See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/267483040

Plant ecophysiological diversity

Chapter · September 2014

DOI: 10.1093/acprof:oso/9780199679584.003.0011

CITATIONS READS

18 316

5 authors, including:

Michael D Cramer Adam Gerard West

University of Cape Town University of Cape Town
174 PUBLICATIONS   5,823 CITATIONS    84 PUBLICATIONS   5,870 CITATIONS   

SEE PROFILE SEE PROFILE

Simon C. Power Robert Skelton

The Ohio State University South African Environmental Observation Network - Fynbos Node
15 PUBLICATIONS   98 CITATIONS    29 PUBLICATIONS   511 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Assessment of floristics and ecosystem risk in Banksia woodlands of the Swan Coastal Plain. View project

Plant species richness, turnover & environmental heterogeneity in the Cape and SW Australia View project

All content following this page was uploaded by Michael D Cramer on 02 June 2015.

The user has requested enhancement of the downloaded file.

 C h a pt er 11
Plant ecophysiological diversity
Michael D. Cramer, Adam G. West, Simon C. Power, Robert Skelton,
and William D. Stock
11.1 Introduction
The world’s mediterranean-type climate regions sup-
port anomalously rich floristic diversity when com-
pared to predictions from global empirical models
incorporating diverse abiotic predictors. Although
these models explain c.70% of variation in global plant
species richness, they underestimate the species rich-
ness of the Cape Floristic Region (CFR) by half (Kreft
and Jetz 2007). The spectacular failure of these models
indicates a role for factors other than current climate,
topography, and productivity in determining the plant
species richness of the CFR. An alternative hypothesis
invokes long-term climatic and geological stability, and
associated low extinction rates (Chapter  5, Cowling
and Lombard 2002; Sniderman et al. 2013). The quartz-
itic mountainous landscapes of the Cape Fold Belt, for
example, are ancient, originating in the Cretaceous and
remaining stable through the Cenozoic (Chapter  2).
While the contemporary summer-arid climate of the
western CFR is somewhat younger, it is nevertheless
old, having been in place probably since the Late Mio-
cene (Linder 2003; Dupont et al. 2011). In the context
of this long-term environmental stability, much of the
contemporary richness of the Cape flora is thought to
have accumulated gradually, over long periods of time
(Chapter 5, Linder 2005, 2008). Crucially, much of the
CFR appears to have been buffered against the dra-
matic climate fluctuations of the Pleistocene (Cowling
and Lombard 2002; Sniderman et al. 2013), resulting in
low rates of extinction and facilitating the survival of
previously accumulated species diversity (Chapter 5,
Dynesius and Jansson 2000).
Functional specialization and associated niche
segregation is likely to facilitate the maintenance of
­diversity over long periods of time (Naeem et al. 1994;
Cowling and Lombard 2002; Finke and Snyder 2008).
Fynbos: Ecology, Evolution, and Conservation of a Megadiverse Region. Edited by Nicky Allsopp,
Jonathan F. Colville and G. Anthony Verboom. © Oxford University Press 2014.
Published 2014 by Oxford University Press.
9780199679584-Allsopp.indb 248
In this context, the potential antiquity of the Cape flora
identifies a key role for ecophysiological trait speciali-
zation in explaining Cape floristic diversity. This has,
in our view, been underappreciated. Approximately
half of all species in the CFR are concentrated in 33
lineages (Linder 2003), suggesting that ­understanding
the coexistence of closely related species has the poten-
tial to provide unique insights into the maintenance of
Cape floristic diversity (Chapter 9). For example, low
levels of coexistence amongst closely related species,
together with evidence of phylogenetic trait conserva-
tism, have been interpreted as a signature of interspe-
cific competition (Slingsby and Verboom 2006). Results
such as these suggest an important role for functional
divergence in facilitating coexistence, and thus in
­determining community composition. Species turno-
ver between communities is often also associated with
ecophysiological specialization, as a consequence of
adaptation to contrasting abiotic (e.g. climatic, ­edaphic,
and fire) and emergent biotic conditions. Despite
­numerous ecophysiological specializations being doc-
umented in the Cape flora, the question of how these
vary within communities and across ­environmental
gradients, and contribute to the maintenance of spe-
cies richness, has received little attention.
Two principal axes of abiotic environmental vari-
ation promote ecophysiological specialization, and
­associated niche segregation, in the Cape flora. Firstly,
the mediterranean-climate regime, characterized by
hot, dry conditions in summer, and cool, wet condi-
tions in winter, is developed to a variable degree
across the ­region. The winter rainfall regime is most
pronounced in the western part of the CFR, becoming
increasingly aseasonal towards the east. Importantly,
these winter rainfall conditions are accompanied by
a light regime in which energy availability is highest
during the drier summers. Secondly, highly leached
22/08/14 10:32 AM

nutrient deficient soils are interspersed with more
nutrient-rich granite-, limestone-, and shale-derived
soils. We postulate that both diminished and variable
resource availability contributes to the availability of
niches and promotes diversity. In addition, flamma-
bility is an important emergent property of fynbos
vegetation (Midgley 2013), which imposes additional
ecophysiological constraints and opportunities.
Here we explore the ecophysiological diversity of
Cape plants, mostly in the CFR but also in the Greater
Cape Floristic Region (GCFR), arguing that significant
niche segregation promotes coexistence in the region
and facilitates the maintenance of s­ pecies ­diversity (i.e.
combined α and β richness). We examine several key
ecophysiological specializations required to overcome
the environmental constraints of the r­egion and show
how different species have separated out along axes
Box 11.1  Common specializations in Cape plants
Cluster roots
Cluster roots, which are common in plants inhabiting sandy
fynbos soils, are dense clusters of rootlets of determinate
growth (terminal), produced along an elongating root axis.
These structures are common in Proteaceae (Lamont 1972),
with analogous structures being found in Cyperaceae (dau-
ciform roots), Restionaceae (capillaroid roots), Fagales, Cu-
curbitaceae, Rosales, and Fabaceae (Lambers et al. 2006).
Here, we collectively term these structures ‘cluster roots’.
Cluster roots vary from small (<1 cm diameter) collections of
root hairs (i.e. dauciform) to large (>5 cm diameter) complex
structures (Lambers et al. 2008). Cluster roots proliferate in a
restricted volume of soil and solubilize phosphorus (P) from
mineral complexes through the release of carboxylates (e.g.
citrate and malate) and acid/alkaline phosphatases, which
hydrolyse organic P complexes (Grierson and Comerford
2000) improving access to both mineral and organic P forms.
As a consequence cluster roots can consume ­between 52%
and 100% of daily photosynthate (Lambers et al. 2006),
although carbon is unlikely to be limiting in open habitats
within the CFR (Stock and Allsopp 1992).
Mycorrhizal symbioses
Mycorrhizal symbioses occur in 86% of terrestrial species,
with arbuscular mycorrhizal symbioses probably being the
ancestral mode of P acquisition for plants (Brundrett 2009).
Within the CFR flora, a smaller proportion of species is
mycorrhizal (72%), 62% having arbuscular, 8% ericoid,
­ Small leaf size
and 2% orchid mycorrhizas (there are no indigenous ecto-
mycorrhizal species), the remainder being non-mycorrhizal
9780199679584-Allsopp.indb 249
P l a nt ec o ph ysi o l o gic a l diversit y    249
of available niches. ­Additionally, we comment on how
ecophysiological ­ specialization may have resulted in
­reduced phenotypic plasticity of Cape plants, with impli-
cations for coexistence and the maintenance of diversity
(Lortie and Aarssen 1996). Given the many ecophysi-
ological specializations found in the Cape fl ­ ora, ­future
changes in climate and nutrients (i.e. a­nthropogenic
deposition) may present a significant threat to the per-
sistence of this flora. Finally, we discuss how, in contrast
to the indigenous flora, highly plastic a­lien invaders
­(Morris et al. 2011) may be better equipped to r­ espond to
such environmental changes, promoting their success.
Since fynbos and southwestern ­ Australian kwongan
share similar selective regimes of infertile soils, ­recurrent
fire, and winter rainfall (e.g. Milewski 1983), we fre-
quently refer to evidence from the kwongan in support
of ecophysiological properties of the fynbos.
(­Chapter 10). Moreover, the incidence of mycorrhizas is
lower in fynbos than in the more nutrient-rich strandveld
and renosterveld vegetation types (Allsopp and Stock 1994).
Indeed, the ­diversity of mycorrhizal symbioses and their
­nutritional functions (Table 11.1) may play an important
role in d­ etermining the species composition of communities
­(Klironomos et al. 2011). Mycorrhizal hyphae increase the
volume of soil from which nutrients can be scavenged, the
latter being transported over relatively long distances (up to
0.25 m). The ­nutritional role of mycorrhizas incurs a carbon
cost, commonly accounting for 10% of the carbon utilized
by roots (Fitter 1991), although P is more likely to be limit-
ing than carbon in open habitats with the CFR (Stock and
Allsopp 1992).
Sclerophyllous leaves
Sclerophyllous leaves are leathery and long lived (Schimper
1903), thus reducing nutrient losses associated with senes-
cence and herbivory, and possibly provide a degree of wa-
ter stress resistance (see 11.3.2). Sclerophylly is commonly
­associated with low specific leaf area (SLA <10 m2 kg−1;
Yates et al. 2010). Although the leaves of many CFR species
are highly sclerophyllous and long lived (up to 8 yr; M­ idgley
and Enright 2000) and thus more carbon and nutrient
‘­expensive’ to produce than deciduous leaves, they amortize
their costs over longer periods of time (Stock et al. 1997).
Small leaf size epitomizes ‘fynbos’, the principal fine-leaved
vegetation type of the CFR (Cowling and Holmes 1992), and
continued
22/08/14 10:32 AM
 250   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n

Box 11.1  Continued

Table 11.1  Taxonomic distributions and nutrient acquisition properties of root specializations in Cape plants. The specializations are scored
as effective (+), ineffective (−), or unknown (?) for whether they exude carboxylates for extraction of mineral-bound P and whether they are
known to access inorganic N, organic N, inorganic P, organic P, or other nutrients. Superscript numbers indicate references.

Dauciform roots Cluster roots/ Arbuscular Ericoid Orchid mycorrhizas

capillaroid roots mycorrhizas mycorrhizas

Main plant families Cyperaceae Proteaceae Widespread Ericaceae Orchidaceae

Restionaceae
Fabaceae
Myricaceae
Carboxylates +1 +3 −7 ? ?
Inorganic N +1 +4 +8 +10 +7
Organic N ? +5 +9 +10 +8
Inorganic P +1 +6 +7 +10 +7
Organic P +2 +6 −7 +10 +11
Other nutrients Cu, Zn, NH4+1 Mn, Fe, Zn, Cu6 Cu, Zn, possibly K7 Fe, C7 C7

1
Shane et al. (2006) Plant, Cell Environment, 29, 1989–99; 2 Playsted et al. (2006) New Phytologist, 170, 491–500; 3 Lambers et al. (2006) Annals of Botany,
98, 693–713; 4 Pate et al. (1993) Plant and Soil, 155, 273–76; 5 Hawkins et al. (2005) Annals of Botany, 96, 1275–82; 6 Shane et al. (2005) Plant and Soil, 274,
101–25; 7 Smith et al. (2002) Mycorrhizal symbiosis (2nd edition). Academic Press, London; 8 Ames et al. (1983) New Phytologist, 95, 381–96; 9 Hodge et al.
(2001) Nature, 413, 297–99; 10 Read (1996) Annals of Botany, 77, 365–74; 11 Antibus et al. (1990) Plant and Soil, 128, 233–40.

is also common in the renosterveld vegetation of the CFR.
­Although small leaf size has often been linked to sclero-
phylly, the relationship of these traits lacks a clear functional
basis and probably lacks a causal basis. Small or highly dis-
sected leaves reduce the boundary layer thickness, thereby
facilitating convective heat loss when conditions are hot and
dry with negligible air movement. Thus small leaves in nutri-
ent poor mediterranean climates facilitate both heat loss in
summer (e.g. Thuiller et al. 2004) and promote water loss in
cool wet periods, aiding nutrient acquisition and transport
(Yates et al. 2010).
Geophytes
Geophytes frequently possess deciduous leaves and per-
ennial underground storage organs (e.g. tuber, corm, bulb,
or rhizome), allowing perennation through the dry season.
Amongst mediterranean-type floras, the CFR has the highest
diversity of geophytes species (2098 species), 84% of which
are endemic (Proches et al. 2005).
Succulents
Succulents are remarkably diverse in the more arid areas
of the CFR and GCFR. Of the approximately 1 700 ­succulent
species in the GCFR, leaf succulents comprise 80% in over
30 lineages (Linder et al. 2010). Strong gradients in soil and
substrate characteristics combined with highly ­ dissected
drainage basins have resulted in a remarkable array of
morphological diversity and specialization, with species
­
ranging in size from small ‘stone plants’ to large shrubs (Ellis
et al. 2006). In general, succulence functions in both water
and nutrient storage (Ripley et al. 2013).

11.2  The challenges of limited nutrient
availability in a mediterranean climate
11.2.1 The edaphic context
Soils are the combined product of regional climate,
biota, topographic relief, parent geology, and soil age
­(Jenny 1941). The soils of the CFR are the product of a
long history of pedogenesis uninterrupted by the inter-
vention of glaciation. Many CFR soils are considered to
be highly leached, leaching being dependent on both
precipitation and the passage of time. Although CFR
landscapes are commonly characterized as old, cli-
matically buffered, infertile landscapes (OCBILs), their
geologies having been subjected to a long history of
leaching (Hopper 2009), this belies the true complexity

9780199679584-Allsopp.indb 250 22/08/14 10:32 AM


of the situation in which intricate geomorphic processes
and variable underlying geology has generated a het-
erogeneous array of both young fertile and old leached
soils (Chapter 2, Cowling et al. 2009). The contrasting
geological origins of CFR soils contribute to diverse
nutritional and hydrological niches. Furthermore,
pedogenesis is strongly influenced by vegetation, as
exemplified by its potential role in the formation of lat-
erites in southwestern Australia (Pate et al. 2001). The
distinct nutrient compositions of soils beneath adja-
cent Southern Afrotemperate Forest (hereafter ‘forest’)
and fynbos vegetation on similar geologies (Manders
1990) are also probably biogenic. The summation of
all of these processes is a heterogeneous collection of
soils that include both relatively nutrient-rich soils and
extremely nutrient poor soils, driving ecophysiological
specializations to cope with these diverse challenges
(Plate 11, Appendix 11.1). Moreover, the ratios of nutri-
ents (e.g. N:Bray II P) are also highly variable, impos-
ing distinct edaphic challenges on the native flora and
possibly requiring narrow specialization.
11.2.2  Sources of nutrients
Prior to pedogenesis, the chemical composition of the
various parent geologies is variable (Young et al. 2004).
Amongst the sandstone, granite, shale, and schist
­formations of the CFR, it is sandstone that is particu-
larly depauperate in the elements important to plants.
For example, the sandstone rocks of the Peninsula For-
mation contain 0.01% P2O5, 0.3% Fe2O3, and less than
0.1% of each of MnO, MgO, CaO, and K2O (Soderberg
and Compton 2007). While the parent geology has
­important influences on soil physical properties (e.g.
bulk density and texture), the sustained nutritional
content of the soil over long time periods is depend-
ent on biogenic and depositional inputs that at least
partially balance or exceed nutrient losses.
Sources of biogenic and depositional nitrogen (N)
include lightning, free-living bacteria, and symbiotic
N2-fixing microorganisms, which reduce atmospheric
N2. In the CFR, symbiotic N2 fixation is common in
Fabaceae, although several non-legumes, including
Encephalartos spp. (Grobbelaar et al. 1987) and Morella
cordifolia (Bond 1971), are also known fixers. Symbiotic
N2 fixation in both legumes and M. cordifolia occurs in
root nodules, and involves bacteria from the genera
Bradyrhizobium, Burkholderia, Frankia, Mesorhizobium,
and/or Rhizobium (Lamont 1982; Elliott et al. 2007). In
Encephalartos spp., by contrast, fixation occurs in coral-
loid roots with cyanobacterial symbionts (Nostoc spp.;
Grobbelaar et al. 1987). Although legumes are able to
9780199679584-Allsopp.indb 251
P l a nt ec o ph ysi o l o gic a l diversit y    251
derive up to 80% of plant N from symbiotic N2 fixation
(e.g Psoralea spp.; Kanu and Dakora 2012), the plants
lack the ability to persist >10 yr post fire in fynbos veg-
etation (Cocks and Stock 2001). Legumes and N2 fixa-
tion have a high P demand (Vitousek et al. 2002), but
P availability in fynbos is generally low, aside from a
temporary post-fire elevation of P (Brown and ­Mitchell
1986), which supports legume growth. Nonetheless,
in order to persist between fires, legumes have to
deal with low levels of sparingly soluble P. Persistent
species in Proteaceae and Restionaceae employ clus-
ter roots to enhance P acquisition (Box 11.1). In com-
parison, cluster roots have only been reported in two
legume genera, Aspalathus and Cyclopia (Allsopp and
Stock 1993; Spriggs 2004), and the capacity of Aspala-
thus to acquire sparingly soluble P is lower than that of
Proteaceae (Power et al. 2010), which may contribute
to their lack of persistence in mature fynbos. Unsur-
prisingly, therefore, legumes contribute only c.26 kg N
ha−1 or c.0.5% of the total N of a mature fynbos stand
(Cocks and Stock 2001). Aside from fynbos, legumes
are also present in renosterveld, strandveld, and suc-
culent karoo, whose higher soil nutrient status may
enable their persistence.
Plants also redistribute nutrients in ecosystems. For
example, cluster roots mobilize P, which may subse-
quently become available to other species. Further-
more, deep-rooted species (e.g. Proteaceae in fynbos;
Elytropappus rhinocerotis in renosterveld; Vermeulen
2010) may mobilize sources of nutrients from deep
in the soil, concentrating them in the topsoil (e.g. N;
Stock and Lewis 1986). The extent, to which this accu-
mulation occurs, depends on soil texture and organic
content, factors which determine the capacity of soils
to bind and resist leaching of nutrients. Where neigh-
bouring forest and fynbos occur on soil derived from
the same parent material, higher soil organic matter
may account for the accumulation of nutrients in for-
est (Manders 1990).
Non-soil derived nutrients may come from atmos-
pheric nutrient depositions for which there are four
main sources: (a) marine aerosols; (b) terrestrial dust;
(c) fire; and (d) pollution. For instance, atmospheric
deposition of c.2 kg N ha−1 yr−1 (Stock and Lewis 1986)
and c.0.2 kg P ha−1 yr−1 (Brown et al. 1984) at a low-
land fynbos site (Pella, c.15 km from coast) is mainly
from marine sources. Given that sandstone is low in
feldspar and mica, it is likely that dust derived from
terrigenous sources is the origin of much of the clay
in sandstone-derived soils, as well as associated Ca, K,
Fe, Mn, and Zn (Soderberg and Compton 2007). Fire,
which is common in fynbos, but less so in other CFR
22/08/14 10:32 AM
 252   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n
vegetation types (Chapter 3), volatilizes and deposits
nutrients, thereby driving massive-scale nutrient
­redistribution. For example, fire both volatilizes a por-
tion of biomass N and increases topsoil N immediately
post fire (persisting for up to nine months), ­resulting
in a pulse of nutrients which percolate into the deeper
soils over subsequent years (Stock and Lewis 1986).
In urban areas, anthropogenic N deposition has been
responsible for an increase in deposition of 6–13 kg
N ha−1 yr−1 since 1950 (Wilson et al. 2009), potential-
ly leading to biodiversity losses (Ochoa-Hueso et al.
2011). The variability in soil derived nutrient avail-
ability is thus compounded by spatial variability in
the sources, forms, and concentrations of atmospheric
nutrient deposition.
11.2.3  Which specific nutrients are missing
from fynbos soils?
Although the soils of the CFR are generally low in
­nutrients, fynbos soils are particularly nutrient depau-
perate (Plate 11). Soil development generally follows
a predictable pattern described by ‘Albrecht’s curve’
in which clay and cation exchange capacity initially
increases with weathering and then decreases, par-
­ In contrast, mineralization in the soils of the relatively
ticularly when precipitation exceeds evapotranspira-
tion (Fig 11.1, Albrecht 1957; Huston 2012). Soils of the
CFR that are highly weathered (i.e. sandstone soils)
have been leached of cations, resulting in retention
of H+, and, consequently, generally low pH. Total P in
CFR soils averages 87 mg kg−1, but ranges from 18 to
310 mg kg−1 (Stock and Verboom 2012). Unlike N, P is a
non-renewable resource in natural systems and, in the
absence of depositional inputs, total P declines monot-
onically with increasing precipitation and increasing
soil age (Fig 11.1, Walker and Syers 1976; Huston 2012).
In contrast, available P follows Albrecht’s curve across
precipitation gradients. The decline in P availability
is a consequence of the main initial soil P-containing
mineral, Ca apatite, being utilized by organisms to
form organic P, and by sorption of P onto the sur-
faces of other minerals (e.g. Ca, Fe, Al; Mitchell et al.
1984). This m ­ ineral-sorbed P is labile and can be des-
orbed in response to diffusion gradients as a result of P
­uptake by plant roots or it can be chemically displaced
by root exudates (Box 11.1). Over geological time,
mineral-sorbed P can also be occluded by Fe and Al,
rendering it essentially unavailable to plants. Organic
P and microbial P become a more important fraction
of total P as soils age (Turner et al. 2013). For exam-
ple, up to 67% of total P in a sandy fynbos soil (Pella)
was found to be organic (Mitchell et al. 1984). These
9780199679584-Allsopp.indb 252
processes result in some soils in the CFR, particularly
sandstone-derived fynbos soils, having extremely low
amounts of available P, while others (e.g. strandveld;
­Appendix 11.1) have relatively high P availability (up
to 252 mg P kg−1).
Many CFR soils have low total N concentrations,
averaging 973 mg kg−1 and ranging between 214 and
5 973 mg kg−1 (Stock and Verboom 2012). The soils of
the CFR are extremely heterogeneous with respect to
total N (e.g. Appendix 11.1), varying tenfold over tens
to hundreds of metres. Variability in total N, which is
greater than that in total P (Richards et al. 1997), may
contribute to species turnover. The amount of inor-
ganic N in the soil is related to the balance between
mineralization, volatilization, and the uptake of these
forms by plants and microbes (Stock et al. 1988). Com-
bining low total N soils with the water and tempera-
ture limitations imposed by the mediterranean climate
leads to low rates of mineralization. Consequently,
fynbos soils typically have low levels of inorganic N,
although not significantly less so than strandveld soils
(Stock et al. 1995). Furthermore, slow mineralization
in fynbos results in an accumulation of litter, which is
only mineralized during fires (e.g. Mitchell et al. 1986).
nutrient-rich renosterveld is dependent on litter N and
P content but is substantially higher than reported for
fynbos vegetation, consistent with the heterogeneous
nature of CFR soils (Bengtsson et al. 2011).
MAP<ET MAP>ET
Total P Clay
Soil properties
Total acidity
Organic matter
Exchange capacity
Base saturation
Increase in weathering
Figure 11.1  Change in soil properties as a function of weathering
and, implicitly, time (modified from Huston 2012). Albrecht’s
curve (Albrecht 1957) provides a theoretical description (recently
substantiated by Huston 2012) of rock weathering to form soil.
The trajectory follows a rising curve of clay production and other
properties until precipitation (MAP) exceeds evapotranspiration (ET)
resulting in soil destruction and a falling curve of the soil properties.
In contrast, clay continues to increase with leaching (i.e. MAP > ET).
Also shown are the effects of leaching on soil acidity. Total P declines
continuously as P is lost from the soil (Walker and Syers 1976) and is
accompanied by changes in the forms of P in the soil from more- to
less-available forms.
22/08/14 10:32 AM

Despite the highly leached component soils of the
CFR being low in most nutrients, there is striking evi-
dence that P is what has been referred to as ‘the ultim-
ate limiting nutrient’ (sensu Vitousek et al. 2010; i.e. P
addition transforms ecosystems). Across diverse plant
families, CFR plants show higher foliar N:P ratios
than do plants from the world’s other mediterranean
ecosystems (Stock and Verboom 2012). The high N:P
ratios and low available P of this system do not, how-
ever, signify proximate P limitation (sensu Vitousek et
al. 2010; i.e. plant growth does not respond positive-
ly to P addition) since the plants occurring here may
be adapted to these conditions (Witkowski et al. 1990)
and may even suffer toxicity with elevated supply (e.g.
Hawkins et al. 2009). Instead of stimulating growth of
native taxa, nutrient addition may result in ecosystem
transformation to alternative states.
11.2.4  N acquisition strategies
The N forms of importance to plants are NO3−, NH4+,
and organic N. There is a long-standing belief that
NH4+ is more important than NO3− for fynbos ­species,
because soil NH4+ concentrations are higher than NO3−
concentrations (Stock and Lewis 1984). In ­addition,
CFR Proteaceae reportedly have low nitrate r­ eductase
activity (Stock and Lewis 1982). Most plants, how-
ever, take up NH4+ more rapidly than NO3− and low
­levels of foliar nitrate reductase activity are ­common in
woody species (reviewed by Miller and Cramer 2005).
In an N­ -limited ecosystem, it is unlikely that plants
would lack the capacity to utilize NO3− even if the con-
centration of NO3− in soil is lower than that of NH4+.
Consistent with this, Banksia prionites (Australian Pro-
teaceae) has high nitrate reductase activity in cluster
roots ­(Jeschke and Pate 1995), and growth of several
species of CFR Proteaceae respond well to NO3− fertili-
zation ­(Hawkins et al. 2007).
Soil organic-N concentrations (mainly amino a­ cids)
can be 100-fold that of inorganic N (Stock et al. 1995).
Mycorrhizal (Box 11.1) uptake of N (Table 11.1) re-
sults in strong influences of both ericoid and arbus-
cular mycorrhizas on plant δ15N values (Spriggs et al.
2003). While it is known that mycorrhizas contribute
to ­ organic-N uptake, non-mycorrhizal species (e.g.
­Cyperaceae, Restionaceae, and Proteaceae) are com-
mon in the CFR (Allsopp and Stock 1992). Moreover, in
most soils microbes outcompete plant roots for organ-
ic N (reviewed by Miller and Cramer 2005). D ­ espite
this, the cluster roots of species from a wide range of
Australian environments (Schmidt et al. 2003) and
­ tats differ in above-ground traits but also differ in
of CFR Proteaceae (Hawkins et al. 2005) can acquire
9780199679584-Allsopp.indb 253
P l a nt ec o ph ysi o l o gic a l diversit y    253
organic N. It seems unlikely that plants in an N-limited
environment would not be able to take up all available
forms of N. The ability of plant roots to compete with
microbes for organic N may be enhanced by the low
organic carbon and low microbial activity in many
CFR soils (van Reenen et al. 1992).
11.2.5 P acquisition strategies
The scarce and sparingly available P of some CFR
soils has resulted in diverse strategies for accessing
P. Generally roots overcome limited mobility of P in
soil through the possession of root hairs and symbiotic
relationships with mycorrhizas, which enable greater
direct ‘interception’ of P (Smith et al. 2002). ­Although
mycorrhizas are common on terrestrial plants, many
species native to the extremely P ­ -deficient soils of
the CFR have discarded, or never had this symbio-
sis, ­apparently in favour of cluster roots (Box 11.1,
­Chapter 10, Lambers et al. 2008). Despite the high car-
bon costs of cluster roots, these structures are likely
to benefit plant growth when growth is limited by P
availability, especially because photosynthesis is com-
monly sink limited. The high carbon costs of cluster
roots partially explain why these roots are short lived,
only being produced when water and P are available.
­Furthermore they are highly sensitive to plant P s­ tatus,
with production being limited by high P (Shane et al.
2004). Species that form cluster roots are also very sen-
sitive to P  ­toxicity, apparently lacking physiological
mechanisms to restrict P uptake when soil P concen-
trations are in excess of plant demand (Hawkins et al.
2008). This lack of physiological regulation may result
from loss of regulatory mechanisms in an environment
where soil P concentrations in excess of plant demand
are rare (Shane et al. 2008). Excess P uptake leads to
binding of other nutrients, resulting in deficiencies of
those nutrients in the plant (Hawkins et al. 2008). This
results in species with cluster roots being unable to
survive on soils with high P concentrations, and is a
clear example of reduced plasticity resulting from eco-
physiological specialization.
The heterogeneous soils of the CFR, and associated
species turnover within the same climate regime, are
often associated with distinct cluster root functional
capabilities. For example, Protea obtusifolia and Leuca-
dendron meridianum are restricted to l­imestone-derived
soils that are relatively P rich in comparison to neigh-
bouring colluvial sands on which Protea compacta
­occurs (Shane et al. 2008). Species from adjacent habi-
their capacity to efficiently utilize P and tolerate P
22/08/14 10:32 AM
 254   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n
toxicity (Shane et al. 2008). There is also variability in
the extent to which CFR Proteaceae cluster roots uti-
lize phosphatase to access organic P in different soils
(Hunter et al. 2009). For example, cluster roots isolated
from plants growing on alkaline calcareous soils have
lower phosphatase activity than those from acidic soils
(Hunter et al. 2009). Specializations in cluster root mor-
phology, size, and physiological activity thus contrib-
ute to ecophysiological specialization and vegetation
turnover with variation in edaphic properties.
Cluster root-forming species that are non-­mycorrhizal
have most likely lost the ability to form this symbi-
otic association (Allsopp and Stock 1994). Mycorrhizal
symbiosis and cluster roots are, however, not mutually
exclusive. Of particular importance in the CFR, some
members of Fabaceae (e.g. Aspalathus spp.; Power et al.
2010) have both cluster roots and mycorrhizas. It is not
clear why some species exclusively have either clus-
ter roots or mycorrhizas and why a few others have
both, although, considering the carbon costs of cluster
roots and mycorrhizal symbiosis, it may be that the
benefit of the dual symbiosis infrequently exceeds the
costs. Cluster roots in highly P-impoverished soils may
represent a more aggressive strategy for P acquisition
than mycorrhizas because cluster roots can chemically
mine P from sparingly soluble P-mineral complexes,
thus facilitating P acquisition to a greater degree than
is achieved via mycorrhizas (Lambers et al. 2008). It is,
however, also possible that cluster roots are restricted
to sandy mineral soils whereas mycorrhizas function
better in finer textured soils, or that mass flow of water
improves the mobility of some P forms (e.g. organic P)
to cluster roots in low cation exchange capacity soils.
While cluster roots and mycorrhizas are common
and may be specialized for different forms and avail-
abilities of N and P, species with one or the other of
these strategies, or neither, do commonly co-occur. The
lack of both cluster roots and mycorrhizas (e.g. some
Cyperaceae) may be because these plants produce very
fine root systems. These different root specializations
may thus also contribute to niche segregation, allow-
ing different species to specialize to different availabil-
ities and forms of P.
11.2.6 Parasitism, carnivory, and coprophagy
as nutrient acquisition strategies
When faced with resource scarcity, some plants re-
sort to theft (see also Chapter 10). Parasitic plants are
commonly associated with low-fertility soils in the
CFR, which is home to nine of the 14 parasitic angio-
sperm families (Visser 1981; Lamont 1982). Parasitic
9780199679584-Allsopp.indb 254
plants make direct connections to neighbouring plants
via haustoria, through which they are able to ­obtain
water, nutrients, and photosynthate. Holoparasites
(e.g. Orobanchaceae) are entirely dependent on host
resources, whereas hemiparasites are capable of
­obtaining some of their resources autotrophically (Press
et al. 2005). Stem-tapping hemiparasitic ‘mistletoes’
(Loranthaceae and Viscaceae) are rare in both forest
and fynbos vegetation of the CFR, despite the presence
of suitable host genera. This may be due to limited N
availability since most CFR mistletoes are associated
with more nutrient-rich vegetation types (Dean et al.
1994). Nonetheless, the relatively nutrient-rich suc-
culent karoo also has few mistletoe species, possibly
­because of the inability of the latter to colonize suc-
culents (Dean et al. 1994). Root-tapping hemiparasites
have access to both soil and host derived nutrients and
are therefore less dependent on their hosts, hemipara-
sitism potentially representing a ‘bet-hedging’ strategy.
Heterotrophy may be most beneficial in systems in
which non-host-derived resources (e.g. soil nutrients)
are scarce and in which competition for light and w ­ ater
is low (Smith 2000). Although parasites commonly
possess poorly developed root systems and leaves that
are reduced or lost, the degree of heterotrophy varies
enormously amongst hemiparasitic species. For exam-
ple, the hemiparasitic genus Thesium of the CFR shows
remarkable diversity in growth form, ranging from
large (>1 m tall) woody individuals with green leaves
to small (<0.1 m tall), often yellow individuals with
few leaves. Within the CFR, Thesium spp. are associ-
ated with the nutrient poor sandstone substrates more
frequently than expected at random, and the degree of
heterotrophy is also correlated with the nutrient pau-
city of the environment (Moore 2010).
Carnivory is common in the CFR (Lamont 1982).
­Although carnivorous plants obtain water and some soil
nutrients through rudimentary roots, they also extract
nutrients from captured fauna (Adlassnig et al. 2005).
Carnivorous plants attract their victims with scent,
­colouration and/or nectar, trap them, digest them, and
utilize their nutrients through highly specialized leaves.
Drosera spp. (13 CFR species), which often occur in
sun-exposed bogs in which nutrients are particularly
scarce, rely extensively on prey for nutrients (N, P, K,
S, and Zn; Lamont 1982). The endemic genus Roridula
­(Roridulaceae) occurs on the moist sandstone uplands
and has resinous glands that capture insects, but lacks
the ability to digest them. Instead these plants absorb
40–70% of their N through coprophagy (­Midgley and
Stock 1998; Anderson and Midgley 2003). The faeces con-
sumed are from an obligate species-specific mutualism
22/08/14 10:32 AM

between Roridula and species of Pameridea (Hemiptera),
which are not deterred by the sticky traps on the leaves,
but consume prey caught by the plants and defecate on
the leaves (Chapter 10, Anderson and Midgley 2003).
11.2.7  Nutrient conservation and exploitation
In oligotrophic environments, nutrient conservation
may be as important as acquisition. Consequently,
very few deciduous species occur in fynbos ­compared
to non-fynbos vegetation (Cowling and C ­ ampbell
1983) and leaves are commonly sclerophyllous
(Box  11.1). CFR forests are also more sclerophyllous
than subtropical and warm temperate forests (Stock
et al. 1997). Furthermore, many graminoids (e.g. Res-
tionaceae, Cyperaceae, and some Poaceae) lack leaves
or have ­ reduced and bract-like, ­non-photosynthetic
leaves, photosynthesizing instead via their culms.
Several other fynbos families (e.g. Bruniaceae,
­ Thamnochortus punctatus (Restionaceae) remobilizes up
Ericaceae, ­
­ Fabaceae) include species with reduced
leaves and photosynthetic stems. These traits may
constitute ­ extreme sclerophylly in which persistent
stems ­ assume the photosynthetic function. Sclero-
phylly is thus a common nutrient conservation strat-
egy in the CFR. Similar to sclerophylly, perennial life
histories might also be considered a nutrient conserva-
tion strategy in that it circumvents the costs of seed
production and growth associated with the annual
life history. Across a broad collection of CFR grasses,
soil substrates were a significant predictor of annual
life histories with ­annuals only being found on richer
­substrates ­(Verboom et al. 2012). Low nutrient envi-
ronments may constrain ­annuals by limiting growth
rates, and the ­association of annual life histories with
richer soils may be general, pertaining to a wide vari-
ety of plant families (Verboom et al. 2012).
Another way to overcome nutrient limitation is to
economize on the requirement for particular nutri-
ents. Reduction of leaf N concentration is, however,
likely to compromise photosynthesis; indeed, globally
­photosynthetic nitrogen use efficiency ­increases with
specific leaf area (Hidaka and Kitayama 2009).
Conversely, some fynbos Proteaceae have a high
­ not ­restricted to more fertile vegetation in the CFR
photosynthetic activity with a relatively low leaf N
­content (Herppich et al. 2002). The high photosynthetic
­phosphorus use efficiency (PPUE) of Proteaceae from
­western Australia (Lambers et al. 2012) is consistent with
global correlations of PPUE with soil P concentrations,
and the negative correlation between PPUE and spe-
cific leaf area (Hidaka and Kitayama 2009). High PPUE
in ­Australian Proteaceae has been associated with the
­replacement of phospholipids with non-­phospholipids
9780199679584-Allsopp.indb 255
P l a nt ec o ph ysi o l o gic a l diversit y    255
during leaf development, without compromising
­photosynthesis (Lambers et al. 2012). It is likely that a
similar specialization exists in the CFR, enabling plants
to cope with P limitations. This may contribute to vari-
ations in N:P ratio, which is high in both fynbos and
kwongan species (Stock and Verboom 2012).
Globally, remobilization and resorption of foliar N
and P prior to leaf senescence accounts for about 50%
of these elements in living tissue (Aerts 1996). Plants
from resource-poor environments have been suggested
to be capable of remobilizing these nutrients to a great-
er extent than those from resource-rich environments.
For example, some western Australia Banksia spp. re-
mobilize over 80% of their leaf P, which is remarkably
efficient considering that mature Banksia leaves have
low leaf P concentrations (Denton et al. 2007). Remobi-
lization from cluster roots of Hakea prostrata (Proteace-
ae) is similarly efficient (Shane et al. 2004). In the CFR,
70% of culm N and relocates nutrients between ramets
(Stock et al. 1987). Other data from the CFR are less
persuasive of efficient remobilization; for example, N
and P remobilization in Leucospermum parile amounted
to 41% and 25–50%, respectively (Mitchell et al. 1986),
while equivalent values for Protea repens were 3–25%
and 33–65%, respectively (Mitchell and Coley 1987).
Surprisingly, P-rich strandveld vegetation remobi-
lizes a large proportion of P (c.46–81%; J. M. Nyaga,
pers. comm.) questioning the assumption that the
proportion of remobilization responds to deficiency.
Moreover, there is a lack of correlation between remo-
bilization efficiency and nutrient availability globally
(Aerts 1996).
The evolutionary forces driving a reduction in
nutrient losses due to herbivory must have been
­
strong within the CFR, although low foliar nutrient
concentrations have been widely assumed to serve as
a herbivory deterrent per se (see also Chapter 10). His-
torical accounts indicate a large herbivore assemblage
in the CFR that is assumed to have been concentrated
on the more fertile shale-based vegetation. Isotope
data, however, indicate that herbivore foraging was
(Radloff et al. 2010). Regardless, fynbos vegetation is
generally low in spinescence, indicating that herbivore
pressure was probably low, historically, relative to that
in non-­fynbos vegetation, which is more spinescent
(Campbell 1986). High concentrations of secondary
metabolites (e.g. oils, tannins, and phenols) in many
fynbos plants could also have adaptive significance
in deterring herbivory (Cowling and Campbell 1983).
This might contribute to the low insect biomass in
22/08/14 10:32 AM
 256   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n
fynbos vegetation compared to that of other mediterra-
nean ecosystems (Cody 1983), despite high CFR insect
diversity (Procheş et al. 2005). Thus although insects
can and do forage on fynbos, it seems that foliar char-
acteristics limit the impact of insect herbivory.
Serotiny, the retention of seeds in cones on the can-
opy beyond one year following maturation, is com-
mon in the CFR. Serotiny is commonly associated
with environments characterized by both nutrient
poor soils and frequent fires (Bradshaw et al. 2011). In
these situations serotiny is typically associated with
­fire-stimulated seed release (e.g. Midgley and E ­ nright
2000), which ­ facilitates nutrient conservation by
­ensuring that r­ ecruitment coincides with the post-fire
­nutrient flush. In the CFR, serotiny is almost exclusive-
ly ­restricted to fynbos vegetation, with the majority of
species in Proteaceae being serotinous (Le Maitre and
Midgley 1992). Apart from representing a substantial
carbon investment, serotinous cones/fruits and asso-
ciated seeds contain substantial amounts of nutrients
(Le Maitre and Midgley 1992), with seed shedding
­incurring considerable N and P costs. In Banksia hooke-
riana, for example, 24% and 48% of above-ground N
and P, respectively, is in seeds (Witkowski and Lamont
1996). Thus, another way in which serotiny aids in the
conservation of nutrients is through the protection of
seed against fire and predators (Bond and van Wilgen
1996). The degree of serotiny (i.e. length of cone reten-
tion) is, however, highly variable in CFR Proteaceae,
with ‘weakly serotinous’ species releasing seeds
­pre-fire (Midgley and E ­ nright 2000). Since the mainte-
nance costs of cones are small, weak serotiny may be
a ­bet-hedging strategy, which allows inter-fire recruit-
ment in more benign habitats, while strong serotiny
aids ­nutrient conservation (Cramer and Midgley 2009).
A number of predominantly geophytic (Box 11.1)
monocots in the CFR exhibit fire-stimulated flower-
ing (c.125 species, 6–11 months post fire; Lamont and
Downes 2011). This phenomenon is largely restricted
to fast-growing species with short lifespans, allowing
these species to exploit the low-competition, nutrient-
rich post-fire environment (Lamont and Downes 2011).
For example, fire-stimulated flowering of Ehrharta cap-
ensis is linked to nutrient availability (Verboom et al.
2002). Furthermore, many geophytes lack refractory
seeds (i.e. requiring fire cues for germination) so post-
fire flowering may also cue recruitment to subsequent
post-fire years (Keeley and Bond 1997).
In fire-prone ecosystems the ability to survive fire is
critical to persistence. The majority of woody species
in the CFR are seeders, which are killed by fire and per-
sist via soil- or canopy-stored seedbanks (Chapter  3,
9780199679584-Allsopp.indb 256
Bond and van Wilgen 1996). Resprouters are c­ ommon
in fynbos but also in the less fire-prone vegetation
types such as strandveld and forest (Le Maitre and
Midgley 1992). Although more numerous, seeders
tend to have a higher resource demand compared to
resprouters. Seeders are larger, invest more biomass
above ground, and grow faster, reaching reproductive
maturity ­before resprouters (Midgley 1996). Moreo-
ver, seeders may have a higher and thus more costly
­reproductive ­effort. For example, in comparing conge-
neric Banksia spp. from southwestern Australia, Low
and Lamont (1990) found that reproductive structures
made up 32% of shoot biomass in seeders, whereas
in resprouters it comprises <20%. Thus resprouting,
which relies on temporal resource flushes and incurs
relatively low vegetative growth and reproductive
costs, could serve to conserve resources. Resprouters
take immediate a­ dvantage of increased nutrient and
water supply, which would give them a head start over
seeders in the post-fire period, providing a degree of
niche separation between these persistence strategies.
CFR Proteaceae seeds can contain between 30 and
75% of the P invested into fruiting bodies (Groom and
Lamont 2010). The high P investment in seeds may be
required because of the edaphic constraints on germin-
ation and seedling survival. High P investment trans-
lates into large amounts of P per seed (up to 15 mg P
per seed), giving the seedlings a better chance of estab-
lishing in soils whose P concentrations are low (Stock
et al. 1990). In serotinous seeds, the amount of P is
greater than in non-serotinous seeds, possibly because
serotiny is a lower-risk seeding strategy or because
more P-rich seeds are required in P-impoverished
habitats (Groom and Lamont 2010). In resprouters, the
nutrient investment in seed is generally lower than in
obligate seeders, which rely entirely on seed produc-
tion. Consequently, resprouters produced fewer, but
larger seeds, with more total seed P than co-occurring
seeders (Groom and Lamont 2010).
11.2.8  Seasonal nutrient acquisition/utilization
The strong seasonality of rainfall in the western CFR
results in a transient period of nutrient availability
in the wet winter and into the spring months. Within
the CFR and the adjacent succulent karoo, the growth
season measured through satellite-based normalized
difference vegetation index (NDVI) analysis predomi-
nantly starts in April/May and reaches its midpoint in
August/September (Wessels et al. 2011), although this
incorporates considerable variance related to climate
heterogeneity. For example, west coast renosterveld
22/08/14 10:32 AM

grows predominantly in winter while south coast
renosterveld grows predominantly in spring and au-
tumn (Pierce 1984). Furthermore, this NDVI analysis
represents a summation of the growing seasons across
diverse life forms whose growth seasonality may vary;
for instance, in contrast to shallow-rooted species,
deep-rooted Proteaceae continue to grow into the sum-
mer (Pierce 1984). Thus shallow-rooted species may
develop partial asynchrony between nutrient avail-
ability and suitable conditions for growth that varies
with habitat. For example, Thamnochortus punctatus
(Restionaceae) extends roots and rhizomes during the
wet winter months while culm elongation occurs in
the warmer and drier spring to summer period, and
reproduction in summer and autumn, thereby ena-
bling maximum utilization of scarce resources (Stock
et al. 1987). Even for the generally deep-rooted Pro-
teaceae, short lived cluster roots are only produced in
the surface soil when the soil is wet (Shane et al. 2006),
resulting in a rather limited window for peak P ­uptake.
Cluster roots are, however, also produced deeper in
the soil (Canham et al. 2012) and it is also possible that
hydraulic lift extends the longevity of cluster roots
into the dry season (Hawkins et al. 2009). This tempo-
ral partitioning of resource availability contributes to
niche diversity, possibly facilitating the coexistence of
species that share similar resource requirements.
11.3  The challenge of being hot when
dry, cold when wet
Trade-offs between waterlogging and drought toler-
ance in plants result in a fundamental, eco-­hydrological
basis for niche segregation, the so-called hydraulic
niche (Silvertown et al. 1999). In the CFR, the generally
inverse relationship between water availability and
temperature results in two competing stresses for the
flora: being hot when dry and cold when wet. Hot and
dry conditions are particularly challenging for plants
because both atmospheric demand for water vapour
and carbon costs of maintenance respiration increase
exponentially with temperature (Zhao and Running
2010). These conditions may also make CFR species
more susceptible to pathogens (Jacobsen et al. 2012).
Hot and dry conditions thus place both hydraulic
and metabolic limitations on plants (McDowell et al.
2011) and can lead to plant death if the water deficit
is severe. Cold and wet conditions also present a chal-
lenge for plants. If temperatures are too cold, growth
cannot coincide with the peak in moisture availability.
Additionally, waterlogging can induce plant death by
anoxia (Justin and Armstrong 1987), although anoxia
9780199679584-Allsopp.indb 257
P l a nt ec o ph ysi o l o gic a l diversit y    257
occurs less rapidly under cooler temperatures, due to
increased oxygen solubility and decreased metabolic
demand (Drew 1997). Thus the seasonal timing of pre-
cipitation is an important factor in plant stress in the
CFR, since both drought and waterlogging stresses are
exacerbated by warmer temperatures.
The combination of drought and waterlogging stress
have been shown to structure plant communities in the
fynbos (Araya et al. 2011), providing evidence of the
importance of niche differentiation in coexistence and
diversity in these communities (Silvertown et al. 2012).
In this section, we describe variation in the abiotic
­environment followed by the predominant plant spe-
cializations for solving the problems of being hot when
dry and cold when wet, and illustrate how variation
in water availability may contribute to the exceptional
floral diversity of the CFR.
11.3.1 The abiotic context
Despite being a predominantly winter rainfall area,
the CFR is climatically heterogeneous (Appendix 11.2,
Chapters 2, 13). The main environmental gradients
relevant to the ecophysiology of drought and water-
logging are
a) an aridity gradient from coast to interior, the inter-
ior being more arid
b) a rainfall seasonality gradient, from predominantly
winter rainfall in the west to all-year rainfall in the
east
c) an elevational gradient, with higher elevations hav-
ing more rainfall, less evaporation and cooler tem-
peratures; higher elevations also have less strongly
seasonal climates (Agenbag et al. 2008) and are ex-
posed to cloud moisture (Marloth 1903); south-facing
slopes receive less solar radiation (see 11.4), are
cooler, and receive more rainfall and cloud moisture
from rain-bearing trade winds in the southern and
southwestern Cape
d) edaphic variability as a consequence of rocky sand-
stone substrate resulting in shallow soils with poten-
tial pathways to deep-water acquisition; in contrast,
shales give rise to finely textured soils which limit
water penetration and form aquitards (bed of low
permeability along an aquifer)
e) water tables of the Cape Fold Mountains are rela-
tively shallow, reaching the surface in many loca-
tions as seeps (February et al. 2004) but are only
reachable by deep-rooted plants in other locations;
this creates a tapestry of seasonal water table varia-
tion across the landscape
22/08/14 10:32 AM
 258   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n
As a consequence of this environmental heterogeneity,
there is great spatial and temporal variation in the in-
tensity of the summer drought as well as winter flood-
ing. This variation occurs at both coarse and very fine
scales.
11.3.2 Evergreen perennials
Across the CFR, evergreen perennials exhibit diverse
strategies for surviving summer drought. The high
proportion of evergreen sclerophyllous species in the
CFR (Campbell and Werger 1988) require some degree
of drought tolerance or avoidance, as leaves are not
simply shed when subjected to water stress. Although
sclerophylly has been linked to nutrient conservation
(see 11.2.7) it may also function in drought tolerance
(e.g. Lamont et al. 2002). Several features of sclerophyl-
ly (e.g. small cells and thick cell walls) may provide
enhanced mechanical support and ensure leaf integrity
during drought (Orians and Solbrig 1977). Despite this
putative role for sclerophylly in drought resistance,
some authors have found scant evidence for a direct
role (e.g. Salleo et al. 1997; Stock et al. 1997), although
water availability strongly modifies nutrient availabil-
ity so that sclerophylly is a benefit when either or both
are limited (Yates et al. 2010).
The cooling requirement imposed by sum-
mer drought has resulted in reductions in leaf size
(Box  11.1). Similarly, highly dissected leaves may
­confer benefits in hot and dry environments and have
been shown to have higher photosynthetic thermal
­optima (Nicotra et al. 2008). An alternative strategy
for reducing reliance on evapotranspiration for leaf
­cooling is to reduce the amount of light absorbed (see
11.4). For example, leaf pubescence in Leucospermum
conocarpodendron has been shown to increase the reflec-
tance of light and result in lower leaf temperatures of
pubescent versus glabrous leaves (Skelton et al. 2012).
Leaves of many fynbos species, in addition to being
small, have rolled margins that enclose the stomata
(i.e. ‘ericoid’ leaf form; Campbell and Werger 1988).
This morphology increases the effective boundary
layer thickness, which may enhance water conserva-
tion ­under still, dry conditions, although this does not
explain the high prevalence of ericoid leaves within
mesic sites in the CFR (Campbell and Werger 1988).
Other stomatal protection traits, such as encryption or
covering with pubescence or papillose pits, are thought
to act similarly to increase boundary layer resistance
(Hassiotou et al. 2009). Despite a strong association
between dry environments and stomatal encryption in
Australian and South African Proteaceae, there was no
9780199679584-Allsopp.indb 258
association with pubescence or papillose pits (Jordan
et al. 2008). Indeed, the role of stomatal crypts in Aus-
tralian Proteaceae may be to reduce the pathway for
CO2 diffusion through the thick sclerophyllous leaves,
rather than to reduce transpiration (Roth-Nebelsick
et al. 2009). It is likely that the factors that determine
leaf size in the CFR are complex, being the products of
­interactions between the avoidance of heat stress and
the promotion of water loss in winter (Yates et al. 2010).
The seasonal progression of whole plant water stress
varies greatly between the predominant functional
types in the CFR (e.g. West et al. 2012). For example,
­responses to water stress are related to whether plants
are resprouters or seeders. Although resprouters tend to
occur in parts of the CFR with lower drought probabil-
ity relative to seeders, they co-exist in most communi-
ties (Le Maitre and Midgley 1992; Ojeda 1998). Seeders
and facultative resprouters reportedly have a higher re-
sistance to drought induced cavitation and thus may be
more drought tolerant than obligate resprouters (Pratt
et al. 2012). Jacobsen et al. (2007) examined minimum
seasonal water potential (Pmin), xylem vulnerability to
cavitation (P50) and associated xylem traits in 17 fynbos
and succulent karoo species along an elevation gradi-
ent in the southwestern Cape and found a wide range
of variation in Pmin (−1.9 to ≤10 MPa) and P50 (−1.9
to −10.3 MPa) across this short gradient, indicating
variable access to soil moisture and water utilization
­between species. They suggested that this variability
may be an important factor determining the plant spe-
cies richness of the area (Jacobsen et al. 2007). A large
component of the variation in Pmin and P50 measured in
these studies, however, was due to the inclusion of two
succulent karoo species (Pteronia fasciculata and P. pan-
iculata) with very negative Pmin and P50. Additionally,
succulent karoo species experienced greater seasonal
loss of hydraulic conductivity than fynbos species, sug-
gesting that species in succulent karoo and fynbos eco-
systems might have fundamentally different water use
strategies (Jacobsen et al. 2009). This is consistent with
the observation that fynbos seedlings are more limited
by water deficit, whereas succulent karoo species are
limited more strongly by amongst-plant interactions
(Lechmere-Oertel and Cowling 2001).
This picture of ecosystem specialization is, however,
confounded by the fact that Pmin is dependent on the
degree of water stress experienced in a given season
and as such will often underestimate the degree of
stress that plants are exposed to over their lifespans
(West et al. 2012). Furthermore, there is considerable
variation in hydraulic strategies within both fynbos
and succulent karoo communities. For example, the
22/08/14 10:32 AM

range of Pmin observed within a mesic fynbos commu-
nity under drought conditions equalled that measured
across the succulent karoo/fynbos ecotone (West et al.
2012). For these species, co-occurring functional types
have divergent functional responses to water deficits,
resulting in a large degree of variation in growth sen-
sitivity, reproductive output and mortality. In a six-
month rain exclusion experiment (West et al. 2012),
large Proteaceae (i.e. Leucadendron laureolum) showed
little discernible drought impact, due to the combina-
tion of deeper water access and tight stomatal control
preventing a high degree of water stress (i.e. isohydric).
By contrast, all three shallow-rooted Erica spp. did not
tightly regulate water status (i.e. anisohydric), which
resulted in increased mortality, reductions in growth,
leaf area, and flowering. The shallow-rooted Restion-
aceae growth form represented yet another functional
type, with no discernible drought impact, possibly due
to access to summer mists (e.g. Marloth 1903) or the
capacity of this growth form to survive with minimal
water loss during summer due to generally leafless
erect culms. Importantly, within these broad functional
responses, there was considerable variation in specific
drought response, with each species displaying unique
‘response pathways’ from physiological traits to fit-
ness outcomes in response to water deficits (Fig 11.2).
Thus variations in drought response may be an impor-
tant ecophysiological axis for the maintenance of high
species diversity in fynbos plant communities.
There is also considerable variation in drought sen-
sitivity in the succulent karoo, with growth form (i.e.
leaf-, stem-, and non-succulent shrubs) emerging as a
poor predictor of drought sensitivity (Hoffman et al.
2009). In their study of ten fynbos and five succulent
karoo species, Jacobsen et al. (2009) recorded both the
highest and lowest P50 values from succulent karoo
species, suggesting a diversity of water use strategies
within succulent karoo communities. Thus for both the
evergreen, perennial fynbos and succulent karoo spe-
cies, there are a large number of morphological and
physiological strategies enabling spatial and tempo-
ral niche segregation, and thus contributing to both
local species coexistence and species turnover across
­diverse hydraulic niches (see 11.3.1).
11.3.3 Annuals
The proportion of annuals in the CFR flora is much
lower than that in the adjacent succulent karoo (c.4%
versus 40%; van Rooyen 1999). While this is partly
attributable to nutritional constraints on the annual
life history (see 11.2.7), there is also a strong climatic
9780199679584-Allsopp.indb 259
P l a nt ec o ph ysi o l o gic a l diversit y    259
link, with annual life-history traits being favoured in
­environments experiencing shorter periods of mois-
ture availability. For example, in a common garden ex-
periment assessing phenological variation in Ehrharta
calycina (Poaceae) across an aridity gradient, plants
from sites experiencing a short moisture growing sea-
son flowered earlier (genotypic) and produced larger
quantities of small seeds, apparently because rates of
late-summer rhizome death at these sites were higher
(Verboom et al. 2012).
11.3.4 Geophytes
The highest regional geophyte (Box 11.1) diversity
occurs in the southwestern CFR, possibly due to the
more reliable rainfall patterns and associated lower
extinction rates in this area (Procheş et al. 2005). Since
deciduous geophytes escape summer drought and
consequently summer fires by persisting underground,
their survival is tightly coupled to their ability to provi-
sion the below-ground storage organ with carbon and
water during winter (Rossa and von Willert 1999). Con-
sequently, geophytic species have been shown to have
low photosynthetic temperature optima, low stomatal
limitation, and low rates of photoinhibition (Rossa
and von Willert 1999). The size of storage organs and
the ability to survive unpredictable extended drought
periods are also correlated. Storage organ size is also
correlated with both winter rainfall amount and reli-
ability, with smaller storage organs predominating in
more mesic and seasonally reliable areas (Procheş et al.
2005). An alternative geophyte survival strategy is to
flower and leaf opportunistically in response to mois-
ture availability (Procheș et al. 2005), a strategy that is
found predominantly in aseasonal areas of the CFR.
Convergence in leaf form amongst unrelated line-
ages of geophytes is common and strongly linked to
environmental selective pressures of the region. Many
CFR geophytes have both vertical and prostrate (ad-
pressed to soil) strap-like leaves (Esler et al. 1999).
Although largely absent in the rest of the world, the
prostrate growth form (occurring in eight families)
is common in the winter rainfall regions of the CFR
­(Esler et al. 1999). Potential explanations for the suc-
cess of this growth form in the CFR include tem-
perature optimization in response to cool growing
conditions (Esler et al. 1999; Rossa and von Willert
1999) and the utilization of soil derived CO2 to boost
assimilation (Cramer et al. 2007). A number of taxa (in
four families) occurring on gravel plains and rocky
sites also produce coiled, wiry, or ‘serpentine’ leaves
(Vogel and Müller-Doblies 2011). These are thought to
22/08/14 10:32 AM
 260   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n

Drought sensitivity
Low High

Flowering
Outcomes

Severely
Unaffected
impacted

Mortality
None High

Growth
sensitivity
Low High

Water
potential
regulation
Isohydric Anisohydric
Traits

Rooting
depth
Deep Shallow

Drought sensitivity
Low High Species pool

E Key to symbols

Proteoids
Ericoids

R
P Restioids

Figure 11.2  ‘Response pathways’ of coexisting fynbos species exposed to experimental drought (redrawn from West et al. 2012). Pathways
represent a spatial depiction of variation in hydraulic traits and the consequent fitness outcomes after drought, in terms of growth sensitivity,
mortality, and flowering output. The response pathways show species-specific variation in both traits and outcomes. Inset: A conceptual view of the
pathways followed by the key functional groups (P, proteoid shrub; E, ericoid shrub; R, restioid).

9780199679584-Allsopp.indb 260 22/08/14 10:32 AM


reduce moisture stress by promoting harvesting of fog
and dew and reduce thermal heat loading in summer
(Vogel and Müller-Doblies 2011).
11.3.5 Succulents
Another feature of the functional trait diversity of the
CFR and GCFR is the unusual diversity of leaf succu-
lents (Box 11.1). An iconic feature of the succulent ka-
roo flora is the cryptic ‘stone plant’ dwarf succulents
(eg. Lithops, Argyroderma spp.), which have two suc-
culent leaves that remain partially embedded in the
soil. This may serve to reduce water loss (Eller and
Ruess 1982) or allow buffering of leaf temperatures
(Turner and Picker 1993), helping these small plants
to survive the hot, dry conditions of summer. These
cryptic leaves may, however, also enable escape from
herbivory (Nobel 1989). Remarkably, these leaves
have ‘windows’ which allow light to be focussed on
internal chlorenchyma and aid in thermal regulation
(Turner and Picker 1993; Egbert et al. 2008). Many leaf
succulents are also characteristically small and shal-
low rooted when compared with other world des-
ert regions (Esler and Rundel 1999), enabling rapid
uptake of small amounts of moisture delivered by
sporadic precipitation events characteristic of the suc-
culent karoo. For example, shallow-rooted Aizoace-
ae are particularly adept at utilizing brief pulses of
shallow soil moisture (February et al. 2013). Sporad-
ic precipitation also increases soil nutrient mobility
allowing plants to accumulate nutrients during wet
periods (Ripley et al. 2013). Together with greatly en-
larged vacuoles in leaf cells, this ensures moisture and
nutrient availability to photosynthetic tissues during
the hot, dry summers.
Co-occurring species in the succulent karoo have
been shown to use all variations of crassulacean acid
metabolism (CAM), including CAM-switching, CAM-
cycling, obligate CAM, and flexible CAM/C3 (Veste
et  al. 2001). Interestingly, these variations in CAM
mechanism occurred within plants from comparable
microhabitats, indicating that environmental stress
might not be the decisive element in the engagement
of CAM photosynthesis (Veste et al. 2001). There also
­appears to be little consistent relationship between the
extent of engagement of CAM and plant morphology or
life-history strategy. Many leaf succulents are drought
deciduous, shedding leaves over the summer drought
to reduce water and carbon costs. Several studies, how-
ever, indicate that the degree of CAM expression is also
not linked to the degree of drought ­induced decidu-
ousness (Veste et al. 2001). Furthermore, considerable
9780199679584-Allsopp.indb 261
P l a nt ec o ph ysi o l o gic a l diversit y    261
variation in CAM has been reported both within and
between succulent growth forms (Rundel et al. 1999).
Thus, it appears that there is little constraint on the
­potential combinations of leaf lifespan, growth form,
and photosynthetic mode in the leaf succulents.
The engagement of CAM may be associated with
leaf anatomy and growth phenology. Leaf succu-
lents are commonly ‘all-cell succulents’ (e.g. Cras-
sulaceae, Portulacaceae), with a uniform distribution
of ­chlorophyll-containing cells through the leaves. In
Aizoaceae and the genus Aloe in the Asphodelaceae
(amongst others), however, there is a distinct outer
chlorophyllous layer (chlorenchyma) and inner achlo-
rophyllous (hydrenchyma) tissue (Metzler 1924). The
all-cell succulents commonly have CAM, possibly
because diffusion of CO2 through succulent leaves to
the sites of photosynthesis requires a steep CO2 gra-
dient generated by the high affinity for CO2 exhibited
by CAM (Ripley et al. 2013). By contrast, succulents
with chlorenchyma may rely more on C3 photosyn-
thesis owing to the lack of mesophyll limitation and
because growth occurs when conditions are cool and
wet (Ripley et al. 2013). Even this pattern is not that
clear, however, because Aloe spp., which have an outer
chlorenchyma layer, commonly exhibit CAM photo-
synthesis (Kluge et al. 1979). Ripley et al. (2013) specu-
late that CAM species continue to grow into the hotter
and drier times of the year, whereas C3 species do not
grow extensively during these periods.
11.3.6 C3 versus C4 photosynthesis
The distribution of C4 photosynthetic taxa globally
is linked to both temperature and precipitation, with
greater C4 representation in hotter and drier climates
(Still et al. 2003). These authors predicted global C4
distributions on the basis of this correlation and indi-
cate that the CFR is expected have relatively few C4
species (<10%). Little is known about the occurrence
of C4 photosynthesis in the CFR, especially in fami-
lies other than Poaceae. Grasses, in which C4 photo-
synthesis is most common, are relatively sparse on
nutrient impoverished western fynbos soils (Mucina
and Rutherford 2006), but do occur in grassy eastern
fynbos (Cowling 1983) and in other more fertile veg-
etation types of the CFR (e.g. renosterveld; Verboom
et al. 2012). In conflict with the predictions of global
models (Still et al. 2003), where grasses do occur in
the CFR, the numbers of C3 and C4 species are simi-
lar, although C4 species are more dominant in terms
of cover (Cowling 1983). Cowling reported that C3
grass cover (relative to C4) was greatest in cool,
22/08/14 10:32 AM
 262   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n
shaded microclimates, but did not find an association
with precipitation (caveat: variations in precipitation
were small). Growth of C3 and C4 species was tempo-
rally distinct, with C3 species growing mainly in the
winter months and C4 species during summer. There
is also limited evidence that C4 species are restricted
to more fertile soils in the CFR (Bond 1981; Cowling
1983).
The global association of C4 distribution with tem-
perature and moisture gradients has commonly been
linked to anatomical and physiological differences
associated with the photosynthetic pathways. The
grass clades in which the C3 and C4 species occur are,
however, also important in determining distributions
(Pau et al. 2013). The importance of photosynthetic
pathway per se in determining the distribution of C3
and C4 species in the CFR has not been evaluated in
the light of this importance of evolutionary history.
­Despite the paucity of information on the occurrence
of C4 photosynthesis in the CFR, however, it does seem
to be largely absent from nutrient poor strongly winter
rainfall systems.
11.3.7 Traits to cope with waterlogging
Segregation of Restionaceae into hydraulic niches has
recently been demonstrated in the fynbos (Araya et al.
2011). The physiological mechanism for this trade-off
is most probably a combination of hydraulic capacity
to cope with drought (West et al. 2012) and its ability
to avoid anoxia during flooding (Justin and Armstrong
1987). The segregation of Restionaceae species into
­hydraulic niches is not, however, associated with vari-
ation in shoot water use efficiency (Araya et al. 2010),
a trait more likely to reflect water stress, but with the
presence or absence of aerenchyma in the roots (­ Huber
and Linder 2012). Root aerenchyma enables anoxia
avoidance in waterlogged conditions, whereas non-
arenchymatous restioid species were excluded from
waterlogged habitats (Huber and Linder 2012). This
neatly demonstrates the link between a­natomical
traits, hydraulic niche differentiation, and coexist-
ence and diversity within these communities. Further
work exploring the generality of these patterns outside
of Restionaceae is necessary. For example, consider-
able plant mortality in fynbos shrubs, but not in the
co-occurring graminoids, was observed due to water-
logging following an anomalously wet summer near
Oudtshoorn (Rebelo et al. 2009). Testing the extent to
which patterns such as these can be related to measur-
able traits that enable plants to cope with waterlogging
remains to be done.
9780199679584-Allsopp.indb 262
11.4  Light surfeits and deficits
Although the CFR is generally considered a
light-­saturated environment, seasonality, variations
in topography, and open and closed-canopy vegeta-
tion create variability in light regimes. Summer ­solar
radiation (28–29 MJ m−2 d−1) is much greater than
­
winter solar radiation (9–10 MJ m−2 d−1) due to the
increased cloud cover from frontal weather systems
(Reid and De Jager 1988). In winter, plants need to cope
with the challenge of low radiation coupled with high
moisture, while the converse is true in summer. In sum-
mer, there is little difference in solar radiation between
north and south mountain slopes, but in winter, north
slopes of 20° can receive between three to five times
more energy than south slopes (Fuggle and Ashton
1979). Patches of closed-canopy forest with reduced
understorey light predominantly occur on mountain
slopes, thus creating a mosaic of light availability.
Given the low stature of the open canopy systems
dominating the CFR (e.g. fynbos, renosterveld, strand-
veld, and succulent karoo), light extinction is low; for
example, ground-level photosynthetically active ra-
diation can range between c.460 and 782 μmol m−2 s−1
in fynbos (Manders 1990). Low stature open canopies
may partially alleviate light limitations in winter by
­allowing light into the sparse canopy. D ­ espite ­adequate
light in summer, CFR species generally have relatively
low instantaneous rates of photosynthesis, ranging
between 2.8 and 14.0 μmol CO2 m−2 s−1 (Mooney et
al. 1983; Herppich et al. 2002), reflecting the highly
sclerophyllous nature of the leaves, low foliar N, and
associated limitations imposed by summer drought,
especially in shallow-rooted species (see 11.3.2). In
addition, the sparse canopy and summer drought
­
conditions require that plants cope with e­ xcess light,
which can induce photoinhibition and cause physi-
ological damage, particularly when temperatures are
high. CFR Proteaceae have stomata on both sides of
their leaves (Jordan et al. 2005), which are held a­ lmost
vertically, especially when young, reducing the area
exposed to direct sunlight. Furthermore, many Pro-
teaceae are variably pubescent, which increases reflec-
tance and reduces chronic levels of photoinhibition
compared to glabrous leaves (Skelton et al. 2012). CFR
Proteaceae also have specialized lignified epidermal
layers, which selectively screen radiation, thereby dis-
sipating ­excess light (Jordan et al. 2005). Aside from
morphological traits, biochemical processes function
to dissipate ­ excess light (e.g. Demmig-Adams and
Adams 2006), although this has not been extensively
explored in the CFR.
22/08/14 10:32 AM

Closed-canopy forests constitute a small percent-
age of the CFR, but are heterogeneous with respect
to light availability, with light intensities as low as
84 μmol m−2 s−1 in the understorey (Manders 1990).
Consequently the ability to tolerate shade is criti-
cal for forest species to persist. Although CFR forest
and open-habitat species exhibit similarly low pho-
tosynthetic rates (9–16 μmol CO2 m−2 s−1; Richardson
and Kruger 1990), the former display traits typical of
shade-tolerant species (e.g. higher specific leaf area
(6.7 versus 4.2 m2 kg−1) and leaf N content (17.2 versus
7.4 mg g−1); Midgley et al. 1995; Lamont et al. 2002).
These traits enhance the ability of forest species to uti-
lize low levels of often dynamic light (i.e. short-lived
sunflecks), which can account for 10–90% of total
­irradiance in understorey canopies, and drive 32–65%
of daily photosynthesis (Chazdon and Pearcy 1991).
While effective utilization of sunflecks is undoubtedly
important for maintaining a positive carbon balance
in the understorey, little is known about sunfleck utili-
zation in CFR forest species.
Within the CFR, open (mostly fynbos) and closed
(forest) canopy systems are commonly closely juxta-
posed, forming distinct, often sharp boundaries. While
a few forest species (e.g Kiggelaria africana) are able
to establish and grow in open fynbos habitat, fynbos
species are unable to survive in the forest understorey
(Manders and Richardson 1992). The reasons for this
shade intolerance in fynbos species remain unclear.
One possibility is that the oligotrophic fynbos environ-
ment requires carbon demanding traits, which maxi-
mize the acquisition, conservation, and protection of
nutrients. A carbon intensive lifestyle may be diffi-
cult to support in shaded habitats, despite the greater
availability of nutrients (Manders 1990). Hence fynbos
taxa may lack sufficient plasticity to thrive in low-light
environments, being constrained by specialization to
light-saturated but nutrient- and water-limited envir-
onment (Lortie and Aarssen 1996). Given that shade is
an emergent property of forest, this represents a case
of biogenic niche construction for shade-tolerant spe-
cies, implying a role for vegetation in generating habi-
tat heterogeneity.
11.5  The ecophysiological niches of alien
invasive species
The CFR has been extensively invaded (Chapter 12)
by alien vegetation (e.g. Pinus spp., Australian Acacia
spp., Hakea spp., and grasses), raising the question as
to why the vegetation of this region is so susceptible to
invasion? Although invasion is linked to introduction
9780199679584-Allsopp.indb 263
P l a nt ec o ph ysi o l o gic a l diversit y    263
history, reproductive strategies, and the absence of
pests and pathogens, invasive plants also have to com-
pete successfully for resources with indigenous spe-
cies. Many of the common invasive species originate
from nutrient impoverished mediterranean-climate
regions and are thus somewhat ‘pre-adapted’ for
the conditions in CFR. Despite the diversity of traits
­required for successful invasion, plant size is probably
the single most important trait that enables invasion
of woody species (Morris et al. 2011). A large biomass
enhances competition for light and reduces competi-
tive understorey vegetation. Deep-rooting systems
may enable access to otherwise untapped water and
nutrient sources.
Several traits contribute to the ability of alien spe-
cies to grow large. The sclerophyllous and/or phyl-
lodinous foliage of many CFR-invasive species (e.g.
Pinus, Hakea, and Acacia spp.) facilitates tolerance of
drought and nutrient limitation by increasing tissue
rigidity and longevity (the average leaf longevity of
Australian Acacia spp. is 1.8 yr; Morris et al. 2011).
Alien Acacia spp. are also prolific nodulators, acquir-
ing c.50% through N2 fixation (Stock et al. 1995) and
possessing arbuscular mycorrhizas for P acquisition.
In contrast, Pinus spp. rely on extensive ectomycorrhi-
zal networks, while Hakea spp. produce cluster roots
which facilitate P acquisition (Richardson et al. 2000).
Invasive species in the CFR also remobilize nutrients
efficiently prior to leaf abscission; for example, Pinus
radiata remobilized >58% of foliar P (Nambiar and
Fife 1987) and A. saligna remobilized 71% of phyllode
P, which was more than that remobilized by an indi-
genous species Leucospermum parile (48%; Witkowski
1991). The fact that Pinus spp. grow tall in environ-
ments that generally support low stature vegetation
(e.g. fynbos) has been cited as counter-evidence to the
importance of edaphic factors in determining vegeta-
tion height (e.g. Bond 2010). Gymnosperms, however,
have low wood nutrient concentrations (see Bond
2010) as do alien Acacia spp. (Taryn Morris, pers.
comm.), which may permit them to grow tall in areas
where nutrients are scarce.
Thus, several ecophysiological traits act synergis-
tically to determine invasive success by contributing
to the ability of invasive species to accumulate great-
er biomass and to dominate both above and below
ground. The obvious unanswered question is why
no element of the native flora exploits this previous-
ly ‘empty niche’ (sensu MacArthur 1970). The answer
may be that the Cape flora evolved under environmen-
tal conditions (e.g. relating to climate or fire frequen-
cy), which constrained biomass accumulation.
22/08/14 10:32 AM
 264   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n
11.6 Synthesis
This chapter documents the highly diverse ecophysi-
ological challenges that the CFR imposes on the flora
of a region in which there is close juxtaposition of
­diverse edaphic and climate regimes. The nutritional
environment cannot simply be described as ‘nutrition-
ally poor’, since apart from the diversity of overall
­nutritional availabilities, there is also extreme diversity
in the forms of nutrients (e.g. mineral complexes with
P), nutrient ratios (e.g. N:P:K:Ca), and temporal avail-
abilities of nutrients. Likewise, the climatic regime is
diverse and cannot be effectively characterized using
annualized data (e.g. mean annual precipitation or
temperature) because the mediterranean-climate lim-
its the availability of resources by temporal separation
of the optimal light and temperature conditions from
peak water and nutrient availabilities. Superimposed
on this complexity are the emergent flammability and
fire survival characteristics of the vegetation, as well as
its biotic interactions (i.e competition and facilitation;
see Chapter 9). Besides contributing to speciation (e.g.
Linder 1985), this environmental and emergent biotic
complexity has probably enabled the continued main-
tenance of the resulting diversity through the provi-
sion of diverse niches.
Much of the older literature on CFR plant ecophysi-
ology was concerned only with the special character-
istics of the fynbos component of the CFR and how
it deals with the challenges imposed by nutrient
­impoverished soils and a summer-dry climate regime.
In order to understand the plant species richness of the
CFR, however, variations in resource access and con-
servation that exist between the different vegetation
types require further investigation. This demands full
consideration of the multiple interacting factors that
control vegetation characteristics and species com-
position. For example, the boundaries between forest
and fynbos vegetation cannot be considered to be due
simply to ‘vegetation resetting’ fires; rather flamma-
bility is an emergent property driving nutrient losses,
nutrient flushes, and open canopy vegetation whereas
prolonged lack of fire results in nutrient accumula-
tion, heterogeneous light regimes, and access to deep-
er soil resources. The various CFR vegetation types,
with their contrasting levels of combustibility, modify
their own fire regimes, this in turn requiring ecophysi-
ological adaptations or exaptations for coping with
fire. As a consequence, many vegetation characteris-
tics emerge through a process of ‘niche construction’
(sensu Odling-Smee et al. 1996). Thus the vegetation
of the CFR needs to be viewed as being a complex and
9780199679584-Allsopp.indb 264
self-regulating entity that has emerged from a deep
evolutionary and developmental (e.g. pedogenic) his-
tory. This vegetation will continue to change in species
composition under the influence of climatic, invasive
alien, and anthropogenic (e.g. pollution, elevated
CO2) challenges, depending on emergent r­esilience
characteristics. The emergent niche diversity of the
region requires ecophysiological diversity, and thus
the high plant species richness of the CFR should not
be surprising. The contribution of ecophysiological
differentiation should take its place amongst other
explanations for CFR plant species richness and be
incorporated into discussions of the antiquity of the
flora, the tempo of speciation/extinction, and the role
of disturbance in determining the unique floristic rich-
ness of the region.
Acknowledgements
Samson Chimphango, Timm Hoffmann, and Richard
Cowling are thanked for contributing soil chemical
composition data.
References
Adlassnig, W., Peroutka, M., Lambers, H., and Lichrscheidl,
I.K. (2005). The roots of carnivorous plants. Plant and Soil,
274, 127–40.
Aerts, R. (1996). Nutrient resorption from senescing leaves
of perennials: are there general patterns? Journal of Ecol-
ogy, 84, 597–608.
Agenbag, L., Esler, K.J., Midgley, G.F., and Boucher, C.
(2008). Diversity and species turnover on an altitudinal
gradient in Western Cape, South Africa: baseline data for
monitoring range shifts in response to climate change.
Bothalia, 38, 161–91.
Albrecht, W.A. (1957). Soil fertility and biotic geography.
Geographical Review, 47, 86–105.
Allen R.G., Pereira, L.S., Raes, D., and Smith, M. (1998).
Crop evapotranspiration: Guidelines for computing crop
requirements. Irrigation and Drainage Paper No. 56, FAO,
Rome.
Allsopp, N. and Stock, W.D. (1992). Mycorrhizas, seed
size and seedling establishment in a low nutrient
­environment. In D.J. Read, D.H. Lewis, A.H. Fitter, and
I.J.  ­Alexander, eds. Mycorrhizas in ecosystems, pp. 59–64.
Cab International, Wallingford.
Allsopp, N. and Stock, W.D. (1993). Mycorrhizal status of
plants growing in the Cape Floristic Region, South Africa.
Bothalia, 23, 91–104.
Allsopp, N. and Stock, W.D. (1994). VA mycorrhizal infec-
tion in relation to edaphic characteristics and disturbance
regime in three lowland plant communities in the south-
western Cape, South Africa. Journal of Ecology, 82, 271–9.
22/08/14 10:32 AM

Anderson, B. and Midgley, J.J. (2003). Digestive mutualism,
an alternate pathway in plant carnivory. Oikos, 102, 221–4.
Araya, Y.N., Silvertown, J., Gowing, D.J., McConway, K.,
Linder, P., and Midgley, G. (2010). Variation in delta 13C
among species and sexes in the family Restionaceae along
a fine-scale hydrological gradient. Austral Ecology, 35,
818–24.
Araya, Y.N., Silvertown, J., Gowing, D.J., McConway, K.J.,
Linder, H.P., and Midgley, G.F. (2011). A fundamental,
eco-hydrological basis for niche segregation in plant com-
munities. New Phytologist, 189, 253–8.
Bengtsson, J., Janion, C., Chown, S.L., and Leinaas, H.P.
(2011). Variation in decomposition rates in the Fynbos
Biome, South Africa: the role of plant species and plant
stoichiometry. Oecologia, 165, 225–35.
Bond, G. (1971). Fixation of nitrogen in two African species
of Myrica. New Phytologist, 70, 1–8.
Bond, W.J. (1981). Vegetation gradients in the southern Cape.
MSc thesis, University of Cape Town, Cape Town.
Bond, W.J. (2010). Do nutrient-poor soils inhibit develop-
ment of forests? A nutrient stock analysis. Plant and Soil,
334, 47–60.
Bond, W.J. and van Wilgen, B.W. (1996). Fire and the evolu-
tionary ecology of plants. Chapman and Hall, London.
Bradshaw, S.D., Dixon, K.W., Hopper, S.D., Lambers, H.,
and Turner, S.R. (2011). Little evidence for fire-adapted
plant traits in mediterranean climate regions. Trends in
Plant Science, 16, 69–76.
Brown, G. and Mitchell, D.T. (1986). Influence of fire on
the soil phosphorus status in sandplain lowland fynbos,
south western Cape. South African Journal of Botany, 52,
67–72.
Brown, G., Mitchell, D.T., and Stock, W.D. (1984). Atmos-
pheric deposition of phosphorus in a coastal fynbos eco-
system of the Southwestern Cape, South-Africa. Journal of
Ecology, 72, 547–51.
Brundrett, M.C. (2009). Mycorrhizal associations and other
means of nutrition of vascular plants: understanding the
global diversity of host plants by resolving conflicting in-
formation and developing reliable means of diagnosis.
Plant and Soil, 320, 37–77.
Campbell, B. (1986). Plant spinescence and herbivory in a
nutrient poor ecosystem. Oikos, 47, 168–72.
Campbell, B.M. and Werger M.J.A. (1988). Plant form in the
mountains of the Cape, South Africa. Journal of Ecology,
76, 637–53.
Canham, C.A, Froend, R.H., Stock, W.D., and Davies, M.
(2012). Dynamics of phreatophyte root growth relative to
a seasonally fluctuating water table in a mediterranean-
type environment. Oecologia, 170, 909–16.
Chazdon, R.L. and Pearcy, R.W. (1991). The importance of
sunflecks for forest understorey plants. Bioscience, 41,
760–6.
Cocks, M.P. and Stock, W.D. (2001). Field patterns of nodu-
lation in fifteen Aspalathus species and their ecological
role in the fynbos vegetation of southern Africa. Basic and
­Applied Ecology, 2, 115–25.
9780199679584-Allsopp.indb 265
P l a nt ec o ph ysi o l o gic a l diversit y    265
Cody, M.L. (1983). Continental diversity patterns and con-
vergent evolution in bird communities. In F.J. Kruger, D.T.
Mitchell, and J.U.M. Jarvis, eds. Mediterranean-type ecosys-
tems: the role of nutrients, pp 357–402. Springer-Verlag,
Berlin.
Cowling, R.M. (1983). The occurrence of C3 and C4 grasses in
fynbos and allied shrublands in the South Eastern Cape,
South Africa. Oecologia, 58, 121–7.
Cowling, R. and Campbell, B. (1983). A comparison of fyn-
bos and non-fynbos coenoclines in the lower Gamtoos
River Valley, southeastern Cape, South Africa. Vegetatio,
53, 161–78.
Cowling, R.M. and Holmes, P.M. (1992). Flora and vegeta-
tion. In R.M. Cowling, ed. The ecology of fynbos: nutrients,
fire and diversity, pp 23–61. Oxford University Press, Cape
Town.
Cowling, R.M. and Lombard, A.T. (2002). Heterogeneity,
speciation/extinction history and climate: explaining the
regional plant diversity patterns in the Cape Floristic
­Region. Diversity and Distributions, 8, 163–79.
Cowling, R.M., Procheş, Ş., and Partridge, T.C. (2009).
­Explaining the uniqueness of the Cape flora: incorporating
geomorphic evolution as a factor for explaining its diver-
sification. Molecular Phylogenetics and Evolution, 51, 64–74.
Cramer, M.D., Kleizen, C., and Morrow, C. (2007). Does the
prostrate-leaved geophyte Brunsvigia orientalis utilize
soil-derived CO2 for photosynthesis? Annals of Botany, 99,
835–44.
Cramer, M.D. and Midgley, J.J. (2009). Maintenance costs of
serotiny do not explain weak serotiny. Austral Ecology, 34,
653–62.
Cramer, M.D., van Cauter, A., and Bond, W.J. (2010). Growth
of N2-fixing African savanna Acacia species is constrained
by below-ground competition with grass. Journal of Ecol-
ogy, 98, 156–67.
Dean, W., Midgley, J.J., and Stock, W.D. (1994). The distribu-
tion of mistletoes in South Africa: patterns of species rich-
ness and host choice. Journal of Biogeography, 21, 503–10.
Demmig-Adams, B. and Adams III, W.W. (2006). Photopro-
tection in an ecological context: the remarkable complex-
ity of thermal energy dissipation. New Phytologist, 172,
11–21.
Denton, M.D., Veneklaas, E.J., Freimoser, F.M., and ­Lambers,
H. (2007). Banksia species (Proteaceae) from severely
phosphorus-impoverished soils exhibit extreme efficien-
cy in the use and re-mobilization of phosphorus. Plant
Cell and Environment, 30, 1557–65.
Drew, M. (1997). Oxygen deficiency and root metabolism:
injury and acclimation under hypoxia and anoxia. Annual
Review of Plant Biology, 48, 223–50.
Dupont, L.M., Linder, H.P., Rommerskirchen, F., and
­Schefuss, E. (2011). Climate-driven rampant speciation of
the Cape flora. Journal of Biogeography, 38, 1059–68.
Dynesius, M. and Jansson, R. (2000). Evolutionary conse-
quences of changes in species’ geographical distributions
driven by Milankovitch climate oscillations. Proceedings of
the National Academy of Sciences USA, 97, 9115–20.
22/08/14 10:32 AM
 266   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n
Egbert, K.J., Martin, C.E., and Vogelmann, T.C. (2008). The
influence of epidermal windows on the light environment
within the leaves of six succulents. Journal of Experimental
Botany, 59, 1863–73.
Eller, B.M. and Ruess, B. (1982). Water relations of Lithops
plants embedded into the soil and exposed to free air.
Physiologia Plantarum, 55, 329–34.
Elliott, G.N., Chen, W.-M., Chou, J.-H., et al. (2007). Burk-
holderia phymatum is a highly effective nitrogen-fixing
symbiont of Mimosa spp. and fixes nitrogen ex planta.
New Phytologist, 173, 168–80.
Ellis, A.G., Weis, A.E., and Gaut, B.S. (2006). Evolution-
ary radiation of ‘stone plants’ in the genus Argyroderma
(Aizoaceae): unraveling the effects of landscape, habitat
and flowering time. Evolution, 60, 39–55.
Esler, K.J. and Rundel, P.W. (1999). Comparative patterns
of phenology and growth form diversity in two winter
rainfall deserts: the Succulent Karoo and Mojave Desert
ecosystems. Plant Ecology, 142, 97–104.
Esler, K.J., Rundel, P.W., and Vorster, P. (1999). Biogeography
of prostrate-leaved geophytes in semi-arid South Africa:
hypotheses on functionality. Plant Ecology, 142, 105–20.
February, E.C., Bond, W.J., Taylor, R., and Newton, R. (2004).
Will water abstraction from the Table Mountain aquifer
threaten endemic species? A case study at Cape Point,
Cape Town. South African Journal of Science, 100, 253.
February, E.C., Matimati, I., Hedderson, T.A., and Musil,
C.F. (2013). Root niche partitioning between shallow root-
ed succulents in a South African semidesert: implications
for diversity. Plant Ecology, 214, 1181–7.
Finke, D. and Snyder, W. (2008). Niche partitioning ­increases
resource exploitation by diverse communities. Science,
321, 1488–90.
Fitter, A. (1991). Costs and benefits of mycorrhizas: impli-
cations for functioning under natural conditions. Experi-
mentia, 47, 350–5.
Fuggle, R.F. and Ashton, E.R. (1979). Climate. In J. Day, W.R.
Siegfried, G.N. Louw, and M.L. Jarman, eds. Fynbos ecol-
ogy: a preliminary synthesis, pp 7–15. South African Nation-
al Programmes Report 40, Pretoria.
Grierson, P.F. and Comerford, N.B. (2000). Non-destructive
measurement of acid phosphatase activity in the rhizo-
sphere using nitrocellulose membranes and image ana-
lysis. Plant and Soil, 218, 49–57.
Grobbelaar, N., Scott, W.E., Hattingh, W., and Marshall, J.
(1987). The identification of the coralloid root endophytes
of the southern African cycads and the ability of the isolates
to fix dinitrogen. South African Journal of Botany, 53, 111–8.
Groom, P.K. and Lamont, B.B. (2010). Phosphorus accumula-
tion in Proteaceae seeds: a synthesis. Plant and Soil, 334, 61–72.
Hassiotou, F., Evans, J.R., Ludwig, M., and Veneklaas, E.J.
(2009). Stomatal crypts may facilitate diffusion of CO2 to
adaxial mesophyll cells in thick sclerophylls. Plant, Cell
and Environment, 32, 1596–611.
Hawkins, H.-J., Hettasch, H., and Cramer, M.D. (2007). Put-
ting back what we take out, but how much? Scientia Hor-
ticulturae, 111, 378–88.
9780199679584-Allsopp.indb 266
Hawkins, H.-J., Hettasch, H., Mesjasz-Przybylowicz, J.,
Przybylowicz W., and Cramer, M.D. (2008). Phosphorus
toxicity in the Proteaceae: a problem in post-agricultural
lands. Scientia Horticulturae, 117, 357–65.
Hawkins, H.-J., Hettasch, H., West, A.G., and Cramer, M.D.
(2009). Hydraulic redistribution by Protea ‘Sylvia’ (Pro-
teaceae) facilitates soil water replenishment and water
acquisition by an understorey grass and shrub. Functional
Plant Biology, 36, 752–60.
Hawkins, H.-J., Wolf, G., and Stock, W.D. (2005). Cluster
roots of Leucadendron laureolum (Proteaceae) and Lupinus
albus (Fabaceae) take up glycine intact: an adaptive strat-
egy to low mineral nitrogen in soils? Annals of Botany, 96,
1275–82.
Herppich, M., Herppich, W.B., and von Willert, D.J. (2002).
Leaf nitrogen content and photosynthetic activity in rela-
tion to soil nutrient availability in coastal and mountain
fynbos plants (South Africa). Basic and Applied Ecology, 3,
329–37.
Hidaka, A. and Kitayama, K. (2009). Divergent patterns
of photosynthetic phosphorus-use efficiency versus
nitrogen-use efficiency of tree leaves along nutrient-­
availability gradients. Journal of Ecology, 97, 984–91.
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., and
Jarvis, A. (2005). Very high resolution interpolated climate
surfaces for global land areas. International Journal of Cli-
matology, 25, 1965–78.
Hoffman, M.T., Carrick, P.J., Gillson, L., and West, A.G.
(2009). Drought, climate change and vegetation response
in the succulent karoo, South Africa. South African Journal
of Science, 105, 54–60.
Hopper, S.D. (2009). OCBIL theory: towards an integrated
understanding of the evolution, ecology and conserva-
tion of biodiversity on old, climatically buffered, infertile
landscapes. Plant and Soil, 322, 49–86.
Huber, M. and H.P. Linder. (2012). The evolutionary loss of
aerenchyma limits both realized and fundamental ecohy-
drological niches in the Cape reeds (Restionaceae). Journal
of Ecology, 100, 1338–48.
Hunter, R., Hawkins, H.-J., and Cramer, M.D. (2009). Clus-
ter roots of Proteaceae exude acid phosphatase enzymes
as an adaptation to low-P soils, facilitating access to soil
organic-Phosphate. South African Journal of Botany, 75, 406.
Huston, M. (2012). Precipitation, soils, NPP, and biodiversi-
ty: resurrection of Albrecht’s curve. Ecological Monographs,
82, 277–96.
Jacobsen, A.L., Agenbag, L., Esler, K.J., Pratt, R.B., Ewers,
F.W., and Davis, S.D. (2007). Xylem density, biomechan-
ics and anatomical traits correlate with water stress in
17 evergreen shrub species of the mediterranean-type
climate region of South Africa. Journal of Ecology, 95,
171–83.
Jacobsen, A.L., Esler, K.J., Pratt, R.B., and Ewers, F.W. (2009).
Water stress tolerance of shrubs in mediterranean-type
climate regions: convergence of Fynbos and Succulent
Karoo communities with California shrub communities.
American Journal of Botany, 96, 1445–53.
22/08/14 10:32 AM

Jacobsen, A.L., Roets, F., Jacobs, S.M., Esler, K.J., and Pratt,
R.B. (2012). Dieback and mortality of South African fyn-
bos shrubs is likely driven by a novel pathogen and
pathogen-induced hydraulic failure. Austral Ecology, 37,
227–35.
Jenny, H. (1941). Factors of soil formation. A system of quan-
titative pedology, pp 281. McGraw-Hill, New York.
Jeschke, W.D. and Pate, J.S. (1995). Mineral nutrition and
transport in xylem and phloem of Banksia prionotes and
proteaceous trees of dimorphic root morphology. Journal
of Experimental Botany, 46, 895–905.
Jordan, G.J., Dillon, R.A., and Weston, P.H. (2005). Solar ra-
diation as a factor in the evolution of scleromorphic leaf
anatomy in Proteaceae. American Journal of Botany, 92,
789–96.
Jordan, G.J., Weston, P.H., Carpenter, R.J. Dillon, R.A., and
Brodribb, T.J. (2008). The evolutionary relations of sunk-
en, covered, and encrypted stomata to dry habitats in Pro-
teaceae. American Journal of Botany, 95, 521–30.
Justin, S. and Armstrong, W. (1987). The anatomical charac-
teristics of roots and plant response to soil flooding. New
Phytologist, 106, 465–95.
Kanu, S.A. and Dakora, F.D. (2012). Symbiotic nitrogen con-
tribution and biodiversity of root-nodule bacteria nodu-
lating Psoralea species in the Cape Fynbos, South Africa.
Soil Biology and Biochemistry, 54, 68–76.
Keeley, J. and Bond, W. (1997). Convergent seed germin-
ation in South African fynbos and Californian chaparral.
Plant Ecology, 133, 153–67.
Klironomos, J., Zobel, M., and Tibbett, M. (2011). Forces that
structure plant communities: quantifying the import-
ance of the mycorrhizal symbiosis. New Phytologist, 189,
366–70.
Kluge, M., Knapp, I., Kramer, D. Schwerdtner, I., and Ritter,
H. (1979). Crassulacean acid metabolism (CAM) in leaves
of Aloe arborescens mill. Planta, 145, 357–63.
Kreft, H. and Jetz, W. (2007). Global patterns and determin-
ants of vascular plant diversity. Proceedings of the National
Academy of Sciences USA, 104, 5925–30.
Lambers, H., Cawthray, G.R., Giavalisco, P., et al. (2012).
Proteaceae from severely phosphorus-impoverished soils
extensively replace phospholipids with galactolipids and
sulfolipids during leaf development to achieve a high
photosynthetic phosphorus-use-efficiency. New Phytolo-
gist, 196, 1098–108.
Lambers, H, Raven, J.A, Shaver, G.R., and Smith, S.E. (2008).
Plant nutrient-acquisition strategies change with soil age.
Trends in Ecology and Evolution, 23, 95–103.
Lambers, H., Shane, M.W., Cramer, M.D., Pearse, S.J., and
Veneklaas, E.J. (2006). Root structure and functioning for
­efficient acquisition of phosphorus: matching morphologi-
cal and physiological traits. Annals of Botany, 98, 693–713.
Lamont, B.B. (1972). The effect of soil nutrients on the pro-
duction of proteoid roots by Hakea species. Australian
Journal of Botany, 20, 27–40.
Lamont, B.B. (1982). Mechanisms for enhancing nutrient up-
take in plants, with particular reference to mediterranean
9780199679584-Allsopp.indb 267
P l a nt ec o ph ysi o l o gic a l diversit y    267
South Africa and Western Australia. The Botanical Review,
48, 597–689.
Lamont, B.B. and Downes, K.S. (2011). Fire-stimulated
flowering among resprouters and geophytes in Australia
and South Africa. Plant Ecology, 212, 2111–25.
Lamont, B.B., Groom, P., and Cowling, R.M. (2002). High
leaf mass per area of related species assemblages may re-
flect low rainfall and carbon isotope discrimination rather
than low phosphorus and nitrogen concentrations. Func-
tional Ecology, 16, 403–12.
Lechmere-Oertel, R.G. and Cowling, R.M. (2001). Abiotic
determinants of the fynbos/succulent karoo boundary,
South Africa. Journal of Vegetation Science, 12, 75–80.
Le Maitre, D.C. and Midgley, J.J. (1992). Plant reproductive
ecology. In R.M. Cowling, ed. The ecology of fynbos, nutri-
ents, fire and diversity, pp 135–74. Oxford University Press,
Cape Town.
Linder, H.P. (1985). Gene flow, speciation, and species diver-
sity patterns in a species-rich area: the Cape Flora. In E.S.
Vrba, ed. Species and speciation, 53–7. Transvaal Museum,
Pretoria.
Linder, H.P. (2003). The radiation of the Cape flora, southern
Africa. Biological Reviews, 78, 597–638.
Linder, H.P. (2005). Evolution of diversity: the Cape flora.
Trends in Plant Science, 11, 536–41.
Linder, H.P. (2008). Plant species radiations: where, when,
why? Philosophical Transactions of the Royal Society B, 363,
3097–105.
Linder, H.P., Johnson, S.D., Kuhlmann, M., Matthee, C.A.,
Nyffeler, R., and Swartz, E.R. (2010). Biotic diversity in the
Southern African winter rainfall region. Current Opinion
in Environmental Sustainability, 2, 109–16.
Lortie, C. and Aarssen, L. (1996). The specialization hypoth-
esis for phenotypic plasticity in plants. International Jour-
nal of Plant Sciences, 157, 484–7.
Low, A.B. and Lamont, B.B. (1990). Aerial and below ground
phytomass of Banksia scrub-heath at Eneabba, south-west
Australia. Australian Journal of Botany, 38, 351–9.
MacArthur, R.H. (1970). Species packing and competitive
equilibrium for many species. Theoretical Population Biol-
ogy, 1, 1–11.
Manders, P.T. (1990). Fire and other variables as determi-
nants of forest/fynbos boundaries in the Cape Province.
Journal of Vegetation Science, 1, 483–90.
Manders, P.T. and Richardson. D.M. (1992). Colonization of
Cape fynbos communities by forest species. Forest Ecology
and Management, 48, 277–93.
Marloth, R. (1903). Results of experiments on Table Moun-
tain for ascertaining the amount of moisture d ­ eposited
from the south-east clouds. Transactions of the South
­African Philosophical Society, 14, 403–8.
McDowell, N.G., Beerling, D.J., Breshears, D.D., Fisher, R.A.,
Raffa, K.F., and Stitt, M. (2011). The interdependence of
mechanisms underlying climate-driven vegetation mor-
tality. Trends in Ecology and Evolution, 26, 523–32.
Metzler, W. (1924). Beitrage zur vergleichenden Anatomie
blattsukkulenter Pflanzen. Botanisches Archiv, 6, 50–83.
22/08/14 10:32 AM
 268   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n
Midgley, J.J. (1996). Why the world’s vegetation is not totally
dominated by resprouting plants; because resprouters are
shorter than reseeders. Ecography, 19, 92–5.
Midgley, J.J. (2013). Flammability is not selected for, it
emerges. Australian Journal of Botany, 61, 102–6.
Midgley, J.J. and Enright, N. (2000). Serotinous species show
correlation between retention time for leaves and cones.
Journal of Ecology, 88, 348–51.
Midgley, J.J. and Stock, W. (1998). Natural abundance of
δ15N confirms insectivorous habit of Roridula gorgonias,
despite it having no proteolytic enzymes. Annals of Bot-
any, 82, 387–8.
Midgley, J.J., van Wyk, G.R., and Everard, D.A. (1995). Leaf
attributes of South African forest species. African Journal
of Ecology, 33, 160–8.
Milewski A.V. (1983). A comparison of ecosystems in medi-
terranean Australia and southern Africa: nutrient-poor
sites at the Barrens and the Caledon Coast. Annual Review
of Ecology and Systematics, 14, 57–76.
Miller, A.J. and Cramer, M.D. (2005). Root nitrogen acquisi-
tion and assimilation. Plant and Soil, 274, 1–36.
Mitchell, D.T., Brown, G., and Jongens-Roberts, S.M. (1984).
Variation of forms of phosphorus in the sandy soils of
coastal fynbos, south-western Cape. Journal of Ecology, 72,
575–84.
Mitchell, D. and Coley, P. (1987). Litter production and de-
composition from shrubs of Protea repens growing in sand
plain lowland and mountain fynbos, south-western Cape.
South African Journal of Botany, 53, 25–31.
Mitchell, D., Coley, P., Webb, S., and Allsopp, N. (1986). Lit-
terfall and decomposition processes in the coastal fynbos
vegetation, South-western Cape, South Africa. Journal of
Ecology, 74, 977–93.
Mooney, H.A., Field, C., Gulmon, S.L., and Bazzazz, F.A.
(1983). Photosynthetic characteristics of South African
sclerophylls. Oecologia, 58, 398–401.
Moore, T.E. (2010). Nutritional niches and the evolution of spe-
cialized foraging traits in the genus Thesium (Santalaceae).
Unpublished MSc thesis, University of Cape Town, Cape
Town.
Morris, T.L., Esler, K.J., Barger, N.N., Jacobs, S.M., and
Cramer, M.D. (2011). Ecophysiological traits associated
with the competitive ability of invasive Australian aca-
cias. Diversity and Distributions, 17, 898–910.
Mu, Q., Heinsch, F.A., Zhao, M., and Running, S.W. (2007).
Development of a global evapotranspiration algorithm
based on MODIS and global meteorology data. Remote
Sensing of Environment, 111, 519–36.
Mucina, L. and Rutherford, M. (2006). The vegetation of South
Africa, Lesotho and Swaziland. Strelitzia 19. South African
National Biodiversity Institute, Pretoria.
Naeem, S., Thompson, L.J., Lawler, S.P., et al. (1994). Declin-
ing biodiversity can alter the performance of ecosystems.
Nature, 368, 734–7.
Nambiar, E.K.S. and Fife, D.N. (1987). Growth and nutrient
retranslocation in needles of radiata pine in relation to
­nitrogen supply. Annals of Botany, 60, 147–56.
9780199679584-Allsopp.indb 268
Nicotra, A.B., Cosgrove, M.J., Cowling, A., Schlichting, C.D.,
and Jones, C.S. (2008). Leaf shape linked to photosynthet-
ic rates and temperature optima in South African Pelargo-
nium species. Oecologia, 154, 625–35.
Nobel, P.S. (1989).Shoot temperatures and thermal toler-
ances for succulent species of Hawthoria and Lithops. Plant
Cell and Environment, 12, 643–51.
Ochoa-Hueso, R., Allen, E.B., Branquinho, C., et al. (2011).
Nitrogen deposition effects on mediterranean-type eco-
systems: an ecological assessment. Environmental Pollu-
tion, 159, 2265–79.
Odling-Smee, F.J., Laland, K.N., and Feldman, M.W. (1996).
Niche construction. American Naturalist, 147, 641–8.
Ojeda, F. (1998). Biogeography of seeder and resprouter
Erica species of the Cape Floristic Region—where are the
resprouters? Biological Journal of the Linnean Society, 63,
331–47.
Orians, G.H. and Solbrig, O.T. (1977). A cost-income mod-
el of leaves and roots with special reference to arid and
­semiarid areas. American Naturalist, 111, 677–90.
Pate, J., Verboom, W., and Galloway, P. (2001). Co-­occurrence
of Proteaceae, laterite and related oligotrophic soils:
­coincidental associations or causative inter-relationships?
Australian Journal of Botany, 49, 529–60.
Pau, S., Edwards, E.J., and Still, C.J. (2013). Improving our
understanding of environmental controls on the distribu-
tion of C3 and C4 grasses. Global Change Biology, 19, 184–96.
Pierce, S. (1984). Synthesis of plant phenology in the Fynbos
Biome. Foundation for Research Development, CSIR, Pre-
toria.
Power, S., Cramer, M.D., Verboom, G.A., and Chimphan-
go, S.B.M. (2010). Does phosphate acquisition constrain
legume persistence in the fynbos of the Cape Floristic
­Region? Plant and Soil, 334, 33–46.
Pratt, R.B., Jacobsen, A.L., Jacobs, S.M., and Esler, K.J. (2012).
Xylem transport safety and efficiency differ among fyn-
bos shrub life history types and between two sites differ-
ing in mean rainfall. International Journal of Plant Sciences,
173, 474–83.
Press, M.C. and Phoenix, G.K. (2005). Impacts of parasitic
plants on natural communities. New Phytologist, 166,
737–51.
Procheş, Ş., Cowling, R.M., and Du Preez, D.R. (2005). Pat-
terns of geophyte diversity and storage organ size in the
winter rainfall region of southern Africa. Diversity and
Distributions, 11, 101–9.
Radloff, F.G.T., Mucina, L., Bond, W.J., and Le Roux, P.J.
(2010). Strontium isotope analyses of large herbivore
habitat use in the Cape Fynbos region of South Africa.
Oecologia, 164, 567–78.
Rebelo, A.G., Le Maitre, D., Schutte-Vlok, A., et al. (2009).
Alarming plant dieback in the Outeniquas: is this an indi-
cation of global warming? Veld and Flora, 95, 38–9.
Reid, P.C.M. and De Jager, J.M. (1988). Geographical dis-
tribution of monthly mean daily global solar radiation
over South Africa. South African Journal of Plant and Soil,
6, 46–9.
22/08/14 10:32 AM

Richards, M., Cowling, R., and Stock, W. (1997). Soil nutrient
dynamics and community boundaries in the fynbos vege-
tation of South Africa. Plant Ecology, 130, 143–53.
Richardson, D.M., Allsopp, N., D’Antonio, C.M., Milton,
S.J., and Rejmánek, M. (2000). Plant invasions-the role of
mutualisms. Biological Reviews of the Cambridge Philosophi-
cal Society, 75, 65–93.
Richardson, D.M. and Kruger, F.J. (1990). Water relations
and photosynthetic characteristics of selected trees and
shrubs of riparian and hillslope habitats in the south-
western Cape Province South Africa. South African Journal
of Botany, 56, 214–25.
Ripley, B.S., Abraham, T., Klak, C., and Cramer, M.D. (2013).
How succulent leaves of Aizoaceae avoid mesophyll
conductance limitations of photosynthesis and survive
drought. Journal of Experimental Botany, 64, 5485–96.
Rossa, B. and von Willert, D.J. (1999). Physiological charac-
teristics of geophytes in semi-arid Namaqualand, South
Africa. Plant Ecology, 142, 121–32.
Roth-Nebelsick, A., Hassiotou, F., and Veneklaas, E.J. (2009).
Stomatal crypts have small effects on transpiration: a
­numerical model analysis. Plant Physiology, 151, 2018–27.
Rundel, P. W., Esler, K.J., and Cowling, R.M. (1999). Eco-
logical and phylogenetic patterns of carbon isotope dis-
crimination in the winter rainfall flora of the Richtersveld,
South Africa. Plant Ecology, 142, 133–48.
Salleo, S., Nardini, A., and Lo Gullo, M.A. (1997). Is scle-
rophylly of Mediterranean evergreens an adaptation to
drought? New Phytologist, 135, 603–12.
Schimper, A.F.W. (1903). Plant geography upon a physiological
basis. Clarendon Press, Oxford.
Schmidt, S., Mason, M., Sangtiean, T., and Stewart, G.R.
(2003). Do cluster roots of Hakea actities (Proteaceae)
­acquire complex organic-Nitrogen? Plant and Soil, 248,
157–65.
Shane, M.W., Cawthray, G.R., Cramer, M.D., Kuo, J.J., and
Lambers, H. (2006). Specialized ‘dauciform’ roots of
Cyperaceae are structurally distinct, but functionally
­ D.M. Richardson, and S.M. Pierce, eds. Vegetation of
analogous with ‘cluster’ roots. Plant, Cell Environment, 29,
1989–99.
Shane, M.W., Cramer, M.D., and Lambers, H. (2008). Root of
edaphically controlled Proteaceae turnover on the Agul-
has Plain, South Africa: phosphate uptake regulation and
growth. Plant, Cell and Environment, 31, 1825–33.
Shane, M.W., Szota, C., and Lambers, H. (2004). A root trait
accounting for the extreme phosphorus sensitivity of
Hakea prostrata (Proteaceae). Plant Cell and Environment,
27, 991–1004.
Silvertown, J., Araya, Y.N., Linder, H.P., and Gowing, D.J.
(2012). Experimental investigation of the origin of fynbos
plant community structure after fire. Annals of Botany, 110,
1377–83.
Silvertown, J., Dodd, M.E., Gowing, D.J.G., and Mountford,
J.O. (1999). Hydrologically defined niches reveal a basis for
species richness in plant communities. Nature, 400, 61–3.
Skelton, R.P., Midgley, J.J., Nyaga, J.M. Johnson, S.D.,
and  Cramer, M.D. (2012). Is leaf pubescence of Cape
9780199679584-Allsopp.indb 269
P l a nt ec o ph ysi o l o gic a l diversit y    269
­loristic Region Proteaceae a xeromorphic or photo-­
F
protective trait? Australian Journal of Botany, 60, 104–13.
Slingsby, J.A. and Verboom, G.A. (2006). Phylogenetic
relatedness limits co-occurrence at fine spatial scales:
­
evidence from the Schoenoid sedges (Cyperaceae: Schoe-
neae) of the Cape Floristic Region, South Africa. American
Naturalist, 168, 14–27.
Smith, D. (2000). The population dynamics and community
ecology of root hemiparasitic plants. American Naturalist,
155, 13–23.
Smith, S.E., Read, D.J., and Harley, J.L. (2002). Mycorrhizal
symbiosis (2nd edition). Academic Press, London.
Sniderman, J.M.K., Jordan, G.J., and Cowling, R.M. (2013).
Fossil evidence for a hyperdiverse sclerophyll flora u ­ nder
a non-mediterranean-type climate. Proceedings of the
­National Academy of Sciences USA, 110, 3423–8.
Soderberg, K. and Compton, J.S. (2007). Dust as a nutrient
source for fynbos ecosystems, South Africa. Ecosystems,
10, 550–61.
Spriggs, A.C. (2004). Symbiotic N2 fixation in cultivated Cyclo-
pia Vent. spp. (honeybush): towards sustainable cultivation in
the Western Cape of South Africa. Unpublished MSc thesis,
University of Cape Town, Cape Town.
Spriggs, A., Stock, W., and Dakora, F. (2003). Mycorrhizal
associations on foliar δ15N values of legume and non-­
legume shrubs and trees in the fynbos of South Africa:
implications for estimating N2 fixation using. Plant and
Soil, 255, 495–502.
Still, C.J., Berry, J.A., Collatz, G.J., and DeFries, R.S. (2003).
Global distribution of C3 and C4 vegetation: carbon cycle
implications. Global Biogeochemical Cycles, 17, 1006.
Stock, W.D. and Allsopp, N. (1992). Functional perspectives
of ecosystems. In R.M. Cowling, ed. The ecology of fynbos;
nutrients, fire and diversity, pp 241–59. Oxford University
Press, Cape Town.
Stock, W.D., Allsopp. N., van der Heyden, F., and ­Witkowski,
E.T.F. (1997). Plant form and function. In R.M.  ­Cowling,
southern Africa, pp 367–97. Cambridge University Press,
­Cambridge.
Stock, W.D. and Lewis, O.A.M. (1982). Extraction of nitrate
reductase from members of the South African Proteaceae.
South African Journal of Botany, 14, 201–21.
Stock, W.D. and Lewis, O.A.M. (1984). Uptake and assimi-
lation of nitrate and ammonium by an evergreen fynbos
shrub species Protea repens L. (Proteaceae). New Phytolo-
gist, 97, 261–8.
Stock, W.D. and Lewis, O.A.M. (1986). Soil nitrogen and
the role of fire as a mineralizing agent in a South African
coastal fynbos ecosystem. Journal of Ecology, 74, 317–28.
Stock, W.D., Lewis, O.A.M., and Allsopp, N. (1988). Soil
­nitrogen mineralization in a coastal fynbos succession.
Plant and Soil, 106, 295–8.
Stock, W.D., Pate, J.S., and Delfs, J. (1990). Influence of seed
size and quality on seedling development under low
­nutrient conditions in five Australian and South African
members of the Proteaceae. Journal of Ecology, 78, 1005–20.
22/08/14 10:32 AM
 270   F y nb o s : E c o l o g y, E v o l u ti o n, a nd C o nservati o n o f a M eg a diverse R egi o n
Stock, W., Sommerville, J., and Lewis, O.A.M. (1987). Sea-
sonal allocation of dry mass and nitrogen in a fynbos en-
demic Restionaceae species Thamnochortus punctatus Pill.
Oecologia, 72, 315–20.
Stock, W.D. and Verboom, G.A. (2012). Phylogenetic ecol-
ogy of foliar N and P concentrations and N:P ratios across
mediterranean-type ecosystems. Global Ecology and Bioge-
ography, 21, 1147–56.
Stock, W.D., Wienand, K.T., and Baker, A.C. (1995). Impacts
of invading N2-fixing Acacia species on patterns of nutri-
ent cycling in two Cape ecosystems: evidence from soil
incubation studies and 15N natural abundance values. Oe-
cologia, 101, 375–82.
Thuiller, W., Lavorel, S., Midgley, G., Lavergne, S., and
­Rebelo, A.G. (2004). Relating plant traits and species dis-
tributions along bioclimatic gradients for 88 Leucadendron
taxa. Ecology, 85, 1688–19.
Thwaites, R.N. and Cowling, R.M. (1988). Soil-vegetation
relationships on the Agulhas Plain, South Africa. Catena,
15, 333–45.
Trabucco, A. and Zomer, R.J. (2009). Global Arid-
ity Index (Global-Aridity) and Global Potential Evapo-­
Transpiration (Global-PET) Geospatial Database. CGIAR
Consortium for Spatial Information. Available at <http://
www.csi.cgiar.org>.
Turner, B.L., Lambers, H., Condron, L.M., et al. (2013). Soil
microbial biomass and the fate of phosphorus during long-
term ecosystem development. Plant and Soil, 367, 225–34.
Turner, J.S. and Picker, M.D. (1993). Thermal ecology of an
embedded dwarf succulent from southern Africa (Lithops
spp: Mesembryanthemaceae). Journal of Arid Environ-
ments, 24, 361–85.
van Reenen, C.A., Visser, G.J., and Loos, M.A. (1992). Soil
microorganisms and activities in relation to season, soil
factors and fire. In B.W. van Wilgen, D.M. Richardson, F.J.
Kruger, and H.J. van Hensbergen, eds. Fire in South A ­ frican
mountain fynbos, pp 258–72. Springer-Verlag, Berlin.
van Rooyen, M.W. (1999). Functional aspects of short-lived
plants. In W.R.J. Dean and S.J. Milton, eds. The karoo:
ecological patterns and processes, pp 107–22. Cambridge
­University Press, Cambridge.
Verboom, G.A., Moore, T.E., Hoffmann, V., and Cramer,
M.D. (2012). The roles of climate and soil nutrients in
shaping the life histories of grasses native to the Cape
Floristic Region. Plant and Soil, 355, 323–40.
Verboom, G.A., Stock, W.D., and Linder, H.P. (2002). De-
terminants of postfire flowering in the geophytic grass
Ehrharta capensis. Functional Ecology, 16, 705–13.
Vermeulen, T. (2010). Plant water relations of Elytropappus rhi-
nocerotis with specific reference to soil restrictions on growth.
MSc Agric thesis, Stellenbosch University, Stellenbosch.
Veste, M., Herppich, W.B., and von Willert, D. J. (2001).
Variability of CAM in leaf-deciduous succulents from the
9780199679584-Allsopp.indb 270
­ ucculent Karoo (South Africa). Basic and Applied Ecology,
S
2, 283–8.
Visser, J. (1981). South African parasitic flowering plants. Juta,
Cape Town.
Vitousek, P.M., Cassman, K., Cleveland, C., et al. (2002).
­Towards an ecological understanding of biological nitro-
gen fixation. Biogeochemistry, 57/58, 1–45.
Vitousek, P.M., Porder, S., Houlton, B.Z., and Chadwick, O.
(2010). Terrestrial phosphorus limitation: mechanisms,
implications, and nitrogen-phosphorus interactions. Eco-
logical Applications, 20, 5–15.
Vogel, S. and Müller-Doblies, U. (2011). Desert geophytes
under dew and fog: the ‘curly-whirlies’ of Namaqualand
(South Africa). Flora, 206, 3–31.
Walker, T.C. and Syers, J.K. (1976). The fate of phosphorus
during pedogenesis. Geoderma, 15, 1–19.
Wessels, K., Steenkamp, K., Von Maltitz, G., and Archibald,
S. (2011). Detecting inter-annual variability in the phenologic-
al characteristics of southern Africa’s vegetation using satel-
lite imagery. CSIR Researchspace, Pretoria.
West, A.G., Dawson, T.E., February, E.C., Midgley, G.F.,
Bond, W.J., and Aston, T.L. (2012). Diverse functional re-
sponses to drought in a mmediterranean-type shrubland
in South Africa. New Phytologist, 195, 396–407.
Wilson, D., Stock, W.D., and Hedderson, T. (2009). Histori-
cal nitrogen content of bryophyte tissue as an indicator
of increased nitrogen deposition in the Cape Metro-
politan Area, South Africa. Environmental Pollution, 157,
938–45.
Witkowski, E.T.F. (1991). Effects of invasive alien acacias on
nutrient cycling in the coastal lowlands of the Cape Fyn-
bos. Journal of Applied Ecology, 28, 1–15.
Witkowski, E.T.F. and Lamont, B.B. (1996). Disproportionate
allocation of mineral nutrients and carbon between vege-
tative and reproductive structures in Banksia hookeriana.
Oecologia, 105, 38–42.
Witkowski, E.T.F., Mitchell, D.T., and Stock, W.D. (1990).
Response of a Cape fynbos ecosystem to nutrient addi-
tions: shoot growth and nutrient contents of a proteoid
(Leucospermum parile) and an ericoid (Phylica cephalantha)
evergreen shrub. Acta Oecologia, 11, 311–26.
Yates, M.J., Verboom, G.A., Rebelo, A.G., and Cramer, M.D.
(2010). Ecophysiological significance of leaf size variation
in Proteaceae from the Cape Floristic Region. Functional
Ecology, 24, 485–92.
Young, G.M., Minter, W.E.L., and Theron, J.N. (2004).
Geochemistry and palaeogeography of upper Ordovi-
­
cian glaciogenic sedimentary rocks in the Table Mountain
Group, South Africa. Palaeogeography, Palaeoclimatology
and Palaeoecology, 214, 323–45.
Zhao, M.S. and Running, S.W. (2010). Drought-induced
reduction in global terrestrial net primary production
­
from 2000 through 2009. Science, 329, 940–3.
22/08/14 10:32 AM
9780199679584-Allsopp.indb 271
Appendix 11.1  Summary of the properties of soils underlying four principal Cape Floristic Region vegetation types (Chapter 1). Soil samples from the top 0.3 m of soil were dried and sieved (1 mm
mesh) and measured as described in Cramer et al. (2010). pH was measured in 1 M KCl extracts and exchangeable cations (cmol+ kg−1) were displaced from 10 g soil with 25 mL of 0.2 M ammonium
acetate. Additional data are from Thwaites and Cowling (1988). Values are mean ± standard error and, in parentheses, the 5% percentile, median, and 95% percentiles. Since sampling was unequal
across vegetation types and unequally dispersed, this is intended as a broad indication of the heterogeneous distribution of nutrients across the CFR, rather than as a basis for quantitative comparison.

Soil property Vegetation type and number of replicate samples

Fynbos n Renosterveld n Thicket n Succulent karoo n

pH (KCl) 4.5 ± 0.1 (3, 4.5, 7.3) 281 5.1 ± 0.1 (4, 4.8, 7.1) 82 6.6 ± 0.2 (4, 7.1, 8.5) 49 5.5 ± 0.5 (4.5, 5, 7.9) 9
EC (mS m−1) 12 ± 1 (3, 8, 31) 199 14 ± 2 (3, 9, 40) 65 27 ± 9 (5, 14, 38) 43 20 ± 6 (4, 13, 52) 9
H+ (cmol kg−1) 1.57 ± 0.07 (0.45, 1.23, 3.79) 229 0.83 ± 0.06 (0.3, 0.66, 1.57) 60 2.13 ± 0.29 (0.47, 2.09, 4.17) 18 0.73 ± 0.1 (0.45, 0.69, 1.04) 7
C (%) 2.3 ± 0.1 (0.5, 1.7, 5.2) 281 1.6 ± 0.1 (0.4, 1, 5.2) 82 2.5 ± 0.4 (0.1, 1.4, 8) 49 1.2 ± 0.4 (0.2, 0.5, 3.3) 9
N (%) 0.17 ± 0.01 (0.04, 0.12, 0.42) 278 0.12 ± 0.01 (0.03, 0.08, 0.31) 80 0.21 ± 0.03 (0.04, 0.12, 0.65) 45 0.12 ± 0.03 (0.04, 0.09, 0.24) 7
Total P (mg kg−1) 249 ± 10 (89, 234, 447) 196 279 ± 45 (28, 293, 463) 11 1313 ± 490 (131, 227, 5184) 22 90 ± 11 (74, 88, 108) 3
Bray II P (mg kg−1) 13.3 ± 1.7 (0.7, 5.6, 50.5) 282 13.3 ± 1.2 (2.2, 10, 32) 82 141.3 ± 62.8 (1.6, 16, 1008.6) 49 16 ± 4.2 (6.4, 11, 36.6) 9
K (mg kg−1) 84 ± 5 (13, 61, 254) 202 143 ± 16 (4, 133, 449) 80 133 ± 23 (4, 85, 282) 43 204 ± 67 (46, 136, 523) 9
+
Na (cmol kg−1) 0.22 ± 0.03 (0.04, 0.14, 0.48) 280 0.35 ± 0.04 (0.03, 0.26, 1.21) 80 0.46 ± 0.25 (0.06, 0.15, 0.57) 48 0.36 ± 0.1 (0.14, 0.24, 0.88) 9
K (cmol+ kg−1) 0.24 ± 0.02 (0.04, 0.17, 0.65) 279 0.38 ± 0.04 (0.01, 0.34, 1.16) 80 0.32 ± 0.05 (0.02, 0.21, 0.71) 48 0.52 ± 0.17 (0.12, 0.35, 1.34) 9
Ca (cmol+ kg−1) 3.7 ± 0.3 (0.4, 1.7, 15.6) 280 5.2 ± 1 (0.1, 2.6, 30.5) 80 10.9 ± 1.2 (1.8, 9.2, 22.8) 48 5.9 ± 2 (1.1, 3.9, 16) 9
Mg (cmol+ kg−1) 1.3 ± 0.1 (0.1, 0.8, 3.9) 278 2.3 ± 0.4 (0, 1.4, 10.8) 80 1.7 ± 0.3 (0.2, 1, 4.6) 48 2 ± 0.5 (0.4, 1.8, 4) 9
Cu (mg kg−1) 3.5 ± 1.2 (0.1, 1.6, 6.1) 121 0.9 ± 0.1 (0.2, 0.9, 1.8) 43 20.8 ± 7.2 (12.4, 14.4, 38.3)  4 0.5 ± 0.4 (0.1, 0.2, 1.2) 3
Zn (mg kg −1) 8.1 ± 1.4 (0.2, 3, 23.4) 122 1.2 ± 0.2 (0.3, 0.8, 3.7) 43 49.9 ± 10.2 (30.1, 50.8, 68.5)  4 2.1 ± 0.8 (1, 1.7, 3.4) 3
Mn (mg kg−1) 65 ± 7 (2, 22, 204) 122 51 ± 6 (10, 35, 105) 43 237 ± 69 (139, 187, 406)  4 34 ± 16 (18, 19, 60) 3
B (mg kg −1) 11.8 ± 0.9 (0.2, 9.3, 28.4) 120 0.9 ± 0.4 (0.2, 0.5, 1.2) 29 43.5 ± 15.5 (24.2, 30.3, 81.1)  4 0.6 ± 0.1 (0.4, 0.6, 0.7) 3
Fe (mg kg−1) 4772 ± 456 (12, 3113, 12,744) 112 295 ± 191 (9, 91, 290) 32 9664 ± 1689 (7309, 8416, 13,768)  4 66 ± 60 (5, 7, 210) 4

22/08/14 10:32 AM
 View publication stats
9780199679584-Allsopp.indb 272
Appendix 11.2  Summary of elevational and climatic conditions within the biomes of South Africa, as defined by Mucina and Rutherford (2006). Values shown are the 5% percentiles, means (in parentheses), and
95% percentiles of points sampled on a 5 km grid (72 < n < 7 688) across South Africa. The mean annual temperatures (MAT), temperature (T) ranges, mean temperatures (MT) in year quarters (q), mean annual
precipitation (MAP), precipitation (P) seasonality, potential evapotranspiration (PET), and actual evapotranspiration (AET) are given. Climate data are averaged 1950–2000 (Hijmans et al. 2005), PET is from the
Penman–Monteith equation (Allen et al. 1998) obtained from Trabucco and Zomer (2009), and modelled estimates of ET were obtained from NASA (MODIS 16; Mu et al. 2007).

Biome Elevation (m) MAT (°C) Mean T range MT MT driest MT MT MAP (mm) P P wettest q P driest q P warmest q P coldest q PET (mm) AET (mm)
diurnal (°C) wettest q q (°C) warmest coldest q seasonality (mm) (mm) (mm) (mm)
T range (°C) q (°C) (°C)
(°C)

Fynbos 77 (742) 1513 12 (15) 18 10 (13) 16 18 (24) 29 8 (13) 19 9 (17) 23 17 (20) 23 6 (10) 14 213 (460) 856 14 (39) 69 75 (171) 361 26 (68) 140 28 (80) 192 56 (154) 359 1097 (1314) 1510 218 (304) 479
Succulent 240 (763) 1398 13 (16) 19 13 (16) 17 22 (28) 31 11 (15) 20 10 (19) 24 19 (22) 25 7 (11) 14 100 (219) 404 19 (40) 69 37 (80) 133 11 (33) 71 12 (41) 111 34 (68) 112 1321 (1513) 1687 206 (231) 284
Karoo
Albany 107 (581) 1061 15 (17) 19 9 (14) 15 16 (24) 28 17 (20) 23 10 (13) 16 19 (22) 24 10 (12) 15 260 (441) 757 16 (35) 46 91 (150) 249 34 (66) 120 69 (134) 243 35 (68) 127 1148 (1414) 1563 212 (380) 869
Thicket
Azonal 324 (923) 1379 15 (18) 20 14 (16) 17 25 (30) 34 13 (21) 25 9 (13) 24 21 (23) 26 8 (11) 14 133 (314) 573 31 (57) 81 49 (137) 265 11 (28) 58 19 (117) 264 11 (34) 77 1442 (1591) 1743 205 (268) 445
Desert 304 (575) 904 17 (19) 22 13 (15) 18 23 (28) 32 14 (21) 26 13 (19) 24 21 (25) 28 12 (13) 15 64 (91) 144 41 (54) 82 24 (38) 65 7 (10) 14 11 (21) 48 8 (21) 34 1411 (1654) 1904 226 (238) 247
Forests 108 (831) 1750 14 (17) 22 9 (12) 15 16 (20) 25 14 (20) 25 9 (13) 18 18 (20) 25 9 (13) 18 570 (899) 1154 11 (53) 80 202 (371) 588 38 (86) 188 189 (365) 588 38 (89) 197 1112 (1291) 1459 526 (853) 117
Grassland 942 (1568) 2465 10 (15) 17 12 (15) 16 20 (26) 32 14 (19) 22 4 (9) 13 15 (19) 22 4 (9) 13 473 (708) 986 48 (66) 79 198 (319) 478 21 (42) 66 178 (310) 477 21 (43) 67 1142 (1382) 1547 200 (403) 704
Indian 26 (195) 445 18 (20) 22 8 (9) 10 14 (16) 19 21 (23) 25 15 (17) 18 21 (23) 25 15 (17) 18 933 (1032) 1137 35 (45) 51 347 (379) 410 86 (112) 146 345 (377) 410 88 (112) 146 1094 (1221) 1388 573 (833) 1208
Coastal
Nama- 708 (1083) 1477 14 (17) 19 15 (16) 17 27 (31) 34 18 (21) 25 7 (11) 13 20 (23) 26 7 (10) 12 158 (250) 411 30 (57) 75 59 (110) 182 11 (26) 47 41 (87) 160 11 (28) 51 1417 (1583) 1736 191 (221) 249
Karoo
Savanna 241 (938) 1456 16 (19) 22 10 (14) 17 18 (26) 32 20 (23) 26 10 (14) 18 20 (23) 26 10 (14) 18 329 (613) 994 48 (76) 93 173 (297) 442 8 (30) 87 147 (290) 442 8 (31) 89 1249 (1576) 1752 206 (472) 910

22/08/14 10:32 AM