chapter 4: plant mineral nutrition

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. 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 (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 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).

Given that extreme soil infertility imposes a severe constraint to plant growth, one might expect the

kwongan flora 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 floristic 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 different types of mycorrhizal strategies that are found in kwongan, focusing on possible relationships between soil fertility and mycorrhizal type. Third, we present several symbiotic

systems that contribute to N2 fixation, 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.

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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). That is where non-mycorrhizal species rule. The 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). This is in contrast with much younger landscapes, where nonmycorrhizal 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). These families that are typically associated with nutrient-rich soils are poorly represented or totally absent on the southwestern 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 nonmycorrhizal (Shane & Lambers, 2005a); an exception is the mycorrhizal species Hakea verrucosa, which grows on the ultramafic rocks of Bandalup Hill which are rich in nickel (Ni) (Boulet & Lambers, 2005).

The carboxylate-releasing strategy, which is typical for species with proteoid roots, would mobilise Ni on

ultramafic 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).

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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 fire; however, when organic matter is present at greater depth, cluster roots can also be found lower in the soil profile (Lamont, 1973). This 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). Therefore, cluster roots effectively ‘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 efficient 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 different 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).

Significant 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). These species differ 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). This suggests a trade-off in plant carbon allocation to either mycorrhizal fungi or carboxylate release for P acquisition.

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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.

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Figure 4. Effects of carboxylates (and other exudates) on inorganic (Pi) and organic P (Po) 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 P1 and Po, 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 Fe2+ 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).

The leaves of Proteaceae in general (Jaffré, 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. This has also been found for Fabaceae species with cluster roots, e.g., Lupinus albus (Gardner et al., 1982) and Aspalathus linearis (Morton, 1983). This 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 dauciformrooted Cyperaceae (Hayes et al., 2013). It is therefore likely that the significance 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 effect. This warrants further investigation.

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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 hydroponicallygrown 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.

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The high abundance of Proteaceae in severely P-impoverished landscapes is not exclusively accounted for

by their very efficient P-acquisition strategy. In addition, at least three other traits determine their high P

efficiency 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 efficient and proficient at remobilising P during leaf senescence (Denton et al., 2007,

Hayes, 2014). Third, their seeds, unlike their vegetative tissues, contain very high concentrations of P (Denton et al., 2007; Groom & Lamont, 2010). These 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 fire; commonly only a few per cent of all the flowers 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-efficiency 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 efficiently, 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). The 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). Their 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). The 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. The 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 107

KWONGAN PLANT LIFE

widespread on the south-western Australian sandplains, but not quite as common as in the rest of the

world (Fig. 7; Brundrett, 2009). This may reflect 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 effective in

enhancing plant P uptake (Parfitt, 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 fixed carbon to the fungal partner (Smith & Read, 2008; Kiers et al., 2011). a

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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.

Chapter 4: Plant mineral nutrition 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). There is evidence that ectomycorrhizas are more effective

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). The 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. They 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 effective 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 Thysanotus form mycorrhizas that have a unique morphology.

The ‘Thysanotus mycorrhizas’ are characterised by hyphae that penetrate between epidermal cells and

ramify between cortex and epidermis (McGee, 1988). Superficially, it appears like an altered morphology, or one that is neither arbuscular mycorrhizal nor ectomycorrhizal. Interestingly, some of the fungi responsible for Thysanotus 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 nutrientacquisition strategies in kwongan than previously thought.

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Finally, orchid mycorrhizas are confined 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 beneficial (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). This 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. The lack of epiphytes (both orchids and non-orchids) on the south-western Australian sandplains might reflect the absence of suitable climatic conditions for this life form. The 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 modification of floral signals (chapter 7B), particularly in the tropics where competition for pollinators is fiercest, have been integral to orchid diversification (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 specific aspects of their nutrient-acquisition strategy.

SYMBIOTIC NITROGEN FIXATION In any terrestrial ecosystem, N is continuously lost through leaching and denitrification. In kwongan, losses as a result of combustion of nitrogenous compounds during fires are also a major component of the N cycle at the ecosystem level. These 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 110


fixed by lightning are less than 10 Tg per year (Tg = 1012 g or 106 metric tons) (Galloway et al., 1995). Biological N2 fixation 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 N2 fixation. The first is qualitative; it is based

on the principle that the enzyme that reduces N2 to NH3 also reduces acetylene (C2H 2) to ethylene (C2H4), which is readily measured by gas chromatography (Dilworth, 1966). This technique demonstrates whether

certain structures are capable of fixing N2 or not, but it cannot reliably be used to assess how much they are fixing, because nodule activity rapidly declines in the presence of acetylene (Minchin et al., 1983). The second is more quantitative, provided basic assumptions are met; it uses the stable isotope 15N, which can be measured by mass spectrometry (Minchin et al., 1983; Hansen et al., 1987). Since the 15N abundance

of N2 in air and of soil N tend to differ, the natural 15N abundance is frequently used to estimate the

contribution of biological N2 fixation to the total amount of N acquired by a plant (Shearer & Kohl, 1986). A non-fixing reference plant is required to determine the 15N abundance in the absence of N2 fixation, 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 differ, i.e. one being arbuscular mycorrhizal and the other ectomycorrhizal, then the natural 15N abundance technique may give erroneous results (Högberg, 1990). If the plants that are compared access their N from different depth and the 15N abundance differs with depth, then the 15N abundance technique cannot be used either (Robinson, 2001). Despite these problems the natural 15N abundance technique is a valuable tool in ecological research (Handley & Scrimgeour, 1997).

Legumes in association with rhizobia play a prominent role in N2 fixation on the south-western

Australian sandplains (Fig. 8), especially during winter after a fire (Hingston et al., 1982; Hansen & Pate, 1987). Water stress is the main reason for a decrease in N2 fixation in summer (Hansen & Pate, 1987).

A decline in symbiotic N2 fixation with increase in time after a fire 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 fire, sharply declines to 30% of its original high density immediately after a fire by year four, and to less than 8% 13 years after a fire (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 fire-following legume acquires most N from soil immediately after a fire, about 70% is derived from symbiotic N2 fixation by year four after a fire (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 N2 into NH3. 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 oxygendamage-avoidance mechanism in N2-fixing 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

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(Brundrett & Abbott, 1991). a

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Figure 8. Structures involved in symbiotic N2 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.

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In addition to numerous legumes, sheoaks (Casuarina and Allocasuarina) also form a N2-fixing symbiosis, with Frankia (Actinomycota) as the microsymbiont (Fig. 8) (Bond, 1957; Becking, 1970). The symbiotic structures in actinorhizal plants are commonly referred to as rhizothamnia (Mowry, 1933) or nodules

(Torrey & Racette, 1989). Most studies on symbiotic N2 fixation in Casuarinaceae species focused on those that are not endemic in Western Australia, and these are the studies summarised here. There is

distinct host specificity 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

fixed N2, 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 N2 (Bond, 1957). Under field conditions, C. equisetifolia can obtain up to 67% of its N from symbiotic N2 fixation (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 significantly to biological N2 fixation 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). These 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 & Staff, 1975; Ahern & Staff, 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). The microsymbonts in coralloid roots may also

produce other toxins, including nodularin (Gehringer et al., 2012). The 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 fix N2 at physiologically significant 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 significantly higher in plants

growing on a recently burnt site. This suggests that rates of N2 fixation are driven by the demand of rapidly regrowing leaves after a fire.

By examining trade-offs inherent in plant carbon, N and P capture, Houlton et al. (2008) suggest

a clear advantage to symbiotic N2-fixing 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. This 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 N2

fixation are three times higher than those in soil sampled beneath non-fixing species. This claim could be broadened in that some N2-fixing 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 N2 fixation may be an important trait to enhance release of phosphatases and carboxylates in

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KWONGAN PLANT LIFE

P-limited ecosystems (Houlton et al., 2008), but this remains to be evaluated in the kwongan.

In addition to N2 fixation occurring in clearly defined 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. This can be a significant 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 N2 fixation 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 ‘sufficient’ 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 effect depends on soil type (Duffner 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 specific 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

sufficient. The same is true for co-occurring Calothamnus quadrifidus, 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 effect’ by large amounts of sclerenchymatic tissue in kwongan plants. There 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 deficiency 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 effect of Banksia attenuata

(Proteaceae) on the growth of co-occurring Scholtzia involucrata (Myrtaceae). This positive effect of 114


Banksia attenuata cannot be explained by mobilisation of P, since addition of P did not enhance the growth of Scholzia involucrata. The 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 carboxylatereleasing 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). The 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


Pilostyles

Apodanthaceae

–


Orobanche

Orobanchaceae

Broomrape

Holoparasitic root parasite

Amyema

Loranthaceae

Mistletoe

Hemiparasitic stem parasite

Euphrasia

Orobanchaceae

Eye–bright

Hemiparasitic root parasite

Exocarpus

Santalaceae

Ballart


Leptomeria

Santalaceae

Currant bush


Nuytsia

Loranthaceae

Christmas tree


Olax

Olacaceae

–


Santalum

Santalaceae

Quandong, sandalwood


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KWONGAN PLANT LIFE

a

d

f

b

c

e

g

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.

116


Byblis and Drosera species produce flypaper 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 15N-labelled Drosophila flies to leaf rosettes of the tuberous Drosera erythrorhiza leads to 76% transfer of the 15N 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 artificial feeding of arthropods, but no apparent benefits from minerals

alone or additive effects of minerals above that due to prey (Karlsson & Pate, 1992). Using natural 15N

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 15N 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). The 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). The 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 inflorescences and stems, very

similar to the flypaper 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 figures 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.

117

KWONGAN PLANT LIFE

PARASITIC PLANTS Although there are many non-mycorrhizal parasitic plants on the south-western Australian sandplains,

as a fraction of the total flora there are actually only about half as many species when compared with

global figures (Fig. 7). This 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 flora 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://florabase.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 flowers

and fruits (Dell et al., 1982; Thiele 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). There 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. 118


a

b

e

c

f

d

g

h

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).

They 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). The parasite

thus imports the nutrients dissolved in the xylem sap. This 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).

119

KWONGAN PLANT LIFE

a

b

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). The haustoria of most root

hemiparasites look like suction cups (Fig. 13), but those of Nuytsia floribunda (Western Australian

Christmas tree) have a remarkably different 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 fitzgeraldii (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 floribunda (Calladine &

Pate, 2000) and Santalum acuminatum (Loveys et al., 2001). The greater suction tension is generally due to

high transpiration rates of the hemiparasite, a significant resistance to the water flow 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 efficiency of hemiparasites (Davidson et al., 1989; Davidson & Pate, 1992).

The 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 15N abundance, it appears to predominantly parasitise N2-fixing 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).

The 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 flora, 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 120


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). There 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 sufficient water. For mistletoes, there is the additional risk due to fire, which may require

re-establishment following re-introduction of seed from populations that were not affected by fire. 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. a

b

c

d

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 crosssection. 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.

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KWONGAN PLANT LIFE

CONCLUDING REMARKS The flora 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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