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PHYLOGENETIC ANALYSIS OF PLANT COMMUNITY ASSEMBLAGES IN
THE KRUGER NATIONAL PARK, SOUTH AFRICA
By
KOWIYOU YESSOUFOU
Thesis submitted in fulfilment of the requirements for the degree
PHILOSOPHIAE DOCTOR
In
BOTANY
In the
Faculty of Sciences
At the
University of Johannesburg
Supervisor: Prof. Michelle van der Bank
Co-supervisor: Prof. Vincent Savolainen
January 2012
Declaration
Declaration
I declare that this thesis has been composed by me and the work contained
within, unless otherwise stated, is my own
-------------------------------------------
K. Yessoufou (January 2012)
Table of contents
Table of contents……………………………………………………………………i
Abstract…………….………………………………………………………………..v
Acknowledgements..…………………………………………………….............vii
List of tables………………………………………………………………………..ix
List of figures……………………………………………………………………….x
Dedication…………………………………………………………………………xiii
List of abbreviations……………………………………………………………..xiv
Table of contents
Table of content
Chapter 1- General introduction…………………………………………………..1
1. Savanna ecology…………………………………………………………………1
1.1. Features of tropical savanna………………………………………………….1
1.2. Role of fire in savanna ecology……………………………………………….3
1.3. Importance of herbivory in savanna ecology………………………………..3
2. Community ecology in a savanna context……………………………………..4
2.1. Theories of tree-grass coexistence…………………………………………..4
2.2. Tree-tree coexistence………………………………………………………….5
3. Phylogenetic investigation of community assembly…………………………..6
3.1. The use of DNA barcoding techniques to reconstruct phylogenetic
tree…………………………………………………………………………………….6
3.2. Rationale of phylogenetic approach in ecology……………………………..7
3.3. Framework in community phylogenetics…………………………………….8
3.4. Emerging patterns in community phylogenetics…………………………..10
4. Study site and objectives of the study………………………………………...12
4.1. Study site………………………………………………………………………12
4.2. Objectives……………………………………………………………………...18
4.3. Outline of the thesis…………………………………………………………..19
Chapter 2- The phylogeny of trees and shrubs in the Kruger National Park
using DNA barcodes…………………….………………………………………...23
1. Introduction……………………………………………………………………..23
2. Materials and methods………………………………………………………..25
i
Table of contents
2.1. Sample collection…………………………………………………………….25
2.2. DNA extraction, PCR and sequencing……………………………………..25
2.3. Sequence alignment………………………………………………………….27
2.4. Tree reconstruction…………………………………………………………...28
3. Results…………………………………………………………………………..29
3.1. Tree statistics……………………………………………………………….29
3.2. Phylogeny of trees and shrubs of the KNP……………………………...30
4. Discussion………………………………………………………………………45
4.1. Clade 1: Fabidae…………………………………………………………...48
4.2. Clade 2: Malvidae………………………………………………………….50
4.3. Clade 3: Vitales…………………………………………………………….52
4.4. Clade 4: Santalales………………………………………………………..52
4.5. Clade 5: Lamiidae………………………………………………………….53
4.6. Clade 6: Campanulidae……………………………………………………55
4.7. Clade 7: Ericales…………………………………………………………...55
4.8. Clade 8: Caryophyllales…………………………………………………...56
4.9. Clade 9: Basal Eudicots…………………………………………………..56
4.10. Clade 10: Magnoliidae…………………………………………………….57
4.11. Clade 11: Monocotyledoneae…………………………………………….57
5. Conclusion………………………………………………………………………58
Chapter 3- Testing suitability of evolutionary models using traits of woody
plants in the KNP…………………………………………………………………..59
1. Introduction..……………………………………………………………………59
2. Materials and methods….…………………………………………………….61
ii
Table of contents
2.1. Plant ecological traits………………………………………………………61
2.2. Data collection and measurements………………………………………63
2.3. Data analysis……………………………………………………………….64
3. Results………………………………………………………………….............65
4. Discussion………………………………………………………………………71
5. Conclusion………………………………………………………………………74
Chapter 4- Characterising diversity and phylogenetic structure of woody plant
communities in the Kruger National Park, South Africa………………………..75
1. Introduction……………………………………………………………………..75
2. Materials and methods………………………………………………………...77
2.1. Dataset………………………………………………………………………77
2.2. Data analysis……………………………………………………………….78
3. Results…………………………………………………………………………..82
3.1. Overall diversity and community structure in the KNP.………………..82
3.2. Community phylogenetic structure within and among sites…………...84
3.3. Community trait-based structure within and among sites……………..86
4. Discussion………………………………………………………………………86
5. Conclusion………………………………………………………………………89
Chapter 5- The role of megaherbivores in shaping the structure of subtropical
plant communities...………………………………………………………………..90
1. Introduction……………………………………………………………………..90
2. Materials and methods………………………………………………………..94
2.1. Study site: exclosures……………………………………………………..94
iii
Table of contents
2.2. Traits of anti-herbivores defences………………………………………..96
2.3. Community sampling in the exclosures………………………………….96
2.4. Statistical analyses………………………………………………………...97
3. Results…………………………………………………………………………..98
4. Discussion……………………………………………………………………..103
4.1. Exclusion of megaherbivores and plant diversity………………………..104
4.2. Exclusion of megaherbivores and phylogenetic diversity………………105
5. Conclusion…………………………………………………………………….106
Chapter 6- General conclusion…..…………………………………………….108
1. Major findings, discussion and contribution to literature..………………..108
1.1. Phylogenetic information database for the KNP………………………108
1.2. Ornstein-Uhlenbeck is more suitable for phylogenetic comparative
analysis of plant traits in the KNP………………………………………109
1.3. Plant community assemblages in the KNP are not neutral………….109
1.4. Megaherbivores leave distinct signature on plant community
structure…………………………………………………………………...109
2. Future challenges…………………………………………………………….111
Chapter 7- References…………………………………………………………..114
Supplementary Information…………………………………………………...139
Appendix- Submitted paper…………………………………………………….176
iv
Abstract
Abstract
What underlies species distribution and species coexistence has long been of key
interest in community ecology. Several methods and theories have been used to
address this question. However, it still remains a controversial debate. The recent
development of plant DNA barcodes with possibility of merging phylogeny with
ecology brings high expectation in uncovering the processes underlying community
assemblages. Previous studies that used molecular approaches in community
ecology focused mainly on rainforests. Using a phylogenetic approach, the current
study contribute to a novel understanding about savanna ecology, especially
regarding how megaherbivores impact plant community composition.
The Kruger National Park (KNP) is one of the world’s largest reserves, but less
studied from a phylogenetic perspective. A DNA database of 445 DNA sequences
(plant DNA barcodes, rbcLa + matK) was generated for the woody plants of the KNP.
This database proves reliable in reconstructing the phylogeny of Angiosperms of the
park. Based on this phylogeny, the present study characterised plant community
composition, and investigated how megaherbivores influence this composition.
Results indicate that plant communities in the KNP are not neutral, i.e. they are more
clustered than expected under various null models. This suggests that ecological
forces, most likely habitat filtering may be playing a key role in dictating community
structure in the KNP. The KNP is well-known for its richness in megaherbivores. The
contribution of these animals to the current shape of plant community structures was
therefore further investigated. Where megaherbivores have been excluded, plant
diversity decreases, but shifts in plant community structure are contingent upon the
initial community composition, suggesting that herbivory might be important filter that
drives the clustering pattern observed.
v
Abstract
These results also have important implications for management of African
woodlands, particularly given the continental decline in megaherbivores. As large
herbivores are lost from these ecosystems, one can predict a subsequent reduction
in plant diversity, whilst the impact on plant community structure will depend upon
the initial composition. Critically, I also show that the loss of phylogenetic diversity (a
surrogate for functional diversity) will depend on the relative shifts in phylogenetic
community structure, information that has never been considered before in
management strategy.
Key words: Community phylogenetics, functional diversity, species coexistence,
under/overdispersion, evolutionary models, megaherbivores, conservation,
extinction, Kruger National Park, South Africa.
vi
Acknowledgements
Acknowledgements
This project was financially supported by the University of Johannesburg (UJ,
South Africa), the National Research Funds (NRF, South Africa), the
Government of Canada through Genome Canada and the Ontario Genomics
Institute (2008-OGI-ICI-03), and the Royal Society (UK). The massive
contribution of the Canadian Centre for DNA Barcoding (CCDB) through
assistance in DNA sequencing is greatly acknowledged.
I am grateful to my supervisors Prof. Michelle van der Bank (UJ, South
Africa) and Prof. Vincent Savolainen (Imperial College London, UK) for the
wonderful roles they played not only during the run of the project, but also for
their guidance that leads to the production of this dissertation. Dr T. Jonathan
Davies (McGill University, Canada), Prof. Herman van der Bank and Dr Erna
Bruwer (UJ, South Africa) also provided invaluable assistance.
The University of Johannesburg through the Department of Botany
provided excellent work and social environment and must receive here my
gratitude. I would like to thank researchers from UJ, especially Dr Cynthia
Motsi Moleboheng (former PhD student), who guided me through the different
molecular processes, and Dr Olivier Maurin for his wonderful knowledge of
the flora of the Kruger National Park, and all the current students of the
African Centre for DNA Barcoding and the Department of Botany at UJ.
I would also like to thank researchers from Imperial College London,
UK for their various helps during my multiple visits to the Ecology and
Evolution Section. I particularly thank Dr Martyn Powell, Dr Hanno Schaefer
vii
Acknowledgements
(now at Harvard University, USA), Dr Guillaume Besnard (now back to
France) and Dr Alex Papadopulos.
Special thank to the Kruger National Park in general and specifically to
the Scientific Services for allowing the project and providing field assistance.
I would also like to acknowledge the wonderful opportunities offered to
me by various Institutions from around the world who invited me to attend,
learn and share findings of this project during different workshops and
conferences. I would like to mention the University of Johannesburg (SA, for
the annual symposium), Imperial College London (UK, for the molecular and
computing statistics courses), National Institute for Mathematical and
Biological Synthesis (NIMBioS, University of Tennessee, USA, for the
workshop on high performance computing in phylogenetics), Mathematical
Biosciences Institute (MBI, Ohio State University, USA), Centre for Discrete
Mathematics and Theoretical Computer Science (DIMACS, Rutgers
University, USA), and the School of Mathematics (University of Nairobi,
Kenya, for the workshop on Conservation Biology at the Kenya Wildlife
Services Training Institute), Rhodes University (South Africa, for the 9th
conference of the Southern African Society for Systematic Biology, and the
University of Pretoria (South Africa, for the 38th conference of South African
Association of Botanists). All these conferences and workshops provided me
with useful information to understand various concepts surrounding
conservation and molecular biology.
Special and very warm thank to Mariam O. Yessoufou and Roees O.
Yessoufou, Semiyou Abdou Rafiou and his wife Souradjatou Rafiou for their
special support.
viii
List of tables
List of tables
Chapter 1
Table 1 Summary of systems included in current phylogenetic structure (as reviewed
in Vamosi et al. 2009)……………………………………………………………………...11
Table 2 Megaherbivores in the KNP, abundance and dietary behaviour…………….17
Chapter 2
Table 1 Characteristics of each partition obtained from PAUP*……………..............29
Table 2 Comparison of bootstrap values of major sub-(clades) in this study with
those of Soltis et al. (2011)………………………………………………………………..47
Chapter 3
Table 1 Tests of phylogenetic signal in the studied traits based on Pagel and
Blomberg’s statistics……………………………………………………………………….66
Table 2 Test of phylogenetic signal in the studied traits based on Abouheif’s
statistics……………………………………………………………………………………..68
Table 3 Models comparison of traits evolution of woody plants using AIC
test…………………………………………………………………………………..............70
IX
List of figures
List of figures
Chapter 1
Figure 1 Interpretation of niche theory based on habitat filtering process. This is an
illustration of Webb et al.’s framework (Webb et al. 2002)………………………..…….9
Figure 2 Frequency of different possible structures of community assemblages in
literature (Vamosi et al. 2009)…………………………………………………………….11
Figure 3 Comparison of frequency of study sites (temperate vs. tropical) of
community phylogenetics (as reviewed in Vamosi et al. 2009)……………………….12
Figure 4 Various habitats in the Kruger National Park………………………..............13
Figure 5 Major vegetation types in the Kruger National Park………………..............15
Figure 6 Giraffe during feeding activity in the KNP…………………………………….16
Figure 7 Diagram indicating the structure of the thesis………………………………..19
Chapter 2
Figure 1 Representation of steps of DNA sequencing at the Canadian Centre for
DNA Barcoding……………………………………………………………………………..27
Figure 2 The maximum likelihood phylogeny of trees and shrubs occurring in the
KNP…………………………………………………………………………………………35
Figure 3 The maximum parsimony majority rule consensus phylogeny of trees and
shrubs occurring in the KNP……………………………………………………………..44
x
List of figures
Figure 4 Summary tree of the maximum parsimony majority-rule consensus analysis
of trees and shrubs occurring in the KNP………………………………………………..44
Figure 5 Comparison of the phylogenetic tree of Angiosperm of the KNP…………..46
Chapter 3
Figure 1 Illustration of Brownian motion (BM) model (A) and Ornstein-Uhlenbeck
(OU) model (B) of trait evolution………………………………………………………….61
Figure 2 Values of Blomberg’s K (dashed red line) for each trait…………………….67
Figure 3 Abouheif test of phylogenetic signal in the studied traits…………..............69
Chapter 4
Figure 1 General pattern of plant diversity and phylogenetic structure along a south-
north gradient in the KNP………………………………………………………………….84
Figure 2 Values of observed phylogenetic species variability (PSV) within
communities (dashed red line)……………………………………………………………85
Chapter 5
Figure 1 Relationships between plant phylogeny and megaherbivory……………….92
Figure 2 Map of the KNP showing major soil types, location of plots and
exclosures…………………………………………………………………………………...95
Figure 3 Location of KNP-plots (small circles) and exclosures (squares) along a
south-north transect in the Park…………………………………………………………..98
xi
List of figures
Figure 4 Comparison of plant diversity and phylogenetic structure between all
exclosures KNP-plots……………………………………………………………..............99
Figure 5 Pairwise comparison of plant diversity between each exclosure and its
adjacent area………………………………………………………………………………100
Figure 6 Pairwise comparison of plant community structure between each exclosure
and its adjacent area……………………………………………………………………..101
Figure 7 Patterns of plant diversity according to age of exclosures contrasted with
pattern in the 110 KNP-plots…………………………………………………………….102
Figure 8 Patterns of plant diversity according to treatment contrasted with pattern in
the 110 KNP-plots………………………………………………………………………..103
xii
Dedication
Dedication
To:
Roees O. Yessoufou;
Mariam O. Yessoufou
Nouratou A. Yessoufou
xiii
List of abbreviations
ACDB African Centre for DNA Barcoding
AIC Akaike Information Criterion
APG Angiosperm Phylogeny Group
BM Brownian Motion Model
BOLD Barcoding of Life Database
BP Bootstrap Percentage
CBOL Consortium of Barcoding of Life
CCDB Canadian Centre for DNA Barcoding
CI Consistency Index
Cij Schoener's Index of Co-occurrence
c.i. Confidence Interval
CIPRES Cyber Infrastructure for Phylogenetic Research
DNA Deoxyribo-Nucleic Acid
xiv
EB Early-Burst
EBI European Bioinformatics Institute
e.g. Exempli Gratia (for example)
F Forward Primer
Full Full Exclosure
GenBank National Centre for Biotechnology Information
GTR + Γ General Time Reversible + Gamma + Proportion
Invariant
H Shannon Diversity Index
ha Hectare
ID Identity
IST Among-site Differences in Species Frequencies
JRAU Herbarium of the University of Johannesburg (UJ),
Johannesburg, South Africa
K Blomberg’s Metric of Phylogenetic Signal
xv
km Kilometre
KNP Kruger National Park
LA Leaf Area
LDM Leaf Dry Mass
LDMC Leaf Dry Matter Content
LFM Leaf Fresh Mass
LT Leaf Thickness
m Meter
m2 Square Meter
matK Maturase K
ML Maximum Likelihood
MP Maximum Parsimony
MUSCLE Multiple Sequence Comparison by Log-
Expectation Program
xvi
NRI Net Relatedness Index
OU Ornstein-Uhlenbeck
Partial Partial Exclosure
PAUP Phylogenetic Analysis Using Parsimony
PCA Phylogenetic Comparative Analysis
PCR Polymerase Chain Reaction
PD Phylogenetic Diversity
PST Gain of Phylogenetic Divergence Among Species
PSV Phylogenetic Species Variability Index
R Reverse Primer
RAxML-VI-HPC Randomized Axelerated Maximum Likelihood for
High Performance Computing
rbcLa Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase
Large Subunit ‘a’
RI Retention Index
xvii
RC Rescaled Index
SI Supplementary Information
SLA Specific Leaf Area
SR Species Richness
Std Standard Deviation
t Student t test
UJ University of Johannesburg, South Africa
vs. Version
WD Wood Density
xviii
Chapter 1 General introduction
Chapter 1
General introduction
1. Savanna ecology
1.1. Features of tropical savannas
Tropical savannas occur under climatic conditions where there are strongly seasonal
rainfall patterns (Frost 1996). They are structured by a continuous grass layer in
which trees and shrubs are sometimes scattered (Nangendo et al. 2006). Meanwhile
savanna landscape may be interspersed with riparian or gallery forests, or patches
of woodland, swamps or marshes (e.g. Kruger National Park; Scholes & Walker
1993).
Globally, savannas cover approximately 20% of the land surface, produce
around 30% of global net primary productivity and provide opportunities for cultural
and economic activities (Scholes & Walker 1993). Tropical savannas represent
about an eighth of the world land area (Scholes & Hall 1996) and account for over
half the area of Africa and Australia, 45 % of South America, and 10% of India and
Southeast Asia (Werner 1991). In addition, savanna areas harbor a large proportion
of the world’s human population and a majority of its rangelands and livestock
(Scholes & Archer 1997). This situation leads to a high pressure on savanna biome,
mostly due to agricultural activities (Scholes & Archer 1997).
Savanna biome is widely distributed in northern and eastern South Africa
where it is referred to as “bushveld” (Schmidt et al. 2007). Bushveld is savanna
woodland dominated by woody vegetation (trees and shrubs) varying from an open
to dense structure with a grassy understorey (Schmidt et al. 2007). Woody species
1
play key roles in the overall ecological function of tropical savannas. They influence
physiological function such as transpiration and production rates and nutrient cycling
and environmental conditions such as soil erosion, and hydrology (Hochberg et al.
1994). The presence or absence of trees and shrubs and their abundance are the
major criteria that assist not only to distinguish between savanna types, but also to
differentiate savanna structure and functions from that of forest and desert biomes
(Scholes & Walker 1993; Burgess 1995; Solbrig et al. 1996). Based on these criteria,
savanna can be referred to as either grassland (no trees/shrubs or presence of very
few that are widely scattered), tree savannas, shrub savannas or savanna
woodlands (Menaut et al. 1990). However, another type of savanna could be defined
as savanna parkland, which is a two-phase mosaic landscape in which circular
clumps, groves of woody plants are dispersed throughout a grassy matrix (Menaut et
al. 1990; San Jose’ et al. 1991).
Tropical savannas are maintained through a complex interaction between
climate (e.g. water availability, rainfall), fire, herbivory, tree growth, and plant
competition, which operate at different scales (Scholes & Archer 1997; Bond 2005;
Bond & Keeley 2005; Biaou 2009). A substantial body of literature has addressed the
individual and interactive effects of these different drivers on savanna structure (e.g.
Biaou 2009; but see Scholes & Archer 1997 for a comprehensive review). The
composition, structure and dynamic of savanna are shaped under fire (Bond & Van
Wilgen 1996) and herbivore pressures (McPherson 1993). The importance of these
two factors (fire and herbivory) in savanna ecology rests on the fact that they are
responsible for the coexistence of two apparently stable states (grassland and
woodland states) that make savanna a particular biome.
2
1.2. Role of fire in savanna ecology
Fire proneness is a well-known feature of African savannas (Bond & Van Wilgen
1996; Anderson et al. 2003). Fire controls the structure of savanna in a simple way
(Scholes & Archer 1997). During dry seasons, grassland experiences periodic fire
that burns grasses, kills vulnerable tree seedlings and eventually prevents trees from
dominating. In doing so, fire ensures the maintenance of the grassland in grassland
state.
In contrast, in savanna woodlands, the relatively high density of trees reduces
the amount of grasses that can grow. The reduction of grass biomass limits
considerably the fire that can burn. As a result, adult trees are safe and many small
trees can grow, thus maintaining the woodland in a woodland state. Meanwhile, a
frequent occurrence of fire within short intervals at high temperature is damageable
for savanna. Frequent fires could kill all trees and force savanna woodland to shift
into a grassland state while the absence of fire causes grassland to shift to closed
woodlands (Scholes & Archer 1997; Higgins et al. 2000; Bond & Archibald 2003;
Govender et al. 2006) and even to forest (Hopkins 1992). Controlling fire intensities
and its frequency is therefore key strategy for the management of savanna
resources. The overall importance of fire resides in that it maintains a dynamic
balance between savanna and forest.
1.3. Importance of herbivory in savanna ecology
Megaherbivores (e.g. elephants, giraffes, rhinos, etc.) play also a crucial role in
shaping savanna landscape (Du Toit et al. 2003; Bond 2005). They eat new tree
seedlings that grow in grassland, thus contributing to maintain grasslands in a
grassland state.
3
Indeed, seedlings and small trees are particularly vulnerable to herbivory from
browsers or grazing herbivores, which trample them or consume them along with
grasses (Borchert et al. 1989; Sankaran et al. 2005). By consuming grasses, grazers
reduce the fuel load (i.e. grasses) and hence reduce fire intensity, frequency and its
capacity to spread (Baisan & Swetnam 1990; Savage & Swetnam 1990). The
reduction of fire effects due to grazing activities favours the release of small trees.
The increase in abundance of small trees could lead to an increase of population
size of megaherbivores. At the same time, due to browsing pressures,
megaherbivores limit tree growth. When grazing and browsing animals are of little
consequence, fire may operate more directly to influence tree-grass mixtures and
may slow, but not prevent, complete tree domination (Hochberg et al. 1994). Thus,
grazer-browser-fire interactions influence strongly savanna ecosystems.
These interactions impose the directionality of savanna dynamic. Forests
change through succession process (after being logged or disturbed), with grasses
growing in, followed by bushes, and then a chain of different trees until some
dominant tree species finish the sequence. In contrast, savannas generally do not
undergo succession, but will switch back and forth between grassland and woodland
without any intermediate stage.
2. Community ecology in a savanna context
2.1. Theories of tree-grass coexistence
What allows species to coexist is one of the major questions that always generate a
great deal of interest in ecology. The question turns out to be even more exciting
when it comes to investigating how two contrasting life-forms (trees and grasses)
could assemble. Absence of niche overlap in resource-use (especially water) could
4
allow such co-existence. Grass roots uptake water from surface soil horizons
whereas tree roots preferentially explore and utilise resources from deeper soil
horizons. This rooting niche separation between grasses and trees results in
absence of competition for resources, thus allowing species coexistence (Webb et
al. 2002; but see Scholes & Archer 1997 for detailed review). Another possible
explanation could be linked to the frequent disturbances occurring in African
savanna (e.g. fire, herbivory). These disturbance events prevent the competitive
ability of one life-form from excluding the other (Scholes & Archer 1997).
Meanwhile, despite these insights, many challenges still remain. For example,
the evolutionary relationships among coexisting species are shown to be critical in
the assembly process (Webb et al. 2002; Hardy & Senterre 2007), but how the
evolutionary history of taxa contributes to the current shape of community
assemblages, especially in tropical savanna ecosystems, is still a debatable
question. Assembly process might be driven by neutral forces such as demographic
drift, dispersal and speciation (neutral theory; Bell 2001; Hubbell 2001; Chave 2004),
but niche differentiation is also likely to play key role in shaping community
composition (deterministic theory; Webb et al. 2002). The increasing availability of
molecular DNA data opens ways of weighing the relative importance of neutral vs.
niche parameters in assembly processes.
2.2. Tree-tree coexistence
In savannas, coexistence of trees has traditionally been attributed to two major
forces: facilitation and competition (Scholes & Archer 1997; Biaou et al. 2011).
Facilitation is the process by which a tree species (nurse species) creates locally
conditions that favour the establishment of other species, which could not persist in
5
the ecosystem in the absence of the nurse tree (Horton & Hart 1998). It is a process
that dominates in harsh ecological conditions (Horton & Hart 1998) such as extreme
temperature, water-deficit, etc.
In contrast, competitive interactions tend to allow a species to exclude others
from the community. Although these two forces play important roles in species
coexistence, one question remains: how to tease apart the effect of each of them in
natural communities (Cahill et al. 2008; Mayfield & Levine 2010).
3. Phylogenetic investigation of community assembly
3.1. The use of DNA barcoding techniques to reconstruct phylogenetic tree
Species identification using morphological characters is well established and widely
used in systematic biology. However, this approach can become challenging due to
phenotypic plasticity, genetic variation in the trait used, and morphological variability
over life cycle (Hebert et al. 2003). It can also mislead especially when it comes to
the identification of small fragments (root, leaf, bark etc.).
DNA barcoding approach is currently increasingly acknowledged as a
potential solution to overcome these challenges (Lahaye et al. 2008; CBOL Plant
Working Group 2009). DNA barcoding has been reputed not only as a tool for
species identification, but also for species discovery (Lahaye et al. 2008). It is
expected to provide accurate, rapid and automatable species identification without
morphological knowledge. It works by means of comparing the DNA sequences from
a small fragment of the genome that is standardised between groups of organisms,
with the aim of contributing to a wide range of ecological and conservation studies in
which traditional morphological identification is not practical (Hebert et al. 2003;
6
Armstrong & Ball 2005; Markmann & Tautz 2005; Savolainen et al. 2005; Smith et al.
2005; Ardura et al. 2010).
Given the performance of DNA barcoding in species identification, it is a
suitable technique for phylogeny reconstruction. Two regions, matK and rbcLa are
identified as DNA barcodes for land plants (Lahaye et al. 2008; CBOL Plant Working
Group 2009). These two regions are used in this study to reconstruct evolutionary
history that connects woody plants occurring in the KNP.
3.2. Rationale of phylogenetic approach in ecology
Several observations have contributed to the current increasing use of phylogeny in
ecology. Firstly, close relatives occur less frequently in local communities (Gotelli &
Graves 1996; Cavender-Bares et al. 2004; Ackerly et al. 2006). Secondly, the
number of species per genus is generally lower in small areas than in larger areas
(Elton 1946). Thirdly, close relatives tend to share similar traits (Darwin 1859;
Felsenstein 1985a; Webb et al. 2002). These observations lead to the conclusion
that there is a phylogenetic driver of community structure. Therefore, the basic
rationale of comparative analysis is that the genetic relatedness of coexisting
species along with the evolutionary pattern of species traits can lead to the dominant
process shaping community structure (Webb et al. 2002; Cavender-Bares et al.
2004; Ackerly et al. 2006; Kembel & Hubbell 2006; Silvertown et al. 2006; Webb et
al. 2006; Hardy & Senterre 2007; Johnson & Stinchcombe 2007; Emerson &
Gillespie 2008; Hardy 2008; Cavender-Bares et al. 2009).
Currently, the use of molecular phylogenetics to investigate patterns in
community structure has largely focused on rainforests (e.g. Webb 2000; Chazdon et
al. 2003; Kembel & Hubbell 2006; Swenson et al. 2006; Webb et al. 2006) with little
7
emphasis on tropical savannas, despite the fact that savanna and forest biomes
represent two distinct systems (Hoffmann et al. 2005).
3.3. Framework in community phylogenetics
The use of phylogeny in ecology is undergoing an exciting development (Chazdon et
al. 2003; Kembel & Hubbell 2006; Swenson et al. 2006; Webb et al. 2006; Cavender-
Bares et al. 2009; Schaefer et al. 2011). Webb et al. (2002) provided a basic
framework, which is guided by Darwin’s (1859) assumption that close relatives could
not coexist due to high competitive exclusion. This theoretical basis of the framework
results in two forces i.e. habitat filtering and competition shaping community
structure (Webb et al. 2002). Habitat filtering is expected to drive either phylogenetic
clustered community when species traits are conserved or overdispersed when traits
are convergent (Figure 1). Meanwhile, when taxa are very similar ecologically and
physiologically (due to close phylogenetic relatedness), there is overlap in resource-
use (niche overlap), resulting in high competitive interactions. Competitive exclusion
should lead to community overdispersion when traits are conserved, but to a random
pattern when traits are convergent.
However, additional forces have been showed to play important roles in
assembly processes, especially facilitation and mutualism (Bruno et al. 2003;
Valiente-Banuet & Verdu 2007; Elias et al. 2009). The most recent limitation to
Webb’s framework was pioneered by Cahill et al. (2008) and Mayfield & Levine
(2010) who demonstrated that competition is not always strong among close
relatives, and that it can also drive clustering pattern.
8
Regional pool Habitat filters Local communities
Figure 1 Interpretation of niche theory based on habitat filtering process. This is an
illustration of Webb et al.’s framework (Webb et al. 2002). Each filled circle indicates
a distinct species; and each colour corresponds to a specific trait. Community
composition is determined by both phylogenetic relatedness and species traits.
During the process, habitat filters (vertical bar in the centre) filter out species lacking
9
a particular trait preventing them to occur in local communities (e.g. red and black
species in A and red and green species in B), while filtering in others exhibiting
compatible traits with the available niches in local communities (green species in A,
and black in B). Local communities in both cases (A and B) are, as a result,
composed of species closely related on the phylogeny (regional pool) and sharing
similar traits (trait conservatism or phylogenetic signal). Such communities are
clustered or underdispersed. In scenario C, taxa less related on the phylogeny and
exhibiting different traits (convergent traits) are filtered in, leading to communities
composed of species with various evolutionary histories. Such communities are
overdispersed or even.
3.4. Emerging patterns in community phylogenetics
Vamosi et al. (2009) recently reviewed studies that investigated assembly processes
from a phylogenetic perspective. This review shows an increase of interest in
phylogenetic study of community ecology, and highlighted three important aspects.
Firstly, the review reveals that three possible expectations of community
structure (clustering, overdispersion and random distribution) are documented in
literature, with clustering emerging as the most frequently observed pattern (Figure
2).
10
15%
Clustering (e.g. Hardy 2008)
Eveness (e.g. Ackerly et al.

2006)
26% 59% Random (e.g. Silvertown et
al. 2006)
Figure 2 Frequency of different possible structures of community assemblages in
literature (Vamosi et al. 2009).
Secondly, the review shows that various systems have been studied, but
plants attracted the most attention (Table 1). Within plant systems, rainforests are
the most dominant (20%) while savannas have received little attention (4%)
(Table1).
Table 1 Summary of systems included in current phylogenetic structure (as reviewed
in Vamosi et al. 2009)
Systems
Microbes Plants Animals
Frequency
in 20.51 64.1 15.39
literature
(%)
Sub-systems
Rainforests Savanna Various Arthropods Vertebrates
(Grassland) trees
Frequency in literature
(%) 20 4 76 33.34 66.66
Thirdly, the majority of these studies were conducted in temperate regions
11
(72%) and only 28% were piloted in tropical biomes (Figure 3). Given that savannas
receive less interest, a better understanding of the phylogenetic structure of savanna
plant communities is urgently needed. For this reason, the current study can be seen
as a contribution to fill this gap, since it is based in the KNP, which is a subtropical
African woodland savanna in South Africa.
28.2
Temperate
Tropical
71.8
Figure 3 Comparison of frequency of study sites (temperate vs. tropical) of
community phylogenetics (as reviewed in Vamosi et al. 2009)
4. Study site and objectives of the study
4.1. Study site
The KNP is situated in the north-eastern part of South Africa between 22°25’ and
25°32’ S and 30°50’ and 32° E. It is part of the ‘Greater Maputaland-Pondoland-
Albany’ biodiversity hotspot (Perera et al. 2011). Rainfall varies from 440 mm in the
north to 740 mm in south (Venter 1990). Mean annual temperature is around 21-
23°C, but in summer temperatures often exceed 38°C, whereas frost can occur
sporadically during Winter.
12
The KNP is one of the largest natural reserves (20,000 km2) in Africa. It is a
savanna ‘woodland biome’ of southern Africa (Schmidt et al. 2007) with various
habitats found within its boundary (Figure 4).
C B
E D
G F
13
Figure 4 Various habitats in the KNP (Photos from O. Maurin): A = View from
Shabeni Hill in the Pretoriuskop section (southern KNP), with from left to right Ship,
Newu and Sitfungwane Mountains. The Pretoriuskop section is an area rich in tree
and shrub species, and several species are restricted to these hills in their
distribution in KNP; B = View on the Biyamiti river (southern KNP, Malelane section).
Many river systems crossed the KNP. Riparian vegetation host many specific trees
and shrubs; C = View of the Lebombo mountains in their northern range. The
Lebombo mountains represent a natural border between South Africa and
Mozambique and are host to a wide number of trees and shrubs; D = View in
foreground on the southern low rolling hills and on background on the Malelane
mountain (southern KNP, Malelane section). The Malelane mountain presents the
highest point in the KNP at 840 m. E = View on the Luvuvhu river and gorge, and the
Matshitshindzudzi mountain range (northern KNP, Pafuri section); F = View on a
rocky outcrop in the Malelane section (Southern KNP). The KNP is scattered with
rocky outcrops that often host species that cannot be found in the surrounding
savanna vegetation; G= View on the Sandveld around Punda Maria (northern KNP,
Punda Maria section). This region has the highest rainfall in the park, estimated
around 530.6 mm/year.
The density of vegetation varies from dense thicket, savanna woodland, tree
savanna and montane savanna to forest with tall trees and closed canopy (Schmidt
et al. 2007; Figure 5). The vegetation of the KNP grows on two major soil types
(basaltic vs. granitic) and consists of approximately 1974 different plant species
including trees and shrubs (458 species), grasses (236 species), ferns (27 species),
lianas (16 species), and aloes (20 species) (Venter 1990). Dominant tree species
14
include Colophospermum mopane (Kirk ex Benth.) Kirk ex J. Leon., Combretum
apiculatum Sond., Acacia nigrescens Oliv., Sclerocarya birrea (A. Rich.) Hochst. and
Combretum imberbe Wawra in the north and Spirostachys africana Sond.,
Terminalia sericea Burch. ex DC., and Dichrostachys cinerea (L) Wight & Arn. in the
south.
Figure 5 Major vegetation types in the KNP (modified from Venter 1990).
15
The fauna of the KNP includes c. 500 bird species (Venter 1990), and it is
home to the largest terrestrial mammals (148 mammal species), of which 30 are
megaherbivores (elephants, rhinos, giraffes, and many species of antelopes; Owen-
Smith & Ogutu 2003; Table 2). These megaherbivores (defined here as herbivorous
mammals weighing over 5 kg) are one of major components of African savanna
because of their ecological importance (ecosystem engineers, Waldram et al. 2008;
or keystone ecosystem species, Owen-Smith 1988). They exert continuous
pressures on plant communities, increasing landscape heterogeneity (Du Toit et al.
2003; Figure 6), but little is known as to the extent of their impacts.
Figure 6 Giraffe during feeding activity in the KNP (Photo from K. Yessoufou)
16
Table 2 Megaherbivores in the KNP, abundance and dietary behaviour. - indicates missing information
Species Common name Diet Feeding behaviour Abundance in KNP
(Prins & Douglas-Hamilton 1990; Gagnon (Prins & Douglas-Hamilton 1990; Gagnon (census 2009;
& Chew 2000) & Chew 2000) www.sanparks.org
Aepyceros melampus Impala Browser-grazer Generalist 127,788
Cephalophus natalensis Red duiker Frugivores Specialist -
Connochaetes taurinus Blue wildebeest Variable grazers Specialist 8,963
Damaliscus lunatus Tsessebe Obligate grazer Specialist 160
Hippotragus equinus Roan Variable grazers Specialist 50
Hippotragus niger Sable Variable grazers Specialist 325
Kobus ellipsiprymnus Waterbuck Variable grazers Specialist 5,000
Neotragus moschatus Suni Browser Specialist -
Oreotragus oreotragus Klipspringer Browser-grazer Generalist -
Ourebia ourebi Oribi Variable grazers Specialist -
Pelea capreolus Grey rhebok Browser Specialist -
Raphicerus campestris Steenbok Browser-grazer Generalist -
Raphicerus sharpei Sharpe’s grysbok Browser-grazer Generalist -
Redunca arundinum Reedbuck Obligate grazer Specialist 300
Redunca fulvorufula Mountain reedbuck Obligate grazer Specialist 150
Sigmoceros lichtensteinii Lichtenstein’s Obligate grazer Specialist -
hartebeest
Sylvicapra grimmia Common duiker Browser Specialist -
Syncerus caffer Buffalo Variable grazers Specialist 37,462
Taurotragus oryx Eland Browser-grazer Generalist 300
Tragelaphus angasii Nyala Browser-grazer Generalist 300
Tragelaphus scriptus Bushbuk Browser Specialist 500
Tragelaphus strepsiceros Kudu Browser-grazer Generalist 8,045
Giraffa camelopardalis Giraffe Browser Specialist 7,091
Hippopotamus Hippo Obligate grazer Specialist 3,000
amphibious
Phacochoerus aethiopicus Warthog Variable grazer Specialist 2,316
Potamochoerus porcus Bushpig Browser Specialist -
Equus burchelli Burchell’s zebra Obligate grazer Specialist 20,868
Ceratotherium simum White rhino Variable grazer Specialist 12,158
Diceros bicornis Black rhino Browser Specialist 627
Loxodonta africana Elephant Browser-grazer Generalist 13,573
17
4.2. Objectives
The current project aims to:
1- Assemble the phylogeny of all trees and shrubs occurring in the KNP;
2- Investigate the suitability of commonly used models of evolution for
plant ecological traits;
3- Investigate the processes of community assembly (deterministic vs.
neutral) in the KNP;
4- Address the impacts of megaherbivores on community structure in the
KNP.
18
4.3. Outline of the thesis
The thesis comprises six chapters briefly described as follow:
Chapter 1
General Introduction
Chapter 2
Phylogeny of trees and shrubs in the KNP using
DNA barcodes
Chapter 3
Testing suitability of evolutionary models using traits
of woody plants in the KNP
Chapter 4
Characterising diversity and phylogenetic structure
of woody plant communities in the KNP
Chapter 5
The role of megaherbivores in shaping the
structure of subtropical plant communities
Chapter 6
General Conclusion
19
Figure 7 Diagram indicating the structure of the thesis (see below for details). Each
Chapter is linked to the next, with link indicated by arrows. For example, the general
introduction (Chapter 1) covers all themes discussed in the entire thesis; the
phylogeny presented in Chapter 2 is used in all chapters that follow; etc. Chapter 6 is
linked to all precedent chapters in that it gives a synthesis of all findings.
- Chapter 1: General introduction
It presents a general overview on savanna ecology with emphasis on theories of
coexistence and the rationale of the phylogenetic approach in assembly processes.
- Chapter 2: Phylogeny of trees and shrubs in the Kruger National Park
using DNA barcodes
I use plant DNA barcodes (rbcLa + matK; CBOL Plant Working Group 2009) to
reconstruct the evolutionary pathways that connect all trees and shrubs occurring in
the study area. This phylogeny is used as the regional pool in all phylogenetic
analyses conducted in this thesis.
- Chapter 3: Testing suitability of evolutionary models using traits of
woody plants in the KNP
Comparative analysis is a widely used technique in modern evolutionary biology
(Felsenstein 1985a; Freckleton & Harvey 2006; Ackerly 2009; Jombart et al. 2010;
Wiens et al. 2010; Davies et al. 2011; Schaefer et al. 2011). Most studies that apply
this technique assume that ecological traits follow a Brownian motion (BM) of
character evolution without prior test (Freckleton & Harvey 2006). However recent
studies suggest that BM model might not be a generalisable model for all traits
20
(Freckleton & Harvey 2006; Ackerly 2009). Here I fit various models of evolution, and
discuss the best candidate for comparative analysis of plant traits in the KNP.
- Chapter 4: Characterising diversity and phylogenetic structure of woody
plant communities in the KNP
How communities assemble and how they respond to change are still controversial
questions in ecology (Webb et al. 2002; Cavender-Bares et al. 2009). Communities
might assemble through a random process (neutral theory; Hubbell 2001), but
several studies challenge this theory (e.g. Cavender-Bares et al. 2004; Hardy &
Senterre 2007), advocating that community composition is determined by niche
characteristics. Characterising community structure is critical as to what are the
major dominant forces that dictate community composition (Hardy & Senterre 2007;
Hardy 2008; Hardy & Jost 2008). In this chapter I discuss these questions in the
KNP using a phylogenetic approach.
- Chapter 5: The role of megaherbivores in shaping the structure of
subtropical plant communities
To date, results of studies that address megaherbivores impacts on plant
communities are mixed. Megaherbivores might favour species diversity (Kalwij et al.
2010), but could also have negative impacts (Asner et al. 2009). The presence of
exclosures in the park, provides an opportunity to address the question in the KNP.
This is discussed, and for the first time, the theoretical predictions of Cavender-
Bares et al. (2009) are tested experimentally.
21
- Chapter 6: General conclusion
The last chapter highlights the main findings and their relevance but also opens
complementary areas for future studies.
22
Chapter 2 The phylogeny of trees and shrubs in the Kruger National Park using DNA barcodes
Chapter 2
The phylogeny of trees and shrubs in the Kruger National Park using DNA
barcodes
1. Introduction
Phylogeny is used to address taxonomical questions and classification of a set of
taxa (e.g. Angiosperms, APG III 2009). Meanwhile, over the past 20 years, it has
been acknowledged as an important tool for ecological investigations (Vamosi et al.
2009; Cavender-Bares et al. 2009). Key ecological questions related to species
coexistence (Vamosi et al. 2009; Cavender-Bares et al. 2009), conservation (Purvis
& Gittleman 2005; Forest et al. 2007), species and ecosystems responses to global
change (Willis et al. 2008), and biological invasions (Proches et al. 2008; Cadotte et
al. 2009; Schaefer et al. 2011) are undergoing phylogenetic investigation.
Furthermore, conservation planning, which traditionally focuses only on species
diversity increasingly acknowledges the necessity of taking phylogenetic information
into account (Forest et al. 2007).
Merging phylogeny and ecology brings additional values to ecological studies
for three main reasons. First, because species delimitation is still a debatable
question, conservation planning based only on species diversity could be biased
(Mace et al. 2003). Therefore, the use of diversity metric, which is not sensitive to
species delimitation (e.g. phylogenetic diversity; Faith 1992) can contribute additional
key information to biodiversity quantification (Isaac et al. 2004; Faith & Williams
2005). Second, phylogenetic diversity (PD) is not a surrogate of species diversity
and therefore conveys different features of diversity (Forest et al. 2007; Knapp et al.
23
2008). Third, the higher the PD the more productive the ecosystem (Maherali &
Klironomos 2007; Cadotte et al. 2008) and stronger its ability to survive
environmental changes (Forest et al. 2007; Knapp et al. 2008). In addition, a high PD
is expected to favour ecosystem resistance to pathogen attacks (Gilbert & Webb
2007) and invasion (Cavender-Bares et al. 2009). Given the importance of utilising
phylogeny in ecology, providing ecologists with a working DNA-based phylogeny for
a biodiversity hotspot, is crucial to fuel ecological investigations that can help
develop practical tools to sustain its biological diversity. Meanwhile, a
comprehensive DNA database to reconstruct the more likely phylogenetic
relationships among taxa occurring in a specific site is not always available
(Anderson et al. 2004). This lack constrains ecologists to use a ‘Phylomatic’
approach (Webb & Donoghue 2005) for phylogeny reconstruction.
Phylomatic is a program that uses a megatree [e.g. Davies et al.’s (2004)
Angiosperm consensus tree] to generate a rapid and instant phylogeny of any set of
higher plant taxa (Webb & Donoghue 2005). It utilises as input file a list of taxa for
which family and genus information are provided. The program performs a series of
match of the input taxa to the most resolved position possible in the indicated
megatree in the database. For each input taxon, a match in the megatree is first
sought for the genus name. Failing this, a match is sought for the family name. As a
result, congeners are attached to a polytomous genus node. However, if no internal
phylogeny is available for a family, the genera nodes are connected directly to a
polytomous family node. To generate a tree, family clades are connected using the
super-familial resolution in the megatree (Webb & Donoghue 2005). Although this
approach has proven useful (e.g. Kembel & Hubbell 2006), recent studies have
24
showed that it could be problematic for ecological analyses because of the
polytomies often generated between congeners (Kress et al. 2009).
In this study I contribute to generate the first and largest plant DNA barcode
database (sensu CBOL Plant Working Group 2009) for a tropical African woodland
reserve, the Kruger National Park (KNP) in South Africa. Although the primary
objective of DNA barcoding is not to assemble phylogenetic trees, it has been
proved extremely valuable for phylogenetic investigations of ecological questions
(Kress et al. 2009). The main objective of the current study is to provide ecologists
with a phylogenetic framework with which to address such questions in the KNP.
2. Material and methods
2.1. Samples collection
From 2006 to 2010, intensive fieldwork was conducted throughout the KNP, during
which leaf materials were collected for 445 tree and shrub species occurring in the
park. Leaf tissue was collected for DNA analyses during field collection, and placed
into plastic bags filled with silica gel. Species identification was facilitated using field
guides (Schmidt et al. 2007). All herbarium vouchers and DNA extracts are housed
at the herbarium JRAU, and the DNA Bank at the University of Johannesburg (UJ),
with all data available online (www.acdb.co.za).
2.2. DNA extraction, PCR and sequences
Leaf samples were sent to the Canadian Centre for DNA Barcoding (CCDB) where
two DNA regions were sequenced: a portion of matK and subunit 'a' of rbcL. These
regions have been identified as suitable 'DNA barcodes' for land plants (CBOL Plant
Working Group 2009), but also for phylogeny reconstruction (Kress et al. 2009).
25
Molecular procedures conducted at CCDB (DNA extraction, amplification and
sequencing) follow several steps which are presented in Figure 1.
DNA extraction was performed using a semi-automated protocol as described
by Hajibabaei et al. (2005) and Ivanova et al. (2008).
Polymerase Chain Reactions (PCR) used a PCR cocktail including 5
trehalose as a PCR enhancer. PCR was run in two rounds, the first round being
essentially the “proper” PCR, and the second round was mainly failure tracking
(Figure 1). Different primers were used at each round. For rbcLa, the primers rbcLa-
F/rbcLa-R was used during the first round of PCR reactions, and rbcLa-
F/rbcLajf634R during the second round whereas 1R_KIM-f/3F-KIM-r (1st round) and
matK-390f/matK-1326r (2nd round) was used for matK. These two sequential PCR
rounds with different primer sets allow improvement of sequencing success for both
rbcLa and matK.
Sequencing of the cleaned PCR products were conducted using the standard
CCDB sequencing protocols described by Hajibabaei et al. (2005). The sequencing
process was followed by sequence editing (Figure 1), whereafter sequences were
uploaded on the Barcoding of Life Data base (BOLD; www.boldsystems.org).
26
Sample’s Entering
CCDB
MATRIX BOX
TISSUE PLATE
LYSIS
DNA Extraction
PCR
PCR Gel Band Verification

(E-Gel)
FAILURE TRACKING
Positive Hit-Picking Cycle Sequencing

SECONDARY PCR
(Different Primer Pair)
Full 96 Well Plate Cycle Sequencing Cleanup PCR Gel Band Verification
(E-Gel)
DNA Sequencing Positive Hit-Picking
Sequence Editing and upload Full 96 Well Plate

to BOLD
Figure 1 Representation of steps for DNA sequencing at CCDB.
2.3. Sequences alignment
Sequences were aligned using Multiple Sequence Comparison by Log-Expectation
program (MUSCLE vs. 3.8.31; Edgar 2004). Subsequent adjustments were made by
eye when there were obvious alignment errors. All aligned sequences were
submitted to GenBank/EBI. All GenBank/EBI accession numbers for gene
sequences (accession numbers JF265241-JF265667 for rbcLa and JF270599-
JF271008 for matK) and voucher information (including photographic images) are
available online (www.acdb.co.za) and listed in Supplementary Information Table S1.
I finally combined all sequences (matK and rbcLa) in a single matrix for phylogenetic
analysis. Tree statistics (consistency index CI, rescaled index RC, and retention
index RI) for each partition (rbcLa and matK) were also calculated using PAUP*
(Swofford 2003). I applied two methods of tree reconstruction.
27
2.4. Tree reconstruction
I reconstructed the phylogeny of 445 species plus Amborella used as outgroup to
root the tree (APG III 2009); these species represent 246 genera, 71 families and 30
orders (sensu APG III 2009; Supplementary Information Table S1). Phylogeny
reconstruction based on combined matK + rbcLa data was performed with maximum
likelihood (ML; Felsenstein 1973). The combined two-gene dataset was
phylogenetically analysed using RAxML-VI-HPC 7.2.6 (Randomized Axelerated
Maximum Likelihood for High Performance Computing; Stamatakis et al. 2008) on
the CIPRES cluster (Miller et al. 2009). Based on the Akaike Information Criterion
(Akaike 1974) as implemented in jModeltest (Posada 2008), all analyses utilised the
GTR + Γ model of nucleotide substitution and the rapid hill-climbing algorithm. This
model indicates six general time-reversible substitution rates, assuming gamma rate
heterogeneity. In the combined analysis, model parameters were estimated and
optimised separately for each gene. Each analysis comprised 1000 alternative runs
from distinct randomised maximum parsimony starting trees. To assess branch
support, non-parametric bootstrap analyses (Felsenstein 1985b) with 1000 replicates
were conducted.
I also reconstructed the phylogeny using maximum parsimony (MP). Tree
searches were conducted using heuristic searches with 1000 random sequence-
additions but keeping only 10 trees per replicate to reduce time spent on branch
swapping in each replicate. Tree bisection-reconnection was performed with all
character transformations treated as equally likely i.e. Fitch parsimony (Fitch 1971).
MP searches and bootstrap resampling were performed using PAUP* (Swofford
2003). Resulting trees (available on TreeBase ID 11232) were summarised as
28
majority-rule consensus tree. Bootstrap support (BP) was classified as high (85-100),
moderate (75–84) or low (50-74).
3. Results
3.1. Tree statistics
Tree statistics are summarised in Table 1. The alignment of each gene including
gaps resulted in 552 and 942 characters for rbcLa and matK respectively, making
the aligned combined-genes consisted of 1494 characters. The aligned matK
contains the most variable sites (80) whereas only 47 of sites in rbcLa are variable.
The number of potentially informative sites is also higher for matK (71) than for rbcLa
(42). Variable positions followed the same trend with matK containing the highest
average number of changes per variable site (9.63) followed by rbcLa (9.23).
Parsimony trees are shorter with rbcLa matrix (2373 steps) and higher with matK
(7220 steps). Comparing the indices values, again rbcLa scored lower for CI, RI and
RC than matK (Table 1).
Table 1 Characteristics of each partition obtained from PAUP*. * = indicate number
of missing sequences for each region.
Characteristics rbcLa matK Combined matrix
Number of taxa included 432 (13*) 412 (33*) 445
Total number of characters 552 942 1494
Number of constant characters 295 192 487
Number of variable sites 257 (47% ) 750 (80%) 1007 (67%)
Number of parsimony informative sites 230 (42% ) 669 (71%) 899 (60%)
Number of steps (tree length) 2373 7220 9707
Consistency index (CI) 0.18 0.22 0.21
Retention index (RI) 0.83 0.84 0.84
29
Rescaled index (RC) 0.15 0.19 0.18
Average number of changes per variable site 9.23 9.63 9.25
(number steps/number variable sites)
3.2. Phylogeny of trees and shrubs of the KNP
In Figure 2, I present the maximum likelihood tree, henceforth referred to as ML tree.
Figure 3 presents the majority-rule consensus phylogeny generated using the
maximum parsimony approach. This tree is referred to as MP tree. There is a strong
similarity between both the trees (high congruence) but with a few noteworthy
differences (see discussion section). Bootstrap supports for all clades and subclades
resulting from MP and ML analyses are presented in Table 2. In discussion section,
when BP values obtained from MP and ML analyses are different, I report only the
highest BP value and specify the type of analysis (MP or ML).
Major clades and subclades obtained from the detailed MP and ML trees are
summarised below (Figure 4). This summary tree reveals 11 major clades:
Monocotyledonae (Arecales, Pandanales, and Asparagales), Magnoliidae
(Canellales, Laurales, and Magnoliales), Basal Eudicots (Ranunculales and
Proteales), Caryophyllales, Ericales, Campanulidae (Apiales and Asterales),
Lamidae (Gentianales, Boraginaceae, Lamiales, Solanales, and Icacinaceae),
Santalales, Vitales, Malvidae (Sapindales, Malvales, Brassicales, Myrtales, and
Geraniales) and Fabidae (Fabales, Fagales, Rosales, Malpighiales, Celastrales, and
Zygophyllales) (Figure 4).
30
69
Albizia versicolor
42 Albizia tanganyicensis
47 Albizia brevifolia
67 Albizia harveyi
32 Albizia anthelmintica
82 Albizia forbesii
99
Albizia petersiana
87
Albizia adianthifolia
Faidherbia albida
67
Acacia caffra
52 27 Acacia nigrescens
12 Acacia welwitschii
28 Acacia erubescens
93 Acacia ataxacantha
Acacia senegal
100
Acacia brevispica
Acacia schweinfurthii
73
Acacia grandicornuta
45 Acacia gerrardii
46
59 Acacia robusta
36 Acacia luederitzii
40 Acacia tortilis
Acacia davyi
19 29
Acacia exuvialis
18 Acacia swazica
40
22 Acacia borleae
38 59 Acacia karroo
97 Acacia xanthophloea
Acacia sieberiana
56
Acacia nilotica
31 Adenopodia spicata
35
Piliostigma thonningii
Acacia burkei
71
Elephantorrhiza burkei
42
100 Elephantorrhiza goetzei Fabaceae
31 Elephantorrhiza elephantina
49 Dichrostachys cinerea
Newtonia hildebrandtii
48
Xylia torreana
19 89
Peltophorum africanum
Burkea africana
41 93
Senna petersiana
Cassia abbreviata
Pterolobium stellatum
93
Erythrina humeana
100 Erythrina latissima
100 Erythrina lysistemon
76 Pseudarthria hookeri
Philenoptera violacea
97
Mundulea sericea
38 74 Xeroderris stuhlmannii
65 98
Indigofera fulgens
Indigofera tinctoria
Baphia massaiensis
100
Dalbergia melanoxylon
75 99 Dalbergia armata
100 Ormocarpum trichocarpum
99
Pterocarpus angolensis
25 43 Pterocarpus rotundifolius
52
69
Calpurnia aurea
100 Crotalaria laburnifolia
Bolusanthus speciosus
57
Cordyla africana
Xanthocercis zambesiaca
35
100
Schotia brachypetala
52 Schotia capitata
100 Colophospermum mopane
79 Afzelia quanzensis
43
Guibourtia conjugata
72 Bauhinia galpinii
Securidaca longepedunculata Polygalaceae
Myrica pilulifera Myricaceae
14
Ficus burkei
17 Ficus petersii
14 Ficus stuhlmannii
13 Ficus tettensis
40 Ficus abutilifolia
Ficus glumosa Moraceae
100 Ficus ingens
77 85
60
Ficus salicifolia
100
72
Ficus sycomorus
Ficus sur
Maclura africana
(k) (l) (m)
31
(k) (l) (m)

44
100
Pouzolzia mixta Urticaceae
100 Obetia tenax
81
Chaetachme aristata Ulmaceae /
100 Celtis africana
Trema orientalis Cannabaceae
100 Berchemia zeyheri
72
100 Berchemia discolor
85 Rhamnus prinoides Rhamnaceae
100
Ziziphus mucronata
68
Helinus integrifolius
Ziziphus rivularis
100
Euphorbia cooperi
100 Euphorbia rowlandii
95 Synadenium cupulare
100 Euphorbia tirucalli
98 Euphorbia espinosa
Spirostachys africana
51
72
Ricinus communis
53 Acalypha glabrata
Alchornea laxiflora Euphorbiaceae
61
Croton menyharti
83 65 Croton pseudopulchellus
Croton madandensis
100 Croton megalobotrys
29
100 52 Croton steenkampianus
46 Croton gratissimus
16 Croton sylvaticus
60
Clutia pulchella
Suregada africana
Parinari curatellifolia Chrysobalanaceae
10
100
Ochna natalitia
100 Ochna inermis Ochnaceae
97 30 Ochna pulchra
Triaspis hypericoides
17 95 Malpighiaceae
Acridocarpus natalitius
14 Hugonia orientalis Linaceae
Erythroxylum emarginatum
100
Erythroxylum delagoense Erythroxylaceae
58
Phyllanthus reticulatus
100
Phyllanthus pinnatus
35
Flueggea virosa
Margaritaria discoidea
97 Bridelia mollis Phyllantaceae
78
94 100 Bridelia cathartica
70 100 Bridelia micrantha
Pseudolachnostylis maprouneifolia
78
99
Hymenocardia ulmoides
Antidesma venosum
Androstachys johnsonii Picrodendraceae
43
Oncoba spinosa
19 Scolopia zeyheri
37 Trimeria grandifolia Salicaceae
23 Flacourtia indica
70 Homalium dentatum
87 Dovyalis caffra
58 Salix mucronata
10 Adenia spinosa
100 Passifloraceae
57 Paropsia braunii
97
Xylotheca kraussiana Achariaceae
79 Kiggelaria africana
100
Drypetes reticulata Putranjavaceae
5 Drypetes gerrardii
Garcinia livingstonei Clusiaceae
63
Gymnosporia maranguensis
60 Gymnosporia putterlickioides
60 Gymnosporia heterophylla
46 Gymnosporia sp. nov C
58 Putterlickia verrucosa
52
Gymnosporia pubescens
79
63 Gymnosporia oxycarpa
62
Gymnosporia senegalansis Celastrasceae
100
Maytenus undata
42 100 Catha edulis
Mystroxylon aethiopicum
Elaeodendron transvaalense
100
99
Loeseneriella crenata
99 Pristimera indica
96 Pristimera longipetiolata
Salacia kraussii
100
Balanites pedicillaris Balanitaceae
Balanites maughamii
63
Searsia chirendensis
40 Searsia pyroides
87 Searsia transvaalensis
99 Searsia leptodictya
87
Searsia pentheri Anacardiaceae
100
Searsia gueinzii
100
Searsia magalismontana
77
Ozoroa sphaerocarpa
Ozoroa englerii
(k) (l) Ozoroa obovata
32
(k) (l)
41
Commiphora glandulosa
33 63 Commiphora pyracanthoides
48 Commiphora africana
58 Commiphora schimperi Burseraceae
62 Commiphora mollis
47 Commiphora edulis
97 100 Commiphora marlothii
64
Commiphora harveyi
Commiphora neglecta
99
Sclerocarya birrea
91 55 Lannea schweinfuthii
100
Harpephyllum caffrum Anacardiaceae
98
Lannea edulis
Lannea discolor
72
100
Kirkia wilmsii Kirkiaceae
Kirkia acuminata
37
Toddaliopsis bremekampii
76 Vepris reflexa
94 Teclea pilosa
Vepris lanceolata
63
74
Zanthoxylum capense Rutaceae
97 Zanthoxylum leprieurii
78 100 64 Zanthoxylum humile
99
Calodendrum capense
Clausena anisata
Ptaeroxylon obliquum
100
Turraea nilotica
98 100 Turraea floribunda
100 Turraea obtusifolia
100
Trichilia emetica Meliaceae
72 Trichilia dregeana
97 100
Ekebergia pterophylla
Ekebergia capensis
Entandophragma caudatum
99
Stadmannia oppositifolia
84
Pappea capensis
100
Deinbollia oblongifolia
92 Deinbollia xanthocarpa Sapindaceae
97
Allophylus decipiens
Allophylus africanus
Hippobromus pauciflorus
95
Grewia monticola
75 Grewia bicolor
100 100 Grewia hexamita
95 Grewia inaequilatera
Grewia sulcata
100
Grewia gracillima
78
Grewia flavescens
Grewia villosa
99 100
Grewia microthyrsa
Grewia caffra
Triumfetta pilosa Malvaceae
61
Hibiscus calyphyllus
72
Hibiscus micranthus
100
79
Gossypium herbaceum
93 Azanza garckeana
78 Abutilon angulatum
Adansonia digitata
100
Sterculia rogersii
89 Sterculia murex
100
Dombeya rotundifolia
99 Dombeya cymosa
97
Maerua rosmarinoides
67 Maerua juncea subsp. crustata
25 Maerua angolensis
71
20
Maerua caffra
76
Thilachium africanum
72 Maerua parvifolia
Maerua decumbens
93 Boscia angustifolia Capparaceae
51
50 87 Boscia mossambicensis
96 100 Boscia foetida
Boscia albitrunca
100 Cadaba termitaria
91
Capparis sepiaria subsp. glabrata
99 Capparis tomentosa
100
Capparis fascicularis
100
Salvadora persica
100 Salvadora australis Salvadoraceae
Azima tetracantha
77
Combretum erythrophyllum
68 Combretum woodii
71 Combretum kraussii
100
Combretum mkuzense
87 Combretum zeyheri
100
Combretum molle Combretaceae
73
Combretum apiculatum
63
100
Combretum collinum
94 Combretum celastroides
94 90 Combretum hereroense
Combretum imberbe
(b) (f) (g) (h) (i) (j)
33
(b) (f) (g) (h) (i) (j)
43
Terminalia prunioides
96 Combretum microphyllum
100
Combretum mossambicense Combretaceae
95
Pteleopsis myrtifolia
100 Terminalia phanerophlebia
100 Terminalia sericea
100 Combretum padoides
100
Syzygium cordatum
87 Syzygium guineense Myrtaceae
100 Eugenia natalitia
54 Heteropyxis natalensis
97 Lythraceae
Galpinia transvaalica
Ludwigia octovalvis Onagraceae
Bersama lucens Melianthaceae
74
Rhoicissus tridentata
100 Rhoicissus tomentosus
100 Rhoicissus revoilii Vitaceae
100
Cissus cactiformis
Cissus cornifolia
64
Pavetta catophylla
100
Pavetta edentula
68
Pavetta schumanianna
97 Pavetta lanceolata
90
Tarenna supra axillaris
53 56 Tarenna zygoon
Leptactina delagoensis
Kraussia floribunda
68 100
Catunaregam spinosa
58 Plectroniella armata
33 Hyperacanthus amoneus
Rothmannia fischeri
39
99
94
Gardenia volkensii
89 Gardenia resiniflua
Coddia rudis Rubiaceae
85
100
Tricalysia junodii
Tricalysia lanceolata
Crossopteryx febrifuga
100
42
Vangueria infausta
100 Lagynias dryadum
100 Vangueria madagascariensis
Canthium inerme
100
86
Pyrostria hystrix
80 Canthium setiflorum
100 Psydrax locuples
Heinsia crinita
98
Cephalanthus natalensis
100 Breonadia salicina
Hymenodictyon parvifolium
99
Strophanthus petersianus
95
Strophanthus kombe
99
Adenium multiflorum
95 Adenium swazicum
100 97
Pachypodium saundersii
Holarrhena pubescens
Wrightia natalensis
100
Acokanthera rotundata
100
43 Acokanthera oppositifolia Apocynaceae
81 Carissa edulis
98
58 51
Carissa bispinosa
32
Carissa tetramera
48 Diplorhynchus condylocarpon
Landolphia kirkii
100 99
Tabernaemontana elegans
Tabernaemontana ventricosa
Rauvolfia caffra
99
Strychnos pungens
91
40 Strychnos madagascariensis
41 Strychnos decussata
Loganiaceae
91 91 Strychnos potatorum
100 Strychnos spinosa
Strychnos usambarensis
Anthocleista grandiflora Gentianaceae
91
Karomia speciosa
30 Clerodendrum glabrum
55 Tinnea rhodesiana
28
Leonotis nepetifolia
44 Premna mooiensis Lamiaceae
67
Vitex patula
100 100 Vitex harveyana
Vitex ferruginea
100
Tetradenia riparia
Pychnostachys reticulata
89
Duvernoia aconitiflora
43 Duvernoia adhatodoides
37 Anisotes rogersii
100 Anisotes formosissimus
100 Metarungia longistrobus Acanthaceae
100
Ruspolia hypocrateriformis
100 Ruttya ovata
26 100
Barleria albostellata
Barleria rotundifolia
(a) (b) (c) (d) (e)
34
(a) (b) (c) (d) (e)
26
Sesamothamnus lugardii Pedaliaceae

95 Markhamia zanzibarica
72 78 Kigelia africana Bignoniaceae
72 Rhigozum zambesiacum
Tecomaria capensis
63
Lippia javanica
100 Lantana rugosa
100 91 Lantana camara Verbenaceae
Duranta erecta
95
Nuxia opposifolia
100 Nuxia congesta Stilbaceae
88 Nuxia floribunda
100
44 Halleria lucida
Chionanthus foveolatus
48 Chionanthus peglerae
76 Olea europaea africana
Schrebera alata Oleaceae
99 53 100
97
Jasminum stenolobum
100 Jasminum multipartitum
Jasminum fluminense
Solanum catombelense
100 Solanum lichensteinii Solanaceae
65 38 Solanum panduriforme
Nicotiana glauca
51
Cordia grandicalyx
57 Cordia ovalis
100 Cordia caffra
98
Cordia monoica Boraginaceae
100 Cordia sinensis
100
100
Ehretia rigida
Ehretia amonea
Cassinopsis ilicifolia Icacinaceae
Apodytes dimidiata
100
Cussonia natalensis Araliaceae
98
Cussonia spicata
100
Heteromorpha arborescens Apiaceae
100
Steganotaenia araliacea
Pittosporum viridiflorum Pittosporaceae
100
92
Vernonia aurantiaca
Vernonia colorata
100 Asteraceae
94
Brachylaena transvaalensis
Brachylaena huillensis
100 53
Euclea divinorum
53 Euclea undulata
85
87
Diospyros galpinii
99 Euclea natalensis
63
Euclea daphnoides
90
Euclea daphnoides var. schimperi Ebenaceae
44
Diospyros lycoides
67 Diospyros whyteana
100 97 Diospyros dichrophylla
Diospyros villosa
99
Diospyros mespiliformis
92 Diospyros natalensis
100 68
Manilkara sp.
93 Manilkara mochisia
94 Manilkara concolor Sapotaceae
79 Mimusops zeyheri
100 Sideroxylon inerme
62 Englerophytum magalismontanum
100 Maesa lanceolata Primulaceae
Plumbago zeylanica
100
Plumbago auriculata Plumbaginaceae
100
Portulacaria afra Portulacaceae
10
100
Ximenia caffra
95 Ximenia americana Olacaceae
Olax dissitiflora
Faurea saligna Proteaceae
Faurea rochetiana
Clematis brachiata Ranunculaceae
99
Uvaria gracilipes
85 Hexalobus monopetalus
86 Monodora junodii var. junodii
58
100
Uvaria lucida Annonaceae
99
Monanthotaxis caffra
100 Annona senegalensis
57 100
Artabotrys brachypetalus
Xylopia parviflora
88
Gyrocarpus americanus Hernandiaceae
Warburgia salutaris Canellaceae
69
Aloe marlothii
87 Aloe spicata Asparagaceae /
99 Aloe excelsa Asphodelaceae
55 Dracaena aletriformis
Xerophyta retinervis Velloziaceae
100
100
Hyphaene coriacea
99 Hyphaene petersiana Arecaceae
100 Borassus aethiopium
Phoenix reclinata
Amborella trichopoda Amborellaceae
Figure 2 The maximum likelihood phylogeny of trees and shrubs occurring in the
KNP. Values indicated on the branches are bootstrap values. Family names are
indicated following APG III (2009). Amborella trichopoda (Amborellaceae) is used as
35
outgroup. Names of species in red indicate species recorded in plot surveys for
analyses in chapters 4 and 5.
36
66 Albizia versicolor
Albizia tanganyicensis
Albizia harveyi
Albizia brevifolia
97 Albizia petersiana
79 Albizia adianthifolia
73 Albizia anthelmintica
Albizia forbesii
'Faidherbia albida
Acacia welwitschii
Acacia senegal
95 Acacia nigrescens
Acacia erubescens
Acacia caffra
Acacia ataxacantha
Acacia burkei
100 Acacia schweinfurthii
Acacia brevispica
Acacia robusta
64 Acacia luederitzii
Acacia grandicornuta
Acacia gerrardii
Acacia tortilis
Acacia davyi
Acacia xanthophloea
53 Acacia swazica
Acacia karroo
Acacia exuvialis
Acacia borleae
52 Acacia sieberiana
Acacia nilotica
'Adenopodia spicata
66 Elephantorrhiza goetzei
100 Elephantorrhiza burkei
68
Elephantorrhiza elephantina
Newtonia hildebrandtii
Dichrostachys cinerea
Xylia torreana
Fabaceae
51 Peltophorum africanum
Burkea africana
64 95 Senna petersiana
Cassia abbreviata
Pterolobium stellatum
82
Erythrina lysistemon
82
Erythrina latissima
Erythrina humeana
69
Pseudarthria hookeri
75 95 Philenoptera violacea
Mundulea sericea
Xeroderris stuhlmannii
100 Indigofera tinctoria
Indigofera fulgens
Baphia massaiensis
100 Dalbergia melanoxylon
97 Dalbergia armata
100 Ormocarpum trichocarpum
99 Pterocarpus rotundifolius
Pterocarpus angolensis
58 Crotalaria laburnifolia
98 Calpurnia aurea
Bolusanthus speciosus
Securidaca longepedunculata Polygalaceae
Cordyla africana
Xanthocercis zambesiaca
Piliostigma thonningii
51 Schotia capitata
86 Schotia brachypetala
99 Guibourtia conjugata
Afzelia quanzensis
Colophospermum mopane
Bauhinia galpinii
Myrica pilulifera
[22 tips] Myricaceae
[70 tips]
[115 tips]
[5 tips]
[3 tips]
[133 tips]
[3 tips]
[3 tips]
[10 tips]
[9 tips]
[1 tip]
37
[72 tips]
74 Ficus salicifolia
Ficus ingens
Ficus sycomorus
Ficus sur
Ficus stuhlmannii
96
Ficus petersii
Ficus tettensis
Moraceae
96
Ficus glumosa
Ficus burkei
Ficus abutilifolia
Maclura africana
100
56 Chaetachme aristata
92 Celtis africana
Trema orientalis
Ulmaceae
100 Pouzolzia mixta
94 Obetia tenax Urticaceae
91 Berchemia zeyheri
100
Berchemia discolor
Rhamnus prinoides
62 100 Ziziphus mucronata
Helinus integrifolius
Rhamnaceae
Ziziphus rivularis
100 Euphorbia rowlandii
100 Euphorbia cooperi
82
100
Synadenium cupulare
84
Euphorbia tirucalli
Euphorbia espinosa
Spirostachys africana
Alchornea laxiflora
Acalypha glabrata
63
Ricinus communis
Croton pseudopulchellus
Euphorbiaceae
54 Croton menyharti
100 Croton madandensis
Croton steenkampianus
99 Croton megalobotrys
Croton gratissimus
Croton sylvaticus
a c eaeaceae
Suregada africana
si alan
Cluhrysob
Clutia pulchella
Garcinia livingstonei
Parinari curatellifolia C
100 Erythroxylum emarginatum
Erythroxylum delagoense Erythroxylaceae
97 Triaspis hypericoides
Acridocarpus natalitius Malpighiaceae
Hugonia orientalis Linaceae
Phyllanthus reticulatus
84 Phyllanthus pinnatus
Margaritaria discoidea
76 Flueggea virosa
94
78 Bridelia mollis Phyllantaceae
93
Bridelia cathartica
Bridelia micrantha
Pseudolachnostylis maprouneifolia
69 Hymenocardia ulmoides
Antidesma venosum
97
Androstachys johnsonii
Ochna natalitia
Picrodendraceae
99
Ochna inermis Ochnaceae
Ochna pulchra
91 Drypetes reticulata
Drypetes gerrardii Putranjivaceae
Trimeria grandifolia
Scolopia zeyheri
Oncoba spinosa
87
85 Flacourtia indica
Homalium dentatum
Salicaceae
Dovyalis caffra
Salix mucronata
73 Paropsia braunii
Adenia spinosa Passifloraceae
91 Xylotheca kraussiana
[16 tips]
Kiggelaria africana Achariaceae
[2 tips]
[115 tips]
[5 tips]
[3 tips]
[133 tips]
[3 tips]
[3 tips]
[10 tips]
[9 tips]
[1 tip]
38
[94 tips]
[52 tips]
Putterlickia verrucosa
Gymnosporia species C
Gymnosporia senegalansis
76 Gymnosporia putterlickioides
Gymnosporia pubescens
Gymnosporia oxycarpa
60 Gymnosporia maranguensis
Gymnosporia heterophylla Celastraceae
96 Maytenus undata
99 Catha edulis
Mystroxylon aethiopicum
87 Pristimera indica
100 96
68
Loeseneriella crenata
Pristimera longipetiolata
Salacia kraussii
Elaeodendron transvaalense
100 Balanites pedicillaris
Balanites maughamii Balanitaceae
60 Searsia pyroides
81 Searsia chirendensis
Searsia transvaalensis
98 Searsia leptodictya
Searsia pentheri
Searsia gueinzii
100 Searsia magalismontana
100
Ozoroa sphaerocarpa Anacardiaceae
Ozoroa obovata
Ozoroa englerii
95 Sclerocarya birrea
Lannea schweinfuthii
100 Harpephyllum caffrum
96 Lannea edulis
Lannea discolor
73 Commiphora pyracanthoides
53 Commiphora glandulosa
Commiphora africana
53
Commiphora schimperi
52 61
Commiphora mollis Burseraceae
Commiphora edulis
100 Commiphora neglecta
Commiphora harveyi
Commiphora marlothii
100 Kirkia wilmsii Kirkiaceae
Kirkia acuminata
63 Vepris reflexa
82 Teclea pilosa
Vepris lanceolata
66
Toddaliopsis bremekampii
54 Zanthoxylum leprieurii
93 93 Zanthoxylum capense
66 67
Zanthoxylum humile Rutaceae
86 Calodendrum capense
Clausena anisata
Ptaeroxylon obliquum
96 Turraea nilotica
56 100 Turraea floribunda
100 Turraea obtusifolia
97 Trichilia emetica Meliaceae
Trichilia dregeana
61 98 Ekebergia pterophylla
Ekebergia capensis
Entandophragma caudatum
99 Stadmannia oppositifolia
59 Pappea capensis
84
99 Deinbollia xanthocarpa
Deinbollia oblongifolia Sapindaceae
86 55 Allophylus decipiens
Allophylus africanus
Hippobromus pauciflorus
[39 tips]
[24 tips]
[1 tip]
[5 tips]
[3 tips]
[133 tips]
[3 tips]
[3 tips]
[10 tips]
[9 tips]
[1 tip]
39
[164 tips]
[51 tips]
Grewia monticola
99 Grewia inaequilatera
88 Grewia hexamita
Grewia bicolor
97 Grewia sulcata
92 Grewia gracillima
64 61 Grewia flavescens
Grewia villosa
87 98 Grewia microthyrsa
'Grewia caffra
Triumfetta pilosa Malvaceae
Hibiscus micranthus
94
Hibiscus calyphyllus
68 84 Gossypium herbaceum
Azanza garckeana
Abutilon angulatum
Adansonia digitata
99 Sterculia rogersii
Sterculia murex
100 Dombeya rotundifolia
Dombeya cymosa
97 Maerua rosmarinoides
Maerua juncea cristata
Thilachium africanum
Maerua parvifolia
Maerua caffra
Maerua angolensis
87 Maerua decumbens
71 Boscia mossambicensis Capparaceae
84 98
Boscia foetida
'Boscia angustifolia
99 Boscia albitrunca
Cadaba termitaria
92 Capparis tomentosa
98 Capparis sepiaria glabrata
99
Capparis fascicularis
100 Salvadora persica
100 Salvadora australis Salvadoraceae
Azima tetracantha
62 Combretum woodii
66 Combretum erythrophyllum
65 Combretum kraussii
75
99 Combretum zeyheri
'Combretum mkuzense
98 Combretum molle
Combretum apiculatum
100 Combretum collinum
82 Combretum celastroides
81 80
Combretum hereroense Combretaceae
Combretum imberbe
96
Terminalia prunioides
100 Combretum mossambicense
Combretum microphyllum
89 Terminalia phanerophlebia
99 Pteleopsis myrtifolia
99
Terminalia sericea
'Combretum padoides
96 Syzygium guineense
91 86 Syzygium cordatum
94
Eugenia natalitia Myrtaceae
Heteropyxis natalensis
68 Ludwigia octovalvis Onagraceae
Galpinia transvaalica Lythraceae
Bersama lucens Methianthaceae
100 Rhoicissus tridentata
Rhoicissus tomentosus
100 Rhoicissus revoilii Vitaceae
100 Cissus cornifolia
Cissus cactiformis
100 Ximenia caffra
58 Ximenia americana Olacaceae
Olax dissitiflora
[133 tips]
[3 tips]
[3 tips]
[10 tips]
[9 tips]
[1 tip]
40
[287 tips]
63 Pavetta edentula
100 Pavetta catophylla
Pavetta schumanianna
88 Pavetta lanceolata
84 Tarenna zygoon
51 Tarenna supra axillaris
Leptactina delagoensis
100 Plectroniella armata
Catunaregam speciosa
Hyperacanthus amoneus
Rothmannia fischeri
93 Gardenia volkensii
98 89 Gardenia resiniflua
Coddia rudis
54 Kraussia floribunda
100 Tricalysia lanceolata Rubiaceae
Tricalysia junodii
Crossopteryx febrifuga
98 Vangueria madagascariensis
99
Vangueria infausta
99
Lagynias dryadum
100 100 Canthium inerme
77 Pyrostria hystrix
83 Canthium setiflorum
97 Psydrax locuples
Heinsia crinita
96 Cephalanthus natalensis
100 Breonadia salicina
Hymenodictyon parvifolium
96 Strophanthus petersianus
64 Strophanthus kombe
86
97 Adenium swazicum
Adenium multiflorum
96 80 Pachypodium saundersii
Holarrhena pubescens
Wrightia natalensis
100 Acokanthera rotundata
Acokanthera oppositifolia Apocynaceae
94 Carissa bispinosa
Carissa tetramera
Carissa edulis
Diplorhynchus condylocarpon
Landolphia kirkii
95 72 Tabernaemontana ventricosa
Tabernaemontana elegans
Rauvolfia caffra
84 88 Strychnos pungens
Strychnos madagascariensis
Strychnos decussata
80
68
100
Strychnos potatorum Loganiaceae
Strychnos spinosa
Strychnos usambarensis
Anthocleista grandiflora Gentianaceae
65
Cordia ovalis
Cordia grandicalyx
100 Cordia caffra
100
80 Cordia sinensis Boraginaceae
Cordia monoica
100 Ehretia rigida
Ehretia amonea
[43 tips]
[1 tip]
[1 tip]
[9 tips]
[19 tips]
[3 tips]
[3 tips]
[10 tips]
[9 tips]
[1 tip]
41
[287 tips]
[60 tips]
100
Vitex patula
Vitex harveyana
Vitex ferruginea
100 Tetradenia riparia
Pychnostachys reticulata Lamiaceae
87
Leonotis nepetifolia
Tinnea rhodesiana
Premna mooiensis
67 Karomia speciosa
Clerodendrum glabrum
86 Duvernoia adhatodoides
Duvernoia aconitiflora
80
100
Anisotes formosissimus
Anisotes rogersii
100 Metarungia longistrobus Acanthaceae
100
100 Ruttya ovata
Ruspolia hypocrateriformis
100 Barleria rotundifolia
Barleria albostellata
Sesamothamnus lugardii Pedaliaceae
90 Markhamia zanzibarica
70 Kigelia africana
63 52
Rhigozum zambesiacum Bignoniaceae
Tecomaria capensis
52 Lippia javanica
100 Lantana rugosa
99 75
Lantana camara Verbenaceae
Duranta erecta
80 Nuxia opposifolia
100 Nuxia congesta Stilbaceae
68
99
Nuxia floribunda
Halleria lucida
99 Chionanthus peglerae
Chionanthus foveolatus
84
Olea europaea africana
98 Schrebera alata Oleaceae
73
100 Jasminum stenolobum
100 Jasminum multipartitum
Jasminum fluminense
100
Solanum panduriforme
100
Solanum lichensteinii Solanaceae
Solanum catombelense
Nicotiana glauca
Cassinopsis ilicifolia
Apodytes dimidiata Icacinaceae
100 Steganotaenia araliacea Apiaceae
78 Heteromorpha arborescens
99 100 Cussonia spicata Araliaceae
Cussonia natalensis
88 Pittosporum viridiflorum Pittosporaceae
81 Vernonia colorata
100 Vernonia aurantiaca
73 Brachylaena transvaalensis Asteraceae
Brachylaena huillensis
63
64 Euclea schimperi
Euclea daphnoides
96
87 Euclea natalensis
Diospyros galpinii
Euclea undulata
80 Euclea divinorum
66
Diospyros whyteana Ebenaceae
100 92
Diospyros lycoides
Diospyros dichrophylla
Diospyros villosa
96 Diospyros natalensis
Diospyros mespiliformis
98
82
Manilkara sp.
87
Manilkara mochisia
54
Manilkara concolor Sapotaceae
100
Mimusops zeyheri
52
Sideroxylon inerme
Englerophytum magalismontanum
Maesa lanceolata Primulaceae
[3 tips]
[3 tips]
[10 tips]
[9 tips]
[1 tip]
42
[420 tips]
Plumbago zeylanica
100
Plumbaginaceae
100 Plumbago auriculata
Portulacaria afra Portulacaceae

Faurea saligna
100
Proteaceae
Faurea rochetiana
Clematis brachiata Ranunculaceae

Uvaria gracilipes
99
83 Hexalobus monopetalus
76
Monodora junodii junodii
80
Uvaria lucida Annonaceae

99
92
Monanthotaxis caffra
100 Annona senegalensis
Xylopia parviflora
98
Artabotrys brachypetalus
59
Gyrocarpus americanus Hernandiaceae
Warburgia salutaris Canellaceae
Hyphaene petersiana
98
89 Hyphaene coriacea
Arecaceae
96 Borassus aethiopium
Phoenix reclinata
Xerophyta retinervis Velloziaceae
90 Aloe spicata
88
Aloe marlothii
61 Dracaena aletriformis Asphodelaceae
Aloe excelsa
Amborella trichopoda Amborellaceae
43
Figure 3 The maximum parsimony majority rule consensus phylogeny of trees and
shrubs occurring in the KNP. Names of species and families follow APG III (2009).
Amborella trichopoda (Amborellaceae) is used as outgroup. Dashed red lines
indicate tip labels for which font has been reduced to fit in the tip label column. Black
dashed line indicates the name of the family Clusiaceae written obliquely also for
fitness purpose. Red branch indicates the family Polygalaceae that has been
embedded within Fabaceae.
Figure 4 Summary tree of the maximum parsimony majority-rule consensus analysis
of trees and shrubs occurring in the KNP. Names of the orders and families follow
APG III (2009), but names of the clades [Monocotyledonae, Magnoliidae,
44
Campanulidae, Lamidae, Malvidae, and Fabidae] follow Soltis et al. (2011). Numbers
above branches are bootstrap values for MP analysis and values below branches
are bootstrap values for ML analysis.
4. Discussion
I compared the topology of the DNA-barcode tree to the latest APG tree (APG III
2009). Results of comparative analysis are presented in Figure 5. The KNP-barcode
tree presented in this Figure is fully resolved, and shows a high congruence in
topology with the APG-tree (APG III 2009). However, there is an important difference
between the two topologies namely the early divergent clades in APG-tree are
sequentially Magnoliids (Magnoliidae) and Monocots (Monocotyledoneae) while in
KNP-barcode tree they appear to be Monocots and Magnoliids. I argue that this is
likely due to a very limited sampling of members of early-divergent clades (only 19
species in this study), compared to a comprehensive sampling in APG III (APG III
2009).
45
Figure 5 Comparison of the phylogenetic tree of Angiosperm of the KNP (referred to
as KNP-Barcode tree) with the overall phylogeny of Angiosperm (APG III 2009).
APG III phylogeny has been pruned to include only orders occurring in the KNP. The
KNP-Barcode tree results from the ML analysis, and values indicated on the
branches are bootstrap values.
I also compared the bootstrap values of MP and ML trees (this study) with
those of Soltis et al. (2011). Results are presented in Table 2. Soltis et al. (2011)
used ML to reconstruct the phylogeny of Angiosperm based on 17-genes (including
nuclear, plastid and mitochondrial genes) and using a broad taxonomic coverage:
640 species, 640 genera, 330 families and 58 of the 59 orders identified for
Angiosperms (sensu APG III 2009). Their study provides the most resolved
Angiosperm phylogeny ever produced. Clades (as identified in this study) are highly
46
supported (BP > 97) and all subclades (as identified in this study) have BP = 100
except Icacinaceae, which was not supported (BP < 50; Table 2). In this study,
clades and subclades received less support compared to Soltis et al. (2011). This is
likely due to differences in sample size (445 taxa vs. 640 taxa) and number of genes
used (2 genes vs. 17 genes).
Furthermore, there are differences in BP values between MP and ML analysis
(Table 2; Figure 4). In ML analysis, only two clades: Malvidae (BP = 63) and
Lamiidae (BP = 73) received low support; all other clades are highly supported (BP >
88). In MP analysis, two clades are not supported (BP < 50): Fabidae and Malvidae;
and three clades received low support: Santalales (BP = 58), Lamiidae (BP = 65)
and Magnoliidae (BP = 59). Supports for subclades are generally higher in ML
analysis than in MP (Table 2).
Table 2 Comparison of bootstrap values ( ) of major sub-(clades) in this study with
those of Soltis et al. (2011). “-” indicates clades identified in this study but not found
in Soltis et al. (2011)
Clades This study Soltis et al. Subclades This study Soltis et al.
(2011) (2011)
MP ML ML tree MP ML ML tree
tree tree tree tree
Fabales 51 72 100
Fagales < 50 < 50 100
Rosales 94 100 100
FABIDAE < 50 97 99 Malpighiales < 50 94 100
Celastrales 100 < 50 100
Zygophyllales 100 < 50 100
Sapindales 93 78 100
Malvales 94 100 100
47
MALVIDAE < 50 63 97 Brassicales 99 100 100
Myrtales 91 < 50 100
Geraniales < 50 < 50 68
VITALES 100 < 50 100 Vitales 100 < 50 100
SANTALALES 58 95 100 Santalales 58 95 100
LAMIIDAE 65 73 100 Gentianales < 50 100 100
Boraginaceae 100 100 100
Lamiales 99 100 100
Solanales 100 < 50 100
Icacinaceae < 50 < 50 < 50
Apiales 99 100 100
CAMPANULIDAE 65 73 100 Asterales 100 100 100
ERICALES 98 100 100 Ericales 98 100 100
CARYOPHYLLALES 100 100 100 Caryophyllales 100 100 100
BASAL EUDICOTS < 50 <50 - Proteales 100 < 50 100
Ranunculales < 50 < 50 100
Magnoliales 100 100 100
MAGNOLIIDAE 59 88 100 Laurales < 50 < 50 100
Canellales < 50 < 50 100
Arecales 96 100 100
MONOCOTYLEDONEAE < 50 100 100 Pandanales < 50 < 50 100
Asparagales 61 99 100
Finally, I investigated the relationships within and between major clades
recovered. Eleven clades and 30 subclades have been identified and are described
below.
4.1. Clade 1: Fabidae
Fabidae is represented in the KNP by six subclades: Fabales, Fagales, Rosales,
Malpighiales, Celastrales, and Zygophyllales (Table 2, Figure 4). Fabidae is a well-
48
supported clade, receiving a support of BP = 97 in ML analysis, and 99 BP in Soltis
et al. (2011). Zygophyllales (MP tree, BP = 100) are sister to [Celastrales +
Malpighiales] but with no support in MP analysis (BP < 50) and low support in ML
analysis (BP = 63) (Figure 4). Members of Fabales, Fagales, and Rosales are all
nitrogen-fixing plants, and group together on the tree as expected (Figures 2 & 3).
Within this nitrogen-fixing group, Fabales are sister to Fagales (no support), and both
are sisters to Rosales (moderate support in ML tree, BP = 77).
In ML analysis, Bauhinia galpinii appears is sister (although no support, Figure
3) to the rest of Fabaceae, further confirming that the genus Bauhinia may be the
early-divergent Fabaceae (Doyle et al. 2000). However in MP analysis, Bauhinia
galpinii is sister to subclade Fabales which include Fabaceae and Polygalaceae
(with poor support, BP = 51).
Subclade Celastrales is recovered in MP and ML trees, but is only supported
in MP analysis (MP tree, BP = 100). It is represented in the KNP by only one family
i.e. Celastraceae, which includes nine genera: Catha, Gymnosporia, Putterlickia,
Elaeodendron, Loeseneriella, Pristimera, Maytenus, Mystroxylon, and Salacia.
Cronquist (1981) excluded the genus Salacia from Celastrales, but in the current
study, Salacia is found embedded within Celastrales, as currently accepted in
modern Angiosperm classification (e.g. Savolainen et al. 1997; APG III 2009; Soltis
et al. 2011). Celastrales is moderately supported as sister to Malpighiales (ML
analysis, BP = 79).
Malpighiales is recovered with high support in ML analysis (ML tree, BP = 94),
and represented by 13 families in KNP: Linaceae, Phyllanthaceae, Ochnaceae,
Picrodendraceae, Achariaceae, Putranjivaceae, Salicaceae, Passifloraceae,
49
Malpighiaceae, Erythroxylaceae, Chrysobalanaceae, Clusiaceae, and
Euphorbiaceae.
The family Linaceae comprises two subfamilies, Linoideae and Hugonioideae.
A recent study showed that this family is monophyletic (McDill et al. 2009). It is
represented by only one species in the KNP (Hugonia orientalis), and therefore the
monophyly of the family cannot be discussed here. Chase et al. (2002) pointed out a
weak relationship between Linaceae and Picrodendraceae, but this is not recovered
in this study. Linaceae is rather sister to [Malpighiaceae + Erythroxylaceae] in MP
analysis, but to [Malpighiaceae + Ochnaceae] in ML analysis, with no support in both
analyses (Figures 2 & 3).
Members of the family Putranjivaceae have been included either in
Euphorbiaceae (Webster 1994) or in Brassicales (Rodman et al. 1997, 1998). In this
study, Putranjivaceae is not sister to either Euphorbiaceae or Brassicales (see also
APG III 2009), but group as sister to Clusiaceae.
In MP analysis, Garcinia livingstonei (Clusiaceae) is “unexpectedly” embedded
within Euphorbiaceae. This may be due to the fact that only rbcLa (that includes high
number of uninformative sites; Table 1) was sequenced for this species. However in
ML tree, Clusiaceae is clearly outside Euphorbiaceae, and appears sister to
Putranjivaceae (although with no support).
4.2. Clade 2: Malvidae
Malvidae, is poorly supported in this study (ML tree, BP = 63; Table 2; Figure 4), but
highly supported (BP = 97) in Soltis et al. (2011). It includes five subclades:
Sapindales, Malvales, Brassicales, Myrtales, and Geraniales. Malvidae is sister to a
well supported (ML tree, BP = 97) Fabidae with moderate support (ML tree, BP =
50
72). This sister relationships between Malvidae and Fabidae was also recovered in
previous studies, but with stronger support (BP = 100, Soltis et al. 2011).
In a recent study, Myrtales were found sister to Geraniales with moderate
support (BP = 79), and [Myrtales + Geraniales] was recovered as sister to the
remaining Malvidae (Soltis et al. 2011). In this study, this topology is not recovered.
Instead, I found that in both MP and ML analyses, Geraniales (represented in this
study by only one species, Bersama lucens) is sister to the rest of the clade (ML
tree, BP = 50). In addition, I also found that Myrtales (MP tree, BP = 91) is sister to a
highly supported group of [Sapindales + (Brassicales + Malvales)] (ML tree, BP =
100). The divergent results between this study and that of Soltis et al. (2011)
regarding relationships within Malvidae are more likely due to both a limited taxon
sampling and genes used in this analysis (445 taxa, 2 genes) compared to Soltis et
al.’s (2011) analysis (640 taxa, 17 genes).
Sapindales (MP tree, BP = 93) is sister to [Brassicales + Malvales]. This
relationship is similar to recent topology resulting from analyses focusing on Rosidae
(Wang et al. 2009). Brassicales (> 18 families) is represented in the KNP by only two
families, Capparaceae (ML tree, BP = 100) and Salvadoraceae (BP = 100 for both
MP and ML trees), showing a strong sister-relationship (ML tree, BP =100).
Salvadoraceae is not included in Soltis et al. (2011). Within Sapindales,
Sapindaceae (ML tree, BP = 97) is sister to [Meliaceae (ML tree, BP = 97) +
Rutaceae (ML tree, BP = 99)]. In MP analysis, Kirkiaceae (BP = 100) is sister to a
moderately supported (BP = 73) group of [Burseraceae (BP = 100) + Anacardiaceae
(BP < 50)], but this sister-relationship is poorly supported. However, in ML analysis,
Burseraceae (BP = 100) are embedded within Anacardiaceae. The relationships
51
within Sapindales showed in MP analysis largely agree with other analyses (e.g.
Gadek et al. 1996; Muellner et al. 2007; Soltis et al. 2011).
In MP analysis, Myrtales (BP = 91) comprises two major groups: [Onagraceae
(BP < 50) + Lythraceae (BP < 50)] and [Myrtaceae (BP = 94) + Combretaceae (BP =
100)]. The topology recovered in ML analysis is slightly different from that of MP.
Although the sister-relationship between Onagraceae and Lythraceae is also found,
Myrtaceae (BP = 100) is not found sister to Combretaceae (BP = 100). The strong
support found in this study for the placement of Combretaceae is not recovered in
previous studies (BP < 50 in Soltis et al. 2011; but see Maurin et al. 2010).
4.3. Clade 3: Vitales
This clade is highly supported in both analyses: MP tree (BP = 100) and ML (BP =
100). It is represented in the KNP by only one family, Vitaceae with two genera
(Rhoicissus and Cissus). Two subclades can be defined, one including members of
the genus Rhoicissus and the other including members of the genus Cissus. Vitales
+ [Malvidae + Fabidae] represent the super-clade Rosidae (Figure 4; Soltis et al.
2011) in the KNP. Vitales was included in Rosidae (Savolainen et al. 2000; Soltis et
al. 2011), and this placement is also recovered in this study.
4.4. Clade 4: Santalales
Santalales is represented in the KNP by one family, Olacaceae (ML tree, BP = 95)
with three species: Olax dissitiflora, sister to [Ximenia caffra + Ximenia americana].
Santalales was recovered as sister to Asteridae (Soltis et al. 2000; Hilu et al. 2003)
with no support. Soltis et al. (2011) included Santalales in their ‘Super-asteridae’
(Soltis et al. 2011), which is in agreement with previous studies (e.g. Soltis et al.
52
2000; Hilu et al. 2003). In ML analysis, Santalales is sister to Caryophyllales (no
support); both orders are included in Super-asteridae in Soltis et al. (2011).
Meanwhile, the MP analysis grouped Santalales sister to Rosidae (no support, BP <
50).
4.5. Clade 5: Lamiidae
This clade is not well supported (MP tree, BP = 73; ML tree, BP = 65) in this study,
unlike in Soltis et al. (2011) where Lamiidae was highly supported (BP = 100).
Lamiidae is represented in the KNP by three orders (Gentianales, Lamiales and
Solanales) and one unplaced family (Boraginaceae) in APG III system.
Within Gentianales (ML tree, BP = 100), Gentianaceae (represented in the
KNP by only Anthocleista grandiflora) is sister to two groups: Rubiaceae (ML tree,
BP = 100) and [Loganiaceae (ML tree, BP = 100) + Apocynaceae (ML tree, BP =
100)]. The sister-grouping of Loganiaceae and Apocynaceae is well supported (BP =
91). The same topology was recovered from MP analysis with similar support.
Similar topology within Gentianales is confirmed by Bremer (1996), Backlund et al.
(2000), Potgieter et al. (2000) and Frasier (2009). However, the sister-relationship
found between Apocynaceae and Gentianaceae in Soltis et al. (2011) is not
recovered in this study. The reason could be due to very limited sampling of
members of Gentianaceae, which is represented in this study by only one species,
Anthocleista grandiflora.
In the KNP, members of Lamiales belong to six well supported families in ML
analysis: Lamiaceae (BP = 100), Acanthaceae (BP = 100), Bignoniaceae (BP = 72),
Verbenaceae (BP = 91), Stilbaceae (BP = 88), Oleaceae (BP = 100), and one
unsupported Pedaliaceae (BP < 50) (represented by only one species). Within
53
Lamiales, Oleaceae is sister to the remaining (BP = 100) and Lamiaceae is sister to
Acanthaceae (with no support). The same topology with similar support was
recovered from the MP analysis.
Solanales, a well supported group (in MP tree only, BP = 100), is represented
in this study by one family, Solanaceae with two genera, Solanum and Nicotiana.
Boraginaceae (BP = 100 in all analyses), an unplaced family in APG system,
comprise two genera, Cordia and Ehretia.
The relationships within Lamiidae vary in literature (e.g. APG III 2009 and
Soltis et al. 2011). In APG III (2009), the relationships are unresolved, but Soltis et
al. (2011) provide a resolved topology within the clade. In this latter study, there is a
sister-relationship between [Lamiales (BP = 100) + Boraginaceae (BP =100)] and
[Solanales (BP = 100) + Gentianales (BP = 99)] (Soltis et al. 2011). In the current
study, the topology observed also varies depending on the methods used. Based on
MP analysis, Icacinaceae is sister to the rest of the clade (BP < 50) and [Solanales
(BP = 100) + Lamiales (BP = 99)] are sister to [Gentianales (BP < 50) +
Boraginaceae (BP =100)]. None of the sister-groupings within Lamiidae in this study,
as well as in previous studies, is well supported. In addition, in MP analysis,
Gentianales is sister to Boraginaceae and Lamiales is sister to Solanales. In ML
analysis, the topology is different. Gentianales is sister to Boraginaceae + [Solanales
+ Lamiales] indicating that the sister-relationship between Gentianales (BP = 100)
and Boraginaceae (BP = 100) is not recovered.
The placement of Icacinaceae is still a debatable question. It was included in
Celastrales by Cronquist (1981, 1988), in Theales by Thorne (1983), and in Cornales
by Dahlgren (1983) and Thorne (1992). In this study, Icacinaceae is embedded
within Lamiidae. The placement of Icacinaceae within Lamiidae is not only confirmed
54
by other molecular studies (Savolainen et al. 1997; Kårehed 2003; Soltis et al. 2011)
but their unitegmic ovules and connate petals also support this placement (APG III
2009). In APG III system, the placement of Apodytes and Cassinopsis, the two
representatives of the family Icacinaceae in the KNP, is unresolved.
4.6. Clade 6: Campanulidae
Representatives of Campanulidae grouped with strong support (ML analysis, BP =
100), and comprise two lineages: Apiales (ML tree, BP = 100) and Asterales (ML and
MP tree, BP = 100). This sister-grouping is well supported (ML tree, BP = 100).
Asterales is represented by the family Asteraceae including two genera, Vernonia
and Brachylaena. Apiales comprise three families with Pittosporaceae (represented
in the KNP by one species, Pittosporum viridiflorum) being sister to [Apiaceae (ML
tree, BP = 100) + Araliaceae (ML tree, BP = 100)]. The sistership between Apiaceae
and Araliaceae is well supported in ML analysis (BP = 98) but less supported in MP
(BP = 78).
4.7. Clade 7: Ericales
A well supported Ericales (ML tree, BP = 100) is recovered in all analyses as sister
to [Lamiidae + Campanulidae]. This sister-grouping is well supported only in ML
analysis (BP = 100). A similar topology was also found in Soltis et al. (2011). Three
families represent this clade in the KNP: Ebenaceae (MP and ML trees, BP = 100)
sister to [Primulaceae + Sapotaceae]. Primulaceae (only one species, Maesa
lanceolata) is sister to a well supported Sapotaceae (BP = 100), but this sister-
grouping is poorly supported in all analyses (MP tree, BP = 52; ML tree, BP = 62).
Ericales + [Campanulidae + Lamiidae] represent the super-clade Asteridae (Figure
55
4) as defined in Soltis et al. (2011). Asteridae is sister to [Santalales + Rosidae] (with
no support) with which they constitute the Core Eudicots in the KNP (Figure 4).
4.8. Clade 8: Caryophyllales
Caryophyllales is represented by Plumbaginaceae (BP = 100 in all analyses) sister
to Portulacaceae (BP = 100). The placement of Caryophyllales has been debated in
Soltis et al. (1997) who showed this clade nested (BP < 50) within Asteridae and in
Soltis & Soltis (1997) who placed the order within Rosidae while recently Hilu et al.
(2003) placed it as sister to Asteridae. Based on MP analysis in this study,
Caryophyllales is recovered as sister (no support, BP < 50) to the rest of Core
Eudicots, while in ML analysis, it is sister to Santalales (with no support, BP < 50).
The ML topology found in this study is similar to that of Soltis et al. (2011). However
the placement in APG III (2009) is similar to that of Hilu et al. (2003) i.e. sister to
Asteridae. The limited sampling in this study combined with the limited genes used
could explain the difference in placement between this study and that of Soltis et al.
(2011).
4.9. Clade 9: Basal Eudicots
Basal Eudicots are represented in this study by Proteales (MP tree, BP = 100) and
Ranunculales (no support in both analyses). Proteales is represented by the family
Proteaceae (MP tree, BP = 100) and Ranunculales by Ranunculaceae (one species
only, Clematis brachiata). Both lineages are sister in MP tree (Figure 4), but this
topology is found neither in ML analysis (Figure 5) nor in APG III (2009) and Soltis et
al. (2011). However the ML analysis in this study (KNP-Barcode tree, Figure 5) as
56
well as APG III (2009) and Soltis et al. (2011) recover Ranunculales as the early-
divergent clade of the Eudicots.
4.10. Clade 10: Magnoliidae
The Magnoliidae or Magnoliids is not extensively represented in the KNP. In MP and
ML analyses, I found the same topology for this clade. Magnoliales (BP = 100 in all
analyses) is sister to Laurales (poor support, ML tree, BP = 57). This sister-
relationship between Magnoliales and Laurales was also observed in previous
analyses (e.g. Zanis et al. 2002; Hilu et al. 2003; Moore et al. 2010; Soltis et al.
2011). I also found Canellales sister to [Magnoliales + Laurales] with high support
(ML tree, BP = 88) but no support in MP analysis (BP < 50).
In Magnoliales, one strongly supported family (i.e. Annonaceae, BP = 100 in
all analyses) including seven species was observed. All other families within
Magnoliidae in the KNP comprise only one species: Laurales (Hernandiaceae,
Gyrocarpus americanus), and Canellales (Canellaceae, Warburgia salutaris).
Previous combined analyses of Graham & Olmstead (2000), Qui et al. (2000)
and Zanis et al. (2002) have excluded Monocotyledoneae (Monocots) from
Magnoliidae whereas Savolainen et al. (2000), Soltis et al. (2000, 2003) have
expanded Magnoliidae to include Monocots. In this study, the phylogeny of the
KNP’s woody plant recovers Magnoliidae excluding Monocotyledonae supporting the
conclusion of Graham & Olmstead (2000), Qui et al. (2000), and Zanis et al. (2002).
4.11. Clade 11: Monocotyledoneae
The Monocotyledoneae or monocot clade is a well supported group (ML tree, BP =
100). It comprises three subclades: Asparagales (ML tree, BP = 99), Arecales (ML
57
tree, BP = 100), and Pandanales (represented by only one species, Xerophyta
retinervis). The relationships within Monocotyledoneae vary with methods of data
analysis. In MP analysis, Asparagales (BP = 61) is sister to [Arecales (BP = 96) +
Pandanales]. However, in ML analysis, Arecales (BP = 100) is sister to [Asparagales
(BP = 99) + Pandanales].
5. Conclusion
This study provides a DNA barcoding database and phylogenetic tree for the
Angiosperm trees and shrubs of the largest subtropical reserve in Africa. This
database is available online on BOLD and at the African Centre for DNA Barcoding,
University of the Johannesburg (South Africa). The topology of the tree assembled in
the current study is in agreement with current knowledge regarding relationships
within Angiosperm. This provides ecologists with a unique phylogenetic tool with
which numerous long-standing conservation questions can be addressed in the
KNP. I anticipate that this well resolved angiosperm tree (ML tree) will be of broad
utility in many areas of biology, including community ecology in savanna biomes,
physiology, and conservation ecology in the KNP.
58
Chapter 3 Brownian motion model is not a suitable model for comparative analysis of
plant traits in the KNP
Chapter 3
Testing suitability of evolutionary models using traits of woody plants in
the KNP
1. Introduction
Phylogenetic comparative analysis (PCA) is a widely used technique in
modern evolutionary biology (Felsenstein 1985a; Freckleton & Harvey 2006;
Ackerly 2009; Jombart et al. 2010; Wiens et al. 2010; Davies et al. 2011;
Schaefer et al. 2011). It has provided new insights into our understanding of
current biological challenges. These challenges include pest management
(Gilbert & Webb 2007), impacts of climate change on biodiversity (Willis et al.
2008, 2010), invasion management (Cadotte et al. 2009; Schaefer et al.
2011), and extinction risk (Davies et al. 2011).
Furthermore, the PCA has also provided several ways of testing
phylogenetic autocorrelation or signal in ecological traits, which is critical, for
example in phylogenetic analysis of community structure (Webb et al. 2002;
Wiens et al. 2010; Krasnov et al. 2011). For instance, demonstrating the
presence of phylogenetic signal may be useful in detecting shifts in correlation
patterns on a phylogeny (Revell & Collar 2009), or specific selective regimes
(Hansen 1997; Butler & King 2004; Hansen et al. 2008). It is also
acknowledged as essential in addressing changes in evolutionary rates
(O’Meara et al. 2006; Ackerly 2009).
Despite the importance of PCA, recent studies have questioned the key
assumption that underlies its application (e.g. Freckleton & Harvey 2006;
59
Ackerly 2009). In particular, these studies assumed that ecological traits
evolve following a Brownian motion (BM) model without prior investigation
(Harvey & Pagel 1991; Hansen 1997; Freckleton et al. 2002), causing
Freckleton & Harvey (2006) to refer to BM as the “conventional model of trait
evolution”. However, this conventional model may be misleading (Freckleton
& Harvey 2006; Ackerly 2009). The BM model corresponds to a model where
trait diverges indefinitely following a random walk (Figure 1A), and where the
likelihood of trait change is unaffected by the state of a trait or by other
species (Felsenstein 1973). As a result, the variance in mean phenotypic
traits of two traits evolving under BM model is expected to increase over time
in an unbounded way (Figure 1A), whilst under selection model [e.g. Ornstein-
Uhlenbeck (OU) model], the variance is expected to grow in a bounded
fashion (Figure 1B; Butler & King 2004; Ackerly 2009).
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Figure 1 Illustration of Brownian motion (BM) model (A) and Ornstein-
Uhlenbeck (OU) model (B) of trait evolution. This illustration results from
analysis of simulations with five replicates.
Figure 1 clearly indicates that if a trait evolving in a OU fashion (e.g. under
natural selection) is analysed assuming a BM model, inferences drawn from
such analyses would be incorrect (Butler & King 2004; Harvey & Rambaut
2000).
The main objective of this study is to test the suitability of BM model
using the ecological data of woody plants in the KNP. The flora of the KNP,
like in several other biodiversity hotspots (e.g. Cape region; Forest et al. 2007;
Davies et al. 2011), is currently receiving great attention from a phylogenetic
perspective. Therefore, providing ecologists with information regarding the
evolutionary model that best-fits plant ecological data in KNP is important.
2. Materials and methods
2.1. Plant ecological traits
Several traits have been identified as strategic for plants due to their
ecological importance (Rosenthal & Kotanen 1994; Wright et al. 2007). For
instance, in African savannas, well known for its rich fauna (see Chapter 1),
plants undergo constant pressures due to herbivory. These pressures include
breaking of branches and trunks, bark stripping, and uprooting, especially
from megaherbivores (e.g. elephants), which can lead to plant death. Dense-
wood plants are better able to resist such herbivores pressures (Turner 2001;
61
Chave et al. 2009). I therefore measured wood density to quantify plant
strength and resistance to pressures.
Growth strategy might also act as a defence trait against
megaherbivory, for example, leaves of taller plants may escape herbivory
(Palo et al. 1993). Taller plants were also shown to better survive herbivory
pressures in tropical African savannas (Field 1971; Guy 1976). Data on plant
maximum height were therefore recorded to represent plant growth strategy.
Leaf-nutrient content or leaf economics might also represent additional
survival strategies. Herbivores preferentially forage for high-quality leaves
containing high nutrient concentration (Grant & Scholes 2006). Plants with low
leaf-nutrient content will therefore be subject to reduced herbivory. Leaf
economics also indicate plant ability to capture, secure and use nutrients
(Wright et al. 2007). As such, plants with high ability to capture nutrients will
be able to store enough resources that could be used later to survive nutrient-
deficit, and meet their physiological, growth and developmental requirements.
Therefore, I measured specific leaf area (leaf area per dry mass) to assess
plant leaf economics (Wright et al. 2004, 2007).
Finally, leaf structure is also key especially for controlling plant
physiology (respiration and transpiration). Also, plants experiencing herbivory
or growing in water-deficit areas develop shorter and narrower leaves
compared to plants free of herbivory pressures or growing in areas where
water is not a limiting factor (Christoph & David 1997). Additionally thicker
leaves may be less palatable (Coley 1983; Cunningham et al. 1999; Wright et
al. 2004). Thus, leaf area and leaf thickness were measured to represent
plant leaf structure and physiology.
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2.2. Data collection and measurements
I collected trait data for 216 species of trees and shrubs in the KNP following
a south-north gradient to include as much intra and interspecific variability as
possible. Four traits were measured: specific leaf area (SLA), leaf area (LA),
leaf thickness (LT) and wood density (WD). Two other traits including
maximum height and spinescence (presence/absence of spines) were
collected from literature.
In the field, leaf samples were sealed in plastic bags and conserved in
a cool box containing ice. In the lab (ACDB, University of Johannesburg),
samples were kept in -4°C until further processing. Prior to the measurement
of leaf area (LA), I scanned 3-12 leaves for each species (representing 1324
leaves scanned in total). These leaves were later oven-dried at 60°C for two
days, and their dry mass was determined. The scanned leaves were used to
determine leaf area using Image-Pro Analyzer 7.0.1.
For other leaf measurements, rehydrated samples were used according
to the standardised protocol described by Garnier et al. (2001). Rehydrated
leaves were immediately weighed to determine the saturated leaf fresh mass
(LFM). I then calculated specific leaf area (SLA) as: SLA = LA/LDM and leaf
dry matter content (LDMC) as LDMC = LDM/LFM where LDM = leaf dry mass
and LFM = leaf fresh mass. Leaf thickness (LT) was calculated as LT = (SLA
x LDMC)-1 following Vile et al. (2005).
To determine wood density (WD), I sampled, from living trees, 3-5 small
pieces of wood per species (764 wood samples in total) and immediately
placed them into plastic-sealed bags on ice, labelled according to the species
voucher. These samples were maintained at constant humidity at -4°C until
63
they were placed into water for 48 hours to ensure adequate swelling. The
volume of fully hydrated samples was measured by the water displacement
method. The same samples were then dried for 2-3 days in a well-ventilated
oven at 80°C until it achieved constant mass. The oven-dry mass was then
measured to calculate the wood density (WD) as: WD = dry mass/hydrated
wood volume.
Maximum plant height and spinescence data were collected from
Schmidt et al. (2007) who conducted intensive fieldwork in the KNP.
2.3. Data analysis
To test the suitability of BM model for the trait data collected, I applied two
analyses. First, I assumed that traits evolve in a BM fashion. I then evaluated
the phylogenetic autocorrelation or phylogenetic signal using two tests:
Pagel’s lambda (Pagel 1999) and Blomberg’s K test (Blomberg et al. 2003).
Pagel’s lambda, calculates a parameter lambda, which is a multiplier of the
off-diagonal elements of the variance/covariance matrix describing tree
topology and branch lengths. Pagel’s test implemented in the R package
Geiger 1.0 (Harmon et al. 2008) transforms the phylogeny in an attempt to
improve the fit of the BM model (Pagel 1999). Values of lambda vary between
0 and 1. A best fit of BM model is indicated by lambda equals 1. Significance
of lambda was assessed using the likelihood ratio test. Blomberg’s K test
implemented in the R package Picante 1.2 (Kembel et al. 2010) evaluates the
phylogenetic signal in a trait against a BM model. If K equals 1, the trait
follows a BM model, but K < 1 is an indication of a non-BM model. Statistical
significance of the K values was evaluated by randomly shuffling traits 1000
times and calculating 95% confidence intervals (ci). Both Lambda and K were
64
calculated from the ML tree (see Chapter 2) with branch lengths transformed
to relative time using penalized likelihood (Sanderson 2002).
To allow comparison of patterns observed under BM-related tests
(lambda and K), I also performed a non-BM test of phylogenetic signal, the
Abouheif’s test (Abouheif 1999) implemented in the R package Adephylo 1.1
(Jombart et al. 2010). Abouheif’s test uses a nonparametric test to detect
signal based on the Moran's index test (Pavoine et al. 2008). This test first
calculates a C-statistic; C = 1-η/2, η as the ratio of the sum of squared
differences between successive observations (i.e. the trait values of
successive taxa on the phylogeny) and sum the squares of each observation.
The mean of the observed C-values is then compared to the mean of
randomised C-values estimated by randomly shuffling the data so that taxa
are randomly placed on the tips of the phylogeny. I used 999 random
permutations to obtain p-values.
In the second analyses, I fitted six commonly used evolutionary models
to the plant ecological traits. These models are lambda, delta, kappa, early-
burst (EB), Ornstein-Uhlenbeck (OU), and Brownian motion (BM). Each model
depicts a different selective regime. The best model was selected using
Akaike Information Criterion (AIC; Burnham & Anderson 2002). The model
with the lowest AIC value is the best model for the data (Burnham & Anderson
2002).
3. Results
Pagel’s lambda and Blomberg’s K values were both lower than 1 for all traits:
(lambda ≤ 0.88; K ≤ 0.05; Table 1), indicating that traits might not evolve in a
65
BM fashion. However, significant signal was detected in all traits (Table 1;
Figure 2)
Table 1 Tests of phylogenetic signal in the studied traits based on Pagel and
Blomberg’s statistics. Significance of lambda values are indicated as follows: *
= p < 0.05; ** = p < 0.01; *** = p < 0.001; Significance of K values are
indicated by confidence intervals ci (see illustrations in Figure 2).
Traits Pagel’s Significanc Blomberg’s K Significance

lambda e (p- values (Confidence
values values) intervals ci) See
also Figure 1
Spines 0.88 < 0.001*** 0.03 ci=0.007-0.012
Wood 0.79 < 0.001*** 0.05 ci=0.005-0.015
density
Leaf 0.70 < 0.001*** 0.03 ci=0.006-0.013
thickness
Leaf area 0.55 < 0.001*** 0.02 ci=0.007-0.013
Specific 0.42 < 0.001*** 0.02 ci=0.007-0.013
leaf area
Maximum 0.30 < 0.001*** 0.02 ci=0.007-0.012
height
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Maximum height Wood density Leaf area
100 200 300 400

200
300
Frequency
Frequency
Frequency
200
100
100
50
0
0
0.006 0.012 0.00 0.02 0.04 0.005 0.015
K values K values K values
Specific leaf area Spines Leaf thickness
200
100 150 200
300
150
Frequency
Frequency
Frequency
200
100
100
50
50
0
0.005 0.015 0.000 0.015 0.030 0.00 0.02 0.04

K values K values K values
Figure 2 Values of Blomberg’s K (dashed red line) for each trait. Histogram
bars represent K-values based on 1000 randomisations. All traits show
significant signal. Dotted lines indicate the 95% confidence interval.
I also applied a non-parametric test (Abouheif test) of phylogenetic
signal. The result was more complex. It supported the presence of significant
phylogenetic autocorrelation in all traits, except in leaf area and specific leaf
area (Table 2; Figure 3).
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Table 2 Test of phylogenetic signal in the studied traits based on Abouheif’s

statistics. Significance of the signal is indicated as follows: * = p < 0.05; ** = p
< 0.01; *** = p < 0.001; NS = non significant. Std = standard deviation; see
text for details about C values.
Traits Observed C Std Observed C p values

Maximum height 0.28 6.32 0.001**
Wood density 0.35 7.54 0.001**
Leaf area 0.004 1.26 0.064NS
Specific leaf area 0.02 0.99 0.091NS
Spinescence 0.36 7.96 0.001**
Leaf thickness 0.12 4.67 0.014*
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Figure 3 Abouheif test of phylogenetic signal in the studied traits. The
histogram indicates the frequency distribution of randomised mean C-
statistics calculated from the trait data along the tips of the phylogeny. The
vertical line with a rectangular black dot indicates the position of the observed
mean C-statistic relative to the null hypothesis sampling distribution.
To further test this finding that BM might not be suitable, I conducted a
model fitting test using the AIC statistic. AIC values for each model are
summarised in Table 3. This test confirmed that BM model was not a suitable
model for any of the traits. However, no single model was able to account for
the evolution of all traits. Instead, two models, lambda and OU were
competing to explain plant trait evolution best. Lambda was best fitted to
maximum height and leaf thickness data whereas the evolution of wood
density, leaf area, specific leaf area, and spinescence was best explained by
OU model. It is important to note that when lambda best fits the evolution of a
trait, OU is the second best model and vice-versa. Early Burst (EB) models
showed the highest AIC value for all traits, indicating that EB was the worst-
fitting model for woody plants.
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Chapter 3 Brownian motion model is not a suitable model for comparative analysis of plant traits in the KNP
Table 3 Models comparison of traits evolution of woody plants using AIC test. Values indicated are the Akaike Information Criterion
AIC. Values in bold are the lowest AIC scores indicating the best model for each trait. Values underlined indicate the second lowest
AIC scores, i.e. the second best model.
Ecological traits
Models Indication of the models Maximum Wood Leaf Specific Spines Leaf
height density area leaf area thickness
Lambda When close relatives are less similar 497.4933 196.5407 803.2391 807.7841 44.50788 785.2892
than expected, it stretches terminal
branches relative to deep branches to fit
Delta When Brownian rate parameter speeds 660.9125 260.6225 1177.385 1150.568 92.6299 1008.862
up or slows down over time
Kappa When change occurs with each 551.6139 215.8766 852.0965 858.6493 47.2106 831.1721
speciation event, but is not proportional
to branch length
Early Burst When there is an initial burst of trait 802.5878 273.2451 2330.057 2248.721 105.8249 1823.565
(EB) diversification but less later
Ornstein- When taxa diverge less on long 513.8413 193.3471 799.2955 795.8571 1.08184 793.0877
Uhlenbeck branches than expected, due to
(OU) stabilising force pulling towards centre
Brownian Trait diverge indefinitely, random walk 800.5878 271.2451 2328.057 2246.721 103.8249 1821.565
motion (BM)
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4. Discussion
Demonstrating phylogenetic conservatism in ecological traits is critical in
comparative analysis (Webb et al. 2002; Wiens et al. 2010; Krasnov et al.
2011). Several tests have been developed to quantify evolutionary
conservatism, but no single test is able to account for all models of
evolutionary processes (Ackerly 2009; Wiens et al. 2010; Krasnov et al.
2011). A weight-of-evidence approach, using a combination of tests, is
therefore best suited to capture information about phylogenetic autocorrelation
of ecological traits where the mode of evolution is unknown and might differ
between traits (Krasnov et al. 2011). Identifying the best model of evolution for
ecological traits is therefore a prerequisite for comparative analysis.
Here I used multiple approaches to test for evolutionary model that best
fits woody plant traits, using the flora of the KNP as a case study. I first tested
for phylogenetic signal in plant traits. In aggregate, the tests indicate that plant
traits demonstrate significant phylogenetic conservatism, but the mixed results
across test statistics suggest that they might not evolve in a BM fashion. A
best fit of BM model is indicated by K = 1 (Blomberg et al. 2003) and lambda =
1 (Pagel 1999). For all traits, I observed K << 1, and lambda < 1, results
consistent with a non-BM model.
To further test this finding, I used the AIC statistic to compare six
commonly used models of character evolution. AIC test also supported the
previous finding in that BM model was not the best model for any of the traits.
In addition, no single model was able to account for evolution of all traits,
providing support to the mixed results of signal tests. Importantly, I found OU
model to be the best model for wood density, leaf area, specific leaf area, and
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spinescence whereas lambda might be a suitable model for plant height and
leaf thickness.
However, lambda model transforms the phylogeny in an attempt to
force the fit of the BM model to the data (Hansen 1997; Pagel 1997;
Freckleton et al. 2002). As a result of phylogeny transformation, phylogenetic
branch lengths or interspecific distances are modified (Grafen 1989; Gittleman
& Kot 1990; Pagel 1997). Two major critics are raised against the fit of
lambda, which is actually an allied model to BM. First, by transforming trees
onto a scale that yield a best fit of BM, comparative methods such as Pagel’s
lambda allow distortion of the phylogeny, making it difficult to infer information
about the most likely evolutionary process (Freckleton & Harvey 2006).
Second, such methods ignore all ecological processes occurring during
evolution (Pagel 1997; Butler & King 2004). Given such limitations, applying
lambda to the data of height and leaf thickness in comparative studies of
woody plants in the KNP might be misleading. I therefore suggest the use of
the OU model, which is the second best model after lambda for these traits.
The very low values of K found for all traits are consistent with deviations from
BM model, likely indicative of underlying ecological mechanisms (e.g.
stabilising selection forces).
The best fit of OU model found for other traits provides evidence
consistent with this expectation, i.e. ecological or physiological constrains
might cause taxa to diverge less on long branches than expected under a BM
model (Garland et al. 1993; Hansen & Martins 1996).
Crucially, the non-fit of BM model revealed by all tests (K, lambda and
AIC tests) could be driven by two major factors (Silvertown et al. 2006; Revell
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et al. 2008). The first factor may be linked to adaptive evolution (e.g. adaptive
radiation) in which case a niche-filling model is more appropriate (Freckleton
& Harvey 2006). The second factor that can account for non-BM model could
be linked to a ‘bounded’ random walk driven by ecological and plant
physiological constrains (Ackerly 2009). It is expected that both scenarios
(adaptive radiation and presence of constrains) could act as stabilising forces
leading to a pattern incompatible with BM model (Butler & King 2004;
Freckleton & Harvey 2006).
Tropical African savannas are characterised by various stressful
pressures (e.g. herbivory, water or nutrient deficit, global change etc.) which
operate in combination to drive savanna composition (Biaou 2009). As a
result, only species that are tolerant to pressures (i.e. with specific traits) are
able to survive in this disturbed environment (Westoby et al. 2002; Walther et
al. 2005; Lavergne et al. 2006). Furthermore plant survival also required shifts
in traits as adaptive response to environmental conditions. The filtering or
selection of traits, and the plant adaptive responses could cause significant
departure of trait from BM model (Freckleton & Harvey 2006). As such, the
application of statistical comparative methods that assume BM model to study
woody plant traits in the KNP could be severely compromised.
However, a question can be raised: why did I find significant signal
when applying tests that assume BM model although traits do not clearly
evolve in a BM fashion? Metrics of phylogenetic signal are excellent measures
of the overall evolutionary pattern of a trait, but can be driven by only a
specific conserved clade on the phylogeny (Ackerly 2009). For instance, the
signal observed could be driven by the most species-rich family alone (here
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Fabaceae, see phylogeny in Chapter 2). It could also indicate that the traits
are highly affected by environmental pressures (biotic and abiotic) leading to a
convergent evolution (Blomberg et al. 2003). Another possible reason is that
forcing the fit of BM by transforming the phylogeny (e.g. lambda model), could
finally lead to a significant signal.
5. Conclusion
Phylogenetic comparative methods are used extensively to investigate
phylogenetic signal in traits or to correct for statistical non-independence
amongst species that arises as a consequence of common ancestry. The
application of these methods requires a specification of a null model
traditionally defined as BM model. OU model instead of BM model is more
suitable for woody plant traits occurring in the KNP. The assumption of BM
should not be used without prior test, especially for traits for which the model
of evolution is unknown.
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Chapter 4 Characterising diversity and phylogenetic structure of woody plant communities in
the KNP, South Africa
Chapter 4
Characterising diversity and phylogenetic structure of woody plant
communities in the KNP, South Africa
1. Introduction
How do species assemble is one of the most debatable questions in ecology
(Vamosi et al. 2009; Elias et al. 2009). Two major contradicting theories known as
deterministic and neutral theories have emerged to address this question. The core
principle of the deterministic theory (also known as niche theory) is that a given
habitat selects for species that share similar phenotypes and physiology (Hutchinson
1959; Webb et al. 2002). Therefore, species assemblages are expected to be
constrained by both their fundamental niche (i.e. abiotic requirements) and biotic
interactions. The abiotic factors act as filters that dictate the composition of a
community by allowing only species that are ecologically similar. As a result, the
community will be composed of species sharing phenotypic characteristics that help
them pass through the environmental barriers (Webb et al. 2002). The biotic
interactions could be either negative (e.g. competition) or positive interactions (e.g.
facilitation and mutualism). Negative interactions prevent phenotypically and
physiologically similar species from coexisting (Darwin 1859; Webb et al. 2002)
whilst positive interactions reduce stress level in local habitats, and in doing so
facilitate species coexistence (Bruno et al. 2003; Valiente-Banuet & Verdu 2007).
Conversely, Hubbell (2001) developed a challenging neutral theory according
to which niche characteristics are not relevant in assembly process. He referred to
communities as just random collections of species driven only by dispersal and
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stochastic demographic processes. As a consequence, differences between species
(e.g. traits differences, competitive ability differences, niche differences, etc.) and
interactions between species and with the environment do not matter in
assemblages processes (Bell 2001; Hubbell 2001; Chave 2004; Vamosi et al. 2009).
Studies that investigated the relative importance of both theories cover several
systems including microbes (e.g. Anderson et al. 2004; Horner-Devine & Bohannan
2006; Newton et al. 2007), arthropods (e.g. Gillespie 2004; Vamosi & Vamosi 2007),
vertebrates (e.g. Peres-Neto 2004; Lovette & Hochachka 2006; Helmus et al.
2007a,b), parasites (Mouillot et al. 2005) and plant communities (e.g. Webb 2000;
Cavender-Bares et al. 2004, 2006; Ackerly et al. 2006; Kembel & Hubbell 2006;
Proches et al. 2006; Silvertown et al. 2006; Slingsby & Verboom 2006; Swenson et
al. 2006; Webb et al. 2006; Hardy & Senterre 2007; Verdu & Pausas 2007; Valiente-
Banuet & Verdu 2007; Silva & Batahla 2009). Of these studies, 71.80% were
conducted in temperate areas and only 28.20% in tropical biomes (see Vamosi et al.
2009 for detailed review). Among studies that focused on plants system, forest
biomes received greatest attention (e.g. Webb 2000; Chazdon et al. 2003;
Cavender-Bares et al. 2004; Hardy & Senterre 2007; Kembel & Hubbell 2006; Kraft
et al. 2007, 2008; Swenson et al. 2006; Webb et al. 2006). However, there have
been only two studies that took place in savanna biomes i.e. grassland savanna (e.g.
Proches et al. 2006) and savanna (e.g. Silva & Batahla 2009). Because forest and
savanna biomes are two ecologically different systems (Hoffmann et al. 2005), there
is therefore a need of furthering research to fill the gaps of knowledge regarding
assembly process in savanna biomes. Due to the ease of their conversion to
agriculture or urban uses, and in the face of global change, savannas are the world’s
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most endangered biomes (Scholes & Archer 1997). Furthermore, savannas also
harbor a large proportion of rangelands and livestock (Scholes & Archer 1997).
Here I focus on the woody plant communities of the KNP, which is a tropical
woodland savanna (Schmidt et al. 2007). Understanding how communities are
structured could give insights into to the ecological forces that shape the structure
(Webb et al. 2002; Hardy & Senterre 2007; Hardy 2008; Hardy & Jost 2008;
Cavender-bares et al. 2009), and identifying those forces is a critical step towards
the protection of biodiversity patterns (Cavender-Bares et al. 2009).
Two questions are addressed in this chapter. First, is plants spatial
distribution in the KNP random with respect to phylogeny? Second, are species
within sites more or less related than species from different sites? The main
objective of this study is thus to test the current plant community structure against
random expectations in a tropical African savanna. Specifically, I test spatial and
traits distribution of woody plants against nulls models.
2.1. Dataset
Two data sets were analysed: plant ecological traits and community species
composition. Plants traits correspond to those traits indicated in Chapter 3.
Community composition data were collected from March 2008 to 2009, during which
I surveyed 110 2,500m2-plots (50m x 50m). These plots were distributed throughout
the KNP following a south-north transect. They were spread within the 15 ‘eco-
zones’; eco-zones being defined by specific vegetation and soil types (Venter 1990).
To avoid edge and fire effects, plots were situated at least 300 m from the nearest
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track in unburnt areas, but were accessible by gravel roads. In each plot I recorded
all species of trees and shrubs and their abundance (counts of individuals). Overall,
222 species were recorded with an average of 22 species and 309 individuals per
plot.
2.2. Data analysis
Three types of analyses were conducted. First, I characterised the community
composition of the 110 plots in the KNP using three common diversity metrics: the
Shannon index (H) calculated using the ‘diversity’ function implemented in the R
package Vegan 1.17 (Dixon 2003), species richness (SR) and phylogenetic diversity
(PD; Faith 1992), both calculated using the ‘pd’ function implemented in the R
package Picante 1.2 (Kembel et al. 2010).
These three diversity metrics differ in the way diversity features are captured
(Faith 1992; Couteron & Pélissier 2004), but also in their sensitivity to sample size
(Gimaret-Carpentier et al. 1998) and species delimitation (Faith 1992; Isaac et al.
2004; Faith & Williams 2005). For example, species SR weights common and rare
species equally, but its dependency on sample size makes it difficult to estimate in
species-rich communities (Gotelli & Colwell 2001). In contrast, Shannon index H
takes account of the relative abundance of each species, but both metrics (SR and
H) are highly dependent on species definition, which is controversial. The difficulty in
species delimitation could cause flaws in diversity measurement (Mace et al. 2003),
giving all importance to PD, which captures evolutionary distinctiveness of each taxa,
so avoiding flaws in species delimitation (Faith 1992; Isaac et al. 2004; Faith &
Williams 2005). It is therefore crucial to consider a multiple diversity metric approach
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if one wants to capture different patterns of biodiversity. I therefore mapped all
metrics onto the KNP map to generate an overall distribution pattern of plant
diversity along a south-north gradient.
Second, I characterised the within-site community structure using three
approaches. The first approach consists of testing whether there is a significant
phylogenetic signal in species co-occurrence. Therefore, I calculated the frequency
of species co-occurrence using the Schoener's index of co-occurrence “Cij”, and the
phylogenetic distance between species. I then calculated the correlation coefficient
between species co-occurrence and phylogenetic distance using ‘comm.phylo.cor’
function implemented in R package Picante 1.2 (Kembel et al. 2010). A significant
positive or negative correlation would indicate that communities are
overdispersed/even (distantly related species co-occur more often) or
underdispersed/clustered (closely related species co-occur more often) respectively.
Absence of significant pattern between co-occurrence frequency and phylogenetic
distance is consistent with random community composition. Using the same function
‘comm.phylo.cor’, I also compared the observed correlation to the expected
correlation under a random community composition. This random community was
generated using the null model ‘pool.taxa.labels’ (also implemented in Picante 1.2)
where tip labels have been shuffled 1000 times across all taxa included in the
phylogenetic tree (ML tree in chapter 2).
The second approach consists of comparing patterns of phylogenetic
relatedness within real communities (110 plots) to those expected under specific null
distributions. I therefore calculated two community metrics, the phylogenetic species
79
variability index (PSV, Helmus et al. 2007a, b) and the net relatedness index (NRI,
Webb et al. 2002, 2008).
Phylogenetic species variability (PSV) was calculated using the function
“phylostruct” implemented in Picante 1.2. Statistical significance of the PSV values
was evaluated by randomising community data matrices 1000 times, based on null
models “frequency” (maintaining species occurrence frequency), and “richness”
(maintaining sample species richness). Significance testing using multiple null
models that capture different degrees of randomness is crucial to provide confidence
in results interpretation. However, null models that involve swapping methods seem
to generate more efficiency and reliability statistically than random-fill procedures
(Gotelli & Entsminger 2001).
I therefore further tested significance in PSV value against the null model of
“independent swap”, and calculating 95% confidence intervals (ci). Independent
swap algorithm randomises patterns of species co-occurrence in samples without
introducing species from the phylogeny pool into the samples. It creates swapped
versions of the sample/species matrix and constrains the swapped matrices to have
the same row and column totals as the original matrix (i.e. number of species per
sample and frequency of occurrence of each species across samples are held
constant as species co-occurrences in samples are randomised). The swap
algorithm searches the presence/absence matrix for ‘checkerboard’ cells (pairs of
species/samples of the form (0...1), (1...0) or vice versa) and swaps these cell
contents when it finds them. I set the number of swaps per run to 1000 and
conducted 1000 runs.
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Net relatedness index (NRI) was calculated using the ‘ses.mpd’ function in
Picante 1.2. Positive values of NRI indicate that closely related species co-occur
more often than predicted by chance (phylogenetic clustering), whereas negative
values indicate greater co-occurrence of more distantly related species (phylogenetic
evenness). I assessed significance of NRI using 1000 simulations and assuming the
complete list of woody species in the KNP as the regional pool (null model
“phylogeny.pool” in Picante 1.2).
The third approach termed ‘Hardy & Senterre’s approach’ characterises
among-site community structure (Hardy & Senterre 2007). These approaches are
complementary methods rather than alternative statistical techniques for the same
question. In the first and second approaches, community structures are based on a
hypothetical regional pool (phylogeny), and could vary with changes in this pool
(Hardy & Senterre 2007) and randomisation models used (Gotelli 2000; Miklo &
Podani 2004). In this third approach, regional pool does not really matter, and
therefore is believed to provide more robust outcome (Hardy & Senterre 2007).
I therefore computed the among-site community structure metrics PST and IST
(Hardy & Senterre 2007; Hardy 2008; Hardy & Jost 2008) using the function
‘spacodi.calc’ in the R package spacodiR 0.11 (Eastman et al. 2011). Both metrics
assess the proportion of the total diversity explained by species turnover among
sites based on species abundances. IST expresses the among-site differences in
species frequencies whereas PST indicates the gain of phylogenetic divergence
among species (Hardy & Senterre 2007; Hardy 2008; Hardy & Jost 2008). When PST
= IST, there is no community phylogenetic structure among sites, whereas PST > IST
(PST < IST) indicates that species found within a same site are more (less) related on
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average than species taken from different sites, indicating a phylogenetic clustering
(overdispersion).
Third, I investigated the phenotypic pattern of plant traits distribution. This
analysis is similar to the previous in that it investigates community structure, but
differs form them in that it includes only phenotypic data (plant ecological traits), but
not phylogenetic information. I therefore calculated the community trait-based
metrics TST and IST (Eastman et al. 2011) using the same package spacodiR. TST >
IST or TST < IST suggests that traits are under- or overdispersed respectively,
indicating that habitat differentiation and ecological sorting are key drivers of
community composition (Webb et al. 2002; Kraft et al. 2007).
3. Results
3.1. Overall diversity and community structure in the KNP
I found a strong south-north gradient for woody plant community diversity across the
KNP, and this was evident in all three diversity metrics H, SR and PD, with high
diversity in the south and extreme north of the park, and low diversity in the centre
(Figure 1). H varied between 1.8 and 3.7 bits; community composition was made of
between 13.28 and 31 species, and phylogenetic information accumulated in
communities was evaluated between 0.58 and 3.11 (changes/sequence site).
Shifts in community phylogenetic structure paralleled changes in community
diversity, but with lower NRI in the south and north of the park, and higher NRI
towards the centre, indicating that communities in the centre are relatively clustered
(Figure 1).
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83
Figure 1 General pattern of plant diversity and phylogenetic structure along a south-
north gradient in the KNP. Plant diversity as indexed by SR (species richness), H
(Shannon index) and PD (phylogenetic diversity). Phylogenetic structure is indexed
by net relatedness index (NRI). Colours reflect interpolated values derived from plot
centre points using Ordinary Kriging with a 12-cell neighborhood.
3.2. Community phylogenetic structure within and among sites
Four analyses were performed. First, I calculated the correlation coefficient r
between species co-occurrence and phylogenetic distance between co-occurred
species. I found that r was significantly negative (r = - 0.023, p = 0.0003), i.e. as
phylogenetic distance between species increased, species co-occurrence frequency
decreased. Even compared with the expected co-occurrence frequency under a
random community composition, the observed correlation coefficient significantly
departed from random expectation (p = 0.01).
Second, I evaluated the PSV value and compared it with the expectation
under three different null models. Observed PSV was always lower than the 95%
central PSV distribution interval, indicating species within plots tend to be more
related than expected by chance (phylogenetic clustering; Figure 2)
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Figure 2 Values of observed phylogenetic species variability (PSV) within
communities (dashed red line). Histogram bars represent PSV values based on 1000
randomisations performed under three different models: frequency, richness and
independent swap. Black dashed lines give the 95% confidence interval.
Third, I calculated the NRI metrics. Across all plots, the vast majority of NRI
values were positive (Supplementary Information, Table S2), indicating that co-
occurring species in the KNP were generally more closely related than expected by
chance, giving further support to the previous findings.
Fourth, I looked at the PST and IST values. I found PST > IST (PST = 0.21; IST =
0.10), indicating that species within plots were more related on average than species
from distinct plots; thus giving support to the phylogenetic clustering found
previously.
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3.3. Community trait-based structure within and among sites
Similarly, I found for trait structure that TST > IST (TST = 0.44; IST = 0.10), indicative of
a non-random distribution of plant traits within and among communities.
4. Discussion
Plant diversity within the KNP is not randomly distributed, i.e. is strongly spatially
structured. Diversity, as indexed by either species richness, phylogenetic diversity or
Shannon’s index is highest in the north and south of the park, and lowest towards
the centre of the park. A strong correlation between SR and PD is expected in
general (Rodrigues & Gaston 2002), but the co-variation with Shannon’s H indicates
that the increase in diversity is not simply a product of more rare species. Northern
and southern communities are both more species rich and have a more even
representation of species. Strong south-to-north gradients in rainfall within the KNP
have been documented (Zambatis 2003) and suggested to be one driver of diversity
gradients in the park (Linder 1991). In addition, the physical structure of the
landscape, including topographic heterogeneity (Thuiller et al. 2006, 2008) and soil
types (Du Toit 2003) are also likely important drivers of species diversity in the
savanna biome.
Further to this, I found that both taxa and traits are also not randomly
distributed in the KNP. They are in contrary under-dispersed, i.e. closely related
species sharing similar traits co-occur more often. This deviation from random
distribution may be indicative of underlying ecological mechanisms (Webb et al.
2002; Kraft et al. 2007; Mayfield & Levine 2010; see Vamosi et al. 2009 for further
references). This finding contradicts Hubbell’s neutral theory (Hubbell 2001), adding
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to the body of evidence that natural community composition may not result from only
a neutral assembly process such as demographic drift, dispersal and speciation
(Webb 2000; Swenson et al. 2006; Hardy & Senterre 2007; but see Proches et al.
2006; Silvertown et al. 2006; Slingsby & Verboom 2006).
Crucially I found that species co-occurring within communities are more
related on average than species from different communities. In other words, species
within the same community are more closely related, but species from different
communities are less related. What could be the major driver of such pattern in the
KNP? Hardy & Senterre (2007) found similar pattern in a tropical forest tree
community (Equatorial Guinea) and argued that it could be a result of habitat
differentiation i.e. communities occur in contrasted habitats. Similar conclusion could
also be drawn here in the KNP. The KNP comprises 15 eco-zones and various
habitats probably characterised by various soil types, specific vegetation, topography
and climate structured along a south-north gradient (Venter 1990; Linder 1991).
Such habitat differentiation might shape the strong spatially structured communities
observed (Figure 1), and could also dictate a specific species to communities of
different habitats (habitat filtering, Webb et al. 2002; Kraft et al. 2008).
However, habitat filters might not be limited to habitat characteristics only
(climate, soil types, topography, etc.). They might also include disturbances (Pierce
et al. 2007) such as herbivory, which are also considered as key driver of under-
dispersion within communities (Pierce et al. 2007; Verdu & Pausas 2007; Cavender-
Bares et al. 2009; Helmus et al. 2010). The KNP is well renowned for its large game
animals - including over 150000 antelopes, 35000 buffalos, 20000 zebras, 13000
elephants (census 2009; www.sanparks.org; see also Chapter 5) exerting
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considerable pressures on plant diversity. These pressures could more likely be one
important factor shaping community structure in the park. This is discussed in
Chapter 5. Habitat filtering acts as a barrier that filters out plants missing specific
phenotype that is compatible to environmental requirements. As a result of filtering
processes, communities are under-dispersed i.e. composed of species sharing
similar traits. Because traits are under-dispersed in the KNP, habitat filtering could
be an active force structuring communities in the park.
Meanwhile, the under-dispersion structure found in the KNP is in sharp
contrast to the over-dispersion reported by Silva & Batahla (2009) in a Brazilian
woodland savanna. These contrasting results may come from the different spatial
scales investigated i.e. 2500 m2 in this study vs. 25 m2 in Silva & Batahla (2009).
Indeed, at small scales competitive interactions are expected to be higher (leading to
overdispersion) than at large scale where niche overlap is less likely and competition
low (Swenson et al. 2006). Furthermore, the contrasting results may also arise from
the differences in approach used to reconstruct the phylogeny of regional pool. I
used DNA data to reconstruct a fully resolved phylogeny (ML tree, Chapter 2). In
Silva & Batahla’s (2009) study, the phylogeny was reconstructed using the
‘Phylomatic’ approach (Webb & Donoghue 2005). Phylomatic program attaches taxa
by genus or family name to a supertree hypothesis for the seed plants constructed
from published phylogenies. If any genus is missing from the supertree, the program
returns a polytomy of genera within that family or polytomy of species in that genus
as the case may be. Although the use of Phylomatic-generated tree is common, it
has been recently showed that such tree could inflate the community structure metric
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(Davies et al., in press), and as a consequence, inferences drawn from analyses
using such tree would be incorrect (Kress et al. 2009).
5. Conclusion
This work is a contribution to the ongoing debate relative to the importance of neutral
vs. niche processes in community assemblages. I show that communities in the KNP
are not random i.e. they are likely structured by deterministic or niche-related
process. Such process may be driven by habitat filtering including herbivory.
Currently, there is a lack of experimental research that can help differentiate
between the effects of each of these factors on community structure. The specific
role of herbivory is addressed in Chapter 5.
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Chapter 5 The role of megaherbivores in shaping the structure of subtropical plant
communities
Chapter 5
The role of megaherbivores in shaping the structure of subtropical plant
communities
1. Introduction
Phylogenetic information is increasingly being used to study patterns and
processes of community assemblages (Cavender-Bares et al. 2004, 2009;
Webb et al. 2002, 2008). Here, I focus on the subtropical woodland biome of
the KNP. The dynamics of plant communities in this woodland are dictated by
various disturbances (Milchunas et al. 1988; Du Toit 2003), including
periodical events such as fire (Govender et al. 2006) and more or less
continuous pressures from megaherbivores (Carson & Root 2000; Van
Langevelde et al. 2003). Recent work has shown the important role of fire in
structuring the savannah ecosystems (Govender et al. 2006), but the impacts
of herbivory on woody species diversity are less clear (Van Langevelde et al.
2003). In Chapter 4, I showed that plant communities in the KNP are not
neutral, and that ecological filtering might be playing critical role. In the current
Chapter, I intend to investigate one of the potential filters that possibly dictate
current community composition – that is megaherbivores. Although
megaherbivores have been shown to reduce the three-dimensional structure
of vegetation in the KNP (Asner et al. 2009), several studies suggest that
herbivores may favour the diversity of woody plants (e.g. Sankaran et al.
2005) while others suggest that frequent and high herbivore pressures has a
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negative impact on woody plant diversity (e.g. Bond & Keeley 2005; Levick &
Rogers 2008).
I employed a phylogenetic framework to characterise the community
structure of woody plant species in the KNP, and evaluate the impact of
megaherbivore exclusion on community diversity and composition. Different
phylogenetic patterns are expected under various regimes of herbivory and
plant defences (Cavender-Bares et al. 2009). Firstly, if most megaherbivores
are generalist, plant species with generalist defences, such as spines, will
tend to dominate the community. If these generalist defences are
evolutionarily conserved, such that closely related plant species share similar
defences, the community will then tend to be phylogenetically clustered –
composed of more closely related species. However, when defence traits are
convergent, the community may demonstrate greater phylogenetic evenness,
such that community members are less closely related. Secondly, when
plants face high specialist herbivory pressures, abundant species are more
likely to be targeted, depressing the strength of competitive exclusion, thereby
allowing more rare species to persist in the community and elevating plant
diversity. Under multiple specialist herbivory pressure, when defence traits are
both matched closely to a specific herbivore and tightly conserved within plant
clades, the community will be phylogenetically evenly dispersed, but less
structured when traits are convergent (Figure 1).
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communities
Fabaceae
Polygalaceae
Myricaceae
Moraceae
Urticaceae
Ulmaceae, Cannabaceae
Rhamnaceae
Euphorbiaceae
Chrysobalanaceae
Ochnaceae
Malpighiaceae, Linaceae, Erythroxylaceae
Phyllantaceae
Picrodendraceae
Salicaceae
Passifloraceae
Achariaceae
Putranjavaceae, Clusiaceae
Celastrasceae
Balanitaceae
Anacardiaceae
Burseraceae
Anacardiaceae
Kirkiaceae
Rutaceae
Meliaceae
Sapindaceae
Malvaceae
Capparaceae
Salvadoraceae
Combretaceae
Myrtaceae
Lythraceae, Onagraceae
Melianthaceae
Vitaceae
Rubiaceae
Apocynaceae
Loganiaceae
Gentianaceae
Lamiaceae
Acanthaceae
Pedaliaceae
Bignoniaceae
Verbenaceae
Stilbaceae
Oleaceae
Solanaceae
Boraginaceae
Icacinaceae
Araliaceae, Apiaceae
Pittosporaceae
Asteraceae
Ebenaceae
Sapotaceae
Primulaceae
Portulacaceae, Plumbaginaceae
Olacaceae
Proteaceae, Ranunculaceae
Annonaceae
Canellaceae, Hernandiaceae
Asparagaceae Asphodelaceae
Velloziaceae
Arecaceae
Amborellaceae
Figure 1 Relationships between plant phylogeny and megaherbivory. The ML
phylogeny of KNP trees and shrubs is depicted on the left (see detailed tree in
Chapter 2), with one defence trait showing conservatism (presence of spines)
in blue. On the right, two examples of megaherbivores are illustrated. On the
top, kudus are generalist and feed on a variety of plants, here represented by
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14 taxa indicated by green arrows for clarity (following Hooimeijer et al. 2005),
but in the KNP they consume up to 148 different species (Apps 2000). Heavy
pressure from generalist megaherbivores and conserved defence traits is
predicted to result in phylogenetic clustering of plant communities (Cavender-
Bares et al. 2009). On the bottom, giraffes are specialist browsers and feed
preferentially on Acacia, Kigelia and Strychnos (Apps 2000) (red arrows).
Heavy pressure from specialist megaherbivores and conserved defence traits
is predicted to lead to phylogenetic overdispersion (Cavender-Bares et al.
2009) (Photos by O. Maurin).
Although large mammal herbivores are well recognised as ecosystem
engineers (Waldram et al. 2008) or keystone ecosystem species (Owen-Smith
1988), it remains possible that plant communities are largely structured by
abiotic factors (Chapter 4), including climate, soil, and disturbances such as
fire. The phylogenetic tree generated for all woody species (Chapter 2) was
used to characterise the community structure and diversity across a north-
south transect spanning approximately 350 km (Chapter 4). I then evaluated
the impacts of megaherbivory by contrasting changes in woody plant
communities within long-term ecological plots, from which megaherbivores
have been excluded for several decades ('exclosures'), to the immediately
surrounding park.
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2.1. Study site: Exclosures
The construction of exclosures in the KNP decades ago facilitated the
investigation of impacts of megaherbivores on plant communities. These
exclosures – where megaherbivores are partly or fully excluded (Figure 2) -
have been established in the park for between eight and 43 years. All
megaherbivores are fully excluded from three exclosures: Hlangwine (220 ha;
38 years old), Nkuhlu (139 ha; eight years old) and Nwashitsumbe (302 ha;
43 years old). In two partial exclosures, Nkuhlu (139 ha) and Letaba (129 ha),
very large mammals such as elephants and giraffes have been excluded for
eight years, but smaller megaherbivores can still gain access (the fence goes
from 1.50 m upwards, Figure 2).
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Chapter 5 The role of megaherbivores in shaping the structure of subtropical plant communities
Figure 2 Map of the KNP showing major soil types, location of plots and exclosures.
95
communities
2.2. Traits of anti-herbivores defences
In Chapter 3, six plant traits were described but only four can be identified as
linked to herbivore ‘defence traits’. These include various physical and
mechanical properties, low leaf nutrient content and various chemical
compounds (Rosenthal & Kotanen 1994). It is important to note that the
different traits provide varying degrees of protection, depending upon the
specific herbivore. For instance, plant woodiness may be effective against
elephant, but it is of less relevance for impala; in contrast spines can protect
trees (e.g. Acacia) against impala, but not against giraffes. Considering a
diverse set of traits is therefore necessary to account for various feeding
behaviors of herbivores in African savannas. I did not consider chemical
defences here because woody plants in African savannas invest more in
physical and mechanical defences against large herbivores than in chemical
defences (Christoph & David 1997).
Physical defences include spines (Cooper & Owen-Smith 1986) and
particular growth strategies. Data on plant maximum height and spinescence
(presence/absence) collected are presented in Chapter 3 and used here as
measures of plant physical defences. Mechanical defences include resistance
to herbivore pressures. I used wood density to quantify resistance to such
damage, and specific leaf area to capture leaf economic spectrum (see
Chapter 3 for details).
2.3. Community sampling in the exclosures
In the KNP 110 plots of 50 x 50 m were sampled (Chapter 4). These data are
completed here by a sampling of 73 plots of the same size in all exclosures.
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The KNP like any other African savanna, is a heterogeneous environment
defined by the variability of its geology, geomorphology, climate, vegetation
and soil (Du Toit 2003). The exclosures were designed to capture this
heterogeneity. They are constructed from the south to the north to account for
climatic south-north variability on the two major soil types: granite and basalt
(Figure 2). Due to cost and practical considerations (i.e. it was not reasonable
to establish new exclosures from which megaherbivores could be excluded
over several decades), I was restricted to contrasting communities across
these pre-existing exclosures. In total, I sampled 183 plots (110 KNP-plots
and 73 exclosure-plots), representing richness and abundance estimates for
216 species (the subset of KNP woody plant diversity found in plots) across
457,500 m2.
2.4. Statistical analyses
To test the major hypothesis of this study, which is presented above and
pioneered by Cavender-Bares et al. (2009), evolutionary conservatism in
defence traits is crucial. This was discussed in Chapter 3 for all traits
considered above as defense traits against megaherbivores. Additionally, it is
essential to characterise community structure within and outside exclosures.
Patterns of community outside the exclosures, i.e. in the KNP where
herbivores have permanent access was presented and discussed in Chapter
4. Here I evaluated the effects of megaherbivores on diversity and community
structure by comparing community patterns of plots within exclosures to plots
in the adjacent park (KNP-plots). Adjacent plots were defined as those falling
within a 25 km radius of each exclosure because this distance was found to
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provide the best compromise between maximising the sample size of included
plots and restricting contrasts to between more or less comparable
communities (Figure 3).
Figure 3 Location of KNP-plots (small circles) and exclosures (squares) along
a south-north transect in the park. Larger circles define areas of 25 km radius
around each exclosure. KNP-plots falling within these areas are considered
as adjacent KNP-plots to the exclosures. These adjacent KNP-plots were
used for pairwise comparisons to evaluate community patterns within versus
outside exclosures. See Figure 2 for location and names of exclosures.
3. Results
In a global comparison of plots within exclosures versus plots outside
exclosures, I found that diversity was consistently lower inside exclosures
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(Figure 4; t test, p <0.001), but observed no obvious trend in phylogenetic
community structure (Figure 4; t test, p = 0.38).

8
50
7
40
6
30
PD
SR
5
20
4
3
10
2
Exclosures KNP Exclosures KNP

Treatment Treatment
5
5
4
4
3
3
NRI
H
2
2
1
0
1
−1
Exclosures KNP Exclosures KNP

Treatment Treatment
Figure 4 Comparison of plant diversity and phylogenetic structure between all
exclosures KNP-plots. Exclosures include 73 plots (full and partial exclosures
combined), and are compared with the 110 KNP-plots, where herbivory is
unrestricted.
To evaluate in more detail shifts in community composition I used
pairwise comparison of plots within exclosures and their adjacent areas.
Confirming the global trend, I found large and significant decreases in
diversity within exclosures (Figure 5). SR was significantly lower within
exclosures Hlangwine, Nkuhlu and Nwashitsumbe (t test, p < 0.002) in
comparison to the adjacent park. In Letaba, although difference in SR
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communities
between exclosure and adjacent KNP-plots was not significant, plots showed
a similar trend. The same patterns were also observed for H but significant
difference occurred only in Hlangwine (t test, p = 0.03). PD also decreases
significantly in exclosures in all sites (t test, p <0.05) except Letaba, where PD
within the exclosure and surrounding KNP was similar.
Letaba Nwashitsumbe Hlangwine Nkuhlu

50
30
35
20
40
25
SR
SR
SR
SR
30
20
15
25
20
15
10
15
10
10
KNP Partial KNP Full KNP Full KNP Full Partial

4.5
3.0
3.5
4.0
3.5
2.5
H
H
2.5
3.0
2.5
2.0
1.5
1.5
2.0
1.5

6.0
8
7.0
5.0
5.0
6.0
6
4.0
PD
PD
PD
PD
4.0
5
5.0
3.0
3.0
4.0
3
2.0
Figure 5 Pairwise comparison of plant diversity between each exclosure and
its adjacent area. Full = full exclosure; Partial = partial exclosure; KNP = plots
situated within 25 km of each exclosure. Location of exclosure sites (Letaba,
Nwashitsumbe, Hlangwine and Nkuhlu) are shown in Figure 2. The bottom
and top of the boxes show the first and third quartiles respectively, the median
is indicated by the horizontal line, the range of the data by the vertical dashed
line and outliers (points outside 1.5 times the interquartile range) by circles.
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communities
The results for the phylogenetic metrics (NRI) of community structure
were more complex (Figure 6). In the South, no difference was found within
and outside exclosures (t test, p >0.05). However, in the centre of the park I
found that NRI was significantly lower in exclosure (Letaba) than in adjacent
KNP-plots (t test, p = 0.004), whilst in the North of the park I found the
opposite pattern, such that NRI values in exclosure (Nwashitsumbe) were
significantly higher than in adjacent KNP-plots (t test, p = 0.0003).
Letaba Nwashitsumbe
4
4
3
3
NRI
NRI
2
2
1
1
0
0
KNP Partial KNP Full
Hlangwine Nkuhlu
3.5
5
4
2.5
NRI
NRI
3
1.5
2
1
0.5
KNP Full KNP Full Partial
Figure 6 Pairwise comparison of plant community structure between each
exclosure and its adjacent area.
Exclosures differ in age (8-43 years) and in the megaherbivore species
excluded (full exclosures versus partial, the latter only excluding very large
animals such as elephants and giraffes). It is possible that differences
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communities
between exclosures might then be explained by plot treatment or history.
However, I found no significant difference in diversity patterns between
exclosures of different ages (8 vs. 38 years; Figure 7), and no consistent
differences between partial and full exclosures, even when comparing
adjacent exclosures of equivalent age (NRIPartial exclosure ≈ NRIFull exclosure in
Nkuhlu, p = 0.27; Figure 8).
Figure 7 Patterns of plant diversity according to age of exclosures contrasted
with pattern in the 110 KNP-plots. Ages are in years. SR= Species richness; H
= Shannon index; PD = Phylogenetic diversity.
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Figure 8 Patterns of plant diversity according to treatment contrasted with
pattern in the 110 KNP-plots. SR= Species richness; H = Shannon index; PD
= Phylogenetic diversity. Full = Full exclosure; Partial = Partial exclosure.
4. Discussion
The KNP represents an important biome that provides crucial ecosystem
services to Africa and beyond, and is included within current lists of the
Earth's biodiversity hotspots (Maputaland-Pondoland-Albany biodiversity
hotspot; Perera et al. 2011). The role of megaherbivores in maintaining these
ecosystems has been debated, particularly the population sizes that the
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biome can sustain (Du Toit 2003). There is a concern that megaherbivores
(especially elephants) impact negatively on plant biodiversity in the KNP
(Levick & Rogers 2008). However, there may be a critical megaherbivore
density below which negative impacts reported elsewhere (e.g. Trollope et al.
1998; Levick & Rogers 2008) are not felt (Baxter & Getz 2005). In this study I
combined diversity information across a series of exclosures and compared
patterns with adjacent sites across the KNP. I showed that when
megaherbivores are excluded, diversity generally decreases (see also Kalwij
et al. 2010), but impacts on plant community structure were more nuanced.
4.1. Exclusion of megaherbivores and plant diversity
In the pairwise comparisons across exclosures, I found a consistent trend for
lower diversity as indexed by SR and Shannon’s H although the strength of
this trend varied among sites. Notably, differences in H were only significant
for Hlangwine in the South of the park. By contrast, differences within and
outside exclosures were less for Letaba, located in the centre of the park.
Further, despite the tight positive correlation between PD and SR, PD was
marginally higher within the Letaba exclosure. One possible explanation for
differences between sites might be variation in their age of establishment; for
example, the Hlangwine exclosure was created 38 years ago, whilst Letaba
has only been in existence for 8 years. However, I found no evidence for a
bias with age, and diversity for plots in exclosures of 8 and 38 years was
statistically indistinguishable. A second possible explanation for site
differences is in the size class of megaherbivores excluded. Partial exclosures
allow access to all but the very largest megaherbivores, whereas the full
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exclosures are more restrictive, also excluding rhino and antelopes. However,
once again I found no difference in diversity between exclosure types when
comparing partial and full exclosures at the same sites.
4.2. Exclusion of megaherbivores and phylogenetic structure
Across the KNP I found significant phylogenetic clustering of plant
communities. This is discussed in Chapter 4. One recent theory predicts
phylogenetic clustering of plant communities under heavy pressure from
generalist herbivores when plant defence traits are evolutionarily conserved
(Cavender-Bares et al. 2009). The majority of megaherbivore browsers in the
KNP are generalist. In addition, most defence traits demonstrate some
significant phylogenetic conservatism (Chapter 3). The findings of
phylogenetic clustering of plant communities, significant conservatism in
defence traits, and evidence for strong generalist herbivory pressure imposed
by megaherbivores fit well theoretical predictions (Cavender-Bares et al.
2009), and indicate that megaherbivory has a significant role in shaping the
phylogenetic structure of plant communities in the park (Helmus et al. 2010).
However, other drivers of community structure, such as habitat filtering might
still be important (Chapter 4).
To evaluate the effect of removing megaherbivores, I compared
phylogenetic community structure between plots inside exclosures to those in
the adjacent park. If megaherbivores drive community clustering, I would then
expect communities in exclosures to be more evenly dispersed (i.e. NRIexclosure
< NRIKNP). In addition, because some megaherbivores can access the partial
exclosures, I might also expect that partial exclosures would demonstrate
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intermediate clustering, weaker than the KNP plots with unrestricted herbivore
access (i.e. NRIPartial exclosure < NRIKNP), but greater than the plots in full
exclosures (i.e. NRIPartial exclosure > NRIFull exclosure). However, across exclosures I
did not find evidence for any consistent trend towards less clustering within
versus outside exclosures or between full and partial exclosures.
Nonetheless, exclosures had an important impact on plant community
structure. Where communities under unrestricted megaherbivore pressure
were the most evenly dispersed (i.e. in the North of the park), excluding
megaherbivores shifted communities to become more clustered. By contrast,
where communities were initially more clustered (i.e. in the centre of the park),
the exclusion of megaherbivores shifted community structure towards greater
evenness. These results therefore indicate that impacts of megaherbivore
exclusion on community structure are contingent upon the initial community
structure.
5. Conclusion
This study shows not only that megaherbivores are key to maintaining a
diversity of species of trees and shrubs, but also that they might impose a
specific phylogenetic structure on plant communities, likely important for
ecosystem functioning. However, excluding megaherbivores has mixed
effects on community structure; the phylogenetic structure of the community
shifts, but the direction depends on the initial community structure. Results
were similar for both partial and full exclosures, suggesting that it is the very
largest megaherbivores (i.e. elephants and giraffes) that are responsible for
driving these changes.
106
communities
The restricted number of exclosures limits the statistical inference one
can draw with regard to mechanism. Nonetheless, the results are critical for
predicting potential losses of phylogenetic diversity (PD) from the woodland
biome of southern Africa as megaherbivores decline across much of the
continent. Phylogenetic diversity is a valuable measure because it can
capture genetic and functional diversity, representing options in an uncertain
future (Faith 1992; Mace et al. 2003; Forest et al. 2007). Loss of PD might
therefore have larger ecosystem consequences for future biodiversity than
loss of species richness per se. These results indicate that losses of PD are
likely to be exacerbated for communities that shift towards greater
phylogenetic clustering, whereas losses may be less for communities shifting
towards greater phylogenetic evenness. I observe this trend in my comparison
between exclosures. In Nwashitsumbe, communities become more clustered
and losses of PD are large, whereas in Letaba, communities become more
evenly dispersed, and there is a weak trend for higher PD in the exclosures,
despite their lower species richness.
Characterising the structure of a wider range of communities using
phylogenetic trees, which can now be easily estimated from DNA barcode
data (Lahaye et al. 2007; Kress et al. 2009), will help us predict community
responses. The results in this study have important implications for
management of African woodlands. Critically, under-herbivory might be as
damaging to plant communities as over-herbivory. As large herbivores are lost
from these ecosystems, I predict a subsequent reduction in plant species
diversity.
107
Chapter 6 General conclusion
Chapter 6
General conclusion
1. Major findings, discussion and contribution to literature
1.1. Phylogenetic information database for KNP
A molecular database of plant DNA barcodes (matK and rbcLa; CBOL Plant Working
Group 2009) was produced for 93% of tree and shrub species of the KNP. This
molecular matrix represents the largest so far made available for a tropical African
woodland savanna. The use of this database to reconstruct the phylogeny of trees
and shrubs in the KNP proves reliable, as it helps generate a phylogeny highly
congruent with the latest phylogenetic studies of angiosperms (APG III 2009; Soltis
et al. 2011). As phylogenetic approach is increasingly acknowledged as key and
unique tool of ecological investigations, this DNA database constitutes an important
tool of sustaining the biodiversity of the park.
More importantly, it provides ecologists with an invaluable tool to investigate
ecological long-standing questions. These questions comprise the assembly theory,
the sustainability of biodiversity and ecosystem functions under global change
(Davies et al. 2008; Willis et al. 2008, 2010), the dynamic nature of species pool, the
primary process that group species together (in situ evolution vs. dispersal ability)
(Ackerly et al. 2006), the feedback influence of within-community interactions on trait
diversity (Cavender-Bares et al. 2009), etc.
108
1.2. Ornstein-Uhlenbeck is more suitable for phylogenetic comparative
analysis of plant traits in the KNP
How species traits evolve over time might be critical to understand what drives
species co-existence. Here I tested the fitness of several evolutionary models to the
ecological data of plants in the KNP using various approaches. I showed that the
conventional mode of evolution, i.e. Brownian model was not the best model. Rather,
I found that Ornstein-Uhlenbeck model was more appropriate for comparative study
in the KNP. This model suggests that a random walk constrained by ecological
forces towards a stabilising selection describes plant traits better.
1.3. Plant community assemblages in the KNP are not neutral
This study revisited the most influential theories i.e. the neutral and niche theories of
community assembly process. Here I mainly investigated whether community
composition is neutral from a phylogenetic perspective. I found that (1) species
within a given community are more phylogenetically related than expected under
various null expectations; and (2) that species of two different communities are less
related. This finding is consistent with a pattern of phylogenetic underdispersion,
which is most likely driven by habitat filtering (Webb et al. 2002; Hardy & Senterre
2007). This provides additional evidence to the body of literature that natural
community assemblages are not neutral, but are dictated by niche characteristics.
1.4. Megaherbivores leave distinct signature on plant community structure
Megaherbivores are well recognised as ecosystem engineers; however, their impact
on plant community structure and diversity remains debated. Several studies
suggest megaherbivores may favour the diversity of woody plants, while others
109
report a negative impact on plant diversity. Here, I asked how plant communities
respond to megaherbivores pressure in an African woodland savanna, using the
KNP as a case study.
To date, attempts to address such a question have been hampered by a lack of
long-term experiments. For instance, Cavender-Bares et al. (2009) predicted
outcomes of herbivores impacts using phylogenetic approach, but lacks
experimental test; Asner et al. (2009) investigated the impacts of megaherbivores on
the three-dimensional structure of plant community, but lacks phylogenetic
information; Helmus et al. (2010) focused on shift in community structure under
disturbance factors in general, but lack information on specificity of disturbances
caused by megaherbivores.
The present thesis provides a more comprehensive study about megaherbivores
and their impacts on plant community structure. I evaluated the impacts of
megaherbivory by contrasting changes in communities within long-term ecological
plots, from which megaherbivores have been excluded for several decades. I found
that diversity decreases where megaherbivores have been excluded. However, shifts
in community structure were more complex. Communities initially clustered become
more evenly dispersed when megaherbivores are excluded, whilst communities
initially more even become more clustered. This indicates that megaherbivory is
essential for maintaining plant diversity; however, impacts on community structure
can only be predicted when we have information on the initial structure. Crucially, the
finding that shifts in community structure are contingent upon the initial community
composition is novel to our understanding of how plant communities could respond
to disturbances.
110
I believe the results presented here will receive considerable attention from
scientists and conservationists. For example, the role of elephants in structuring the
vegetation in South Africa is hotly debated, and culling has been put forward as an
urgent necessity - my results challenge this view.
Furthermore, the results also have important implications for management of
African woodlands, particularly given the continental decline in megaherbivores. As
large herbivores are lost from these ecosystems, I predict a subsequent reduction in
plant diversity, whilst the impact on plant community structure will depend upon the
initial composition. Critically, I also showed that the loss of phylogenetic diversity (a
surrogate for functional diversity) will depend on the relative shifts in phylogenetic
community structure, information that has never been considered before in
management strategy.
The KNP is part of a biodiversity hotspot and represents an important biome that
provides crucial ecosystem services beyond Africa. The preservation of this
important biome requires continued commitment to understand how its flora will
respond to future changes, including climate shifts, and the continued continental
decline in megaherbivores. The study provides significant novel information in this
regard.
2. Future challenges
The emerging field of community phylogenetics has proved promising in addressing
long-standing controversies in ecology such as how species assemble, how species
interactions influence evolutionary process, and how communities and ecosystems
respond to global change (Willis et al. 2008; Cavender-Bares et al. 2009). It is now
clear that evolutionary relationships among co-occurring taxa play key role in the
111
assembly process. Meanwhile, despite the improvement phylogenetics brought into
the ecologically important debate, key questions still remain poorly understood.
First, numerous ecological data were gathered by various researchers
investigating various ecological questions in the KNP. Now there is a need to
reinvestigate (where possible) these questions from a phylogenetic perspective. This
thesis provides researchers with a phylogenetic tool (DNA database) to do so, which
will more likely bring additional key information about how to sustain the biodiversity
of the park.
Second, information on how plant communities and ecosystems are
responding to ongoing global change (especially climate change) is lacking in
tropics. Establishing a predictive model in this regard will help mitigate global change
effects on biodiversity. In recent studies conducted by Willis et al. (2008, 2010) in
temperate regions, they demonstrated a phylogenetic selectivity effect of climate
change on biodiversity. In other words, they showed that climate change is causing
loss of species in some specific clades, and concluded that if the ‘tree of life’ is
continuously pruned due to climate change, we might end up losing a huge amount
of evolutionary diversity.
In tropical zones especially in tropical Africa, there is a conspicuous lack of
information on how climate change operates within and among clades. This required
a serious commitment from researchers. The increasing volume of DNA database
(e.g. DNA barcode project) is a crucial step forward in providing molecular
information with which several questions related to biodiversity could be investigated.
Third, little is known about edge effects on community phylogenetic structure.
Finally, although this study showed a positive correlation between megaherbivores
and species diversity, it is more likely that an increasing population of
112
megaherbivores will end up having negative effects. This raises the necessity of
conducting studies that provide conservation officers in the KNP with information
regarding the population size of megaherbivores than can be compatible with plant
diversity. Baxter et al. (2005) provided general information for African savanna in this
regards, and suggested that a negative effect on plant diversity could only be
observed at a density of elephant higher than one elephant/km2. Specific studies that
address this question in the KNP are urgently needed for management purposes.
Given the patchy distribution of megaherbivores (e.g. elephants) in the park due to
inconsistent distribution of resources, such studies should look at the question in
high-density area vs. low-density area of the park.
113
Chapter 7 References
Chapter 7
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Supplementary information
Supplementary Information Table S1 Voucher information and GenBank/EBI accession numbers for trees and shrubs of the
Kruger National Park.
GenBank Accession
Family APGIII Genus & Species Voucher (Herbarium) Numbers
rbcLa matK
Acanthaceae Anisotes formosissimus (Klotzsch) Milne-Redh. OM 868 (JRAU) JF265288 JF270643
Acanthaceae Anisotes rogersii S.Moore OM 865 (JRAU) — —
Acanthaceae Barleria albostellata C.B.Clarke OM 899 (JRAU) JF265299 JF270653
Acanthaceae Barleria rotundifolia Oberm. OM 1327 (JRAU) JF265300 JF270654
Acanthaceae Duvernoia aconitiflora A.Meeuse OM 1816 (JRAU) JF265402 JF270752
Acanthaceae Duvernoia adhatodoides E.Mey. OM 1759 (JRAU) JF265403 JF270753
Acanthaceae Metarungia longistrobus (C.B.Clarke) Baden CS 15 (JRAU) JF265518 JF270864
Acanthaceae Ruspolia hypocrateriformis (Vahl) Milne-Redh. OM 777 (JRAU) JF265577 JF270920
Acanthaceae Ruttya ovata Harv. OM 1150 (JRAU) JF265578 JF270921
139
Achariaceae Kiggelaria africana L. OM 1978 (JRAU) JF265491 JF270838
Achariaceae Xylotheca kraussiana Hochst. OM 1825 (JRAU) JF265662 JF271003
Amborellaceae Amborella trichopoda Baill. — L12628 AJ506156
Anacardiaceae Harpephyllum caffrum Bernh. ex Krauss OM 1555 (JRAU) JF265467 JF270814
Anacardiaceae Lannea discolor Engl. RL 1235 (JRAU) JF265496 JF270843
Anacardiaceae Lannea edulis Engl OM 1971 (JRAU) JF265497 JF270844
Anacardiaceae Lannea schweinfurthii Engl. RL 1108 (JRAU) JF265498 JF270845
Anacardiaceae Ozoroa engleri R.Fern. & A.Fern. OM 1154 (JRAU) JF265536 JF270879
Anacardiaceae Ozoroa obovata (Oliv.) R.Fern. & A.Fern. OM 840 (JRAU) JF265537 JF270880
Anacardiaceae Ozoroa sphaerocarpa R.Fern. & A.Fern. OM 940 (JRAU) JF265538 JF270881
Anacardiaceae Sclerocarya birrea Hochst. subsp. caffra (Sond.)
J.O.Kokwaro OM 498 (JRAU) JF265586 JF270929
Anacardiaceae Searsia chirindensis (Baker f.) Moffett OM 1987 (JRAU) JF265588 JF270931
Anacardiaceae Searsia gueinzii (Sond.) F.A.Barkley OM 248 (JRAU) JF265589 JF270932
140
Anacardiaceae Searsia leptodictya (Diels) T.S.Yi, A.J.Mill. &
J.Wen RBN 205 (JRAU) JF265590 JF270933
Anacardiaceae Searsia magalismontana (Sond.) Moffett OM 1836 (JRAU) JF265591 JF270934
Anacardiaceae Searsia pentheri (Zahlbr.) Moffett OM 942 (JRAU) JF265592 JF270935
Anacardiaceae Searsia pyroides (Burch.) Moffett OM 713 (JRAU) JF265593 JF270936
Anacardiaceae Searsia transvaalensis (Engl.) Moffett OM 943 (JRAU) JF265594 JF270937
Annonaceae Annona senegalensis Pers. OM 1214 (JRAU) JF265289 JF270644
Annonaceae Artabotrys brachypetalus Benth. OM 1298 (JRAU) JF265293 JF270647
Annonaceae Hexalobus monopetalus Engl. & Diels OM 753 (JRAU) JF265472 JF270819
Annonaceae Monanthotaxis caffra (Sond.) Verdc. OM 276 (JRAU) JF265520 JF270866
Annonaceae Monodora junodii Engl. & Diels RBN 288 (JRAU) — —
Annonaceae Uvaria gracilipes N.Robson OM 1960 (JRAU) JF265642 JF270983
Annonaceae Uvaria lucida Boj. ex Sweet RBN 138 (JRAU) JF265643 JF270984
Annonaceae Xylopia parviflora Benth. RBN 255 (JRAU) JF265661 JF271002
141
Apiaceae Heteromorpha arborescens Cham. & Schltdl. OM 592 (JRAU) JF265470 JF270817
Apiaceae Steganotaenia araliacea Hochst. OM 566 (JRAU) JF265604 JF270946
Apocynaceae Acokanthera oppositifolia (Lam.) Codd OM 1782 (JRAU) JF265265 JF270622
Apocynaceae Acokanthera rotundata (Codd) Kupicha OM 2009 (JRAU) JF265266 JF270623
Apocynaceae Adenium multiflorum Klotzsch OM 786 (JRAU) JF265270 JF270626
Apocynaceae Adenium swazicum Stapf OM 538 (JRAU) JF265271 JF270627
Apocynaceae Carissa bispinosa Desf. OM 253 (JRAU) JF265326 JF270679
Apocynaceae Carissa edulis Vahl OM 1692 (JRAU) JF265327 JF270680
Apocynaceae Carissa tetramera Stapf OM 1492 (JRAU) JF265328 JF270681
Apocynaceae Diplorhynchus condylocarpon (Müll. Arg.) Pichon OM 1498 (JRAU) JF265394 JF270746
Apocynaceae Holarrhena pubescens Wall. OM 1926 (JRAU) JF265476 JF270823
Apocynaceae Landolphia kirkii Dyer RBN 295 (JRAU) — —
Apocynaceae Pachypodium saundersii N.E.Br. OM 463 (JRAU) JF265539 JF270882
Apocynaceae Rauvolfia caffra Sond. RBN 216 (JRAU) JF265569 JF270912
142
Apocynaceae Strophanthus kombe Oliv. RBN 128 (JRAU) JF265607 JF270949
Apocynaceae Strophanthus petersianus Klotzsch OM 1616 (JRAU) JF265608 JF270950
Apocynaceae Tabernaemontana elegans Stapf RBN 176 (JRAU) JF265618 JF270961
Apocynaceae Tabernaemontana ventricosa Hochst. ex A.DC. OM 1877 (JRAU) JF265619 —
Apocynaceae Wrightia natalensis Stapf RBN 337 (JRAU) JF265654 JF270995
Araliaceae Cussonia natalensis Sond. OM 975 (JRAU) JF265381 JF270733
Araliaceae Cussonia spicata Thunb. OM 1553 (JRAU) JF265382 JF270734
Arecaceae Borassus aethiopium Mart. OM 1318 (JRAU) JF265306 JF270659
Arecaceae Hyphaene coriacea Gaertn. OM 755 (JRAU) JF265482 JF270829
Arecaceae Hyphaene petersiana Klotzsch ex Mart. OM 236 (JRAU) JF265483 JF270830
Arecaceae Phoenix reclinata Jacq. OM 274 (JRAU) JF265548 JF270891
Asparagaceae Dracaena aletriformis (Haw.) J.J.Bos OM 1778 (JRAU) JF265398 —
Asphodelaceae Aloe excelsa A.Berger OM 1621 (JRAU) JF265284 JF270640
Asphodelaceae Aloe marlothii A.Berger OM 1490 (JRAU) JF265285 JF270641
143
Asphodelaceae Aloe spicata L.f. OM 1522 (JRAU) JF265286 JF270642
Asteraceae Brachylaena huillensis O.Hoffm. OM 247 (JRAU) JF265311 JF270664
Asteraceae Brachylaena transvaalensis Hutchinson ex
Phillips & Schweick. OM 571 (JRAU) JF265312 JF270665
Asteraceae Vernonia aurantiaca N.E.Br. OM 877 (JRAU) JF265648 JF270989
Asteraceae Vernonia colorata Drake OM 980 (JRAU) JF265649 JF270990
Balanitaceae Balanites maughamii Sprague OM 223 (JRAU) JF265296 JF270650
Balanitaceae Balanites pedicellaris Mildbr. & Schltr. OM 901 (JRAU) JF265297 JF270651
Bignoniaceae Kigelia africana Benth. OM 217 (JRAU) JF265490 JF270837
Bignoniaceae Markhamia zanzibarica K.Schum. OM 629 (JRAU) JF265516 JF270862
Bignoniaceae Rhigozum zambesiacum Baker OM 1324 (JRAU) JF265571 JF270914
Bignoniaceae Tecomaria capensis (Thunb.) Spach OM 1475 (JRAU) JF265623 JF270965
Boraginaceae Cordia caffra Sond. OM 1561 (JRAU) JF265366 JF270719
Boraginaceae Cordia grandicalyx Oberm. OM 837 (JRAU) JF265367 JF270720
144
Boraginaceae Cordia monoica Roxb. OM 1423 (JRAU) JF265368 JF270721
Boraginaceae Cordia ovalis R.Br. ex DC. OM 1311 (JRAU) JF265369 JF270722
Boraginaceae Cordia sinensis Lam. OM 354 (JRAU) JF265370 JF270723
Boraginaceae Ehretia amoena Klotzsch OM 1123 (JRAU) JF265404 JF270754
Boraginaceae Ehretia rigida Druce OM 1235 (JRAU) JF265405 JF270755
Burseraceae Commiphora africana (A.Rich) Engl. OM 769 (JRAU) JF265357 JF270710
Burseraceae Commiphora edulis Engl. RBN 341 (JRAU) JF265358 JF270711
Burseraceae Commiphora glandulosa Schinz RBN 160 (JRAU) JF265359 JF270712
Burseraceae Commiphora harveyi Engl. OM 1415 (JRAU) JF265360 JF270713
Burseraceae Commiphora marlothii Engl. OM 1587 (JRAU) JF265361 JF270714
Burseraceae Commiphora mollis Engl. OM 328 (JRAU) JF265362 JF270715
Burseraceae Commiphora neglecta Verdoorn RL 1343 (JRAU) JF265363 JF270716
Burseraceae Commiphora pyracanthoides Engl. OM 621 (JRAU) JF265364 JF270717
Burseraceae Commiphora schimperi Engl. OM 1361 (JRAU) JF265365 JF270718
145
Canellaceae Warburgia salutaris (G.Bertol.) Chiov. OM 1853 (JRAU) JF265653 JF270994
Cannabaceae Celtis africana Burm.f. OM 1225 (JRAU) JF265333 JF270686
Cannabaceae Trema orientalis Blume RBN 246 (JRAU) JF265631 JF270972
Capparaceae Boscia albitrunca Gilg & Benedict OM 312 (JRAU) JF265307 JF270660
Capparaceae Boscia angustifolia Harv. RBN 268 (JRAU) JF265308 JF270661
Capparaceae Boscia foetida Schinz OM 296 (JRAU) JF265309 JF270662
Capparaceae Boscia mossambicensis Klotzsch RL 1212 (JRAU) JF265310 JF270663
Capparaceae Cadaba termitaria N.E.Br. OM 1930 (JRAU) JF265318 JF270671
Capparaceae Capparis fascicularis DC. subsp. fascicularis OM 1640 (JRAU) JF265323 JF270676
Capparaceae Capparis sepiaria subsp. glabrata OM 1604 (JRAU) JF265324 JF270677
Capparaceae Capparis tomentosa Lam. OM 232 (JRAU) JF265325 JF270678
Capparaceae Maerua angolensis DC. OM 1186 (JRAU) JF265507 JF270853
Capparaceae Maerua cafra Pax OM 1975 (JRAU) JF265508 JF270854
Capparaceae Maerua decumbens (Brongn.) DeWolf OM 1928 (JRAU) JF265509 JF270855
146
Capparaceae Maerua juncea Pax subsp. crustata (Wild) Wild OM 1905 (JRAU) JF265510 JF270856
Capparaceae Maerua parvifolia Pax OM 1108 (JRAU) JF265511 JF270857
Capparaceae Maerua rosmarinoides Gilg & Benedict OM 1998 (JRAU) JF265512 JF270858
Capparaceae Thilachium africanum Lour. OM 823 (JRAU) JF265628 JF270970
Celastraceae Catha edulis (Vahl) S.Endlicher OM 482 (JRAU) JF265331 JF270684
Celastraceae Elaeodendron transvaalense (Burtt Davy)
R.H.Archer OM 403 (JRAU) JF265407 JF270757
Celastraceae Gymnosporia heterophylla (Eckl. & Zeyh.) Loes. OM 623 (JRAU) JF265458 JF270805
Celastraceae Gymnosporia maranguensis Loes. OM 1637 (JRAU) JF265459 JF270806
Celastraceae Gymnosporia oxycarpa (N.Robson) Jordaan OM 1913 (JRAU) JF265460 JF270807
Celastraceae Gymnosporia pubescens (N.Robson) M.Jordaan OM 1929 (JRAU) JF265461 JF270808
Celastraceae Gymnosporia putterlickioides Loes. ex Engl. RBN 242 (JRAU) JF265462 JF270809
Celastraceae Gymnosporia senegalensis Loes. RBN 294 (JRAU) JF265463 JF270810
Celastraceae Gymnosporia sp. C NQ 5 (JRAU) JF265464 JF270811
147
Celastraceae Loeseneriella crenata (Klotzsch) R. Wilczek ex
N. Hallé OM 1270 (JRAU) JF265504 JF270851
Celastraceae Maytenus undata (Thunb.) Blakelock OM 1469 (JRAU) JF265517 JF270863
Celastraceae Mystroxylon aethiopicum subsp. schlechteri
(Loes.) R.H.Archer OM 243 (JRAU) JF265523 JF270869
Celastraceae Pristimera indica (Willd.) A.C. Sm. OM 1925 (JRAU) — —
Celastraceae Pristimera longipetiolata (Oliv.) N. Hallé OM 393 (JRAU) JF265558 JF270901
Celastraceae Putterlickia verrucosa Sim OM 1404 (JRAU) JF265566 JF270909
Celastraceae Salacia kraussii Harv. RBN 102 (JRAU) JF265579 JF270922
Chrysobalanaceae Parinari curatellifolia Planch. ex Benth. RBN 357 (JRAU) JF265541 JF270884
Clusiaceae Garcinia livingstonei T.Anders. OM 246 (JRAU) JF265444
Combretaceae Combretum apiculatum Sond. subsp. apiculatum OM 1068 (JRAU) JF265344 JF270697
Combretaceae Combretum celastroides Welw. ex M.A.Lawson
subsp. orientale Exell OM & MvdB 27 (JRAU) — —
148
Combretaceae Combretum cf. mkuzense J.D.Carr & Retief RBN 154.2 (JRAU) JF265345 JF270698
Combretaceae Combretum collinum Fresen. subsp. taborense
(Engl. & Diels) OM 1610 (JRAU) JF265346 JF270699
Combretaceae Combretum erythrophyllum (Burch.) Sond. RL 1466 (JRAU) JF265347 JF270700
Combretaceae Combretum hereroense Schinz OM 238 (JRAU) JF265348 JF270701
Combretaceae Combretum imberbe Wawra RBN 336 (JRAU) JF265349 JF270702
Combretaceae Combretum kraussii Hochst. OM 1536 (JRAU) JF265350 JF270703
Combretaceae Combretum microphyllum Klotzsch OM 205 (JRAU) JF265351 JF270704
Combretaceae Combretum molle Engl. & Diels OM 1526 (JRAU) JF265352 JF270705
Combretaceae Combretum mossambicense (Klotzsch) Engl. RL 1537 (JRAU) JF265353 JF270706
Combretaceae Combretum padoides Engl. & Diels OM 1285 (JRAU) JF265354 JF270707
Combretaceae Combretum woodii Dummer OM 1421 (JRAU) JF265355 JF270708
Combretaceae Combretum zeyheri Sond. OM 295 (JRAU) JF265356 JF270709
Combretaceae Pteleopsis myrtifolia Engl. & Diels OM 1283 (JRAU) JF265563 JF270905
149
Combretaceae Terminalia phanerophlebia Engl. & Diels OM 1179 (JRAU) JF265624 JF270966
Combretaceae Terminalia prunioides M.Laws. OM 1061 (JRAU) JF265625 JF270967
Combretaceae Terminalia sericea Burch. ex DC. OM 478 (JRAU) JF265626 JF270968
Ebenaceae Diospyros dichrophylla (Gand.) De Winter OM 1758 (JRAU) JF265388 JF270740
Ebenaceae Diospyros lycioides Desf. OM 965 (JRAU) JF265389 JF270741
Ebenaceae Diospyros mespiliformis Hochst. ex A.DC. OM 218 (JRAU) JF265390 JF270742
Ebenaceae Diospyros natalensis (Harv.) Brenan OM 1763 (JRAU) JF265391 JF270743
Ebenaceae Diospyros villosa (L.) De Winter OM 1575 (JRAU) JF265392 JF270744
Ebenaceae Diospyros whyteana (Hiern) F.White OM 1805 (JRAU) JF265393 JF270745
Ebenaceae Euclea daphnoides Hiern OM 1381 (JRAU) JF265422 JF270771
Ebenaceae Euclea divinorum Hiern OM 1102 (JRAU) JF265418 JF270767
Ebenaceae Euclea natalensis A.DC. OM 211 (JRAU) JF265420 JF270769
Ebenaceae Euclea natalensis A.DC. RL 1166 (JRAU) JF265419 JF270768
Ebenaceae Euclea undulata Thunb. OM 1206 (JRAU) JF265423 JF270772
150
Erythroxylaceae Erythroxylum delagoense Schinz OM 1499 (JRAU) JF265416 JF270765
Erythroxylaceae Erythroxylum emarginatum Thonn. OM 1531 (JRAU) JF265417 JF270766
Euphorbiaceae Acalypha glabrata Thunb. OM 1375 (JRAU) JF265264 JF270621
Euphorbiaceae Alchornea laxiflora Pax & K.Hoffm. RBN 144 (JRAU) JF265282 JF270638
Euphorbiaceae Clutia pulchella L. RBGK 5876 (K) AM234976 —
Euphorbiaceae Croton gratissimus Burch. OM 785 (JRAU) JF265374 JF270727
Euphorbiaceae Croton madandensis S.Moore OM 979 (JRAU) JF265375 —
Euphorbiaceae Croton megalobotrys Müll.Arg. OM 774 (JRAU) JF265376 JF270728
Euphorbiaceae Croton menyharti Pax RL 1503 (JRAU) JF265377 JF270729
Euphorbiaceae Croton pseudopulchellus Pax RBN 186 (JRAU) JF265378 JF270730
Euphorbiaceae Croton steenkampianus Gerstner RBN 364 (JRAU) JF265379 JF270731
Euphorbiaceae Croton sylvaticus Hochst. OM 1550 (JRAU) JF265380 JF270732
Euphorbiaceae Euphorbia cooperi N.E.Br. ex A.Berger OM 1464 (JRAU) JF265425 JF270774
Euphorbiaceae Euphorbia espinosa Pax RBN 189 (JRAU) JF265426 JF270775
151
Euphorbiaceae Euphorbia rowlandii R.A.Dyer RBN 263 (JRAU) JF265427 JF270776
Euphorbiaceae Euphorbia tirucalli L. RBN 274 (JRAU) JF265428 JF270777
Euphorbiaceae Ricinus communis L. OM 1359 (JRAU) JF265575 JF270918
Euphorbiaceae Spirostachys africanus Sond. OM 254 (JRAU) JF265602 JF270944
Euphorbiaceae Suregada africana Kuntze OM 1839 (JRAU) JF265615 JF270957
Euphorbiaceae Synadenium cupulare (Boiss.) Wheeler ex
A.White OM 757 (JRAU) JF265616 JF270958
Fabaceae Acacia ataxacantha DC. OM 1046 (JRAU) JF265242 JF270600
Fabaceae Acacia borleae Burtt Davy OM 314 (JRAU) JF265243 JF270601
Fabaceae Acacia brevispica Harms RL 1333 (JRAU) JF265244 JF270602
Fabaceae Acacia burkei Benth. OM 705 (JRAU) JF265245 —
Fabaceae Acacia caffra Willd. RBN 177 (JRAU) JF265246 JF270603
Fabaceae Acacia davyi N.E.Br. in Burrt-D RL 1315 (JRAU) JF265247 JF270604
Fabaceae Acacia erubescens Welw. ex Oliver OM 780 (JRAU) JF265248 JF270605
152
Fabaceae Acacia exuvialis Verdoorn OM 260 (JRAU) JF265249 JF270606
Fabaceae Acacia gerrardii Benth. RL 1103 (JRAU) JF265250 JF270607
Fabaceae Acacia grandicornuta Gerstner OM 337 (JRAU) JF265251 JF270608
Fabaceae Acacia karroo Hayne RL 1282 (JRAU) JF265252 JF270609
Fabaceae Acacia luederitzii Engl. var. luederitzii RL 1306 (JRAU) JF265253 JF270610
Fabaceae Acacia nigrescens Oliver OM 225 (JRAU) JF265254 JF270611
Fabaceae Acacia nilotica (L.) Delile OM 626 (JRAU) JF265255 JF270612
Fabaceae Acacia robusta Burch. subsp. clavigera (E. Mey.) RBN 354 (JRAU) JF265256 JF270613
Fabaceae Acacia schweinfurthii Brenan & Exell OM 604 (JRAU) JF265257 JF270614
Fabaceae Acacia senegal Willd. OM 255 (JRAU) JF265258 JF270615
Fabaceae Acacia sieberiana DC. OM 966 (JRAU) JF265259 JF270616
Fabaceae Acacia swazica Burtt Davy RL 1327 (JRAU) JF265260 JF270617
Fabaceae Acacia tortilis Hayne OM 261 (JRAU) JF265261 JF270618
Fabaceae Acacia welwitschii Oliver subsp. delagoensis OM 239 (JRAU) JF265262 JF270619
153
(Harms) J.H.Ross & Brenan
Fabaceae Acacia xanthophloea Benth. OM 298 (JRAU) JF265263 JF270620
Fabaceae Adenopodia spicata C.Presl SA 193.5 (JRAU) JF265272 JF270628
Fabaceae Afzelia quanzensis Welw. OM 291 (JRAU) JF265273 JF270629
Fabaceae Albizia adianthifolia W.Wight OM 1811 (JRAU) JF265274 JF270630
Fabaceae Albizia anthelmintica Brongn. OM 363 (JRAU) JF265275 JF270631
Fabaceae Albizia brevifolia Schinz OM 826 (JRAU) JF265276 JF270632
Fabaceae Albizia forbesii Benth. OM 228 (JRAU) JF265277 JF270633
Fabaceae Albizia harveyi Fourn. OM 1402 (JRAU) JF265278 JF270634
Fabaceae Albizia petersiana Oliver OM 745 (JRAU) JF265279 JF270635
Fabaceae Albizia tanganyicensis Baker f. OM 1972 (JRAU) JF265280 JF270636
Fabaceae Albizia versicolor Welw. ex Oliver OM 560 (JRAU) JF265281 JF270637
Fabaceae Baphia massaiensis Taub. RBN 130 (JRAU) JF265298 JF270652
Fabaceae Bauhinia galpinii N.E.Br. OM 279 (JRAU) JF265301 —
154
Fabaceae Bolusanthus speciosus Harms OM 240 (JRAU) JF265305 JF270658
Fabaceae Burkea africana Hook. RBN 235 (JRAU) JF265317 JF270670
Fabaceae Calpurnia aurea (Lam.) Benth. OM 1532 (JRAU) JF265320 JF270673
Fabaceae Cassia abbreviata Oliver OM 235 (JRAU) JF265329 JF270682
Fabaceae Colophospermum mopane (J.Kirk ex Benth.)
J.Léonard OM 778 (JRAU) JF265343 JF270696
Fabaceae Cordyla africana Lour. OM 1210 (JRAU) JF265371 JF270724
Fabaceae Crotalaria laburnifolia L. subsp. australis (Baker
f.) Polhill OM 608 (JRAU) JF265373 JF270726
Fabaceae Dalbergia armata E.Mey. OM 1414 (JRAU) JF265383 JF270735
Fabaceae Dalbergia melanoxylon Guill. & Perr. OM 268 (JRAU) JF265384 JF270736
Fabaceae Dichrostachys cinerea (L.) Wight & Arn. subsp.
africana Brenan & Brummitt RBN 359 (JRAU) JF265387 JF270739
Fabaceae Elephantorrhiza burkii Benth. OM 1635 (JRAU) JF265408 JF270758
155
Fabaceae Elephantorrhiza elephantina Skeels OM 483 (JRAU) JF265409 JF270759
Fabaceae Elephantorrhiza goetzei (Harms) Harms OM 812 (JRAU) JF265410 JF270760
Fabaceae Erythrina humeana Spreng. OM 741 (JRAU) JF265413 JF270763
Fabaceae Erythrina latissima E.Mey. OM 1428 (JRAU) JF265414 —
Fabaceae Erythrina lysistemon Hutch. RBN 329 (JRAU) JF265415 JF270764
Fabaceae Faidherbia albida (Delile) A.Chev. RBN 165 (JRAU) JF265429 JF270778
Fabaceae Guibourtia conjugata (Bolle) J.Léonard OM 1287 (JRAU) JF265457 JF270804
Fabaceae Indigofera fulgens Baker RBN 155 (JRAU) JF265484 JF270831
Fabaceae Indigofera tinctoria L. var. arcuata J.B. Gillett OM 1933 (JRAU) JF265485 JF270832
Fabaceae Mundulea sericea (Willd.) A.Chev. OM 338 (JRAU) JF265522 JF270868
Fabaceae Newtonia hildebrandtii (Vatke) Torre SA 191 (JRAU) — —
Fabaceae Ormocarpum trichocarpum (Taub.) Engl. OM 1437 (JRAU) JF265535 JF270878
Fabaceae Peltophorum africanum Sond. OM 271 (JRAU) JF265546 JF270889
Fabaceae Philenoptera violacea (Klotzsch) Schrire OM 242 (JRAU) JF265547 JF270890
156
Fabaceae Piliostigma thonningii (Schumach.) Milne-Redh. OM 277 (JRAU) JF265551 —
Fabaceae Pseudarthria hookeri Wight & Arn. OM 1473 (JRAU) JF265559 JF270902
Fabaceae Pterocarpus angolensis DC. OM 490 (JRAU) JF265564 JF270906
Fabaceae Pterocarpus rotundifolius Druce RL 1181 (JRAU) JF265565 JF270907
Fabaceae Pterolobium stellatum (Forssk.) Brenan RBN 219 (JRAU) — JF270908
Fabaceae Schotia brachypetala Sond. OM 252 (JRAU) JF265583 JF270926
Fabaceae Schotia capitata Bolle OM 1159 (JRAU) JF265584 JF270927
Fabaceae Senna petersiana (Bolle) Lock OM 987 (JRAU) JF265596 JF270938
Fabaceae Xanthocercis zambesiaca (Baker) Dumaz-le-
Grand OM 500 (JRAU) JF265655 JF270996
Fabaceae Xeroderris stuhlmannii (Taubert) Mendonca &
E.P.deSousa RBN 158 (JRAU) JF265656 JF270997
Fabaceae Xylia torreana Brenan RBN 171 (JRAU) JF265660 JF271001
Gentianaceae Anthocleista grandiflora Gilg OM 262 (JRAU) JF265290 JF270645
157
Hernandiaceae Gyrocarpus americanus Jacq. subsp. africanus
Kubitzki OM 874 (JRAU) JF265465 JF270812
Icacinaceae Apodytes dimidiata E.Mey. ex Arn. OM 1560 (JRAU) JF265292 JF270646
Icacinaceae Cassinopsis ilicifolia (Hochst.) Kuntze OM 1892 (JRAU) JF265330 JF270683
Kirkiaceae Kirkia acuminata Oliver OM 758 (JRAU) JF265492 JF270839
Kirkiaceae Kirkia wilmsii Engl. RL 1230 (JRAU) JF265493 JF270840
Lamiaceae Clerodendrum glabrum E.Mey. OM 768 (JRAU) JF265341 JF270694
Lamiaceae Karomia speciosa (Hutch. & Corbish.) R.Fern. OM 700 (JRAU) JF265489 JF270836
Lamiaceae Leonotis nepetifolia (L.) R.Br. RBN 258 (JRAU) JF265501 JF270848
Lamiaceae Premna mooiensis W.Piep. OM 1424 (JRAU) JF265557 JF270900
Lamiaceae Pycnostachys reticulata (E.Mey.) Benth. OM 1992 (JRAU) JF265567 JF270910
Lamiaceae Tetradenia riparia (Hochst.) Codd OM 881 (JRAU) JF265627 JF270969
Lamiaceae Tinnea rhodesiana S.Moore OM 1303 (JRAU) JF265629 JF270971
Lamiaceae Vitex ferruginea Schumach. & Thonn. RBN 141 (JRAU) JF265650 JF270991
158
Lamiaceae Vitex harveyana H.Pearson OM 528 (JRAU) JF265651 JF270992
Lamiaceae Vitex patula E.A.Bruce OM 1300 (JRAU) JF265652 JF270993
Linaceae Hugonia orientalis Engl. RBN 145 (JRAU) JF265478 JF270825
Loganiaceae Strychnos decussata (Pappe) Gilg OM 292 (JRAU) JF265609 JF270951
Loganiaceae Strychnos madagascariensis Poir. RL 1538 (JRAU) JF265610 JF270952
Loganiaceae Strychnos potatorum L.f. RBN 179 (JRAU) JF265611 JF270953
Loganiaceae Strychnos pungens Solered. MvdB 22 (JRAU) JF265612 JF270954
Loganiaceae Strychnos spinosa Lam. OM 220 (JRAU) JF265613 JF270955
Loganiaceae Strychnos usambarensis Gilg ex Engl. OM 2006 (JRAU) JF265614 JF270956
Lythraceae Galpinia transvaalica N.E.Br. OM 319 (JRAU) JF265443 JF270791
Malpighiaceae Acridocarpus natalitius A.Juss. OM 2034 (JRAU) JF265267 JF270624
Malpighiaceae Triaspis hypericoides Burch. subsp. nelsonii
(Oliv.) OM 1263 (JRAU) JF265632 JF270973
Malvaceae Abutilon angulatum (Guill. & Perr.) Mast. OM 822 (JRAU) JF265241 JF270599
159
Malvaceae Adansonia digitata L. OM 747 (JRAU) JF265268 JF270625
Malvaceae Azanza garckeana (F.Hoffm.) Exell & Hillc. OM 1865 (JRAU) JF265294 JF270648
Malvaceae Dombeya cymosa Harv. OM 898 (JRAU) JF265395 JF270747
Malvaceae Dombeya rotundifolia Planch. RL 1161 (JRAU) JF265396 JF270748
Malvaceae Gossypium herbaceum L. OM 907 (JRAU) JF265447 JF270794
Malvaceae Grewia bicolor Juss. OM 329 (JRAU) JF265448 JF270795
Malvaceae Grewia caffra Meisn. RBN 182 (JRAU) JF265449 JF270796
Malvaceae Grewia flavescens Juss. OM 323 (JRAU) JF265450 JF270797
Malvaceae Grewia gracillima Wild OM 870 (JRAU) JF265451 JF270798
Malvaceae Grewia hexamita Burret OM 351 (JRAU) JF265452 JF270799
Malvaceae Grewia inaequilatera Garcke OM 872 (JRAU) JF265453 JF270800
Malvaceae Grewia microthyrsa K.Schum. ex Burret OM 1286 (JRAU) — —
Malvaceae Grewia monticola Sond. OM 1954 (JRAU) JF265454 JF270801
Malvaceae Grewia sulcata Mast. OM 871 (JRAU) JF265455 JF270802
160
Malvaceae Grewia villosa Willd. OM 392 (JRAU) JF265456 JF270803
Malvaceae Hibiscus calyphyllus Cav. OM 381 (JRAU) JF265473 JF270820
Malvaceae Hibiscus micranthus L.f. OM 435 (JRAU) JF265474 JF270821
Malvaceae Sterculia murex Hemsl. RL 1229 (JRAU) JF265605 JF270947
Malvaceae Sterculia rogersii N.E.Br. OM 1227 (JRAU) JF265606 JF270948
Malvaceae Triumfetta pilosa Roth RBN 231 (JRAU) JF265638 JF270979
Meliaceae Ekebergia capensis Sparrm. OM 1540 (JRAU) — JF270756
Meliaceae Ekebergia pterophylla (C. DC.) Hofmeyr OM 2017 (JRAU) JF265406 —
Meliaceae Entandrophragma caudatum Sprague OM 794 (JRAU) JF265412 JF270762
Meliaceae Trichilia dregeana Harv. & Sond. OM 1793 (JRAU) JF265635 JF270976
Meliaceae Trichilia emetica Vahl OM 1178 (JRAU) JF265636 JF270977
Meliaceae Turraea floribunda Hochst CS 21 (JRAU) JF265639 JF270980
Meliaceae Turraea nilotica Kotschy & Peyr. OM 1497 (JRAU) JF265640 JF270981
Meliaceae Turraea obtusifolia Hochst. OM 744 (JRAU) JF265641 JF270982
161
Melianthaceae Bersama lucens Szyszył. OM 1562 (JRAU) JF265304 JF270657
Moraceae Ficus abutilifolia Miq. OM 280 (JRAU) — —
Moraceae Ficus burkei Miq. OM 972 (JRAU) JF265432 JF270781
Moraceae Ficus glumosa Delile RL 1407 (JRAU) JF265433 —
Moraceae Ficus ingens Miq. OM 593 (JRAU) JF265434 JF270782
Moraceae Ficus petersii Warb. OM 1850 (JRAU) JF265435 JF270783
Moraceae Ficus salicifolia Vahl OM 1981 (JRAU) JF265436 JF270784
Moraceae Ficus stuhlmannii Warb. OM 749 (JRAU) JF265437 JF270785
Moraceae Ficus sur Forssk. OM 1556 (JRAU) JF265438 JF270786
Moraceae Ficus sycomorus L. OM 485 (JRAU) JF265439 JF270787
Moraceae Ficus tettensis Hutchinson OM 1354 (JRAU) JF265440 JF270788
Moraceae Maclura africana (Bur.) Corner OM 1935 (JRAU) JF265506 JF270852
Myricaceae Myrica pilulifera Rendle OM 2024 (JRAU) JF265521 JF270867
Myrtaceae Eugenia natalitia Sond. OM 1796 (JRAU) JF265424 JF270773
162
Myrtaceae Heteropyxis natalensis Harv. OM 559 (JRAU) JF265471 JF270818
Myrtaceae Syzygium cordatum Hochst. ex C.Krauss RBN 304 (JRAU) JF265617 JF270959
Myrtaceae Syzygium guineense (Willd.) DC. OM 204 (JRAU) — JF270960
Ochnaceae Ochna inermis (Forssk.) Schweinf. OM 1196 (JRAU) JF265529 —
Ochnaceae Ochna natalitia Walp. OM 286 (JRAU) JF265530 —
Ochnaceae Ochna pulchra Hook. RBN 307 (JRAU) JF265531 —
Olacaceae Olax dissitiflora Oliver OM 970 (JRAU) JF265532 JF270875
Olacaceae Ximenia americana L. OM 1185 (JRAU) JF265658 JF270999
Olacaceae Ximenia caffra Sond. OM 263 (JRAU) JF265659 JF271000
Oleaceae Chionanthus foveolatus (Meyer) Stearn OM 1832 (JRAU) JF265336 JF270689
Oleaceae Chionanthus peglerae (C.H.Wright) Stearn OM 1766 (JRAU) JF265337 JF270690
Oleaceae Jasminum fluminense Vell. OM 456 (JRAU) JF265486 JF270833
Oleaceae Jasminum multipartitum Hochst. OM 1541 (JRAU) JF265487 JF270834
Oleaceae Jasminum stenolobum Rolfe OM 1325 (JRAU) JF265488 JF270835
163
Oleaceae Olea europaea L. subsp. africana (Mill.)
P.S.Green OM 269 (JRAU) JF265533 JF270876
Oleaceae Schrebera alata Welw. OM 318 (JRAU) JF265585 JF270928
Onagraceae Ludwigia octovalvis (Jacq.) P.H.Raven OM 213 (JRAU) JF265505 —
Passifloraceae Adenia spinosa Burtt Davy OM 1618 (JRAU) JF265269 —
Passifloraceae Paropsia braunii Gilg — DQ123395 —
Pedaliaceae Sesamothamnus lugardii N.E.Br. ex Stapf OM 1622 (JRAU) JF265597 JF270939
Phyllanthaceae Antidesma venosum E.Mey. ex Tul. OM 808 (JRAU) JF265291
Phyllanthaceae Bridelia cathartica Bertol.f. OM 294 (JRAU) JF265314 JF270667
Phyllanthaceae Bridelia micrantha Baill. OM 1435 (JRAU) JF265315 JF270668
Phyllanthaceae Bridelia mollis Hutchinson OM 1632 (JRAU) JF265316 JF270669
Phyllanthaceae Flueggea virosa (Willd.) Royle OM 1145 (JRAU) JF265442 JF270790
Phyllanthaceae Hymenocardia ulmoides Oliver RBN 178 (JRAU) JF265479 JF270826
Phyllanthaceae Margaritaria discoidea subsp. nitida (Pax) OM 1922 (JRAU) JF265515 JF270861
164
G.L.Webster
Phyllanthaceae Phyllanthus pinnatus (Wight) G.L.Webster OM 843 (JRAU) JF265549 JF270892
Phyllanthaceae Phyllanthus reticulatus Poir. OM 224 (JRAU) JF265550 JF270893
Phyllanthaceae Pseudolachnostylis maprouneaefolia Pax RBN 100 (JRAU) JF265560 —
Picrodendraceae Androstachys johnsonii Prain OM 1912 (JRAU) JF265287 —
Pittosporaceae Pittosporum viridiflorum Sims OM 1784 (JRAU) JF265552 JF270894
Plumbaginaceae Plumbago auriculata Lam. OM 1686 (JRAU) — JF270896
Plumbaginaceae Plumbago zeylanica L. RBN 352 (JRAU) JF265554 JF270897
Polygalaceae Securidaca longipedunculata Fresen. OM 1965 (JRAU) JF265595 —
Portulacaceae Portulacaria afra Jacq. OM 1257 (JRAU) JF265555 JF270898
Primulaceae Maesa lanceolata Forssk. OM 2020 (JRAU) JF265513 JF270859
Proteaceae Faurea rochetiana Chiov. ex Pic.Serm. OM 1413 (JRAU) JF265430 JF270779
Proteaceae Faurea saligna Harv. MvdB 27 (JRAU) JF265431 JF270780
Putranjavaceae Drypetes gerrardii Hutch. OM 1840 (JRAU) JF265399 —
165
Putranjavaceae Drypetes reticulata Pax RBN 270 (JRAU) JF265400 JF270750
Ranunculaceae Clematis brachiata Thunb. OM 1974 (JRAU) JF265340 JF270693
Rhamnaceae Berchemia discolor Hemsl. OM 1175 (JRAU) JF265302 JF270655
Rhamnaceae Berchemia zeyheri (Sond.) Grubov OM 600 (JRAU) JF265303 JF270656
Rhamnaceae Helinus integrifolius (Lam.) Kuntze OM 2015 (JRAU) JF265469 JF270816
Rhamnaceae Rhamnus prinoides L'Hér. OM 1744 (JRAU) JF265570 JF270913
Rhamnaceae Ziziphus mucronata Willd. OM 258 (JRAU) JF265666 JF271007
Rhamnaceae Ziziphus rivularis Codd OM 1383 (JRAU) JF265667 JF271008
Rubiaceae Breonadia salicina (Vahl) Hepper & J.R.I.Wood RL 1194 (JRAU) JF265313 JF270666
Rubiaceae Canthium inerme Kuntze OM 1742 (JRAU) JF265321 JF270674
Rubiaceae Canthium setiflorum Hiern OM 882 (JRAU) JF265322 JF270675
Rubiaceae Catunaregam spinosa (Thunb.) Tirveng. OM 1406 (JRAU) JF265332 JF270685
Rubiaceae Cephalanthus natalensis Oliver OM 1583 (JRAU) JF265334 JF270687
Rubiaceae Coddia rudis (E.Mey. ex Harv.) Verdc OM 1292 (JRAU) JF265342 JF270695
166
Rubiaceae Crossopteryx febrifuga Benth. OM 1924 (JRAU) JF265372 JF270725
Rubiaceae Gardenia resiniflua Hiern OM 864 (JRAU) JF265445 JF270792
Rubiaceae Gardenia volkensii K. Schum. OM 1100 (JRAU) JF265446 JF270793
Rubiaceae Heinsia crinita (Afzel.) G.Taylor RBN 129 (JRAU) JF265468 JF270815
Rubiaceae Hymenodictyon parvifolium Oliver OM 789 (JRAU) JF265480 JF270827
Rubiaceae Hyperacanthus amoenus (Sims) Bridson OM 1457 (JRAU) JF265481 JF270828
Rubiaceae Kraussia floribunda Harv. OM 924 (JRAU) JF265494 JF270841
Rubiaceae Lagynias dryadum Robyns OM 896 (JRAU) JF265495 JF270842
Rubiaceae Leptactina delagoensis K.Schum. OM 1598 (JRAU) JF265502 JF270849
Rubiaceae Pavetta catophylla K.Schum. OM 1103 (JRAU) JF265542 JF270885
Rubiaceae Pavetta edentula Sond. OM 1431 (JRAU) JF265543 JF270886
Rubiaceae Pavetta lanceolata Eckl. OM 2001 (JRAU) JF265544 JF270887
Rubiaceae Pavetta schumanniana F.Hoffm. ex K.Schum. RBN 251 (JRAU) JF265545 JF270888
Rubiaceae Plectroniella amata Robyns OM 962 (JRAU) JF265553 JF270895
167
Rubiaceae Psydrax locuples (K.Schum.) Bridson OM 1639 (JRAU) JF265561 JF270903
Rubiaceae Pyrostria hystrix (Bremek.) Bridson OM 234 (JRAU) JF265568 JF270911
Rubiaceae Rothmannia fischeri (K.Schum.) Bullock in
Oberm. OM 888 (JRAU) JF265576 JF270919
Rubiaceae Tarenna supra-axillaris (Hemsl.) Bremek. OM 1951 (JRAU) JF265620 JF270962
Rubiaceae Tarenna zygoon Bridson OM 1908 (JRAU) JF265621 JF270963
Rubiaceae Tricalysia junodii (Schinz) Brenan var. junodii OM 1399 (JRAU) JF265633 JF270974
Rubiaceae Tricalysia lanceolata Burtt Davy OM 1765 (JRAU) JF265634 JF270975
Rubiaceae Vangueria infausta Burch. OM 377 (JRAU) JF265644 JF270985
Rubiaceae Vangueria madagascariensis J.F. Gmel. OM 2018 (JRAU) JF265645 JF270986
Rutaceae Calodendrum capensis Thunb. OM 1540 (JRAU) JF265319 JF270672
Rutaceae Clausena anisata (Willd.) Hook. f. ex Benth. Logie C. FBG 67 (NBG) AM235116 —
Rutaceae Ptaeroxylon obliquum Radlk. OM 815 (JRAU) JF265562 JF270904
Rutaceae Teclea pilosa Verdoorn OM 359 (JRAU) JF265622 JF270964
168
Rutaceae Toddaliopsis bremekampii Verdoorn RBN 366 (JRAU) JF265630 —
Rutaceae Vepris lanceolata (Lam.) G.Don OM 1528 (JRAU) JF265646 JF270987
Rutaceae Vepris reflexa Verdoorn OM 244 (JRAU) JF265647 JF270988
Rutaceae Zanthoxylum capense Harv. OM 1775 (JRAU) JF265663 JF271004
Rutaceae Zanthoxylum humile (E.A.Bruce) Waterman OM 431 (JRAU) JF265664 JF271005
Rutaceae Zanthoxylum leprieurii Guill. & Perr. RBN 152 (JRAU) JF265665 JF271006
Salicaceae Dovyalis caffra Warb. OM 349 (JRAU) JF265397 JF270749
Salicaceae Flacourtia indica (Burm.f.) Merr. OM 581 (JRAU) JF265441 JF270789
Salicaceae Homalium dentatum Warb. OM 1508 (JRAU) JF265477 JF270824
Salicaceae Oncoba spinosa Forssk. OM 631 (JRAU) JF265534 JF270877
Salicaceae Salix mucronata Thunb. OM 1198 (JRAU) JF265580 JF270923
Salicaceae Scolopia zeyheri (Nees) Harv. OM 1552 (JRAU) JF265587 JF270930
Salicaceae Trimeria grandifolia (Hochst.) Warb. OM 1549 (JRAU) JF265637 JF270978
Salvadoraceae Azima tetracantha Lam. OM 300 (JRAU) JF265295 JF270649
169
Salvadoraceae Salvadora australis Schweick. OM 1317 (JRAU) JF265581 JF270924
Salvadoraceae Salvadora persica L. OM 824 (JRAU) JF265582 JF270925
Sapindaceae Allophylus decipiens Radlk. OM 1846 (JRAU) JF265283 JF270639
Sapindaceae Deinbollia oblongifolia Radlk. OM 1774 (JRAU) JF265385 JF270737
Sapindaceae Deinbollia xanthocarpa Radlk. RBN 275 (JRAU) JF265386 JF270738
Sapindaceae Hippobromus pauciflorus Radlk. OM 1551 (JRAU) JF265475 JF270822
Sapindaceae Pappea capensis Eckl. & Zeyh. OM 380 (JRAU) JF265540 JF270883
Sapindaceae Stadmannia oppositifolia Lam. OM 863 (JRAU) JF265603 JF270945
Sapotaceae Englerophytum magalismontanum (Sonder)
T.D.Penn. RBN 290 (JRAU) JF265411 JF270761
Sapotaceae Manilkara concolor (Harv.) Gerstner RL 1218 (JRAU) — —
Sapotaceae Manilkara mochisia Dubard OM 1392 (JRAU) JF265514 JF270860
Sapotaceae Manilkara sp OM 1271 (JRAU) —
Sapotaceae Mimusops zeyheri Sond. OM 1220 (JRAU) JF265519 JF270865
170
Sapotaceae Sideroxylon inerme L. OM 1760 (JRAU) JF265598 JF270940
Solanaceae Nicotiana glauca Graham OM 2010 (JRAU) JF265524 JF270870
Solanaceae Solanum catombelense Peyr. OM 934 (JRAU) JF265599 JF270941
Solanaceae Solanum lichtensteinii Willd. OM 1904 (JRAU) JF265600 JF270942
Solanaceae Solanum panduriforme Dunal OM 326 (JRAU) JF265601 JF270943
Stilbaceae Halleria lucida L. CS 16 (JRAU) JF265466 JF270813
Stilbaceae Nuxia congesta R.Br. OM & MvdB 52 (JRAU) JF265525 JF270871
Stilbaceae Nuxia floribunda Benth. OM 2025 (JRAU) JF265526 JF270872
Stilbaceae Nuxia oppositifolia Benth. OM 206 (JRAU) JF265527 JF270873
Ulmaceae Chaetachme aristata Planch. OM 275 (JRAU) JF265335 JF270688
Urticaceae Obetia tenax (N.E.Br.) Friis OM 1416 (JRAU) JF265528 JF270874
Urticaceae Pouzolzia mixta Solms OM 572 (JRAU) JF265556 JF270899
Velloziaceae Xerophyta retinervis Baker OM 516 (JRAU) JF265657 JF270998
Verbenaceae Duranta erecta L. OM 939 (JRAU) JF265401 JF270751
171
Verbenaceae Lantana camara L. OM 739 (JRAU) JF265499 JF270846
Verbenaceae Lantana rugosa Thunb. OM 1238 (JRAU) JF265500 JF270847
Verbenaceae Lippia javanica Spreng. OM 215 (JRAU) JF265503 JF270850
Vitaceae Cissus cactiformis Gilg OM 594 (JRAU) JF265338 JF270691
Vitaceae Cissus cornifolia Planch. OM 1110 (JRAU) JF265339 JF270692
Vitaceae Rhoicissus revoilii Planch. OM 1258 (JRAU) JF265572 JF270915
Vitaceae Rhoicissus tomentosus (Lam.) Wild &
R.B.Drumm. OM 1546 (JRAU) JF265573 JF270916
Vitaceae Rhoicissus tridentata subsp. cuneifolia (Eckl. &
Zeyh.) N.R.Urton OM 249 (JRAU) JF265574 JF270917
172
Supplementary Table S2. Values of NRI in 110 KNP-plots, with indication of
plot labels; (A-P) indicate ecozones where the plots were laid out), and p-
values.
Plots NRI p-values

A1 2.119855 0.03*
A2 1.685609 0.056 NS
A3 3.583059 0.005**
A4 3.209846 0.009**
A5 1.889003 0.04*
A6 1.251039 0.106 NS
A7 3.234434 0.007**
A8 1.541846 0.065 NS
B1 0.764178 0.204 NS
B2 2.177118 0.028*
B3 0.312845 0.339 NS
B4 2.415209 0.022*
B5 2.889419 0.008**
B6 0.823867 0.176 NS
B7 -0.02045 0.486 NS
B8 1.994717 0.033*
B9 1.607806 0.056 NS
C1 3.130329 0.01*
C2 2.692955 0.014*
C3 3.477835 0.005**
C4 1.480792 0.069 NS
C5 1.387529 0.082 NS
C6 3.799116 0.005**
D1 1.97448 0.035*
D2 1.557799 0.064 NS
D3 2.164704 0.021*
D4 1.400358 0.082 NS
D5 1.658455 0.06 NS
D6 3.258605 0.002**
D7 1.50431 0.07 NS
D8 3.424889 0.002**
D9 0.141103 0.42 NS
D10 2.40758 0.02*
D11 2.071436 0.041*
D12 3.56253 0.001**
D13 3.780273 0.002**
D14 2.071787 0.032*
E1 4.370929 0.001**
E2 3.203047 0.005**
E3 1.444869 0.076 NS
173
E4 3.266814 0.004**
E5 1.17905 0.124 NS
E6 1.759509 0.056 NS
F1 1.077502 0.135 NS
F2 1.590732 0.066 NS
F3 0.060194 0.462 NS
F4 1.291868 0.106 NS
F5 1.493413 0.07 NS
F6 0.658327 0.202 NS
F7 0.9793 0.141 NS
F8 2.108971 0.036*
F9 2.960389 0.006**
F10 2.302632 0.022*
F11 2.151061 0.034*
F12 2.089669 0.034*
F13 2.15774 0.027*
G1 3.613605 0.001**
G2 3.468257 0.002**
G3 2.554069 0.018*
G4 3.329771 0.004**
G5 1.961138 0.033*
I1 2.423625 0.022*
I2 0.34229 0.363 NS
I3 2.669247 0.018*
I4 1.15163 0.11 NS
I5 0.167753 0.43 NS
I6 1.934234 0.043*
I7 2.189815 0.029*
J1 3.75438 0.006**
J2 2.571347 0.008**
J3 2.489878 0.016*
K1 2.799909 0.007**
K2 2.69683 0.018*
K3 1.130086 0.124 NS
K4 2.77477 0.015*
K5 3.170609 0.012*
L1 4.021254 0.004**
L2 2.864477 0.011*
L3 2.423077 0.021*
L4 1.950028 0.046*
L5 2.433123 0.032*
L6 -0.58905 0.744 NS
L7 0.131402 0.388 NS
L8 2.103888 0.034*
L9 2.058029 0.036*
L10 0.194093 0.405 NS
L11 1.298553 0.101 NS
L12 0.585283 0.252 NS
174
L13 1.203987 0.107 NS

L14 -0.26139 0.589 NS
L15 2.294206 0.017*
M1 1.920008 0.037*
M2 3.205931 0.009**
M3 1.429129 0.069 NS
N1 1.029717 0.139 NS
N2 0.339476 0.345 NS
N3 0.739511 0.194 NS
N4 0.217091 0.395 NS
N5 -1.42182 0.926 NS
N6 1.674839 0.057 NS
N7 0.405026 0.301 NS
N8 2.423483 0.022*
O1 1.662468 0.047*
O2 1.772225 0.049*
O3 -0.32367 0.621 NS
O4 3.087537 0.008**
O5 1.056014 0.141 NS
P1 0.253312 0.396 NS
P2 2.144656 0.024*
P3 3.832837 0.004**
175
Appendix: Submitted Paper currently under review
176
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Thesis · May 2012

The user has requested enhancement of the downloaded file.

Thesis submitted in fulfilment of the requirements for the degree

Supervisor: Prof. Michelle van der Bank

Co-supervisor: Prof. Vincent Savolainen

within, unless otherwise stated, is my own

Chapter 1- General introduction…………………………………………………..1

1.1. Features of tropical savanna………………………………………………….1

1.2. Role of fire in savanna ecology……………………………………………….3

1.3. Importance of herbivory in savanna ecology………………………………..3

2. Community ecology in a savanna context……………………………………..4

2.1. Theories of tree-grass coexistence…………………………………………..4

2.2. Tree-tree coexistence………………………………………………………….5

3. Phylogenetic investigation of community assembly…………………………..6

3.1. The use of DNA barcoding techniques to reconstruct phylogenetic

3.2. Rationale of phylogenetic approach in ecology……………………………..7

3.3. Framework in community phylogenetics…………………………………….8

3.4. Emerging patterns in community phylogenetics…………………………..10

4. Study site and objectives of the study………………………………………...12

4.1. Study site………………………………………………………………………12

4.3. Outline of the thesis…………………………………………………………..19

using DNA barcodes…………………….………………………………………...23

2. Materials and methods………………………………………………………..25

2.1. Sample collection…………………………………………………………….25

2.2. DNA extraction, PCR and sequencing……………………………………..25

2.3. Sequence alignment………………………………………………………….27

2.4. Tree reconstruction…………………………………………………………...28

3.1. Tree statistics……………………………………………………………….29

3.2. Phylogeny of trees and shrubs of the KNP……………………………...30

4.1. Clade 1: Fabidae…………………………………………………………...48

4.2. Clade 2: Malvidae………………………………………………………….50

4.3. Clade 3: Vitales…………………………………………………………….52

4.4. Clade 4: Santalales………………………………………………………..52

4.5. Clade 5: Lamiidae………………………………………………………….53

4.6. Clade 6: Campanulidae……………………………………………………55

4.7. Clade 7: Ericales…………………………………………………………...55

4.8. Clade 8: Caryophyllales…………………………………………………...56

4.9. Clade 9: Basal Eudicots…………………………………………………..56

4.10. Clade 10: Magnoliidae…………………………………………………….57

4.11. Clade 11: Monocotyledoneae…………………………………………….57

Chapter 3- Testing suitability of evolutionary models using traits of woody

plants in the KNP…………………………………………………………………..59

2. Materials and methods….…………………………………………………….61

2.1. Plant ecological traits………………………………………………………61

2.2. Data collection and measurements………………………………………63

2.3. Data analysis……………………………………………………………….64

Chapter 4- Characterising diversity and phylogenetic structure of woody plant

communities in the Kruger National Park, South Africa………………………..75

2. Materials and methods………………………………………………………...77

2.2. Data analysis……………………………………………………………….78

3.1. Overall diversity and community structure in the KNP.………………..82

3.2. Community phylogenetic structure within and among sites…………...84

3.3. Community trait-based structure within and among sites……………..86

Chapter 5- The role of megaherbivores in shaping the structure of subtropical

2. Materials and methods………………………………………………………..94

2.1. Study site: exclosures……………………………………………………..94

2.2. Traits of anti-herbivores defences………………………………………..96

2.3. Community sampling in the exclosures………………………………….96

2.4. Statistical analyses………………………………………………………...97

4.1. Exclusion of megaherbivores and plant diversity………………………..104

4.2. Exclusion of megaherbivores and phylogenetic diversity………………105

Chapter 6- General conclusion…..…………………………………………….108