Plant mineral nutrition

Abstract

Plant life in the kwongan has evolved on some of the world’s most nutrient-impoverished sandy soils. The availability of phosphorus (P) is particularly low on these sandy soils, but soil nitrogen (N), potassium (K) and micronutrients are also notoriously scarce (McArthur, 1991). The extreme infertility of most kwongan soils is primarily due to the low nutrient content of the parent material that gave rise to the sand and to their old age and strong degree of weathering. Over time, weathering leads to the loss of key rock-derived nutrients (e.g., P) in the absence of major soil-rejuvenating processes (e.g., glaciations, volcanic eruptions) (Walker & Syers, 1976; Laliberté et al., 2012). On the other hand, nitrogen, a nutrient derived from the atmosphere, is continuously lost from the system, predominantly as a result of fire, when most N is volatilised (Orians & Milewski, 2007). Nitrogen fixation is therefore crucially important to compensate for these losses (see also Chapter 1). As a result, widespread agricultural development of these infertile sandy soils in the 1950s commenced only after the critical need for application of P, sulfur (S), K and micronutrients, particularly copper (Cu) and zinc (Zn), for pasture establishment, had been established (Yeates, 1993).

Full text

101
CHAPTER 4: PLANT MINERAL NUTRITION
Hans Lambers, Michael W. Shane, Etienne Laliberté,
Nigel Swarts, François Teste, Graham Zemunik
INTRODUCTION
PLANT LIFE IN THE KWONGAN has evolved on some of the world’s most nutrient-impoverished sandy
soils. e availability of phosphorus (P) is particularly low on these sandy soils, but soil nitrogen (N), potassium
(K) and micronutrients are also notoriously scarce (McArthur, 1991). e extreme infertility of most kwongan
soils is primarily due to the low nutrient content of the parent material that gave rise to the sand and to their old
age and strong degree of weathering (see chapter 1A for more information). Over time, weathering leads to the
loss of key rock-derived nutrients (e.g., P) in the absence of major soil-rejuvenating processes (e.g., glaciations,
volcanic eruptions) (Walker & Syers, 1976; Laliberté et al., 2012). On the other hand, N, a nutrient derived
from the atmosphere, is continuously lost from the system, predominantly as a result of re, when most N
is volatilised (Orians & Milewski, 2007). Nitrogen xation is therefore crucially important to compensate
for these losses (see also chapter 1). As a result, widespread agricultural development of these infertile sandy
soils in the 1950s commenced only after the critical need for application of P, sulfur (S), K and micronutrients,
particularly copper (Cu) and zinc (Zn), for pasture establishment, had been established (Yeates, 1993).
Given that extreme soil infertility imposes a severe constraint to plant growth, one might expect the
kwongan ora to show low diversity, composed of only a restricted number of plant species that evolved
the necessary adaption(s) to successfully grow on these infertile soils. Yet the exact opposite is actually
found, and a key feature of kwongan is its exceptionally high degree of oristic and functional diversity
(Lambers et al., 2010). Interestingly, the greatest biodiversity on the sandplains is found on the most
severely P-impoverished soils (Fig. 1).
In this chapter, we present the main nutrient-acquisition strategies displayed by kwongan species and
discuss their functioning. First, we focus on non-mycorrhizal species with specialised root adaptations
to acquire P, as they are especially abundant on the sandplains (Lambers et al., 2010). Many of these
specialised root adaptations would also enhance the acquisition of micronutrients, as discussed below.
Second, we present the dierent types of mycorrhizal strategies that are found in kwongan, focusing on
possible relationships between soil fertility and mycorrhizal type. ird, we present several symbiotic
systems that contribute to N
2
xation, including the nodules of the legume-rhizobium symbiosis (Lange,
1961), the rhizothamnia of sheoaks and Frankia, an actinomycete (Becking, 1970), and the coralloid
roots of cycads and cyanobacteria (Halliday & Pate, 1976). Finally, the specialised nutrient-acquisition
strategies of the many carnivorous and parasitic species in the kwongan are discussed.

KWONGAN PLANT LIFE
1 0 2
Figure 1. Plant diversity and soil phosphorus
(P) status in south-western Australia’s
global biodiversity hotspot. Note the relative
abundance of non-mycorrhizal species on
soils with the lowest P content / total P
concentration. Plant diversity and soil data
are from a comprehensive floristic survey
of over 1000 quadrats in the wheatbelt of
Western Australia by Gibson
et al.
(2004).
Modified after Lambers
et al.
(2010).
ADAPTATIONS TO COPE WITH A LOW P AVAILABILITY
Non-mycorrhizal strategies
On the most severely P-impoverished soils in south-western Australia, plant diversity is greatest (Lambers
et al., 2010). at is where non-mycorrhizal species rule. e number of non-mycorrhizal species
is greatest when soil P level is lowest (Fig. 1), and this is where the relative cover of non-mycorrhizal
Proteaceae species is highest (Fig. 2). Conversely, on less P-impoverished soils, mycorrhizal species
dominate (Lambers et al., 2006; 2010). is is in contrast with much younger landscapes, where non-
mycorrhizal species belonging to certain families, e.g., Amaranthaceae, Brassicaceae, Caryophyllaceae,
Chenopodiaceae, Polygonaceae and Urticaceae (Tester et al., 1987; Wang & Qiu, 2006) tend to occupy
disturbed and relatively nutrient-rich sites (Allen & Allen, 1980; Francis & Read, 1994). ese families
that are typically associated with nutrient-rich soils are poorly represented or totally absent on the south-
western Australian sandplains (Lambers & Teste, 2013).
A plant family that is richly represented on severely P-impoverished soils in the kwongan and similar
landscapes in South Africa are the Proteaceae (Cowling & Lamont, 1998; Pate & Bell, 1999). Most of
the species in this family produce proteoid roots (Fig. 3) (Purnell, 1960) and almost all of them are non-
mycorrhizal (Shane & Lambers, 2005a); an exception is the mycorrhizal species Hakea verrucosa, which
grows on the ultramac rocks of Bandalup Hill which are rich in nickel (Ni) (Boulet & Lambers, 2005).
e carboxylate-releasing strategy, which is typical for species with proteoid roots, would mobilise Ni on
ultramac soils (Robinson et al., 1996), and thus cause Ni toxicity (Lambers et al., 2008a). Proteoid roots
are dense clusters of rootlets of limited growth; the rootlets develop numerous root hairs (Lamont, 2003;
Shane & Lambers, 2005a). Since proteoid roots are not restricted to Proteaceae, the term ‘cluster roots’ is
commonly used as an alternative (Shane & Lambers, 2005a).

CHAPTER 4: PLANT MINERAL NUTRITION
103
Figure 2. The canopy cover of Proteaceae and
non-Proteaceae species as dependent on soil
phosphorus (P) concentration along the Jurien
Bay chronosequence. Proteaceae are generally
only found on P-impoverished soils, where
their cover is about half of all other species
combined. Note that the values do not add up
to 100%, because of the presence of bare soil.
On the sandplains, cluster roots are predominantly produced near the surface, just under the litter layer or
an ash bed after a re; however, when organic matter is present at greater depth, cluster roots can also be
found lower in the soil prole (Lamont, 1973). is suggests that cluster roots are produced in response
to slightly elevated levels of P, but they are suppressed at higher P supply (Lamont et al., 1984; Shane
& Lambers, 2005a). Cluster roots release vast amounts of carboxylates in an ‘exudative burst’ (Watt &
Evans, 1999; Shane et al., 2004a); the carboxylates mobilise P that is sorbed onto soil particles; the P
then becomes available for uptake by plant roots (Fig. 4) (Lambers et al., 2006). erefore, cluster roots
eectively ‘mine’ P that is unavailable for plants without this strategy. Outside the Proteaceae, cluster roots
in kwongan species can be expected in some Casuarinaceae (Reddell et al., 1997), Fabaceae (Lamont,
1972; Brundrett & Abbott, 1991) and Restionaceae species (Lambers et al., 2006), but it should be noted
that in Casuarinaceae and Restionaceae so far only deal with species outside Western Australia. Both the
Restionaceae and Anarthriaceae also produce capillaroid roots (Lamont, 1982), but whether capillaroid
roots are associated with ecient P acquisition remains to be explored.
Dauciform (i.e. carrot-shaped) roots occur in some tribes of the Cyperaceae (Davies et al., 1973;
Lamont, 1974; Shane et al., 2006b), another common predominantly non-mycorrhizal family on nutrient-
impoverished soils in the kwongan. Dauciform roots are morphologically very dierent from cluster roots
(Fig. 5), but functionally quite similar; they also release vast amounts of carboxylates in an exudative
burst, and are suppressed at high P supply (Shane et al., 2006a).
Signicant amounts of carboxylates can also be exuded by kwongan species in the absence of
specialised structures like cluster roots and dauciform roots, e.g., in a range of Kennedia species (Fabaceae)
from south-western Australia (Ryan et al., 2012). ese species dier vastly in the amount of carboxylates
they release. However, they have in common that their carboxylate exudation is reduced in the presence of
arbuscular mycorrhizal fungi, which colonise the roots of some Kennedia species. Other Kennedia species
are non-mycorrhizal (Ryan et al., 2012). is suggests a trade-o in plant carbon allocation to either
mycorrhizal fungi or carboxylate release for P acquisition.

KWONGAN PLANT LIFE
1 0 4
Figure 3. Variation in cluster-root morphology of different woody species of Proteaceae. (a) ‘Simple’ proteoid roots, typical of,
e
.
g
.,
Hakea
species, develop a
bottlebrush-like morphology. The main root is perennial and proteoid rootlet initiation (far left) to senescence (far right) occurs over approximately 21 days in
Hakea
prostrata
grown in hydroponics at extremely low [Pi] ≤ 1 µM (photos: Michael W. Shane). (b) and (c) Relatively large volumes of soil become tightly bound to maturing
proteoid roots of field-grown
Hakea
ceratophylla
(photos: Michael W. Shane). (d) ‘Compound’ proteoid roots typical of
Banksia
species develop a Christmas-tree-like
morphology. Hydroponically-grown
Banksia attenuata
showing proteoid rootlet initiation (far left) to maturity (far right) over 15 days (photos: Michael W. Shane). (e) A
thick proteoid root-mat typically develops just beneath leaf litter of field-grown
Banksia
attenuata
. (f) Rootlets of
Banksia attenuata
growing in an ash bed after a fire
(photos: Marion L. Cambridge). Scale bars in mm (a) 13; (b) 30; (c) 7; (d) 22; (e) 34; (f) 15.
a
b
e
d
c
f

CHAPTER 4: PLANT MINERAL NUTRITION
105
Figure 4. Effects of carboxylates (and other
exudates) on inorganic (P
i
) and organic P (P
o
)
mobilisation in soil. Carboxylates (organic
anions) are released via an anion channel.
The exact way in which phosphatases are
released is not known. Carboxylates mobilise
both inorganic and organic P
1
and P
o
, which
both sorb onto soil particles. The carboxylates
effectively take the place of P, thus pushing it
in solution. Phosphatases hydrolyse organic P
compounds, once these have been mobilised
by carboxylates. Carboxylates will also chelate
some of the cations that bind P, especially iron
(Fe), and other micronutrients. Chelated Fe
moves to the root surface, where it is reduced
followed by uptake by the roots, via a Fe
2+
transporter. This transporter is not specific,
but also transports other micronutrients,
such as manganese (Mn), copper (Cu) and
zinc (Zn), which have been mobilised by
carboxylates in soil. The carboxylates allow P
to be ‘mined’, as opposed to the ‘scavenging’
strategy of mycorrhizas. For further
explanation, see text; modified after Lambers
et al.
(2008a).
e leaves of Proteaceae in general (Jaré, 1979; Rabier et al., 2008; Fernando et al., 2009), including
species in the kwongan (Shane & Lambers, 2005b), produce carboxylate-releasing cluster roots, and
contain relatively high levels of manganese (Mn) in their leaves. is has also been found for Fabaceae
species with cluster roots, e.g., Lupinus albus (Gardner et al., 1982) and Aspalathus linearis (Morton,
1983). is is explained by the ability of cluster roots to mobilise Mn (Gardner et al., 1981; Grierson
& Attiwill, 1989; Dinkelaker et al., 1995). Leaf Mn levels might therefore provide an indication of the
extent to which roots rely on carboxylate release to acquire P (Shane & Lambers, 2005b). Following this
approach, we recently found that non-mycorrhizal species along a 2-million-year chronosequence near
Jurien Bay (chapter 1; Laliberté et al., 2012) have higher leaf Mn concentrations than their neighbours
without any of the carboxylate-releasing strategies discussed above, regardless of soil age. High Mn levels
were found in leaves that produce sand-binding roots, similar to cluster-rooted Proteaceae and dauciform-
rooted Cyperaceae (Hayes et al., 2013). It is therefore likely that the signicance of sand-binding roots in
Haemodoraceae, Restionaceae and Anarthriaceae (Fig. 5) (Shane et al., 2011; Smith et al., 2011) is also,
at least partly, that of mobilisation of P due to the release carboxylates or compounds with a similar eect.
is warrants further investigation.

KWONGAN PLANT LIFE
1 0 6
Figure 5. Variation in root morphology of different grass-like species. (a and b) Cyperaceae. (a) Field-grown
Schoenus unispiculatus
showing a shoot with attached
perennial roots and ephemeral ‘dauciform’ (= carrot-shaped) roots (arrow). Dauciform roots tightly bind numerous sand grains (inset). (b) Root axes of hydroponically-
grown plants showing numerous, relatively large, dauciform roots (
Schoenus unispiculatus
, left axis) compared with smaller dauciform roots developed in series
(three arrow heads) (
Carex fascicularis
, right axis). (c – f) Anarthriaceae (c) Field-grown
Lyginia
barbata
showing relatively large sand-covered perennial main
root axis (sand-binding root) with small ephemeral branch roots attached (capillaroid roots, arrows). Individual sand-binding roots were collected after one year’s
growth initially directed (arrow) into 500-mm PVC tubes (20 mm diameter) containing native soil. Tubes were open at the top and sealed at the bottom (inset). (d)
Remarkable development of numerous, long roots hairs on a main root, and of fine capillaroid roots of a
L
.
barbata
plant grown in hydroponics at extremely low [P] ≤
1 µM. (e) Field-grown perennial sand-binding roots of
L
.
barbata
and (f) a thick sheath of sand grains tightly bound at the root surface (photos: Michael W. Shane).
Scale bars in mm (a) 7 (inset) 3; (b) 3; (c) 12 (inset) 52; (d) 28; (e) 21; (f) 1.5.
a
e
c
b
f
d

CHAPTER 4: PLANT MINERAL NUTRITION
107
e high abundance of Proteaceae in severely P-impoverished landscapes is not exclusively accounted for
by their very ecient P-acquisition strategy. In addition, at least three other traits determine their high P
eciency and their success on P-impoverished soils. First, their leaf P concentrations are extremely low
(Pate & Dell, 1984; Denton et al., 2006), and their rate of photosynthesis per unit leaf P is among the
highest ever recorded (Wright et al., 2004; Denton et al., 2007) which is partly accounted for by extensive
replacement of phospholipids by lipids that do not contain P (Lambers et al., 2012). Second, their long-
lived leaves are very ecient and procient at remobilising P during leaf senescence (Denton et al., 2007,
Hayes, 2014). ird, their seeds, unlike their vegetative tissues, contain very high concentrations of P
(Denton et al., 2007; Groom & Lamont, 2010). ese nutrient reserves, rather than the reserves of carbon,
determine the early growth of Hakea seedlings (Lamont & Groom, 2002). In Banksia hookeriana, half of
all the P in aboveground plant parts may be in their seeds, which comprise only half a per cent of all the
aboveground biomass (Witkowski & Lamont, 1996). Very similar results have been found for Banksia
species in South Australia (Groves et al., 1986). Seed set in Banksia species in kwongan tends to be very
low, especially in species that resprout after re; commonly only a few per cent of all the owers produce
seeds (Fuss & Sedgley, 1991; Lamont & Wiens, 2003). Since seed set can be increased by addition of
nutrients (Stock et al., 1989), low seed set appears to be a mechanism allowing seedlings to grow without
an external P source for a prolonged period (Hocking, 1982; Milberg & Lamont, 1997). Some of the
P-eciency traits that are common in Proteaceae may well occur in other kwongan species, but these have
received far less attention.
While Proteaceae and several other species that are endemic to south-western Australia are very good
at acquiring P and using it eciently, many are extremely sensitive to P-toxicity symptoms (Shane et al.,
2004b; Standish et al., 2007; Hawkins et al., 2008; Lambers et al., 2013). Even a slight increase of the low
P concentration that is common in their natural environment is enough to severely disturb their growth
and may cause death. While it is relatively common in P-impoverished landscapes, P sensitivity is by
no means universal among species from P-impoverished habitats, and even some Proteaceae species are
insensitive to elevated P supply, e.g., Grevillea crithmifolia (Shane & Lambers, 2006). e physiological
mechanism accounting for P toxicity in higher plants is their very low capacity to down-regulate their P
uptake system (Shane et al., 2004c; Shane & Lambers, 2006; de Campos et al., 2013a). eir low capacity
to down-regulate P uptake is associated with a high capacity to remobilise P from senescing leaves, and
vice versa (de Campos et al., 2013a), but whether this association is based on a mechanistic link involving
the control of P transporters is not known.
Mycorrhizal symbioses
Mycorrhizal associations can enhance P acquisition from low-P soils by their ‘scavenging’ strategy
(Lambers et al., 2008b; Smith & Read, 2008). e mycorrhizal hyphae extend the surface available for
P uptake beyond that of root hairs, exploring sites that the root hairs cannot reach. All mycorrhizal
symbioses are capable of this, including the most widespread and ancient arbuscular mycorrhizal
symbiosis. e other main mycorrhizal symbioses include ectomycorrhizas, ericoid mycorrhizas, and
orchid mycorrhizas.
Unlike ectomycorrhizas, arbuscular mycorrhizal fungi give rise to intracellular structures, that are
invariably outside the root cells’ plasma membrane (Fig. 6; Cairney, 2000). Arbuscular mycorrhizas are

KWONGAN PLANT LIFE
1 0 8
widespread on the south-western Australian sandplains, but not quite as common as in the rest of the
world (Fig. 7; Brundrett, 2009). is may reect the fact that most south-western Australian soils are very
old and thus depleted in P. At very low soil P concentrations, arbuscular mycorrhizas are not as eective in
enhancing plant P uptake (Partt, 1979), because the strategy relies mostly on ‘scavenging’ easily-available
P, and not on enhancing P availability through chemical alteration of the mycorhizosphere (Lambers et
al., 2006; 2008b). Following uptake, P is transported via hyphae towards the roots; inside the root cortex,
P is released from the hyphae in intracellular structures called arbuscules, and subsequently taken up by
root cells (Parniske, 2008). In exchange, root cells provide photosynthetically xed carbon to the fungal
partner (Smith & Read, 2008; Kiers et al., 2011).
Figure 6. Mycorrhizal structures. (a–c)
Arbuscular mycorrhizal structures, including
a mycorrhizal spore (b) and an arbuscule
in a root of
Spyridium globulosum
(c). (d)
Hartig net of an ectomycorrhizal fungus
in a root of
Spyridium globulosum
. (e–f)
Ericoid mycorrhizal structures; (e)
Astroloma
xerophyllum
hair root stained with lactophenol
cotton blue. (g) Orchidaceous mycorrhizal
fungi of the genus
Pterostylis
; seedling
stem of
Pterostylis sanguinea
with hyphal
outgrowths on water agar. Photos: a–b,
François P. Teste; c–d, Graham Zemunik; e–h,
Kingsley W. Dixon.
a
e
c
g
b
f
d

CHAPTER 4: PLANT MINERAL NUTRITION
109
Figure 7. The relative importance of
specialised nutritional strategies for flowering
plants in Western Australia (
i.e.
not just
the south-west, but the south-west would
represent ¾ of the total flora) in comparison
with the whole world. Data are the ratio of
actual over expected numbers of species.
Categories of plants with bars extending to
the right of the vertical broken line are more
diverse in Western Australia than they are
on a global scale. Modified after Brundrett
(2009). EM: ectomycorrhizal species; NM all
non-mycorrhizal species; Monocot RC SB: all
species with dauciform roots (Cyperaceae),
capillaroid roots (Restionaceae and
Anarthriaceae) and sand-binding roots; AM,
arbuscular mycorrhizal.
Ectomycorrhizal symbioses are far more common in the ancient landscapes of Western Australia than
they are elsewhere (Fig. 7; Brundrett, 2009). ere is evidence that ectomycorrhizas are more eective
than arbuscular mycorrhizas at enhancing plant P uptake when soil P concentrations are lower (e.g.,
older, more strongly-weathered soils; Lambers et al., 2006; 2008b). Ectomycorrhizas function not only
as ‘scavengers’ of P, like arbuscular mycorrhizas, but they may also release carboxylates and enzymes that
give them access to organic forms of both P and N (Landeweert et al., 2001; Van Hees et al., 2006; Van
Schöll et al., 2008). e fungal hyphae usually penetrate the roots intercellularly to form the Hartig net,
where exchange of nutrients acquired by the fungal hyphae and carbon provided by the plant take place
(Smith & Read, 2008) (Fig. 6). Ectomycorrhizas are common in species belonging to Casuarinaceae,
Fabaceae, Myrtaceae and Rhamnaceae, but some of these can also form arbuscular mycorrhizal symbioses
(Brundrett, 2009) or produce cluster roots, e.g., Viminaria juncea (Lamont, 1972; de Campos et al., 2013b).
Ericoid mycorrhizas are typical for species belonging to Ericaceae (Fig. 6) (Brundrett, 2009). Similar
to arbuscular mycorrhizas, a large fraction of the fungal tissues is within the root cortical cells (Smith
& Read, 2008). Ericoid mycorrhizal roots, like ectomycorrhizas, also have access to additional chemical
pools of P. ey may release phosphatases, which enhance the availability of organic P, and exude
carboxylates, which increase the availability of sparingly soluble P (Landeweert et al., 2001; Van Leerdam
et al., 2001; Van Hees et al., 2006). As a result, it has been suggested that ericoid mycorrhizas should be
particularly eective at enhancing plant P uptake on very old, P-impoverished soils, where organic P can
represent an important fraction of the total soil P pool and where P can be strongly sorbed to soil minerals
(Lambers et al., 2008b).
About 50 plant species from the genus ysanotus form mycorrhizas that have a unique morphology.
e ‘ysanotus mycorrhizas’ are characterised by hyphae that penetrate between epidermal cells and
ramify between cortex and epidermis (McGee, 1988). Supercially, it appears like an altered morphology,
or one that is neither arbuscular mycorrhizal nor ectomycorrhizal. Interestingly, some of the fungi
responsible for ysanotus mycorrhizas do form arbuscular mycorrhizas and ectomycorrhizas on other
host plants, and some growth promotion has been observed (McGee, 1988). Studies on the Jurien Bay
chronosequence (chapter 1A), have provided evidence of additional altered mycorrhizal morphologies on
other plant genera(G. Zemunik, unpubl.). We suspect there is likely even greater diversity of nutrient-
acquisition strategies in kwongan than previously thought.

KWONGAN PLANT LIFE
11 0
Finally, orchid mycorrhizas are conned to the family Orchidaceae (Fig. 6) (Brundrett, 2009).
Like in arbuscular mycorrhizas, a large fraction of the fungal tissues is within the root cortical
cells, as fungal coils, rather than arbuscules (Smith & Read, 2008). As soon as the orchid seeds have
germinated, the seedlings, which have very few reserves, depend on nutrients contained in the organic
matter soil layer which are supplied via the mycorrhizal fungus. Most terrestrial orchid mycorrhizal
fungi are basidiomycetes and belong to the form-genus Rhizoctonia, a diverse group of asexual fungi also
comprising plant pathogens and saprophytes. Rhizoctonia species may form mycorrhizal associations
with both orchids and conifers; however, the very few conifers in kwongan have not yet been studied
in this context. Orchids with a limited capacity to photosynthesise (mycoheterotrophs), such as orchids
from south-western Australia, are generally considered parasitic on the fungus, where the association
between host and fungus does not appear to be mutually benecial (Leake, 2004). Even orchids that
have the ability to photosynthesise may form an ectomycorrhizal association with forest trees, and their
stable nitrogen- and carbon-isotope signatures indicate a dependency on ectomycorrhizas (Bidartondo et
al., 2004). However, more recent research is challenging this notion, with some photosynthetically active
orchids demonstrating net exchange of carbon between plant and fungus (Cameron et al., 2008). In the
underground orchid, Rhizanthella gardneri, which remains non-photosynthetic during its entire life cycle,
the fungus continues to play this role (Batty et al., 2004).
Orchids appear to be substantially under-represented in the Southwest Australian Floristic Region
(SWAFR), relative to plants with other nutrient-acquisition strategies (Fig. 7). is may seem surprising,
given that the region is well known for its large orchid diversity (approx. 400 species) (Brown et al.,
2008). However, the Orchidaceae contain over 25,000 species worldwide, with the vast majority of
orchids being either tree-dwelling or rock-dwelling in equatorial rainforests. e lack of epiphytes (both
orchids and non-orchids) on the south-western Australian sandplains might reect the absence of suitable
climatic conditions for this life form. e hot, dry summers and cool conditions in winter and spring
are much more suited to terrestrial species, which live underground as tubers in summer, re-sprouting
in autumn and winter, when conditions are cooler and soils moist. Epiphytes may also require some of
the traits that succulents have; this is another life style that is poorly represented in kwongan (chapter
5). Yet, it is unlikely that only these selection pressures or the competition for mycorrhizal partners to
acquire nutrients have contributed to the vast diversity in the Orchidaceae. Rather, the specialisation of
pollination systems through modication of oral signals (chapter 7B), particularly in the tropics where
competition for pollinators is ercest, have been integral to orchid diversication (Johnson & Steiner,
2000). In summary, the under-representation of orchids in kwongan (Fig. 7) is most likely due to the
scarcity of epiphytic species in kwongan, rather than specic aspects of their nutrient-acquisition strategy.
SYMBIOTIC NITROGEN FIXATION
In any terrestrial ecosystem, N is continuously lost through leaching and denitrication. In kwongan,
losses as a result of combustion of nitrogenous compounds during res are also a major component of
the N cycle at the ecosystem level. ese losses have to be compensated for the cycle to continue. While
lightning does generate nitrous oxides, this component is small (Hill et al., 1984). Global estimates of N

CHAPTER 4: PLANT MINERAL NUTRITION
111
xed by lightning are less than 10 Tg per year (Tg = 1012 g or 106 metric tons) (Galloway et al., 1995).
Biological N
2
xation accounts for most of the input into ecosystems, estimated at 90–130 Tg per year on
the continents (Galloway et al., 1995; Vitousek et al., 1997).
Two techniques are commonly used to assess biological N
2
xation. e rst is qualitative; it is based
on the principle that the enzyme that reduces N
2
to NH
3
also reduces acetylene (C
2
H
2
) to ethylene (C
2
H
4
),
which is readily measured by gas chromatography (Dilworth, 1966). is technique demonstrates whether
certain structures are capable of xing N
2
or not, but it cannot reliably be used to assess how much they
are xing, because nodule activity rapidly declines in the presence of acetylene (Minchin et al., 1983). e
second is more quantitative, provided basic assumptions are met; it uses the stable isotope
15
N, which can
be measured by mass spectrometry (Minchin et al., 1983; Hansen et al., 1987). Since the
15
N abundance
of N
2
in air and of soil N tend to dier, the natural
15
N abundance is frequently used to estimate the
contribution of biological N
2
xation to the total amount of N acquired by a plant (Shearer & Kohl, 1986).
A non-xing reference plant is required to determine the
15
N abundance in the absence of N
2
xation, and
therein lays a problem in that the basic assumption is that both species access the same source of soil N.
If the mycorrhizal partners of the two plants dier, i.e. one being arbuscular mycorrhizal and the other
ectomycorrhizal, then the natural
15
N abundance technique may give erroneous results (Högberg, 1990).
If the plants that are compared access their N from dierent depth and the
15
N abundance diers with
depth, then the
15
N abundance technique cannot be used either (Robinson, 2001). Despite these problems the
natural
15
N abundance technique is a valuable tool in ecological research (Handley & Scrimgeour, 1997).
Legumes in association with rhizobia play a prominent role in N
2
xation on the south-western
Australian sandplains (Fig. 8), especially during winter after a re (Hingston et al., 1982; Hansen & Pate,
1987). Water stress is the main reason for a decrease in N
2
xation in summer (Hansen & Pate, 1987).
A decline in symbiotic N
2
xation with increase in time after a re is at least partly accounted for by a
decrease in P availability (Hingston et al., 1982; Hansen et al., 1991). Acacia pulchella, a species that is
very common following a re, sharply declines to 30% of its original high density immediately after a re
by year four, and to less than 8% 13 years after a re (Monk et al., 1981). Progressive death of the plants
in the populations returns 1.9 kg N per ha per yr; the remainder is provided by litter (1 kg N per ha per
yr) and shed seed (1 kg N per ha per yr). While this re-following legume acquires most N from soil
immediately after a re, about 70% is derived from symbiotic N
2
xation by year four after a re (Monk et
al., 1981). Legumes tend to have a high demand for P (Hartwig, 1998), which is at least partly accounted
for by rapid rates of turnover of oxygen-damaged nitrogenase, the enzyme responsible for converting N
2
into NH
3
. Nitrogenase is very sensitive to oxygen, and its repair by turnover requires ribosomal RNA,
which represents a major fraction of P in nodules. Raven (2012) estimated that a maximum of 12% of
non-storage P could occur in RNA associated with replacement of damaged nitrogenase and/or oxygen-
damage-avoidance mechanism in N
2
-xing organisms. While the dogma is that legumes have a high
demand for P, this may be biased by most studies focusing on crop species (Sprent, 1999). Moreover,
many legumes on south-western Australian sandplains also have adaptations to acquire P from low-P
soils, including cluster roots in Viminaria juncea (Lamont, 1972) and Daviesia species (Brundrett &
Abbott, 1991), release of phosphatases in Lotus australis and Kennedia prorepens (Denton et al., 2006),
and exudation of carboxylates in the absence of specialised structures, e.g., in several Kennedia species
(Pang et al., 2010; Ryan et al., 2012). Most legumes in the kwongan also establish mycorrhizal symbioses

KWONGAN PLANT LIFE
11 2
(Brundrett & Abbott, 1991).
Figure 8. Structures involved in symbiotic N
2
fixation in species of (a) sheoak, (b) legume, and (c – d) cycad. (a) Rhizothamnia (arrow heads) composed of
dichotomously branched nodules on a perennial root of
Allocasuarina humilis
collected in Lesueur National Park. Nodules contain Actinobacteria (
Frankia
). (b)
Senesced remains of short-lived cluster roots (white arrows), and living nodules (orange arrows) on a perennial root of
Viminaria juncea
(broom bush). Reddish
coloration in a cross-section of a nodule (inset) shows location of symbionts. (c) Intact apogeotropic coralloid roots, freshly unearthed and attached to (d)
Macrozamia
fraseri
where coralloid roots encircle the base of the plant and are exposed underneath a thin layer of soil or litter. (e) Blue–green coloration in a transverse section
through a coralloid root shows location of symbionts inside the root (arrow heads) (photos: Michael W. Shane). Scale bars in mm (a) 14; (b) 18; (inset) 1.5; (c) 5; (d)
24; (e) 12.
a
c
b
ed

CHAPTER 4: PLANT MINERAL NUTRITION
113
In addition to numerous legumes, sheoaks (Casuarina and Allocasuarina) also form a N
2
-xing symbiosis,
with Frankia (Actinomycota) as the microsymbiont (Fig. 8) (Bond, 1957; Becking, 1970). e symbiotic
structures in actinorhizal plants are commonly referred to as rhizothamnia (Mowry, 1933) or nodules
(Torrey & Racette, 1989). Most studies on symbiotic N
2
xation in Casuarinaceae species focused on
those that are not endemic in Western Australia, and these are the studies summarised here. ere is
distinct host specicity among Casuarina and Allocasuarina species, with some Frankia strains capable
of forming nodules on many species and others on very few (Reddell & Bowen, 1985; Torrey & Racette,
1989). As with the growth of legumes, growth of Casuarina equisetifolia, when dependent on symbiotically
xed N
2
, is more sensitive to low levels of P than is growth of seedlings supplied with nitrate; at higher
levels of P, the growth-response curves are similar for both N-fertilised and inoculated plants (Sanginga
et al., 1989). Under glasshouse conditions, nodulated plants of C. cunninghamiana and C. equisetifolia grow
vigorously in nutrient solution free of an N source other than N
2
(Bond, 1957). Under eld conditions, C.
equisetifolia can obtain up to 67% of its N from symbiotic N
2
xation (Parrotta et al., 1994). Since studies
on Casuarinaceae species in the kwongan are rare, we can only extrapolate from studies on species that
occur elsewhere, leading to the impression that sheoaks could contribute signicantly to biological N
2
xation on the south-western Australian sandplains.
Coralloid roots are structures arising from the roots of cycads (Grobbelaar et al., 1971; Lindblad et al.,
1985) (Fig. 8). ese structures can host cyanobacterial symbionts of the genus Nostoc and Calothrix, with
little evidence for host specialisation (Gehringer et al., 2010). Precoralloid structures form in the absence
of a microsymbiont (Wittmann et al., 1965; Nathanielsz & Sta, 1975; Ahern & Sta, 1994). Like other
cyanobacteria, those in coralloid roots produce neurotoxins, and this accounts for the severe toxicity of
cycad tissues (Lindblad et al., 1990; Charlton et al., 1992). e microsymbonts in coralloid roots may also
produce other toxins, including nodularin (Gehringer et al., 2012). e toxicity of Macrozamia riedlei to
cattle was well-known to early settlers, and known as ‘rickets’ or ‘wobbles’ (Gardiner & Bennetts, 1956;
Gabbedy et al., 1975). Coralloid roots x N
2
at physiologically signicant rates, mainly during the wet
season in winter, capable of doubling plant N content every 8–11 years (Halliday & Pate, 1976). Grove
et al. (1980) found that the ratio of weight of coralloid roots to weight of boles of M. riedlei plants was
greatest on a recently burnt site. Concentrations of N in coralloid roots were signicantly higher in plants
growing on a recently burnt site. is suggests that rates of N
2
xation are driven by the demand of rapidly
regrowing leaves after a re.
By examining trade-os inherent in plant carbon, N and P capture, Houlton et al. (2008) suggest
a clear advantage to symbiotic N
2
-xing species in some P-limited systems in that these species invest
N into P-acquisition, i.e. phosphatases, which provide them access to organic P. is can be a major
component of total soil P in old soils (Turner et al., 2013). Indeed, in their global comparison, Houlton
et al. (2008) found that soil phosphatase activities under plants known to be capable of symbiotic N
2
xation are three times higher than those in soil sampled beneath non-xing species. is claim could
be broadened in that some N
2
-xing species, including kwongan species, also invest N in Rubisco to
assimilate carbon, of which a large fraction is released as carboxylates from cluster roots, e.g., in Viminaria
juncea (Lamont, 1972) and Casuarina species (Reddell et al., 1997), or from non-cluster roots, e.g., in
Cullen, Glycine, Lotus and Kennedia species (Denton et al., 2006; Pang et al., 2010; Ryan et al., 2012).
Symbiotic N
2
xation may be an important trait to enhance release of phosphatases and carboxylates in

P-limited ecosystems (Houlton et al., 2008), but this remains to be evaluated in the kwongan.
In addition to N
2
xation occurring in clearly dened symbiotic structures involving higher plants
(Fig. 8) and in soil crusts (Pate, 1998), there is increasing evidence that this process also occurs in the
absence of such structures by endophytic bacteria. is can be a signicant source of N for sugarcane in
Brazil (Boddey et al., 2003), and likely also plays a role in trees (Bal et al., 2012) and other plants growing
on N-poor substrates (Reinhold-Hurek & Hurek, 2011). We envisage that non-symbiotic N
2
xation may
also play a role in kwongan, especially on very young dunes where the soil N levels are very low, without
a prominent presence of the symbiotic systems, discussed above, contributing to the system when soil N
accumulates (Laliberté et al., 2012; Hayes et al., 2013).
ACQUISITION OF MICRONUTRIENTS
Soils on south-western Australia’s sandplains are notoriously low in micronutrients, especially Cu and Zn
(Yeates, 1993). With the exception of Mn and Ni, micronutrient levels in Banksia leaves are less than what
is generally considered ‘sucient’ for crop growth (Denton et al., 2007). High levels of Ni are remarkable,
since this is a micronutrient for legumes and a few other species that metabolise urea (Broadley et al.,
2012), and we are unaware of any function of Ni in Proteaceae. Leaf Mn concentrations are most likely
high because the activity of cluster roots that mobilises P through release of carboxylates and protons
will also enhance the mobility of Mn (Godo & Reisenauer, 1980; Jauregui & Reisenauer, 1982). Perhaps
the same mechanism accounts for high Ni concentrations (Lee et al., 1978). Release of citrate can also
mobilise Zn, but its eect depends on soil type (Duner et al., 2012) (Fig. 4). Exudates released from
tomato and spinach roots mobilise both Zn and Cu (Degryse et al., 2008). It is therefore highly likely that
the exudates released by cluster roots of Proteaceae grown under low-P conditions will not only mobilise
P, but also micronutrients. Since P is the major limiting macronutrient in kwongan soil (Laliberté et al.,
2012), it is unlikely that specic adaptations evolved in Proteaceae to acquire micronutrients.
Despite a likely capacity to mobilise Zn in the rhizosphere, Zn concentrations in leaves of a range
of Banksia and other species (Denton et al., 2007; Hayes et al., 2014) are lower than what is considered
sucient. e same is true for co-occurring Calothamnus quadridus, Allocasuarina humilis, Banksia sessilis
and Xanthorrhoea preissii, but not for Eucalyptus todtiana (Myrtaceae) and Jacksonia furcella (Fabaceae)
(Pate & Dell, 1984). We have to bear in mind that low nutrient concentrations partly result from a
‘dilution eect’ by large amounts of sclerenchymatic tissue in kwongan plants. ere is no information
in the literature to indicate how these plants can function at such remarkably low Zn levels. Zinc plays a
role in a very wide range of enzymes in all organisms; in humans, 10% of all proteins require Zn (Broadley
et al., 2012). Zinc can play both a catalytic and a structural role in proteins. Zinc deciency reduces the
activity of a Zn-dependent superoxide dismutase, which play a role in scavenging toxic reactive oxygen
species (Cakmak, 2000).
Since species without specialised carboxylate-releasing roots coexist with those that produce cluster
roots or dauciform roots in kwongan, can the latter enhance nutrient acquisition by plants that lack
specialised roots? Muler et al. (2014), indeed, obtained evidence for a positive eect of Banksia attenuata
(Proteaceae) on the growth of co-occurring Scholtzia involucrata (Myrtaceae). is positive eect of
KWONGAN PLANT LIFE
11 4

Banksia attenuata cannot be explained by mobilisation of P, since addition of P did not enhance the
growth of Scholzia involucrata. e Mn uptake and leaf Mn concentration, and possibly those of other
micronutrients, are enhanced in S. involucrata when grown together with the cluster-rooted B. attenuata.
It is likely that facilitation is the result of the nutrient-mobilising strategy of B. attenuata, based on release
of carboxylates, as discussed above. It has yet to be explored how common facilitation by carboxylate-
releasing species on severely P-impoverished soils is.
CARNIVOROUS PLANTS
Carnivorous and protocarnivorous plants are relatively common on the south-western Australian
sandplains (Fig. 7). In Western Australia there are 5.5 times more carnivorous species than expected
based on the total number of species (Brundrett, 2009). Carnivorous plants tend to be non-mycorrhizal
and use their carnivorous habit as an alternative nutrient-acquisition strategy (Brundrett, 2009). In
kwongan, carnivorous species belong to the genera Byblis, Cephalotus, Drosera and Utricularia (Table 1).
e only known protocarnivorous genus is Stylidium (Darnowski et al., 2006); protocarnivorous species
lack the easily recognisable insect-trapping structures of true carnivorous species, but they do obtain
nutrients from captured prey.
Table 1. Genera of the different groups of parasitic species of the south-western Australian sandplains and the families they belong to. For references, see text.
GENUS FAMILY COMMON NAME PARASITIC HABIT
Cassytha Lauraceae Dodder laurel Holoparasitic stem parasite
Cuscuta Convolvulaceae Dodder Holoparasitic stem parasite
Pilostyles Apodanthaceae – Holoparasitic stem parasite
Orobanche Orobanchaceae Broomrape Holoparasitic root parasite
Amyema Loranthaceae Mistletoe Hemiparasitic stem parasite
Euphrasia Orobanchaceae Eye–bright Hemiparasitic root parasite
Exocarpus Santalaceae Ballart Hemiparasitic root parasite
Leptomeria Santalaceae Currant bush Hemiparasitic root parasite
Nuytsia Loranthaceae Christmas tree Hemiparasitic root parasite
Olax Olacaceae – Hemiparasitic root parasite
Santalum Santalaceae Quandong, sandalwood Hemiparasitic root parasite
CHAPTER 4: PLANT MINERAL NUTRITION
115

Figure 9. Carnivorous plants in the kwongan, and their flypaper, pitcher or suction traps. (a)
Drosera erythrorhiza
; (b)
Drosera pallida
; (c)
Drosera heterophylla
; (d)
Cephalotus follicularis
(Albany pitcher plant); (e)
Byblis gigantea
; (f):
Utricularia
menziesii
and (g) its belowground suction traps (utricles); photos: b, c, Graham
Zemunik; a and d–g, Hans Lambers.
a b c
d
f
e
g
KWONGAN PLANT LIFE
11 6

Byblis and Drosera species produce ypaper traps, i.e. leaves with glandular emergences (tentacles) that
secrete glistening, adhesive glue drops for attracting and capturing prey (Fig. 9). Watson et al. (1982)
concluded that captured arthropods could provide all the N and P that was required for growth of Drosera
erythrorhiza, but only a negligible proportion of K. Feeding
15
N-labelled Drosophila ies to leaf rosettes
of the tuberous Drosera erythrorhiza leads to 76% transfer of the
15
N in the prey to the plants. Most of
the acquired N is transferred to the tubers, and then to the new rosette during the next season (Dixon
et al., 1980). Drosera closterostigma and D. glanduIigera show an increase in growth, N and P content, and
reproductive performance from articial feeding of arthropods, but no apparent benets from minerals
alone or additive eects of minerals above that due to prey (Karlsson & Pate, 1992). Using natural
15
N
abundance of a range of Drosera species in their natural habitats, neighbouring non-carnivorous plants
and arthropods near or on each Drosera species, Schulze et al. (1991) estimated that for self-supporting
erect and climbing species 50% of their N was derived from their prey. Lower values were found for
rosette species.
Cephalotus follicularis, the Albany pitcher plant, is the only species in the family of Cephalotaceae and
not related to other pitcher plants (Chase et al., 2009). Using a similar
15
N natural abundance method as
discussed above for Drosera, Schulze et al. (1997) showed a dependence on soil N until four pitchers had
opened. Beyond that stage, plant size increased with the number of catching pitchers, but the fraction of
soil N remained high. Large pitcher plants derive a quarter of their N from insects.
Utricularia is a genus of carnivorous plants from wet habitats, producing suction traps under water or
in very wet soil (Chase et al., 2009). e bladders have a lower hydrostatic pressure than the surrounding
water, so when the trap door opens, upon touching a sensitive hair near the entrance, the prey is sucked
in (Sydenham & Findlay 1975). Using labelled N and P, it has been shown that the traps export 30% of
the N from captured prey to growing leaves within two days (Friday & Quarmby, 1994). e plants also
heavily depend on prey as a source of P (Adamec, 2013).
Stylidium is considered a protocarnivorous genus, because some species in this genus trap small insects
such as gnats and midges, using mucilage-secreting glandular hairs on their inorescences and stems, very
similar to the ypaper traps referred to above (Darnowski et al., 2006; Chase et al., 2009). Many species of
the genus form ectomycorrhiza-like structures (Warcup, 1980) as well as forming arbuscular mycorrhizas
(Brundrett & Abbott, 1991).
Given that P, rather than N, is the major limiting nutrient in the kwongan, it would be interesting
to know what fraction of their total P is derived from the prey they caught and digested. To assess this,
we need to know the N:P ratio of plant and insect material. For tubers of Drosera erythrorhyza, the N:P
is 3.8–10 (Pate & Dixon, 1978). For the insects that were captured, this ratio is about 8 (Pate & Dixon,
1978). If we use these gures to get a rough idea about the fraction of plant P that is derived from prey,
then we would conclude that it is perhaps similar to the fraction of N derived from prey. However, it is
also likely that the N locked up in the prey’s chitin is not available for the plant, so perhaps the fraction is
even greater.
CHAPTER 4: PLANT MINERAL NUTRITION
117

PARASITIC PLANTS
Although there are many non-mycorrhizal parasitic plants on the south-western Australian sandplains,
as a fraction of the total ora there are actually only about half as many species when compared with
global gures (Fig. 7). is is in stark contrast with other non-mycorrhizal plants with cluster roots, of
which there are 8.5 times more than expected based on global data (Brundrett, 2009). As discussed above,
the non-mycorrhizal species in kwongan tend to be the ones on the most P-impoverished soils, and this
also pertains to parasites (Fig. 10). Although parasitism is generally considered an alternative nutrient-
acquisition strategy, the under-representation of parasites in terms of number of species in the kwongan
ora suggests that it is not a very successful one, possibly because of its inherent risks, when compared
with other strategies. After discussing the mechanisms that parasites use to acquire nutrients from their
host, we will explore what those risks might be.
Figure 10. Parasitic plant species richness
as dependent on total soil phosphorus (P)
concentration. Plant diversity and soil data
are from a comprehensive floristic survey
of over 1000 quadrats in the wheatbelt of
Western Australia by Gibson
et al.
(2004).
Parasitic plants in the kwongan belong to holoparasitic stem parasites (Cassytha, Cuscuta, Pilostyles),
holoparasitic root parasites (Orobanche, athough it is not quite clear if it is native or alien), hemiparasitic stem
parasites (Amyema) or hemiparasitic root parasites (Euphrasia, Exocarpus, Leptomeria, Nuytsia, Olax, Santalum)
(http://orabase.dpaw.wa.gov.au/) (Table 1; Fig. 11). Pilostyles species in kwongan are unusual in that they live
as endophytes, embedded in the stems of Daviesia, Gastrolobium or Jacksonia species, except for their owers
and fruits (Dell et al., 1982; iele et al., 2008) (Fig. 12). All other parasitic plants on the sandplains form
a haustorium, which connects to the phloem (in holoparasites) or the xylem (in hemiparasites) (Fig. 13)
(Lambers et al., 2008a). ere are no studies on the functioning of kwongan holoparasites, which are not as
common as hemiparasites on the sandplains, so what follows is based on information on other holoparasitic
species. Holoparasites do not contain chlorophyll and thus depend on their host for a supply of both carbon and
nutrients. In their haustoria, they increase leakage of sugars and nutrients from the phloem, and rapidly take up
what is released. In contrast, hemiparasites do contain chlorophyll and connect via their haustoria to the xylem.
KWONGAN PLANT LIFE
11 8

Figure 11. Hemiparasitic and holoparasitic species in the kwongan. (a) The root hemiparasite
Nuytsia floribunda
(the Western Australian Christmas tree) in Lesueur
National Park (photo: Marion L. Cambridge). (b)
Nuytsia floribunda
, covered by the stem holoparasite
Cassytha
(dodder laurel) (photo: Graham Zemunik). (c)
Cassytha
attached to a twig of
Melaleuca
(photo: H. Lambers). (d) The stem hemiparasite
Amyema miquelii
(mistletoe) on
Corymbia calophylla
(marri) (photo: H. Lambers). (e)
The root hemiparasite
Santalum acuminatum
(quandong). (f) Two individuals of the hyperparasitic stem hemiparasite
Amyema miraculosa
on the root hemiparasite
Santalum acuminatum
. (g) Young individual of
Amyema miraculosa
on
Santalum acuminatum
(photos: Hans Lambers); (h) flowering
Amyema miraculosa
(photo: G.
Zemunik).
ey require a more negative water potential (greater suction tension) in their xylem than that of their host
in order to provide a gradient for water to move in the xylem towards the parasite (chapter 5). e parasite
thus imports the nutrients dissolved in the xylem sap. is may include some carbon, in the form of amino
acids and organic acids, but no sugars (Tennakoon et al., 1997b). Unlike holoparasites, hemiparasites can
photosynthesise, though rates may be low (Lambers et al., 2008).
b dc
e f hg
a
CHAPTER 4: PLANT MINERAL NUTRITION
119

Figure 12. Flowers (A) and fruits (B) of
Pilostyles hamiltonii
growing on stems of
Daviesia angulata in situ
(Thiele
et al.
, 2008)
(photos: Kevin R. Thiele).
Haustoria allow holoparasites to tap into their host’s phloem (Fig. 13). e haustoria of most root
hemiparasites look like suction cups (Fig. 13), but those of Nuytsia oribunda (Western Australian
Christmas tree) have a remarkably dierent appearance (Herbert, 1919; Fineran, 1985). A
sclerenchymatous ‘horn’ or ‘prong’ formed within the haustorium acts as a sickle-like cutting device,
which transversely severs the host root and then becomes lodged in haustorial collar tissue directly
opposite to that where it originated (Calladine & Pate, 2000).
Both stem and root hemiparasites that are common on the south-western Australian sandplains
typically have a more negative water potential (greater suction tension) than their hosts: Amyema
tzgeraldii (Davidson & Pate, 1992), A. linophyllum (Davidson et al., 1989), A. miquelii (Whittington &
Sinclair, 1988; Miller et al., 2003), Olax phyllanthi (Pate et al., 1990), Nuytsia oribunda (Calladine &
Pate, 2000) and Santalum acuminatum (Loveys et al., 2001). e greater suction tension is generally due to
high transpiration rates of the hemiparasite, a signicant resistance to the water ow in the haustoria, or a
combination of both (Hellmuth, 1971; Whittington & Sinclair, 1988; Davidson & Pate, 1992; Cernusak
et al., 2004). Rapid transpiration rates without similarly rapid rates of photosynthesis accounts for the low
water-use eciency of hemiparasites (Davidson et al., 1989; Davidson & Pate, 1992).
e host range of stem hemiparasites (mistletoes) tends to be narrow (Davidson et al., 1989; Davidson
& Pate, 1992), but that of root hemiparasites is generally very wide (Pate et al., 1990; Tennakoon et al.,
1997a; Calladine et al., 2000). Santalum acuminatum (quandong) has a wide host range, but, based on
the similarity in natural
15
N abundance, it appears to predominantly parasitise N
2
-xing hosts (legumes
and Allocasuarina) (Tennakoon et al., 1997a). Haustoria are not simply the organ that allows access to
the host, but may also allow selectivity of what is derived from the host and even convert some of the
compounds that arrive in the xylem (Lamont & Southall, 1982; Pate, 2001).
e strategy deployed by the many parasitic species in the kwongan appears to be a highly specialised
way to obtain nutrients; yet parasites are under-represented in the kwongan ora, whereas other nutrient-
acquisition strategies are abundant (Fig. 7). Why is that so? We surmise that there are major costs
associated with the parasitic lifestyle. For hemiparasites to maintain a high suction tension requires either
a b
KWONGAN PLANT LIFE
1 2 0

rapid transpiration rates or a low haustorial or stem conductance as well as accumulation of large amounts
of osmotic solutes, e.g., mannitol in Santalum acuminatum (quandongs) (Loveys et al., 2001). ere are also
risks. Stomatal control to allow transpiration to continue at much more negative water potentials than
occur in their hosts may cause dehydration, xylem cavitation and possibly death when the hosts can no
longer provide sucient water. For mistletoes, there is the additional risk due to re, which may require
re-establishment following re-introduction of seed from populations that were not aected by re. To
some extent, this may also be true for dodder laurels (Cassytha), but these can also germinate in soil, and
do not require a host for germination.
Figure 13. Root haustoria of hemiparasitic species. (a) Collar-like morphology of haustorium (white) of the hemiparasitic tree,
Nuytsia floribunda
(Western Australian
Christmas tree), encircling a host root. (b–d) Root haustoria of hemiparasitic
Santalum acuminatum
(quandong, Santalaceae). (b) Cap-like morphology of haustorium
(orange) latched onto host root of a
Melaleuca
sp. A single fine root (arrow) connects the haustorium to the parasitic plant (arrow). (c and d) Hand-cut sections of
fresh tissue stained with phloroglucinol/HCl. Xylem vessel elements stained red. (c) Longitudinal section of haustorium in (b) with attached host-root (hr) in cross-
section. A pair of overarching bundles, each composed of numerous strands of xylem (red), originate close to the point of fine root attachment at the dorsal surface of
the haustorium (arrow in (b)). Bundles fan out over outermost layers of the host root (hr) xylem vessels. (d) Higher magnification of (c) show xylem strands made up
of short vessel elements joined in series up to the interface where xylem elements of the haustorium join with the host root xylem vessels (photos: Michael W. Shane).
Scale bars in mm (a) 4; (b) 2; (c) 1; (d) 0.3.
b
d
a
c
CHAPTER 4: PLANT MINERAL NUTRITION
121

CONCLUDING REMARKS
e ora on the sandplains exhibits an astounding number of specialised nutrient-acquisition and
nutrient-use strategies on some of the world’s most nutrient-impoverished soils. While mycorrhizal
associations are common, non-mycorrhizal species are prominently present on the most infertile sites,
because of their strategy to ‘mine’ P and micronutrients, rather than ‘scavenge’ for it, as mycorrhizas do.
Fascinating discoveries have been made since the original book covered plant life on the sandplain (Pate
& Beard, 1984). Much is still to be learned, especially if we aim to apply some of the knowledge gained
for agriculture in a world with a growing population and a diminishing availability of rock phosphate
(Cordell et al., 2009; Lambers et al., 2011).
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