woodlands,
C. kirkii
river banks, rocky hillsides in both clay and sand at low to medium elevation
9b Leaves opposite, fruit decurrent at the base, stipe up to 1.2(2.0) mm, shrub to small tree up to
4 m high sometimes scandent; occurring in savanna woodland
C. gillettianum
6b Inflorescences of elongate spikes, usually between 25 and 50 mm:
10a Inflorescence of around 2.5 cm long, multistem shrub, with long slender branches occurring
on sand:
11a Cotyledons large and obovate, occurring on deep Kalahari sand in dense woody vegetation
C. nwambiyana
11b Cotyledons large but narrow, occurring on coastal sand in dense woody vegetation
C. mkuzense
10b Inflorescences of around 5 cm; fruits up to 8 x 8 cm, cotyledons fused forming a peltate
organ, shrub to small tree up to 10 m, occurring in bushveld, open woodland on rocky hillsides
and sometimes along rivers
C. zeyheri
.
138
nwambiyana
FIGURE 3.1 Distribution maps for members of Combretum sections Angustimarginata, Spathulipetala and
Macrostigmatea s.s.: (a) Combretum caffrum, (b) Combretum engleri, (c) Combretum erythrophyllum, (d)
Combretum gillettianum (e) Combretum kirkii, (f) Combretum kraussii, (g) Combretum mkuzense, (h) Combretum
nelsonii, (i) Combretum nwambiyana, (j) Combretum schumanni, (k) Combretum vendae, (l) Combretum woodii,
(m) Combretum zeyheri. Thick black line demarcates potential geographical range.
139
nwambiyana
140
nwambiyana
4
13
70/0.98
4
35
99/1.0
2
Combretum nelsonii
Combretum caffrum
Angustimarginata
13
Combretum woodii
13
100/1.0
4
Combretum kraussii
44
99/1.0
1
Combretum vendae
3
15
52/0.91
6
60/
0.98
Combretum mkuzense
11
15
99/1.0
3
4
61
Combretum zeyheri
Spathulipetala
Combretum nwambiyana
Macrostigmatea
4
86
15
47
100/1.0
14
27
Combretum engleri
Combretum kirkii
Combretum edwardsii
33
Ciliatipetala
23
49
42
Combretum molle
Combretum celastroides
Combretum imberbe
FIGURE 3.2 One of the six most parsimonious trees (364 steps, CI = 0.83, RI = 0.85) of section Ciliatipetala from
the combined plastid and nuclear ITS data. Branch lengths (DELTRAN optimisation) are indicated above the
branches, and bootstrap percentages above 50%/Bayesian posterior probabilities below. Current sectional (Stace,
1980a) classification is indicated on the right.
141
Angustimarginatta
6. Young branches
4. Bark
3. Habit
2. Climate
1. Habitat
``
5. Branchlets
nwambiyana
Combretum nelsonii
Combretum caffrum
Combretum woodii
Combretum kraussii
Combretum vendae
Macrostigmatea and Spathulipetala
Combretum mkuzense
Combretum zeyheri
Combretum engleri
Combretum kirkii
Combretum edwardsii
Combretum molle
Combretum imberbe
=0
=1
=2
=3
=0/1
=0/2
=1/2
?
=Unknown
FIGURE 3.3 Habit, habitat, climate, bark and stem morphological characters plotted on the most parsimonious tree
(Figure 3.2). Legends are described under the figure.
142
Angustimarginatta
14. Reticulation
13.Primcipal laterals veins
12.Combretaceous hairs
11.Leaf autumnal color
10. Leaf spring color
9. Leaf margin (2)
8. Leaf margin (1)
``
7. Leaf apex
nwambiyana
Combretum nelsonii
Combretum caffrum
Combretum woodii
Combretum kraussii
Combretum vendae
Combretum mkuzense
Combretum zeyheri
Combretum engleri
Combretum kirkii
Combretum edwardsii
Combretum molle
Combretum imberbe
=0
=1
=2
=3
=0/1
=0/2
=1/2
?
=Unknown
FIGURE 3.4 Leaf anatomical characters plotted on one of the most parsimonious trees (Figure 3.2). Legends are
described under the figure.
143
Angustimarginatta
21: Hairtuft domatia
20. Leaf scales
glistening
19. Leaf scales density
18. Leaf scales, type
of walls
17. Leaf scales shape
(margin)
16.Number of cells
per leaf scale
15. Leaf scales size
nwambiyana
Combretum nelsonii
Combretum caffrum
?
Combretum woodii
Combretum kraussii
Combretum vendae
Combretum mkuzense
Combretum zeyheri
Combretum engleri
Combretum kirkii
Combretum edwardsii
Combretum molle
Combretum imberbe
=0
=1
=2
=3
=0/1
=0/2
=1/2
?
=Unknown
FIGURE 3.5 Leaf scales characters plotted on one of the most parsimonious trees (Figure 3.2). Legends are described
under the figure.
144
26. Flower, disck margin (2)
24. Flower,lower receptacle
25. Flower, disck margin (1)
Angustimarginatta
23. Flower, calyx lobes
22. Inflorescence shape
nwambiyana
?
?
?
?
Combretum nelsonii
Combretum caffrum
Combretum woodii
Combretum kraussii
Combretum vendae
Combretum mkuzense
Combretum zeyheri
?
Combretum engleri
Combretum kirkii
?
Combretum edwardsii
Combretum molle
Combretum imberbe
=0
=1
=2
=3
=0/1
=0/2
=1/2
?
=Unknown
FIGURE 3.6 Inflorescence and flower characters plotted on one of the most parsimonious trees (Figure 3.2). Legends
are described under the figure.
145
Angustimarginatta
32. Cotyledons (2)
31. Cotyledons (1)
30. fruit glutinous
29. Fruit hairness
28. Fruit size
27. Fruit color
nwambiyana
Combretum nelsonii
?
Combretum caffrum
Combretum woodii
Combretum kraussii
Combretum vendae
Combretum mkuzense
Combretum zeyheri
?
Combretum engleri
?
Combretum kirkii
Combretum edwardsii
Combretum molle
?
Combretum imberbe
=0
=1
=2
=3
=0/1
=0/2
=1/2
?
=Unknown
FIGURE 3.7 Fruits and germination characters plotted on one of the most parsimonious trees (Figure 3.2). Legends
are described under the figure.
146
nwambiyana
FIGURE 3.8 Combretum kraussii: scale from leaf.
FIGURE 3.9 Combretum mkuzense: scale from leaf.
FIGURE 3.10 Scale details of Combretum nwambiyana.
147
nwambiyana
FIGURE 3.11 Herbarium specimen of Combretum nwambiyana (Bryden 154), with fruit details.
148
nwambiyana
FIGURE 3.12 Combretum nwambiyana: habitat and slender habit.
.
FIGURE 3.13 Combretum nwambiyana: a multi-stem low branching tree with young branches showing a slender
habit.
149
nwambiyana
FIGURE 3.14 Combretum nwambiyana: yellowish
pale bark largely covered with lichens.
FIGURE 3.15 Combretum nwambiyana: branchlet
with large sized fruits.
FIGURE 3.16 Combretum nwambiyana: germinating seed.
150
nwambiyana
FIGURE 3.17 Herbarium specimen of Combretum nwambiyana (Brynard & Pienaar 4259), with inflorescence and
flower details.
151
152
Chapter 4: Notes on Combretum section Ciliatipetala and C. stylesii
CHAPTER 4: NOTES ON PHYLOGENETICS, MORPHOLOGY AND BIOGEOGRAPHY OF COMBRETUM
SECTION CILIATIPETALA (COMBRETACEAE), WITH THE DESCRIPTION OF A NEW SPECIES FROM
SOUTH AFRICA
4.1 INTRODUCTION
Combretum section Ciliatipetala is restricted to Africa and Arabia (Stace, 1980a). Currently the
section comprises ten species, namely Combretum acutifolium Exell, C. albopunctatum Suess.,
C. apiculatum, C. edwardsii Exell, C. moggii Exell, C.molle, C. nigricans Lepr. ex Guill & Perr.,
C. petrophilum Retief, C. psidioides, and C. viscosum Exell. A taxonomic reassessment of the
section (Maurin et al., 2010; Chapter 2) has revealed at least four undescribed species in southern
Africa: A from Sekhulhuneland, B from the Tugela Valley, C from Maputaland and D from
Maputaland.
Macromorphology as well as molecular data support the taxonomic status and sectional
position of the new species. Three of the new species are known from limited material only and
in this paper they are referred to as A (Winter 7225), C (Boon 3174) and D (Ward 2644). The
fourth new species, B, hitherto only recorded from the Tugela Valley, KwaZulu-Natal, was
extensively studied in the field by David Styles and is described in a paper submitted to South
African Journal of Botany as C. stylesii O.Maurin, M.Jordaan & A.E.van Wyk.
The most widespread member of C. section Ciliatipetala, C. molle R.Br. ex G.Don,
extends from southern, eastern and western Africa to the southern parts of the Arabian Peninsula.
Some species of this section are morphologically heterogeneous, and C. molle is one of these, an
example of a complex “aggregate” species (Stace, 1969). This variation is sometimes formally
153
recognised at the infraspecific level (e.g. Combretum apiculatum with two subspecies and
Combretum psidioides with four).
Most representatives of section Ciliatipetala are shrubs to small trees that occur in
savanna or woodland. Species A is a shrub or small tree confined to Sekhukhuneland (South
Africa). Combretum edwardsii and three of the new species are, however, notable exceptions in
being climbers. Combretum edwardsii is restricted to high elevation coastal and temperate
mistbelt forest, and C and D are associated with tropical sand forest in Maputaland (northeastern
KwaZulu-Natal and southern Mozambique), whereas C. stylesii is restricted to the subtropical
Tugela River Valley, in KwaZulu-Natal, where conditions are humid, extremely hot and
seasonally dry.
Members of section Ciliatipetala are floriferous and characterised by flowers with petals
that are small to absent. Petals are usually apically ciliate or pilose, hence the name of the
section. Combretum psidioides subsp. glabrum Exell is the only member of the section without
hairs at the apex of the petals (Stace, 1969; Exell, 1970, 1978; Wickens, 1973). According to
Exell (1970, 1978) small petals are vestigial structures that have lost their role of insect
attraction, a function that has been taken over by the masses of flowers, conspicuous stamens and
strong scent. The margin of the floral disc is short, free and pilose. The fruits are small, generally
not larger than 20 x 20 mm, and 4-winged. In seedlings the paired cotyledons are produced at or
below soil level, except in C. albopunctatum and C stylesii, in which they are produced well
above soil level. Seedlings of A, C and D have not been seen. The location of the apical and two
cotyledonary axillary buds under the soil in these seedlings is hypothesised to provide protection
against fire, which is a frequent natural occurrence in the habitats of most these taxa.
Leaf scales in section Ciliatipetala vary in size from 40–120 µm in diameter, with 7–12
radial walls, often with additional tangential walls (Exell, 1978). Scale morphology is, however,
154
not uniform in the section but varies from a simple 8-celled construction (e.g. C. apiculatum) to a
more elaborate structure with large numbers of cells subdivided by tangential and concentric
walls (e.g. C. molle, C. moggii), with all possible intermediate forms (Stace, 1969). In
Combretum leaf scale structure has proven to be taxonomically useful at the sectional and
occasionally species level (Stace, 1969, 1980a; Verhoeven & van der Schijff, 1973; Van Wyk
1984). Stace (1969) suggested that complex scales may have derived from an 8-celled stage. In
section Angustimarginata, Van Wyk (1984) suggested that the 8-celled scales found in C.
kraussii represented the ancestral state from which the 10–16-celled scales of the other species in
the section could have been derived. The exact function of the scales also remains speculative,
but they may protect young growth. On young leaves, for example, the scales are intact, alive and
densely arranged, potentially providing protection against ultra-violet (UV) radiation. However,
as the leaves grow older, scale cells often burst and their contents form a glutinous layer on the
lamina surface, which probably offers further protection against UV radiation, but also against
bacterial and fungal attack. It would be informative to identify the chemical compounds released
by the cells of the scales as this may assist in establishing their role.
This chapter provides a phylogenetic evaluation of the taxonomic status of section
Ciliatipetala, notably the interspecific relationships suggested by Stace (1969). The range of each
species is related to the African phytochoria of White (1983). A new species from KwaZuluNatal, South Africa, is described; its position within section Ciliatipetala is evaluated, and an
identification key for this section is presented.
155
4.2.1 Plant material
Material for most species currently recognised within the section was available for DNA
extraction, with the exception of C. acutifolium, C. nigricans, C.viscosum and new species D.
Several subspecies of C. apiculatum and forms of C. molle were included in the study. Material
was collected during fieldwork in southern Africa or obtained from the Millennium Seed Bank
(Royal Botanic Gardens, Kew, United Kingdom). Combretum micranthum and Meiotemon
tetrandrus were selected as outgoup, and three taxa representing sections Angustimarginata,
Glabripetala and Spathilipetala were also included. In total 17 taxa were analysed, including
three of the four undescribed species. Voucher information is presented in Appendix 4.1.
4.2.2 Scale morphology
Leaf and fruit material (from herbarium specimens) was used to obtain scales for light
microscopic study. Intact leaves or fruit were partly rehydrated in boiling water and stained for
one hour in a 1% aqueous solution of toluidine blue. After washing with water to remove excess
stain, the material was dehydrated in an ethanol series, transferred through two changes of
absolute ethanol:xilene (50:50) and finally two changes of xilene. A drop of the mountant
entellan (Product 7961, E. Merck, Darmastadt), diluted with xylene, was deposited onto the
material. The surface of the leaf/fruit below the drop of entellan was then gently scraped with a
scalpel to loosen the scales. This is best done under a dissecting microscope, which allows for the
mostly darkly stained scales to be viewed. A drop of entellan with suspended scales was removed
from the plant surface with a Pasteur pipette and mounted on a microscope slide with a cover
slip. Slides were observed under a Zeiss Axioplan 2 compound microscope, and images were
156
captured on an Axiovision 4.7 light microscope. The Z-option of the image capture software was
used to produce a sequence of digital pictures of the same scale at different focusing levels.
These images were then stacked using the Combine ZM free software
(http://www.hadleyweb.pwp.blueyonder.co.uk/CZM/Manual/Install.htm).
4.2.3 Phylogenetic analyses
analyse the combined sequence data of the taxa included in this analysis. Tree searches were
conducted using 1,000 replicates of random taxon addition, retaining 10 trees at each step, with
tree-bisection-reconnection (TBR) branch swapping and MulTrees in effect (saving multiple
equally parsimonious trees). The trees collected in the 1000 replicates were then used as starting
trees for another search without a tree limit. Support for clades in all analyses was estimated
using bootstrap analysis (Felsenstein, 1985) with 1000 replicates, simple sequence addition and
TBR swapping with MulTrees in effect but saving a maximum of 10 trees per replicate.
Bootstrap percentages (BP) were classified as high (85–100), moderate (75–84) or low (50–74).
All data sets were analysed separately, and the individual bootstrap consensus trees examined by
eye to identify topological conflicts, i.e. moderate to high support for different placement of taxa.
'Congruence tests' such as the incongruence length test (ILD) can be unreliable (Reeves et al.,
2001; Yoder et al., 2001) and therefore were not used in this study. Delayed transformation
character optimisation (DELTRAN) was used to calculate branch lengths, due to reported errors
was performed using MRBAYES v. 3.1.2 only on the combined data set. For each matrix, ITS,
157
rbcL, psaA-ycf3, trnH-psbA, the most appropriate model was selected using MODELTEST v.
3.06 (Posada & Crandall, 1998). For ITS, rbcL and psaA-ycf3, GTR+I+G was selected, and for
trnH-psbA, TIM + G, in which the two resulting models share the same number of substitutions =
6 and rates = gamma, base frequency = empirical and clock = unconstrained; 2,000,000
generations were used with trees sampled every 200. The resulting trees were plotted against
their likelihoods to determine the point where likelihoods converged on a maximum value, and
all the trees before the convergence were discarded as ‘burn-in’ (1000 trees). All remaining trees
were imported into PAUP 4.0b10, and a majority-rule consensus tree was produced showing
frequencies (i.e. posterior probabilities or PP) of all observed bi-partitions. PPs are shown on the
MP trees because the topologies are identical. The following scale was used to evaluate PPs:
below 0.95, weakly supported; 0.95–1.0, well supported.
4.2.4 Evaluation of morphological and biogeographical data
Morphological data were recorded from field observations, herbarium specimens and the
literature (Carr,1988; Exell, 1970, 1978). Scale structures were observed in material collected in
the present study as well as herbarium specimens by other collectors and were combined with
data from Stace (1969). Species distributions are based on new collections made for this study
and existing information from Klopper et al. (2006), www.tropicos.org, Missouri Botanical
Garden (2009), and the International Plant Name Index (2008). Distribution maps and ecological
data (climate and habitat) for all species are presented in the results. The map template was
obtained from Hester Steyn (SANBI) and is based on Van Wyk & Smith (2001; map 3).
Morphological characters used are presented in Appendix 4.2 and characters states in Appendix
4.3. Characters states in extant taxa were investigated and plotted by hand on one of the most
parsimonious trees.
158
4.2.5 Species description and identification key
A description for a new species from KwaZulu-Natal is presented. To formally describe this
species, more flowering material will be needed. An identification key for all species of section
Cilatipetala, including the species not present in the molecular analyses is provided.
4.3 PHYLOGENETICS, CLASSIFICATION AND BIOGEOGRAPHY OF SECTION CILIATIPETALA
4.3.1 Distribution, habitat and habit
Distribution maps of all species are presented in Figure 4.1. Most taxa occur in savanna
(woodland) and relatively arid vegetation types with the exceptions of C. edwardsii, which is a
climber of mist-belts and coastal forests, and C. molle, an ecological and chorological
transgressor with a widespread distribution in Africa,associated with different vegetation types,
depending on the area. Here, for each species, I review first the distribution and habitat, followed
by the habit. Species are related to the African phytochoria of White (1983), as modified by
Huxley et al. (1998).
Combretum acutifolium Exell (provisional) — Present in Angola, Democatic Republic of Congo
(DRC, Katanga), Tanzania and Zambia (Figure 4.1a). The species occurs in the Zambesian
regional centre of endemism associated to Brachystegia – Julbenardia and Kalahari woodland
between 1 200 and 1 500 a.s.l.
Combretum albopunctatum Suesseng. — Present in Botswana, Namibia (Caprivi Strip),
Zimbabwe and Zambia (Figure 4.1b). The species occurs in the Zambesian regional centre of
endemism and the Kalahari-Highveld regional transition zone. It is found in dry savanna,
159
woodland (Baikiaea woodland, Colophospermum mopane savanna and woodland) and riverine
thicket, on Kalahari sand and alluvial soils, in well watered to semi arid and hot environments
(Exell, 1970, 1978; Carr, 1988; Coates-Palgrave, 2002). It generally occurs at elevations around
1 000 m a.s.l.
Combretum apiculatum Sond. — Combretum apiculatum subsp. apiculatum occurs in Angola,
Kenya, Malawi, Mozambique, Namibia, South Africa, Swaziland, Tanzania, Zambia (Figure
4.1c). The species has been reported from the Zambesian regional centre of endemism, in the
Kalahari-Highveld regional transition zone, Afromontane archipelago-like centre of endemism,
and the Maputaland-Pondoland regional mosaic. It occurs in various types of savanna and dry
deciduous woodland under moderate to semi arid conditions up to 1 800 m a.s.l. Combretum
apiculatum subsp. leutweinii (Schinz) Exell is known from Namibia and Botswana (Figure 4.1d).
The species is present in the Kalahari-Highveld regional transition zone and in some scattered
locations, where is it mainly associated with mopane savanna and woodland. This subspecies
occurs at lower elevations than subsp. apiculatum.
Combretum edwardsii Exell — Present in South Africa, provinces of Mpumalanga and KwaZuluNatal (Figure 4.1e), as well as in Swaziland. It has a disjunct distribution with populations in the
KwaZulu-Natal midlands and South Coast, and on the Mpumalanga and Swaziland part of the
Great Escarpment, marginally extending into Limpopo Province (Schmidt et al., 2002). It occurs
in the Afromontane archipelago-like centre of endemism and in the Maputaland-Pondoland
regional mosaic where it is found in evergreen forest, along forest margins and in densely
vegetated ravines in humid and misty environments, generally at elevations between 1100 and
1500 m a.s.l.
160
Combretum moggii Exell — Present in South Africa in the provinces of Gauteng, Limpopo and
Mpumalanga, as well as in Swaziland (Figure 4.1f). It occurs in the Zambezian regional centres
of endemism and the Kalahari Highveld regional transition zone but is scattered in often widely
separated populations among rocks, on mountain tops and in canyons, often in misty
environments and at elevations between 1 200 and 1 600 m a.s.l.
Combretum molle R.Br. ex G.Don — A species with an extensive distribution in western, eastern
and southern Africa, and the southern Arabian Peninsula (Figure 4.1g), but absent from the
Congo Basin (Equatorial Guinea, Gabon, Congo Kinshasa and DRC). It is present in the
Sudanian, Somali-Masai and Zambesian regional centres of endemism, in the Afromontane
archipelago-like centre of endemism, in the Guineo-Congolian/Sudanian and SwahilanMaputaland regional transition zones and in the Maputaland-Pondoland regional mosaic. Due to
its wide distribution, this species is found in many different environments; from humid areas with
high rainfall to semi-arid conditions, mainly in savanna and woodland, up to 1 500 m a.s.l. This
is a polymorhic species and a detailed study of its distribution and habitat would be necessary to
identify and demarcate distinct infraspecific forms.
Combretum nigricans Lepr. ex Guill. & Perr. (provisional) — The species has two varieties, the
type and C. nigricans var. eliottii. Both varieties occur north of the equator in western and central
Africa (Figure 4.1h). The species occurs in the Sudanian regional centres of endemism in
savanna vegetation, Combretum – Terminalia woodland on recent lava flows, fringing forest,
“cuirass”, concretions and skeletal soils up to 1 900 m a.s.l.
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Combretum petrophilum Retief — This species is endemic to the Limpopo and Mpumalanga
Provinces of South Africa (Figure 4.1i). It occurs in the Zambesian regional centres of endemism
in mountainous and hilly areas. The species is sometimes associated with Terminalia
phanerophlebia Engl. & Diels, Portulacaria afra and various arborescent succulent Euphorbia.
Combretum psidioides Welw. — Combretum psidioides subsp. dinteri (Schinz) Exell is present in
Angola, Mozambique, Namibia, Zambia, Zimbabwe and in some parts of the DRC (Figure 1j). It
is associated with the Zambesian regional centre of endemism and the Kalahari-Highveld
regional transition zone. Combretum psidioides subsp. psidioides has a similar distribution, but it
also occurs in Botswana. Combretum psidioides subsp. glabrum has a scattered distribution in
Zimbabwe. Combretum psidioides occurs in savanna and woodlands, under semi arid conditions,
in general on Kalahari sands between 1 000 and 1 500 m a.s.l.
Combretum stylesii O.Maurin, M.Jordaan & A.E.van Wyk — Present in South Africa in the
province of KwaZulu-Natal (Figure 4.1k), known only from the Tugela Valley, occurring in the
Maputaland-Pondoland regional mosaic; it is found in hot, semi-arid riverine vegetation
generally associated with savannas dominated by Spirostachys africana.
Combretum viscosum Exell (provisional) — Present in Angola (Figure 4.1l), mainly in the
Zambesian regional centres of endemism and possibly marginally in the Kalahari-Highveld
regional transition zone. It occurs in poor sandy soils, in short thicket-overgrown pastures in
rocky and gravelly situations at 60 m a.s.l.
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Combretum species A — Present in Mpumalanga, South Africa, where it has a localised
distribution in the Sekhukhuneland region (Figure 4.1m). It is present in the Zambesian regional
centre of endemism.
Combretum species C— Present in KwaZulu-Natal, South Africa, bordering Swaziland and
southern Mozambique, with a localised distribution (Figure 4.1n), but often sympatric with
Combretum sp. nov. D. It is present in the Maputaland-Pondoland regional mosaic, where it is
associated with Sand Forest.
Combretum species D (provisional) — Present in KwaZulu-Natal, South Africa, bordering
Swaziland and southern Mozambique, with a localised distribution (Figure 4.1o), but often
sympatric with Combretum C. It is present in the Maputaland-Pondoland regional mosaics, where
it is associated with sand forest.
Section Ciliatipatala comprises trees, shrubs, lianas and geoxylic suffrutices. Most
species not considered to be lianas show a climbing tendency in the young shoots, which possibly
represents an ancestral state (for example C. moggii). Occasional scrambling shoots are also
encountered in some species, reappearing under specific conditions (i.e. when the plants have
been strongly pruned). Most true climbers are included within the South African clade, namely
C. edwardsii, C. stylesii, species C and D. Combretum acutifolium is also a climber, but was not
included in my DNA sampling as no fresh material was available and amplification of herbarium
material failed. Most other species within C. section Cilitipetala are considered trees with the
exception of Combretum albopunctatum, which is a shrub, and C. viscosum, which is a geoxylic
suffrutex.
163
Several species (C. molle, C. apiculatum, C. albopunctatum and C. psidioides) are
adapted to frequent fire. These species survive fires because of their thick bark and ability to
resprout. Other species, for example C. viscosum and C. platypetalum Welw. ex M.A.Lawson
(subgenus Cacoucia section Conniventia), have an underground rootstock from which young
vegetative and flowering shoots appear after fire. Another adaptation to fire in Combretum, and
present in several representatives within section Ciliatipetala, is the mode of germination and
position of their cotyledons, either above, at or below soil level. In C. molle, C. apiculatum and
C. psidioides the bark is thick, and cotyledons appear at or below ground level.
4.3.2 Phylogenetic data
Maximum parsimony analysis of the combined matrix provided the following statistics. Number
of included characters = 3675; number of constant characters = 3395; number of variable sites =
280 (7.61%); number of parsimony informative sites = 116 (3.15%); number of trees (Fitch) = 1;
number of steps (tree length) = 466; CI = 0.72; and RI = 0.61. The most parsimonious tree is
presented in Figure 4.2. Section Ciliatipetala is strongly supported as monophyletic (99 BP/1.0
PP) with two main clades. The first, with 89 BP/1.0 PP, includes C. albopunctatum, C.
apiculatum subsp. apiculatum, C. apiculatum subsp. leutweinii, C. molle and C. psidioides subsp.
dinteri. The second clade (100 BP/1.0 PP) comprises C. moggii, C. petrophilum, C. stylesii, C.
edwardsii, species A and C.
4.3.3 Morphological characters
Characters were mapped by hand in the most parsimonious way onto the most parsimonious tree;
Figures 4.3 to 4.6 (Appendix 4.2 and 4.3).
164
Three of the 28 scored characters proved to be informative in delimitating the section and
the two clades (A and B; Figure 4.2), namely the bark, which can be smooth or rough, the
inflorescence shape (elongate, capitate or sub-capitate) and position of the cotyledons at
germination (epigeal or hypogeal germination).
4.3.4 Leaf scale anatomy
Observations show a wide range of scale shapes, sizes, and number of cells present, as well as the
presence or absence of additional radial and/or tangential walls. Three scale types were identified
within section Ciliatipetala, namely: (i) simple 8-celled scales in C. stylesii, C. albopunctatum,
and C. psidioides. (see type specimen, Figure 4.7); (ii) 8–16-celled and variable occurrence of
primary and secondary radial and/or tangential walls, as in C. apiculatum subsp. apiculatum, C.
apiculatum subsp. leutweinii, C. edwardsii (Figure 4.8) and C. molle; and (iii) more complex
scales, generally of 16 or more cells with both primary and secondary radial and/or tangential
walls, as seen in C. molle (Figure 4.9), C. edwardsii and C. moggi. Taxa such as Combretum
molle and C. edwardsii possess both scale types i and ii.
4.4 DISCUSSION
Section Ciliatipetala was previously viewed as taxonomically complex and considered one of the
most problematic sections within Combretum (Stace, 1969). Stace (1969) even mentioned that
each of the aggregate species (e.g. aggregates C. albopunctatum, C. apiculatum, C. moggii, C.
molle, C. nigricans, and C. psidioides) could be placed in their own sections. Adding to the
confusion is the large number of nomenclatural synonyms that exist; for example, C. molle has at
least 27 synonyms (Klopper et al., 2006). Some taxa were also initially excluded from the section
165
because they possess glabrous petals; for example C. psidioides was initially included within
section Glabripetala Engler & Diels because C. psidioides subsp. glabrum does not have hairy
petals.
Although the sampling lacks important taxa such as C. acutifolium and C. nigricans,
delimitation of the section is clear and its monophyly strongly supported (99 BP/1.0 PP). It is
separated into two well-supported clades (Figure 4.2). Clade A (89 BP/1.0 PP) includes C.
albopunctatum, C. apiculatum, C. molle and C. psidioides. Species of this clade have a wide
distribution with the most widespread species, C. molle, present in most parts of Africa. Clade B
(100 BP/1.0 PP) consists of only southern African taxa, namely C .edwardsii, C. moggii, C.
petrophilum, C. stylesii, species A and C. Most of the taxa of clade B have a restricted
distribution, sometimes occurring in highly specific habitats (e.g. C. moggii occurs in often
widely disjunct localities on mountains and rocky ridges).
It would be possible to subdivide the section into two sub-sections given the results of the
molecular analyses. Morphological characters useful to distinguish between clades A and B are:
(i) smoothness of the bark, (ii) inflorescence shape, and (iii) position of cotyledons during
germination. Taxa in clade A are characterised by mostly rough bark, hypogeal cotyledons and
elongate spikes, whereas those in clade B have smooth bark (Figure 4.3), capitate to sub-capitate
inflorescences and epigeous cotyledons (with the exception of C. albopunctatum; Figure 4.6).
However, it is premature to suggest a further splitting of Ciliatipetala until the taxa missing from
this study and a potential new species from Mozambique (Coates-Palgrave, pers. com) are
included. Assessment of the robustness of the morphological characters that could be used to
divide the section would also be essential.
Results of phylogenetic dating (see chapter 5) show that Ciliatipetala originated during
the Early Miocene (Burdigalian; 18 mya) with the crown ages of the two main clades within the
166
section: clade A 14 mya (Middle Miocene; Langhian) and clade B 9 mya (Late Miocene;
Tortonian). The geological time scale used here is from Walker & Geissman (2009). In Figure
4.2 it is also evident that clade B displays much lower levels of divergence than clade A, which
could indicate a much more recent and rapid radiation within clade B compared to clade A.
Stace (1968) viewed C. apiculatum as a “central point” within the section, but his view is
debatable, considering that C. molle has the widest distribution and greatest tolerance to
environmental conditions; therefore, it could also be considered as the most primitive member of
the section. Within section Ciliatipetala, C. molle also possesses some of the most complex
scales, although no convincing evolutionary pattern is obvious with respect to leaf scales; taxa
within each clade possess both simple and complex scales.
It is difficult to assess the ancestral states for characters within Combretaceae due to
homoplasy. It is possible that some characters have experienced reversals. Stace (1969)
mentioned that section Hypocrateropsis is often viewed as the most primitive or least derived
section as its upper hypanthium is almost flat. In section Angustimarginata, Van Wyk (1984)
considered C kraussii Hochst. as the most primitive species within the section, with the two
closely related species C. kraussii and C. woodii having elongated spikes, which tend to be
reduced to sub-capitate spikes in the remaining more derived taxa of the section. This statement
could suggest that elongated spikes are an ancestral character state. Within section Ciliatipetala
clade A is composed mainly of taxa exhibiting elongated spikes, such as C. molle, C. apiculatum
or C. psidioides, whereas in clade B, species such as C. petrophilum, C. moggii or C. stylesii have
congested spikes. The fact that species within clade A have mostly elongated spikes and a crown
dates that are earlier than in clade B would support my hypothesis that clade A within section
Ciliatipetala contains the most oldest species within the section. The most complex scales
observed within the section belong to C. molle although these seem to vary. Combretum molle
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also has the most widespread distribution within Ciliatipetala, and I thus hypothesise that C.
molle may well be the most ancestral taxon in section Ciliatipetala.
In conclusion, my results contribute considerably to a better taxonomic understanding of
section Ciliatipatela, a section hitherto considered one of the most poorly understood sections in
Combretum (Stace, 1969). Molecular and morphological analyses recover it as well defined, but
still it remains a section that needs further investigation to assess relationships between some
groups of its species. For example, molecular results suggest a close relationship between C.
albopunctatum and C. apiculatum subsp. leutweinii. These two taxa can easily be confused, the
former being differentiated from the latter only by its glistening white scales. The status of C.
apiculatum subsp. leutweinii needs to be reconsidered carefully to decide whether to elevate it to
species level or not. It would also be imperative to obtain molecular data for the aggregates
around C. nigricans mentioned by Stace (1969), as well as more representatives of each
aggregate (for example the different forms or ecotypes of C. molle and subspecies of C.
psidioides) to improve our understanding of this section and indicate possible sectional divisions.
4.5 DESCRIPTION OF NEW SPECIES
Combretum stylesii O.Maurin, M.Jordaan & A.E.van Wyk.
C. stylesii, C. edwardsii simillima sed savannicola non silvatica, foliis uniformibus non
biformibus, petalis apice pilis paucis albidis, non glabris, squamis foliorum 8-cellularibus,
cellulis omnibus radialibus sine parietibus tangentialibus, non 16-cellularibus cum parietibus
tangentialibus radialibusque ut in C. edwardsii, fructu non concpicue lepidoto, non laeviusculo,
differt.
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TYPE.― South Africa, KwaZulu-Natal, Mabhobhane near Mapumulo, on the bank of the Tugela
River, 2931AA, 29°7′30.0″S, 31° 7′30.0″, 2 Nov. 2008, Styles 2489 (NH, holotype!; K, M, PRE,
PRU, isotype!; Figure 4.10).
Robust climber (twining to the right) usually up to 14 m high, also a scrambler, using
associated woody vegetation as support to reach the canopy (Figure 4.11), occasionally a lax
scandent tree, deciduous or semi-deciduous; bark ± smooth, greyish. Young branches pale
greenish, becoming darker and densely tomentose, with whitish to translucent indumentum.
Second year branches pale brownish with first-formed bark showing slight longitudinal peeling.
Leaves opposite, drooping; petiole (2–)3–4(–5) mm long, tomentose and remaining densely hairy
lamina elliptic to broadly elliptic, sometimes elliptic to lanceolate, (20–)25–75(–90) mm x (10–)
15–30(–35) mm wide, base rounded to slightly cuneate, sometime with tiny lobes, apex acute,
sometimes apiculate or mucronate (up to 1 mm long), pale green and densely covered with
whitish or greyish indumentum on both sides when young, becoming sparsely hairy to almost
glabrous except along the midrib on both sides; first leaves in spring often partly and temporarily
yellowish pale on both sides but reddish above; midrib slightly sunken above near the petiole and
generally remaining locally hairy; principal and lateral veins usually opposite, 5–8 pairs (Figure
4.12). Inflorescences short axillary spikes (10–)12–20(–25) mm long, peduncle and rachis
yellowish to pale green, glabrous, bracts ± 1 mm, ± linear, caducous; flowers distributed along
the spikes from 0.5–0.8 mm above the base and more densely grouped towards the apex. Flowers
tetramerous, creamish, ± congested (Figure 4.13). Lower receptacle ± 2–3 mm long, 1 mm wide,
sparsely tomentose to glabrous, glutinous. Upper receptacle ± 2 mm long, 3 mm wide, obviously
divided into a lower ± tubular part containing the disc and an expanded ± cupuliform upper part,
slightly pubescent, scales sometimes visible and source of glutinous secretions. Sepals ± 1 mm
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long, ± deltate. Petals ± 2.5 mm x 1.5 mm, narrowly obovate, oblanceolate or elliptic, with a few
scattered hairs on the margin of the apex. Stamens 8, ± uniseriate, inserted shortly above the
margin of the disc; filaments ± 2–4 mm long; anthers ± 0.9 mm long. Disc free for ± 0.5 mm,
glabrous with the margin pilose and reddish. Style ± 5 mm long. Fruit (3)4-winged, green when
young, turning brownish when mature, ± 11–22 mm x 16–24 mm, broadly elliptic, circular to
subcircular in outline; apical peg ± 0.2 mm long or absent; wings 7–10 mm wide; stipe 3–7 mm
long (Figure 4.14). Scales conspicuous on lower surface of the leaf, often concealed by glutinous
secretions in young leaves, absent or rarely present above, ± 45–55 µm in diam., ± circular,
margin slightly undulate, delimited by 8 primary radials walls alone (8-celled). Cotyledons 2,
epigeal, first leaves covered with long white hairs when young (Figure 4.15). Flowering recorded
between October and December, but must have started earlier in some cases since ripe fruits were
observed from October to March.
4.5.1 Diagnostic characters
Combretum stylesii is similar to C. edwardsii, from which it differs by possessing a single leaf
form similar both at the base of the plant and in the canopy. Petals of C. stylesii have a few
whitish hairs at the tip, whereas those of C. edwardsii are glabrous except marginal hairs. Leaf
scales of C. stylesii are 8-celled, with all the cells radially arranged and without subdividing
tangential walls. The scales of C. edwardsii are more complex with 16-cells with tangential and
radials walls. Fruits of C. edwardsii are lepidote, covered with scales, whereas those of C. stylesii
are smooth.
170
4.5.2 Distribution and habitat
The earliest known collection of C. stylesii dates from 2004. It is highly localised, moderately
abundant and at present only known along a small portion of the Tugela River Valley, KwaZuluNatal, South Africa (Figure 4.16–4.17). Extensive surveys within the valley and surrounding area
will be necessary to assess its full distribution range. Combretum stylesii normally occurs in
savanna were Acacia species are lacking, the so-called eastern valley Bushveld vegetation
(Mucina & Rutherford, 2006), where it is mainly associated with the trees Combretum woodii
Dümmer, Spirostachys africana Sond. (often dominant), Euphorbia tirucalli L., and
Vittelariopsis dispar (N.E.Br.) Aubrév., the latter an endemic to the valley. The climate is
characterised by summer rainfall (mean 750 mm per annum), infrequent frost and a mean
monthly temperature varying between 9°C in June and 29°C in December (Schulze, 1997).
4.5.3 Eponymy
The specific epithet honours David Gordon Alexander Styles [1968– ], an amateur botanist from
Durban, KwaZulu-Natal, who seemingly was the first person to collect herbarium material of the
new species. Styles has conducted extensive field work in KwaZulu-Natal and the Eastern Cape
and has made significant contributions to our knowledge of the flora of these regions.
4.5.4 Conservation status
Although localised, C. stylesii can be abundant in small areas, but it is nevertheless rare and
threatened. Much of the valley vegetation in the vicinity of the populations is still intact, and only
small numbers of homesteads are located in the area. However, their impact is visible on the
woody vegetation in surrounding areas where in some places only Euphorbia tirucalli L. remains
since it is not useful as firewood. Croton menyhartii Pax seems to expand in the area since it is
171
unpalatable or toxic to livestock. Alien vegetation is also becoming more abundant in this area.
The area is not well supplied in terms of basic services (electricity and water); it is possible to
foresee an exodus from the area to urban areas. In the last decade, roadwork by the KwaZuluNatal Department of Transport and the Mapumulo Municipality were completed; it has favored
the development of homesteads along the roads that will certainly in the near future have an
impact on the natural vegetation, with possible loss of some of the populations of C. stylesii.
4.5.5 Further collections
KwaZulu-Natal, Mapumulo, Tugela Valley, Mabhobhane, 2931AA, 29°7′30.0″S,
31° 7′30.0″E, 6 Oct. 2004, Styles 2067 (NH); 2931AA, 29°7′30.0″S, 31° 7′30.0″E, 2 Nov. 2008,
Styles 3309 (NH); 2931AA, 29°7′30.0″S, 31° 7′30.0″E, 2 Nov. 2008, Styles 2034 (NH).
4.6 KEY TO SPECIES OF COMBRETUM SECTION CILIATIPETALA
Molecular data were not available for Combretum acutifolium, C. nigricans, C. viscosum and
species D. Inclusion of these four species within section Ciliatipetala is provisional pending
confirmation of their taxonomic position. ‘Hairs’ in the key refers to combretaceous hairs.
1a Leaf apex usually apiculate and often twisted, if rounded or truncate, then plants suffrutices up
to 1 m tall:
2a Suffrutices up to 1 m tall; leaf apex rounded to truncate; Angola
C. viscosum
2b Shrubs or trees, more than 2 m tall; leaf apex not rounded or truncate; tropical and southern
Africa:
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3a Leaves sparsely to densely pubescent on both surfaces; Namibia, Botswana and tropical
Africa
C. apiculatum subsp. leutweinii
3b Leaves glabrous or only margin and midrib with hairs; widespread:
4a All leaves on plant with apices apiculate; hair-tuft domatia present in axils of veins below;
leaf-base symmetrical; reticulate venation not prominent below; widespread
C. apiculatum subsp. apiculatum
4b Some leaves with apices apiculate; hair-tuft domatia absent in axils of veins below; leaf-base
often asymmetrical, rounded to subcordate; reticulate venation very prominent below; South
Africa (Limpopo and Mpumalanga)
C. petrophilum
1b Leaf apex rounded, obtuse, acute, abruptly to long acuminate, rarely apiculate; shrubs, trees or
climbers:
5a Leaves glabrous except for few hairs on margins and midrib; margin mostly not ciliate, or if
so, then only basally; fruit glabrous; Maputaland (northeastern KwaZulu-Natal and southern
Mozambique:
6a Leaf apex abruptly acuminate, occasionally apiculate; lamina margin glabrous, often undulate
and rolled-under when dry
species C
6b Leaf apex rounded to acute; lamina margin flat, ciliate towards base, not rolled-under when
dry
species D
5b Leaves hairy; lamina margin ciliate; fruit glabrous or hairy; widespread:
7a Woody climbers or scrambling shrubs with trailing branches:
8a Hair-tuft domatia present in axils of veins below; leaf apex long-acuminate; Angola, DRC,
Zambia, Tanzania
C. acutifolium
8b Hair-tuft domatia absent in axils of veins below; apex acute to abruptly acuminate; South
Africa (Mpumalaga, KwaZulu-Natal):
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9a Leaf base rounded, lobed or subcordate; hairs on leaves dark brown or reddish brown
C. edwardsii
C. stylesii
9b Leaf base broadly cuneate to rounded, not lobed; hairs on leaves whitish
7b Multi-stemmed shrubs or single-stemmed trees:
10a Leaves glaucous above, finally puberulous below, drying blackish; tropical West Africa
C. nigricans
10b Leaves not glaucous above; hairs on both sides, not drying blackish; widespread:
11a Bark of branchlets peeling off in large, ± cylindrical or hemicylindrical pieces revealing an
exposed cinnamon-red surface
C. psidioides
11b Bark of branchlets peeling off in untidy, irregular, fibrous strips or threads:
species A
12a Fruit glabrous, sometimes glutinous; Limpopo Province
12b Fruit densely to sparsely hairy, sometimes only on body or sometimes glabrous; widespread:
13a Plants sometimes forming thickets, often with scrambling branches; scales glistening; stipe
up to 8 mm long; northern parts of Botswana and Namibia, Zambia and Zimbabwe
C. albopunctatum
13b Plants free standing, not forming thickets, without scrambling branches; scales not
glistening; stipe up to 3(5) mm long; southeastern-most parts of Botswana, Swaziland, South
Africa and tropical Africa:
14a Plants with silky silvery appearance; usually multi-stemmed shrubs growing on rocks;
lamina with reticulate venation not prominently raised below; fruit densely covered with longish
appressed hairs over whole surface
C. moggii
14b Plants not with silvery appearance; usually single-stemmed trees; lamina with reticulate
venation prominently raised below; fruit sparsely hairy with short appressed hairs mainly on the
body or glabrous, but densely covered with scales
C. molle
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FIGURE 4.1 Distribution maps for members of Combretum section Ciliatipetala: (a) Combretum acutifolium, (b)
Combretum albopunctatum, (c) Combretum apiculatum subsp. apiculatum, (d) Combretum apiculatum subsp.
leutweinii (e) Combretum edwardsii, (f) Combretum moggii, (g) Combretum molle, (h) Combretum nigricans, (i)
Combretum petrophilum, (j) Combretum psidioides (all subspecies), (k) Combretum stylesii, (l) Combretum
viscosum, (m) Combretum sp. nov. A, (n) Combretum sp. nov. C., (o) Combretum sp. nov. D. Thick black line
demarcates potential geographical range.
175
176
4
Clade A
8
97/1.0
8
14
99/1.0
10
Combretum apiculatum
8
9
Combretum molle 1
9
96/1.0
13
89/1.0
3
16
Combretum molle 2
14
Clade B
Ciliatipetala
Combretum edwardsii
2
51/1.0
29
99/1.0
1
Combretum sp A
4
-/0.99
7
5
5
-/0.62
20
100/1.0
7
7
6
Combretum moggii
2
51/0.99
Combretum stylesii
Combretum sp C
27
Combretum fragrans
Glabripetala
31
54
44
11
50
44
Combretum vendae
Combretum zeyheri
Spathulipetala
Angustimarginata
57
10 changes
FIGURE 4.2 The most parsimonious tree (466 steps, CI = 0.72, RI = 0.60) of Combretum section Ciliatipetala from
the combined plastid and nuclear ITS data. Branch lengths (DELTRAN optimisation) are indicated above the
branches, and bootstrap percentages above 50%/Bayesian PPs > 0.5 below. Arrows indicate branches that collapse
in the strict consensus tree. Current sectional classification (Stace, 1980a) is indicated on the right.
177
6. Young branches
4. Bark
3. Habit
5. Branchlets
Clade A
2. Climate
1. Habitat
?
?
Combretum molle 1
Combretum molle 2
Clade B
Combretum edwardsii
Combretum sp A
Combretum moggii
Combretum stylesii
?
Combretum sp C
Combretum fragrans
Combretum zeyheri
Combretum vendae
?
?
=0
=1
=2
=3
=0/1
=0/2
=1/2
?
=Unknown
FIGURE 4.3 Habit, habitat, climate, bark and stem morphological characters plotted on the most parsimonious tree
(Figure 4.2). Legends are described under the figure.
178
8. Leaf margin (1)
9. Leaf margin (2)
10. Leaf aurumn color
11.Combretaceous hairs
(Abaxial)
12. Principal lateral
veins (Abaxial)
13. Reticulation
(Abaxial)
Clade A
7. Leaf apex
?
?
?
?
?
?
?
Combretum molle 1
Combretum molle 2
Clade B
Combretum edwardsii
Combretum sp A
Combretum moggii
Combretum stylesii
Combretum sp C
Combretum fragrans
Combretum zeyheri
Combretum vendae
=0
=1
=2
=3
=0/1
=0/2
=1/2
?
=Unknown
FIGURE 4.4 Leaf anatomical characters plotted on the most parsimonious tree (Figure 4.2). Legends are described
under the figure.
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18. Leaf scales density
19. Leaf scales
glistening
?
?
?
?
?
?
?
?
?
20. Hairtuft domatia
17. Leaf scales, type
of walls
?
16. Leaf scales shape
(margin)
Clade A
15.Number of cells
per leaf scale
14. Leaf scales size
Combretum molle 1
Combretum molle 2
Clade B
Combretum edwardsii
Combretum sp A
Combretum moggii
Combretum stylesii
?
Combretum sp C
Combretum fragrans
Combretum zeyheri
Combretum vendae
?
=0
=1
=2
=3
=0/1
=0/2
=1/2
?
=Unknown
FIGURE 4.5 Leaf scale characters plotted on the most parsimonious tree (Figure 4.2). Legends are described under
the figure.
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28. Cotyledon, position
in seedlings
27. Fruit glutinous
secretions
?
26. Fruit hairiness
("pod part")
?
25. Fruit size (longuest
dimensions)
23. Flower, petals
hairiness at apex
?
24. Fruits; color when
mature (but not yet dry)
22. Flower; disk margin
Clade A
21. Inflorescnces shape
Combretum molle 1
Combretum molle 2
Clade B
Combretum edwardsii
Combretum sp A
?
Combretum moggii
?
Combretum stylesii
?
?
Combretum sp C
?
?
?
Combretum fragrans
?
Combretum zeyheri
Combretum vendae
?
?
?
?
?
?
?
=0
=1
=2
=3
=0/1
=0/2
=1/2
?
=Unknown
FIGURE 4.6 Inflorescence and fruit characters plotted on the most parsimonious tree (Figure 4.2). Legends are
described under the figure.
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FIGURE 4.7 Combretum stylesii: scale structure. Photograph. A.E. van Wyk.
FIGURE 4.8 Combretum edwardsii: scale from leaf.
FIGURE 4.9 Combretum molle: scale from leaf.
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FIGURE 4.10 Combretum stylesii, Herbarium specimen (Styles 2489) showing flower (Styles 3309) and fruit details
(Styles 2489).
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FIGURE 4.11 Combretum stylesii: climbing habit
showing stem strangling Euphorbia tirucalii.
Photograph. D. Styles.
FIGURE 4.12 Combretum stylesii, branch with fruits.
Photograph. D. Styles.
FIGURE 4.13 Combretum stylesii, flower details. Photograph. D. Styles.
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FIGURE 4.14 Combretum stylesii: fruit details. Photograph. D. Styles.
FIGURE 4.15 Combretum stylesii: germinating seed. Photograph. D. Styles.
FIGURE 4.16 Tugela Valley, KwaZulu-Natal; habitat of Combretum stylesii. Photograph. D. Styles.
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FIGURE 4.17 Tugela Valley, KwaZulu-Natal; habitat of Combretum stylesii. Photograph. D. Styles.
186
187
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Chapter 5: The evolutionary history and biogeography of Combretaceae
CHAPTER 5: THE EVOLUTIONARY HISTORY AND BIOGEOGRAPHY OF COMBRETACEAE
5.1 INTRODUCTION
The number of families recognised within order Myrtales has been contentious. Table 5.1
summarises the families included in Myrtales by five different studies. All authors concur in
including the following seven families in the order: Alzateaceae, Combretaceae, Crypteroniaceae,
Lythraceae, Melastomataceae, Myrtaceae, Onagraceae, Penaeaceae, and Vochysiaceae (APG III,
2009). Combretaceae R. Br. have historically been viewed as a distinct family that diverged early
in the evolution of Myrtales (Systma et al., 2004; Stace, 2007). They are a taxonomically
complex family (see sections 1.3 and 2.1) comprising 17 genera and approximately 525 species
of trees, shrubs, lianas and mangroves that occur throughout the tropics with short minor
extensions into warmer part of the temperate zones. According to Exell & Stace (1972) the
Amazon, Madagascar and Indomalaysia have been areas of particularly active speciation within
Combretaceae. The two largest genera, Combretum Loefl. and Terminalia L., occur on all
continents with the greatest genetic diversity of Combretum in Africa and that of Terminalia in
Southeast Asia. Biogeography and classification of Combretaceae with geographical ranges for
genera and subgenera are presented in Table 5.2.
The fossil record of Combretaceae is plentiful, but the chronology of Combretaceae is not
clear from these records because of uncertainties in taxonomic assignments. The oldest
Combretaceae fossil (Terminalioxylon Schönfeld) was dated to the Upper Cretaceous (MädelAngeliewa & Müller-Stoll, 1973). Friis et al. (1992) described a fossil genus, Esgueiria, based on
flowers dating from the late Cretaceous. Two species were described from Portugal, Esgueria
adenocarpa and E. miraensis (Friis et al., 1992) and one from Japan, E. futabensis (Takahashi et
al., 1999). Anogeissoxylon was reported by Ahmed et al. (2007) to have an age of 54-65 mya.
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Recent fossils of Terminalia have also been reported from the Late Oligocene/Miocene (De
Franscheschi et al., 2008). Systma et al. (2004) estimated the crown radiation of extant
Combretaceae at +/- 45 mya, which means that the putative combretaceous fossil Esgueiria (84
mya) is considerably earlier than the node defining Combretaceae. Systma et al. (2004) stated
that the flowers of Esgueria differ significantly from those of extant Combretaceae, and
placement of it in Combretaceae is not at all certain.
Reconstructing the evolutionary history of a clade relies on our ability to infer ancestral
habitats and distribution of lineages (Hardy & Linder, 2005). Combretaceae are, however, one of
the families within Myrtales that has not been adequately sampled; Systma et al. (2004) used
only four taxa, and Tan et al. (2002) included 21 taxa in their analysis. A more recent study on
Combretaceae (Maurin et al., 2010; Chapter 2) provided the most complete sampling to date.
Thus, I use phylogenetic data for Myrtales and for Combretaceae from Chapter 2; I aim to: (1)
estimate the ages of Combretaceae and clades within the family using a thorough sampling of all
available data and including the largest number of Combretaceae taxa so far, and (2) reconstruct
the paelo-biogeography of Combretaceae to evaluate the importance of vicariance and dispersal
in explaining the current distribution of Combretaceae.
5.2 MATERIAL AND METHODS
5.2.1 Sampling
The Myrtales dataset (analysis 1) based on one DNA region comprises a total of 145 taxa
(Appendix 5.1), including Alzateaceae (1), Combretaceae (100), Crypteroniaceae (1),
Heteropyxidaceae (1), Lythraceae (4), Melastomataceae (15; including Memecylaceae),
Myrtaceae (7), Oliniaceae (1), Onagraceae (6), Pennaeaceae (1), Psiloxylaceae (1),
Rhynchocalycaceae (1), Vochysiaceae (2), and Brassicaceae (4). Representatives of Malvaceae
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and Tropaeolaceae were used as outgroup taxa. The analysis was used to position Combretaceae
within Myrtales and produce a chronogram with an age estimate for diversification.
The more narrowly focused Combretaceae dataset (analysis 2) comprises the sampling
used by Maurin et al. (2010; Chapter 2), with most genera of the family represented with the
exception of Finetia, Dansiea and Macropteranthes. It comprises 14 genera, 100 taxa, two
subgenera and 15 sections of Combretum and 24 species of Terminalia (including Bucida and
Pteleopsis). Representatives from Combretum and Terminalia are mostly from eastern and
southern Africa. I could not include the third subgenus of Combretum (subgen. Apetalanthum
Exell & Stace) since I could not obtain fresh material or DNA from herbarium specimens.
Voucher information and distributions of taxa used in this study are listed in Appendix 5.1.
Strephonema taxa were used as outgroups
5.2.2 DNA extraction, amplification, sequencing & alignment
DNA was extracted from 0.3 g of silica-gel dried leaf material (Chase & Hills, 1991) or
herbarium material using the 2X CTAB method described by Doyle & Doyle (1987), with the
addition of 2% polyvinyl pyrolidone (PVP) to help reduce the effects of high polysaccharide
concentration in the samples. To avoid problems of PCR inhibition, all samples were purified
using QIAquick purification columns (QIAgen, Inc., Hilden, Germany) according to the
manufacturer’s protocol.
Amplification of rbcL was carried out in two overlapping fragments using the following
primer combinations: 1F-724R and 636F-1426R (Olmstead et al., 1992; Fay et al., 1997). The
trnH-psbA spacer was sequenced using primers 1F and 2R (Sang et al., 1997). The psaA-ycf3
spacer was amplified using the PG1f and PG2r primers (Huang & Shi, 2002). Additional
Combretum-specific internal primers were designed to overcome regions of micro-satellites
located within the psaA-ycf3 spacer: psaA-ycf3 IR 5-CTA GGA ACT TCT AAT TGA GA-3 was
191
used to sequence past a poly-T region located around 350bp from the beginning in several taxa;
psaA-ycf3 IF 5-CAT GTA TTT CGA GTC TGT TT-3 was used to sequence past a similar region
located at the 3’ end of the fragment. ITS was amplified in two non-overlapping pieces using two
internal primers with a pair of external primers: 17SE-ITS2 and ITS3-26SE (White et al., 1990;
Sun et al., 1994).
All reactions were performed using Ready Master mix (Advanced Biotechnologies,
Epsom, Surrey, UK), with addition of 4.5% of dimethyl sulfoxide (DMSO) to ITS amplification
reactions to reduce secondary structure problems common in ribosomal DNA (Álvarez &
Wendel, 2003). PCR amplification was performed using the following programs: for rbcL and
trnH-psbA spacer 3 min at 94°C followed by 28 cycles of 1 min 94°C, 1 min at 48°C, and 1 min
at 72°C, with a final extension at 72°C for 7 min; for psaA-ycf3 spacer and ITS 1 min at 94°C
followed by 26 cycles of 1 min at 94°C, 1 min at 48°C and 3 min at 72°C followed by a final 7
min extension (72°C). Amplified products were purified using QIAquick columns (QIAgen,
Germany) following the manufacturer’s protocol. Cycle sequencing reactions were carried out
using BigDye© V3.1 Terminator Mix (Applied Biosystems, Inc., ABI, Warrington, Cheshire,
UK) and cleaned using the EtOH-NaCl method provided by ABI; they were then sequenced on
an ABI 3130xl genetic analyser.
Complementary strands were assembled and edited using Sequencher version 4.6 (Gene
Codes Corp., Ann Arbor, Michigan, USA) and sequences were aligned manually in PAUP*
(version 4.0b1; Swofford, 2002) without difficulty due to low levels of insertions/deletions
(indels) except for the trnH-psbA spacer for which large regions were excluded from analyses
due to alignment difficulties. Nineteen indels were included for the plastid DNA analyses as
presence/absence characters. The aligned matrices are available from the author
(olive.maurin@gmail.com).
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5.2.3 Divergence time estimation (using Beast)
Divergence times were estimated using a Bayesian MCMC approach implemented in BEAST (v.
1.4.8; Drummond & Rambaut, 2007), which allows simultaneous estimation of the topology,
substitution rates and node ages (Drummond & Rambaut, 2007). The dataset was partitioned into
four parts according to the DNA regions used in this study (ITS, rbcL, psaA-ycf3 and psbA-trnH).
I implemented the GTR + I + G model of sequence evolution for each partition based on the
Akaike information criterion (AIC) scores for substitution models evaluated using MrModeltest
(version 2.3; Nylander, 2004) with a gamma-distribution with four rate categories. A speciation
model following a Yule process was selected as the tree prior, with an uncorrelated log normal
(UCLN) model for rate variation among branches.
Seven fossil dates or calibration points taken from previous analysis were used to
constrain specific nodes to minimum, maximum or fixed ages. In the first dataset (analysis 1)
based on rbcL I use the following calibration points. First, 111 mya (fixed; node A, Figure 5.1) as
the crown group age for Myrtales based on the results from Systma et al. (2004). I used the two
fossils from Melastomataceae as in Systma et al. (2004) assigned to the node representing the
most recent common ancestor (MRCA) of Pternandra and all other Melastomataceae, an (min.)
age of 53 mya (Wehr & Hopkins, 1994; node B, Figure 5.1) and the node representing the
MRCA of Monachaetum and Rhexia an (min.) age of 23 mya (node C, Figure 5.1). I also
followed Systma et al. (2004) and assigned an (min.) age of 86 mya to the crown node of
Psiloxylaceae/Heteropyxidaceae/Myrtaceae/Vochysiaceae clade (PHMV) by using the pollen
fossil Myrtaceidites from Gabon (Herngreen, 1975; Muller, 1981; node D, Figure 5.1).
I then used the mean age of the rbcL analysis of Myrtales to calibrate Combretaceae in the
second analysis (analysis 2) at a minimum age 65 mya (node A, Figure 5.2), which permits the
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age of this node to be adjusted to be older if warranted by the other calibration points, and the
split of the clade containing the three closely related taxa Terminalia catappa, T. littoralis and T.
kaernbachii with an MRCA at 4 mya (node B, Figure 5.2) based on a fossil dated from the Upper
Pliocene to Pleistocene (Mehrotra et al., 2003) and the MRCA for the three closely related
species Terminalia arujna, T. myriocarpa and T. tomentosa (Terminalioxylon) at (min.) 28 mya
(node C, Figure 5.2). I did not use the Anogeissoxylon fossil (Ahmed et al., 2007) from the
Palaeocene (65.5 to 55.8 mya) because it pushed the age estimates back far too early, which does
not correspond well with dates obtained in the study of Systma et al. (2004). In this second
analysis the calibration date of Combretaceae reported from the first analysis was set as log
normal prior when the three other calibration points were selected as uniform.
5.2.4 Optimisation of habitat, climate, and morphological characters
Several characters were coded that were thought to be significant in terms of the evolutionary
history of subtribe Combretinae Combretaceae and were mapped on the Bayesian tree obtained in
chapter 2, namely: (a) habitat: 0 = forest and forest edge; 1 = savanna and woodlands; (b)
climate: 0 = humid; 1 = dry; (c) upper hypanthium shape: 0 = flat; 1 = campanulate; and 2 =
elongated to cylindric; according to Stace (1969) in Combretum an open upper hypanthium is
generally considered as ancestral (section Hypocrateropsis, Haplostemon and Plumbea),
whereas tubular shapes are viewed as more derived (section Quisqualis); (d) type of glandular
hairs: 0 = scales; 1 = glandular hairs; and (e) the number of cells per leaf scale was coded in order
to investigate possible evolutionary pattern of these structures in subgenus Combretum: 0 = 8–
16; 1 = 17+; scales within Combretum subgenus Combretum can either be simple (8–16)
with/without radials walls or complex (17–300+) delimited by a multitude of walls. I decided on
this delimitation for the following reasons: (1) the basic number of scales in a radial arrangement
is eight, (2) the very common occasional duplication (radial or tangential) of each of these cells
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brings number of scales to a maximum of 16, and (3) scales from 17 cells upward have a more
complex structure due to additions and divisions. Currently there is no hypothesis on the
significance of this division but it does seem to indicate taxon and scale size associations. These
five characters were traced on the Bayesian tree obtained in chapter 2 using MacClade version
4.04 with DELTRAN optimisation (Maddison & Maddison, 2001).
5.3 RESULTS
The chronograms are presented in Figures 5.1 and 5.2. Estimated ages for all major clades within
the order and the family are reported in Table 5.3 and 5.4, respectively. Ecological characters
within Combretoideae are mapped on phylogenetic trees in Figures 5.3 to 5.7.
5.3.1 rbcL analysis with a broad outgroup sampling (analysis 1; Figure 5.1)
The first analysis within Myrtales estimated an origin for Combretaceae/Onagraceae/Lythraceae
(node 1) at 96.6 mya and the rest of the order at 105.3 mya (node 2). The clade delimited by node
1 split Combretaceae from Onagraceae/Lythraceae with respective diverging dates at 65.3 mya
(node 3) and 76.8 mya (node 4).
5.3.2 Combined plastid and nuclear analysis (analysis 2; Figure 5.2)
In the second analysis, Combretaceae diversified at 82.6 mya (node 1), corresponding to the split
between Strephonematoideae and Combretoideae. This is older than the minimum age set for this
node, 65 mya – it was pushed back by the other more interior nodes used to calibrate the tree,
which BEAST permits. These two subfamilies experienced their first splits at 10.8 mya (node 2)
and 77.5 mya (node 3), respectively. Combreteae diversified at 69.1 mya (node 4), with tribe
Laguncularieae diverging at 42.8 mya (node 5).
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5.3.2.1 Subtribe Terminaliinae (Figure 5.2)
Within tribe Combreteae, subtribe Terminaliinae has a divergence date at 54.4 mya (node 6) and
Combretinae at 59.4 mya (node 7). Within Terminaliinae, Conocarpus first diversified at 8.9 mya
(node 8), and the rest of the subtribe diverged at 43.9 mya (node 9). Within Terminaliinae two
clades are identified, the first containing mainly Asian species of Terminalia and Anogeissus
diverging at 38.6 mya (node 10) and the second clade containing Buchenavia, Bucida, Pteleopsis
and species of Terminalia from Africa, tropical Asia and the Pacific diverging at 37.0 mya (node
11).
5.3.2.2 Subtribe Combretineae (Figure 5.2)
Within subtribe Combretinae, Calycopteris and Guiera are sister to the rest of the subtribe with a
date of 37.1 mya (node 12). Thiloa is sister to Combretum (including the genera recently
transferred to Combretum: Quisqualis, Calopyxis, and Meiostemon) with a divergence date of
46.5 mya (node 13). The two subgenera of Combretum diverged 43.9 mya (node 14) with
subgenus Cacoucia diverging at 28.4 mya (node 15) and subgenus Combretum at 39.2 mya (node
16). Subgenus Cacoucia is divided into two main clades, the first comprising sections Quisqualis
(= genus Quisqualis), Grandiflora (= section Poivrea), Calopyxis (= genus Calopyxis) and
Trichopetala (= section Poivrea) diverging at 20.0 mya (node 17). Section Quisqualis (= genus
Quisqualis) diverged at 15.2 mya (node 18), with a diversification of the African taxa at 8.9 mya
(node 19) and for Asian taxa included in my sampling at 5.6 mya (node 20). The second main
clade within subgenus Cacoucia includes sections Conniventia, Megalantherum, Oxystachia and
Poivrea, which diverged at 23.6 mya (node 21).
In subgenus Combretum, section Haplostemon is sister to the rest and diverged at 13.3
mya (node 22). Two clades are observed within the rest of subgenus Combretum (excluding
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section Haplostemon), with the first delimited by node 23 and including Combretum imberbe
(section Plumbea) placed as sister to sections Campestria, Breviramea and Metallicum, diverging
from these sections at 31.9 mya (node 23), with the sections mentioned above diversifying at 25.5
mya (node 24), 22.0 mya (node 25) and 11.9 mya (node 26), respectively. In the second clade
delimited by node 28 section Hypocrateropsis is sister and diverged from the rest of the clade at
32.8 mya (node 28) and diversified within the section at 18.2 mya (node 29). The remaining
sections within subgenus Combretum have the following node dates: Ciliatipetala, at 18.0 mya
(node 30); with two distinct subclades, a southern African and an African subclade diverging
respectively at 8.7 (node 31) and 13.8 mya (node 32), Angustimarginata at 7.4 mya (node 33),
Macrostigmatea/Spathulipetela at 11.2 mya (node 34), and Glabripetala at 1.4 mya (node 35).
5.4 DISCUSSION
A relatively complete generic-level tree was used to date the crown node of Combretaceae. Only
three of the 14 genera were missing, Dansiea and Macropteranthes (Australia; Lagunculariae),
and Finetia (Indochina). Sampling is, however, mostly limited to Africa, and future studies
should include more taxa from the New World and Asia. It will also be imperative to add the
third, monotypic, subgenus Apetalanthum. Despite these limitations, my sampling provides the
opportunity to investigate possible evolutionary patterns within Combretaceae and assess
biogeographical patterns within African Combretinae; given the limitations in sampling outside
of Africa, the conclusions presented here should be considered as preliminary.
5.4.1 Origin of Combretaceae
A crown date for Combretaceae, obtained from the rbcL analysis of Myrtales (analysis 1; Figure
5.1), suggested an origin of around 65 mya (Figure 5.1, node 3). This date is 18 mya older than
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that proposed by Systma et al. (2004) in their study, which used a combination of two genes
(rbcL and ndhF), and produced a slightly different, but weakly supported, topology at the basal
nodes of Myrtales. According to Systma et al. (2004), Combretaceae had not been adequately
sampled as several important groups were excluded, for example representatives of the subfamily
Strephonematoideae. On the basis of their study the authors concluded that the crown radiation of
Combretaceae might possibly be older than they predicted and more consistent with the
Esgueiria fossil dates. For the Combretaceae data analysed here (four DNA regions), the tree
was calibrated using a minimum date of 65 mya for the stem Combretaceae lineages (Figure 5.2,
node A/1) based on analysis 1. Constraints were not enforced on this node, resulting in a higher
estimate (82.6 mya, 65.08–113.24; Figure 5.2, node A/1) for the crown date of Combretaceae.
Although the date is older that the date reported from analysis 1, it still falls within the range
(46.99–87.05) reported by the first analysis. This date proved to be more consistent with
estimates based on the fossil Esgueiria. Esgueiria is represented by two fossils, one from the
Campanian-Maastichtian epoch that was found in Portugal (Friis et al., 1991) and a second from
the early Santonian discovered in Japan (Takahashii et al., 1999). These fossils were not used in
Systma et al. (2004) because they believed the flowers differ significantly in stylar branches from
extant Combretaceae. They argued that placement of it within Combretaceae is not at all certain,
and that it might represent a member of an early stem lineage sister to extant Combretaceae (Friis
et al., 1991).
The evolution of the angiosperms began in the early Cretaceous, from 130 mya, and
underwent a major diversification up to the late Cretaceous 90 mya, as well as during the Tertiary
(Crane, 1993; Crane et al., 1995). However, molecular dating (Moore et al., 2007) suggested that
extant angiosperms began to diversify in the mid-Jurassic (170 mya) and that the five major
angiosperm lineages diversified relatively rapidly in the early Cretaceous around 140 mya. The
data in the current study suggest that Combretaceae would have appeared during the late
198
Cenezoic, in the Campanian epoch (end of the Cretaceous and the beginning of the Tertiary).
Radial symmetry is the most common type found within Combretaceae, but slight zygomorphism
evolved in several clades independently in the early Tertiary, during the Paleocene and early
Eocene epoch, for example in some species of Combretum subgenus Cacoucia (section
Calopyxis) and in the Australian genus Dansiea (not included in my analyses). This shift in floral
symmetry might be explained as an adaptation to pollinators that are better able to exploit this
peculiar flower morphology (e.g. hawkmoths or sunbirds). The absence of a well-supported
phylogenetic tree prevented detailed studies of the evolution of pollination systems within the
family from being conducted. It would be worthwhile evaluating floral characters, such as the
shape of the upper hypanthium, floral symmetry, nectar production, development of staminodes,
and pollinators across Combretum; these characters could then be mapped onto a phylogenetic
tree to set up hypotheses concerning the evolution of pollination syndromes. This is, however,
beyond the scope of this study as crucial missing taxa, such as Combretum apetalum, and more
representatives of New World taxa, should be included in the analyses (Chapter 2).
5.4.2 Split between the two subfamilies Strephonematoideae and Combretoideae
According to the multi-gene dataset and the use of a relaxed clock to date the Combretaceae
crown node, the split between Strephonematoideae and Combretoideae occurred around 82 mya
(Figure 5.2, node A/1) in the Santonian, Late Cretaceous. Strephonema, the only genus belonging
to Strephonematoideae, which is restricted to west and central Tropical Africa and is absent in the
Dahomey gap, diverged during the Miocene (10.8 mya, Figure 5.2, node 2). This was a period
when this part of the African continent was slowly getting warmer, with tropical forests
diminishing and eastern Africa gradually becoming drier, leading to the range expansion of
woodland and savanna vegetation. It can therefore be hypothesised that Strephonema diverged at
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an earlier time, with a much wider distribution, when tropical forests were covering the continent
from west to east, for example during the Eocene period, when these conditions were prevalent.
5.4.3 Tribe Laguncularieae and the evolution of mangroves
Within subfamily Combretoideae, tribe Laguncularieae are mostly mangrove or mangroveassociated taxa. The data in the current study suggest a split between Laguncularieae and the rest
of Combretoideae at approximately 77 mya (Figure 5.2, node 3), with a diversification around 42
mya (Figure 5.2, node 5). The estimated age of diversification is congruent with the results of
Plaziat et al. (2001), who found that mangroves originated with a pantropical-subtropical
distribution in the early Tertiary from 70.6 mya. In Rhizophoraceae, Bruguiera and Ceriops are
known from the early Eocene (55.8–33.9 mya), Kandelia from the middle Eocene, and
Rhizophora from the late Eocene (Graham, 2006). Combretocarpus (Anisophylleaceae) is likely
to have been present from the middle Miocene (23.03–5.33 mya; Graham, 2006). Genera
included in the current study often occurr in tropical mangroves. As mentioned previously, the
two Australian mangrove taxa, Macropteranthes and Dansiea, were not included in this study.
According to Ellison et al. (1999), regional species diversity of mangroves resulted from
in situ diversification following continental drift. Plaziat et al. (2001), however, re-examined
fossil evidence of Avicennia, Pelliciera, Sonneratia, Rhizophora, Bruguiera and Ceriops and
concluded that modern mangrove flora occurred throughout the tropics by the Eocene and appear
to have originated during Palaeocene times. Earlier Palaeozoic and Mesozoic candidates for a
mangrove ecology lack conclusive evidence of their exclusive association to tidal environments.
It is therefore clear, according to these authors, that continental drift had a limited role in the
dispersal and development of modern mangrove floras.
The early Tertiary is considered a period of pantropical/subtropical homogeneity of the
mangrove ecosystem, and the period between the Eocene (55.8–33.9 mya)/Oligocene (33.9–
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23.03 mya) is marked by the first important tectonic phase of upheaval of the Alpine mountains
that affected the tropical seaways that lead to cooling event of major global importance (Plaziat et
al., 2001). These events represent the starting point towards the modern biogeographic split
(Plaziat et al., 2001) between eastern and western mangroves, with the formation of the
Eurafrican gap (Figure 5.8). The period is marked by a cooling event that can be viewed as a
possible cause for the bipartition of the clade. Within Laguncularieae, the split between
Lumnitzeria and Laguncularia occurred in the middle of the Eocene at 42 mya (Figure 5.2, node
5). Laguncularia is distributed from the New World tropics to tropical West Africa, and
Lumnitzeria occurs from tropical West Africa to Australia and the Pacific. The distribution of
Laguncularia in eastern and western New World tropics can also be observed in other mangrove
taxa, which show similarities between the Pacific and Caribbean mangroves. Until the early
Pliocene (the epoch starts at 5.33 mya), North and South America were separated, and the
Panamanian land bridge was formed due to movement of the South American continental plate
into North America, which blocked movement of water and mangrove seeds between the Atlantic
and Pacific Oceans at a relatively late time in history.
Although not part of Laguncularieae, Conocarpus, a mangrove-like taxa, can also be
discussed here, because of its distribution, habit, and divergence in the chronogram. Conocarpus
was derived from the remainder of subtribe Terminaliinae 54 mya (Figure 5.2, node 6), at a
similar time to the diversification of tribe Laguncularieae, and its distribution is restricted to
tropical America and tropical West Africa. In the latter, mangroves do not occur further south
than Gabon, and only a few localised patches exist, which can be explained by the cold oceanic
current in this part of the African coast. On the eastern side of Africa, mangroves are present at
more southern locations, being found all the way to Mozambique, in addition to localised areas as
far south as Kwazulu-Natal (South Africa). Lumnitzeria racemosa follows this distribution and
has its southernmost distribution on the border between South Africa and Mozambique.
201
5.4.4 Split between Combretinae and Terminaliinae
The two subtribes Combretinae and Terminaliinae, containing the two largest genera Combretum
and Terminalia, respectively, split at the end of the Late Cretaceous around 69 mya (Figure 5.2,
node 4). This period was marked by a number of mass extinctions, both in plants and animals.
Several hypotheses exist about the causes of these extinctions. The more prominent of the new
hypotheses invoked extra-terrestrial forces such as meteorite impacts or comet showers, whereas
older hypotheses involved mechanisms such as volcanism or glaciation. Whatever the cause, it
affected the diversification rate of the angiosperm flora during the Cretaceous. The recovery of
angiosperm groups could have happened through a process similar to that seen in vegetation
destroyed by a volcanic eruption, where the new terrain is first colonised by ferns. The lineages
that persisted through this period of extinction represent Terminaliinae and Combretinae, which
possibly survived by being adapted to different niches and then later diversified.
5.4.5 Subtribe Terminaliinae
Within subtribe Terminaliinae, Conocarpus separated from the rest of Terminaliinae about 54
mya (Figure 5.2, node 6, see discussion above). Within this subtribe, rapid diversification
occurred during the Eocene. This epoch (around 55 mya) is generally characterised by abrupt
global warming of 5 to 10ºC, making it the warmest period of the Tertiary. It would be premature
to make a definite conclusion at this stage regarding diversification within Terminaliineae,
because of the limited sampling in this study. It can, however, be postulated that fragmentation of
the forests that started within the Oligocene, around 35 mya, had a direct effect on diversification
in this subtribe; for example, the divergence that occurred around 38 mya (Figure 5.2, node 10) in
the Asian clade of Terminalia could have had this sort of event as a factor (including former
202
Anogeissus), as well as the split at 36 mya in the mostly African Terminalia clade (Figure 5.2,
node 11).
Terminalia is mostly known for production of timber, and it primarily occurs in tropical
forests; however, many species are known to have become adapted to more arid savanna
vegetation. In such conditions, Terminalia species have a tendency to change their habit,
becoming large shrubs to small trees, for example T. phanerophlebia, T. stenostachya, T.
sambesiaca, T. brachystemma and T. mollis. These taxa are members of a clade that shows an
important speciation event during the end of the Miocene (which ends at 5.33 mya) and start of
the Paleocene (start 5.33–1.81 mya) at a time where competition is significant in open vegetation
dominated by Poaceae. Therefore, it can be hypothesised that Terminalia diversified due to the
expansion of drier types of vegetation.
5.4.6 Subtribe Combretinae
A split between the clade containing Guiera and Calycopteris and the remaining members of the
subtribe took place in the Paleocene around 59 mya (Figure 5.2, node 7). This epoch is after the
mass extinction event that marks the end of the Cretaceaous, when the climate was generally
warmer, and a similar scenario to the split between the two subtribes Combretinae and
Terminaliinae can be postulated (see above). The branch leading to the two monotypic genera
Guiera and Calycopteris is relatively long, with a split between the two genera only occurring
around 37 mya (Figure 5.2, node12; 22 mya elapsed between the two events). The relationship
between these two taxa remains surprising, as they have different distributions, with Guiera
restricted to dry to semi-dry regions of western and central tropical Africa, and Calycopteris from
Southeast Asia. The long branch before the split could suggest multiple lineages arising from the
previous split (Figure 5.2, node 7) followed by extinction, with only two succeeding and
becoming relics.
203
Stace (2007) recently suggested that Thiloa should be included in Combretum, which in
my analyses is sister to the rest of Combretum. Thiloa comprises three species restricted to the
northern parts of South America; it diverged from Combretum around 46 mya (Figure 5.2, node
13). A wider sampling of Combretum from the New World will be necessary to fully assess the
relationship between Combretum and Thiloa.
The next split in the chronogram represents that of the two largest subgenera of
Combretum, Combretum and Cacoucia. Although the sampling does not cover the whole
distribution of the genus and is mostly focused on Africa, it is important to keep in mind that the
center of diversity for Combretum is in Africa with around 163 taxa. As mentioned previously, it
will also be imperative to add the third, monotypic, subgenus Apetalanthum, which occurs in
Thailand and Burma, to understand the relationships and distributions between the three
subgenera. This split occurred in the middle Eocene at a time when global temperatures were
high, possibly supporting a rapid diversification within the genus, with two lineages succeeding
in their adaptation to a wide range of climatic conditions. The split is marked by major and
taxonomically useful morphological characters, namely the type of trichomes (Figure 5.7), scales
only being observed in subgenus Combretum and glandular hairs only found in subgenus
Cacoucia. It is impossible to make any accurate assessment at this stage on possible causes for
the split between the two subgenera, with each one possessing a specific type of trichomes
(glandular hairs or leaf scales). It is even more difficult to evaluate the potential causes of the
split, as the phylogenetic history between these two subgenera and Apetalanthum is unknown.
Within subgenus Cacoucia the shape of the glandular hairs and their structure can be useful
taxonomically, but differences are not as obvious as with leaf scales of subgenus Combretum. It
is not possible with the current knowledge of these structures to suggest a straight and simple
evolutionary scenario for development of scale structure (Figure 5.8). Simple scales are observed
in section Haplostemon (= Meiostemon), which contains species that represent early diverging
204
taxa in Combretum. In sections Plumbea and Hypocrateropsis, scales are mostly complex due to
possession of a large number of scales, and these two sections represent the following more
morphologically derivative taxa in the genus. Within the other sections, which appeared later,
shape and complexity of scales do not follow a uniform pattern, with some cases displaying a
reversion back to simple structures (section Angustimarginata) and others more complex (section
Mettalicum). Evolution of scales seems to have followed complex evolutionary patterns.
Floral structure is also slightly different between the two subgenera. In subgenus
Combretum, the upper hypanthium is slightly shorter, being almost flat in some sections such as
Hypocrateropsis (Figure 5.9) and Plumbea (Figure 5.10), to tubular in Chionanthoidea (Stace,
1968), with intermediate forms found between the two extremes (Figures 5.11, 5.12 and 5.13). In
subgenus Cacoucia, the upper hypanthium is mostly campanulate and infundibuliform to an
extremely tubular form. Section Conniventia (subgenus Cacoucia) includes species with
relatively short tubes (Figures 5.14, 5.15), with the extreme being recorded in section Quisqualis
(subgenus Cacoucia; ex genus Quisqualis, Figure 5.16). Intermediate forms are observed
between the extremes in sections Grandiflora (Figure 5.17), Poivrea (Figure 5.18) and
Trichopetala (Figure 5.19).
Subgenus Combretum diversified at an earlier time than subgenus Cacoucia (39 mya, and
29 mya, respectively, nodes 16 and 15; Figure 5.2). Diversification in Cacoucia is greater during
the Miocene, at a time when speciation slowed down in subgenus Combretum. Subgenus
Cacoucia is characterised by far more colourful flowers with well-developed petals than in
subgenus Combretum. As mentioned previously, it is also in subgenus Cacoucia that slight
zygomorphism can be observed. The floral structure is thus probably attracting a wider range of
pollinators that are not usually involved in pollination within subgenus Combretum (e.g.
hawkmoths in section Quisqualis, sunbirds in section Calopyxis). The evolutionary system
involving insect pollination could explain diversification within subgenus Cacoucia.
205
In subgenus Combretum, an early split is observed between section Haplostemon (=
Meiostemon) and the rest of the subgenus. In Meiostemon, there is simplification of floral
structure, namely it lacks one whole whorl of stamens. Furthermore, flowers in this section have
an flattened upper hypanthium. It could be hypothesised that a single row of stamens is primitive
in subgenus Combretum. Flattened flowers as observed in section Haplostemon are similar to
those found in section Hypocrateropsis, which has been viewed as the most primitive (or least
derived) section due to its almost completely flattened upper hypanthium (Stace, 1969). Sections
Haplostemon, Hypocrateropsis, and newly created Plumbea, comprise early diverging lineages,
which support the idea that species with flat hypanthia represent a primitive floral state for the
genus (Figure 5.5).
Sections Hypocrateropsis and Plumbea split from the remaining taxa included in their
respective clades at the beginning of the Oligocene, which was characterised by drastic global
cooling, resulting in part from development of a permanent ice sheet in Antarctica and involving
a drier climate in equatorial areas of Africa. This led to fragmentation of the pan-Africa forest
and development of grasslands that would dominate the Miocene epoch. Closure of the Thethys
Sea resulting from the collision of the African and Eurasian plates tended to reduce the moist
influence of its former latitudinal circulation, which resulted in a temperature rise and subsequent
drier conditions, aiding development and spread of savannas. Several plant families and genera
(i.e. Combretaceae, Fabacaeae, Burseraceae) seem to have been more efficient in adapting to the
rapid expansion of these Poaceae-dominated habitats. Within subgenus Combretum, however, the
Miocene seems to have been marked by a decrease in diversification rate, with the Pliocene
showing some acceleration within several sections. Section Ciliatipetala, and most particularly
the clade restricted to southern Africa, shows a high rate of diversification, with species often
displaying restricted distributions. Section Macrostigmatea (including Combretum zeyheri) also
shows a high diversification rate in savanna vegetation at the Pliocene. Section Mettalicum shows
206
an origin in the middle Miocene with a split from C. hypopilinum, which has a wider distribution,
and the remaining members of the section include mostly southern and eastern African taxa.
Several species of subgenus Combretum have, however, not adapted to these conditions (open
vegetation and dry conditions) and instead found refuge in remote places such as humid lowland
or high-elevation wet forests (i.e. C. edwardsii, C. caffrum).
5.5 CONCLUSIONS
Results from the dating analyses indicate a date of origin for the family Combretaceae in the Late
Cretaceous, at a time of high angiosperm diversification. This date is more consistent than were
earlier studies with Esgueiria fossil dates, which demonstrates that Esgueiria is potentially a
reliable calibration point for the family.
Although origins of mangroves are still debated, mostly because the mangrove fossils
prior to 40 mya have been proved to be unreliable, diversification of mangrove species belonging
to Combretaceae is comparable with that of other mangrove families (Rhizophoraceae). The
modern distribution of mangroves shows a biogeographic disjunction, with the African continent
representing a barrier between the Atlantic taxa occurring in western African and tropical
America (both on the Pacific side and Atlantic side) and the Indian Ocean, Asian and Pacific
island taxa.
The split between subtribes Terminaliinae and Combretineae is estimated in the Late
Cretaceous prior to the mass extinction event that marked the end of this period. Their divergence
occurred at the beginning of the Eocene, most probably while angiosperms were recovering from
the mass extinction. The Eocene represents a period of important radiation within these subtribes;
during this time, temperatures were relatively high and vegetation was largely continuous. The
end of the Eocene/beginning of the Oligocene is marked by a dry period that caused the
207
fragmentation of forests, as shown in both subtribes; this split corresponds to subgenera
Combretum and Cacoucia in Combretum and within Terminalia the split between clades
comprising mostly African and Asian taxa.
Morphological characters such as scales did not have a straightforward evolutionary
pattern, i.e. from simple to complex scales (or opposite), but these remain useful nontheless as a
taxonomic tool. I however hypothesise that floral structure, and more particularly the shape of the
upper hypanthium, followed an evolutionary pathway from open (most probably pollinated by
insects and wind) towards a more complex tubular shape, and in some cases presenting a slight
zygomorphism, which would involve specialised pollinators such as hawkmoths and sunbirds.
208
TABLE 5.1 Circumscription of Myrtales according to different authors.
Cronquist (1988)
Thorne (1992)
Takhtajan (1997)
APG II (2003)
APGIII (2009)
Alzateaceae
Alzateaceae
Alzateaceae
Alzateaceae
Alzateaceae
Combretaceae
Combretaceae
Combretaceae
Combretaceae
Combretaceae
Crypteroniaceae
Crypteroniaceae
Crypteroniaceae
Crypteroniaceae
Crypteroniaceae
Lythraceae
Lythraceae
Lythraceae
Lythraceae
Lythraceae
Melastomataceae
Melastomataceae
Melastomataceae
Melastomataceae
Melastomataceae
= Melastomataceae
= Melastomataceae
Memecylaceae
Memecylaceae
= Melastomataceae
Myrtaceae
Myrtaceae
Myrtaceae
Myrtaceae
Myrtaceae
Heteropyxidaceae
= Myrtaceae
Heteropyxidaceae
Heteropyxidaceae
= Myrtaceae
Psiloxylaceae
= Myrtaceae
Psiloxylaceae
Psiloxylaceae
= Psiloxylaceae
Onagraceae
Onagraceae
Onagraceae
Onagraceae
Onagraceae
Penaeaceae
Penaeaceae
Penaeaceae
Penaeaceae
Penaeaceae
Oliniaceae
Oliniaceae
Oliniaceae
Oliniaceae
= Penaeaceae
Rhynchocalycaceae
Rhynchocalycaceae
Rhynchocalycaceae
Rhynchocalycaceae
= Penaeaceae
= Polygalales
= Polygalales
= Vochysiales
Vochysiaceae
Vochysiaceae
Punicaceae
= Lythraceae
Punicaceae
= Lythraceae
= Lythraceae
= Sonneratiaceae
= Lythraceae
Duabangaceae
= Lythraceae
= Lythraceae
Sonneratiaceae
= Lythraceae
Sonneratiaceae
= Lythraceae
= Lythraceae
Trapaceae
Trapaceae
Trapaceae
= Lythraceae
= Lythraceae
209
TABLE 5.2 Biogeography and classification of Combretaceae according to Mabberley (2008), Exell & Stace (1966), and Stace (1968, 1980a, 1980b). Geographical range:
Am = America; Af = Africa; As = Asia; Au = Australasia. In brackets is the total; under genus total number of species worldwide; under continent total number of species
per geographic area.
Subfamily
Tribe
Subtribe
Genus
Total number of
Estimated number of species
species
Strephonematoideae
Am
Af
As
Au
Strephonema Hook.f.
3
–
3 (3)
–
–
1
1(1)
1(1)
–
–
Lumnitzera Willd.
2
–
1(1)
2(2)
2(2)
Terminaliinae (DC)
Anogeissus (DC.)Wall (=
7
–
1(1)
Exell & Stace
Terminalia)
24
24
–
–
–
Conocarpus L.
2
1(2)
2(2)
1(2)
–
Bucida L.
4
4 (4)
–
–
–
9
–
9(9)
–
–
Engl. & Diels
Combretoideae Engl. & Laguncularieae
Diels
Engl. & Diels
Combreteae DC.
Buchenavia Eichler (=
Terminalia)
(= Terminalia L.)
Pteleopsis Engl. (=
Terminalia)
Terminalia L.
Combretinae Exell &
+/- 150
Calycopteris Lam.
1
–
–
1(1)
–
Calopyxis Tul. (=
23
–
–
23(23)
–
Stace
210
Combretum)
Combretum Loefl.
+/- 250
Guiera Adans
1
–
1(1)
–
–
2
–
2(2)
–
–
16
–
2
15
–
3
3
–
–
–
(= Combretum)
Quisqualis L. (=
Combretum)
Thiloa Eichler
211
TABLE 5.3 Node ages in millions of years (mya). For each node, the estimated age, along with the 95% high
posterior density interval (95%HPD), are presented. Node numbers correspond to those in Figure 5.2.
Node
Description
Age
95% (HPD)
1
Crown age of Combretaceae/Onagraceae/Lythraceae
96.6
[80.65,109.81]
2
Remaining genera of Myrtales
105.3
[96.39,112.41]
3
Crown age of Combretaceae
65.3
[46.99,87.05]
4
Crown age for Onagraceae/Lythraceae
76.8
[58.99,93.68]
5
Crown age for PHMV
91.3
[86,100.01]
6
Crown age for Psiloxylaceae/Heteropyxidaceae
32.9
[9.3,66.77]
(PsiHet)
7
Split between Myrtaceae and Vochysiaceae
71.1
–
8
Crown age for Myrtaceae
45.7
[26.05,67.49]
9
Vochysiaceae
35.2
[16.36,54.58]
10
Split of Melastomataceae s. l. and CAROP
89.9
[75.55,103.35]
11
Crown age for CAROP
58.6
[32.18,84.79]
12
Crown age for Melastomataceae
61.0
[53,71.98]
13
Crown age for Memecylaceae
24.8
[8.82,44.09]
212
Table 5.4 Node ages in millions of years (mya). For each node, the estimated age along with the 95% high
posterior density interval (95%HPD) are presented. Node numbers correspond to those in Figure 5.3.
Node
Description
Age
95% (HPD)
1
Crown age of Combretaceae.
82.6
[65.08,113.24]
2
Crown age of Strephonematoideae.
10.8
[4.29,19.17]
3
Crown age of Combretoideae.
77.5
[59.49,105.32]
4
Crown age of Combreteae.
69.1
[52.02,92.61]
5
Crown age of Laguncularieae (split
42.8
[18.84,72.32]
54.4
[40.81,72.06]
between Laguncularia and Lumnitzera).
6
Crown age of Terminaliinae (Split
between Conocarpus and rest of
Terminaliinae.
7
Crown age for Combretinae.
59.4
[43.3,81.43]
8
Crown age for Conocarpus.
8.9
[2.68,16.81]
9
Crown age of Terminaliinae (excluding
43.9
[34.55,56.48]
38.6
[31.59,47.81]
37.0
[34.55,56.48]
Conocarpus).
10
Crown age of Anogeissus and Asian
Terminalia.
11
Crown age of Buchenavia, Bucida,
Pteleopsis and Terminalia species from
Africa, tropical Asia, Australia and the
Pacific.
12
Crown age for Guiera and Calycopteris
37.1
[17.9,56.41]
13
Split between Thiloa and rest of
46.5
[34.23,62.88]
43.9
[32.04,59.01]
Combretum (includes Calopyxis,
Meistemon and Quisqualis).
14
Crown age of Combretum (including
Calopyxis, Meistemon and Quisqualis)
corresponding to the split between
subgenus Combretum and Cacoucia.
213
15
Crown age of subgenus Cacoucia.
28.4
[18.42,40.41]
16
Crown age of subgenus Combretum - split
39.2
[29.02,52.31]
20.0
[12.85,28.64]
between section Haplostemon (= genus
Meiostemon) and rest of Combretum
subgenus Combretum
17
Collective age of sections Calopyxis,
Grandiflorum, Quisqualis and
Trichopetalum .
18
Crown age of section Quisqualis.
15.2
19
Crown age of African taxa of section
8.9
Quisqualis.
20
Crown age of Asian taxa of section
5.6
Quisqualis.
21
Collective age of sections Conniventia,
23.6
[14.86,33.85]
Oxystachia, Megalantherum and Poivrea.
22
Crown age of section Haplostemon.
13.3
23
Collective age of sections Plumbea
31.9
[22.51,43.51]
25.5
[17.38,35.61]
22.0
[14.04,31.09]
11.9
[6.35,18.08]
2.7
[1.01,4.63]
32.8
[23.71,44.31]
Breviramea, Campestria and Mettalicum.
24
Split between section Campestria and
Breviramea, Mettalicum.
25
Split between section Breviramea and
Mettalicum.
26
Crown age of section Mettalicum
corresponding to the split between
southern African and tropical African subspecies
27
Crown age of southern African species of
section Mettalicum
28
Split between section Hypocrateropsis and
rest of subgenus Combretum
214
29
Crown age of section Hypocrateropsis.
18.2
30
Crown age of section Ciliatipatela.
18.0
[12.14,25.14]
31
Within section Ciliatipetala, crown age of
8.7
[4.53,13.69]
13.8
[8.79,19.84]
South African clade.
32
Within section Ciliatipetala, crown age of
and African clade.
33
Crown age of section Angustimarginata.
7.4
[3.63,11.63]
34
Collective age of sections Macrostigmatea
11.2
[6.74,16.39]
and Spathulipetala.
35
Crown age section Glabripetala.
1.4
215
FIGURE 5.1 Chronogram obtained based on rbcL for the order Myrtales. Abbreviations: Memec =
Memecylaceae; CAROP = Crypteroniaceae, Alzateaceae, Rhynchocalycaceae, Oliniaceae and Penaeaceae;
Vochys = Vochysiaceae; PsiHet = Psiloxylaceae and Heteropyxidaceae. Values at nodes are age estimates,
and numbers underneath branches refer to the text.
216
217
FIGURE 5.2 Chronogram of Combretaceae obtained from the combined analysis of rbcL, ITS, trnH-psbA and
psaA-ycf3. Abbreviations: Glabrip.= Glabripetala; Mic.= Micrantha; Brev. = Breviramea; Cam.=
Campestria, Imberb.= Plumbea; Haplos.= Haplostemon; Trichopetal.= Trichopetala; Calopyx.= Calopyxis;
Gra. = Grandiflora; Poiv.= Poivrea; Ox.= Oxystachia; Meg.= Megalanthara. Values at nodes are age
estimates, and numbers underneath branches refer to the text.
218
FIGURE 5.3 Habitat mapped onto the phylogenetic tree for subtribe Combretinae.
219
FIGURE 5.4 Climate mapped on phylogenetic tree for subtribe Combretinae.
220
FIGURE 5.5 Shape of the upper hypanthium mapped on phylogenetic tree for subtribe Combretinae.
221
FIGURE 5.6 Type of trichomes mapped on phylogenetic tree for subtribe Combretinae.
222
FIGURE 5.7 Number of cells per leaf scale mapped on phylogenetic tree for subtribe Combretinae.
223
FIGURE 5.8 Mangrove distribution, where Geomorphic and climatic barriers explain the Eurafrican gap. Illustration
from Plaziat et al., 2001.
FIGURE 5.9 Flowers of Combretum celastroides. The Upper hypanthium is flat shaped and such characters is viewed
as possible ancestral state within Combretum.
FIGURE 5.10 Flowers of Combretum imberbe, previously part of section Hypocrateropsis, which is now transferred
into its own section, Plumbea. The species also present an upper receptacle almost flat. Petals are almost inexistent.
224
FIGURE 5.11 Inflorescences and flowers of Combretum apiculatum. The upper receptacle is conical, petals are
absent.
FIGURE 5.12 Inflorescence and flowers of Combretum kraussii. The shape of the upper hypanthium is cupuliform to
infudibuliform. Petals are smalls but the upper hypanthium is colourfull.
FIGURE 5.13 Inflorescence and flowers of Combretum elaeagnoides.
225
FIGURE 5.14 Flower of Combretum platypetalum. The species belongs to section Conniventia (subgen. Cacoucia)
and is closely related to C. paniculatum and C. microphyllum. The red colour is also observed on other species such
as C. bracteosum, which belong to section Trichopetala.
FIGURE 5.15 Inflorescence and flowers of Combretum paniculatum (section Conniventia).
FIGURE 5.16 Flower of Combretum indica (syn. Quisqualis indica). The floral structure in section Quisqualis
(subgen. Cacoucia) present the extreme form in term of upper hypanthium shape where it is long and tubular. Petals
are well developed and colourfull.
226
FIGURE 5.17 Inflorescence and flowers of Combretum grandiflorum (section Grandiflora).
FIGURE 5.18 Inflorescence and flowers of Combretum coccineum (section Poivrea). Illustration from
http://www.mobot.org, voucher Andrianjafy 1618 CB.
FIGURE 5.19 Flower of Combretum mossambicense (section Trichopetala). The upper hypanthium is comical to
campanulate. The flowers show a tendency to the elongation of the upper receptacle and petals are well developed.
.
227
228
Chapter 6: Conclusions
CHAPTER 6: CONCLUSIONS
Combretaceae have been the focus of previous morphological (Engler & Diels, 1899; Exell,
1953, 1954, 1968, 1970, 1978; Stace, 1965, 1969, 1980a, 1980b; Wickens, 1973; Tilney, 2002;
Tilney & Van Wyk, 2004) and molecular (Tan et al., 2002) studies, but up to date no detailed
phylogenetic analysis exists for the family. The starting point of this study was therefore to
reconstruct a phylogeny for Combretaceae (based on rbcL, trnH-psbA, psaA-ycf3, and ITS DNA
data), which was then used to study phylogenetic relationships (Chapter 2, 3 and 4) and estimate
dates of divergence within Combretaceae (Chapter 5). The results obtain in this study represent
the most comprehensive and complete study of Combretaceae up to date and were useful to
assess the position of several key genera within the family (outlined below).
The results (Chapter 2) generally support the current infrageneric taxonomy with
Combretaceae strongly supported as monophyletic and Strephonematoideae representing the
sister of the rest of the family. The two subtribes Terminaliinae and Combretinae were well
supported. Two main clades were observed within Terminaliinae, with Conocarpus sister to both.
Clade 1 contained representatives of Terminalia from Africa, Asia, Australia and the Pacific
islands, Buchenavia, Bucida and Pteleopsis. The second clade consisted of Asian Terminalia taxa
and Anogeissus. The position of Calycopteris and Guiera as sister to Combretum was supported
in the current study. Two main clades were observed in Combretinae (1) all representatives of
Combretum subgenus Combretum and Meiostemon and (2) all taxa belonging to Combretum
subgenus Cacoucia as well as Quisqualis and Calopyxis. The position of Thiloa was unresolved.
Results from this study supported the recent taxonomic transfer of Quisqualis and
Calopyxis to Combretum subgenus Cacoucia. The following taxonomic changes will be proposed
in publication elsewhere:
229
(1) Terminalia, Buchenavia, Anogeissus and Pteleopsis should be united with the name
Terminalia having priority; (2) the two species of Meiostemon should be transferred to
Combretum; (3) Combretum section Haplostemon should be reinstated; (4) Quisqualis should be
tranferred to Combretum; (5) sections Grandiflora and Trichopetala should be reinstated; and (6)
a new section for C. imberbe should be established.
In Chapters 3 and 4, I focused on one and three African sections, respectively Cilitipetala
and Angustimargina/Macrostigmatea/Spathulipetala. Diagnostic characters were mapped onto
the phylogenetic tree with possible interspecific relationships within the sections discussed.
These results were correlated with morphological data, and taxonomic conclusions include four
proposals: (1) Combretum stylesii O. Maurin, Jordaan & A.E.van Wyk, a liana or slender tree
from the Tugela River Valley (KwaZulu-Natal), South Africa, will be proposed as new.
Molecular data support its inclusion within subgenus Combretum section Ciliatipetala with its
closest relative being Combretum edwardsii. The new species differs from C. edwardsii in
having a single mature leaf form and less complex 8-celled leaf scales. (2) Combretum mkuzense
should be included in section Macrostigmatea, (3) A new species from the Kruger National Park
will be described; it is closely related to, but geographically differentiated from, Combretum
mkuzense and is to be included in section Macrostigmatea. (4) The transfer of section
Spathulipetala (C. zeyheri) into section Macrostigmatea will need to be proposed.
In Chapter 5, I used multiple fossil calibrations of the Combretaceae phylogenetic tree to
estimate the age of the root node of Combretaceae and clades within the family. The hypothetical
evolutionary history of the family was also discussed. The results support the relevance of the
extinct genus Esgueiria as a reliable fossil for assessing the age of Combretaceae and suggest the
family appeared in the Late Cretaceous when angiosperms where diversifying at a high rate. The
mangrove taxa of Combretaceae (tribe Laguncularieae) have followed an evolutionary history
230
comparable to other mangrove taxa such as Rhizophoraceae, presenting today a disjunct
distribution with the African continent as a barrier. The split between the two subtribes
Combretinae and Terminaliinae occured during the Paleocene, most probably after the cataclysm
marking the end of the Cretaceous. Morphological characters such as scales did not have simple
evolutionnary development in which ancestral states developed in the more evolved ones with
possible reversals back to the ancestral state. The shape of the upper hypanthium in Combretum
went from an open structure towards a more complex tubular one and in some cases exhibits a
slight zygomorphism involving more specialised pollinators. These observations are, however,
preliminary and will be investigated in greater detail in future.
FUTURE RESEARCH
Future studies on Combretaceae should focus firstly on increasing the sample size. Adding the
two Australian genera, Dansiea and Macropteranthes, is necessary to assess relationships with
tribe Laguncularieae. To have a better understanding of the generic and subgeneric relationships
with the tribe Combreteae, addition of species from Buchenavia, Pteleopsis, Quisqualis, Thiloa
and Combretum subgenus Combretum section Calopyxis will be necessary. It will also be
imperative to add the third and monotypic subgenus Apetalanthum as well as representatives of
all sections of Combretum and Terminalia.
Secondly, future research should also focus on improving resolution within the genera
and strengthening the ‘backbone’ of the tree. Sequence data from rbcL, trnH-psbA, psaA-ycf3,
and ITS were valuable in this study, but it is clear that low-copy nuclear regions are becoming
more important in phylogenetic analyses and might be an important future step in the
phylogenetic reconstruction of Combretaceae.
231
Once crucial missing taxa such as Combretum apetalum and more representatives of New
World taxa are included in the analysis it will be possible to examine how pollination systems
have evolved within the family.
Conclusions presented here regarding biogeographical patterns should be considered as
preliminary due to the fact that sampling was mainly limited to African taxa and future studies
investigating possible evolutionary and biogeographical patterns within Combretaceae should
include more taxa from the New World and Asia.
232
233
234
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254
255
256
Appendices
APPENDICES
APPENDIX 2.1 Voucher information and GenBank accession numbers for taxa used in this study. A dash indicates
DNA regions not sampled and DNA sequences obtained from GenBank are underlined. Voucher specimens are
deposited in the following herbaria: BISH = Bishop Museum, Honolulu, U.S.A.; JRAU = University of
Johannesburg (UJ), Johannesburg, South Africa; K = Royal Botanic Gardens, Kew, Richmond, United Kingdom;
PRE = South African National Botanical Institute, Pretoria, South Africa; MO = Missouri Botanical Garden, St.
Louis, U.S.A.
Family. Taxon — Voucher (Herbarium), Country where collected, GenBank accession no.: ITS, rbcL, psaA-ycf3,
psbA-trnH.
Annonaceae. Xylopia hypolampra Mildbr., —; AY337731; —; —. Combretaceae. Anogeissus
acuminata Wall., AF334765; AF425708; AF425692; —; Anogeissus leiocarpa Guill. & Perr.,
AF334766; AF425709; AF425693; —; Buchenavia reticulata Eichler, van der Werff H. & R.
Vasquez 13866 (MO), Peru, FJ381770; FJ381804; FJ381841; FJ381877; Buchenavia tetraphylla
(Aubl.) R.A. Howard, Taylor, C.M. 11671 (MO), Puerto Rico, —; FJ381805; FJ381842; —;
Bucida buceras L. Harder, D.K. & M. Merello 1184 (MO),US Florida, FJ381771; FJ381806;
FJ38184; FJ572675; Bucida buceras L. Maurin 1670 (JRAU), Cult., FJ381772; FJ381807;
FJ381844; FJ381878; Calopyxis grandidieri (Drake) Capuron ex Stace, Phillipson &
Rabesihanaka 3147 (K), Madagascar, FJ381762; FJ381796; —; FJ381870; Calopyxis grandidieri
(Drake) Capuron ex Stace, Willing s.n. (K), Madagascar, FJ381761; FJ381795; FJ381834;
FJ381869; Calycopteris floribunda (Roxb.) Lam. ex Poir., AF334770; —; AF425691; —;
Combretum albopunctatum Suess., Maurin 1038 (JRAU), Namibia, EU338031; EU338141;
EU338086; EU338196; Combretum apiculatum Sond. subsp. apiculatum, Lahaye 1355 (JRAU),
South Africa, EU338032; EU338142; EU338087; EU213796; Combretum apiculatum Sond.
subsp. leutweinii (Schinz) Exell , Maurin 1015 (JRAU), Namibia, EU338033; EU338143;
EU338088; EU338197; Combretum bracteosum (Hochst.) Brandis Maurin & van der Bank 22
(JRAU), South Africa, EU338018; EU338128; EU338073; EU338183; Combretum caffrum
(Eckl. & Zeyh.) Kuntze, Maurin & van der Bank 11 (JRAU), South Africa, EU338057;
EU338167; EU338112; EU338221; Combretum celastroides Welw. ex M.A.Lawson subsp.
celastroides, Maurin & van der Bank 28 (JRAU), South Africa, EU338042; EU338152;
257
Appendices
EU338097; EU338206; Combretum celastroides Welw. ex M.A.Lawson subsp. orientale Exell,
Maurin & van der Bank 27 (JRAU), South Africa, EU338043; EU338153; EU338098;
EU338207; Combretum coccineum Engl. & Diels, Archer 2972 (PRE), Madagascar, FJ381766;
FJ381800; FJ381838; FJ381874; Combretum collinum Fresen., Maurin 1524 (JRAU), South
Africa, EU338041; EU338151; EU338096; EU338205; Combretum collinum Fresen. subsp.
gazense (Swynn. & Baker f.), Maurin 1024 (JRAU), South Africa, EU338048; EU338158;
EU338103; EU338212; Combretum collinum Fresen. subsp. suluense (Engl. & Diels) Okafor,
EU338213; Combretum collinum Fresen. subsp. taborense (Engl.) Okafor, Bryden 170 (JRAU),
South Africa, EU338050; EU338160; EU338105; EU338214; Combretum collinum Fresen.
subsp. hypopilinum (Diels) Okafor, Sanou 004 (K), Burkina Faso, FJ381756; FJ381790;
FJ381829; FJ381865; Combretum edwardsii Exell, Maurin 1584 (JRAU), South Africa,
EU338034; EU338144; EU338089; EU338198; Combretum elaeagnoides Klotzsch, Maurin
1021 (JRAU), Namibia, EU338040; EU338150; EU338095; EU338204; Combretum engleri
Schinz, Maurin 1025 (JRAU), Namibia, EU338051; EU338161; EU338106; EU338215;
Combretum erythrophyllum (Burch.) Sond., Maurin 201 (JRAU), South Africa, EU338023;
EU338133; EU338078; EU338188; Combretum fragrans F.Hoffm., Slageren & Sanou 866 (K),
Burkina Faso, FJ381754; FJ381788; —; —; Combretum glutinosum Perr. ex DC., Slageren &
Sanou 854 (K), Burkina Faso, FJ381755; FJ381789; FJ381828; —; Combretum goldieanum
F.Muell., P.Hayers FL-1125 (BISH), Cult., FJ381767; FJ381801; FJ381839; FJ381875;
Combretum grandiflorum G.Don, P.C. Hutchinson 2849 (BISH), Cult., FJ381763; FJ381797;
FJ381835; FJ381871; Combretum hereroense Schinz, Maurin 238 (JRAU), South Africa,
EU338028; EU338138; EU338083; EU338193; Combretum holstii Engl., Palgrave 504 (JRAU),
Mozambique, EU338019; EU338129; EU338074; EU338184; Combretum imberbe Wawra,
Maurin 1012 (JRAU), Namibia, EU338044; EU338154; EU338099; EU338208; Combretum
imberbe Wawra, Lahaye 1380 (JRAU), South Africa, EU338045; EU338155; EU338100;
258
Appendices
EU338209; Combretum kirkii M.A.Lawson, Palgrave 512 (JRAU), Mozambique, EU338052;
EU338162; EU338107; EU338216; Combretum kraussii Hochst., Maurin & van der Bank 36
(JRAU), South Africa, EU338024; EU338134; EU338079; EU338189; Combretum micranthum
G.Don, Slageren & Diallo 673 (K), Burkina Faso, FJ381759; FJ381793; FJ381832; FJ381868;
Combretum microphyllum Klotzsch, Maurin 205 (JRAU), South Africa, EU338020; EU338130;
EU338075; EU338185; Combretum mkuzense J.D.Carr & Retief, Maurin 1574 (JRAU), South
Africa, EU338054; EU338164; EU338109; EU338218; Combretum moggii Exell, Maurin 1585
(JRAU), South Africa, EU338035; EU338145; EU338090; EU338199; Combretum molle R.Br.
ex G.Don , Maurin 1571 (JRAU), South Africa, EU338036; EU338146; EU338091; EU338200;
Combretum molle R.Br. ex G.Don, Maurin 558 (JRAU), South Africa, EU338037; EU338147;
EU338092; EU338201; Combretum mossambicense (Klotzsch) Engl., Maurin 1011 (JRAU),
Namibia, EU338021; EU338131; EU338076; EU338186; Combretum nelsonii Dummer, van der
Bank 26 (JRAU), South Africa, EU338025; EU338135; EU338080; EU338190; Combretum
oxystachyum Welw. ex M.A.Lawson, Maurin 1052 (JRAU), Namibia, EU338017; EU338127;
EU338072; EU338182; Combretum padoides Engl. & Diels, Maurin 1285 (JRAU), South Africa,
EU338046; EU338156; EU338101; EU338210; Combretum paniculatum Vent., Maurin & van
der Bank 16 (JRAU), South Africa, EU338022; EU338132; EU338077; EU338187; Combretum
petrophilum Retief, Maurin & van der Bank 31 (JRAU), South Africa, EU338038; EU338148;
EU338093; EU338202; Combretum platypetalum Welw. ex M.A.Lawson, Maurin 1020 (JRAU),
Namibia, EU338014; EU338124; EU338069; EU338179; Combretum platypetalum Welw. ex
M.A.Lawson, Maurin 1658 (JRAU), Zimbabwe, EU338015; EU338125; EU338070; EU338180;
Combretum psidioides Welw. subsp. dinteri (Schinz) Exell, Maurin 1039 (JRAU), Namibia,
EU338039; EU338149; EU338094; EU338203; Combretum sp. nov. A, Winter 7225 (PRE),
South Africa, FJ381757; FJ381791; FJ381830; FJ381866; Combretum sp. nov. B, Maurin 997
(JRAU), South Africa, EU338059; EU338169; EU338114; EU338222; Combretum sp. C, Boon
3174 (PRE), South Africa, FJ381758; FJ381792; FJ381831; FJ381867; Combretum sp. nov. E,
259
Appendices
Bryden 154 (JRAU), South Africa, EU338053; EU338163; EU338108; EU338217; Combretum
tenuipes Engl. & Diels, Maurin 1089 (JRAU), South Africa, EU338047; EU338157; EU338102;
EU338211; Combretum wattii Exell, Maurin 995 (JRAU), Namibia, EU338016; EU338126;
EU338071; EU338181; Combretum woodii Dummer, Maurin 1421 (JRAU), South Africa,
EU338027; EU338137; EU338082; EU338192; Combretum zeyheri Sond., Maurin 1041
(JRAU), Namibia, EU338056; EU338166; EU338111; EU338220; Conocarpus erectus L.,
AY050562; —; AF425700; —; Conocarpus sericeus (Griseb.) Jimenez, Maurin 1668 (JRAU),
Cult., FJ381784; FJ381822; FJ381860; FJ381894; Guiera senegalensis J.F.Gmel., Daramola 233
(K), West tropical Africa, FJ381769; FJ381803; FJ381840; FJ381876; Laguncularia racemosa
(L.) C.F.Gaertn., PrinzieTh 132 (MO), US Florida, —; FJ381826; FJ381863; —; Laguncularia
racemosa (L.) C.F.Gaertn., Taylor, C.M. 11787 (MO), Puerto Rico, FJ381787; FJ381825; —; —;
Lumnitzera littorea Voigt, AF160468; AF425718; AF425704; —; Lumnitzera racemosa Willd.,
Maurin 1675 (JRAU), South Africa, —; FJ381827; FJ381864; FJ381897; Meiostemon humbertii
(H.Perrier) Exell & Stace, Phillipson 2870 (K), Madagascar, FJ381760; FJ381794; FJ381833; —
; Meiostemon tetrandrus (Exell) Exell & Stace, Maurin 1653 (JRAU), Zimbabwe, EU338012;
EU338122; EU338067; EU338177; Pteleopsis anisoptera (Welw. ex. M.A.Lawson) Engl. &
Diels, Maurin 1656 (JRAU), Zimbabwe, EU338005; EU338115; EU338060; EU338170;
Pteleopsis myrtifolia (M.A.Lawson) Engl. & Diels, Maurin & van der Bank 17 (JRAU), South
Africa, EU338006; EU338116; EU338061; EU338171; Pteleopsis myrtifolia (M.A.Lawson)
Engl. & Diels, Maurin & van der Bank 19 (JRAU), South Africa, EU338007; EU338117;
EU338062; EU338172; Quisqualis caudata Craib, AF160469; AF425706; AF425689; —.
Quisqualis indica L., Maurin 1669 (JRAU), Cult., FJ381764; FJ381798; FJ381836; FJ381872;
Quisqualis littorea (Engl.) Exell, Maurin & van der Bank 30 (JRAU), Cult., EU338013;
EU338123; EU338068; EU338178; Quisqualis parviflora Gerr. ex Harv. & Sond., Abbott 8891
(JRAU), South Africa, FJ381765; FJ381799; FJ381837; FJ381873; Strephonema mannii Hook f.,
Sainge, M. & P. Mambo 807 (MO), Cameroon, FJ381785; FJ381823; FJ381861; FJ381895;
260
Appendices
Strephonema pseudocola A.Chev., Sainge, M. & P. Mambo 823 (MO), Cameroon, FJ381786;
FJ381824; FJ381862; FJ381896; Terminalia arjuna Wight & Arn., Maurin 1671 (JRAU), Cult.,
FJ381783; FJ381821; FJ381859; FJ381893; Terminalia bellirica (Gaertn.) Roxb., Maurin 1673
(JRAU), Cult., FJ381773; FJ381808; FJ381845; FJ381879; Terminalia brachystemma Welw. ex
Hiern subsp. brachystemma, Maurin & van der Bank 18 (JRAU), South Africa, FJ381774;
FJ381810; FJ381847; FJ381881; Terminalia catappa L., Archer 2941 (PRE), Madagascar, —;
FJ381811; FJ381848; FJ381882; Terminalia chebula Willd. ex Flem., Annable 3580 (BISH),
Philippines, FJ381775; FJ381812; FJ381849; FJ381883; Terminalia hainanensis Exell.,
AF160466; AY050563; AF425694; —; Terminalia ivorensis A.Chev., Annable & Canham 3718
(BISH). Nigeria, FJ381776; FJ381813; FJ381850; FJ381884; Terminalia kaernbachii Warb.,
Kampong 3179 (BISH), Cult., —; —; FJ381851; FJ381885; Terminalia litoralis Seem Miller &
Merelo 7911 (BISH). Tonga, FJ381777; FJ381814; FJ381852; FJ381886; Terminalia mantaly
H.Perrier, Maurin 1088 (JRAU), Cult., FJ381778; FJ381815; FJ381853; FJ381887; Terminalia
mollis M.Lawson, Maurin & van der Bank 15 (JRAU), South Africa, EU338008; EU338118;
EU338063; EU338173; Terminalia muelleri Benth., AF160472; AF425712; AF425697; —;
Terminalia myriocarpa Van Heurck & Müll.Arg., Lyon s.n., Cult., FJ381779; FJ381816;
FJ381854; FJ381888; Terminalia phanerophlebia Engl. & Diels, Maurin 1179 (JRAU), South
Africa, EU338009; EU338119; EU338064; EU338174; Terminalia prunioides M.Lawson,
Maurin 327 (JRAU), South Africa, EU338010; EU338120; EU338065; EU338175; Terminalia
sambesiaca Engl. & Diels, Maurin & van der Bank 20 (JRAU), South Africa, FJ381780;
FJ381817; FJ381855; FJ381889; Terminalia sericea Burch. ex DC., Maurin 478 (JRAU), South
Africa, EU338011; EU338121; EU338066; EU338176; Terminalia stenostachya Engl. & Diels,
Maurin 1665 (JRAU), Cult., —; FJ381818; FJ381856; FJ381890; Terminalia stuhlmannii Engl.,
Zimba, N.B. et al. 899 (MO), Zambia, —; FJ381809; FJ381846; FJ381880; Terminalia
tomentosa (Roxb.) Wight & Arn., Maurin 1667 (JRAU), Cult., FJ381781; FJ381819; FJ381857;
FJ381891; Terminalia trichopoda Diels, Maurin 1657 (JRAU), Cult., FJ381782; FJ381820;
261
Appendices
FJ381858; FJ381892; Thiloa glaucocarpa Eichler, Giulietti et all. H51200 (K), Brasil, FJ381768;
FJ381802; —; —. Cryperoniaceae. Alzatea verticillata Ruiz & Pav.,—; AVU26316; —; —.
Olinia vanguerioides Baker f., — AM235626; —; —. Escalloniaceae. Escallonia pulverulenta
Pers., —; AJ419696; —; —. Geraniaceae. Erodium gruinum (L.) L'Hér., —; DQ452874; —; —
.Lauraceae. Laurus nobilis L., —; AY841668; —; —. Lamiaceae. Teucridium parvifolium
Hook.f., —; TPU78715; —; —. Lythraceae. Cuphea llavea Lindl., —; AF495773; —; —;
Galpinia transvaalica N.E.Br., —; AY905409; —; —. Lythrum salicaria L., —; AF495760; —;
—; Punica granatum L., —; PUGRBCLX; —; —. Malvaceae. Abroma augustum L.f., —;
AJ012208; —; —; Theobroma cacao L., —; AF022125; —; —. Melastomataceae. Melastoma
beccarianum Cogn., —; AM235646; —; —. Myrtaceae. Eugenia uniflora L., —; AM235654;
—; —; Heteropyxis natalensis Harv., —; AM235662; —; —. Leptospermum scoparium
J.R.Forst. & G.Forst., —; AM235656; —; —; Melaleuca alternifolia Cheel, —; AM235658; —;
—; Psiloxylon mauritianum Thou. ex Benth., —; AM235663; —; —. Onagraceae. Camissonia
boothii (Douglas) P.H.Raven, —; AF495766; —; —; Clarkia xantiana A.Gray, —;
CLRRBCLX; —; —; Ludwigia peploides (Kunth) P.H.Raven, —; LUDRBCLY; —; —;
Oenothera macrocarpa Pursh, —; AM235671; —; —. Vochysiaceae. Erisma floribundum
Rudge, —; EFU26324; —; —; Qualea Aubl., —; U02730; —; —; Ruizterania albiflora
(Warm.) Marc.-Berti, —; AM235664; —; —; Vochysia tucanorum Mart.,—; AM235665; —; —.
Zygophyllaceae. Zygophyllum cordifolium L.f.,—; EF655993; —; —.
262
Appendices
APPENDIX 3.1 Voucher information and GenBank accession numbers for taxa used in this study. Voucher specimens
are deposited in the following herbaria: JRAU = University of Johannesburg (UJ), Johannesburg, South Africa.
psbA-trnH.
Combretum erythrophyllum (Burch.) Sond., Maurin 201 (JRAU), South Africa, EU338023;
EU338133; EU338078; EU338188; Combretum caffrum (Eckl. & Zeyh.) Kuntze, Maurin & van
der Bank 11 (JRAU), South Africa, EU338057; EU338167; EU338112; EU338221; Combretum
celastroides Welw. ex M.A.Lawson subsp. celastroides, Maurin & van der Bank 28 (JRAU),
South Africa, EU338042; EU338152; EU338097; EU338206; Combretum edwardsii Exell,
Maurin 1584 (JRAU), South Africa, EU338034; EU338144; EU338089; EU338198;
Combretum engleri Schinz, Maurin 1025 (JRAU), Namibia, EU338051; EU338161; EU338106;
EU338215; Combretum imberbe Wawra, Maurin 1012 (JRAU), Namibia, EU338044;
EU338154; EU338099; EU338208; Combretum kirkii M.A.Lawson, Palgrave 512 (JRAU),
Mozambique, EU338052; EU338162; EU338107; EU338216; Combretum kraussii Hochst.,
EU338189; Combretum mkuzense J.D.Carr & Retief, Maurin 1574 (JRAU), South Africa,
EU338054; EU338164; EU338109; EU338218; Combretum molle R.Br. ex G.Don , Maurin
1571 (JRAU), South Africa, EU338036; EU338146; EU338091; EU338200; Combretum nelsonii
Dummer, van der Bank 26 (JRAU), South Africa, EU338025; EU338135; EU338080;
EU338190; Combretum nwambyana O.Maurin, M.Jordaan & A.E.van Wyk, Bryden 154 (JRAU),
South Africa, EU338053; EU338163; EU338108; EU338217; Combretum vendae A.E.van Wyk,
Maurin & van der Bank 9 (JRAU), South Africa, EU338026; EU338136; EU338081; EU338191;
Combretum woodii Dummer, Maurin 1421 (JRAU), South Africa, EU338027; EU338137;
EU338082; EU338192; Combretum zeyheri Sond., Maurin 1041 (JRAU), Namibia, EU338056;
EU338166; EU338111; EU338220.
263
Appendices
APPENDIX 3.2 Characters, character states, and explanatory notes on characters used in the cladistic analyses of the
morphological data matrix
1. Habitat: 0= forest; 1= savanna or woodland.
2. Climate: 0= humid; 1= dry.
3. Habit: 0= tree; 1= shrub; 2= liana.
4: Bark (on trunk or older stems): 0= smooth; 1= flaking.
5: Branchlets (first-formed bark): 0= smooth; 1= peeling longitudinally; fibrous; 2= peeling in
cylindrical or semi-cylindrical pieces.
6: Young branches (hairiness): 0= glabrous; 1= tomentose to hairy.
7: Leaf apex: 0= apiculate; 1= not apiculate.
8: Leaf margin(1): 0= Flat or slightly wavy; 1= Conspicuously wavy.
9: Leaf margin(2): 0= smooth; 1= ciliate.
10: Leaf spring colour: 0= leaves fresh green; 1= upper surface of the first leaves creamcoloured.
11: Leaf autumn colour: 0= most leaves yellowish, sometimes slightly red-tinged; 1= most
leaves turning red-tinged to brownish.
12: Combretaceous hairs on lamina surface (abaxial): 0= glabrous or sparsely hairy; 1=
densely hairy.
13: Principal laterals veins (abaxial): 0= plane; 1= raised.
14: Reticulation (abaxial): 0= plane or slightly raised; 1= prominently raised.
15: Leaf scales size: 0= 0–50 µm; 1= 51–100 µm; 2= 101–200 µm.
16: Number of cells per leaf scale: 0= 8–16; 1= 17–50; 2= 51–100; 3= >100.
17: Leaf scales; shape (margin): 1= scalloped; 2= irregular.
18: Leaf scales; type of walls: 0= primary radials walls; 1= primary and secondary radial and/or
tangential walls.
264
Appendices
19: Leaf scales; density: 0= very sparse, sometimes seemingly absent; 1= dense but not
contiguous.
20: Scales glistening (lustrous shine): 0= usually not glistening; 1= mostly glistening.
21: Hairtuft domatia in junctures of veins (abaxial): 0= absent; 1= present.
22: Inflorescence shape: 0= capitate to sub-capitate; 1= short spikes.
23: Flower; calyx lobes (outside): 0= greenish; 1= partly to completely tinged reddish purple.
24: Flower; lower receptacle: 0= glabrous; 1= hairy to tomentose.
25: Flower; disk margin (1): 0= shortly free or not free; 1= margin free.
26: Flower; disk margin (2): 0= glabrous; 1= pilose.
27: Fruits; colour when mature, but not yet dry: 0= greenish yellow, tinged pink to dark red,
or uniformly pink to dark red; 1= greenish yellow not conspicuously tinged pink or red.
28: Fruit size (longest dimension): 0= 0–20 mm; 1= 21–40; 2=>40 mm.
29: Fruit hairiness (“pod part”): 0= not hairy; 1= hairy.
30: Fruit glutinous secretions: 0= not present; 1= present.
31: Cotyledons (1); position in seedlings: 0= arising above soil level; 1= arising at or below soil
level.
32: Cotyledons (2); distinct or fused : 0= not fused; 1= fused forming a peltate structure.
265
Appendices
APPENDIX 3.3 Character states for the 32 morphological characters scored for accessions included in the molecular analyses. See appendix 3.2. for character definition.
TAXA
Combretum caffrum (Eckl. &
CHARACTER STATES
0
0
0
0
0
0
1
0
1
0
1
0/1
1
1
0
0
Combretum edwardsii Exell
0
0
0/2
0
0/1
1
1
Combretum engleri Schinz
1
0
1
0
1
1
1
0
0
0
0
Combretum imberbe Wawra
1
0
0
1
Combretum kirkii M.A.Lawson
1
0
2
Combretum kraussii Hochst.
0
0
Combretum molle R.Br. ex
1
0
1
1
0
0
0
?
0
0
0
1
1
1
0
1
1
0
1
0
0
0
1
0
0
0
0
0
0/1
1
0
3
3
0
1
1
0
0
1
?
0
0
1
1
0
1
0
?
0
0
0
0
1
0
1
0
1
1
0
1
1
0
0
1
?
1
0
1
0
0
0
0
0
0
0
1
½
0
0
0
1
0
0/1
0/1
0
1
1
0
1
0/1
?
0
0
0
1
1
0
1
?
0
1
1
0
1
1
1
1
1
0
0/1
0
0
0
1
1
1
0
1
1
0
1
1
0
1
0
0
0
0
0
0
1
0
0
0
0
0
0
3
3
0
1
1
0
0
1
?
0
0
1
1
0
0
0
1
0
1
1
0
0
0
1
0
0
0
0
0
1
1
0
1
1
0
0
1
?
0
0
1
1
1
0
1
0
0
0
0
1
1
1
1
0
1
1
0
0
0
0/1
0
0
0
1
1
1
1
1
1
0
1
0
0
1
1
0
0
0
0
1
0
1
1
0
1
0
1
1
1
1
2
0
0
1
1
0
0
1
?
1
0
1
0
0
0
0
1
0
1
0
1/2
0
0
1
1
0
0
0
0
0
1
0
0
1
0/1
1
1
1
1
1
?
1
?
?
1
1
1
0
0
0
Combretum nelsonii Dummer
1
0
1
0
0
0
1
0/1
0
1
1
0
0
0
0/1
0
0
0
1
1
0
0
1
1
0
1
0
0
0
1
?
0
1
0
1/2
0
?
?
?
?
?
?
?
?
?
?
0
1
0/1
1
1
?
0
?
?
?
?
?
1
1
?
?
1
0
1
0
1
0
1
1
0
0
0
1
1
1
1
1
0/1
0
0
0
1
1
0
0
1
1
0
1
0
0
1
1
0
0
Combretum woodii Dummer
0/1
0
0/2
0
1
0
1
1
0
1
1
0
0
0
0/1
0
0
0
1
1
1
1
1
1
0
1
0
0
0
1
0
0
Combretum zeyheri Sond.
1
0
0
0
1
1
0
0/1
1
0
0
1
1
0
0
0/1
0
1
1
0
1
1
?
1
1
1
1
1
0
0
0/1
1
Zeyh.) Kuntze.
Combretum celastroides Welw.
ex M.A.Lawson
(Burch.) Sond.
G.Don
Combretum mkuzense J.D. Carr
& Retief
Maurin et al.
Combretum vendae A.E.van
Wyk
266
Appendices
deposited in the following herbaria: JRAU = University of Johannesburg (UJ), Johannesburg, South Africa; PRE =
South African National Botanical Institute, Pretoria, South Africa; MO = Missouri Botanical Garden, St. Louis,
U.S.A.
psbA-trnH.
Combretum albopunctatum Suess., Maurin 1038 (JRAU), Namibia, EU338031; EU338141;
EU338086; EU338196; Combretum apiculatum Sond. subsp. apiculatum, Lahaye 1355 (JRAU),
South Africa, EU338032; EU338142; EU338087; EU213796; Combretum apiculatum Sond.
subsp. leutweinii (Schinz) Exell , Maurin 1015 (JRAU), Namibia, EU338033; EU338143;
EU338088; EU338197; Combretum edwardsii Exell, Maurin 1584 (JRAU), South Africa,
EU338034; EU338144; EU338089; EU338198; Combretum fragrans F.Hoffm., Slageren &
Sanou 866 (K), Burkina Faso, FJ381754; FJ381788; —; —; Combretum micranthum G.Don,
Slageren & Diallo 673 (K), Burkina Faso, FJ381759; FJ381793; FJ381832; FJ381868;
Combretum moggii Exell, Maurin 1585 (JRAU), South Africa, EU338035; EU338145;
EU338090; EU338199; Combretum molle R.Br. ex G.Don , Maurin 1571 (JRAU), South
Africa, EU338036; EU338146; EU338091; EU338200; Combretum molle R.Br. ex G.Don,
Maurin 558 (JRAU), South Africa, EU338037; EU338147; EU338092; EU338201; Combretum
petrophilum Retief, Maurin & van der Bank 31 (JRAU), South Africa, EU338038; EU338148;
EU338093; EU338202; Combretum psidioides Welw. subsp. dinteri (Schinz) Exell, Maurin
1039 (JRAU), Namibia, EU338039; EU338149; EU338094; EU338203; Combretum sp. nov. A,
Winter 7225 (PRE), South Africa, FJ381757; FJ381791; FJ381830; FJ381866; Combretum sp.
C, Boon 3174 (PRE), South Africa, FJ381758; FJ381792; FJ381831; FJ381867; Combretum
stylesii, Maurin 997 (JRAU), South Africa, EU338059; EU338169; EU338114; EU338222;
Combretum vendae A.E.van Wyk, Maurin & van der Bank 9 (JRAU), South Africa, EU338026;
EU338136; EU338081; EU338191; Combretum zeyheri Sond., Maurin 1041 (JRAU), Namibia,
267
Appendices
EU338056; EU338166; EU338111; EU338220; Meiostemon tetrandrus (Exell) Exell & Stace,
Maurin 1653 (JRAU), Zimbabwe, EU338012; EU338122; EU338067; EU338177.
268
Appendices
APPENDIX 4.2 Characters, character states, and explanatory notes on characters used in the cladistic analyses of the
morphological data matrix.
1. Habitat: 0=forest; 1=savanna or woodland.
2. Climate: 0=humid; 1=dry.
3. Habit: 0=tree; 1=shrub; 2=liana.
4: Bark (on trunk or older stems): 0=smooth; 1=flaking.
5: Branchlets (first-formed bark): 0=smooth; 1=peeling longitudinally, fibrous; 2=peeling in
cylindrical or semi-cylindrical pieces.
6: Young branches (hairiness): 0=glabrous; 1=tomentose to hairy.
7: Leaf apex: 0=apiculate; 1=not apiculate.
8: Leaf margin (1): 0=flat or slightly wavy; 1=conspicuously wavy.
9: Leaf margin (2): 0=smooth; 1=ciliate.
10: Leaf autumn colour: 0=most leaves yellowish, sometimes slightly red-tinged; 1=most
leaves turning orange or red-tinged to brownish.
11: Combretaceous hairs on lamina surface (abaxial): 0=glabrous or sparsely hairy;
1=densely hairy.
12: Principal laterals veins (abaxial): 0=plane; 1=raised.
13: Reticulation (abaxial): 0=plane or slightly raised; 1=prominently raised.
14: Leaf scales size: 0=0–50 µm; 1=51–100 µm; 2=101–200 µm.
15: Number of cells per leaf scale: 0=8–16; 1=17–50; 2=51–100; 3= >100.
16: Leaf scales shape (margin): 0=scalloped; 1=irregular.
17: Leaf scales; type of walls: 0=primary radials walls only; 1=primary and secondary radial
and/or tangential walls.
18: Leaf scales density: 0=very sparse, sometimes seemingly absent; 1=dense but not
contiguous.
19: Scales glistening (lustrous shine): 0=usually not glistening; 1=mostly glistening.
269
Appendices
20: Hairtuft domatia in axils of veins (abaxial): 0=absent; 1=present.
21: Inflorescence shape: 0=capitate to subcapitate; 1=short spikes.
22: Flower; disc margin: 0=free; 1=not free margin.
23: Flower; petals hairiness at apex: 0=glabrous; 1=ciliate.
24: Fruits; colour when mature, but not yet dry: 0=greenish yellow, flushed with pink to
dark red, or uniformly dark pink to dark red brown; 1=uniformly greenish yellow not
conspicuously tinged pink or red.
25: Fruit size (longest dimension): 0= <20 mm; 1= >20 mm.
26: Fruit hairiness (“pod part”): 0=glabrous; 1=hairy.
27: Fruit glutinous secretions ( at least when young): 0=not present; 1=present.
28: Cotyledons; position in seedlings: 0=arising above soil level; 1=arising at or below soil
level.
270
Appendices
APPENDIX 4.3 Character states for 28 morphological characters scored for accessions included in the molecular analyses. See appendix 4.2. for character definitions.
TAXA
CHARACTER STATES
Combretum albopunctatum Suess
1
1
1
1 1
1
1
0
0
0
0
1
1
1
0
0
0/1
1
1
0
1
0
1
0
0
0
1
0
Combretum apiculatum Sond. subsp. apiculatum
1
1
0
1 1
1
0
1/2
0
0
0
1
0
1
0
0
1
1
0
1
1
0
1
0
1
0
1
1
Combretum apiculatum Sond. subsp. leutweinii
1
1
0
1 1
1
0
1
0
0
1
1
1
1
0
0
1
1
0
1
1
0
1
0
1
1
0
1
Combretum edwardsii Exell
0
0
2
1 1
1
1
0
0
1
0
1
0
1
1/2
0
1
1
0
0
1
1
1
0
0/1
0
0
0
Combretum fragrans F.Hoffm.
1
1
0
1 1
0
1
0
0
1
0
1
0
1
0
1
0
1
1
0
1
0
0
0
1
0
1
1
Combretum micranthum G.Don
?
0
1
?
?
?
?
?
?
?
?
?
?
0
0
0
0
0/1
0
1
0
?
?
?
?
?
?
?
Combretum moggii Exell
1
1
1
1 1
1
1
0
1
1
1
1
0
1/2
1
0
1
1
0
0
0
0
1
0
0
1
0
0
Combretum molle R.Br. ex G.Don
1
1
0
1 1
1
1
0
1
1
1
1
1
2
0
0
1
1
0
0
1
0
1
0
0
0
0
1
Combretum petrophilum Retief
1
1
1
0 1
0
0
1
1
0
0
0
0
1
0
0
0
0
1
0
0
0
0
0
0
0
1
0
Combretum psidioides Welw. subsp. dinteri
1
1
0
1 2
1
1
0
1
0
1
1
1
0
0
0
1
1
0
0
1
0
1
0
1
1
1
1
Combretum stylesii Maurin et al.
1
1
2
0 0
1
1
1/2
1
1
0
1
0
0
0
0
0
1
0
0
0
?
1
0
0
0
0
?
Combretum sp. A
1
1
1
0 0
1
1
0
1
0
0
1
0
0
?
?
?
?
?
0
?
?
?
0
0
0
0
?
Combretum sp. B
0
1
0/2
?
1
0
1
0
1
1
0
0
0
?
?
?
?
0
0
0
?
?
?
1
1/0
0
0
?
Combretum vendae A.E.van Wyk
1
1
1
0 1
1
0
0
0
1
1
1
1
1
0
0
0
1
0
0
0
0
0
0
0
1
0
0
Combretum zeyheri Sond.
1
1
0
1 1
1
1
0
0
0
0
1
1
0/1
0
0
1
1
0
1
1
?
0
1
1
0
0
0
Meiostemon tetrandrus (Exell) Exell & Stace
1
1
1
0 2
0
1
0
1
1
0
1
0
0
0
0
0
0/1
0
1
1
0
0
0
0
0
0
0
(Schinz) Exell
(Schinz) Exell
271
Appendices
deposited in the following herbaria: BISH = Bishop Museum, Honolulu, U.S.A.; JRAU = University of
Johannesburg (UJ), Johannesburg, South Africa; K = Royal Botanic Gardens, Kew Richmond, United Kingdom;
PRE = South African National Botanical Institute, Pretoria, South Africa; MO = Missouri Botanical Garden, St.
Louis, U.S.A; Taxa distribution is mentioned, and for voucher use as for the large rbcL analysis, distribution is for
the genus.
Family. Taxon — Voucher (Herbarium), Distribution, GenBank accession no.: ITS, rbcL,psaA-ycf3, psbA-trnH.
Alzateaceae. Alzatea verticillata Ruiz & Pav., center and north of South America ,—;
AVU26316; —; —. Brassicaceae, Arabidopsis thaliana (L.) Heynh., north temperate,—;
NC003074; —; —.Combretaceae. Anogeissus acuminata Wall., Thailand, Vietnam, AF334765;
AF425708; AF425692; —; Anogeissus leiocarpa Guill. & Perr., Africa, north of the Equator,
AF334766; AF425709; AF425693; —; Buchenavia reticulata Eichler, van der Werff H. &
R.Vasquez 13866 (MO), north of South America, FJ381770; FJ381804; FJ381841; FJ381877;
Buchenavia tetraphylla (Aubl.) R.A.Howard, Taylor, C.M. 11671 (MO), north of South America,
—; FJ381805; FJ381842; —; Bucida buceras L. Harder, D.K. & M. Merello 1184 (MO),Center
America and Florida, FJ381771; FJ381806; FJ38184; FJ572675; Bucida buceras L. Maurin 1670
(JRAU), Center America and Florida, FJ381772; FJ381807; FJ381844; FJ381878; Calopyxis
grandidieri (Drake) Capuron ex Stace, Phillipson & Rabesihanaka 3147 (K), Madagascar,
FJ381762; FJ381796; —; FJ381870; Calopyxis grandidieri (Drake) Capuron ex Stace, Willing
s.n. (K), Madagascar, FJ381761; FJ381795; FJ381834; FJ381869; Calycopteris floribunda
(Roxb.) Lam. ex Poir., tropical Asia, AF334770; —; AF425691; —; Combretum albopunctatum
Suess., Maurin 1038 (JRAU), Southern Africa, EU338031; EU338141; EU338086; EU338196;
Combretum apiculatum Sond. subsp. apiculatum, Lahaye 1355 (JRAU), Southern Africa,
EU338032; EU338142; EU338087; EU213796; Combretum apiculatum Sond. subsp. leutweinii
(Schinz) Exell , Maurin 1015 (JRAU), Southern Africa, EU338033; EU338143; EU338088;
EU338197; Combretum bracteosum (Hochst.) Brandis Maurin & van der Bank 22 (JRAU),
South Africa, EU338018; EU338128; EU338073; EU338183; Combretum caffrum (Eckl. &
272
Appendices
Zeyh.) Kuntze, Maurin & van der Bank 11 (JRAU), South Africa, EU338057; EU338167;
EU338112; EU338221; Combretum celastroides Welw. ex M.A.Lawson subsp. celastroides,
Maurin & van der Bank 28 (JRAU), Southern Africa, EU338042; EU338152; EU338097;
EU338206; Combretum celastroides Welw. ex M.A.Lawson subsp. orientale Exell, Maurin &
van der Bank 27 (JRAU), Southern Africa, EU338043; EU338153; EU338098; EU338207;
Combretum coccineum Engl. & Diels, Archer 2972 (PRE), Madagascar, FJ381766; FJ381800;
FJ381838; FJ381874; Combretum collinum Fresen., Maurin 1524 (JRAU), Southern Africa,
EU338041; EU338151; EU338096; EU338205; Combretum collinum Fresen. subsp. gazense
(Swynn. & Baker f.), Maurin 1024 (JRAU), Southern Africa, EU338048; EU338158; EU338103;
EU338212; Combretum collinum Fresen. subsp. suluense (Engl. & Diels) Okafor, Maurin & van
der Bank 34 (JRAU), Southern Africa, EU338049; EU338159; EU338104; EU338213;
Combretum collinum Fresen. subsp. taborense (Engl.) Okafor, Bryden 170 (JRAU), Southern
Africa, EU338050; EU338160; EU338105; EU338214; Combretum collinum Fresen. subsp.
hypopilinum (Diels) Okafor, Sanou 004 (K), west and east Africa, FJ381756; FJ381790;
FJ381829; FJ381865; Combretum edwardsii Exell, Maurin 1584 (JRAU), South Africa,
EU338034; EU338144; EU338089; EU338198; Combretum elaeagnoides Klotzsch, Maurin
1021 (JRAU), Southern Africa, EU338040; EU338150; EU338095; EU338204; Combretum
engleri Schinz, Maurin 1025 (JRAU), Southern Africa, EU338051; EU338161; EU338106;
EU338215; Combretum erythrophyllum (Burch.) Sond., Maurin 201 (JRAU), Southern Africa,
EU338023; EU338133; EU338078; EU338188; Combretum fragrans F.Hoffm., Slageren &
Sanou 866 (K), west and east Africa FJ381754; FJ381788; —; —; Combretum glutinosum Perr.
ex DC., Slageren & Sanou 854 (K), west and center Africa, FJ381755; FJ381789; FJ381828; —;
Combretum goldieanum F.Muell., P.Hayers FL-1125 (BISH), New Guinea, FJ381767;
FJ381801; FJ381839; FJ381875; Combretum grandiflorum G.Don, P.C. Hutchinson 2849
273
Appendices
(BISH), west tropical Africa, FJ381763; FJ381797; FJ381835; FJ381871; Combretum
hereroense Schinz, Maurin 238 (JRAU), Southern Africa, EU338028; EU338138; EU338083;
EU338193; Combretum holstii Engl., Palgrave 504 (JRAU), Southern Africa, EU338019;
EU338129; EU338074; EU338184; Combretum imberbe Wawra, Maurin 1012 (JRAU),
Southern and Eastern Africa, EU338044; EU338154; EU338099; EU338208; Combretum
imberbe Wawra, Lahaye 1380 (JRAU), Southern and Eastern Africa, EU338045; EU338155;
EU338100; EU338209; Combretum kirkii M.A.Lawson, Palgrave 512 (JRAU), Southern and
Eastern Africa, EU338052; EU338162; EU338107; EU338216; Combretum kraussii Hochst.,
Maurin & van der Bank 36 (JRAU), Southern Africa, EU338024; EU338134; EU338079;
EU338189; Combretum micranthum G.Don, Slageren & Diallo 673 (K), west Africa, FJ381759;
FJ381793; FJ381832; FJ381868; Combretum microphyllum Klotzsch, Maurin 205 (JRAU),
Southern and Eastern Africa, EU338020; EU338130; EU338075; EU338185; Combretum
mkuzense J.D.Carr & Retief, Maurin 1574 (JRAU), South Africa, EU338054; EU338164;
EU338109; EU338218; Combretum moggii Exell, Maurin 1585 (JRAU), South Africa,
EU338035; EU338145; EU338090; EU338199; Combretum molle R.Br. ex G.Don , Maurin
1571 (JRAU), Africa, EU338036; EU338146; EU338091; EU338200; Combretum molle R.Br.
ex G.Don, Maurin 558 (JRAU), Africa, EU338037; EU338147; EU338092; EU338201;
Combretum mossambicense (Klotzsch) Engl., Maurin 1011 (JRAU), Southern and Eastern Africa,
EU338021; EU338131; EU338076; EU338186; Combretum nelsonii Dummer, van der Bank 26
(JRAU), South Africa, EU338025; EU338135; EU338080; EU338190; Combretum oxystachyum
Welw. ex M.A.Lawson, Maurin 1052 (JRAU), Southern Africa, EU338017; EU338127;
EU338072; EU338182; Combretum padoides Engl. & Diels, Maurin 1285 (JRAU), Southern and
Eatern Africa, EU338046; EU338156; EU338101; EU338210; Combretum paniculatum Vent.,
Maurin & van der Bank 16 (JRAU), Africa, EU338022; EU338132; EU338077; EU338187;
274
Appendices
Combretum petrophilum Retief, Maurin & van der Bank 31 (JRAU), South Africa, EU338038;
EU338148; EU338093; EU338202; Combretum platypetalum Welw. ex M.A.Lawson, Maurin
1020 (JRAU), Southern Africa, EU338014; EU338124; EU338069; EU338179; Combretum
platypetalum Welw. ex M.A.Lawson, Maurin 1658 (JRAU), Southern Africa, EU338015;
EU338125; EU338070; EU338180; Combretum psidioides Welw. subsp. dinteri (Schinz) Exell,
Maurin 1039 (JRAU), Southern Africa, EU338039; EU338149; EU338094; EU338203.
Combretum sp. nov. A, Winter 7225 (PRE), South Africa, FJ381757; FJ381791; FJ381830;
FJ381866; Combretum sp. nov. B, Maurin 997 (JRAU), South Africa, EU338059; EU338169;
EU338114; EU338222; Combretum sp. C, Boon 3174 (PRE), South Africa, FJ381758;
FJ381792; FJ381831; FJ381867; Combretum sp. nov. E, Bryden 154 (JRAU), South Africa,
EU338053; EU338163; EU338108; EU338217; Combretum tenuipes Engl. & Diels, Maurin
1089 (JRAU), Southern and Eatsern Africa, EU338047; EU338157; EU338102; EU338211;
Combretum vendae A.E.van Wyk, Maurin & van der Bank 9 (JRAU), South Africa, EU338026;
EU338136; EU338081; EU338191; Combretum wattii Exell, Maurin 995 (JRAU), Southern
Africa, EU338016; EU338126; EU338071; EU338181; Combretum woodii Dummer, Maurin
1421 (JRAU), South Africa, EU338027; EU338137; EU338082; EU338192; Combretum zeyheri
Sond., Maurin 1041 (JRAU), Southern and Eastern Africa, EU338056; EU338166; EU338111;
EU338220; Conocarpus erectus L., American and African tropics, AY050562; —; AF425700;
—; Conocarpus sericeus (Griseb.) Jimenez, Maurin 1668 (JRAU), American and African tropics,
FJ381784; FJ381822; FJ381860; FJ381894; Guiera senegalensis J.F.Gmel., Daramola 233 (K),
West Africa, FJ381769; FJ381803; FJ381840; FJ381876; Laguncularia racemosa (L.)
C.F.Gaertn., PrinzieTh 132 (MO), American and African tropics, —; FJ381826; FJ381863; —;
Laguncularia racemosa (L.) C.F.Gaertn., Taylor, C.M. 11787 (MO), American and African
tropics, FJ381787; FJ381825; —; —; Lumnitzera littorea Voigt, Eastern Africa to Pacific,
275
Appendices
AF160468; AF425718; AF425704; —; Lumnitzera racemosa Willd., Maurin 1675 (JRAU),
Eastern Africa to western Pacific, —; FJ381827; FJ381864; FJ381897; Meiostemon humbertii
(H.Perrier) Exell & Stace, Phillipson 2870 (K), Madagascar, FJ381760; FJ381794; FJ381833; —
; Meiostemon tetrandrus (Exell) Exell & Stace, Maurin 1653 (JRAU), Zimbabwe, EU338012;
EU338122; EU338067; EU338177; Pteleopsis anisoptera (Welw. ex. M.A.Lawson) Engl. &
Diels, Maurin 1656 (JRAU), Africa, EU338005; EU338115; EU338060; EU338170; Pteleopsis
myrtifolia (M.A.Lawson) Engl. & Diels, Maurin & van der Bank 17 (JRAU), Africa, EU338006;
EU338116; EU338061; EU338171; Pteleopsis myrtifolia (M.A.Lawson) Engl. & Diels, Maurin
& van der Bank 19 (JRAU), Africa, EU338007; EU338117; EU338062; EU338172; Quisqualis
caudata Craib, Thailand AF160469; AF425706; AF425689; —. Quisqualis indica L., Maurin
1669 (JRAU), tropical Asia, FJ381764; FJ381798; FJ381836; FJ381872; Quisqualis littorea
(Engl.) Exell, Maurin & van der Bank 30 (JRAU), tropical Africa, EU338013; EU338123;
EU338068; EU338178; Quisqualis parviflora Gerr. ex Harv. & Sond., Abbott 8891 (JRAU),
South Africa, FJ381765; FJ381799; FJ381837; FJ381873; Strephonema mannii Hook f., Sainge,
M. & P. Mambo 807 (MO), west tropical Africa, FJ381785; FJ381823; FJ381861; FJ381895;
Strephonema pseudocola A.Chev., Sainge, M. & P. Mambo 823 (MO), west tropical Africa,
FJ381786; FJ381824; FJ381862; FJ381896; Terminalia arjuna Wight & Arn., Maurin 1671
(JRAU), India, FJ381783; FJ381821; FJ381859; FJ381893; Terminalia bellirica (Gaertn.) Roxb.,
Maurin 1673 (JRAU), tropical Africa, FJ381773; FJ381808; FJ381845; FJ381879; Terminalia
brachystemma Welw. ex Hiern subsp. brachystemma, Maurin & van der Bank 18 (JRAU),
Southern Africa, FJ381774; FJ381810; FJ381847; FJ381881; Terminalia catappa L., Archer
2941 (PRE), Madagascar to Pacific, —; FJ381811; FJ381848; FJ381882; Terminalia chebula
Willd. ex Flem., Annable 3580 (BISH), Asia, FJ381775; FJ381812; FJ381849; FJ381883;
Terminalia hainanensis Exell., China AF160466; AY050563; AF425694; —; Terminalia
276
Appendices
ivorensis A.Chev., Annable & Canham 3718 (BISH). west tropical Africa, FJ381776; FJ381813;
FJ381850; FJ381884; Terminalia kaernbachii Warb., Kampong 3179 (BISH), Papua New
Guinea, —; —; FJ381851; FJ381885; Terminalia litoralis Seem Miller & Merelo 7911 (BISH).
Pacific, FJ381777; FJ381814; FJ381852; FJ381886; Terminalia mantaly H.Perrier, Maurin 1088
(JRAU), Madagscar, FJ381778; FJ381815; FJ381853; FJ381887; Terminalia mollis M.Lawson,
Maurin & van der Bank 15 (JRAU), Africa, EU338008; EU338118; EU338063; EU338173;
Terminalia muelleri Benth., Australia, AF160472; AF425712; AF425697; —; Terminalia
myriocarpa Van Heurck & Müll.Arg., Lyon s.n., India, FJ381779; FJ381816; FJ381854;
FJ381888; Terminalia phanerophlebia Engl. & Diels, Maurin 1179 (JRAU), South Africa,
EU338009; EU338119; EU338064; EU338174; Terminalia prunioides M.Lawson, Maurin 327
(JRAU), Southern and Eastern Africa Africa, EU338010; EU338120; EU338065; EU338175;
Terminalia sambesiaca Engl. & Diels, Maurin & van der Bank 20 (JRAU), Southern and Eastern
Africa, FJ381780; FJ381817; FJ381855; FJ381889; Terminalia sericea Burch. ex DC., Maurin
478 (JRAU), Africa, EU338011; EU338121; EU338066; EU338176; Terminalia stenostachya
Engl. & Diels, Maurin 1665 (JRAU), Southern and Eastern Africa, —; FJ381818; FJ381856;
FJ381890; Terminalia stuhlmannii Engl., Zimba, N.B. et al. 899 (MO), Southern and Eastern
Africa, —; FJ381809; FJ381846; FJ381880; Terminalia tomentosa (Roxb.) Wight & Arn.,
Maurin 1667 (JRAU), India, FJ381781; FJ381819; FJ381857; FJ381891; Terminalia trichopoda
Diels, Maurin 1657 (JRAU), Southern and Eatern Africa, FJ381782; FJ381820; FJ381858;
FJ381892; Thiloa glaucocarpa Eichler, Giulietti et all. H51200 (K), South America, FJ381768;
FJ381802; —; —. Crypteroniaceae. Crypteronia paniculata Blume, South-east Asia, —;
AF215545 —; —.Heteropyxidaceae. Heteropyxis natalensis Harv.,Center and South Africa, —;
AF206775; —; —.Lythraceae Cuphea llavea Lex., America, —; AF495773; —; —. Lawsonia
inermis L., North Africa and Old Wold tropics, —; AY905413; —; —; Lythrum salicaria L.,
277
Appendices
cosmopolite, —; AF495760; —; —; Trapa natans L., cosmopolite, —; TAZRBCLX; —; —.
Malvaceae. Byttneria aculeata (Jacq.) Jacq., pantropical, —;AF022123; —; —; Tilia americana
L., temparate north, —; AF022127; —; —. Melastomataceae. Amphiblemma cymosum Naudin,
West Africa, —; AF215543; —; —; Arthrostemma ciliatum Pav. ex D.Don, tropical America,—;
AF215522; —; —; Astronia macrophylla Blume, Malysia to Pacuific, —;AF215510; —; —;
Bertolonia maculata DC., South America, —; AF215512; —; —; Dichaetanthera asperrima
Cogn., Tropical Africa, —; AF215523; —; —; Macrocentrum repens (Gleason) Wurdack,
Tropical and Southern America, —; AF215513; —; —; Melastoma malabathricum L.,Inde,
Malaysia to Pacific, —; AF270748; —; —; Monochaetum calcaratum (DC.) Triana, Tropical
America, —; —. AF215524; —; —; Osbeckia chinensis L., Old Woled tropics, —; AF215525;
—; —; Pternandra caerulescens Jack, Malaysia, —;AF215518; —; —; Rhexia virginica L.,
North America, —; RVU26334; —; —; Tibouchina urvilleana (DC.) Cogn., America, —;
TUU26339; —; —; Triolena obliqua (Triana) Wurdack, America, —; AF215515; —; —.
Memecylaceae Memecylon edule Roxb., Old World tropics, —; AF215528; —; —; Mouriri
cyphocarpa Standl., tropical America—; AF206796; —; —. Myrtaceae. Acmena DC., South
East Africa to Pacific, —; ASU26315; —; —; Angophora Cav., Australia, —; AHU26317; —;
—; Backhousia Hook. & Harv., Australia, —; BCU26318; —; —; Baeckea ramosissima A.Cunn.,
Australia, —; BRU26319; —; —; Eugenia uniflora L., world tropics ,—; AF294255; —; —;
Metrosideros nervulosa C.Moore & F.Muell., Malaysia, Pacific, South Africa, —; AJ235785; —;
—; Myrcianthes fragrans (Sw.) McVaugh, tropical America, —; MFU26328; —; —. Oliniaceae
Olinia ventosa (L.) Cufod., South Africa, —; AF215546; —; —.Onagraceae Calylophus
hartwegii (Benth.) P.H.Raven, America, —; AF495767; —; —; Camissonia boothii (Douglas)
P.H.Raven, Pacific, America, —; AF495766; —; —. Circaea alpina L., northern hemisphere, —;
CIZRBCLX; —; —; Gaura mutabilis Cav., northern hemisphere, —; AF495769; —; —;
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Appendices
Ludwigia peploides (Kunth) P.H.Raven, cosmopolite, —; LUDRBCLY; —; —; Xylonagra
arborea (Kellogg) Donn.Sm. & Rose, Center America, —; AF495764; —; —. Penaeaceae
Penaea mucronata L., South Africa, —; AY078155; —; —. Psiloxylaceae Psiloxylon Thouars
ex Tul., Indian ocean Islands, —; AM235663; —; —. Rhynchocalycaceae Rhynchocalyx
lawsonioides Oliv., South Africa, —; AF215547; —; —. Tropaeolaceae Tropaeolum majus L.,
Center and South America, —; TRUCPRBCL; —; —. Vochysiaceae Erisma Rudge, South
America, —; EFU26324; —; —; Qualea Aubl., tropical America, —; QSU02730; —; —;
Vochysia hondurensis Sprague, tropical America, —; VHU26340; —; —.
279
280
Annexes
ANNEXES
ANNEXE 1: Taxonomy and distribution of Quisqualis parviflora
Notes on African plants
COMBRETACEAE - TAXONOMY AND DISTRIBUTION OF QUISQUALIS PARVIFLORA
M. JORDAAN*†, A.E. VAN WYK** and O. MAURIN***
INTRODUCTION
Quisqualis L., a genus comprising ± 17 species, occurs in Africa, India and the Philippine Islands (Bredenkamp
2000). It shares a number of morphological similarities with Combretum Loefl. Subgenus Cacoucia (Aubl.) Exell &
Stace section Poivrea (Comm. ex DC.) G.Don. Locally C. mossambicense (Klotzsch) Engl. and C. bracteosum
(Hochst.) Brandis belong to this section. Quisqualis parviflora Gerrard ex Sond., the only southern African member
of the genus, as well as the latter two species of Combretum, are characterised by the absence of epidermal scales but
presence of long combretaceous hairs (sharp-pointed, thick-walled with a bulbous base) on the leaf lamina as well as
gland-tipped hairs on the petiole, midrib and lateral veins. Leaf surfaces in the aforementioned two species of
Combretum are densely covered with translucent gland dots and there are hairy domatia (pockets) in axils of the
principal side veins below in C. bracteosum, but these are not obvious in C. mossambicense. Leaves of Quisqualis
lack translucent gland dots and hairy domatia, but may have extrafloral nectaries (Tilney & Van Wyk 2004),
structures not yet recorded in Combretum. Furthermore, C. mossambicense, C. bracteosum and Quisqualis parviflora
all have hooked or straight spines derived from persistent petioles by means of which they climb in or over
vegetation. The flowers vary from white with long protruding stamens in C. mossambicense, bright red in C.
bracteosum, to greenish with included stamens in Quisqualis parviflora. C. mossambicense has 5-winged, softly
hairy fruits, but those of C. bracteosum are quite different in being wingless, hairless and indistinctly 5-angled nuts.
Quisqualis parviflora, according to Carr (1986), has 5-winged fruits. However, we could not find any
fruiting material of this species in South African herbaria and it is possible that Carr inferred the fruit morphology
from generic descriptions of the genus, the latter which are based mainly on non-African material. The 4-winged
fruit attributed to Quisqualis parviflora and depicted in plate 1925 of Flowering Plants of Africa (Carr 1986) is said
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to have come from Mariepskop, Mpumalanga. Considering the known distribution of this species in southern Africa
(Figure 1), the fruit most probably belonged to a member of Combretum and not to Quisqualis. Tony Abbott (pers.
comm.) has confirmed that he has not seen any fruits on this species in the Umtamvuna Nature Reserve for the last
30 years. As Carr (1986) states, even flowering seems to be a rare event, only a handful of flowering specimens
exists in South African herbaria. On the other hand, the paucity of flowering material in herbaria may well be due to
the fact that the flowers are inconspicuous and borne in the canopy of tall forest trees well out of the reach of plant
collectors. The flowering and reproductive behaviour of Q. parviflora is clearly in need of further investigation.
History of the genus Quisqualis
The genus Quisqualis was established by Linnaeus (1762). Engler & Diels (1899) recognised Quisqualis based on
the alleged presence of dehiscent fruit, compared to indehiscent fruit in Combretum. However, this character proved
not to be reliable because many species of Combretum have tardily dehiscent fruit. Hooker (1867) and Lawson
(1871) separated Quisqualis on the grounds of its tubular upper hypanthium, a state which is absent in Combretum.
Exell (1931) proposed a new delimitation of Quisqualis and Combretum based on the insertion of the style
in the upper hypanthium: if the style is adnate to the upper hypanthium it is a Quisqualis. Subsequently some
specimens from tropical Africa were found in which the style is very shortly adnate to the upper hypanthium, but in
other features, such as the presence of glandular scales on the leaves, they are clearly members of Combretum. To
avoid this ambiguity, Exell & Stace (1964, 1966) redefined Quisqualis and separated it from Combretum by a
combination of two characters: 1, adnation of the style to the upper hypanthium and 2, the non-exsertion of stamens
from the flower. Exell & Stace (1964) provided a useful key to distinguish between Quisqualis and Combretum.
Jongking (1991) proposed the amalgamation of Quisqualis with Combretum and formally transferred a number of
species to Combretum (Jongkind 1999). Stace (2007) and Mabberley (2008) follow Jongkind’s lumping of the two
genera.
Phylogeny
In provisional phylogenetic studies by Maurin et al. (2010), Quisqualis as a genus is recovered as a clade embedded
within Combretum subgenus Cacoucia. One of us (O.M.) supports Jongkind (1999), Stace (2007) and Mabberley
(2008) in considering Quisqualis congeneric with Combretum. In this paper, however, we (M.J. & A.E.v.W) retain
Quisqualis as a separate genus for practical purposes, considering the evolutionary specialisation showed by the
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particular clade. Although there might be intermediate states in the degree of adnation of the style to the upper
hypanthium in some species of Quisqualis and Combretum as noted by Exell & Stace (1966) and Jongking (1991),
there are still enough characters to distinguish between these two genera and they can easily be keyed out. In
Quisqualis the upper hypanthium is produced into a long tube (see Figure 1) above the ovary compared to
Combretum which has a hypanthium produced into a short, campanulate or cup-shaped limb above the ovary.
Furthermore, Quisqualis has the stamens included, whereas in Combretum they are long-exserted (Bredenkamp
2000). The fact that Combretum subgenus Cacoucia is rendered paraphyletic if Quisqualis is maintained as a genus
may be objected to by those strictly adhering to Hennigian phylogenetic philosophy, but this is completely
acceptable to those prescribing to the more pragmatic evolutionary school of plant classification (Mayr & Bock
2002; Brummitt 2008). Nevertheless, to cater for the alternative point of view, a new combination and new name are
provided for Q. parviflora below.
Pollination strategies
Differences in pollination strategy are most likely responsible for the floral differences between Combretum and
Quisqualis. In the case of Quisqualis the elongated hypanthium might represent a modification for pollination by
long-proboscid sphingid moths (Stace 2007). The white- and yellow-flowered species of Combretum with relatively
small and reduced petals and with nectaries suggest pollination by insects with short mouthparts, notably honeybees,
whereas those with red flowers and abundant liquid nectar are probably bird-pollinated (Stace 2007). For
Combretum this is confirmed by casual observations on the southern Africa species.
Distribution
Quisqualis parviflora is endemic to South Africa (Bredenkamp 2000; Jordaan 2003, 2006). Van der Schijff &
Schoonraad (1971), Carr (1986) and Bredenkamp (2000) give the distribution of Q. parviflora as occurring in
Mpumalanga (Mariepskop and Graskop), KwaZulu-Natal and Eastern Cape. Subsequently all the specimens claimed
to have been of Q. parviflora in Mpumalanga were shown to be of Combretum edwardsii (Verhoeven & Van der
Schijff 1975; McCleland 2002). Sterile material collected from more inland localities of KwaZulu-Natal and
previously named Q. parviflora also belong to C. edwardsii and/or probably an undescribed species of Combretum.
Therefore Q. parviflora only grows with certainty as a woody climber in mainly coastal forest from Ndumu Game
Reserve in the north, through most of KwaZulu-Natal to the Eastern Cape (Port St. Johns) in the south (Figure 2).
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Although no records have been found in Mozambique, it may well occur there, at least in the far south where it
borders KwaZulu-Natal (Carr 1986).
Taxonomy
Quisqualis have microscopic stalked glands similar to those in Combretum Subgenus Cacoucia, and the scales so
characteristic of Combretum Subgenus Combretum are absent (Exell & Stace 1966; Wickens 1973). Fruit of
Quisqualis are generally 5-winged, usually 4-winged in Combretum. The petals are well-developed in Quisqualis:
red in Q. indica L. (rangoon creeper), a decorative species originally from India and commonly cultivated in
gardens, and green in the South African Q. parviflora. Specimens seen on the Aluka Library website,
http://www.aluka.org/ (accessed July 2009) are distinguished by the code e! in the citations below.
Quiqualis parviflora Gerrard ex Sond. in Flora capensis 2: 512 (1862); Dümmer: 232 (1913); Bews: 147
(1921); J.D.Carr: t. 1925 (1986); Pooley: 362 (1993); M.Coates Palgrave: 809 (2002). Type: South Africa,
KwaZulu-Natal, ‘Nototi’ [Umhtoti], Gerrard & McKen s.n. (TCD e!, holo.; K e!, iso.).
For description see Carr (1986).
Selected specimens examined
KWAZULU-NATAL.—2632 (Bella Vista): Ndumu Game Reserve, Khondo Sand Forest, (–CD), 03-1968, P. de
Moor 35 (PRE). 2732 (Ubombo): Mkuzi Station, from Ubombo Magistracy to uGaza Mountain, (–CA), 26-04-1944,
J. Gerstner 4552 (PRE); Hlabisa Distr., False Bay, lower Mzinene River, (–CD), 26-10-1944, J. Gerstner 4963
(PRE). 2831 (Nkandla): Eshowe, Memorial Hill, (–CD), 15-05-1951, J.G. Lawn 1974 (PRE); Ngoye Forest Reserve,
(–DC), 19-11-1993, R. Williams 1106 (NH, PRE). 2930 (Pietermaritzburg): Durban, Burman Bush, (–DD), 11-071970, R.G. Strey 9839 (NH, PRE), Isipingo, Jeffels Hill South, (–DD), 16-02-1966, C.J. Ward 5313 (PRE). 2931
(Stanger): Stanger Distr., 4 miles from Mapumulo to Kranskop, (–AA), 20-01-1966, E.J. Moll 2958 (PRE); Mtunzini
forest, (–BA), 17-02-1961, M. Wells & D. Edwards 22 (PRE); Inanda Distr., 5 miles W of Verulam, (–CA), 15-091965, E.J. Moll 2083 (PRE). 3030 (Port Shepstone): Vernon Crookes Nature Reserve, (–BC), 15-03-1986, C.J. Ward
9831 (PRE); Port Shepstone, Farm Tigerhole, (–CB), 08-08-1965, R.G. Strey 5927 (PRE). 3130 (Port Edward):
Umtamvuna Nature Reserve, Bululu River, (–AA), 09-04-1981, H.B. Nicholson 2171 (PRE).
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EASTERN CAPE.—3129 (Port St Johns): Lotana Forest near Ntafufu, (–DA), 11-04-1991, K.H. Cooper 283 (NH,
PRE), Port St Johns, on road to Agate terrace, (–DA), 10-03-2001, P.M. Gavhi, P.J.H. Hurter & E. van Wyk 39
(PRE).
Alternative taxonomic treatment
If Quisqualis is sunk under Combretum, a new combination and name is required for Q. parviflora. The specific
epithet ‘parviflorum’ cannot be used in Combretum since it is already been used by Reichenbach (1825). Exell
(1953) pointed out that Index kewensis incorrectly attributes C. parviflorum to De Candolle (1828), where it was
cited as a synonym of C. micranthum Don, a mistake still reflected in The International Plant Name Index (IPNI),
accessed July 2009. The name C. parviflorum was validly published three years earlier by Reichenbach (1825), thus
invalidating C. parviflorum Eichler (1867). The latter name was proposed for a species from Brazil, but because it is
a later homonym, this species is now known by the new name C. vernicosum Rusby (1927).
Combretum sylvicola O.Maurin, M. Jordaan & A.E.van Wyk, comb. et nom. nov.
Quisqualis parviflora Gerrard ex Harv.: 512 (1862), non Combretum parviflorum Rchb. (1825), nec C. parviflorum
Eichl. (1867), nom. illegit. Type: South Africa, KwaZulu-Natal, 'Nototi' [Umhtoti], Gerrard & McKen s.n. (TCD e!,
holo.; K e!, iso.).
ACKNOWLEDGEMENTS
We would like to thank Hester Steyn for preparing the distribution map, and Tony Abbott for sharing with us his
field observations on Quisqualis parviflora.
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Botanic Gardens Kew, London.
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* National Herbarium, South African National Biodiversity Institute, Private Bag X101, 0001 Pretoria. † Student
affiliation: Department of Botany, University of Pretoria, 0002 Pretoria.
** H.G.W.J. Schweickerdt Herbarium, Department of Plant Science, University of Pretoria, 0002 Pretoria.
*** Molecular Systematics Laboratory, Department of Botany and Plant Biotechnology, APK Campus, University
of Johannesburg, PO Box 524, 2006 Auckland Park, South Africa.
MS. received: 2009-07-29.
CAPTIONS
FIGURE 1.—Quisqualis parviflora. Lawn 629 in PRE. Photographer: A. Romanowski.
FIGURE 2.—Known distribution of Quisqualis parviflora.
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289
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290
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291
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ANNEXE 2: A conspectus of Combretum (Combretaceae) in southern Africa, with taxonomic and
nomenclatural notes on species and sections
A conspectus of Combretum (Combretaceae) in southern Africa, with taxonomic and nomenclatural notes on
species and sections
M. JORDAAN*†, A.E. VAN WYK** & O. MAURIN***
Keywords: Combretaceae, Combretum, lectotypification, phylogeny, sections, southern Africa, taxonomy
ABSTRACT
Two subgenera of Combretum occur in the FSA-region. Previous sectional classifications were assessed in
view of molecular evidence and accordingly modified. Ten sections in subgenus Combretum, 25 species and eight
subspecies are recognised. Subgenus Cacoucia comprises four sections and seven species. Combretum engleri
Schinz, C. paniculatum Vent. and C. tenuipes Engl. & Diels are reinstated as distinct species separate from C.
schumannii Engl., C. microphyllum Klotzsch and C. padoides Engl. & Diels, repectively. C. schumanni occurs
outside the FSA region. Records of C. adenogonium Steud. ex A.Rich., C. platypetalum Welw. ex M.A.Lawson
subsp. oatesii (Rolfe) Exell and subsp. baumii (Engl. & Gilg) Exell in Botswana are doubtful. C. celastroides Welw.
ex M.A.Lawson subsp. orientale Exell is elevated to species level as C. platelliforme Engl. & Diels. C. grandifolium
F.Hoffm. is reduced to C. psidioides Welw. subsp. grandifolium (F.Hoffm.) Jordaan. A new section, C. section
Plumbea Jordaan, A.E.van Wyk & O.Maurin is described to accommodate C. imberbe Wawra. Twenty four names
are lectotypified. The type, a full synonymy, other nomenclatural and taxonomic information, the full distribution
range and a distribution map are provided for each taxon. Selected specimens examined are given for poorly known
species. Keys to subgenera, sections and species are provided.
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CONTENTS
Introduction
Materials and methods
Taxonomy
COMBRETUM subgenus COMBRETUM
Key to the sections of subgenus Combretum
GROUP 1
I. Combretum section Angustimarginata
II. Combretum section Spathulipetala
III. Combretum section Macrostigmatea
IV. Combretum section Glabripetala
V. Combretum section Ciliatipetala
Key to the species of Combretum section Ciliatipetala
GROUP 2
VI. Combretum section Hypocrateropsis
Key to the species of Combretum section Hypocrateropsis
VII. Combretum section Metallicum
Key to the subspecies of Combretum section Metallicum
VIII. Combretum section Breviramea
IX. Combretum section Campestria
X. Combretum section Plumbea
COMBRETUM subgenus CACOUCIA
Key to the sections of subgenus Cacoucia
XI. Combretum section Poivrea
XII. Combretum section Conniventia
XIII. Combretum section Megalantherum
XIV. Combretum section Oxystachya
Acknowledgements
References
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INTRODUCTION
Combretum Loefl. belongs to family Combretaceae, one of the 14 core families of the Myrtales (Dahlgren & Thorne
1984; Sytsma et al. 2004) one that is characterised by mainly opposite leaves and the absence of stipules or stipules
are rudimentary (Stace 2007). Combretaceae is sister to all the other 13 families combined and diverged early in the
evolution of the Myrtales (APweb). Combretum (excluding Quisqualis L.) comprises about 250 species
(Bredenkamp 2000) and occurs in tropical and subtropical regions (America, Africa, Madagascar, India, Asia,
Malesia, Australia), but is absent from the Pacific Islands (Stace 2007). Although Bredenkamp (2000) gives the
distribution as excluding Australia, C. trifoliatum Vent., a vigorous woody climber, was discovered in northern
Australia in the 1980s (Clakson & Hyland 1986; Pedley 1990). The greatest species diversity occurs in Africa,
namely 163 in Sub-Saharan Africa (Klopper et al. 2006), with 43 in Gabon (Jongkind 1999), 36 in Cameroon (Liben
1983), and about 30 in southern Africa (Jordaan 2003). It is widespread in the FSA region in all countries and
provinces, except in the Free State (rare), Lesotho and Western Cape (Bredenkamp 2000).
Combretum are mostly deciduous or semi-deciduous trees (rarely evergreen), shrubs, scandent shrubs
(scramblers), subshrubs with woody rootstocks (so-called geoxylic suffrutices; rare in southern Africa) or woody
climbers (lianas), sometimes with spine-tipped lateral shoots (C. imberbe Wawra). Bark on stems is often flaking
and peeling in stringy strips or threads in most species or in large ± cylindrical or hemicylindrical pieces revealing an
exposed cinnamon-red surface (C. psidioides group). Leaves are opposite, sub-opposite (or locally alternate),
sometimes 3- or 4-whorled, exstipulate, simple and the margins are always entire, rarely crenulate, or sometimes
undulate (C. elaeagnoides Klotzsch, C. petrophilum Retief and C. tenuipes Engl. & Diels). Indumentum on leaves,
flowers and fruit are unicellular, compartmented or combretaceous hairs (sharp-pointed, thick-walled with a bulbous
base), multicellular stalked glands and multicellular scales. Mature scales can be classified into three major groups
and have proved to be important in assessing taxon boundaries and phylogenetic relationships (Exell & Stace 1972).
Leaves are pinnately veined where the lateral veins are arranged parallel to each other, somewhat spaced and looping
before they reach the margin (brochidodromous). Hair-tuft domatia (marsupiiform) in axils of the veins below are
present in a number of species (Stace 1965). Bases of leaf petioles may persist as straight spines or recurved hooks
as in C. bracteosum (Hochst.) Brandis, C. mossambicense (Klotzsch) Engl. and C. microphyllum Klotzsch. Flowers
are bisexual and are borne in axillary or terminal branched or unbranched spikes, sometimes subcapitate and are
bracteate. Flowers are 4- or 5-merous and usually sweetly scented. Petals vary from white, cream, yellow, yellow-
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green in most species, but are sometimes pale to deep pink or bright red as in C. bracteosum, C. microphyllum, C.
paniculatum Vent., C. platypetalum Welw. ex M.A.Lawson and C. wattii Exell. In deciduous species the flowers
appear before or with the new leaves, e.g. C. elaeagnoides Klotzsch, C. microphyllum, C. platypetalum, C.
psidioides and C. zeyheri Sond. The calyx is produced into a short, campanulate or cup-shaped limb above the
inferior ovary. Stamens are inserted on the hypanthium, usually twice as many as the sepals or petals, and usually
always exserted beyond the petals. The stamens vary in colour from yellow, orange, pinkish, crimson or reddish to
red-brown. A glabrous or pilose, green or red, well-developed nectariferous discs are often present at the base of the
upper hypanthium. Nectar production is indicative of the fact that the flowers are pollinated by a wide range of
insects or birds (Stace 2007). The ovary is inferior and 1-locular with 2 pendulous anatropous ovules of which only
one develops into a seed. The fruit is glabrous or covered with scales and/or hairs and is mainly a 4-winged, or
occasionally 5-winged (C. mossambicensis, C. oxystachyum, C. wattii) indehiscent samara, except in C. brateosum
which has wingless fruit (nuts). In most cases winged fruit are wind-dispersed and the wingless fruit seem to be an
adaptation to water dispersal (Exell & Stace 1972).
Despite extensive taxonomical and anatomical studies on Combretum in tropical and southern Africa by
Engler & Diels (1899), Dümmer (1913), Stace (1961; 1965; 1969; 1980; 1981), Exell (1968; 1978), Verhoeven &
Van der Schijff (1972), Wickens (1973), Carr (1988), Van Wyk (1984), Rodman (1990) and Tilney (2002), there are
still taxonomic and nomenctural problems remaining as well as new taxa to be described. Some names are
misapplied and the identity of some taxa in southern African herbaria is uncertain. Recent molecular work (Maurin
et al. 2010) has indicated that taxa boundaries need revising to reflect more accurately the phylogeny of Combretum
and its allies. Maurin et al. (2010) deal mostly with the subgeneric, sectional and generic delimitation of Combretum,
whereas the present paper deals with species delimitation, the status elevation of infraspecific taxa and
lectotipyfication of some names. The description of five newly discovered species will be dealt with in forthcoming
publications.
MATERIALS AND METHOD
All material of Combretum in the National Herbarium, Pretoria (PRE) and H.G.W.J Schweickerdt Herbarium,
University of Pretoria (PRU) were examined. Two websites were consulted for type material: (i) www.aluka.org and
(ii) the Zürich Herbarium: www.zuerich-herbarien.unizh.ch. Types seen electronically is cited as e! Where the
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holotype has been destroyed in the Berlin Herbarium (B) during World War II, lectotypification is covered by
Article 9.15 of the Code (McNeill et al. 2006) which provides for the narrowing the lectotype to a single specimen.
Jongkind (1992, 1993) chosen some lectotypes in various herbaria by means of determinative slips, but these have
not yet been validated by publication and are therefore designated in the present paper.
Sectional classifications of Engler & Diels (1899.), Exell (1978) and Stace (1981) were assessed in view of
the phylogenetic studies done by Maurin at al. (2010) and adjusted where necessary. Sections are arranged from
ancestral to derived according to the mentioned molecular studies. A new section is described to accommodate C.
imberbe and C. mkuzense is treated as belonging to section Spathulipetala. Species are arranged alphabetically
within each section. An index is provided at the end for easy access to species. The following species are
widespread, well defined and well known or recently described and no voucher specimens are cited for them: C.
apiculatum Sond. subsp. apiculatum, C. erythrophyllum (Burch.) Sond., C. hereroense Schinz, C. imberbe, C.
kraussii Hochst., C. molle R.Br. ex G.Don, C. vendae A.E.van Wyk and C. zeyheri Sond. Geographical distributions
mentioned in the keys refer primarily to the Flora of southern Africa (FSA) region, namely Botswana, Lesotho,
South Africa, Namibia and Swaziland. Species occurring further north of southern Africa are indicated by an arrow
on the distribution maps. Full range distribution, including all countries, is given under each species.
TAXONOMY
Subgeneric classification
Combretum is subdivided into three subgenera, namely (i) subgen. Combretum, (ii) subgen. Cacoucia (Aubl.) Exell
& Stace and (iii) subgen. Apetalanthum Exell & Stace (Stace 1981). The latter is represented by only one species, C.
apetalum Wall. ex Kurz which is restricted to Asia. It has leaves with scales and stalked glands, petals are absent and
it has 10 stamens in two whorls. The first two mentioned subgenera have scales or stalked glands, petals are present,
although sometimes reduced and they have eight stamens in one or two whorls. Subgenera are mainly based on the
presence or absent of petals, presence or absence of scales on the leaves, presence or absence of stalked glands, the
flowers being 4- or 5-merous, colour of the flowers and length of petals.
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Key to the subgenera of Combretum as modified from Exell (1978)
1a Scales present though sometimes inconspicuous or hidden by hairs; microscopic stalked glands absent; flowers
and fruit usually 4-merous; petals cream, white, yellow or greenish, usually not red, <3.5 mm long subgen.
Combretum
1b Scales absent; microscopic stalked glands present; flowers and fruit 5-merous or if 4-merous then petals red;
petals >4 mm long
subgen. Cacoucia
Sectional classification
COMBRETUM Loefl. Subgen. COMBRETUM
Scales present, although sometimes inconspicuous or hidden by combretaceous hairs; microscopic stalked
glands absent; flowers usually 4-merous; petals usually not red; stamens usually 8, in 1 or 2 whorls; fruit usually 4winged. The structure and arrangement of scales are of great taxonomic significance (Stace 1965) and the southern
African material is divided into ten sections (Engl & Diels 1899; Wickens 1973; Exell 1978; Stace 1980, 1981;
Rodman 1990) which fall into two groups. The sectionional grouping is based on the size of the scales on the leaves
and the resultant two groups are congruent with the two major grouping recovered in phylogenetic analyses (Maurin
et al. 2010). Each group is represented by five sections. The first five sections treated here belong to the group with
small, inconspicuous scales, usually smaller than 100 µm, ± circular in outline or slightly scalloped in sect.
Ciliatipetala and are divided by few radial and tangential walls and sometimes the tangential walls are absent as in
sect. Angustimarginata, sect. Glabripetala and sometimes in sect. Ciliatipetala. (Figure 1). The last five sections
have conspicuous scales, usually larger than 100 µm, scalloped or irregular undulate in outline and the scales are
divided by many radial and tangential walls (Figure 2). C. imberbe is placed in its own section, sect. Plumbea, newly
described here. Note that although 100 µm is taken as the cut off measurement to separate the two groups,
intermediates do occur.
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Key to the sections of subgen. Combretum for species of the FSA-region
1a Scales inconspicuous, usually less than 100 µm in diam.; scales divided by few radial and tangential walls
(tangential walls sometimes absent); stamens 1-seriate (GROUP 1) (Figure 1):
2a Petals apex ciliate or pilose; petals small, 0.5–1.5 mm long (if apex not ciliate then petals less than 1 mm long as
in C. petrophilum); leaf apices often apiculate; fruit 15–30 mm long
V. Sect. Ciliatipetala
2b Petals apex glabrous; petals 1.5–2.5 mm long; leaf apices not apiculate; fruit 15–50(100) mm long:
3a Fruit up to 22 mm long; often with hair-tuft domatia in axial of veins below (except in C. erythrophyllum and C.
vendae); cotyledons 2(3) arising above soil level:
4a Spring leaves at least partly cream-coloured or with some leaves turning bright red in autumn; petals narrowly
spathulate; disc margin pilose; style without expanded stigma; fruit sparsely to moderately hairy, not lepidote,
mature fruit tinged pink to dark red (rare in C. erythrophyllum); stipe 4–8 mm long
I. Sect.
Angustimarginata
4b Spring leaves not cream-coloured and autumn leaves no reddish; petals broadly spathulate; disc glabrous with
only a very short free margin; style sometimes with expanded stigma; fruit green, glabrous and glutinous, yellowish
green, with reddish brown scales, giving it a satiny sheen, wings papery; stipe up to 10 mm long
III. Sect.
Macrostigmatea
3b Fruit 35–50(100) mm and longer; hair-tuft domatia in axial of veins below absent; cotyledons arising below soil
level and borne above ground on a long stalk formed by connate petioles (Figure 3):
5a Leaves large, 100–200 mm long; style without swollen apex; fruit up to ± 35 mm long; glutinous when young,
glabrous, yellowish green tinged reddish brown; stipe up to 7 mm long IV. Sect. Glabripetala
5b Leaves medium-sised, 30–100 mm long; style with swollen apex; fruit up to 50(–100) mm long, pale green,
glutinous only on body, sparsely hairy or glabrous, drying pale brown, straw-coloured or limegreen; stipe 10–30 mm
long
II. Sect. Spathulipetala
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1b Scales conspicuous and large, usually more than 100 µm in diam. (84–160 µm in sect. Breviramea); scales
divided by many radial and tangential walls; stamens 1- or 2-seriate (GROUP 2) (Figure 2):
6a Trees; petals subcircular; fruit dark brown or reddish grey to dark purple, glabrous to densely hairy, metallic in
appearance, often acute at apex; disc with free pilose margin; cotyledons arising below soil level on stalk formed by
connate petioles VII. Sect. Metallicum
6b Trees, shrubs, scrambling shrubs or woody climbers; petals linear-elliptic, obovate to spathulate; fruit densely
rufous-, golden- or silvery-lepidote, otherwise glabrous; disc without free margin; cotyledons arising above or below
soil level:
7a Inflorescences usually terminal panicles of spikes or branched spikes; upper hypanthium little developed,
flattened; stamens 1-seriate, inserted at margin of disc; fruit usually smaller than 20 mm; stipe 1–3 mm long;
cotyledons arising above or below soil level; scales contigous or not:
8a Scrambling shrubs or woody climbers, usually multi-stemmed, not with spine-tipped short branches; dic glabrous
or pilose at least on margin; style without stalked scales; fruit not densely silvery lepidote; stipes less than 2 mm
long; cotyledons borne above soil level; scales conspicuous but not contiguous or overlapping
VI. Sect.
Hypocrateropsis
8b Erect trees up to 15 m, occasionally up to 30 m tall, single-stemmed, with short lateral branches often spinetipped; disc margin densely tomentose; style with stalked scales; fruit densely silvery lepidote; stipe 2–3 mm long;
cotelydons arising below soil level; scales conspicuous, contiguous and/or overlapping
X. Sect. Plumbea
7b Inflorescences usually axillary unbranched spikes; upper hypanthium well developed, campanulate or cupshaped, not flattened; stamens 2-seriate
; fruit 20–35 mm long; stipe up to 11(15) mm long; cotyledons arising
above soil level; scales contiguous or overlapping:
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9a Leaves with only 3 or 4(5) pairs of primary lateral veins; reticulate venation conspicuous below; hair-tuft domatia
absent in axils of veins below; leaf margin flat, usually ciliate; flowers long hairy, not conspicuous lepidote; disc
with free pilose margin; fruit densely reddish- or golden-lepidote
VIII. Sect. Breviramea
9b Leaves with 9–13 pairs of primary lateral veins; only midrib and primary lateral veins conspicuous and
prominently raised below; hair-tuft domatia in axial of veins below; leaf margin often undulate, glabrous; flowers
not hairy but densely and conspicuous lepidote; disc without free margin; fruit silvery-lepidote
IX. Sect.
Campestria
GROUP 1
I. Combretum section Angustimarginata Engl. & Diels
Engler & Diels (1899) and Exell (1978) included C. woodii Dümmer under C. kraussii Hochst. Rodman
(1990) considers C. woodii as conspecific with C. erythrophyllum. Burtt Davy (1926), Van Wyk (1984), Carr (1988)
and Jordaan (2003, 2006) consider C. woodii as a distinct species. There are ample DNA and morphological
differences to separate C. woodii from C. kraussii and C. erythrophyllum. See Carr (1988) for differences between
these three species. Exell (1970, 1978) included C. nelsonii and C. woodii in the synonymy of C. kraussii.
Chemosystematic studies conducted by Carr & Rogers (1987) support the recognition of C. nelsonii Dümmer, C.
kraussii and C. woodii as three distinct species. C. caffrum (Eckl. & Zeyh.) Kuntze and C. vendae also belong to this
section. This section is a natural taxon of closely related species restricted to southern Africa. It is characterised by
the scales on the leaves which are very inconspicuous and often obscured by hairs/or glutinous secretions. Young
leaves associated with the appearance of inflorescences in spring are often conspicuously white to cream or pale
green. The disc is glabrous with a pilose margin that is very shortly free. A table with summarised differences
between species and a key to species in this section is provided by Van Wyk (1984). A form of C. vendae with
glabrous leaves occur in the western Soutpansberg and comprises a new subspecies to be described elsewhere.
1. Combretum caffrum (Eckl. & Zeyh.) Kuntze, Revisio Generum Plantarum 3,2: 87 (1898); J.D.Carr: 40
(1988); M.Coates Palgrave: 797 (2002). Type: South Africa, Eastern Cape, 'ad ripas fluminum Kat et Vischrivier
(Albany), Zondagsrivier (Uitenhage), Keyskamma et Keyrivier (Caffraria)', Ecklon & Zeyher 421 (SAM
(SAM0036373-2) e!, lecto., designated here; ?FR e!, HBG e!, K e!, M e!, W e!, isolecto.). Figure 4.
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Dodonaea caffra Eckl. & Zeyh.: 55 (1834–1835).
Dodonaea conglomerata Eckl. & Zeyh.: 55 (1834–1835). Type: South Africa, Eastern Cape, ‘Inter frutices
fluvii Katrivier prope Fort Beaufort Caffraria terminis’, Ecklon & Zeyher 422 (SAM e!, lecto., designated here; K, M
e!, isolecto.).
C. salicifolium E.Mey. ex Hook.: t. 592 (1843); Sond.: 511 (1862); Dümmer: 182 (1913). Type specimen:
South Africa, Eastern Cape, 'Sundays River', Burke 592 (K e!, holo.; BM e!, iso.).
C. dregeanum C.Presl: 73 (1844). Type: South Africa, Eastern Cape, Klein Winterhoek between
Zoutpansnek and Enon, Drège 6849a (?PR, holo.; BM e!, HBG e!, K e!, MO e!, SAM e!, W e!, iso.).
Note: Ecklon & Zeyher 421 and Ecklon & Zeyher 422, both at SAM, are chosen as lectotypes for C. caffrum
(=Dodonaea caffra), and Dodonaea conglomerata respectively, because they have the protologues and annotations
attached to the specimens.
Distribution
South Africa (Eastern Cape).
EASTERN CAPE.—3029 (Kokstad): Umzimvubu Cutting, (–CC), 22-03-1973, R.G. Strey 11148 (NH, PRE). 3226
(Fort Beaufort): Fort Beaufort Dist., Fort Fordyce, (–CB), 12-03-1947, R. Story 2120 (PRE); Fort Beaufort Dist.,
Farm Good Hope, 10 km E of Alice, (–DD), 12-10-1977, G.E. Gibbs Russell 4007 (PRE). 3227 (Stutterheim):
Queenstown Dist., on Junction Farm, Queenstown Valley of Zwart Kei River, (–AB), 15-04-1911, E.E. Galpin 8116
(PRE); 15 miles N of Cathcart, (–AC), 04-1962, B.R. Roberts 1821A (PRE); Msenge Ridge, 1.3 miles from King
William’s Town on road to Alice, (–CD), 24-09-1957, D.M. Comins 1715 (PRE); Komgha Dist., banks of Kei River
at Kei Bridge, (–DB), 27-09-1942, J.P.H. Acocks 9132 (PRE); East London Dist., Horseshoe Valley, (–DD), 011927, C.A. Smith 3874 (PRE). 3228 (Butterworth): Butterworth, (–AC), 10-02-1914, A. Pegler 2076 (PRE); Qora
River crossing, 10 miles from sea, (–AD), 23-02-1966, M.J. Wells 3587 (PRE). 3325 (Port Elizabeth): Jansenville
Dist., Perdepoort, along river bank, (–AC), 19-10-1951, G.C. Theron 1067 (PRE); Somerset East Dist., Farm
Kaboega, (–BA), 09-11-1973, R.D. Bayliss 677 (PRE); Kranspoort, 4 km from Paterson on road Zuurberg National
Park, Superbus, (–BC), 09-01-1986, B.-E. van Wyk & C.M. van Wyk 1423(g) (PRE); to Suurberg Pass, (–BD), 0601-1974, E. Retief 247 (PRE). 3326 (Grahamstown): Alicedale Dist., Bushman’s River Poort, (–AC), 28-12-1898,
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E.E. Galpin 2977 (PRE); Adelaide Dist., banks of Koonap River, (–BA), 13-07-1931, E.E. Galpin 11554 (PRE);
Albany Dist., Farm Glen Boyd (–BB), 17-04-1928, G. Lindstedt 86 (PRE); Bathurst Dist., Lushington Valley, (–
BD), 25-05-1925, R.A. Dyer 26 (PRE); Alexandria Dist., W banks of Bushman’s River, below bridge on Port
Elizabeth – Grahamstown road, (–CB), 29-01-1952, E.E.A. Archibald 3959 (PRE); Bathurst State Forest, (–DB), 0406-1985, P. Herman 856 (PRE). 3327 (Peddie): Peddie on road to Cross Roads, bridge over Bira River, (–AA), 0712-1979, A.E. van Wyk 3215 (PRE); Peddie, Junction of Kap and Great Fish Rivers, (–AC), 23-03-1984, A. Jacot
Guillarmod 9471 (PRE); Keiskamma, near town, (–CA), 22-11-1967, P.A. Kirkman 3089 (PRE).
2. Combretum erythrophyllum (Burch.) Sond. in Linnaea 23: 43 (1850); Sond.: 509 (1862); Engl. &
Diels: 26 (1899); Dümmer: 140 (1913); Bews: 146 (1921); Exell & Roessler: 8 (1966); Exell: 7 (1968); Exell: 112
(1978); J.D.Carr: 69 (1988); Pooley: 356 (1993); A.E.van Wyk & P.van Wyk: 330 (1997); McCleland: 460 (2002);
M.Coates Palgrave: 802 (2002). Type: South Africa, Northern Cape, 'on the banks of the Ky-gariep' (Griqualand
West, Kalahari region, Herbert Division, right bank of the Vaal River at Blaauwbosch Drift), Burchell 1749 (K e!,
holo.; PRE!, iso.). Figure 5.
?Terminalia erythrophylla Burch.: 400 (1822).
C. glomeruliflorum Sond.: 47 (1850); Sond.: 509 (1862); Engl. & Diels: 26 (1899); Burtt Davy: 247 (1926);
Codd: 130 (1951). Type: South Africa, KwaZulu-Natal, Durban [Port Natal], Gueinzius 62 (?S, holo.; K e!, P e!, W
e!, iso.).
C. riparium Sond.: 47 (1850); Sond.: 511 (1862). C. glomeruliflorum Sond. var. riparium (Sond.) Burtt
Davy: 247 (1926); O.B.Mill.: 42 (1948). Type: South Africa, ?Gauteng, ‘On Magalisriver’, Zeyher 549 (S e!, holo.;
BM, K e!, SAM, iso.).
C. sonderi Gerrard ex Sond.: 511 (1862). Type: South Africa, KwaZulu-Natal, ‘On the Nototi River, near
Port Natal’, Gerrard 138 (BM, holo.).
C. erythrophyllum (Burch.) Sond. var. obscurum Van Heurck & Müll.Arg.: 237 (1871); Dümmer: 147
(1913). C. glomeruliflorum Sond. var. obscurum (Van Heurck & Müll.Arg.) Burtt Davy: 37, 247 (1926). Type:
South Africa, ‘Africa australis, woods on Crocodile River’, Zeyher 550 (K e!, holo.; P e!, iso.).
C. lydenburgianum Engl. & Diels: 26 (1899); Eyles: 428 (1916). Type: South Africa, Mpumalanga, near the
waterfall in the town of Lydenburg, Wilms 212 (B, holo.†; K e!, lecto., designated here; BM, E e!, isolecto.).
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Note: Wilms 212, the holotype of C. lydenburgianum, was destroyed in Berlin during World War II and the Kew
specimen is chosen as lectotype, which is the better specimen of all the isotypes that are available.
Distribution
Botswana, Mozambique, South Africa (Eastern Cape, Gauteng, KwaZulu-Natal, Limpopo Province, Mpumalanga,
Northern Cape, North-West), Swaziland, Zambia, Zimbabwe.
3. Combretum kraussii Hochst. in Flora 27: 424 (1844); Sond.: 510 (1862); Dümmer: 164 (1913); Bews:
147 (1921); Burtt Davy: 246 (1926); Exell: 7 (1968); Exell: 114 (1978); J.D.Carr: 89 (1988); Pooley: 358 (1993);
A.E.van Wyk & P.van Wyk: 332 (1997); McCleland: 462 (2002); M.Coates Palgrave: 804 (2002). Type: South
Africa, KwaZulu-Natal, Durban [Port Natal], 'in sylvis primitivis circa Umlaas River', Oct. 1839, Krauss 253 [B,
holo.†; K (00022665) e!, lecto., designated here; BM e!, M e!, MO e!, OXF, TCD e!, W e!, Z e!, isolecto.]. Figure 6.
C. lucidum E.Mey. ex Drège: 174 (1843); Dümmer: 164 (1913). Type: South Africa, KwaZulu-Natal,
between Umkomanzi and Umzimkulu Rivers, Drège s.n. (HBG e!, holo.; K e!, iso.).
Note: The holotype of C. kraussii at Berlin was destroyed in World War II and from all the extant isotypes, the
fruiting specimen at Kew was chosen, because it shows the leaf characters the best, namely totally glabrous, obovate
with a rounded to emarginate apices, with very conspicuous reticulate venation below, margin flat, not wavy and
longitudinally folded upwards along the midrib as in C. woodii and the apices not acute to acuminate as in C.
erythrophyllum, its two closiest allies; most of the other isotypes are just fragments, except the BM specimen which
is a flowering specimen.
Distribution
Mozambique, South Africa (Eastern Cape, KwaZulu-Natal, Limpopo Province, Mpumalanga), Swaziland.
4. Combretum nelsonii Dümmer in The Gardeners' Chronicle, ser. 3: 164 (1913); Burtt Davy: 246 (1926);
A.E.van Wyk: 132 (1984); A.E.van Wyk & P.van Wyk: 334 (1997); McCleland: 466 (2002); M.Coates Palgrave:
807 (2002). Type: South Africa, Limpopo Province, mountain gorge, near Groot Vley, Pienaars River, Nelson 91
(TVM 25192) (K e!, holo.; PRE!, iso.). Figure 6.
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Distribution
South Africa (Limpopo Province, Mpumalanga).
LIMPOPO PROVINCE.—2328 (Baltimore): between Potgietersrust and Marken, just after 58 km sign on road from
Potgietersrust, (–DC), M.H. Steyn 10 (PRE). 2428 (Nystroom): Farm Dwarsfontein 10 KR, Eransa Game Farm,
camp on N side of Visgat road, (–AA), 11-06-1994, R.W. Dehning RWD9413 (PRE); Farm Rietfontein, near
Nylstroom, (–AD), 04-04-1987, F. von Breitenbach 20288 (PRE); Waterberg Dist., Farm Nyhoffsbult, (–BA), R.H.
Westfall 1578 (PRE); Potgietrsrust Dist., Waterberg, Farm Houtboschkloof 309 KR, (–BC), F. Venter 10338 (PRE);
Nylstroom Dist., Sterkfontein, Farm Krantzkop, 9 miles E of Nylstroom, (–CB), A.O.D. Mogg 37485 (PRE); 16,6
km from Klein Kariba on Vaalkop road in Waterberg Mountains, (–CD), 03-03-1972, B.J. Coetzee 1195 (PRE);
Lapalala Wilderness, Melkrivier, Farm Doornlaagte, 6.5 km from main gate of Lapalala Game Reserve, (–DD), 2903-2004, N. Swelankomo 29 (PRE).
5. Combretum vendae A.E.van Wyk in South African Journal of Botany 3: 125 (1984); J.D.Carr: 140
(1988); M.Coates Palgrave: 811 (2002). Type: South Africa, Limpopo Province, Vuvuha NE of Thengwe, near
Muledzhi Village, Van Wyk 3913 (PRU!, holo.; K e!, P e!, PRE!, iso.). Figure 4.
Distribution
South Africa (Limpopo Province).
6. Combretum woodii Dümmer in The Gardeners' Chronicle, ser. 3: 181 (1913); Burtt Davy: 245 (1926);
Compton: 395 (1976); J.D.Carr: 147 (1988); Pooley: 358 (1993); McCleland: 468 (2002); M.Coates Palgrave: 812
(2002). Type: South Africa, Mpumalanga, Barberton Dist., Kaap River Valley, Galpin 1176 (K e!, lecto., designated
here; NH e!, PRE!, SAM e!, isolecto.). Figure 4.
Note: Dümmer (1913) mentioned two specimens in his protologue, Wood 522 and Galpin 1176. The latter syntype in
Kew where Dümmer worked for a few years is chosen, because it contains flowers and fruit and duplicates are
housed in many other herbaria. This specimen (lectotype here chosen) shows the distinguished characters which
separates C. woodii from C. kraussii, namely leaves membraneous, widest in middle, folded along the midrib and
305
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narrower elliptic fruit which are totally glabrous. The syntypes, Wood 522 in BM was not examined and is not
available on the Aluka website, but a duplicate exists in Zürich Herbarium, which does not show the leaves folding
along the midrib as clearly as the Galpin specimens.
Distribution
South Africa (KwaZulu-Natal, Limpopo Province, Mpumalanga), Swaziland and probably also Mozambique.
LIMPOPO PROVINCE.—2430 (Pilgrim’s Rest): near Strydom Tunnel, (–BC), 12-04-1997, M.H. Steyn 15 (PRE).
MPUMALANGA.—2530 (Lydenburg): Sabie, Langverwag, (–BB), 14-04-1963, W.J. Louw 2721 (PRE); Thorncroft
Nature Reserve, off Agnes Mine road W of Barberton, (–DD), 14-11-1968, D. Edwards 4115 (PRE). 2531
(Komatipoort): Kruger National Park, Skipberg [Ship Mountain], 9 miles SE of Pretorius Kop, (–AB), 09-05-1950,
L.E. Codd 6031 (PRE), 15-01-1953, H.P. van der Schijff 1657 (PRE).
SWAZILAND.—2631 (Mbabane): Stegi Dist., Chilobe Forest, (–BD), 02-06-1960, R.H. Compton 30065 (PRE).
2632 (Bela Vista): Blue Jay Ranch, S of Umbuluzi Gorge, (–AA), 04-09-1977, J. Culverwell 955 (PRE); Farm
Mlawula, 5 miles SW of Goba/Mhlumeni bordergate, Lebombo Mountains, (–AC), 13-03-1977, J. Culverwell 654
(PRE).
KWAZULU-NATAL.—2731 (Louwsburg): Itala Nature Reserve, along river near Guest cottage, (–AC), 09-011980, A.A. Mauve 5256 (PRE); Pongola Bosveldplaas, (–BC), 01-1972, M.D.S. Nel 237 (PRE); N of Jozini on new
road from Ingwavuma to Jozini at Joulous Down Store, (–BD), 31-08-1978, L. Smook 1335 (PRE). 2732 (Ubombo):
near Ingwavuma, (–AA), 18-01-1963, L.E. Codd 10291 (PRE); Jozini Dam, Pongola River, (–AC), 08-08-1963, D.
Hardy & Scott-Smith 1534 (PRE); ± 3 km from Ubombo to Mkuzi, (–CA), 05-12-1983, A.E. van Wyk 6673 (PRE).
2830 (Dundee): Krantzkop Dist., Mambuba, (–DD), 11-05-1943, R.A. Dyer 4349 (PRE). 2831 (Nkandla):
Entonjaneni Dist., 8 miles N of Biyela Store, (–AC), 10-10-1946, J.P.H. Acocks 12985 (PRE). 2832 (Mtubatuba):
Hlabisa Dist., Hluhluwe Game Reserve, (–AA), 17-02-1954, C.J. Ward 2130 (PRE). 2930 (Pietermaritzburg):
Inanda Dist., 5 miles W of Verulam, (–DB), 15-09-1965, E.J. Moll 2091 (PRE); Pinetown, (–DD), 28-03-1958, M.J.
Wells 1855 (PRE). 2931 (Stanger): Mapumulo Dist., Oqaqeni, (–AA), 31-03-1957, D. Edwards 1835 (PRE).
II. Combretum section Spathulipetala Engl. & Diels
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Annexes
Traditionally Combretum zeyheri has been the only member of this section. It has large fruit up to 50 × 50 mm and
occasionally up to 100 × 80 mm, with rigid wings. According to Exell & Stace (1972) the fruit are adapted for
blowing along by wind at ground level. It has distinctive fused cotyledons, arising below soil level and borne above
ground on a long stalk formed by the connate petioles (Figure 3). This is a rare type of germination in Combretum
where four main types are known (Exell & Stace 1972). Flowers of C. zeyheri have a disc with the margin pilose and
free for 15–20 mm.
Although provisional molecular data have indicated that a re-evaluation of the taxonomic concepts of
sections Spathulipetala and Macrostigmatea are needed (Maurin et al. 2010), formal taxonomic adjustment must
await further phylogenetic analyses based on more taxa and more gene sequences. This should also take into account
data derived from all other fields, including micro- and macromorphology, vegetative and reproductive characters,
phytogeography and chemistry. Only a combination of such evidence will provide a clear picture of the true
phylogeny and evolution of the group. Tentatively C. mkuzense is placed in this section. Hennessy & Rodman (1995)
reduced C. mkuzense to synonymy under C. zeyheri. The latter is a single-stemmed tree, whereas C. mkuzense is a
scrambling shrub. C. mkuzense and C. zeyheri also have markedly different seedlings (Figure 3). There are abundant
morphological and molecular (Maurin et al. 2010) evidence that C. mkuzense, C. zeyheri and a third undescribed
species from the northern Kruger National Park (as C. mkuzense in McCleland 2002: 464) with much smaller size
fruit are separate entities.
7. Combretum mkuzense J.D.Carr & Retief in Bothalia 19: 38 (1989); Pooley: 360 (1993); McCleland:
458 (2002); M.Coates Palgrave: 805 (2002). Type: South Africa, KwaZulu-Natal, Mkuze Game Reserve
headquarters, Carr 187 (PRE!, holo.!; K e!, iso.). Figure 7.
Distribution
South Africa (KwaZulu-Natal).
KWAZULU-NATAL.—2632 (Bela Vista): Ndumu Game Reserve, (–CD), 17-02-1964, K.L. Tinley 1004 (PRE).
2732 (Ubombo): 16 miles Ndumu/Ingwavuma, (–AA), 06-11-1969, E.J. Moll 4359 (NH, PRE); Tembe area, on road
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D1845, (–AB), 09-05-2001, E van Wyk & P.M. Gavhi evw300 (PRE); Mkuze Game Reserve, (–CA), 11-09-1979,
J.D. Carr 192 (PRE); E side of Farm Shotton 13810 (–CD), 30-06-1975, C.J. Ward 8793 (PRE).
8. Combretum zeyheri Sond. in Linnaea 23: 46 (1850); Sond.: 511 (1862); Dümmer: 116 (1913); Burtt
Davy: 248 (1926); O.B.Mill.: 44 (1948); Codd: t. 1230 (1956); Exell & Roessler: 11 (1966); Exell: 8 (1968); Exell &
J.G.Garcia: 66 (1970); Wickens: 31 (1973); Exell: 122 (1978); Vollesen: 54 (1980); J.D.Carr: 151 (1988); Pooley:
360 (1993); A.E.van Wyk & P.van Wyk: 338 (1997); McCleland: 470 (2002); Coates Palgrave: 812 (2002); Curtis &
Mannheimer: 488 (2005). Type: South Africa, 'Africa australis, in silvis montis Magalisberg', Zeyher 552 (S e!,
holo.; BM, K e!, MEL, P e!, SAM e!, TCD, W e!, Z e!, iso.). Figure 7.
C. tinctorum Welw. ex M.A.Lawson: 430 (1871); Engl. & Diels: 30 (1899). Type: Angola, Cuanza Norte,
Cacuso, Pedras de Guinga, Welwitsch 4373 (LISU e!, holo.; BM e!, COI, K e!, P e!, iso.).
C. antunesii Engl. & Diels: 58 (1899). Type: Angola, Lubango, Huila, Antunes 17 (COI, holo.).
C. odontopetalum Engl. & Diels: 60 (1899). Type: Namibia, ‘Amboland, Omupanda, Unkuanyama’,
Wulfhorst 14 (Z e!, lecto., designated here; K e!, isolecto.).
C. calocarpum Gilg ex Dinter: 169 (1919); Suesseng.: 336 (1953). Type: Namibia, ‘Hereroland’, Neitsas,
Dinter 795 (E e!, lecto., designated here; BM, SAM e!, isolecto.).
Note: Both syntypes of C. odontopetalum, Schinz 1050 and Wulhorst 14, are housed in the Zürich Herbarium, but
only the Wulhorst specimen has a duplicate in another herbarium, namely in Kew, and is therefore chosen as the
lectotype.
Dinter (1919) mentioned syntypes in his protologue of C. calocarpum, Dinter 2877, Dinter s.n. and Dinter
795. The large fruit, the most distinctive character of this species in Namibia, is best seen in the Dinter 795 specimen
in SAM; it is here chosen as the lectotype.
Distribution
Angola, Botswana, DRC, Kenya, Malawi, Mozambique, Namibia, South Africa (Gauteng, KwaZulu-Natal, Limpopo
Province, Mpumalanga, North-West), Swaziland, Tanzania, Zambia, Zimbabwe.
III. Combretum section Macrostigmatea Engl. & Diels: 24 (1899); Stace: 158 (1969); Exell: 176 (1970); Wickens:
21 (1973); Exell: 115 (1978); Stace: 336 (1981).
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Species in this section have yellow, 4-merous, glutinous flowers arranged in subcapitate spikes. The nectariferous
disc is glabrous with only a very short free margin in C. schumannii Engl. and C. engleri Schinz. C. kirkii
M.A.Lawson (Malawi, Mozambique, Zambia, Zimbabwe) and C. gillettianum Liben (DRC, Tanzania, Zambia) also
belong to this section. Whether sections Macrostigmatea and Spathulipetala should be united, as suggested by
provisional molecular analyses, must await further study (see under section Spathulipetala above).
Dinter (1919) published the name Combretum parvifolium, but the ephitet was antedated by C. parvifolium
Engl. (1895). Schinz’s name ‘engleri’ is however the earliest. Exell (1970) keeps C. engleri and C. schumanii as two
separate species, but Wickens (1973) and Exell (1978) consider C. engleri conspecific with C. schumannii on the
basis that the flowers of both entities have a glabrous nectariferous disc with a short free margin and the fruit are
glabrous except for peltate scales. However, Carr (1988) maintains these two entities as separate species as they
differ in habit and geographical distribution. He also points out that C. schumannii has been successfully propagated
from seed in cultivation, whereas all attempts to germinate seed of C. engleri has failed. Based on flower and scale
morphology, Hennessy & Rodman (1995) also concluded that C. engleri and C. schumannii are separate species.
Engler (1895) based C. schumannii on a Holst specimen collected in Lushoto District, Tanzania. C. engleri is a
multi-stemmed shrub up to 4 m tall, growing in mixed woodland and savanna, often semi-arid and on Kalahari sands
in Angola, Zambia, Namibia, Botswana and western Zimbabwe (Wankie District). After viewing the type on the
Aluka Digital Library it is clear that C. schumannii does not occur in the FSA region and it is therefore a misapplied
name in this region. Specimens from Namibia and Botswana previously named C. schumanni are all C. engleri. Carr
(1988) mentions that C. schumannii is a tree up to 18 m tall with flaky bark, occurring in coastal and inland forest of
Kenya, Tanzania, Malawi and northern Mozambique. There are enough morphological distinctions between these
two species to keep them separate (Carr 1988, Hennessy & Rodman 1995).
9. Combretum engleri Schinz in Bulletin de l'Herbier Boissier sér. 2,1: 878 (1901); Stace: 14 (1961); Exell
& Roessler: 8 (1966); Exell: 7 (1968); Exell: 176 (1970); Exell & J.G.Garcia: 55 (1970); J.D.Carr: 66 (1988);
M.Coates Palgrave: 801 (2002); Curtis & Mannheimer: 476 (2005). Type: Namibia, Ombalambuenge, Apr. 1896,
Rautanen 236 (Z e!, holo.). Figure 5.
C. parvifolium Dinter: 170 (1919), nom. illegit.
C. myrtillifolium Engl.: 695 (1921). Type: Namibia, Naruchas, Dunen, Dinter 7278 (PRE!, lecto.,
designated here; BOL, K e!, isolecto.) & Namibia, Neitsas, Dinter 668 (BM, fragment, e!, SAM e!, paralecto.).
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C. chlorocarpum Exell: 167 (1928). Type: Angola, Oct. 1906, Gossweiler 3241 (BM e!, holo.; COI, LISJC,
iso.).
Note: Dinter (1919) mentioned two Dinter specimens in his protologue of C. parvifolium, numbers 668 and 7278,
collected in Namibia. This name is a later homonym and therefore illegitimate and Engler (1921) renamed it C.
myrtillifolium. The PRE specimen of Dinter 7278 which must be an isosyntype is chosen as lectotype for C.
myrtillifolium because it has flowers and fruit.
Distribution
Angola, Botswana, DRC, Namibia, Zambia.
NAMIBIA.—1715 (Ondangua): Oshikango, (–BD), 06/07-1948, E.M. Loeb 297 (PRE). 1716 (Enana): near Oshandi,
25 km SE of Oshikango, (–AC), 19-03-1973, R.J. Rodin 9119 (PRE); S of airstrip at Eenhana, (–AD), 06-05-1977,
J.P. le Roux 151 (PRE); Eenhana Dist., Ohangwena, along road E of Eenhana, (–DB), 06-04-2002, M.M. Uiras
MU652 (PRE). 1718 (Kuring-Kuru): Kavango, Runtu Dist., Makambu, (–AD), 25-06-1975, C.J. Geldenhuys 328
(PRE). 1719 (Runtu): 5 miles W of Runtu on road to Kapako, (–DC), 29-11-1955, B. de Winter 3734 (PRE). 1720
(Sambio): 14.8 miles E of Nyangana Mission Station, (–DD), 20-02-1956, B. de Winter 4778 (PRE). 1721
(Mbambi): Kavango, 2 km W of Mbambi, (–CC), 26-04-1977, M. Müller & W. Giess 585 (PRE). 1723
(Singalamwe): Western Caprivi, Singalamwe, Olifantkamp, (–CD), 07-1974, J.N. Pienaar & J. Vahrmeijer 483
(PRE); ± 78 km W of Katima Mulilo on Rundu road, (–DC), 22-04-1993, P. van Wyk BSA918 (PRE, PRU). 1724
(Katima Mulilo): Eastern Caprivi, Katima Mulilo Dist., (–AD), 30-06-1975, C.J. Geldenhuys 334 (PRE). 1816
(Namutoni): 40 miles SE of Ondangua on road to Namutoni, near Omuramba Ovambo, (–AD), 13-02-1959, B. de
Winter & W. Giess 6953 (PRE); Etosha National Park, at Stinkwater, near Namutoni, (–DB), 08-03-1976, W. Giess
& B. Loutit 14166 (PRE). 1820 (Tarikora): Kavango, Ndiyona Rest Camp, (–BB), 27-04-1977, M. Müller & W.
Giess 602 (PRE). 1821 (Andara): Grootfontein North, on road from Andara to Bagani, (–AB), 09-03-1958, H.
Merxmüller & W. Giess 2002 (PRE). 1918 (Grootfontein): Grootfontein Dist., on road to Omaramba - Omataka, (–
BA), 06-03-1995, P.M. Burgoyne 3262 (PRE); Kanovlei Dist., Nurugas, Grootfontein, (–BD), 11-1957, P.J. le Roux
85 (PRE); 4 km S of Otjituuo Depot, Vormdurst, in Omatako Omuramba, (–DA), 07-07-1976, D. Edwards 4398
(PRE). 1920 (Tsumkwe): ± 35 miles N of Gautscha Pan, (–BC), 14-02-1958, R. Story 6493 (PRE). 2015
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(Otjihorongo): Fransfontein, (–AB), L. Liebenberg 4910 (PRE). 2019 (Eiseb): Otjozondjupa, (–AC), 11-05-2001,
B.A. Curtis 996 (PRE). 2020 (Kaukauveld): ± 41 km from Gam on road to the Eiseb Valley, (–DA), 17-04-1996,
N.H.G. Jacobsen 5142 (PRE); 10 miles N of Eiseb Omuramba in direction of Kanovlei, (–DB), 12-04-1967, W.
Giess 9793 (PRE). 2119 (Epukiro): Omaheke, (–AB), 15-05-2001, B.A. Curtis 1081 (PRE); Hereroland, (–CA), 041970, J. MacKenzie 40 (PRE). 2120 (Rietfontein): Epukiro GO 329 Reserve, 10 km S of Rooiboklaagte Omuramba,
(–AA), 10-07-1976, D. Edwards 4416 (PRE).
BOTSWANA.—1725 (Livingstone): Chobe Dist., Serondela, (–CC), 11-1951, O.B. Miller B/1199 (PRE, SRGH);
Kazungula, near Zambezi River, (–CD), 08-1948, O.B. Miller B/641 (PRE). 1821 (Andara): on track to the Tsodilo
Hills, ± 10 km NE, (–DB), 18-04-1995, N.H.G. Jacobsen 5043 (PRE). 1822 (Kangara): Samoqoma Lediba, (–CD),
22-10-1979, P.A. Smith 2864 (PRE). 1823 (Siambisso): near Xauna Pan, (–AA), 01-01-1973, P.A. Smith 322 (PRE).
1921 (Aha Hills): 38 km N of Aha Hills, near Dobe, (–CA), 13-03-1965, H. Wild & R.B. Drummond 6986 (PRE); 64
km W of Nokaneng on road to Qangwa, (–DA), 22-03-1979, J.D. Carr 99 (PRE). 2022 (Lake Ngami): Mabeleapudi
Hills, between Maun and Ghanzi, (–CD), 03-08-1955, R. Story 5093 (PRE). 2121 (Ghanzi): Ghanzi Dist., Farm 68,
D’Kar, (–BD), 20-01-1970, R.C. Brown 7966 (PRE). 2122 (Kobe): Mkaku Pan area, near Kuki Fence, (–AB), 23-041968, A. Boshoff & M. Mason 283 (PRE).
VI. Combretum section Glabripetala Engl. & Diels
While working on the Flora of Ethiopia, Vollesen (1986) realised that C. adenogonium is an earlier name for C.
fragrans F.Hoffm. Wickens (1973) considers C. adenogonium (=C. fragrans) as occurring from Ethiopia in the
north through Uganda, Kenya, Tanzania, Malawi, Zimbabwe, Mozambique, Zambia, Malawi, southwards to
Zimbabwe and Botswana and westwards to Burkina Faso, Benin, Nigeria and the Congo. It is characterised by
relatively large leaves up to 180 x 90 mm and glutinous leaves and fruit. This taxon is represented in the FSA region
by two old specimens in PRE, both dated pre 1950 and collected in Botswana. Therefore it needs to be recollected to
confirm the existence of this species in the FSA region.
10. Combretum adenogonium Steud. ex A.Rich., Tentamen Florae Abyssinicae 1: 266 (1848);
F.W.Andrews: 204 (1950); Vollesen: 962 (1986); Wickens: 29 (1973); Vollesen: 117 (1995); A.E.van Wyk & P.van
Wyk: 326 (1997); M.Coates Palgrave: 795 (2002). Type: Ethiopia, Sabra, May 1840, Schimper 1289 (P e!, holo.; BR
e!, K e!, MO e!, W e!, Z e!, iso.). Figure 8.
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Annexes
C. fragrans F.Hoffm.: 31 (1889); Engl.: 289 (1895); Wickens: 29 (1973); Exell: 183 (1970); Exell: 120
(1978); Liben: 18 (1983). Type: Tanzania, Pa-Kabombue, Oct. 1881, Böhm 16a (B, syn.†; Z e!, lecto., designated
here; K e!, isolecto.).
C. ghasalense Engl. & Diels: 47 (1899); F.W.Andrews: 206 (1950); Exell: 8 (1968). Type: Sudan, Bahr el
Ghazal, Sabbi [Ssabi], 1869, Schweinfürth 2730 (B, syn.†; P e!, lecto., designated here; K e!, isolecto.).
C. multispicatum Engl. & Diels: 47 (1899). Type: Sudan, ‘Im lande der Bongo’, Sabbi, Nov. 1864,
Schweinfurth 2662 (B, syn.†; P e!, lecto., designated here; K e!, PRE!, WU e!, isolecto.).
C. undulatum Engl. & Diels: 48 (1899). Type: Sudan, Ngama, im Lande der Mittu, 1869, Schweinfurth
2815 (B, syn.†; P e!, lecto., designated here; K e!, PRE!; WU e!, isolecto.).
C. ternifolium Engl. & Diels: 49 (1899); O.B.Mill.: 43 (1948). Type: Tanzania, Morogoro Dist., Mgeta,
Stuhlmann 9272 (B, holo.†; K, fragment, e!, lecto., designated here; ?BM, isolecto.).
Notes: Hoffmann (1889) mentioned two syntypes in his protologue of Combretum fragrans, Böhm 16a and Böhm
32a, both been destroyed in World War II, but fortunately duplicates survived in Zürich (Z) and Kew (K). Böhm 16a
in Z which shows the large ternate leaves the best is chosen as the lectotype. The isosyntype, Böhm 16a, is not
available on the Aluka Library, whereas only a fragment of the other isosyntype, Böhm 32a, survived in Kew.
Engler & Diels (1899) described Combretum ghasalense, C. multispicatum and C. undulatum, all three
names based on types collected in the Sudan and C. ternifolium based on specimen collected in Tanzania. The holoand syntypes all at Berlin were destroyed and lectotypes are selected from material in Paris (P) and Kew (K).
Distribution
Benin, Botswana, Burkina Faso, Central African Republic, Cameroon, Cote d'Ivoire, DRC, Ethiopia, Ghana, GuineaBissau, Kenya, Malawi, Mozambique, Nigeria, Sudan, Tanzania, Togo, Uganda, Zambia, Zimbabwe.
BOTSWANA.—2022 (Lake Ngami): Ngamiland (–BA), 01-1931, H.H. Curson 119 (PRE). 1824 (Kachikau):
between Nunga Vlei and Mabebe, No. 3 borehole, (–CB), 21-09-1949, I.B. Pole-Evans 4598 (PRE).
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Annexes
V. Combretum section Ciliatipetala Engl. & Diels (1899)
This section comprises about 60 species and is the largest in the genus. Although the species are morphologically
divers they do seem to form a natural group. All members of this section have small petals which are ciliate or pilose
at the apex, except in C. petrophilum, and the disc has a short, free, pilose margin. The scales are relatively small
(40–130) µm in diam., ± circular, scalloped at the margin with radial and tangential walls. Stace (1969) separates this
section into two large aggregates centred on C. apiculatum and C. molle, but these two groups are not supported as
natural entities by molecular evidence (Maurin et al. 2010). Leaves in the section vary from very glabrous, glutinous
and with always apiculate apices in C. apiculatum subsp. apiculatum and C. petrophilum, hairs only on margin and
main vein and with acute to rounded apices in C. edwardsii Exell, to very hairy leaves in C. albopunctatum
Suesseng., C. apiculatum subsp. leutweinii (Schinz) Exell (apiculate apices), C. moggii Exell, C. molle and C.
psidioides. Apices of leaves in C. molle are usually round, emarginate to abruptly acuminate with a long acumen or
mucron, but are occasionally apiculate.
Combretum apiculatum subsp. apiculatum is widespread in Angola, Namibia, Botswana, northern parts of
South Africa, Zimbabwe, Zambia, Malawi and Mozambique and grows in savanna woodland, often on Kalahari
sands, whereas subsp. leutweinii has a more restricted range in Namibia and Botswana, mainly in karstveld and
mopaneveld. C. apiculatum subsp. boreale Exell is reinstated for the narrow-leaved form of C. apiculatum mainly
from Tanzania and Kenya. Wood (1908) mentions C. glutinosum Guill. & Perr. ex DC. as occurring in KwaZuluNatal, but the latter is a West African species that does not occur in southern Africa.
Combretum moggii and C. molle are both very hairy, especially their leaves and young stems. C. moggii is
usually a multi-stemmed, small shrub up to 3 (–5) m tall growing in sandy soil in the crevices between outcropping
quartzitic rocks (Carr 1988). It has a smoother bark, smaller and narrower leaves with more silky type of hairs and
longer inflorescences than C. molle. The latter is usually a single-stemmed tree up to 9 m tall, with main branching
commencing 1.5–3.0 m above ground level (Carr 1988). Besides the former Transvaal records of C. moggii (Exell
1968; Carr 1988; Hennessy 1991) addisional localities were recorded in Swaziland (Loffler & Loffler 2005) and
northern KwaZulu-Natal (see map).
Combretum molle has a very wide distribution, from Saudi Arabia, Yemen and Ethiopia (where the type is
from) in the north to KwaZulu-Natal (=C. gueinzii Sond.) in the south and westwards to West Africa, Democratic
Republic of Congo (DRC) and Angola, but it is absent from Namibia and most parts of Botswana. Exell (1978)
points out that there are a great deal of variation in leaf shape, size and indumentum, and that the species grows in
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various ecological habitats. A polimorphic species, C. molle is one of the aggregate groups of Combretum in Africa
that needs to be investigated further for the possibility of recognizing distinct subspecies. Wickens (1973) for
instance, recognised three forms of C. molle in East Africa.
Combretum petrophilum, as currently defined, constitutes populations from the Strydom Tunnel in the Abel
Erasmus Pass, Mariepskop, Loskop Dam, Doornkop and Mogol Nature Reserve. Leaves have an undulate margin,
the base is often asymmetric and subcordate; the often twisted apex tapers to a long, narrow acumen with a mucron
and is therefore described as apiculate.
Engler & Diels (1899) placed C. psidioides in sect. Glabripetalae, but Exell & Garcia (1970) and Stace
(1981) later transferred it to sect. Ciliatipetalae. Maurin et al. (2010) supports the latter placement. In the FSA
region, C. psidioides is represented by two subspecies: the typical one which occur in northern Botswana and
Namibia (Caprivi) and subsp. dinteri (Schinz) Exell from Angola, Namibia and Zimbabwe. Wickens (1971b)
described a third subspecies, subsp. psilophyllum. The isotype of subsp. psilophyllum, Haerdi 174/87 in PRE, shows
that the leaves are large, obovate, up to 80–125 × (32–)65–115 mm, with narrowly cuneate bases and are totally
glabrous on both sides, except for scales, and with network of reticulate venation prominently raised on both sides.
Specimens from the Chimanimani Mountains, Mozambique side, (T. Muller 1239 in SRGH) (Meg Coates Palgrave,
pers. com.) and Tunduru Dist., Tanzania (Greenway & Hoyle 8340 in PRE), belong to this taxon. They also match
Busse 325 (HBG, K), the type of C. anacardifolium from Tanzania, but this is an unpublished manuscript name used
by Adolf Engler.
Wickens (1971b) placed C. grandifolium F.Hoffm. in synonymy under C. psidioides subsp. psidioides. The
holotype of the former, Boehm 30a, was destroyed in World War II in Berlin, but a fragment of the isotype survived
in the Zürich Herbarium. The isotype shows large leaves which match specimens in the National Herbarium (PRE)
and Harare Herbarium (SRGH). These specimens are of tall trees with the bark very rough, grey, thick, corky and
deeply fissured, and with large leaves, (110–)120–240(–300) × (80–)130–160(–200) mm, densely hairy on midrib
and veins, but glabrous on the areoles. The leaf bases are usually cordate to truncate, but sometimes (as in the
isotype) are broadly cuneate. The fruit are up to 36 × 28 mm, with scales and a few scattered hairs. Young leaves are
sparsely glabrous and glutinous. It ranges from Tanzania, through Malawi, Zambia and Zimbabwe to Mozambique.
This form is here proposed as a distinctive subspecies of C. psidioides. See key to section Ciliapetala.
Nearly all specimens of the C. psidioides complex examined in PRE are either sterile or in fruit, the latter
which are crimson to blood red. An exception are collections from northern Zambia and the DRC (Milne-Redhead
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Annexes
2728, Robertson 138, Robson 142, Van Meel 4158), all with flowers only. The leaves, 62–115 × 30–48 mm, are very
thickly tomentose on both sides, whereas the midrib and lateral veins are very prominently raised on both sides, with
reticulate venation inconspicuous above, the apices tapering to an acute to acuminate point or when rounded with a
mucron, and the bases are broadly cuneate to rounded. These specimens represent a distinct entity and either
comprises a new subspecies of C. psidioides or belong to C. brachypetalum R.E.Fr.
Key to the species of Combretum section Ciliatipetala
Partly from Wickens (1971b) and Exell (1978)
1a Leaf apex usually apiculate and often twisted:
2a Leaf sparsely to densely pubescent on both surfaces; Namibia and Botswana C. apiculatum subsp. leutweinii
2b Leaves glabrous, or only margin and midrib with hairs; glossy, glutinous and sometimes sticky when young:
3a All leaves of plants with apiculate apices; leaf margin flat; often with hair-tuft domatia in axils of veins below;
leaf-base symmetrical; reticulate venation not prominent below; upper hypanthium 2–3 mm long; petal margin
ciliate; fruit 17–28 mm long; widespread
C. apiculatum subsp. apiculatum
3b Only few leaves of plants with apiculate apices, but margins often undulate; without hair-tuft domatia in axils of
veins below; leaf-base asymmetrical, rounded to subcordate; reticulate venation very prominent below; upper
hypanthium up to 1.5 mm long; petal margin glabrous, not ciliate; fruit 16–19 mm long; South Africa (Limpopo and
Mpumalanga)
C. petrophilum
1b Leaf apex round, obtuse, acute to acuminate, rarely apiculate:
4a Woody climbers
C. edwardsii
4b Multi-stemmed shrubs or single-stemmed trees:
5a Fruit glabrous except for scales, sometimes glutinous; bark of branchlets peeling off in large ± cylindrical or
hemicylindrical pieces revealing an exposed cinnamon-red surface:
6a Leaves obovate, bases cuneate, glabrous on both sides; Tanzania and Mozambique
C. psidioides subsp.
psilophyllum
6b Leaves oblong to oblanceolate to elliptic, bases broadly cuneate, or cordate to truncate, variously hairy on both
sides; FSA and tropical Africa:
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Annexes
7a Leaves usually more than 110 mm long C. psidioides subsp. grandifolium
7b Leaves usually less than 105 mm long; bases cuneate:
8a Leaves pubescent on the reticulation below, but glabrous on the areolae when mature
C. psidioides
subsp. psidioides
8b Leaves shortly tomentose on the reticulation and on the areole belowC. psidioides subsp. dinteri
5b Fruit densely to sparsely hairy, sometimes only on body or sometimes glabrous; bark of branchlets peeling off in
untidy, irregular, fibrous strips or threads:
9a Scales glistening; stipe up to 8 mm long; northern parts of Botswana and Namibia
C. albopunctatum
9b Scales not glistening; stipe up to 3(5) mm long; most southeastern parts of Botswana, Swaziland and South
Africa:
10a Plants with silky silvery appearance; usually multi-stemmed shrubs growning on rocks; leaves usually shorter
than 60 mm; reticulate venation not prominently raised below; fruit densely covered with longish appressed hairs
over whole surface
C. moggii
10b Plants without silky appearance; usually single-stemmed trees; leaves usually longer than 60 mm; reticulate
venation prominently raised below; fruit very sparsely hairy mainly on the body or glabrous, but densely covered
with scales
C. molle
11. Combretum albopunctatum Suess. in Mitteilungen der Botanischen Staatssammlung München 1: 336
(1953); Exell & Roessler: 7 (1966); Exell: 126 (1978); J.D.Carr: 29 (1988); M.Coates Palgrave: 795 (2002); Curtis
& Mannheimer: 490 (2005). Type: Namibia, Popa Falls, 1938, Volk 2105 [M (M0106663) e!, lecto., designated
here]. Figure 9.
Combretum sp. 2. in White: 287 (1962).
Note: Suessenguth, curator of the Botanische Staatssammlung, München from 1927–1955 (Stafleu & Cowan 1986),
mentioned two collections in the protologue of C. albopunctatum, namely Volk 2119 and 2105, which he must have
examined in the München Herbarium (M). Both syntypes were collected in Namibia, at the Popa Falls. Volk 2105
(two specimens in M) are available on the Aluka Library website and the better of the two (M0106663) which show
the characters described the best is here selected as the lectotype. An isosyntype, Volk 2119 is housed in PRE, but
unfortunately there is no specimen of the original syntype at M available on the Aluka Library.
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Distribution
Botswana, Namibia, Zambia, Zimbabwe.
NAMIBIA.—1821 (Andara): 12 km ESE of Andara to Okavango, (–AB), 25-04-1977, W. Giess 14898 (PRE);
Western Caprivi Strip, near Popa falls, (–BA), 06-1966, K.L. Tinley 1496 (PRE).
BOTSWANA.—1821 (Andara): Samochima Camp, ± 25 km S of Shakawe, Okavango River, (–BD), 26-04-1975,
Müller & Biegel 2274 (PRE, SRGH). 1823 (Siambisso): between Hunter’s Africa No. 2 Camp and Smith’s Camp, (–
BD), 06-11-197, P.A. Smith 1164 (PRE, SRGH). 1824 (Kachikau): Lower Ngwezumba, (–BD), 02-1938, O.B.
Miller 181/B (PRE). 1921 (Aha Hills): Botswana/Namibia boundary, (–AA), 22-03-1979, J.D. Carr 107 (PRE).
1923 (Maun): Motamini Island, Mborogha River, (–AC), 21-04-1976, P.A. Smith 1707 (PRE); Qoroque Island,
Santantadibe River, (–CB), 22-04-1976, P.A. Smith 1710 (PRE); 7 miles on Maun-Shorobe road, (–CD), 06-021964, A.M. Yalala 416 (PRE); The lip of the Thamalakane fault line, (–DC), 08-11-1972, P.A. Smith 249 (PRE,
SRGH). 1924 (Joverega): Nxai Pan, (–DD), 25-12-1971, P.A. Smith 173 (PRE). 2023 (Kwebe Hills): on Maun-Toten
road, (–AD), 10-03-1965, H. Wild & R.B. Drummond 6840 (PRE); Kgwebe Hills, (–CA), 10-01-1980, P.A. Smith
2943 (PRE). 2024 (Bushman Pits): Makgadikgadi Pans Game Reserve, (–AD), 02-05-1976, D.C. Biggs 273 (PRE);
Boteti River in Xhumaga-Sukwane area, (–CD), 11-12-1978, P.A. Smith 2593 (PRE, SRGH). 2022 (Lake Ngami): to
NW of Mabele-a-Pudi Hills on road to Sehitwa, (–CD), 20-03-1979, J.D. Carr 79 (PRE). 2122 (Kobe): Kobe Pan,
Farm 107, (–AA), 21-02-1970, R.C. Brown 8713 (PRE).
12a. Combretum apiculatum Sond. in Linnaea 23: 45 (1850); Sond.: 510 (1862); Dümmer: 164 (1913);
Bews: 146 (1921); Burtt Davy: 245 (1926); O.B.Mill.: 42 (1948); Exell: 3 (1961); Stace: 13 (1961); Exell &
Roessler: 7 (1966); Exell: 7 (1968); Exell & J.G.Garcia: 61 (1970); Wickens: 35 (1973); Exell: 129 (1978);
Vollesen: 53 (1980); J.D.Carr: 32 (1988); Pooley: 352 (1993); A.E.van Wyk & P.van Wyk: 328 (1997); McCleland:
456 (2002); M.Coates Palgrave: 796 (2002); Curtis & Mannheimer: 469 (2005). Type: South Africa, ?Gauteng,
Magaliesberg, Zeyher 553 (S e!, holo.; BM e!, K e!, P e!, SAM e!, TCD e!, W e!, iso.). Figure 10.
C. buchananii Engl. & Diels: 40 (1899). Type: Malawi, without precise locality, Buchanan 1263 (K e!,
lecto., designated here.).
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Annexes
C. apiculatum Sond. var. parvifolium Baker f.: 46 (1905). Type: Zimbabwe, Bulawayo, Eyles 1094 (BM,
holo.; SRGH, iso.).
C. glutinosum sensu Wood: 156 (1908), non Guill. & Perr.: 288 (1833) ex DC.: 21 (1828).
Note: Buchanan 1263 in Kew (K) is the only extant specimen, which is chosen here as the lectotype of C.
buchananii.
Distribution
Angola, Botswana, DRC, Kenya, Malawi, Mozambique, Namibia, South Africa (Gauteng, KwaZulu-Natal, Limpopo
Province, Mpumalanga, North-West), Swaziland, Tanzania, Zambia, Zimbabwe.
12b. Combretum apiculatum Sond. subsp. leutweinii (Schinz) Exell in Mitteilungen der Botanischen
Staatssammlung München 4: 3 (1961); Exell & Roessler: 8 (1966); Exell: 19 (1968); Exell: 195 (1970); Exell: 132
(1978); Curtis & Mannheimer: 471 (2005). Type: Namibia, Otjiwarongo, Waterberg, Mar. 1899, Dinter 413 (Z e!,
holo.). Figure 11.
C. leutweinii Schinz: 878 (1901).
C. kwebense N.E.Br.: 111 (1909); O.B.Mill.: 43 (1948). Type: Botswana, Ngamiland, Kwebe Hill, Lugard
48 (K e!, holo.).
Distribution
Botswana, Malawi, Mozambique, Namibia, Zambia, Zimbabwe.
NAMIBIA.—1712 (Posto Velho): Baynesberge, at Otjipemba, (–BB), 15-06-1965, W. Giess 8967 (PRE). 1713
(Swartbooisdrif): 64 km from Opuwo on road to Epembe, (–DA), 30-03-1979, J.D. Carr 146 (PRE). 1718 (KuringKuru): road between Katwitwi and Makambo Camp, (–AD), 09-12-1955, B. de Winter 3861 (PRE). 1723
(Singalamwe): Eastern Caprivi, Zipfel, Libumbo Dist., (–CC), 04-04-1975, H.J. Steyl 67 (PRE). 1917 (Tsumeb):
Farm Auros GR 595, (–DA), 14-11-1976, W. Giess 14795 (PRE); Farm Awagobib GR 45, (–DB), 12-03-1974, H.
Merxmüller & W. Giess 30238 (M, PRE). 1920 (Tsumke): Grootfontein Dist., W slopes of Aha Mountains, (–DB),
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Annexes
29-01-1958, R. Story 6356 (PRE). 2017 (Waterberg): Waterberg, on plateau at Police Station, (–AC), 20-04-1963,
W. Giess, O.H. Volk & B. Bleissner 6571 (PRE); Waterberg Plateau, Farm Bergtuine OTJ 455, (–AD), 21-07-1972,
W. Giess 12385 (PRE).
BOTSWANA.—1821 (Andara): plains near Tsodilo Hills, (–DB), 15-07-1963, C.H. Banks 58 (PRE). 1824
(Kachikau): Gubatsa Hills, (–CA), 24-10-1972, Biegel, G. Pope & B. Gibbs Russell 4049 (PRE, SRGH). 2022 (Lake
Ngami): Ngamiland, Nwako Pan area, (–DA), 23-04-1968, A. Boshoff & M. Mason 257 (PRE).
13. Combretum edwardsii Exell in Boletim da Sociedade Broteriana, sér. 2, 42: 19 (1968); Verhoeven &
Van der Schijff: 39 (1975); J.D.Carr: 59 (1988); Pooley: 354 (1993); McCleland: 460 (2002); M.Coates Palgrave:
800 (2002). Type: South Africa, KwaZulu-Natal, Impendle Dist., Lundy's Hill, upper edge of Umkomaas Valley,
Edwards 3147 (PRE!, holo.; K e!, NH e!, NU e!, iso.). Figure 9.
Distribution
South Africa (KwaZulu-Natal, Limpopo Province, Mpumalanga).
LIMPOPO PROVINCE.—2330 (Tzaneen): Woodbush, (–CC), 20-10-1919, N.M. Botha FDH2889 (PRE).
MPUMALANGA.—2430 (Pilgrim’s Rest): Mariepskop, Bedford road, Inkwane Forest, (–DB), 05-07-1961, H.P.
van der Schijff 5585 (PRE); Graskop Dist., ‘Fairyland’, next to Fanie Botha Trail, (–DD), 16-03-1978, P.R. Kruger
282 (PRE). 2531 (Komatipoort): Barberton Dist., Pedlars Bush, Farm Zeist, turnoff to Shiyalonuba Dam, (–CC), 0404-1979, E. Buitendag 1237 (PRE).
KWAZULU-NATAL.—2830 (Dundee): on Kranskop-Middeldrift road, (–DD), 12-02-1966, D. Edwards 3330
(PRE). 2929 (Underberg): Impendle Dist., Lundy’s Hill, upper edge of Umkomaas Valley, (–DB), D. Edwards 3147
(PRE). 2930 (Pietermaritzburg): Lions River Dist., Lions Bush Forest, (–AC), 18-05-1964, E.J. Moll 813 (PRE);
Karkloof Forest, near Morton’s Bush, (–AD), 30-01-1990, J.O. Wirminghaus 1144 (PRE); Lions River Dist., Dargle
area, near Kilgobbin Cottage, (–CA), 14-04-1984, K. Balkwill & M-J. Cadman 1418 (NU, PRE); Lions River Dist.,
Farm Maritzdaal, Dargle, (–CB), 21-05-1963, D. Edwards 3139 (PRE); Krantzkloof Nature Reserve, (–DD), 23-011969, J.H. Ross 1892 (NH, PRE). 3029 (Kokstad): Polela Dist., Ingwangwane Forest Reserve, (–BA), 17-04-1958,
H.C. Taylor 2129 (PRE). 3030 (Port Shepstone): Port Shepstone Dist., Mgai Farm, (–BC), 18-12-1980, H.B.
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Annexes
Nicholson 2122 (PRE); Umtamvuna Nature Reserve, Smedmore krans, (–CC), 11-07-1982, A. Abbott 82 (PRE).
3130 (Port Edward): Umtamvuna Nature Reserve, 20 km NW of Port Edward on Izingolweni road, (–AA), 20-051982, H.B. Nicholson 2250 (PRE).
14. Combretum moggii Exell in Boletim da Sociedade Broteriana, sér. 2, 42: 21 (1968); J.D.Carr: 98
(1988); Hennessy: t. 2027 (1991a); McCleland: 464 (2002); M.Coates Palgrave: 805 (2002). Type: South Africa,
Mpumalanga, Middelburg Dist., Olifants River gorge, Farm Slaghoek, 126.20 miles NW, Oct. 1953, Mogg 22400
(PRE!, holo.; BM e!, J, K e!, iso.). Figure 12.
Distribution
South Africa (Gauteng, KwaZulu-Natal, Limpopo Province, Mpumalanga), Swaziland.
LIMPOPO PROVINCE.—2229 (Waterpoort): Swarthoek, N of Hanglip Forest Reserve, (–DD), 07-10-1985, M.
Poynton 19428 (PRE). 2230 (Messina): Tsanda road in Soutpansberg, (–CB), E. van Wyk EVW0117 (PRE); Venda,
Farm Seville 250 MT, (–CC), 03-11-1979, A.E. van Wyk 2944 (PRE); Sibasa Dist., Tate Vondo Forest Reserve, (–
CD), 14-12-1976, G. Hemm 36 (PRE). 2329 (Pietersburg): Lejuma, slopes of Soutpansberg, (–AB), 14-02-1958, B.
de Winter 6008 (PRE); Farm Holworth 783 MS, (–BB), 14-01-1987, P. Raal & G. Raal 1332 (PRE). 2427
(Thabazimbi): Thabazimbi Dist., Kransberg, (–BC), 17-03-1980, R.H. Westfall 998 (PRE). 2428 (Nylstroom):
Naboomspruit Dist., Farm Stepping Stones, 26 miles NW of Naboomspruit, (–BA), 10-10-1972, A.O.D. Mogg
37502 (PRE); Waterberg, Palala, Farm Bokpoort 312, (–BC), 07-11-1978, G. Germishuizen 949 (PRE). 2429
(Zebediela): near Pietersburg, Chuniespoort, 30 km from Pietersburg, (–BA), 29-09-1995, M.H. Steyn PRE61956
(PRE). 2430 (Pilgrim’s Rest): Lekgalameetse Nature Reserve, Malta, (–AB), 03-04-1986, M. Stalmans 1215 (PRE);
Blyde Nature Reserve, Farm Steenveld 229 KT, (–DA), 1980, S.P. Fourie 1332 (PRE); Pilgrim’s Rest Dist., Farm
Clermont, (–DB), 22-02-1963, L.E. Codd 10326 (PRE).
NORTH-WEST.—2527 (Rustenburg): Silkaatsnek, Magaliesberg range, (–DB), 25-11-1951, J.E. Repton 3861
(PRE).
GAUTENG.—2528 (Pretoria): Cullinan Dist., Farm Doringkraal, (–DA), 27-03-1980, G.H. Burger 596 (PRE);
Bronkhortspruit Dist., Farm Kranspoort, (–DB), 15-01-1995, H.F. Glen 3743 (PRE).
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Annexes
MPUMALANGA.—2529 (Witbank): Middelburg Dist., 17 miles NW of town, S of road to Loskop Irrigtion Dam,
(–AB), 29-04-1944, A.O.D. Mogg 17300 (PRE); Middelburg Dist., Farm Doornkop 273 JS, (–CB), 25-01-1968, C.J.
du Plessis 279 (PRE).
SWAZILAND.—2631 (Mbabane): Malolotja Nature Reserve, upper Mahulungwane Falls, (–AA), 01-04-1987, L.M.
Heath 560 (PRE).
KWAZULU-NATAL.—2731 (Louwsburg): Vryheid Dist., Coronation, Farm Paris 13437, 23 km N of Coronation
above the Bivane River, (–CA), 20-02-1997, N.H.G. Jacobsen 5492 (PRE).
15. Combretum molle R.Br. ex G.Don in Transactions of the Linnean Society of London 15: 431 (1827);
F.W.Andrews: 201 (1950); Exell: 7 (1968); Exell & J.G.Garcia: 62 (1970); Wickens: 33 (1973); Exell: 127 (1978);
Vollesen: 53 (1980); Liben: 18 (1983); J.D.Carr: 102 (1988); Pooley: 356 (1993); Thulin: 249 (1993); Vollesen: 118
(1995); A.E.van Wyk & P.van Wyk: 334 (1997); McCleland: 466 (2002); M.Coates Palgrave: 806 (2002). Type:
Ethiopia, without locality, Salt s.n. (BM e!, holo.). Figure 11.
C. velutinum DC.: 20 (1828). Type: Guinea, collector unknown (P e!, holo.).
C. ferrugineum A.Rich.: 267 (1847). Type: Ethiopia, Selassaquilla, Schimper 767 (P e!, holo.; BR e!, K, W
e!, iso.).
C. gueinzii Sond.: 43 (1850); Sond.: 509 (1862); Engl. & Diels: 38 (1899); Dümmer: 116 (1913); Bews:
147 (1921); F.W.Andrews: 202 (1950). Type: South Africa, KwaZulu-Natal, Durban [Port Natal], 'in silvis',
Gueinzius 567 (S, holo.; K e!, SAM e!, TCD e!, iso.).
C. holosericeum Sond.: 44 (1850); Sond.: 510 (1862); M.A.Lawson: 430 (1871); Dümmer: 116 (1913);
Burtt Davy: 247 (1926); O.B.Mill.: 43 (1948). C. guenzii Sond. var. holosericeum (Sond.) Exell ex Rendle: 93
(1932). Type: South Africa, ?Gauteng, 'Magalisberg', Zeyher 575 (S e!, holo.; BM e!, K, fragment, e!, P, fragment,
e!, PRE!, SAM e!, W e!, WU, fragment, e!, Z e!, iso.).
C. splendens Engl.: 289 (1895). C. gueinzii Sond. subsp. splendens (Engl.) Exell ex Brenan: 137 (1947).
Type: Malawi, locality unknown, Buchanan 859 (K e!, lecto., designated here).
C. welwitschii Engl. & Diels: 40 (1899). Type: Angola, Cuanza Norte, Golungo Alto, near banks of rivulet
Quiposa, not far from Canguerasange, Welwitsch 4318 [LISU e!, lecto., designated by Garcia (1961); BM e!, BR e!,
G e!, P e!, isolecto.].
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C. galpinii Engl. & Diels: 41 (1899); Dümmer: 147 (1913); Burtt Davy: 246 (1926). Type: South Africa,
Mpumalanga, Barberton Dist., Avoca, near Barberton, Galpin 1112 (Z e!, lecto., designated her; BOL, K e!, NH e!,
PRE!, SAM e!, Z e!, isolecto.).
C. obtusatum Engl. & Diels: 58 (1899). Type: Angola, Lubango, Huila, Antunes A50,61 [BM fragment, e!,
lecto., designated by Exell & Garcia (1970); COI, isolecto.].
C. dekindtianum Engl.: 136 (1902). Type: Angola, Lubango, Huila, Dekindt 51 [LUA, lecto., designated by
Exell & Garcia (1970)].
C. arengense Sim: 62, tab. 63, fig. B (1909). Type: Mozambique, Maganja da Costa, Sim 5916 (probably =
Sim 20902) (NU e!, holo.; PRE!, iso.).
C. ellipticum Sim: 63, tab. 63, fig. D (1909). Type: Mozambique, without precise locality, Sim 6068 (NU e!,
holo.; K e!, PRE!, iso.).
Note: In their protologue of C. galpinii Engler & Diels (1899) mentioned Galpin 112 in the Zürich Herbarium (Z)
and Wood 6547 in Berlin Herbarium (B). The Galpin specimen in Z is the only specimen that survived. It was
examined by Engler and Diels and is therefore chosen as lectotype.
Engler (1895) cites syntypes from Tanzania and Malawi in his protologue of C. splendens, but only an
isotype of Buchanan survived in Kew, which is here chosen as the lectotype.
Distribution
Benin, Botswana, Burkina Faso, Cameroon, Cote d'Ivoire, Ethiopia, Ghana, Guinea, Guinea-Bissau, Kenya, Malawi,
Mozambique, Nigeria, Sierra Leone, Somalia, South Africa (Free State, Gauteng, KwaZulu-Natal, Limpopo
Province, Mpumalanga, North-West), Sudan, Swaziland, Tanzania, Togo, Uganda, Zambia, Zimbabwe; also Saudi
Arabia and Yemen.
16. Combretum petrophilum Retief in Bothalia 16: 44 (1986); J.D.Carr: 124 (1988); McCleland: 468
(2002); M.Coates Palgrave: 809 (2002). Type: South Africa, Limpopo Province, Strydom Tunnel, Oct. 1982, Carr
203 (PRE!, holo.; K, MO e!, iso.). Figure 13.
Distribution
South Africa (Limpopo Province).
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Annexes
17. Combretum psidioides Welw. in Annaes Conselho Ultramarino, sér. 1, 24: 249 (1856); Exell: 5 (1961);
Exell & Roessler: 10 (1966); Exell: 8 (1968); Exell & J.G.Garcia: 64 (1970); Wickens: 36 (1971b); Wickens: 37
(1973); Exell: 133 (1978); J.D.Carr: 135 (1988); A.E.van Wyk & P.van Wyk: 336 (1997); M.Coates Palgrave: 810
(2002); Curtis & Mannheimer: 484 (2005). Type: Angola, 'in dumetosis interioris Provinciae Angolensis, rarioir
avis. Arbuscula elegans filiis maximis, habitu exacte Psidiorum. Quicuze', Welwitsch 4378 (LISU e!, holo.; BM, BR
e!, COI, K e!, P e!, iso.). Figure 14.
17a. subsp. psidioides
Distribution
Angola, Botswana, Namibia, Zimbabwe.
NAMIBIA.—1720 (Sambio): 80 km W of Mukuwi on road from Andara to Rundu, (–CD), 25-03-1979, J.D. Carr
115 (PRE). 1722 (Chirundi): Western Caprivi, near Bwabwata N boundary, (–DC), 06-1966, K.L. Tinley 1478
(PRE). 1723 (Singalamwe): Eastern Caprivi, Zipfel, Singalamwe area, (–CB), 30-12-1958, D.J.B. Killick & O.A.
Leistner 3207 (PRE). 1724 (Katima Mulilo): Eastern Caprivi, Impola, (–AD), 1969, D.C. McFerren 8a (PRE);
Eastern Caprivi, Katima Mulilo, ± 40 km W of Katima Mulilo, (–CA), 22-04-1993, P. van Wyk BSA916 (PRE,
PRU); Katima Mulilo, 6 km S on road joining Liyanti road, (–DA), 17-04-1993, P. van Wyk BSA905 (PRE, PRU).
1817 (Tsintsabis): ± 40 miles SE of Ondangua on road to Namutoni, near Omuramba Ovambo, (–DA), 13-02-1959,
B. de Winter & W. Giess 6961 (PRE). 1820 (Tarikora): Kavango, 1.5 km S of Ndiyona Rest Camp, (–BB), 21-041977, M. Müller & W. Giess 444 (PRE). 1821 (Andara): Shitangadimba Camp, near Andara Mission Station, (–AB),
16-01-1956, B. de Winter & H.J. Wiss 4267 (PRE). 1823 (Siambisso): Lizauli, (–AB), 20-03-1974, H.J. Steyl 21
(PRE). 1920 (Tsumkwe): Kaukauveld, 1.5 km S Diederichs Kreuz, near Botswana Boundary, (–DD), 17-04-1967,
W. Giess 9881 (PRE).
BOTSWANA.—1724 (Katima Mulilo): Chobe Dist., 12 miles SW of Kabulabula, (–DD), 05-1952, O.B. Miller
B/1318 (PRE). 1821 (Andara): 6 km S of Shakawe (–BD), 24-04-1975, Müller & Biegel 2257 (PRE). 1822
(Kangara): near Seronga road at Gwiligwa, (–DB), 19-10-1979, P.A. Smith 2851 (PRE, SRGH). 1823 (Siambisso):
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near Movembe Village, (–AA), 15-02-1983, P.A. Smith 4051 (PRE); Okavango Swamps, Kwando area, Alab Dunes,
(–BC), 15-03-1971, P.A. Smith 85 (PRE). 1921 (Aha Hills): XaiXai-Quangwa roadside (–CC), 25-04-1980, P.A.
Smith 3433 (PRE, SRGH); 32 km W of Nokaneng, (–DB), 21-03-1979, J.D. Carr 96 (PRE).
17b. subsp. dinteri (Schinz) Exell in Mitteilungen der Botanischen Staatssammlung München 4: 3 (1961);
Exell & Roessler: 10 (1966); Exell & J.G.Garcia: 66 (1970); Wickens: 38 (1971b); Exell: 135 (1978); J.D.Carr: 135
(1988). Type: Namibia, Hereroland, Apr. 1899, Dinter 580 (Z e!, holo.). Figure 6.
C. dinteri Schinz: 877 (1901).
C. quirirense Engl. & Gilg: 318 (1903). Type: Angola, Bié, Quiriri River, Baum 722 [B, holo.†; BM e!,
lecto., designated by Exell & Garcia (1970); BR e!, COI, E e!, HBG e!, K, S e!, W e!, Z e!, isolecto.].
C. omahekae Gilg & Dinter ex Engl.: 698 (1921). Type: Namibia, Omaheke, ‘bei Otjituo und Naitsas’ (type
not traced).
Distribution
Angola, Namibia, Zambia, Zimbabwe.
NAMIBIA.—1715 (Ondangua): 5 miles E of Oshikango near Ondipa Mission Station, (–BD), B. de Winter & W.
Giess 6999 (PRE). 1716 (Enana): 33 km E of Oshikango, (–AC), 23-02-1973, R.J. Rodin 8978 (PRE); 104 km E of
Oshikango, (–BD), 19-04-1973, R.J. Rodin 9310 (PRE); Oshikango - Eenhana road, (–CB), 05-04-2002, M.M. Uiras
MU622 (PRE). 1718 (Kuring-Kuru): 1 mile W of Katwitwi, (–AD), 09-12-1955, B. de Winter 3854 (PRE);
Nkurenkuru, 3 km S of Nkurenkuru, (–DA), 18-07-1976, D. Edwards 4446 (PRE). 1719 (Runtu): Okavango, 5 miles
of Runtu on road to Kapako, (–DC), 29-11-1955, B. de Winter 3726 (PRE); Grootfontein North, Omuramba, S of
Mavanze, (–DD), 13-03-1958, H. Merxmüller & W. Giess 2149 (PRE). 1818 (Tsitsib): Grootfontein Dist., Choantsas
Farm, (–CC), 11-04-1973, O.H. Volk 238 (PRE); Grootfontein, Farm 1047 on road D3016 next to road at waterpoint,
(–DC), 25-02-2001, W.J. Friederich FR12/77 (PRE). 1917 (Tsumeb): Tsumeb Dist., Farm Ombanje 787 GR, (–BC),
14-11-1976, W. Giess 14803 (PRE); Tsintsabis Kuringkuru (–DD), 01/02-1934, E.B. Schoenfelder S531 (PRE). 1918
(Grootfontein): Neitsas, (–BA), 09-04-1939, O.H. Volk 419 (PRE). 1920 (Tsumkwe): Grootfontein Dist., ± 30 miles
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N of Gautscha Pan, (–BC), 10-02-1958, R. Story 6461 (PRE); Tsumkwe, 6 km NW of Tsumkwe, (–DA), 03-041990, D.S. Hardy 7122 (PRE); Kaukauveld, Aha Mountains, (–DD), 17-04-1967, W. Giess 9891 (PRE). 2017
(Waterberg): Waterberg Plateau Park, (–AC), 24-07-1976, M. Müller 321 (PRE); Waterberg Plateau, Farm Onjoka
333 OTJ, (–AD), 20-07-1972, W. Giess 12365 (PRE); Grootfontein Dist., Farm Omega 978 GR, (–BB), 07-05-1967,
W. Giess 10139 (PRE); Grootfontein Dist., Farm Biesiespan 971 GR, (–BC), 7-05-1967, W. Giess 10146a (PRE).
2018 (Gunib): Hereroland, Otjituuo Reserve 235, 6 km E of Ovitjete Fountain, (–AB), 08-07-1976, D. Edwards
4404 (PRE); Otjozondjupa, (–CB), 09-05-2001, B.A. Curtis 962A (PRE). 2019 (Eiseb): Omaheke, (–AB), 11-052001, B.A. Curtis 1022 (PRE). 2119 (Epukiro): Epukiro, (–CA), 04-1970, J. MacKenzie 30 (PRE).
17c. subsp. psilophyllum Wickens in Kew Bulletin 26: 39 (1971b); Wickens: 38 (1973). Type: Tanzania,
Ulanga Dist., Ifakara, Haerdi 174/87 (K e!, holo.; EA e!, PRE!, iso.).
Distribution
Tanzania and probably Mozambique.
TANZANIA.—Tunduru Dist., Matamanda to Songea Road, Greenway & Hoyle 8340 (PRE).
17d. subsp. grandifolium (F.Hoffnm.) Jordaan, stat. nov.
C. grandifolium F.Hoffnm. in Beiträge zu Kenntnis der Flora von Central-Ost-Afrika: 29 (1889); Engl.: 289
(1895); Engl. & Diels: 39 (1899); Engl.: 698 (1921). Type: Tanzania, Mpanda Dist., Pa-Kabombue, Boehm 30a (B,
holo.†; Z fragment, e!, iso.).
Distribution
Malawi, Mozambique, Tanzania, Zambia, Zimbabwe.
MALAWI.—Locality unknown, Smuts 2078, 2277 (PRE).
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Annexes
MOZAMBIQUE.—From frontier to Amaramba flats, A.J.W. Hornby 2413 (PRE, SRGH). SW Niassa, A.J.W.
Hornby 2611 (PRE). Zambezia Dist., Bowbrick BA625 (SRGH).
ZAMBIA.—Abercorn Dist., Katenga Falls, Ricards 10035 (SRGH), Abercorn Dist., Lungwe Electric Power Station,
Ricards 19084 (SRGH). Kasama, J.H. van Rensburg 3034 (SRGH). Ndola, J. Lemmer 13539 (PRE). Luangwa South
Game Reserve, J. Uys 2/65 (SRGH).
ZIMBABWE.—Mrewa Dist., Mangwende T.T.L., just E of Shamva River, Orpen 200,971 (PRE, SRGH). Melsetter
Dist., Martin Forest Reserve, L.J. Mullin 1/52 (PRE, SRGH).
TANZANIA.—Mbeya Dist., Pungaluma Hills, 08° 47´ S 33° 15´ E, C.J. Kayombo 976, 977 (MO, PRE). Magangwe,
Rangers Post, Greenway & Kanuri 14299 (PRE).
GROUP 2
Species with large scales, usually larger than 100 µm, divided by many radial and tangential walls (Figure 2).
VI. Combretum section Hypocrateropsis Engl. & Diels
Species in this section are woody climbers, scramblers or sometimes trees, usually multi-stemmed and without
spinescent tipped lateral branches. The scales on the leaves are the largest in Combretum and are circular, divided by
many radial and tangential walls.
Engler & Diels (1899) described two species: (i) Combretum tenuipes from a plant collected at Louw’s
Creek in the Barberton District and (ii) C. padoides from a plant collected in Mozambique. C. tenuipes was
subsequently placed in synonymy with C. padoides by Exell (1968, 1970, 1978), Wickens (1973), Carr (1988) and
Rodman (1990). Rogers (1989) conducted chemotaxonomic studies on the leaves of C. padoides (his “coastal form”)
and C. tenuipes (his “inland form”). He found significant differences between the oxidation states of some of the
compounds isolated from coastal and inland trees and suggests that the differences could be due to geographic or
genetic factors and need to be investigated further. Rogers’s samples of his “inland species” came from a plant
growing in the Pretoria National Botanic Gardens, which is without any doubt C. tenuipes. Samples of his “coastal
species” came from a tree in Durban, grown from seed originating from a tree growing in the National Botanic
Gardens, Harare, Zimbabwe. C. tenuipes is confined to the Barberton Centre of Endemism (Van Wyk & Smith
2001) whereas C. padoides grows in eastern tropical Africa, from Kenya southwards to Tanzania, Malawi, Zambia,
eastern Zimbabwe, Mozambique, as well as the DRC and just enters South Africa into the far most northern parts of
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Limpopo Province. Pooley (1993) included C. padoides as occurring in KwaZulu-Natal and the accompanied photos
to illustrate the species were taken in the Pretoria National Botanical Garden which means that the photos depict C.
tenuipes. C. padoides has not yet been recorded in KwaZulu-Natal, but there is a new, undescribed species of
Combretum growing as a climber in the sand forest of Maputaland with which it may be confused. However, this
new species does not belong to section Hypocrateropsis. C. tenuipes and C. padoides are here reinstated as separate
species since there are several differences, including geographical (map 1), molecular (Maurin et al. 2010) and
morphological (see the key) to distinguish between them.
Exell (1968) described a third subspecies of C. celastroides, namely C. celastroides subsp. orientale based
on a plant from Mozambique, collected by Schlechter at Maputo [Delagoa Bay]. Schlechter 11957 is also one of the
syntypes of C. patelliforme Engl. & Diels (1899). The other syntype of C. patelliforme is from Angola, namely
Antunes A155, which was destroyed in World War II, but this belongs to subsp. celastroides. The two subspecies of
C. celastroides in the FSA region, the typical subspecies and subsp. orientale, are quite different morphologically
and this is supported by molecular evidence (Maurin et al. 2010) and the fact that the two taxa are geographically
disjunct. Hence C. celastroides subsp. orientale is elevated to species level as C. patelliforme Engl. & Diels. See the
key for differences between it and subsp. celastroides. C. celastroides subsp. laxiflorum (Welw. ex M.A.Lawson)
Exell has larger flowers than the other subspecies, the leaves are nearly glabrous, and it is usually a tree. It occurs in
Zambia, Angola, Tanzania and DRC.
Key to the species of Combretum section Hypocrateropsis
1a Disc glabrous:
2a Leaves pubescent (hairs present on entire leaf surface) below; disc up to 4 mm in diam.; fruit ± 18–20 × 17–22
mm; peg ± 1.0–2.5 mm long; Caprivi, Botswana
C. celastroides
2b Leaves almost glabrous below (except for hair-tuft domatia in axils of veins below); disc 2.0–2.5 mm in diam.;
fruit ± 15 × 15 mm; peg up to 1 mm long; Limpopo Province, KwaZulu-Natal
C. platelliforme
1b Disc pilose:
3a Ultimate twigs hairy; leaves narrowly elliptic, usually longer than 55 mm; margin flat, principal lateral veins in ±
5–8 pairs; fruit usually larger than 17 × 17 mm; Limpopo Province
C. padoides
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3b Ultimate twigs glabrous; leaves ovate, usually shorter than 45 mm; margin markedly wavy; principal lateral veins
3(4) pairs; fruit usually 15 × 15 mm or smaller; Mpumalanga and Swaziland (Barberton Centre of Endemism)
C. tenuipes
18. Combretum celastroides Welw. ex M.A.Lawson in Flora of tropical Africa 2: 422 (1871); Engl. &
Diels: 12 (1899); O.B.Mill.: 42 (1948); F.White: 284 (1962); Exell & Roessler: 8 (1966); Exell: 16 (1968); Exell:
168 (1970); Exell & J.G.Garcia: 50 (1970); Wickens:17 (1973); Exell: 107 (1978); J.D.Carr: 45 (1988); M.Coates
Palgrave: 798 (2002); Curtis & Mannheimer: 472 (2005). Type: Angola, Huila, Welwitsch 4370 [LISU, lecto.,
designated by Exell & Garcia (1970); BM e!, BR e!, COI, K e!, P e!, PRE!, isolecto.]. Figure 15.
C. patelliforme Engl. & Diels: 12, t. 1, fig. C (1899) pro parte quoad specim. Antunes A155 (B†).
Distribution
Angola, Botswana, Mozambique, Namibia, Tanzania, Zambia, Zimbabwe.
NAMIBIA.—1714 (Ruacana Falls): Ruacana, plateau S of mountain pass leading to Ruacana waterfall, (–AD), 1401-1994, P. van Wyk BSA1724 (PRE, PRU); 2 miles S of Otjekua, (–CA), 13-06-1963, W. Giess & H. Leippert 7581
(PRE). 1718 (Kuring-Kuru): 10 miles NW of Kuring-Kuru, (–DA), 05-1960, C.J. Esterhuyse 441 (PRE). 1723
(Singalamwe): Eastern Caprivi, Zipfel, (–CC), 30-12-1958, D.B. Killick & O.A. Leistner 3204 (PRE); Eastern
Caprivi, Singalamwe, ± 20 km E of the Kwando River, (–CD), 11-01-1986, C.J.H. Hines 533 (PRE); Western
Caprivi, Kwando floodplain area, (–DC), 12-05-1966, K.L. Tinley 1427 (PRE). 1724 (Katima Mulilo): Eastern
Caprivi, Katimo Mulilo, (–AD), 30-01-1975, Vahrmeijer & Du Preez 2510 (PRE). 1817 (Tsintsabis): Omytheya, 15
km N of 61 Mech. Inf. Batt. Grp. Camp, 04-09-1989, (–AC), J.A. Bodenstein 619 (PRE). 1818 (Tsitsib): Okavango
Reserve, 30 km S of Omaheke Omuramba, (–AC), 19-07-1976, D. Edwards 4449 (PRE); Easten Caprivi, Mpacha,
(–CA), 27-07-1975, D. Edwards 4337 (PRE); Kavango, Mangetti Quarantine Area, (–DA), 01-1994, Horn 167
(PRE).
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BOTSWANA.—1725 (Livingstone): Chobe Dist., Serondela, (–CC), 01-1952, O.B. Miller B/1274 (PRE);
Kazungula, Mukusi forest, (–CD), 01-1936, O.B. Miller B/106 (PRE). 1824 (Kachikau): Savuti, Chobe National
Park, (–CA), 25-03-1984, N.H.C. Jacobsen 3122 (PRE).
19. Combretum padoides Engl. & Diels in Monographieen Afrikanischer Pflanzenfamilien und Gattungen
3: 13 (1899); Exell: 7 (1968); Wickens: 17 (1973); Exell: 168 (1970): Exell: 107 (1978); Vollesen: 53 (1980);
J.D.Carr: 17 (1988); Thulin: 248 (1993); Pooley: 354 (1993); McCleland: 468 (2002), pro parte; M.Coates Palgrave:
808 (2002). Type: Mozambique, Zambezi, Boroma, Menyharth 878 [Z e!, lecto., designated by Exell (1970); K e!,
WU e!, isolecto.]. Figure 16.
C. homblei De Wild.: 196 (1914). Type: Democratic Republic of the Congo, Katanga, Kapiri Valley, 1913,
Homblé 113 (BR e!, holo.; BM, fragment, e!, iso.).
C. minutiflorum Exell: 245 (1930). Type: Tanzania, Kilosa Dist., Kipera [Kipela], Oct. 1921, Swynnerton
s.n. (BM e!, holo.).
Distribution
DRC, Kenya, Malawi, Mozambique, Somalia, South Africa (Limpopo Province), Tanzania, Zambia, Zimbabwe.
LIMPOPO PROVINCE.—2230 (Messina): Messina – Pafuri, Madimbu Reserve, on banks of Limpopo River near
army quarters, (–BD), 22-05-1997, M.H. Steyn 13 (PRE); Venda, Tshikondeni ridge, (–DB), 23-01-2000, M.C.
Lötter 753 (PRE), Mutele “B” on the way from Dulutulu to Ha-Mutele, (–DB), 14-08-2001, E. van Wyk & P.M.
Gavhi ewv353 (PRE). 2231 (Pafuri): Pafuri, Mutale River/Levubu River confluence, (–AC), 15-12-1992, N. van
Rooyen & G.J. Bredenkamp 609 (PRE, PRU); Kruger National Park, Madzaringwe mouth, along Levubu River, (–
CA), P. van Wyk 4763 (PRE); Punda Maria [Punda Milia], (–CA), 19-03-1968, R. Verhoeven 61 (PRE); Kruger
National Park, near Pafuri on Njala road, (–DC), 18-8-1993, C.B.S. van der Merwe 62 (PRE).
20. Combretum platelliforme Engl. & Diels in Monographieen Afrikanischer Pflanzenfamilien und
Gattungen 3: 12, t. 1, fig. C (1899); Dümmer: 183 (1913). Type: Mozambique, Delagoa Bay [Maputo], Schlechter
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11957 [BM e!, lecto., designated by Exell (1968); BOL, BR e!, COI, E e!, HBG e!, K e!, L e!, MO e!, P e!, PRE!,
SAM, WAG e!, Z e!, iso.]. Figure 15.
C. celastroides Welw. ex M.A.Lawson subsp. orientale Exell: 16 (1968); Wickens: 17 (1973); Exell: 107
(1978); J.D.Carr: 45 (1988); Pooley: 354 (1993); McCleland: 458 (2002).
Note: Engler & Diels (1899) described three species in this section, C. platelliforme, C. padoides and C. tenuipes. In
the protologue of C. platelliforme two syntypes are cited: Antunes A155 from Angola and Schlechter 11957 from
Mozambique. The specimen from Angola belongs now to C. celastroides subsp. celastroides and Mozambique
specimern to C. platelliforme, pro parte. Exell (1968) reduced this name to subspecific level and prefer to use a new
ephitet, namely orientale and lectotypified this name with the Schlechter specimen. Once this taxon is elevated now
to species level the old epithet platelliforme must be used, because no name has priority outside its rank according to
the International Code of Botanical Nomenclature (Vienna Code): 11.2 (McNeill et al. 2006).
Distribution
Mozambique, South Africa (KwaZulu-Natal, Limpopo Province), Tanzania, Zambia, Zimbabwe.
LIMPOPO PROVINCE.—2231 (Pafuri): SE of Klopperfontein at Mozambique border, (–CA), 29-04-1953, H.P.
van der Schijff 2898 (PRE); Pafuri, Wambia sandveld, (–CB), 29-02-1984, D.J. Botha 3401 (PRE); Vlakteplaas, 1.4
km N of Sisal/Shirhombe crossing, (–CB), 22-01-1995, J.L. van der Walt 9510 (PRE); Pafuri, Nwambiya sandveld,
(–CB), 03-04-1994, P. van Wyk BSA2029 (PRE, PRU); Kruger National Park, Dzundzwini Hill, 2 miles SE of Punda
Maria, (–CC), 01-11 -1948, L.E. Codd & R.A. Dyer 4585 (PRE), Kruger National Park, Dzundwini, (–CC), 19-021954, H.P. van der Schijff 2151 (PRE).
KWAZULU-NATAL.—2632 (Bela Vista): Tembe Elephant Park, (–CD), 03-03-1988, M.C. Ward 2286 (NH, PRE);
6 km W of Muzi (–CD), 07-06-1972, Moll & Muller 5688 (NH, PRE); 8 km W of Muzi Border Post, (–CD), 09-031972, Moll 5655 (NH, PRE); Tembe Elephant Park, (–DC), 20-04-1988, M.C. Ward 2301 (NH, PRE).
21. Combretum tenuipes Engl. & Diels in Monographieen Afrikanischer Pflanzenfamilien und Gattungen
3: 13, t. 3, fig. b (1899); Dümmer: 182 (1913); Burtt Davy: 246 (1926). Type: South Africa, Mpumalanga, Barberton
Dist., Louws Creek, Galpin 885 (Z e!, holo.; BOL, K e!, PRE!, SAM e!, iso.). Figure 16.
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Annexes
Distribution
South Africa (Mpumalanga) and probably Swaziland.
MPUMALANGA.—2531 (Komatipoort): Hectorspruit, Farm Thornhill 171 JU, (–BC), 18-04-1989, Krynauw 1351
(PRE); Louw’s Creek, (–CA), 12-1916, G. Thorncroft TVM22210 (PRE); Kaapmuiden Dist., Farm Three Sisters 254
JV, near Louw’s Creek, (–CB), 04-05-1989, G.J. Ley 154 (PRE); 7 km from Holnekt, Louw’s Creek road towards
Shiya-lo-Ngubo dam, (–CB), 23-03-1976, E.J. van Jaarsveld 1164 (PRE); off road from Malelane to Kaalrug, 8 km
on Louisville road to Louw’s Creek next road on left, (–DA), 15-04-1997, M.H. Steyn 17 (PRE).
VII. Combretum section Metallicum Exell & Stace
Species in this section are nearly always glutinous, especially when young. The scales on the leaves are usually
extensively divided by many radial and tangential walls to give raise of ± 10–40 marginal cells. The disc has a free,
pilose margin. The fruit are glabrous to densely hairy in C. collinum subsp. suluense, and are usually somewhat
‘metallic’ in colour.
Okafor (1967) recognised four subspecies of C. collinum in the FSA region. Carr (1988) regards the
separation of C. collinum into subspecies as unjustified because of the largely overlapping geographical distribution
patterns of these four subspecies. Here, however, we uphold the four subspecies as recognised by Okafor (1967). C.
coriaceum described by Schinz (1888) is conspecific with C. gazense and is the oldest validly published name for
this subspecies but not used by Okafor when he raised this taxon to subspecific rank.
There are four synonyms of subsp. suluense described earlier than 1899, but Okafor chosed to use the name
suluense over the other four (C. fischeri, C. brosigianum, C. fulvotomentosum and C. schinzii). Type material for C.
fisheri, C. brosigianum and C. fulvotomentosum had been destroyed and could be considered as uncertain names.
There is however an isotype of C. schinzii in Zürich Herbarium (Z) described in 1899 that could suffice as a
lectotype. It seems however that this taxon rather belongs to C. collinum subsp. ondongense (1899) and not C.
collinum subsp. suluense as stated by Rodman (1990).
Pooley (1993) gives a group of records for C. collinum subsp. suluense from around False Bay and Mkuze
Game Reserve, but specimens growing in these sand forest areas belong to an undescribed species. There is,
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Annexes
however, one specimen in the Natal Herbarium collected in the mountains north of Vryheid which gives the
distribution for subsp. suluense as far north as Kenya and southwards as far south as Swaziland and far northern
KwaZulu-Natal. C. collinum subsp. ondongense (Engl. & Diels) Okafor is confined to the Kalahari sands of Angola,
Namibia, Botswana, Zambia and eastern fringe of Zimbabwe, and has not been recorded in South Africa. The
holotype of subsp. taborense is based on Stuhlmann 506, collected in Tabora, Tanzania, but is destroyed in World
War II and no isotypes existed nor survived. Okafor was confident enough to use this name despite the lack of type
material. In absence of good material from Tanzania in the National Herbarium in Pretoria we have refrained from
selecting a neotype for this taxon.
Key to the species of Combretum sect. Metallicum
1a Leaves densely grey-hairy below; fruit glabrous; Namibia, Botswana, Limpopo Province and Mpumalanga
C. collinum subsp. gazense
1b Leaves glabrous below, except for hairs in axils of veins; fruit glabrous or hairy:
2a Fruit densely hairy, red scales conspicuous
C. collinum subsp. suluense
2b Fruit glabrous:
3a Leaf apices acute to acuminate to apiculate, lamina silvery below, with conspicuous darker venation; Limpopo
Province and Mpumalanga C. collinum subsp. taborense
3b Leaf apices rounded to subacute, lamina yellowish below, without conspicuous darker venation; Namibia,
Botswana
C. collinum subsp. ondongense
22a. Combretum collinum Fresen. subsp. gazense (Swynn. & Baker f.) Okafor in Boletim da Sociedade
Broteriana, sér. 2, 41: 145 (1967); Exell: 182 (1970); Wickens: 27 (1973); Coates Palgrave: 665 (1977); Exell: 120
(1978); J.D.Carr: 51 (1988); McCleland: 458 (2002); M.Coates Palgrave: 799 (2002); Curtis & Mannheimer: 474
(2005). Type: Mozambique, Gazaland, between upper Buzi and Mount Umtereni, Swynnerton 587 (BM e!, holo.; K
e!, Z e!, iso.). Figure 17.
C. gazense Swynn. & Baker f.: 68 (1911); Burtt Davy: 248 (1926); O.B.Mill.: 42 (1948); Codd: 129 (1951).
C. mechowianum O.Hoffm. subsp. gazense (Swynn. & Baker f.) Duvign.: 81 (1956).
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C. coriaceum Schinz: 247 (1888); Dinter: 169 (1919); O.B.Mill.: 42 (1948). Type: Namibia, Ngamigebiet,
1888, Fleck 422a (Z e!, holo.; K e!, iso.).
C. bajonense Sim: 63, t. 63 (1909). Type: Mozambique, Magenja da Costa, 1908, Sim 5715 (renumbered as
20901) (PRE!, holo.; NU, iso.).
C. eylesii Exell: 170 (1939). Type: Zimbabwe, Harare [Salisbury], Eyles 849 (BM e!, holo.; K e!, iso.).
Distribution
Botswana, DRC, Malawi, Mozambique, Namibia, South Africa (Limpopo Province, Mpumalanga), Tanzania,
Zambia, Zimbabwe.
NAMIBIA.—1713 (Swartbooisdrif): 5 km NW of Ohandungu, (–DC), 21-03-1974, H. Merxmüller & W. Giess
30445 (M, PRE). 1714 (Ruacana Falls): 35.9 miles from Tsandi on road to Ruacana Falls, (–AB), 14-11-1955, B. de
Winter 3644 (PRE); 15 km S of Ruacana, (–AC), 14-04-1966, W. Giess 9303 (PRE); Ruacana, flats S to SW of the
airport, (–AD), 10-07-1976, Leistner, Oliver, Steenkamp & Vorster 70 (PRE); Kaokoveld, between Ruacana and
Ohopoho, (–CA), 14-04-1966, W. Giess 9311 (PRE); 37km NW of Mahenene on tar road to Ruacana, (–DD), 24-011996, H.H. Kolberg 746 (PRE). 1717 (Omboloka): E Oshikoto, Okongo, Oshiweda Village, (–DC), 08-12-1997, M.
Seely SEE/47 (PRE). 1718 (Kuring-Kuru): 1 mile W of Katwitwi, (–AD), 09-12-1955, B. de Winter 3850 (PRE);
Kavango, Sitopogo, 12 miles E of Kurenkuru, (–DA), 04-12-1969, P.J. le Roux 1086 (PRE). 1719 (Runtu): 4 miles E
of Mission Station at Sambusu, (–CD), 02-10-1966, W. Giess 9515 (PRE); near Runtu by the Okavango River, (–
DD), 3-1973, R.J. Rodin 9139 (PRE). 1723 (Singalamwe): Singalamwe area, ± 70 miles from Katima Mulilo, (–CB),
30-12-1958, D.J.B. Killick & O.A. Leistner 3205 (PRE). 1724 (Katima Mulilo): Caprivi Strip, 3.5 miles E of Katima
Mulilo, (–AD), 13-02-1969, B. de Winter 9147 (PRE); Eastern Caprivi, Mpacha, (–CA), 27-02-1975, D. Edwards
4339 (PRE); 10 km S of Katima Mulilo, Kalumba area, (–CB), 24-03-1977, Cawood & Ward 9 (PRE); Katima
Mulilo Dist., 150 km S of Zambezi - ferry to Zambia, (–DA), 16-04-1993, P. van Wyk BSA900 (PRE, PRU); 13
miles NW of Ngoma, (–DC), 16-07-1952, L.E. Codd 7079 (PRE). 1817 (Tsintsabis): N of Omaramba Ovambo,
Farm Ondera, (–CB), 14-01-1981, D. Goosen 41 (PRE); Farm Vaalwater GR/TS 875, (–DA), 19-04-1978, W. Giess
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15108 (PRE); 16 km N of Tsintsabis, (–DB), 27-09-1966, W. Giess 9469 (PRE). 1818 (Tsitsib): 64 km N of
Tsintsabis, (–AB), 29-09-1966, W. Giess 9478 (PRE); Grootfontein, Farm 1047, on road D3016 next to waterpoint,
(–DC), 25-02-2001, W.J. Friederich FR12/79 (PRE); 65 miles from Grootfontein to Rundu, (–DD), 03-12-1973, J.V.
van Greuning 247 (PRE). 1820 (Tarikora): Kaukauveld, 12.5 km S of Kapupahedi, (–AB), 24-04-1967, W. Giess
10003 (PRE). 1821 (Andara): Shamvura Camp, 12.3 miles E of Nyangana Mission Station, (–AA), 10-01-1956, B.
de Winter & H.J. Wiss 4204 (PRE); at Dikundu, 19.2 km S of Andara, (–AB), 19-06-1971, W. Giess 11473 (PRE).
1918 (Grootfontein): Hereroland, Otjituuo Reserve, 3 km S of Otjituuo Depot, (–DA), 07-07-1976, D. Edwards 4395
(PRE). 1919 (Kanovlei): on road to Tsumkwe, (–AA), 08-03-1995, P.M. Burgoyne 3417 (PRE); on road to the
Omuramba Omataka, (–AD), 07-03-1995, P.M. Burgoyne 3358 (PRE). 1920 (Tsumkwe): 17 km N of Klein Dobe, (–
AD), 08-06-1985, Botha & Bredenkamp 3608 (PRE); Grootfontein Dist., near Tsumkwe, (–DA), 16-12-1966, I.
Kruger s.n. (PRE); Nama Pan, (–DC), 22-08-1955, R. Story 5270 (PRE). 2017 (Waterberg): Waterberg Plateau Park,
(–AC), 24-07-19 76, M. Müller 322 (PRE); Waterberg Plateau, Farm Onjoka, OTJ 333, (–AD), 20-07-1972, W.
Giess 12363 (PRE); Waterberg, Farm Omega GR978, (–BB), 07-05-1967, W. Giess 10142 (PRE); Waterberg, Farm
Ruimte GR968, (–BC), 08-05-1967, W. Giess 10149 (PRE). 2018 (Gunib): Hereroland, Otjituuo Reserve 235, 6 km
of Ovitjete Fountain, (–AB), D. Edwards 4405 (PRE). 2019 (Eiseb): locality unknown, (–BC), B.A. Curtis 1043
(PRE). 2020 (Kaukauveld): 7 miles from Gam on way to Windhoek, (–BB), 30-08-1955, R. Story 5330 (PRE); 10
miles N of Eiseb Omuramba in direction of Kanovlei, (–DB), 12-04-1967, W. Giess 9790 (PRE). 2119 (Epukiro):
Hereroland, Epukiro, (–CA), 04-1970, J. MacKenzie 62 (PRE). 2219 (SAndfontein): Omaheke, Farm Kom Nader
(Kroonster 448), (–BA), 13-02-2000, C. Silver SIL28 (PRE).
BOTSWANA.—1725 (Livingstone): Chobe, Serondela, (–CC), 08-1952, O.B. Miller B/1341 (PRE). 1821 (Andara):
Ngamiland, Shakawe Village, (–BD), 18-11-1993, P.A. Smith 5686 (PRE). 1823 (Siambisso): Nxauna Pan, (–AA),
31-12-1972, P.A. Smith 314 (PRE, SRGH). 1824 (Kachikau): just within N boundary of Chobe Game Reserve, near
Goha Hills, (–AC), 16-07-1967, C. Cresswell 34 (PRE); Zwezwe Flats, (–BC), 02-1938, O.B. Miller B/178 (PRE).
1921 (Aha Hills): near the Xai-Xai – Qangwa road, (–CC), 25-04-1980, P.A. Smith 3434 (PRE, SRGH); 61 km W of
Nokaneng, (–DA), 22-03-1979, J.D. Carr 98 (PRE). 1923 (Maun): Ngamiland, Moremi Wildlife Reserve, (–AA),
07-1964, K.L. Tinley 1075 (PRE); 73 miles NE of Maun (–BB), 14-06-1930, G. van Son TVM28827 (PRE); ½ mile
from Maun, (–CD), 08-11-1972, P.A. Smith 244 (PRE, SRGH). 2022 (Lake Ngami): Mabele-a-pudi, (–CD), 19-091954, R. Story 4723 (PRE). 2121 (Ghanzi): 43 miles on road from Ghanzi to Sandfontein (–CC), 25-04-1968, M.
Mason & A. Boshoff 301 (PRE); on road from Kang to Ghanzi, (–DA), 18-03-1979, J.D. Carr 73 (PRE). 2122
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(Kobe): ± 50 miles NE of Ghanzi, (–AB), 27-07-1955, R. Story 5052 (PRE). 2221 (Okwa): 7 km SE of Okwa Valley
along Kang-Ghanzi main road, (–BD), 28-01-1979, A.R. Kreulen 538 (PRE); 15 km NW of Maneka Pan along
Kang-Ghanzi main road, (–DB), 26-01-1979, A.R. Kreulen 534 (PRE). 2321 (Lehututu): 55 km W of
Matloaphuduhudu along Ncojane-Lokalane track, (–AB), 29-12-1978, A.R. Kreulen 493 (PRE). 2525 (Mafeking): 2
km from Lobatsi on Ghanzi road, (–BA), 24-03-1976, Du Preez & Steenkamp 104 (PRE).
LIMPOPO PROVINCE.—2229 (Waterpoort): Wyllies Poort, Farm Princess Hill 704 MS, (–DD), 26-03-1982, F.
Venter 7821 (PRE). 2230 (Messina): Malonga Flats, on road between Tsipise and Mabilingwe, (–BD), 22-08-2000,
E. van Wyk avw112 (PRE); Louis Trichardt, Farm Vreemdeling, (–CC), 26-03-1994, G.L. Rossouw 248 (PRE);
Louis Trichardt, Witvlag road, (–CD), 17-09-1934, I.B. Pole-Evans 3702 (PRE); Venda, Mufulwi Village, (–DA),
09-10-1989, H.F. Glen 1827 (PRE); Venda, Ha-Makuya, Makuya Park, (–DB), 14-03-1991, J.C. van Daalen 504b
(PRE); between Toyandou and Thembe, ± 2 km on turnoff to Thembe where tarred road to Hamakuya stops, (–DC),
02-04-1997, M.H. Steyn 16 (PRE). 2231 (Pafuri): Kruger National Park, 500 m from radio mass at end of 598, (–
AC), 18-06-1993, C.B.S. van der Merwe 58 (PRE): junction of Limpopo and Pafuri Rivers, (–AD), 05-1938, H.
Bower 9148 (PRE); Kruger National Park, Punda Maria, (–CA), 13-08-1953, H.P. van der Schijff 3153 (PRE);
Kruger National Park, Wambia, (–CB), 15-05-1971, G.K. Theron 2604 (PRE); Ngwendu Waterhole, (–CC), 28-051954, H.P. van der Schijff 3822 (PRE); Kruger National Park, Shingomeni area, (–CD), 27-05-1954, H.P. van der
Schijff 3816 (PRE). 2330 (Tzaneen): Klein Australia Forest Station, (–AA), 28-01-1946, J. Gerstner 5887 (PRE);
near Mookeisi, Tzaneen Forest District, (–AD), 25-10-1953, B. Walsh 10842 (PRE); Letaba, Duiwelskloof,
Westfalia Estate, (–CA), 21-03-1961, J.C. Scheepers 1133 (PRE); Hans Merensky Nature Reserve, (–DA), 04-031972, I. von Teichman 233 (PRE).
MPUMALANGA.—2530 (Lydenburg): Schoemanskloof, (–AD), 06-1932, J.C. Smuts 56 (PRE); Sudwala’s Kraal,
at caves, (–BD), 06-03-1972, J.P. Nel 180 (PRE). 2430 (Pilgrim’s Rest): Ga-Mabins-Simoari, (–BC), 27-10-1981, F.
Venter 7265 (PRE). 2431 (Acornhoek): 5 miles from Newington to Bushbuckridge, (–CD), 19-01-1972, E.
Buitendag 911 (PRE).
22b. subsp. ondongense (Engl. & Diels) Okafor in Boletim da Sociedade Broteriana, Sér. 2,41: 147 (1967);
Exell: 120 (1978); J.D.Carr: 50 (1988); M.Coates Palgrave: 799 (2002); Curtis & Mannheimer: 474 (2005). C.
ondongense Engl. & Diels: 56 (1899). Type: Namibia, 'Amboland zwischen Ondonga und Unkussyama', July 1897,
Rautanen 234 (HBG, holo.; BM, fragment, K e!, WU e!, Z e!, iso.). Figure 18.
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C. schinzii Engl. ex Engl. & Diels: 54 (1899). Type: Namibia, Onkumbi, Sep. 1885, Schinz 1037 (B, holo.†;
Z e!, iso.).
Distribution
Botswana, Namibia, Zimbabwe.
NAMIBIA.—1714 (Ruacana Falls): Ruacana, flats S to SW of the airport, (–AD), 10-07-1976, Leistner, Oliver,
Steenkamp & Vorster 39 (PRE); Mahenene Research Station, (–BD), 07-12-1998, H. Kolberg & S. Loots HK965
(PRE). 1715 (Ondangua): 5 miles E of Oshikango near Ondipa Mission Station, (–BD), 14-02-1959, B. de Winter &
W. Giess 7000 (PRE). 1817 (Tsintsabis): ± 40 miles SE of Ondangua on sand road to Namutoni, near Omuramba,
Ovambo River, (–DB), 13-02-1959, B. de Winter & W. Giess 6954 (PRE). 2017 (Waterberg): Waterberg Plateau (–
AC), 12-1935, J. Boss TVM34971 (PRE). 2018 (Gunib): Otjozondjupa, (–BC), 09-05-2001, B.A. Curtis 966 (PRE).
BOTSWANA.—1923 (Maun): Marula Railway Station, (–CB), 28-05-1930, Milne-Redhead 405 (PRE). 2127
(Francistown): Francistown to Bosoti, (–AB), 17-04-1931, I.B. Pole-Evans 3236 (PRE). 2221 (Okwa): just N of
Butsivango River on road from Kang to Ghanzi, (–BB), 17-03-1979, J.D. Carr 72 (PRE).
22c. subsp. suluense (Engl. & Diels) Okafor in Boletim da Sociedade Broteriana, Sér. 2,41: 143 (1967);
Wickens: 28 (1973); Exell: 120 (1978); Vollesen: 53 (1980); J.D.Carr: 51 (1988); McCleland: 458 (2002); M.Coates
Palgrave: 799 (2002); Curtis & Mannheimer: 474 (2005). Type: Swaziland, hill slopes, Horo Mine, Dec. 1890-1894,
Galpin 1264 (Z e!, holo.; BOL, K e!, NH, PRE!, SAM e!, iso.). Figure 8.
C. suluense Engl. & Diels: 54 (1899); Dümmer: 183 (1913); Burtt Davy: 248 (1926); O.B.Mill.: 43 (1948).
C. junodii Dümmer: 183 (1913); Bews: 147 (1921). Type: South Africa, Limpopo Province, hills,
Shilouvane, Junod 613 (K e!, holo.; PRE!, Z e!, iso.).
C. griseiflorum S.Moore: 227 (1921); Burtt Davy: 246 (1926); O.B.Mill.: 43 (1948). Type: South Africa,
Mpumalanga, Nelspruit, Breyer s.n. sub Rogers 24018 (BM e!, holo.).
C. angustilanceolatum Engl.: 702 (1921). Type: Mozambique, Lower Umswirizwi River, Swynnerton 45
(B, holo.†; BM e!, lecto., designated here; K e!, isolecto.).
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C. makindense Gilg ex Engl.: 703 (1921). Type: Kenya, Machakos Dist., Kibwezi, Makinde Steppe,
Scheffler 210 (B, holo.†; K e!, lecto., designated here; BM, E e!, HBG e!, P e!, PRE!, WAG e!, Z e!, isolecto.).
C. millerianum Burtt Davy: 279 (1921). Type: Swaziland, Buckham’s to Forbes’ Coal Mine, June 1911,
Burtt Davy 10681 (BOL, holo.; K e!, iso.).
Note: The holotype of C. angustilanceolatum was destroyed and from the two extant isotypes in BM and K, the first
mentioned specimen is chosen as lectotype, because it is the better one of the two.
The holotypes, Scheffler 210, of C. makindense was destroyed and the Kew specimen is chosen as lectotype
which is verified by Wickens (1968).
Distribution
Angola, Kenya, Malawi, Mozambique, ?Namibia, South Africa (Limpopo Province, Mpumalanga), Swaziland,
Tanzania, Zambia, Zimbabwe.
NAMIBIA.—1715 (Ondangua): Oshikango, (–BD), 06/07-1948, E.M. Loeb 144 (PRE). 1714 (Ruacana Falls): 6 km
from Ruacana on road to Ruacana Falls, (–AC), 03-1975, J. Vahrmeijer & P. du Preez 2626 (PRE); mountains S of
Ruacana, (–AD), 15-06-1963, W. Giess & H. Leippert 7004 (PRE).
LIMPOPO PROVINCE.—2230 (Messina): Venda, Tshipise, along road at Klein Tshipise, (–BC), 01-10-1979, E.
Netshiungani 996 (PRE); Venda, ± 5 km NE from Madimbo, (–BD), 06-10-1985, J.J. Wentzel 14 (PRE); Venda,
Sibasa Dist., Tate Vondo Forest Reserve, (–CD), 15-09-1977, G. Hemm 97a (PRE); Venda, at T-junction from
Tshamavhudzi, (–DA), 04-11-1979, A.E. van Wyk 3069 (PRE); Venda, Thohoyandou, ± 20 km past Thohoyandou
on road from Louis Trichardt to Punda Maria, (–DC), 17-03-1997, H. Joffe 1079 (PRE). 2231 (Pafuri): Kruger
National Park, Punda Maria, (–CA), 13-06-1973, J.N. Pienaar 49 (PRE). 2329 (Pietersburg): 68 km on road to
Duiwelskloof from Pietersburg, (–DB), 07-04-1997, M.H. Steyn 18 (PRE). 2330 (Tzaneen): Zoutpansberg Dist.,
Elim, (–AA), 06-19430, A.A. Obermeyer 542 (PRE); Gazankulu, Giyani Dist., Giyani, (–BC), 24-04-1980, C.
Liengme 431 (PRE); 13.6 km from Soekmekaar on road to Duiwelskloof, (–CA), 12-03-1972, B.J. Coetzee 1342
(PRE); Modjadjies, (–CB), 23-11-1967, D.J.B. Killick 3842 (PRE); Hans Merensky Nature Reserve, (–DA), 18-091969, L.G. Oates 33 (PRE). 2430 (Pilgrim’s Rest): Lekgalameetse Nature Reserve, E border of Schelem, (–AB), 1102-1986, M. Stalmans 1046 (PRE); Hoedspruit Dist., Tamboti Botanical Trails, Farm Chester 235 KT, (–BD), 01-
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02-1996, M. Jordaan 3068 (PRE). 2431 (Acornhoek): Timbavati Private Game Reserve, Farm Albatross, (–AD), 1103-1970, R.N. Porter 330 (PRE); ± 5 km N of Klaserie on road to Mica, (–CA), 10-10-2000, J.J. Meyer BP00354
(PRE); Timbavati Private Game Reserve, Farm Springvalley, (–CB), R.N. Porter 342 (PRE).
MPUMALANGA.—2430 (Pilgrim’s Rest): Sabie, hills near MacMac Falls, (–DD), 06-07-1956, A.O.D. Mogg
37096 (PRE). 2431 (Acornhoek): Lothian Forest Reserve, Graskop Conservancy, (–CC), 07-1935, Forester Joubert
8721 (PRE). 2530 (Lydenburg): Nelspruit Dist., Lowveld Botanic Garden, (–BD), 22-09-1971, E. Buitendag 862
(PRE). 2531 (Komatipoort): 23 miles from Hector’s Spruit, towards Hora, (–BC), 08-01-1929, J. Hutchinson 2522
(PRE); 23 km from Nelspruit towards Malelane, (–CA), E. Buitendag 948 (PRE).
SWAZILAND.—2531 (Komatipoort): Piggs Peak Dist., Horo, (–CD), 07-09-1956, R.H. Compton 26036 (PRE);
Swaziland Irrigation Scheme, (–DC), 03-1973, D.N.H. Horler 209 (PRE). 2631 (Mbabane): Mbabane, Forbes Reef,
Komati River bridge on the Oshoek-Piggs Peak road, (–AA), 18-04-1992, F. Brusse 6330 (PRE); Hhohho Dist., N
banks of Komati River, E of Mhlatane River, (–AB), 05-03-1993, G. Germishuizen 6107 (PRE); Mpala Ranch, on
Mliba/Tshaneni road, (–BA), 16-04-1977, J. Culverwell 787 (PRE); Mpisi, (–BC), 10-09-1965, R.H. Compton 32363
(PRE); Stegi Dist., Namahasha Road, (–BD), 04-05-1959, R.H. Compton 28852 (PRE); Mankaiana Dist., Ntondozi,
(–CA), 26-10-1961, M. Karsten s.n. (PRE); 10 miles ESE of Manzini on Sipofaneni road, (–DA), 08-04-1977, J.
Culverwell 709 (PRE).
22d. Combretum collinum Fresen. subsp. taborense (Engl.) Okafor in Boletim da Sociedade Broteriana,
sér. 2, 41: 144 (1967); Exell: 182 (1970); Wickens: 26 (1973); Exell: 120 (1978); Vollesen: 53 (1980); J.D.Carr: 51
(1988); McCleland: 460 (2002); M.Coates Palgrave: 800 (2002). Type: Tanzania, Tabora, Stuhlmann 506 (B,
holo.†). Figure 18.
C. taborense Engl.: 290 (1895). C. mechowianum O.Hoffm. subsp. taborense (Engl.) Duvign.: 80 (1956).
C. goetzenianum Diels: 500 (1907). Type: Tanzania, Dondoland, between Kilwa and Likemba, Busse 570
(B, holo.†; EA, lecto., designated here; BM e!, fragment, isolecto.).
C. psammophilum Diels: 502 (1907). Type: Tanzania, Lindi, Ruaha, Busse 1122 (B, holo.†; EA e!, lecto.,
designated here; BM, isolecto.).
C. burttii Exell: 169 (1939). Type: Zambia, 25 miles from Kassama on road to Issaka, near Malole Mission,
Burtt 5951 (BM e!, holo.; BR e!, EA e!, K, iso.).
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Note: Diels (1907) described two species, C. goetzenianum and C. psammophilum, based on Busse’s specimens he
collected in Tanzania. Both species proved to be C. collinum subsp. taborense. The original material of both names
were destroyed and the isotypes in East African Hebarium (EA) in Kenya are chosen here as lectotypes. The material
in BM are merely fragments.
Distribution
DRC, Malawi, Mozambique, South Africa (Limpopo Province, Mpumalanga), Tanzania, Zambia, Zimbabwe.
LIMPOPO PROVINCE.—2231 (Pafuri): N of Pafuri gate of Kruger National Park, 8 km before hoof and mouth
control gate from Pafuri gate, (–AC), 02-04-1997, M.H. Steyn 11 (PRE).
MPUMALANGA.—2431 (Acornhoek): Kruger National Park, 31 km from Skukuza on tarred road to Pretoriuskop,
(–AB), 08-06-1987, B.S. Steel 463 (PRE); Kruger National Park, Pumbe Sandveld, (–BB), 15-12-1960, Brynard &
Adendorff 4504 (PRE); Lothian Forest Reserve, (–CC), 05-1943, B. Joubert PRF9513 (PRE); 16 miles from
Newington towards Hazyview (–DA), 19-06-1971, J.P. Nel 119 (PRE). 2530 (Lydenburg): Schoemanskloof near
Schagen, (–BD), 28-03-1937, A.A. Obermeyer TVM36098 (PRE); Ngodwana (–DA), 11-05-1986, F. von
Breitenbach 19831 (PRE). 2531 (Komatipoort): Mawewe, (–DC), 07-06-2000, E. van Wyk evw0095 (PRE).
VIII. Combretum section Breviramea Engl. & Diels
Combretum hereroense Schinz belongs to this section. It has leaves mostly with only 3 or 4(5) pairs of principal
lateral veins. The scales are very densely packed, contiguous, sometimes hidden by the dense indumentum of
combretaceous hairs on the leaves below. Contiguous scales also occur in C. imberbe and this species is closer
related to C. hereroense than to other members in section Hypocrateropsis where Exell (1978) places it. C.
hereroense is an extremely variable species in leaf shape and indumentum and sometimes in size of fruit. The
indumentum varies from densely tomentose to nearly glabrous. Wickens (1971a) subdivided C. hereroense into three
subspecies and subsp. hereroense into two varieties on behalf their hairiness. Only the typical subspecies occur in
our area. We do not recognize these varieties.
Combretum hereroense, C. imberbe and C. elaeagnoides are clearly related according to the molecular
analysis by Maurin et al. (2010), although currently placed in three different sections. They are charaterised by 4-
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Annexes
merous flowers, in dense often subcapitate axillary spikes, a glabrous disc and lepidote fruit. Leaves in all these
species are densely lepidote with scales contiguous or overlapping, silver or golden or rusty brown; cells divided by
numerous radial and tangential walls. All three species are deciduous trees, although C. elaeagnoides has a tendency
to scramble. Young stems of C. imberbe have short, opposite, spine-tipped lateral shoots.
23. Combretum hereroense Schinz in Verhandelungen des Botanischen Vereins der Prov. Brandenburg
30: 245 (1888); Engl. & Diels: 63 (1899); Dümmer: 201 (1913); Exell & Roessler: 8 (1966); Exell: 8 (1968); Exell
& J.G.Garcia: 56 (1970); Wickens: 411 (1971a); Wickens: 40 (1973); Exell: 138 (1978); Vollesen: 53 (1980);
J.D.Carr: 77 (1988); Pooley: 356 (1993); Vollesen: 118 (1995); A.E.van Wyk & P.van Wyk: 332 (1997);
McCleland: 462 (2002); M.Coates Palgrave: 803 (2002); Curtis & Mannheimer: 478 (2005). Type: Namibia,
Otjovazandu, Schinz 431 (Z e!, holo.; B, iso.†). Figure 19.
C. eilkeranum Schinz: 246 (1888); Engl. & Diels: 61 (1899); O.B.Mill.: 42 (1948). Type: Namibia, Kunene,
Schinz 420 (Z e!, holo.).
C. transvaalense Schinz: 202 (1894); Dümmer: 201 (1913); Burtt Davy: 246 (1926); O.B.Mill.: 43 (1948).
Type: South Africa, Limpopo Province, Makapansberge, Rehmann 5470 (Z e!, holo.).
C. sambesiacum Engl. & Diels: 63 (1899). Type: Mozambique, Boroma, Menyharth 892b (Z e!, holo.; K,
fragment, e!, WU, fragment, e!, iso.).
C. hereroense Schinz subsp. hereroense var. villosissimum Engl. & Diels: 63 (1899); Dümmer: 201 (1913);
Wickens: 41 (1973). C. villosissimum (Engl. & Diels) Engl.: 705 (1921). C. transvaalense Schinz var. villosissimum
(Engl. & Diels) Burtt Davy: 246 (1926). Type: South Africa, Limpopo Province, Makapansberge, Streydpoort,
Rehmann 5471 (Z e!, holo.).
C. porphyrolepis Engl. & Diels: 63 (1899), nom. illegit.
C. rautanenii Engl. & Diels: 64 (1899); O.B.Mill.: 43 (1948). Type: Namibia, Katumare, Rautanen 199 (Z
e!, lecto., designated here).
C. rhodesicum Baker f.: 435 (1899); Eyles: 428 (1916); O.B.Mill.: 43 (1948). Type: Zimbabwe, Bulawayo,
Rand 582 (BM, syn.) and Rand 583 (BM, syn.).
C. transvaalense Schinz var. bolusii Dümmer: 201 (1913). Type: South Africa, Mpumalanga, ‘Juxta ripas
flum. Kaup prope Barberton’, Bolus 7763 (K e!, holo.).
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Note: Engler & Diels (1899) mentioned Rautanen 199 and three specimens of Fleck in their protologue of C.
rautanenii. None of the Fleck specimens are available on the Zürich Herbarium website, only Rautanen 199, after
which the species was named.
Distribution
Angola, Botswana, Kenya, Malawi, Mozambique, Namibia, South Africa (Gauteng, KwaZulu-Natal, Limpopo
Province, Mpumalanga, North-West), Swaziland, Tanzania, Uganda, Zambia, Zimbabwe.
IX. Combretum section Campestria Engl. & Diels (=sect. Elaeagnoidea Engl. & Diels)
Exell (1978) placed C. elaeagnoides Klotzch in section Elaeagnoidea Engl. & Diels, but Stace (1981) sunk it under
sect. Campestria, stating that there are four species in Africa belonging to this section. Of these C. elaeagnoides is
the only species belonging to this section south of the Zambezi River where it is restricted to the Flora Zambesiaca
region (including the Caprivi Strip in Namibia). It has a peculiar type of scale and the leaves, flowers and fruit are
densely silvery-lepidote. The flowers are 4-merous, arranged in dense, often subcapitate axillary spikes; the disc is
without a free margin. C. elaeagnoides growing in the Zambezi valley often forming dense thickets and is known in
Zimbabwe as jesse-bush.
24. Combretum elaeagnoides Klotzsch in Peters, Natürwissenschaftliche Reise nach Mossambique,
Botanik 1: 73 (1861); Engl.: 290 (1895); O.B.Mill.: 42 (1948); Exell: 7 (1968); Exell: 140 (1978); J.D.Carr: 63
(1988); A.E.van Wyk & P.van Wyk: 330 (1997); M.Coates Palgrave: 801 (2002); Curtis & Mannheimer: 491
(2005). Type: Mozambique, Sambesi Jitsch, Tete, Peters s.n. (B, holo.†; BM, K, fragment, e!, iso.). Figure 20.
C. prunifolium Engl. & Diels: 28 (1899), pro parte. Type: Mozambique, Boroma, Menyharth 893 (Z e!,
holo.; WU e!, iso.).
C. stevensonii Exell: 171 (1939); O.B.Mill.: 44 (1948). Type: Zambia, Mazabuka, Oct. 1929, Stevenson 99
(BM e!, holo.; FHO, iso.).
Note: The type of C. prunifolium Engl. & Diels, Menyhardt 893 (Z), consists of three specimens, the two upper ones
being C. elaeagnoides and the lower one C. hereroense (Exell 1978).
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Distribution
Botswana, Mozambique, Namibia, Zambia Zimbabwe.
NAMIBIA.—1723 (Singalamwe): Caprivi Strip, 49 miles W of Katima Mulilo, (–DB), 17-02-1969, B. de Winter
9220 (PRE); Western Caprivi Strip, Kwando Flood Plain, (–DC), 12-05-1966, K.L. Tinley 1425 (PRE). 1724
(Katima Mulilo): Katima Mulilo, (–AD), 04-04-1975, H.J. Steyl 60 (PRE); Caprivi Strip, Ngoma area, (–DC), 1902-1969, B. de Winter 9247 (PRE).
BOTSWANA.—1725 (Livingstone): Serondela, Chobe Game Reserve, (–CC), 11-1951, O.B. Miller B/1200 (PRE);
10 miles NW of Dodo Bross roads on Kazungula road, (–CD), 20-03-1966, A.D. McKay 1978 (PRE, SRGH). 1824
(Kachikau): Goha Hill, (–AC), 19-05-1977, P.A. Smith 2063 (PRE, SRGH); 8 miles N of Kachikau, (–BA), 09-071937, J. Erens 365 (PRE); Tsotsoroga Pan, (–CD), 17-06/07-1930, G. van Son TVM28828 (PRE).
X. Combretum section Plumbea O.Maurin, M. Jordaan & A.E.van Wyk, sect. nov.
sectioni Hypocrateropsidi valde affinis sed habitu arboris unicaulis discretae, juventute ramis decussatis, ramulis
brevibus lateralibus apice spinescente; foliis perdense lepidotis, squamis plerumque contiguis vel superpositis,
magnis 120--300µm diametro, cellulis permultis parvis, solum costa nervisque primariis lateralibus conspicuis,
margine disci dense tomentoso, stylo cum squamis stipitatis, cotyledonibus infra planum humi orientibus, differt.
Type species: Combretum imberbe Wawra.
This section is named Plumbea, derived from the Latin word plumbum which mean lead, referring to the heartwood
of C. imberbe which is extremely hard, heavy and durable; hence the common name leadwood.
Exell (1978) placed C. imberbe Wawra in section Hypocrateropsis but separate it from all the other species
in this section by its very densely lepidote leaves with scales mostly contiguous. It has rather large scales, 120–300
µm in diam, rougly circular, cells very numerous and small, divided by radial and tangential walls. A molecular
phylogenetic study (Maurin et al. 2010) shows that C. imberbe is more closely related to C. elaeagnoides and C.
hereroense than to the other members of sect. Hypocrateropsis and is treated here in a section of its own. In young
growth the branches are decussate and short lateral shoots end in a spinescent tip. The fruit is very small, less than 18
mm long and densely covered with silvery scales.
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25. Combretum imberbe Wawra in Sitzungsberichte der Mathem.-Natürw. Classe der Kaiserlichen
Akademie der Wissenschaften in Wien 38: 556 (1860); Engl. & Diels: 14 (1899); O.B.Mill.: 43 (1948); Exell &
Roessler: 9 (1966); Exell: 7 (1968); Exell & J.G.Garcia: 52 (1970); Wickens: 18 (1973); Exell: 109 (1978);
Vollesen: 53 (1980); J.D.Carr: 81 (1988); Pooley: 358 (1993); A.E.van Wyk & P.van Wyk: 332 (1997); McCleland:
462 (2002); M.Coates Palgrave: 803 (2002); Curtis & Mannheimer: 480 (2005). Type: Angola, Benguela, Wawra
247 (W e!, holo.; BM e!, iso.). Figure 21.
Argyrodendron petersii Klotzsch: 101 (1861). Combretum petersii (Klotzsch) Engl.: 290 (1895). C.
imberbe Wawra var. petersii (Klotzsch) Engl. & Diels: 14 (1899); Engl. & Gilg: 314 (1903); Diels: 491 (1907).
Type: Mozambique, Sena, Peters s.n. (B, holo.†;). Mozambique, Zambezia entre Mocuba e Mugeba, a 36 km de
Mocuba (Marata), Barbosa & de Carvalho 2667 [WAG e!, neo., designated by Jongkind (1993)].
C. truncatum Welw. ex M.A.Lawson: 427 (1871); Dümmer: 231 (1913); O.B.Mill.: 44 (1948). C. imberbe
Wawra var. truncatum (Welw. ex M.A.Lawson) Burtt Davy: 246 (1926). Type: Angola, Benguela, Catumbela,
Welwitsch 4372 [LISU e!, lecto., designated by Exell & Garcia (1970); BM e!, K e!, isolecto.].
C. primigerum Marloth ex Engl.: 49 (1888); Engl. & Diels: 14 (1899); O.B.Mill.: 43 (1948). Namibia,
Hereroland, Usakos, Omumborombonga, Marloth 1264 (B, holo.†; GRA e!, K e!, M e!, PRE!, W e!, iso.).
Distribution
Angola, Botswana, Malawi, Mozambique, Namibia, South Africa (Gauteng, KwaZulu-Natal, Limpopo Province,
Mpumalanga, North-West), Swaziland, Tanzania, Zambia, Zimbabwe.
COMBRETUM subgenus CACOUCIA
Combretum subgen. Cacoucia (Aubl.) Exell & Stace (Exell & Stace 1966, Wickens 1973)
Cacousia Aubl.: 450, t. 179 (1775).
Four sections are recognised.
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Key to the sections of subgen. Cacoucia
1a Scrambling shrubs or woody climbers, with persistent petiole bases developing into curved spines; leaf lamina
densely covered with translucent gland dots; flowers orange to scarlet-red or white tinged pink; petals minutely hairy
or pilose; fruit hairy or glabrous, with wings or wingless
Sect. X Poivrea
1b Scrambling shrubs, erect shrubs, climbers or suffrutices, without persistent petiole bases developing into curved
spines; leaf lamina without gland dots; petals glabrous or velvety; flowers red, grey-green or white; fruit sparsely
hairy to velvety, always with wings:
2a Climbers, shrubs or suffrutices; flowers red; petals glabrous; fruit sparsely hairy on body only; Botswana,
northern provinces of South Africa, Swaziland and KwaZulu-Natal
Sect. XI. Conniventia
2b Scrambling shrubs; flowers not red; fruit with velvety covering all over; endemic to Kaokoveld (Namibia and
Angola):
3a Leaves opposite or in whorls of three, not longitudinally folded; flowers grey-green with a pinkish or reddish
tinge
Sect. X1I Megalantherum
3b Leaves opposite, longitudinally folded; flowers white with crimson to reddish brown stamens Sect. XIII
Oxystachya
X. Combretum section Poivrea (Comm. ex DC.) G.Don (1832); Wickens: 57 (1973); Exell: 154 (1978)
Combretum mossambicensis and C. bracteosum belong to this section. They are characterised by the lack of
epidermal scales and the presence of gland-tipped hairs on the midrib and lateral veins, hairy pockets in the axils of
veins below and translucent gland dots in the leaf lamina. Species in this section have relatively large and showy
flowers, usually 5-merous and up to 10 mm long with protruding stamens. The fruit are usually 5-winged or 5angled. C. mossambicensis has white or pinkish flowers and is one of the few species of Combretum in southern
Africa with hairy fruit. The only other species of Combretum with pubescent or woolly fruit in our region belong to
other sections, namely C. albopunctatum, C. collinum subsp. suluense, C. hereroense, C. moggii, C. oxystachyum
and C. wattii. C. bracteosum and C. mossambicense have petioles which persist as a recurved woody spine or hook.
Similar recurved hooks are found in Quisqualis parviflora Gerrard ex Sond. C. bracteosum is a free-standing, muchbranched, many-stemmed shrub, but may climb on other vegetation. It has scarlet or red flowers, but differs from all
other southern African species of Combretum in having wingless fruit.
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26. Combretum bracteosum (Hochst.) Brandis in Engl. & Prantl, Die Natürlichen Pflanzenfamilien 3,7:
125 (1893); Engl. & Diels: 95 (1899); Dümmer: 68 (1913); Bews: 146 (1921); J.D.Carr: 37 (1988); Hennessy: t.
2028 (1991b); Pooley: 354 (1993); M.Coates Palgrave: 796 (2002). Type: South Africa, KwaZulu-Natal, ‘in sylvis
prope fl. Umlaas’, Krauss 350 [B, holo.†; BM (BM000902273) e!, lecto., designated here; G e!, MO, fragment, e!,
S, fragment, e!, W, fragment, e!, isolecto.]. Figure 22.
Poivrea bracteosa Hochst.: 424 (1844); Sond.: 512 (1862); Sim: 223 (1907).
Codonocroton triphyllum E.Mey.: 149 (1843), nom. nud. Type: South Africa, Eastern Cape, between
Omtata [Umtata] and Omsamvubo [Umzimvubu] Rivers, Drège s.n. (S e!, holo.).
Note: Krauss 350 in the British Museum (BM), type of Combretum bracteosum is a decent flowering specimen
chosen here as the lectotype; the isotypes in the other herbaria are merely fragments.
The name Codonocroton triphyllum does not seem to be validly published and only appeared in Meyer’s,
Zwei Pflanzengeographische Documente von J.F. Drège (1843), collected by Drège in the Eastern Cape, a year
before Hochstetter pulished the name Poivrea bracteasa, based on a specimen from KwaZulu-Natal. The Drège
specimen at Sweden Herbarium has a handwritten label and was mounted on the same sheet as S08-899, the type of
Poivrea bracteosa, the name under which it is filed.
Distribution
South Africa (Eastern Cape, KwaZulu-Natal).
KWAZULU-NATAL.—2831 (Nkandla): Mtunzini, (–DD), 02-10-1975, V. Steenis 24011 (PRE). 2832 (Mtubatuba):
Richard Bay Dist., Enseleni Nature Reserve, (–CA), 03-10-1970, H.J.T. Venter 6032 (PRE). 2930
(Pietermaritzburg): Reunion Rocks, (–DD), 02-02-1966, R.G. Strey 6422 (PRE). 2931 (Stanger): Umhlanga River, (–
CA), 12-05-1974, C.J. Ward 8614 (PRE); Durban, Umgeni Lagoon, (–CC), 18-01-1967, R.G. Strey 7320 (PRE).
3030 (Port Shepstone): Port Shepstone Dist., Umsimkulu River bank, (–AC), 10-09-1966, R.G. Strey 6850 (PRE);
Isipingo Beach, (–BB), 02-10-1948, C.J. Ward 526 (PRE); Scottburgh, (–BD), 27-09-1959, A.A. Mauve 1055 (PRE);
Port Shepstone Dist., Shelly Beach, (–CD), 07-1935, C. Letty 212 (PRE).
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Annexes
EASTERN CAPE.—3128 (Umtata): Mqanduli Dist., Umtata River Mouth, (–DD), C.E. Moss PRE32234 (PRE).
3129 (Port St Johns): Ntsubane, (–BC), 24-10-1957, A.S. van Rensburg PRF11303 (PRE); Umgazi River Mouth, (–
CB), 01-10-1973, J.N. Pienaar 139 (PRE); Umngazana area (Xamara Flats), (–CB), 01-09-1974, C.J. Ward 8727
(PRE); Coffee Bay, (–CC), 20-02-1966, M.J. Wells 3515 (PRE); Hluleka Forest, (–CD), 09-1923, O.B. Miller
PRF5377 (PRE); Port St Johns, 13 miles W of Port St Johns, (–DA), 17-10-1953, G.C. Theron 1569 (PRE); Intafufu
River, (–DD), 11-10-1968, A.P. Mills 397 (PRE). 3327 (Peddie): East London Dist., Buffalo River, (–BB), 12-051962, Bokelmann s.n. (PRE).
27. Combretum mossambicense (Klotzsch) Engl., Die Pflanzenwelt Ost-Afrikas und der Nachbargebiete
C: 292 (1895); Engl. & Diels: 98 (1899); O.B.Mill.: 43 (1948); Stace: 14 (1961); Exell & Roessler: 9 (1966); Exell:
6 (1968); Exell: 219 (1970); Exell & J.G.Garcia: 78 (1970); Wickens: 63 (1973); Exell: 156 (1978); A.E.van Wyk &
P.van Wyk: 334 (1997); M.Coates Palgrave: 807 (2002); Curtis & Mannheimer: 482 (2005). Type: Mozambique,
Manica e Sofala, Sena, Peters s.n. (B, holo.†; BM e!, K, fragments, e!, iso.). Figure 22.
Poivrea mossambicensis Klotzsch: 78, t. 13 (1861).
C. ukambense Engl.: 291 (1895). Type: Kenya, Kitui in Ukamba, Hildebrandt 2779 (B, holo.†; K e!, lecto.,
designated here; M e!, P e!, W e!, isolecto.).
C. trichopetalum Engl.: 292 (1895); Engl. & Diels: 97, t. 28, fig. C (1899). Tanzania, Mwanza Dist.,
Makolo, Stuhlmann 722 & Bukumbi, Stuhlmann 822 & without locality, Fischer 250 (all syn. at B†).
C. guangense Engl. & Diels: 98 (1899). Type: Angola, Cuanza Norte, Golungo Alto, Welwitsch 4282 [BM
e!, lecto., designated by Exell & Garcia (1970); COI, G e!, K e!, LISU e!, P e!, isolecto.].
C. cataractarum Diels: 508 (1907); N.E.Br.: 111 (1909); Burtt Davy: 248 (1926); Eyles: 427 (1916);
O.B.Mill.: 42 (1948). Type: Zimbabwe, Victoria Falls, Oct. 1904, Allen s.n. (B, syn.†) and Ufer, country unknown,
Sept. 1905, Engler 2925 (B, syn.†).
C. phillipsii Dümmer: 116 (1913). Type: South Africa, Mpumalanga, Komatipoort, Kirk 57 (K e!, holo.).
C. detinens Dinter: 170 (1919). Type: Namibia, between Franzfontein and Outjo, Dinter 2645 (SAM e!,
iso.).
Note: The holotype of C. ukambense was destroyed and of the three extant isotypes, the one in Kew has the best
preserved flowering material and is therefore chosen as the lectotype.
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Distribution
Botswana, DRC, Kenya, Malawi, Mozambique, Namibia, South Africa (Limpopo Province, Mpumalanga),
Tanzania, Uganda, Zambia, Zimbabwe.
NAMIBIA.—1713 (Swartbooisdrif): 25 km N Etengua, Kaokoveld, (–AC), 10-09-1968, W. Giess 10504 (PRE); 1.5
km NW from Quelle Ombazu in Kaokoveld, (–DC), 09-09-1968, W. Giess 10500 (PRE). 1724 (Katima Mulilo):
Katima Mulilo, just outside Nature Conservation’s Camp (–AD), 01-03-1982, M. Müller 1833 (PRE). 1813
(Ohopoho): 58 km along road D3704 from junction at Opuwo - Kaoko Otavi road, (–BD), 13-06-2001, H.H.
Kolberg, S. Loots & R. Moses HK1166 (PRE). 1820 (Tarikora): 15 miles W of Nyangana on road to Runtu, (–BB),
11-02-1956, B. de Winter & W. Marais 4593 (PRE). 1821(Andara): Caprivi Strip, Buffalo, along road verge, (–BB),
24-05-1999, E. Klaassen & S. Austaller EK169 (PRE). 1915 (Okaukuejo): Etosha National Park, E of Ombika, (–
BD), 05-03-1976, W. Giess & B. Loutit 14111 (PRE). 1916 (Gobaub): Etosha Pans, Halali Rest Camp, (–BA), W.
Giess 15463 (PRE).
BOTSWANA.—1725 (Livingstone): Serondela, Chobe River, (–CC), 09-1944, O.B. Miller B/334 (PRE);
Kazungula, Thorn Forest, (–CD), O.B. Miller B/43 (PRE). 1821 (Andara): Tsodilo Hills, (–DB), 13-07-1963, C.H.
Banks 25 (PRE). 1823 (Siambisso): Savuti Channel, near drift above Gubatsa Hills, (–DA), 23-10-1972, H. Biegel,
G. Pope & B. Gibbs Russell 4043 (PRE, SRGH). 1923 (Maun): Mukoba Kraal, (–AC), 10-06-1972, K. Babich 9
(PRE); Matlapaneng Drift, Tamlakane River, 8 miles NE of Maun, (–CD), 11-09-1954, R. Story 4651 (PRE). 2022
(Lake Ngami): Ngwanalekau Hills area, (–DD), 19-09-1969, A.D. Burger 1260 (PRE). 2227 (Palapye): Central Dist.,
Selebi-Phikwe, (–BB), 30-09-1978, O.J. Hansen 3473 (PRE). 2228 (Maasstroom): Tuli Block, Farm Nitoni, (–BB),
15-09-1993, K.C. Baytopp 275 (PRE); Tuli Block, 20 km NE of Sherwood, (–CC), 31-10-1994, D.T. Cole 978
(PRE).
LIMPOPO PROVINCE.—2228 (Maasstroom): SE of Zanzibar, Koperfontein Farm 161MR, (–DA), 24-10-1996,
G.J. du Toit 5133 (PRE). 2229 (Waterpoort): Messina, 56 miles NW of Farm Greefswald, (–AB), 08-01-1974, J.N.
Pienaar 435 (PRE); Pont Drift, Breslau 2MS, (–AC), 06-10-1996, C.C. Straub 633 (PRE); Dongola Rest Camp, (–
BC), 12-10-1948, L.E. Codd 4448 (PRE); Blouberg Nature Reserve, Farm Auf der Haard 445 MS, (–CC), 04-121990, R.H. Archer 494 (PRE); Great Salt Pan, (–CD), 15-09-1960, Hardy & Wells 376 (PRE); Njlele River, (–DD),
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Annexes
Van Graan & Hardy 543 (PRE). 2230 (Messina): near Msekwa Poort, 4 miles from Poort on rioad to Messina, (–
CC), 15-10-1956, A.D.J. Meeuse 9701 (PRE); Georgenholz, Makonde, (–DC), 10-1930, J. Westphal 16 (PRE). 2231
(Pafuri): Kruger National Park, Punda Maria, (–CA), 16-10-1952, H.P. van der Schijff 1010 (PRE); Kruger National
Park, Pafuri, 600 m W of Wambiya Pan, (–CB), 21-06-1985, Botha & Cilliers 3678 (PRE). 2328 (Baltimore):
Potgietersrust, Glen Alpine Dam, (–BA), 22-02-1964, J.E. Repton 6415 (PRE). 2431 (Acornhoek): Klaserie Private
Nature Reserve, (–CA), 10-10-1973, N. Zambatis 323 (PRE).
MPUMALANGA.—2431 (Acornhoek): Kruger National Park, between Olifants Camp and Nwanedsi, (–BB), 2611-1981, A.E. van Wyk 5188a (PRE); Kruger National Park, near Tshokwana, (–DD), L.E. Codd 5726 (PRE). 2531
(Komatipoort): Barberton Dist., Lower Sabie, (–BB), H. Lang TVM30169 (PRE); Komatipoort, (–BD), 30-09-1906,
F.A. Rogers 2608 (PRE).
XII. Combretum section Conniventia Engl. & Diels (1899)
This section falls under subgen. Cacoucia because scales are absent but the leaves have stalked glandular hairs.
Flowers are red, 4-merous and the petals are glabrous. Ventenat (1808) described C. paniculatum from a plant
collected in Senegal, West Africa and C. microphyllum is described by Klotzsch (1861) from a plant collected in
Mozambique. Wickens (1971c, 1973) reduced C. microphyllum to a subspecies of C. paniculatum. Exell (1968,
1978) raised C. microphyllum to species level. Coates Palgrave (1977) placed C. microphyllum under C.
paniculatum and therefore considers this as one aggregate species occurring in most parts of tropical and subtropical
Africa. Exell (1978) and Carr (1988) consider C. paniculatum and C. microphyllum as two distinct species and there
seems to be enough molecular evidence (Maurin et al. 2010) to maintain these two species. Chemotaxonomical
studies conducted by Carr & Rogers (1987) however found identical extracts for these two species suggesting that
they are closely related, but they unfortunately have not included C. platypetalum Welw. ex M.A.Lawson in their
studies, a species from the Flora Zambesiaca region and further north which form part of this complex (see below).
C. paniculatum flowers usually in autumn (March–May) and the leaves remains on the plant when in flower. The
leaves and flowers are larger than in C. microphyllum, a deciduous species that flowers usually in spring (September
and October) when no leaves are visible on the plants. Exell (1978) pointed out that although difficult to separate C.
microphyllum and C. paniculatum in the herbarium, the two species are different in the field and they are also
ecologically distinct. C. paniculatum occurs in forest and forest edges in the Soutpansberg region of South Africa. C.
microphyllum grows on river banks of, for example, the Limpopo, Letaba, Olifants, Crocodile, Sabi, Komati,
348
Annexes
Ngwavuma, Pongola and Mkuze Rivers in South Africa in open lowveld savanna in full sun. It has become a popular
garden plant in subtropical gardens. Flowers in both species are rich in nectar and are eagerly visited by
nectarfeeding sunbirds and passerine birds. The flowers are also visited by honeybees.
Combretum platypetalum is a multi-stemmed, sparsely branched to virgate dwarf shrub (geoxylic suffrutex)
up to 1.5 m high (subsp. oatesii does not exceed 500 mm) with a thick woody rhizome, occurring in the Flora
Zambesiaca region as well as Namibia, Botswana, DRC, Angola and Tanzania. The differences between subsp.
platypetalum and subsp. baumii (Engl. & Gilg) Exell is not clear because both have leaves and flowers that are hairy
and we accept the view of Exell (1978) and Carr (1988) that only the typical subspecies occurs in northeastern
Namibia crossing the border into Botswana. Subsp. oatesii (Rolfe) Exell differs from the other two subspecies by its
glabrous leaves. Exell (1978) cites one specimen from Botswana, Rogers 6109 (SRGH) collected at Lobatsi, under
C. platypetalum subsp. oatesii (Rolfe) Exell. No specimens of this taxon have been located in the National
Herbarium, Pretoria (PRE) and it is doubtful whether subsp. oatesii actually occurs in southeastern Botswana.
Further investigation is needed to confirm its presence in southern Africa.
28. Combretum microphyllum Klotzsch in Peters, Natürwissenschaftliche Reise nach Mossambique,
Botanik 1: 74 (1861); Dümmer: 183 (1913); Burtt Davy: 246 (1926); I.Verd.: t. 978 (1945); O.B.Mill.: 43 (1948);
Exell: 6 (1968); Exell: 150 (1978); Vollesen: 53 (1980); Pooley: 360 (1993); McClelan: 464 (2002); M.Coates
Palgrave: 804 (2002). Type: Mozambique, rios de Sena and Tete, Peters s.n. [B, holo.†; BM, fragment, e!, iso.).
Figure 23.
C. paniculatum Vent. subsp. microphyllum (Klotzsch) Wickens: 66 (1971c); Wickens: 53 (1973).
C. lomuense Sim: 62, t. 61/B (1909). Type: Mozambique, without precis locality, Sim 6393 (not traced).
Distribution
Botswana, Malawi, Mozambique, South Africa (KwaZulu-Natal, Limpopo Province, Mpumalanga), Swaziland,
Tanzania, Zambia, Zimbabwe.
BOTSWANA.—2229 (Waterpoort): Tuli Block, Nitani Game Reserve, (–AA), Baytopp 156 (UNIN) (fide Miller
1948, Setshogo & Venter 2003).
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Annexes
LIMPOPO PROVINCE.—2229 (Waterpoort): Pont Drift, Breslau 2 MS, at camp on Limpopo River banks, (–AC),
30-08-1996, C.C. Straub 438 (PRE); Dongola, Weipe 617 Farm, (–BA), 18-8-1948, Codd 4334 (PRE); near the
main drift of the Limpopo River, N of Messina, (–BB), 18-12-1928, J.B. Gillett 3034 (PRE). 2230 (Messina):
Messina, junction of Limpopo & Sand Rivers, (–AC), 26-11-1919, J. Foye 14 (PRE); Northern Soutpansberg,
Njelele River, (–AD), 07-1916, H.G. Breijer TRV 16043 (PRE); Palmaryville PO, 4 miles SW of Palmaryville, (–
CD), 5-9-1947, L.E. Codd 3025 (PRE); Thengwe area, on road to Masisi, (–DA), 14-11-2002, E. van Wyk, L.A.
Nkuna & M.D. Dlamini 557 (PRE), Venda, Vuvha, (–DA), 07-10-1981, A.E. van Wyk & G.K. Theron 4913 (PRE);
Venda, Lwamondo Location, along road to Punda Milia, (–DC), 10-09-1977, C.A. Liengme 199 (PRE). 2231
(Pafuri): Waller's Camp, Mutale (Mavhulani) River, near Pafuri, (–AC), 10-09-1997, E.P. Nienaber EN 223 (PRE);
Kruger National Park, Punda Maria, (–CA), 28-3-1971, J.J.F. Stephen 335 (PRE). 2327 (Ellisras): Ellisras, Tamboti
River, Huwi Private Native Reserve, (–DB), 11-8-1975, P.C.V. du Toit 875 (PRE). 2330 (Tzaneen): Spelonken (–
CA), 09-1910, T.J. Jenkins TRV 8145 (PRE); Hans Merensky Nature Reserve, Letaba River, (–DA), 15-10-1981, N.
Zambatis 1225 (PRE). 2331 (Phalaborwa): Pietersburg Dist., 50 miles N of Gravelotte station, on Letaba Ranch, (–
CA), 2-8-1934, E.E. Galpin 13853 (PRE); Kruger National Park, Letaba Rest Camp, (–DC), 24-9-1932, H. Lang
TRV 30935 (PRE); Pietersburg East Dist., Great Letaba, (–DD), 0-10-1931, H. Lang TRV 30579 (PRE). 2431
(Acornhoek): Phalaborwa Dist., Sheila 10 KU, 14 km S of Phalaborwa, near water course, (–AA), 03-10-1984, I.M.
Retief 205 (PRE).
MPUMALANGA.—2431 (Acornhoek): Kruger National Park, Olifants River, 1 mile E of Olifants River Rest Camp,
(–BA), 30-01-1950, R. Story 3962 (PRE); Kruger National Park, Olifants River, Seekoeigat, (–CD), 26-9-1952, H.P.
van der Schijff 819 (PRE); Kruger National Park, Sabie River, between Skukuza and Tshokwane, (–DC), 09-091982, J.J.H. Onderstall 777 (PRE); Kruger National Park, Mnondozispruit, 5 miles E of dam, (–DD), 5-9-1951, H.P.
van der Schijff 61 (PRE). 2531 (Komatipoort): Kruger National Park, 4 miles W of Malelane camp, on N bank of
Crocodile River, (–AD), 6-9-1948, L.E.W. Codd 4364 (PRE); Marloth Park, ± 10 km NE of Hectorspruit, (–BD), 2709-2002, J.J. Meyer 4158 (PRE); Kaapmuiden, 4.3 km towards Malelane, (–CB), 21-09-1975, E.J. van Jaarsveld
735 (PRE).
SWAZILAND.—2531 (Komatipoort): Tshaneni, (–DD), 17-07-1969, S.C.H. Barrett 12 (PRE). 2632 (Bela Vista):
Stegi Dist., Mbuluzi Poort, (–AA), 27-9-1960, R.H. Compton 30145 (PRE), Mlawula Nature Reserve, along road
down Mbuluzi Gorge, (–AA), 16-08-1986, K.P. Braun 153 (PRE).
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KWAZULU-NATAL.—2632 (Bela Vista): Ndumo, S of Ndumo, (–CC), 05-10-1984, D.J. Botha 3522 (PRE);
Ndumu Game Reserve, edge of Nyameti Pan, (–CD), 21-11-1967, R.G. Strey & E.J. Moll 3750 (PRE). 2731
(Louwsburg): Lebombo Flats, S bank of Pongola River, (–BD), 08-09-1932, E.E. Galpin 13697 (PRE); Kwa
Mugaisa, Mkuze River, (–CB), 18-10-1971, C.J. Ward 7276 (PRE). 2732 (Ubombo): Makane's Drift, S of drift, (–
AB), 05-09-1985, M.C. Ward 1027 (PRE); Ingwavuma Dist., Otobotini, (–AC), 12-05-1965, J. Vahrmeijer & H.R.
Tolken 970 (PRE); Ubombo Dist., Mkuze Game Reserve, (–CA), 18-09-1962, R.D. Gush 24 (PRE).
29. Combretum paniculatum Vent., Choix de Plantes, sub. T. 58 (1808); G.Don: 424 (1827);
M.A.Lawson: 425 (1871); Exell: 171 (1928); Exell: 175 (1944); F.W.Andrews: 203 (1950); F.White: 283 (1962);
Exell: 212 (1970); Exell & J.G.Garcia: 69 (1970); Wickens: 52 (1973); Exell: 149 (1978); Vollesen: 53 (1980);
Liben: 37 (1983); D.J.Carr: 120 (1988); Vollesen: 120 (1995); A.E.van Wyk & P.van Wyk: 336 (1997); Jongkind:
70 (1999); M.Coates Palgrave: 809 (2002). Type: Senegal, Roussillon 60 in Herb. Jussieu 13632 (P-JU, holo.).
Figure 24.
C. ramosissimum Engl. & Diels: 72 (1899). Type: Sierra Leone, Afzelius s.n. (B, syn.†); Bioko, Mann 203
(B, syn.†; K, P, isosyn.); Gabon, Soyaux 86 (B, syn.†; K, iso.); Cameroun, Zenker 210 (B, syn.†); Cameroun, Zenker
& Staudt 177 (B, syn.†; K, lecto., designated by Jongkind (1999), BM, isolecto.].
Distribution
Angola, Benin, Bioko, Burkina Faso, Cameroon, Cote d'Ivoire, DRC, Ethiopia, Gambia, Guinea, Guinea-Bissau,
Kenya, Liberia, Malawi, Mali, Mozambique, Nigeria, São Tomé, Senegal, Sierra Leone, South Africa (Limpopo
Province), Sudan, Tanzania, Uganda, Zimbabwe.
LIMPOPO PROVINCE.—2230 (Messina): Rambuda Location, (–CD), 19-12-1951, N.J. van Warmelo 51z19/27
(PRE); Thohoyandou Dist., along road between Sibasa and Thengwe, (–DC), 05-08-1993, P. van Wyk BSA940
(PRE, PRU). 2329 (Pietersburg): Louis Trichardt, (–BB), 21-09-1932, E.C.S. Koker 17 (PRE). 2330 (Tzaneen):
Sibasa Dist., Tshakhuma, (–AB), 11-1931, A.A. Obermeijer 978 (PRE).
351
Annexes
30. Combretum platypetalum Welw. ex M.A.Lawson subsp. platypetalum in Flora of tropical Africa 2:
433 (1871); Engl. & Diels: 68 (1899); Exell: 7 (1968); Exell: 214 (1970); Exell & J.G.Garcia: 71 (1970); Wickens:
54 (1973); Exell: 151 (1978); Curtis & Mannheimer: 493 (2005). Type: Angola, Huila, Mumpula-Humpata,
Welwitsch 4356 (LISU, holo.; BM e!, COI, K e!, P e!, iso.). Figure 23.
C. zastrowii Dinter: 174 (1919); O.B.Mill.: 44 (1948). Type: Namibia, Grootfontein to Okavango, Zastrow
in Herb. Dinter 3135a (SAM e!, iso.).
Distribution
Angola, Botswana, DRC, Namibia, Zambia.
NAMIBIA.—1718 (Kuring-Kuru): Okavango, Omuramba Mpungu on Tsinsabis- Kuring-Kuru road, (–CA), 13-121955, B. de Winter 3923 (PRE); Grootfontein North, Okavango, at Muparara, 69 miles S of Runtu in Omuramba
Osatako, (–CD), 02-05-1967, W. Giess 10114 (PRE). 1719 (Runtu): Zanza, SE of Runtu, (–CC), 16-07-1952, B.
Maguire 1628 (PRE). 1721 (Mbambi): Western Caprivi Strip, near Okavango Flood Plain, (–CC), 06-1966, K.L.
Tinley 1501 (PRE). 1819 (Karakuwisa): just E of Karakuwise, (–DC), 18-12-1952, B. Maguire 2064 (PRE), 3 miles
N of 7 miles dune, Okavango, (–DC), 09-1957, P.J. le Roux 166 (PRE). 1820 (Tarikora): Okavango River, S of
Omataka mouth, (–AB), 06-1948, J.D. Keet 1657 (PRE); 5 km NE of Kandtara School, on way to Rundu-Andara
main road, (–BB), 22-04-1977, M. Müller & W. Giess 502 (PRE); Kavango Area 1, Kaudom Game Reserve, (–BC),
03-10-1988, C.J. Ward & C.J. Hines 10334 (PRE). 1821 (Andara): Andara Mission Station, (–AB), 16-01-1956, B.
de Winter & H.J. Wiss 4286 (PRE). 1920 (Tsumkwe): Grootfontein Dist., ± 30 miles N of Gautscha Pan, (–BC), 1102-1958, R. Story 6465 (PRE).
BOTSWANA.—1821 (Andara): Mohembo, (–BD), 06-1946, O.B. Miller B/424 (PRE).
XII. Combretum section Megalantherum Exell (1968)
Only one very distinct species, Combretum wattii Exell endemic to the Kaokoveld Centre of endemism in
northwestern Namibia and southwestern Angola (Van Wyk & Smith 2001), belongs to this section. It has leaves in
pairs or in whorls of three and the foliage is confined mainly to short lateral shoots emerging from older wood. A
single flower terminates the lateral shoots, accompanied by further individual flowers in one or two sets of distal
352
Annexes
axils, up to five flowers per lateral shoot. The colour of the flowers is also unusual in being grey-green with a
pinkish or reddish tinge. They have a nectariferous disc and are densely pubescent with dark brown stalked glands.
The stamens and style are exserted beyond the petals, green at first, becoming reddish. The fruits are 5-winged.
31. Combretum wattii Exell in Mitteilungen der Botanischen Staatssammlung München 4: 5 (1961); Exell
& Roessler: 11 (1966); Exell & J.G.Garcia: 79 (1970); A.E.van Wyk & P.van Wyk: 336 (1997); M.Coates Palgrave:
812 (2002); Curtis & Mannheimer: 486 (2005). Type: Namibia, Kaoko-Otavi, 1939, Watt 1766 (M e!, holo.). Figure
24.
Distribution
Angola, Namibia.
NAMIBIA.—1712 (Posto Velho): 5 miles S of Kunene at Otjinungua on road to Orupembe, (–AD), 08-05-1957, B.
de Winter 5760 (PRE); 9.5 km N of Okombambi and W of Otjimbobombonga in the Baynesberg Mountains, (–BB),
11-09-1968, W. Giess 10505 (PRE). 1812 (Sanitatas): 16 miles E of Sanitatas, (–BA), 18-08-1956, R. Story 5870
(PRE). 1813 (Ohopoho): Kaokoveld, Kaoko Otavi, Wasserstelle, (–BC), 27-01-1958, H. Merxmüller & W. Giess
1392 (M, PRE). 1913 (Sesfontein): Khorixas Dist., Khowarib Schlucht, (–CD), 31-07-1996, H. Kolberg & T.
Tholkes HK768 (PRE). 1914 (Kamanjab): Kaokoveld, at the Quelle Kowares, (–AB), 02-02-1958, H. Merxmüller &
W. Giess 1555 (M, PRE). 2013 (Unjab Mouth): Torra Bay, 73 miles from Farm Wereldsend 715 OUT, (–AC), 0104-1963, Ihlenfeldt, De Winter & Hardy 3215 (PRE).
XIII. Combretum section Oxystachya Exell (1968)
Only one species from the FSA region, C. oxystachyum Welw. ex M.A.Lawson from Kaokoveld in Namibia, belongs
to this section. It is a scrambling shrub or climber and the leaves are longitudinally folded, with dense white hairs
and stalked glands. The flowers are white with crimson to reddish brown stamens. The fruit is 5-winged.
32. Combretum oxystachyum Welw. ex M.A.Lawson in Flora of tropical Africa 2: 422 (1871); Hiern: 341
(1898); Exell & Roessler: 10 (1966); Exell: 26 (1968); Exell & J.G.Garcia: 77 (1970); Curtis & Mannheimer: 492
(2005). Type: Angola, Bumbo, Quitibe de Cima, 1860, Welwitsch 4309 (LISU, holo.; BM e!, iso.). Figure 25.
353
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Distribution
Angola, Namibia.
NAMIBIA.—1712 (Posto Velho): Otjipemba, (–BB), 21-01-1968, B.J. Grobbelaar 66a (PRE); Otjitanda, (–DB),
10-07-1969, P.G. Meyer 1287 (PRE). 1713 (Swartbooisdrif): 39 km from Okanguati on road to Epupa Falls, (–AC),
09-06-2001, H.H. Kolberg, S. Loots & R. Moses HK1125 (PRE); Ehomba Mountains, on road to Swartbooisderift to
Ohopoho, (–BD), 20-02-1959, B. de Winter & W. Giess 7106 (PRE); Otjiwero, (–CD), 05-04-1957, B. de Winter &
O. Leistner 5392 (PRE); Ovikange, 21 miles NW of Ombazu, (–DA), 29-05-1957, B. de Winter & O. Leistner 5906
(PRE); 1714 (Ruacana Falls): Ruacana, edge of plateau, E of the falls, (–AC), 09-07-1976, Leistner et al. 7 (PRE);
Northern Border, Ruacana, (–AD), 18-03-1998, M.H. Steyn 23 (PRE); 35 km E of Ohopoho, (–CC), 07-04-1973, W.
Giess & J. van der Walt 12635 (PRE); Omusati, (–DC), 01-04-1999, C.A. Mannheimer & B.A. Curtis CM726 (PRE).
1715 (Ondangua): Ovamboland, in field next to Oshikuku - Okalanga road, ± 30 km from Oshikuku, (–AB), 29-031999, C.A. Mannheimer & B.A. Curtis CM709 (PRE). 1813 (Ohopoho): 15 miles E Ohopoho, (–BB), 31-01-1958, H.
Merxmüller & W. Giess 1512 (M, PRE).
ACKNOWLEDGEMENTS
We would like to thank Hester Steyn for the distribution maps, Hugh Glen for the Latin diagnoses, Daleen Roodt for
the line drawings and Meg Coates Palgrave for checking certain specimens in the Harare Herbarium (SRGH).
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INDEX
Argyrodendron petersii Klotzsch
Codonocroton triphyllum E.Mey., nom. nud.
Combretum Loefl.
adenogonium Steud. ex A.Rich.
albopunctatum Suess.
angustilanceolatum Engl.
antunesii Engl. & Diels
apetalum Wall. ex Kurz
apiculatum Sond. subsp. apiculatum
subsp. leutweinii (Schinz) Exell
apiculatum Sond. var. parvifolium Baker f.
arengense Sim
bajonense Sim
bracteosum (Hochst.) Brandis
burttii Exell
caffrum (Eckl. & Zeyh.) Kuntze
calocarpum Gilg ex Dinter
cataractarum Diels
celastroides Welw. ex M.A.Lawson
celastroides Welw. ex M.A.Lawson subsp. orientale Exell
chlorocarpum Exell
collinum Fresen. subsp. gazense (Swynn. & Baker f.) Okafor
subsp. ondongense (Engl. & Diels) Okafor
subsp. suluense (Engl. & Diels) Okafor
subsp. taborense (Engl.) Okafor
coriaceum Schinz
dekindtianum Engl.
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detinens Dinter
dinteri Schinz
dregeanum C.Presl
edwardsii Exell
eilkeranum Schinz
elaeagnoides Klotzsch
ellipticum Sim
engleri Schinz
erythrophyllum (Burch.) Sond.
erythrophyllum (Burch.) Sond. var. obscurum Van Heurck & Müll.Arg.
eylesii Exell
fragrans F.Hoffm.
galpinii Engl. & Diels
gazense Swynn. & Baker f.
ghasalense Engl. & Diels
gillettianum Liben
glomeruliflorum Sond.
glomeruliflorum Sond. var. obscurum (Van Heurck & Müll.Arg.) Burtt Davy
glutinosum sensu Wood
goetzenianum Diels
grandifolium F.Hoffnm.
griseiflorum S.Moore
guangense Engl. & Diels
gueinzii Sond.
guenzii Sond. var. holosericeum (Sond.) Exell ex Rendle
hereroense Schinz
hereroense Schinz subsp. hereroense var. villosissimum Engl. & Diels
holosericeum Sond.
homblei De Wild.
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imberbe Wawra
imberbe Wawra var. petersii (Klotzsch) Engl. & Diels
imberbe Wawra var. truncatum (Welw. ex M.A.Lawson) Burtt Davy
junodii Dümmer
kirkii M.A.Lawson
kraussii Hochst.
kwebense N.E.Br.
leutweinii Schinz
lomuense Sim
lucidum E.Mey. ex Drège
lydenburgianum Engl. & Diels
makindense Gilg ex Engl.
mechowianum O.Hoffm. subsp. gazense (Swynn. & Baker f.) Duvign.
mechowianum O.Hoffm. subsp. taborense (Engl.) Duvign.
microphyllum Klotzsch
millerianum Burtt Davy
minutiflorum Exell
mkuzense J.D.Carr & Retief
moggii Exell
molle R.Br. ex G.Don
mossambicense (Klotzsch) Engl.
multispicatum Engl. & Diels
myrtillifolium Engl.
nelsonii Dümmer
obtusatum Engl. & Diels
odontopetalum Engl. & Diels
omahekae Gilg & Dinter ex Engl.
ondongense Engl. & Diels
orientale (Exell) Jordaan & O.Maurin
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oxystachyum Welw. ex M.A.Lawson
padoides Engl. & Diels
paniculatum Vent.
paniculatum Vent. subsp. microphyllum (Klotzsch) Wickens
parvifolium Dinter
patelliforme Engl. & Diels, p. p.
patelliforme Engl. & Diels, p. p.
petersii (Klotzsch) Engl.
petrophilum Retief
phillipsii Dümmer
platypetalum Welw. ex M.A.Lawson subsp. baumii (Engl. & Gilg) Exell
subsp. oatesii (Rolfe) Exell
subsp. platypetalum
porphyrolepis Engl. & Diels, nom. illegit.
primigerum Marloth ex Engl.
prunifolium Engl. & Diels
psammophilum Diels
psidioides Welw. subsp. dinteri (Schinz) Exell
subsp. grandifolium (F.Hoffnm.) Jordaan
subsp. psidioides
subsp. psilophyllum Wickens
quirirense Engl. & Gilg
ramosissimum Engl. & Diels
rautanenii Engl. & Diels
rhodesicum Baker f.
riparium Sond.
salicifolium E.Mey. ex Hook.
sambesiacum Engl. & Diels
schinzii Engl. ex Engl. & Diels
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schumannii Engl.
sonderi Gerrard ex Sond.
stevensonii Exell
suluense Engl. & Diels
taborense Engl.
tenuipes Engl. & Diels
ternifolium Engl. & Diels
tinctorum Welw. ex M.A.Lawson
transvaalense Schinz
transvaalense Schinz var. bolusii Dümmer
var. villosissimum (Engl. & Diels) Burtt Davy
trichopetalum Engl.
truncatum Welw. ex M.A.Lawson
ukambense Engl.
undulatum Engl. & Diels
vendae A.E.van Wyk
villosissimum (Engl. & Diels) Engl.
wattii Exell
woodii Dümmer
zastrowii Dinter
zeyheri Sond.
Dodonaea caffra Eckl. & Zeyh.
conglomerata Eckl. & Zeyh.
Poivrea bracteosa Hochst.
mossambicensis Klotzsch
?Terminalia erythrophylla Burch.
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(*) National Herbarium, South African National Biodiversity Institute, Private Bag X101, Pretoria, 0001 South
Africa. † Student affiliation: Department of Plant Science, University of Pretoria, 0002 Pretoria.
(***) H. G. W. J. Schweickerdt Herbarium, Department of Plant Science, University of Pretoria, 0002 Pretoria.
(***) Molecular Systematics Laboratory, Department of Botany and Plant Biotechnology, APK Campus, University
of Johannesburg, PO Box 524, 2006 Auckland Park, Johannesburg.
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CAPTIONS
FIGURE 1.—Scales of Combretum subgen. Combretum. GROUP 1. Sections I–V, showing the smaller size, ±
circular in outline and divided by few radial and tangential walls and sometimes the tangential walls are absent as in
sect. Angustimarginata, sect. Glabripetala and sometimes in sect. Ciliatipetala. A, C. erythrophyllum (sect.
Angustimarginata); B, C. kraussii (sect. Angustimarginata); C, C. zeyheri (sect. Spathulipetala); D, C. engleri (sect.
Macrostigmatea); E, C. adenogonium (sect. Glabripetala); F, C. apiculatum subsp. apiculatum (sect. Ciliatipetala);
G, C. albopunctatum (sect. Ciliatipetala); H, C. molle (sect. Ciliatipetala). Taken from Stace (1969) and Exell
(1978). Scale bar: 80µm. Artist: Daleen Roodt.
FIGURE 2.—Scales of Combretum subgen. Combretum. GROUP 2. Sections VI–X, showing the larger size, ±
scalloped in outline and divided by many radial and tangential walls. A, C. celastroides (sect. Hypocrateropsis); B,
C. platelliforme (sect. Hypocrateropsis); C, C. collinum (sect. Metallicum); D, C. hereroense (sect. Breviramea); E,
C. elaeagnoides (sect. Campestria); F, C. imberbe (sect. Plumbea). Scale bar: 80µm. Artist: Daleen Roodt.
FIGURE 3.—Seedling morphology of Combretum zeyheri (A) and C. mkuzense (B). Solid transverse lines depict
ground level. In C. zeyheri the cotyledons are fused to form a sub-circular peltate structure which terminates the
primary stem. Growth in length is resumed by a lateral bud from a point below the fused cotyledons (sympodial
growth). In C. mkuzense growth in length of the stem commences from what seems be the primary growing tip
located between the two opposite cotyledons (monopodial growth). Artist: Daleen Roodt.
FIGURE 4.—Known distribution of Combretum vendae () and Combretum woodii () and Combretum caffrum
().
FIGURE 5.—Known distribution of Combretum erythrophyllum () and C. engleri ().
FIGURE 6.—Known distribution of Combretum kraussii () and C. nelsonii ().
FIGURE 7.—Known distribution of Combretum zeyheri () and C. mkuzense ().
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Annexes
FIGURE 8.—Known distribution of Combretum adenogonium () and C. collinum subsp. suluense ().
FIGURE 9.—Known distribution of Combretum albopunctatum () and C. edwardsii ().
FIGURE 10.—Known distribution of Combretum apiculatum subsp. apiculatum.
FIGURE 11.—Known distribution of Combretum apiculatum subsp. leutweinii () and C. molle ().
FIGURE 12.—Known distribution of Combretum moggii.
FIGURE 13.—Known distribution of Combretum petrophilum.
FIGURE 14.—Known distribution of Combretum psidioides subsp. psidioides () and C. psidioides subsp. dinteri
().
FIGURE 15.—Known distribution of Combretum celastroides subsp. celastroides () and C. platelliforme ().
FIGURE 16.—Known distribution of Combretum padoides () and C. tenuipes ().
FIGURE 17.—Known distribution of Combretum collinum subsp. gazense.
FIGURE 18.—Known distribution of Combretum collinum subsp. ondongense () and C. collinum subsp. taborense
().
FIGURE 19.—Known distribution of Combretum hereroense.
FIGURE 20.—Known distribution of Combretum elaeagnoides.
370
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FIGURE 21.—Known distribution of Combretum imberbe.
Figure 1
371
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Figure 2
372
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Figure 3
373
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Figure 4
Figure 5
374
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Figure 6
Figure 7
375
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Figure 8
Figure 9
376
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Figure 10
Figure 11
377
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Figure 12
Figure 13
378
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Figure 14
Figure 15
379
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Figure 16
Figure 17
380
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Figure 18
Figure 19
381
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Figure 20
Figure 21
382
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Figure 22
Figure 23
383
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Figure 24
Figure 25
384

Olivier Maurin Philosophiae Doctor Botany Faculty of

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