Soil salinity: A neglected factor in plant ecology and biogeography

Journal of Arid Environments 92 (2013) 14e25

Contents lists available at SciVerse ScienceDirect

Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv

Review

Soil salinity: A neglected factor in plant ecology and biogeography E.N. Bui* CSIRO Land and Water, GPO Box 1666, Canberra, ACT 2601, Australia

a r t i c l e i n f o

a b s t r a c t

Article history: Received 11 June 2011 Received in revised form 13 August 2012 Accepted 31 December 2012 Available online 11 February 2013

This paper argues that soil salinity needs to be more broadly acknowledged as a driving factor in plant ecologydnot only in the ecology of halophytesdin order to understand and make more accurate predictions for the impact of environmental change on biodiversity and vegetation patterns throughout the semi-arid world. It summarizes recent research on soil salinity and plant distributions in semi-arid environments throughout the world: there is empirical as well as experimental evidence that soil salinity, even at low levels, is an abiotic stress factor that influences vegetation patterns and diversification. Lines of evidence demonstrating salinity’s potential influence as a selective agent in East Africa and North America are presented. The paper then synthesizes recent results from spatial ecology, plant and insect systematics and behavioral ecology, focusing on Australia, that support a role for salinity in evolutionary ecology of Acacia. On a shorter time scale, soil salinity may play a role in weed invasion and woody vegetation encroachment in Australia. Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved.

Keywords: Acacia Evolutionary ecology Halophytes Non-halophytes Speciation

1. Introduction Recently there has been much activity related to predicting the impact of climate change on biodiversity, nevertheless the question of what determines the distribution of species, one of the most basic in ecology, is still unanswered for most of Australia and much of the rest of the world (Austin and Van Niel, 2011; Hughes, 2003; Kier et al., 2005). Five categories of factors that determine distribution and abundance of plant species are recognized (MuellerDombois and Ellenberg, 1974): climatic; edaphic; geographichistoric factors; species interactions; and perturbations. These factors also govern the composition and structure of plant communities. They also act as evolutionary stress factors. That climatic and topographic data are not always sufficient to explain vegetation patterns is evident (e.g., Austin and Van Niel, 2011; Bertrand et al., 2012; Bui and Henderson, 2003; Dirnbock et al., 2002; Martin et al., 2006; Reed et al., 2009). Yet even when edaphic factors are taken into consideration by plant ecologists and biogeographic modelers, soil moisture/texture, pH, and nutrients are generally the only variables considered. Although soil salinity is recognized as a major limitation to cropping (e.g., Lauchli and Luttge, 2002; US Salinity Laboratory, 1969; Zhu, 2001) and the focus of many plant breeding efforts to produce salt-resistant crops (e.g., Flowers et al., 2010; Lauchli and Luttge, 2002; Parida and Das, 2005), generally, it is neglected as a factor in plant ecology, except

* Tel.: þ61 2 6246 5935. E-mail address: [email protected].

in the ecology of deserts (salt pans and playas) and wetlands (salt marshes, mangroves) where its importance is obvious given the prevalence of halophytes. This paper first considers definitions of saline soils and halophytes, and reviews the role of soil salinity in plant ecology and geography around the world but then focuses on Australia. It presents new evidence that salinity plays a role at the macro-level, in the diversification of the genus Acacia, with more than 900 native Australian species. Australia is one of the most biologically unique areas of the world, with one of the most extensive arid zones; natural salinity is widespread, with extensive playa lake systems and saline and sodic soils (Northcote and Skene, 1972; Rengasamy, 2006). 1.1. What is soil salinity? The definition of saline soil is confusing.1 Soils are considered saline if they contain salt in a concentration sufficient to interfere with the growth of most crop species. Saline soils have an electrical conductivity >4 dS m
1 (w36 mM NaCl) measured on a saturated soil paste extract at 25  C (US Salinity Laboratory, 1969). Electrical

1 Soil scientists distinguish saline soils with an electrical conductivity >4 dS m
1, pH < 8.5, and Na < 15% of total exchangeable cations from sodic soils with Na > 15%, and in older literature, alkali soils with pH > 8.5. Here I will be discussing broadly salt-affected soil: soil that has been adversely modified for the growth of most crop plants by the presence of soluble salts, with or without high amounts of exchangeable Na (SSSA glossary, https://www.soils.org/publications/soilsglossary#). Salt-affected soils can be saline and alkaline.

0140-1963/$ e see front matter Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jaridenv.2012.12.014

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25

conductivity is a measure of the ease with which electrical current will pass through water: the greater the salinity, the greater the conductivity; however, the relationship is a function of the specific ions present in the solution and their concentrations. Depending on the soil texture, the relative water and salt content, and osmotic pressure of the saturation extract can be very different (Fig. 7, US Salinity Laboratory, 1969). When soil water content less than saturation, plants will experience salt concentration higher than that measured in the test for soil salinity. Salinity level will change down a soil profile with seasonal moisture fluctuations and relative soil water content but salt is generally localized below the root zone. Expressing salinity as a soil profile-integrated value (e.g. Bui and Henderson, 2003) dilutes the presence of salt concentrated in a single horizon only. Salt accumulation is a phenomenon that is not unique to any particular soil type in many soil classifications but it is typically associated with “Soils influenced by water” especially Solonetz (alkaline) and Solonchak (salt enrichment upon evaporation) Soil Groups in the World Reference Base (IUSS, 2006). It occurs where evaporation is high relative to precipitation (there is a seasonal water deficit) and leaching is insufficient to move salts out of the soil profile (Duchaufour, 1982; Schofield and Kirkby, 2003). Secondary salinization can arise when salts accumulate near the soil surface as a result of rising water tables due to land management practices such as irrigation or tree clearing (Cisneros et al., 1999; Rengasamy, 2006; Runyon and D’Odorico, 2010; Silburn et al., 2009; Williamson, 1986). Thus a large fraction of natural and secondary salinity occurs in desert and grassland biomes, in savanna ecosystems, which are often used as rangelands, and are closely associated with semi-arid, seasonally contrasted climates in the tropics and sub-tropics. Nevertheless the occurrence of saltaffected soils is not a perfect match with climate, even when also taking lithology (a potential source of solutes released by weathering) into account (Schofield and Kirkby, 2003). Saline and sodic soils often occur in or near local topographic lows in the landscape where soluble salts accumulate under endorheic drainage conditions, thus they are often seasonally waterlogged and can be associated with wetlands. Approximately 10% of the Earth’s total land surface may be salt-affected (Schofield and Kirkby, 2003). Soil salinity can imply the presence of chlorides, sulfates, nitrates, (and bicarbonates) of sodium (Na), calcium (Ca), magnesium (Mg), and potassium (K). High levels of carbonates are reflected by soil pH >8.3. Saline soils often have a typical sequence of horizon chemistry that reflects the position and salt content and chemistry of the underlying water table, the dominant upward trend of water movement through the profile, and the solubility of salts (e.g., Fig. 1). Microbial activity can also influence saline soil chemistry and vice versa (Miletto et al., 2008; Whittig and Janitsky, 1963; Wolicka and Jarzynowska, 2012). Vegetation zonation is demarcated as a function of salts and their chemical composition (e.g., Cisneros et al., 1999; Richardson et al., 1994; Stewart and Kantrud, 1972) and changes in vegetation cover lead to changes in the soil hydrology and chemistry (e.g., Cisneros et al., 1999; Runyon and D’Odorico, 2010; Silburn et al., 2009). Global patterns of salinization have changed over geologic time with climate (Kershaw et al., 2003). Importantly, as Schofield and Kirkby (2003) have shown, climate change will impact on the spatial pattern of soil salinity by changing patterns of precipitation and evapotranspiration, and landscape hydrology. 1.2. Plant response to soil salinity Most plants are glycophytes that tolerate only low concentrations of salt before they are adversely affected as evidenced by decrease in productivity and/or death. The threshold salt

15

Fig. 1. Well developed Solonetz at Keyneton, South Australia with a typical horizon sequence: a brown or black surface horizon with organic matter dispersed by Na cations; pale (albic) eluviation horizon directly over a horizon with exchangeable Na >15% (natric), columnar structure, and pH of about 8.5 (indicative of the presence of free sodium carbonate); a horizon with Ca-carbonate (calcic) is present below the natric horizon. The sequence of mineral precipitates in the profile follows the Hardie and Eugster (1970) sequence for the evolution of closed basin brines thus indicating the presence of a shallow (w2 m) water table with Ca < CO3 during the soil’s formation. (Photo courtesy of Rob Fitzpatrick). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

concentration that separates halophytes from glycophytes has been set at different levels by different authors. Flowers et al. (2010) use a threshold of 200 mM NaCl which corresponds roughly to 20 dS m
1 but others have used 80 mM NaCl (w8 dS m
1) to distinguish between halophytes and non-halophytes. Obligate halophytes require saline conditions to grow whereas facultative halophytes are found in less saline habitats and are characterized by broader physiological diversity that enables them to cope with saline and non-saline conditions2 (Parida and Das, 2005). Salttolerant glycophytes exhibit some physiological mechanisms to reduce sodium toxicity although they are not halophytes (e.g. Flowers et al., 2010; Hamilton et al., 2001; Parida and Das, 2005). Even low soil salinity levels (<4 dS m
1) can exert physiological stress on plants by affecting osmotic potential, ion toxicity (Na, Cl, and other ions could be toxic), photosynthesis (reduction in

2 Thus they apparently show phenotypic plasticity (the ability of a single genotype to produce multiple phenotypes in response to variation in the environment) as defined by Pfennig et al. (2010). Phenotypic plasticity can promote diversification because the developmental pathways that underlie environmentally induced phenotypes consist of many genetic components that can potentially respond to selection.

16

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25

efficiency of photosynthesis is linked to reduction in stomatal conductance), nutrient absorption, and N-fixing symbioses (Lauchli and Luttge, 2002; Parida and Das, 2005; US Salinity Laboratory, 1969; Zhu, 2001). As a result, plants have developed a plethora of biochemical and molecular mechanisms to cope with salt stress including: (i) selective accumulation or exclusion of ions; (ii) control of ion uptake by roots and transport into leaves; (iii) compartmentalization of ions at the cellular and whole-plant levels; (iv) synthesis of compatible solutes, e.g., proline; (v) change in photosynthetic pathway, e.g., a shift from the C3 to the C4 pathway in response to salinity is observed in the halophyte Atriplex lentiformis; (vi) alteration in membrane structure; (vii) induction of antioxidative enzymes; and (viii) induction of plant hormones, e.g., abscissic acid (Flowers et al., 2010; Lauchli and Luttge, 2002; Parida and Das, 2005; Zhu, 2001). Response starts at low levels of salt and the mechanisms involved are based on regulatory processes for ions, water, and CO2 common to all plants that also may control responses to other environmental stress such as drought (Flowers et al., 2010; Hamilton et al., 2001; Parida and Das, 2005; Zhu, 2001). Plant responses to salinity vary with the degree and duration of stress and the developmental stage at time of exposure. Biochemical pathways leading to products and processes that improve salt tolerance are likely to act additively and probably synergistically, controlled by multiple genes (Flowers et al., 2010; Javid et al., 2011; Parida and Das, 2005; Zhu, 2001). For example, adaptive differentiation of the halophyte Helianthus paradoxus from its glycophyte parental species has been related to transgressive trait expression, in which trait values in hybrids are higher or lower than those of both parents (Edelist et al., 2009).3 Transgressive traits in H. paradoxus include more succulent leaves and higher leaf contents of Na and sulfur than both parental species (Karrenberg et al., 2006; Rieseberg et al., 2003). Previous genetic studies imply that such transgressive traits result from complementary gene action where alleles with opposing effects are recombined in hybrids (Rieseberg et al., 2003). Although the mechanisms for coping with alkalinity stress are similar to those for salt stress, different genes may be involved (Javid et al., 2011; Yang et al., 2012) and neither the mechanisms nor the genes have been studied as much as those for salt stress which have been investigated intensively for three decades at least (Flowers et al., 2010; Parida and Das, 2005). Given the frequent coincidence of alkalinity and sodicity in salt-affected soils, genes that confer tolerance to alkalinity may play a role in salt tolerance too. Salt tolerance is widely distributed across the plant kingdom and is thought to have evolved polyphyletically but exactly how and how many times salt tolerance has evolved since the emergence of land plants 450e470 Mya is unresolved (Flowers et al., 2010). Given that Na is an essential element for many plants that use the C4 photosynthetic pathway (Subbarao et al., 2003), is there any relationship between salt-tolerance and the evolution of a photosynthetic pathway adapted to low CO2, high irradiance, and dry conditions? Is it only coincidental that of the order Caryophyllales, the Chenopodiaceae use C4 carbon fixation the most, with 550 or 39% of species in this family using this pathway or was salt-tolerance a pre-condition (Sage, 2001)? New phylogenetic analyses suggest that salt-tolerance pre-dates evolution of the C4 pathway in Chenopodiaceae, in contrast to Poaceae where the reverse appears true (Kadereit et al., 2012).

3 Under- or over-expressed genes related to potassium and calcium transport were homologs of KT1, KT2, ECA1; homologs of the potassium transporter HAK8 and of a transcriptional regulator were generally over-expressed in saline treatments.

2. A role for soil salinity in ecology over geologic time Biogeographic patterns emerge over time scales of hundreds to tens of thousands of years as organisms adjust to prevailing environmental conditions. Evolutionary processes, such as selection, adaptation, speciation, and extinction act over longer geologic time scales (to 106 years). There is some evidence that salinity plays a part in both and thus may be an agent an evolutionary ecology (evolution of biodiversity and plant communities). 2.1. Phytogeography Because grasslands and seasonally flooded savannas are some of the most poorly studied biomes in the world (Kier et al., 2005) and salinity is associated with them, there has been comparatively little work to draw on to review the influence of soil salinity as a driver in plant ecology and phytogeography. Most studies on factors explaining vegetation distribution focus on the role of climate and soil moisture or fire but there is evidence that salinity plays a role in current patterns of plant distribution at a regional scale in Central Europe, the Middle East, Africa, the Americas, and Australia. Except for the Prairie Pothole Region in North America, there is little detail on the chemistry of salts present. 2.1.1. Europe, the Mediterranean basin and Middle East In seminal work published in the 1970s, Heinz Ellenberg assigned ‘indicator values’ to vascular plants in Central Europe with respect to climatic factors (light, temperature, continentality), soil moisture, acidity, available nitrogen, salt, and to a lesser degree of success, heavy metal content of soil (Ellenberg et al., 1991). The occurrence of salinity and sodicity in the Danube-Tisza floodplain is well documented (Toth and Rajkai, 1994) and Ellenberg’s proximity to this region may have influenced his consideration of salinity as a factor in plant distribution. In coastal ecosystems in southern Europe (Molina et al., 2003; Rogel et al., 2001), and around the Mediterranean, in north Africa and the Middle East (El-Bana et al., 2002; Le Houerou, 2003; Shaltout et al., 1997), plant distribution in dune, marshland, and aquatic habitats can be related to soil electrical conductivity and chemistry. Focusing principally on identifying floristic domains and salt-tolerant fodder and timber species, a comprehensive review of vegetation patterns in the Red Sea basin (810,000 km2) describes vegetation zonation that reflects climate, topography, and soil salinity and gives a useful classification of halophytes and salt-tolerant glycophytes in terms of their ecology (Le Houerou, 2003). In the Red Sea lowlands (210,000 km2), vegetation is characterized by desert contracted vegetation with many halophyte communities to the north, and tropical Acacia-Commiphora savanna and halophytic communities to the south (Le Houerou, 2003). Many halophyte and salt-tolerant glycophyte species (100 with 20 endemics) are present in the coastal plains of Egypt, the Sudan, Eritrea, Djibouti, the Gulf of Aden, and northern Somalia and their habitat varies in its level of salinity. Because this review is trying to demonstrate the role of soil salinity in ecology beyond that of halophytes, some of the salt-tolerant glycophyte communities identified by Le Houerou (2003) are worth noting: Sporobolus spicatus community, Acacia tortilis s.l., Acacia ehrenbergiana, and Acacia oerfota. These occur on soil where only the subsoil is saline. 2.1.2. Africa In the savannas of east Africa, grasses respond to a climate, topography, and soil chemistry gradient (Banyikwa, 1976, cited by Belsky, 1986; Hamilton et al., 2001). Whereas Andropogon greenwayi occurs on soils with low Na concentrations, Sporobolus ioclados, Sporobolus kentrophyllus and S. spicatus reflect an increasing

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25

level of Na in the Serengeti plains (w30,000 km2). These individual Sporobolus species have been shown to respond differently to increasing Na concentrations in laboratory experiments, in a manner that reflects their distribution in East Africa (Hamilton et al., 2001). S. spicatus tolerates the highest levels of Na in the field and experimentally (Fig. 2) and qualifies as a halophyte under the Flowers et al. (2010) threshold. Sub-surface concentrations of Na and presenceeabsence of mound-building termites accounted for 55% of the variability in vegetational heterogeneity in the Serengeti (Belsky, 1988). In her review of East African savanna ecology models, Belsky (1990) explains that the vegetation pattern of the Serengeti is complex, reflecting rainfall, grazing, and soil salinity and pH. She continues to explain that these factors are not independent since salts are leached out by the higher rainfall in the north, and that grazing patterns reflect grass productivity that increases with rainfall northward. She concludes “in the Serengeti Plains it is the high salinity and shallow soils that exclude trees, not herbivores or rainfall.” Recent modeling work by Reed et al. (2009) concludes that both rainfall and topography are important contributors to the distribution of woodlands and grasslands in the Serengeti but unfortunately does not consider soil chemistry. Electrical conductivity and carbonate content are the main soil attributes that account for the vegetation groups along the Turkwel River floodplain in Kenya (Stave et al., 2003). The effect of electrical conductivity is reflected at levels below those that would characterize a saline soil. The A. tortilis/Cadaba rotundifolia and Hyphaene compress/C. rotundifolia wooded shrubland communities reflect the highest salt and carbonate levels. In southern Africa, Ellery et al. (1997) concluded that groundwater salinity and chemistry were one of the major determinants of vegetation species distribution in the Okavango delta, where again S. spicatus was associated with high Na and soil electrical conductivity levels. Ellery et al. (1997) explained the dynamic fluctuations in plant zonation patterns in the Okavango as a feedback effect between groundwater depth and chemistry, and evapotranspiration. Similar observations were made on endorheic pans in South Africa by Cilliers and Bredenkamp (2003). In quartz fields of southern Africa, where 70% of the plant species are endemic,

Fig. 2. Mean  1 SE field leaf blade Na concentrations and mean  1 SE field soil Na concentrations (mg/kg dry mass) for Andropogon greenwayi, Sporobolus ioclados, S. kentrophyllus, and S. spicatus paired leaf and soil samples collected in the Serengeti short-grass plains. Diamonds (A) represent experimental Na treatment concentrations (from Hamilton et al., 2001, with permission). Except for S. spicatus, photosynthetic activity and biomass production of all species were significantly reduced by the addition of Na.

17

Schmiedel and Jurgens (1999) found two dominant patterns of growth forms, one associated with high salt content, neutral to slightly acid soil pH, and low stoniness, the other characterized by low soil salinity, acid soil pH, and high stoniness. Further, Schmiedel and Jurgens (1999) observed that diversification of Mesembryanthemaceae reflects subtle edaphic gradients in the saline quartz fields. 2.1.3. Americas In North America, the Prairie Pothole Region, which occupies 900,000 km2 across north central USA and south central Canada, is characterized by thousands of small wetlands whose chemistry and vegetation patterns are highly variable over short distances. For example, in surface water of wetlands, total soluble salts, dominantly sulfates and carbonates, can vary from 150 mg kg
1 to 3000 mg kg
1 over a distance of 300 m (Goldhaber et al., 2011; Heagle et al., 2013) and salinity level is associated with concentric zonation of herbaceous plant communities (Richardson et al., 1994; Stewart and Kantrud, 1972). In the Prairie Pothole wetlands, the occurrence of different species of Typha and Scirpus across the salinity gradient (Fig. 3) suggests that speciation may be associated with salinity. Salinity is one of the drivers for the distribution of Helianthus (sunflower) species in North America, H. paradoxus having adapted to saline soil (Bush and Van Auken, 2004; Rieseberg et al., 2003). In South America, in the Chaco of Argentina, plant communities are distributed along a soil moisture and salinity gradient (Hilgert et al., 2003). In the flooding pampas of Argentina, where more than 60% of the soils over the 90,000 km2 area are saline or sodic, edaphic factors associated with subtle topographic features are the principal environmental factors explaining vegetation structure (Perelman et al., 2001). C4 grasses are more common than C3 in more saline environments (Perelman et al., 2001); this is not surprising given Na is an essential element for many C4 plants (Subbarao et al., 2003). 2.1.4. Australia In Australia, the local role of soil salinity (and alkalinity) in structuring plant communities is recognized widely (Bell and Williams, 1997; Fensham et al., 2007; Froend et al., 1987; Keighery et al., 2004; Kreeb et al., 1995; Wardell-Johnson et al., 1997). The potential regional role of environmental factors including salinity in plant ecology was investigated in the Murray basin of Australia by Noy Meir (1974) who found it significant but concluded that the role of salinity reinforced that of soil texture and moisture. Crowley (1994) suggested that salinity played a role in determining vegetation patterns in the southeast over the Quaternary. The low relief landscapes of southwest Australia where saline ground- and surface water systems have persisted for millennia have promoted the evolution of halophyte diversity in many phylogenetically independent lineages including Chenopodiaceae and Eucalyptus (Hopper, 2009). Other evidence that salinity has been a major driver in plant ecology in Australia over geological time is from Queensland in northern Australia. There, Bui and Henderson (2003) analyzed modern geo-referenced vegetation data that cover three of Australia’s biodiversity ‘hotspots’, the Einasleigh Uplands, Desert Uplands, and northern Brigalow Belt.4 Their results also extend over the southern Brigalow Belt. Their work shows that profileintegrated soil salinity and topsoil pH, respectively, are strongly associated with the first two score axes after correspondence

4 The map of Australia’s bioregions is at http://www.environment.gov.au/parks/ nrs/science/bioregion-framework/ibra/index.html.

18

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25

PLANT COMMUNITY In order of increasing electrical conductivity Scirpus heterochaetus (8)

EXPLANATION Geometric mean

Scirpus fluviatilis (13) Range Standard deviation Standard error of the mean

Typha spp. (32) Typha spp.-Scirpus acutus (33)

Scirpus acutus (42) Scirpus acutus-Scirpus paludosus (22) Scirpus paludosus-Scirpus acutus (16)

Scirpus paludosus (13) 0.1

0.316

1

3.16

10

31.6

100

Electrical conductivity at 25°C, dS m-1 Fig. 3. Relationship of dominant deep-marsh emergent communities to electrical conductivity of pond water (from Stewart and Kantrud (1972)). Number of ponds sampled for each community is shown in parentheses. For details, see page D11 in Stewart and Kantrud (1972).

analysis of site by species data, an indirect environmental gradient method (Fig. 4A). While three Acacia species (Acacia argyrodendron Domin., Acacia harpophylla F. Muell., and Acacia cambagei R. T. Bak.) are indicative of saline soil, the distribution of 20 other individual species across many genera responds strongly to a salinity gradient, starting at very low levels of salinitydbelow those that would typify a saline soil (Fig. 4B). Until this work, climate, soil texture, and soil moisture were believed to be the most important variables in the ecology of A. harpophylla (brigalow) communities but adding soil salinity to these other environmental variables in a Generalized Additive Model to account for site scores improved the results dramatically (Mean Squared Error decreased from 0.89 to 0.65 and R2 improved from 0.41 to 0.57). 2.2. A role for soil salinity in evolutionary biology Environment-dependent selection may be important in speciation but the conceptual frameworks of speciation genetics and environmental stress physiology have not been fully integrated (Lexer and Fay, 2005). Perhaps the best illustration of soil salinity’s role in evolutionary biology comes from Rieseberg and colleagues (e.g. Edelist et al., 2006, 2009; Rieseberg et al., 2003) who demonstrated experimentally how speciation in sunflowers (Helianthus spp.) in North America has been a response to environmental stress, including soil salinity, over the Quaternary. The role of abiotic environmental stress factors on plant evolution is difficult to study and Helianthus, because of its relatively recent (60,000e 200,000 years ago) speciation and niche adaptation, is one of only a few genera that have been studied from the molecular, physiological, and evolutionary angles. Unlike its progenitors, Helianthus annuus and Helianthus petiolaris, the homoploid hybrid H. paradoxus grew better and had strongly reduced leaf potassium, Ca, and Mg contents upon saline treatment while supporting more than nine times higher leaf Na loads than its parental species, suggesting that Na may replace other cations as vacuolar osmotica (Karrenberg et al., 2006). Under- or over-expressed genes related to

K and Ca transport; thus, alterations in the expression or activity of ion transport genes may have been important in the evolution of salt tolerance in H. paradoxus (Edelist et al., 2009). Also experimentally, Hamilton et al. (2001) showed that Natolerance in C4 grasses (including three Sporobolus species) was associated with heat-shock protein (Hsp) production and proline accumulationdboth provide protection against salt stress by regulating osmotic potential. They demonstrated induction of Hsps in response to Na levels similar to those in which each species grows in the field. Photosynthetic tolerance correlated with the observed levels of Na in field tissues, and with the molecular adaptation of Na-induced Hsp production. Long-term biomass responses were correlated with short- and long-term physiological responses in a direct relationship with the field Na gradient. Their experimental results supported the hypothesis that the individual species have evolved species-specific tissue Na tolerances in relation to their field soil Na concentrations. Hamilton et al. (2001) noted that S. spicatus exudes Na salts from its leaves as do other halophytic Sporobolus species.5 Further evidence from Australia supports a role for salinity as a driver in speciation. Several independent lines of evidenced phytogeography, plant and insect systematics, and insect behavioral ecologydpoint to a potential role for soil salinity in macroevolutionary processes for the genus Acacia and, indirectly, for the insect order Thysanoptera. Investigations of Acacia thrips systematics and their host-plant relationships (Crespi et al., 2004) show that: 1) A. harpophylla and A. cambagei harbor two sister-species pairs of elongate and round gall thrips (Kladothrips spp.); 2) phyllode-glueing thrips also show host specificity; and 3) thrips on A. harpophylla and A. cambagei display high species richness. Chronological phylogenetic analyses indicate that the approximate

5 The existence of salt glands in species across several genera of the Poaceae suggests that they had a common halophytic ancestor to Liphschitz and Waisel (1974).

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25

19

A

TRMIT EUSET CYBOM EUSIM EUPE1 EUSHI MESP1

2

ACSHI TRSP1

EUCA1

0

ACAR2

log(tss)

ERMIT SPCAR SPSP1

LYCA1

ACHAR ACCAM TEOB1

ERSP4 MENE1 HASP1 EUME1 PEPUB GRSP1 ACSP2 ENSP1 EUPER GRPAREUPOL ARSP1 PLCAR GRSTR ERSP1 EUSP1 ERAU1 HETRI BUINC CHFAL EUBR1 PASP1 EUPL1 DISP2 THTRI EUTE2 RHREP ACSA1 EUPAP HECO1 CYSP1 CHSP1 ATHEM BOSP1EUCR1 EUTES ALBAS BODE1 EUAUR

DISP1

BOEWA

ACBID EUER1

DISE1 URMOS EUCOO

-2

site occurence profile (species scores 2)

4

EUNOR

ACFAR

BOPER

CECIL

pH

OPEXA

EUORG

-4

-3

-2

-1

0

site occurrence profile (species scores 1)

-3

ACCAM ACHAR ACAR2 TEOB1 EUCA1 LYCA1 CECIL SPSP1 EUCOO SPCAR ERMIT ATHEM CHSP1 EUAUR CYSP1 EUNOR EUBR1 ACSA1 DISP2 DISP1 PASP1 GRSTR EUPER ACSHI TRSP1 ERAU1 ERSP1 ACFAR ENSP1 DISE1 ARSP1 OPEXA TRMIT GRSP1 BOEWA BUINC URMOS GRPAR BOSP1 EUORG ERSP4 CHFAL ACSP2 PLCAR EUTE2 BODE1 EUME1 MESP1 CYBOM EUSHI EUSP1 EUPE1 EUPAP PEPUB HECO1 MENE1 EUPL1 EUCR1 EUPOL EUTES HASP1 ALBAS THTRI EUSET BOPER EUSIM EUER1 RHREP ACBID HETRI

-6

-5

-4

log(TSS)

-2

-1

0

B

Fig. 4. A) Results of correspondence analysis; B) Response of vegetation to salinity starts at very low %TSS (TSS¼Total Soluble Salts) (from Bui and Henderson (2003), with permission). See Appendix for list of species names.

age of origin of gall thrips (Kladothrips spp.) is Miocene and that their subsequent diversification is closely linked to host-plant evolution; host affiliation with Plurinerves is estimated to date from 7.5 Mya (McLeish et al., 2007). Thus the congruence between planteinsect phylogenies and apparent co-speciation may have been driven by environmental factors including salinity. Other

recent work on Acacia biogeography in western and central Australia (Ladiges et al., 2006) suggests that speciation has been driven by aridity, but it does not consider salinity specifically. Salinity in Queensland dates back to the mid-Tertiary (Gunn and Richardson, 1978; van Dijk, 1980). Salinity in the area studied by Bui and Henderson (2003) is associated with the Campaspe Formation

20

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25

which is dated at 3.5e1.3 Mya (Nind, 1988). Acacia appears to have been established in eastern Australia by early Miocene and became an important component of sclerophyll communities by late Neogene (Macphail and Hill, 2001). That salt stress may have played a role in evolutionary ecology by exerting selection pressure on Australian vegetation is supported by taxonomic and recent chloroplast-DNA evidence that A. harpophylla, A. cambagei and A. argyrodendron are closely related species of microneurous Plurinerves (Crespi et al., 2004; Maslin, 2004; confirmed by J.T. Miller, CSIRO Plant Industry, pers. comm.). These are the three Acacia Table 1 Acacia species, their reported habitat and associated species (http://www. worldwidewattle.com). Section

Species

Juliflorae

A. catenulata

Habitat and assoc species

invariably in pure stands or with emergent eucalypts on shallow soils on scarps of weathered sediments, sometimes adjoining, but not mixing with, stands of A. shirleyi or A. aneura A. shirleyi Grows in shallow gravelly or skeletal sandy soils on sandstone or laterite often in dense stands, also in closed forests, low open forests or mixed savannah woodlands A. stowardii Common in shallow soils of stony or rocky ridges and breakaways, also on sand dunes; often in A. aneura communities on low hills A. adsurgens Grows in reddish sandy and gravelly soils, on flat plains and hillsides, commonly in spinifex grassland communities A. aneura var. usually on loamy or sandy soils in areas of low aneura relief or on shallow rocky soils on hills Plurinerves A. melanoxylon favors fertile soils in valleys and on flats in mountainous areas, often growing in wet sclerophyll forest and cooler rainforest. A. oswaldii in arid, semi-arid and subtropical areas in all mainland states S of 19 S; mainly in calcareous sands or loam. A. melvillei Grows in loam, clay and sand often in mixed open woodland and woodland A. papyrocarpa Grows in sandy loam, clay and calcareous soil, in low open woodland and shrubland, often with chenopods A. pendula Grows mainly on floodplains in fertile alluvial clay (and red earth soils in the South), sometimes dominant in woodland and open woodland A. tephrina Grows mainly in heavier soils, including alkaline and saline clays, in tall open woodland and, in drier areas, low woodland and shrubland A. loderi Grows in solonized brown and red soils, in low woodland and tall shrubland, sometimes associated with chenopods, Casuarina cristata or Acacia aneura A. microsperma grows in shallow loam or clay over weathered rock, often forming dense stands alone or with A. cambagei or Eucalyptus thozetiana A. cana Grows along watercourses on gibber plains and on sandhills as pure stands of scattered trees and in mixed woodland A. maranoensis Grows in texture contrast soils, usually in woodland of Eucalyptus populnea A. harpophylla Grows on fertile clay and loamy clay A. argyrodendron Grows mostly in dark cracking clay, either alone or, on the southern and eastern edge of its range, with Acacia harpophylla A. cambagei Tolerates a wide range of soils but occurs most commonly in dark cracking clay or loam, as scattered individuals or in dense, almost pure stands A. georginae Usually grows on plains and along watercourses in clay and loam, often dominating in low woodland and low open woodland

Fig. 5. Suggested environmental factors (see Table 1) associated with the splits of the phylogram from Crespi et al. (2004) with additional species closely related botanically in parentheses. Parkia timoriana is an outgroup. A. catenulata, A. stowardii, A. adsurgens, and A. aneura are Juliflorae (boxed). All others are Plurinerves.

species that exhibit tolerance of the highest levels of salt in Queensland (Bui and Henderson, 2003). Using published data (Orchard and Wilson, 2001), Table 1 synthesizes the ecology of Acacia species from sections Plurinerves and Juliflorae of subgenus Phyllodineae (see Maslin, 2004) for which phylogenetic relations have been advanced by Crespi et al. (2004). The habitats described for these species suggest that environmental factors could have played a role in the speciation of these acacias as schematized in Fig. 5. Alkalinity (calcareous habitat) and salinity are factors that appear to characterize the habitats of the Plurinerves closely related to A. harpophylla. Although tolerance to alkalinity seems to have appeared many times over the Acacia phylogeny, not all Plurinerves are salt-tolerant, thus salinity appears to have played a role in the speciation within this clade. The influence of environmental factors in biogeography and evolutionary ecology are notoriously difficult to unravel and the long record of landscape evolution in Australia suggests that climate and soil have interacted at length in driving the phylogeny of Acacia (C. Gonzalez-Orozco, pers. comm.). The trend toward aridity over the continent began in the mid-late Miocene (Martin, 2006) and the current monsoonal pattern over Queensland became established in the Holocene around 9000 years ago (Kershaw, 1978). Acacia are legumes and in some species form symbioses with rhizobia that are known to be tolerant of salt, drought, and high temperatures (Thrall et al., 2009; Zahran, 2001; Zhang et al., 1991). Fierer and Jackson (2006) found that edaphic variables and most importantly pH control soil bacterial biogeography across the Americas. Salinity may mediate subterranean processes that influence plantemicrobial interactions. Progress in the systematics of bacterial N-fixing legume symbionts (Sawada et al., 2003; Zheng et al., 2004) may shed further light on the role of salt-stress in evolutionary ecology. The convergence of three independent lines of evidence provides an exciting insight into the potential role of soil alkalinity and salinity on macroevolutionary processes for the genus Acacia. Acacia is a widespread genus (Maslin et al., 2003)6 and salinity may play a role in its distribution and speciation outside of Australia.

6

See http://www.worldwidewattle.com/infogallery/distribution.php.

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25

3. A role for soil salinity over short time scales Whereas the previous section has discussed the role of natural variations in salinity over geologic time, this section addresses the impact of changes in soil salinity brought about through anthropogenic activity, that occur over short time frames (years to decades). The threat of secondary dryland salinity to current patterns of biodiversity in Australia has been dealt with by others (e.g., Briggs and Taws, 2003; Cramer and Hobbs, 2002 and other papers in a special issue of Australian Journal of Botany; Keighery et al., 2004; Seddon et al., 2007) and this paper will only consider two aspects that have been overlooked: the possible role of salinity in weed invasion and woody vegetation encroachment. In the western USA, Scott et al. (2010) investigated possible mechanisms driving the invasion of Bromus tectorum L. which was introduced from Eurasia in the 1800s. B. tectorum is a selfing winter annual grass that has achieved widespread dominance in semiarid western North America since the 1930s and is actively invading salt desert habitats. They found that seeds from saline playa populations were able to establish better than those of most other populations across all habitats, including two highly saline sites. They concluded through molecular analysis that local population differentiation in B. tectorum resulted from differential selection on pre-adapted genotypes with characteristic micro-satellite marker fingerprints and found little evidence for selection favoring novel genotypes. 3.1. Invasive species and soil salinity in Australia Weed invasions are currently a major concern for land managers and conservation biologists in Australia. Current research has focused on dispersal mechanisms, recruitment and survival, subterranean root competition, functional traits, the role of grazing animals, the impact of fire, and control strategies but the role of soil salinity as a potential factor has been neglected. However, the data in Bui and Henderson (2003) show that the spatial pattern of Buffel grass (Cenchrus ciliaris L.), an introduced pasture grass now considered an invasive species (Fairfax and Fensham, 2000), is driven largely by soil pH and salinity (CECIL in Fig. 4A), even though C. ciliaris is only weakly salt-tolerant (Graham and Humphreys, 1970).7 Personal field observations in Queensland suggest that the woody weed Parkinsonia aculeata L. appears to colonize saline discharge areas where it forms monostands and that Parthenium hysterophorus L. also seems to be widespread in saline areas. Others have also reported a dominance of groundcover species by exotics, including weeds, on salinized sites in Queensland and New South Wales (Briggs and Taws, 2003). Tomar et al. (1998) have found P. aculeata a suitable species for afforestation of saline soils in India. Acacia nilotica (L.) Del. ssp. indica (Benth.) Brenan. is a woody weed in Australia (Miller et al., 2011) that has received much attention in the last decade (e.g. Kriticos et al., 2003). A. nilotica is known to perform well under water-logged, saline conditions (e.g. Marcar et al., 2003; Tomar et al., 1998). This raises the question of invasion by A. niloticadis it related in part to soil salinity? A similar question arises regarding Acacia farnesiana (L.) Willd., a woody weed (Miller et al., 2011) that grows on calcareous cracking clay soils and along saline artesian drains8 and is suitable for afforestation of saline soils (Tomar et al., 1998). The results of Bui and Henderson (2003) support an important role for soil pH in its

7 According to the FAO grassland species database, it grows optimally on soils with pH 7e8 and the Australian cultivar Biloela is more salt-tolerant than others (http://www.fao.org/ag/AGP/AGPC/doc/Gbase/DATA/Pf000196.HTM). 8 See http://www.fao.org/ag/AGP/AGPC/doc/Gbase/DATA/Pf000113.HTM.

21

distribution in Queensland (ACFAR in Fig. 4A). Interestingly, chloroplast-DNA analysis shows that A. nilotica and A. farnesiana are sister species (Bukhari et al., 1999). Since A. nilotica originates from Africa-Asia whereas A. farnesiana is from Central America, the adaptation to similar edaphic conditions appears ancestral to both. Prosopis L. is another woody weed in Australia with known salttolerant species (e.g. Le Houerou, 2003) so the same question applies to its ability to invade. Tomar et al. (1998) found Prosopis juliflora (Swartz) DC. to be suited for reclamation of saline soil in India. Stave et al. (2003) report that Prosopis chilensis (Mol.) Stuntz, introduced in Kenya around 1985, is invading the floodplain of the Turkwel River where electrical conductivity and carbonate content account for vegetation distribution. Thus the physical environment, stressed by salinity, may play a key role in defining a niche opportunity for weed invasion for plants that tolerate salt to a degree, especially at the seedling recruitment stage. In 1999 the Australian Government and state and territory governments endorsed a list of 20 Weeds of National Significance (WONS).9 Of these, twelve show some salt-tolerance (Table 2). Many WONS are phreatophytes or amphibious aquatic species that invade seasonal wetlands. It appears that areas that are affected by the interaction between shallow water tables and salt are particularly susceptible to weed invasions in Australia. Tree clearing, which changes the hydrological balance of landscapes and can promote soil salinization (Runyan and D’Odorico, 2010; Williamson, 1986), may be a human activity that also provides an advantage to opportunistic invaders. Nevertheless salinity has been neglected as a potential factor in invasion biology inland, although its role in coastal ecosystems in America has been demonstrated (e.g. Silliman and Bertness, 2004).

3.2. Woody vegetation encroachment into grassland and salinity A. harpophylla, although a native Australian species endemic to the Brigalow Belt, is considered a weed by rangeland managers because of its suckering habit (Bortolussi et al., 2005; Nix, 1994). An association between A. harpophylla and saline seeps is acknowledged by Nix (1994) and empirically demonstrated again in Bui and Henderson (2003) (ACHAR in Fig. 1). Emergent seedlings of A. harpophylla can tolerate high salinity (Nix, 1994; Reichman et al., 2006). Thickening of brigalow communities and encroachment of woody plants into grasslands has been a reported “nuisance” by Regional Vegetation Management Planning Committees across the Brigalow Belt, Desert Uplands, Mitchell Grass Downs, Gulf Plains biogeographic regions in Queensland. Woodland thickening is reportedly occurring on vast areas of rangelands, however, because it is not possible to assess with the resolution of Landsat TM data used to monitor statewide landcover change (Goulevitch et al., 1999, 2002), it is difficult to assess the actual area affected. According to Goulevitch et al. (1999), 20 sites show evidence of woodland encroachment into grassland from d13C which discriminates between C produced by trees using the C3 photosynthetic pathway from C produced by grasses using the C4 pathway. At one such site in Queensland where A. cambagei R.T. Bak., a salt-tolerant acacia species closely related to A. harpophylla (Bui and Henderson, 2003; Maslin, 2004), is encroaching on grassland, Krull et al. (2005) found that there was a strong shift from C4- (grass) to C3-derived (trees) soil C in the thickened woodland. Woodland thickening in savannas is generally attributed to changes in land management such as decreased fire incidence,

9

http://www.weeds.gov.au/weeds/lists/wons.html.

22

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25

Table 2 Of the 20 WONS, twelve show some salt- or alkalinity-tolerance; seven are phreatophytes; five are nitrogen-fixing legumes. Clearly soil chemistry and moisture are key variables in the ecology of weeds. Weeds of National Significance (WONS)

Salt-tolerant

Phreatophyte

Alligator weed (Alternanthera philoxeroides) Athel pine or tamarisk (Tamarix aphylla) Bitou bush (Chrysanthemoides monilifera ssp. rotundata) Boneseed (Chrysanthemoides monilifera ssp. monilifera) Blackberry (Rubus fruticosus aggregate) Bridal creeper (Asparagus asparagoides) Cabomba (Cabomba caroliniana) Chilean needle grass (Nassella neesiana) Gorse (Ulex europaeus) Hymenachne or Olive hymenachne (Hymenachne amplexicaulis) Lantana (Lantana camara) Mesquite (Prosopis species) Mimosa (Mimosa pigra) Parkinsonia (Parkinsonia aculeata) Parthenium weed (Parthenium hysterophorus) Pond apple (Annona glabra) Prickly acacia (Acacia nilotica) Rubber vine (Cryptostegia grandiflora) Salvinia (Salvinia molesta) Serrated tussock (Nassella trichotoma) Willow (Salix spp.)

Y Y Y

Y, facultative

a b

Aquatic

Leguminous (N2-fixer)

CRC Weed Managementa Di Tomaso (1998) CRC Weed Management

Y

? grows in gullies Alkalinity N

Y

N “not brackish water”

Y

Y

N Y Y Y Y? Y Y Y N Y

Y Facultative? Facultative?

Y Y Y

Y Y Facultative?

Y Y

Y

Reference for salttolerance

CRC CRC CRC CRC CRC CRC

Weed Weed Weed Weed Weed Weed

Management Management Management Management Management Management

CRC Weed Management FAOb ABRS (2007) FAOb Personal observation CRC Weed Management FAOb CRC Weed Management CRC Weed Management CRC Weed Management Kennedy et al. (2003)

CRC Weed Management data sheets for WONS: http://www.weeds.gov.au/publications/guidelines/index.html. FAO Grassland Index: http://www.fao.org/ag/AGP/AGPC/doc/Gbase/mainmenu.htm.

increasing grazing pressure, climate change and increasing atmospheric CO2 concentration (Archer, 1995; Bond and Midgley, 2012; Burrows, 2002; Fensham and Fairfax, 2005) but may be due to or reinforced byein some places at leastethe interaction between recent changes in landscape hydrology and soil salinity. Given that most of the Brigalow Belt has been cleared, it is possible that more water is moving laterally through local recharge areas into seepage areas, that salt is being transported, and that Acacia remnants and re-growth are encroaching on grassland that is becoming more saline close to the soil surface. Fairfax and Fensham (2005) found that episodes of thickening and encroachment of A. cambagei coincide with wet periods. Bui and Moran (2000) show that soil salinity is greater downslope of saline seepage areas under remnant brigalow stands in northern Queensland; this is confirmed in Silburn et al. (2009). Woodland encroachment, possibly responding to landscape salinization in the Brigalow Belt of Australia, may be a good example of habitat tracking in real time. In East Africa however, the situation appears reversed: if trees and bush thickets in low rainfall areas are left undisturbed long enough, they develop into grasslands (Belsky, 1990). Belsky (1990) concludes that trees do not grow in the Serengeti and Amboseli plains, even when protected from herbivory and fire, and that it is the high salinity and shallow soils that exclude trees from grasslands. There it seems that grasses are better adapted than trees to prevailing environmental conditions including soil salinity. But this situation may reflect in part the paleoenvironmental history of East Africa and the relatively smaller number of Acacia species in Africa (144) compared to Australian ones (w1000). 4. Implications for global change research Evidence from Australia and elsewhere suggests a role for soil salinity in biogeography and ecology (i.e., niche definition and selection pressure), at a range of spatio-temporal scales. Over the geologic time scale, it has played a part in driving speciation while in more recent time, over decades, it is changing current patterns of biodiversity.

Good predictive models of the distribution of biota and of their responses to environmental stress are essential for evidence-based management of biodiversity in Australia and throughout the world. To construct such models, predictor variables are required that can represent the underlying environmental gradient and processes that control spatial distribution. Biogeographic models throughout the world frequently rely on climatic and topographic datasets for predictions of species distribution (e.g., Austin and Meyers, 1996; Eeley et al., 1999; Reed et al., 2009). Perhaps this worldwide tendency to focus on climate and topography data in biogeographical studies also reflects the availability of those datasets. The existence of computer programs such as ANUCLIM makes the estimation of climatic variables as a function of meteorological and topographic data, and the definition of bioclimatic zones, readily achievable (Houlder et al., 1999). Because plant available water (and often other soil properties too) is a function of the interaction between climate and topography, commonly environmental gradient analyses focus on transects along climate and topographic gradients. The recent focus on assessment of climate change on ecosystems may also contribute to the relative neglect of edaphic factors. Even so, soil data are often not available. For Australia, that lacuna has been filled by the Australian Soil Resources Information System (ASRIS) datasets which generated digital maps of soil pH, % organic C, total P, total N, texture, % clay, and thickness for surface and subsurface horizons at 1-km resolution (Johnston et al., 2003). On a global scale, soil texture, pH, and soil type maps are also relatively more accessible than geochemical (salinity, major and trace element) maps but substrate geochemistry may be critical to account for observed floristic patterns (e.g. Martin et al., 2006; Reed et al., 2009). Better global hydrology coverage, including depth-to-groundwater and geochemistry, is also badly needed. Access to a comprehensive range of digital environmental datasets linked with biological datasets will give biogeographers and ecological modelers an opportunity to determine which factors are major drivers for the distribution of biota in any given region. It will be critical to evidence-based management of biodiversity; extinction risks could be higher than predicted if future locations of

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25

suitable climate do not coincide with other essential resources such as suitable soils (Austin and Van Niel, 2011; Bertrand et al., 2012; Thomas et al., 2004). At the same time, it will open the door to an emerging science area of “phylo-environmental modelling”, integrative research for reconstructing genetic and spatial patterns of change through geological time. Acknowledgments I want to thank Laurence Mound and the Australian Biological Resources Study for encouragement and permission to use Fig. 32 from Crespi et al. (2004), and the two anonymous reviewers for providing many useful comments and references for improving the paper. Appendix Species name

Species abbreviation

Acacia argyrodendron A. bidwilii A. cambagei A. farnesiana A. harpophylla A. salicina A. shirleyi A. species Albizia basaltica Aristida species Atalaya hemiglauca Bothriochloa decipiens Bothriochloa ewartiana Bothriochloa pertusis Bothriochloa species Bursaria incana Cenchrus ciliaris Chrysopogon fallax Chloris species Cymbopogon bombycinus Cyperus species Dichanthium sericeum Dichanthium species Digitaria species Enneapogon species Erythroxylon australe Eremophila mitchelii Eragrostis species Eriachne species Eulalia aurea Eucalyptus brownii E. cambageana E. coolibah E. crebra E. erythrophloia E. melanophloia E. normantonensis E. orgadophylla E. papuana E. peltata E. persistens E. platyphylla E. polycarpa E. setosa E. shirleyii E. similis E. species E. tereticornis E. tessellaris Grevillea parallela G. species G. striata Hakea species Heteropogon contortus

ACAR2 ACBID ACCAM ACFAR ACHAR ACSA1 ACSHI ACSP2 ALBAS ARSP1 ATHEM BODE1 BOEWA BOPER BOSP1 BUINC CECIL CHFAL CHSP1 CYBOM CYSP1 DISE1 DISP1 DISP2 ENSP1 ERAU1 ERMIT ERSP1 ERSP4 EUAUR EUBR1 EUCA1 EUCOO EUCR1 EUER1 EUME1 EUNOR EUORG EUPAP EUPE1 EUPER EUPL1 EUPOL EUSET EUSHI EUSIM EUSP1 EUTE2 EUTES GRPAR GRSP1 GRSTR HASP1 HECO1

23

(continued ) Species name

Species abbreviation

Heteropogon triticeus Lysiphillum carronii Melaleuca nervosa Melaleuca species Ophiurous exaltatus Panicum species Petalostigma pubescens Planchonia careya Rhynchelytrum repens Sporobolus caroli Sporobolus species Terminalia oblongata Themeda triandra Triodia mitchelii Triodia species Urochloa mosambicensis

HETRI LYCA1 MENE1 MESP1 OPEXA PASP1 PEPUB PLCAR RHREP SPCAR SPSP1 TEOB1 THTRI TRMIT TRSP1 URMOS

References ABRS, 2007. Flora of Australia On-line. http://www.environment.gov.au/ biodiversity/abrs/online-resources/flora/main/index.html (accessed 13.04.11.). Archer, S., 1995. Harry Stobbs Memorial Lecture, 1993: herbivore mediation of grass-woody plant interactions. Tropical Grasslands 29, 218e235. Austin, M.P., Meyers, J.A., 1996. Current approaches to modelling the environmental niche of eucalypts: implication for management of forest biodiversity. Forest Ecology and Management 85, 95e106. Austin, M.P., Van Niel, K.P., 2011. Impact of landscape predictors on climate change modelling of species distributions: a case study with Eucalyptus fastigata in southern New South Wales, Australia. Journal of Biogeography 38, 9e19. Bell, D.T., Williams, J.E., 1997. Eucalypt ecophysiology. In: Williams, J.E., Woinarski, J.C.Z. (Eds.), Eucalypt Ecology: Individuals to Ecosystems. Cambridge University Press, Cambridge, pp. 168e196. Belsky, A.J., 1990. Tree/grass ratios in East African savannas: a comparison of existing models. Journal of Biogeography 17, 483e489. Belsky, A.J., 1988. Regional influences on small scale vegetational heterogeneity within grasslands in the Serengeti National Park, Tanzania. Plant Ecology 74, 3e 10. Belsky, A.J., 1986. Population and community processes in a mosaic grassland in the Serengeti, Tanzania. Journal of Ecology 74, 841e856. Bertrand, R., Perez, V., Gégout, J.C., 2012. Disregarding the edaphic dimension in climate change: the case of Quercus pubescens in France. Global Change Biology 18, 2648e2660. Bond, W.J., Midgley, G.F., 2012. Carbon dioxide and the uneasy interactions of trees and savannah grasses. Philosophical Transactions of the Royal Society B 367 (1588), 601e612. http://dx.doi.org/10.1098/rstb.2011.0182 1471e2970. Bortolussi, G., McIvor, J.G., Hodgkinson, J.J., Coffey, S.G., Holmes, C.R., 2005. The Australian beef industry: a snapshot. 4. Condition and management of natural resources. Australian Journal of Experimental Agriculture 45, 1109e1120. Briggs, S.V., Taws, N., 2003. Impacts of salinity on biodiversitydclear understanding or muddy confusion? Australian Journal of Botany 51, 609e617. Bui, E.N., Henderson, B.L., 2003. Vegetation indicators of soil salinity in north Queensland. Austral Ecology 28, 539e552. Bui, E.N., Moran, C.J., 2000. Regional-scale investigation of the spatial distribution and origin of soluble salts in central north Queensland. Hydrological Processes 14, 237e250. Bukhari, Y.M., Koivu, K., Tigerstedt, P.M.A., 1999. Phylogenetic analysis of Acacia (Mimosaceae) as revealed from chloroplast RFLP data. Theoretical and Applied Genetics 98, 291e298. Burrows, W.H., 2002. Seeing the wood(land) for the trees e an individual perspective of Queensland woodland studies (1965e2005). Tropical Grasslands 36, 202e217. Bush, J.K., Van Auken, O.W., 2004. Relative competitive ability of Helianthus paradoxus and its progenitors, H. annuus and H. petiolaris (Asteraceae), in varying soil salinities. International Journal of Plant Sciences 165, 303e310. Cilliers, S.S., Bredenkamp, G.J., 2003. Vegetation of inland endorheic pans in the North-West Province, South Africa. Phytocoenologia 33, 289e308. Cisneros, J.M., Cantero, J.J., Cantero, A., 1999. Vegetation, soil hydrophysical properties, and grazing relationships in saline-sodic soils of Central Argentina. Canadian Journal of Soil Science 79, 399e409. Cramer, V.K., Hobbs, R.J., 2002. Ecological consequences of altered hydrological regimes in fragmented ecosystems in southern Australia: impacts and possible management responses. Austral Ecology 27, 546e564. Crespi, B.J., Morris, D.C., Mound, L.A., 2004. Evolution of Ecological and Behavioural Diversity: Australian Acacia Thrips as Model Organisms. Australian Biological Resources Study and Australian National Insect Collection, CSIRO, Canberra. Crowley, G.M., 1994. Quaternary soil-salinity events and Australian vegetation history. Quaternary Science Review 13, 15e22.

24

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25

Dirnbock, T., Hobbs, R.J., Lambeck, R.J., Caccetta, P.A., 2002. Vegetation distribution in relation to topographically driven processes in southwestern Australia. Applied Vegetation Science 5, 147e158. Di Tomaso, J.M., 1998. Impact, biology, and ecology of saltcedar (Tamarix spp.) in the southwestern United States. Weed Technology 12, 326e336. Duchaufour, P., 1982. Pedology. George Allen and Unwin. Edelist, C., Lexer, C., Dillmann, C., Sicard, D., Rieseberg, L.H., 2006. Microsatellite signature of ecological selection for salt tolerance in a wild sunflower hybrid species, Helianthus paradoxus. Molecular Ecology 15, 4623e4634. Edelist, C., Raffoux, X., Falque, M., Dillmann, C., Sicard, D., Rieseberg, L.H., Karrenberg, S., 2009. Differential expression of candidate salt-tolerance genes in the halophyte Helianthus paradoxus and its glycophyte progenitors H. annuus and H. petiolaris (Asteraceae). American Journal of Botany 96 (10), 1830e1838. Eeley, H.A.C., Lawes, M.J., Piper, S.E., 1999. The influence of climate change on the distribution of indigenous forest in KwaZulu-Natal, South Africa. Journal of Biogeography 26, 595e617. http://dx.doi.org/10.1046/j.1365-2699.1999.00307.x. El-Bana, M., Khedr, A.H., Van Hecke, P., Bogaert, J., 2002. Vegetation composition of a threatened hypersaline lake (Lake Bardawil), North Sinai. Plant Ecology 163, 63e75. Ellenberg, H., Weber, H.E., Dull, R., Wirth, V., Werner, W., Paulisen, D., 1991. Scripta Geobotanica, vol. 18. Verlag Erich Goltze KG, Göttingen. Ellery, W.N., Ellery, K., McCarthy, T.S., 1997. Plant-distribution in islands of the Okavango delta, Botswanaddeterminants and feedback interactions. African Journal of Ecology 31, 119e134. Fairfax, R.J., Fensham, R.J., 2000. The effect of exotic pasture development on floristic diversity in central Queensland, Australia. Biological Conservation 94, 11e21. Fairfax, R.J., Fensham, R.J., 2005. Preliminary assessment of gidgee (Acacia cambagei) woodland thickening in the Longreach district, Queensland. Rangeland Journal 27, 159e168. Fensham, R.J., Silcock, J., Biggs, A., 2007. Vegetation-soil relations in a highly sodic landscape, Yelarbon, southern Queensland. Cunninghamia 10 (2), 273e284. Fierer, N., Jackson, R.B., 2006. The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America 103, 626e631. Flowers, T.J., Galal, H.K., Bromham, L., 2010. Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biology 37, 604e612. Froend, R.H., Heddle, E.M., Bell, D.T., McComb, A.J., 1987. Effects of salinity and waterlogging on the vegetation of Lake Toolibin, Western Australia. Australian Journal of Ecology 12, 281e298. Goldhaber, M.B., Mills, C., Stricker, C.A., Morrison, J.M., 2011. The role of critical zone processes in the evolution of the Prairie Pothole Region wetlands. Applied Geochemistry 26, S32eS35. Goulevitch, B.M., Danaher, T.J., Stewart, A.J., Harris, D.P., Lawrence, L.J., 2002. Mapping woody vegetation cover over the state of Queensland using Landsat TM and ETMþ imagery. In: Proceedings of the 11th Australasian Remote Sensing and Photogrammetry Conference, Brisbane, Australia, September 2002. http:// www.nrme.qld.gov.au/slats/pdf/0127anav.pdf. Goulevitch, B.M., Danaher, T.J., Walls, J.W., 1999. The Statewide Landcover and Trees Study (SLATS) e monitoring land cover change and greenhouse gas emissions in Queensland. In: Proceedings of IEEE International Geoscience and Remote Sensing Symposium, Hamburg, June 1999. http://www.nrme.qld.gov.au/slats/ pdf/igarss99overview.PDF. Graham, T.W.G., Humphreys, L.R., 1970. Salinity response of cultivars of buffel grass (Cenchrus ciliaris). Australian Journal of Experimental Agriculture and Animal Husbandry 10, 725e728. Gunn, R.H., Richardson, D.P., 1978. The nature and possible origins of soluble salts in deeply weathered landscapes of eastern Australia. Australian Journal of Soil Research 17, 197e215. Hamilton, E.W., McNaughton, S.J., Coleman, S.J., 2001. Molecular, physiological, and growth responses to sodium stress in C4 grasses from a soil salinity gradient in the Serengeti ecosystem. American Journal of Botany 88, 1258e1265. Hardie, L.A., Eugster, H.P., 1970. The evolution of closed-basin brines. Mineralogical Society of America Special Publication 3, 273e290. Heagle, D., Hayashi, M., van der Kamp, G., 2013. Surfaceesubsurface salinity distribution and exchange in a closed-basin prairie wetland. Journal of Hydrology 478, 1e14. Hilgert, N.I., Pensiero, J.F., Marino, G., Lewis, J.P., D’Angelo, C., 2003. Vegetation of the Saladillo area (province of Santa Fe) in the south Chaco, Argentina. Interciencia 28, 512e520. Hopper, S.D., 2009. OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant and Soil 322 (1), 49e86. Houlder, D., Hutchinson, M., Nix, H., McMahon, J., 1999. ANUCLIM Version 5.0. User Guide. Centre for Resource and Environmental Studies, The Australian National University, Canberra. Hughes, L., 2003. Climate change and Australia: trends, projections and impacts. Austral Ecology 28, 423e443. IUSS Working Group WRB, 2006. World Reference Base for Soil Resources 2006. World Soil Resources Reports No. 103. FAO, Rome. Javid, M., Nicolas, M., Ford, R., 2011. Current knowledge in physiological and genetic mechanisms underpinning tolerances to alkaline and saline subsoil constraints of broad acre cropping in dryland regions. In: Shanker, Arun, Venkateswarlu, B. (Eds.), Abiotic Stress in Plants e Mechanisms and Adaptations. InTech, pp. 193e 214. Available from: http://www.intechopen.com/books/abiotic-stress-in-

plants-mechanisms-and-adaptations/current-knowledge-in-physiological-andgenetic-mechanisms-underpinning-tolerances-to-alkaline-and-sa. Johnston, R.J., Barry, S.J., Bleys, E., Bui, E.N., Moran, C.J., Simon, D.A.P., Carlile, P., McKenzie, N.J., Henderson, B., Chapman, G., Imhoff, M., Maschmedt, D., Howe, D., Grose, C., Schokneckt, N., Powell, B., Grundy, M., 2003. ASRIS: the database. Australian Journal of Soil Research 41, 1021e1036. Kadereit, G., Ackerly, D., Pirie, M.D., 2012. A broader model for C4 photosynthesis evolution in plants inferred from the goosefoot family (Chenopodiaceae s.s.). Proceedings of the Royal Society B 279 (1741), 3304e3311. http://dx.doi.org/ 10.1098/rspb.2012.0440 1471e2954. Karrenberg, S., Edelist, C., Lexer, C., Rieseberg, L., 2006. Response to salinity in the homoploid hybrid species Helianthus paradoxus and its progenitors H. annuus and H. petiolaris. New Phytologist 170 (3), 615e629. Keighery, G.J., Halse, S.A., McKenzie, N.L., Harvey, M.S. (Eds.), 2004. A Biodiversity Survey of the Western Australian Agricultural Zone. Western Australian Museum, Perth, Records of the Western Australian Museum. Supplement 67, 384 p. Kennedy, S.A., Ganf, G.G., Walker, K.F., 2003. Does salinity influence the distribution of exotic willows (Salix spp.) along the Lower River Murray? Marine Freshwater Research 54, 825e831. Kershaw, A.P., 1978. Record of last interglacial cycle from north-eastern Queensland. Nature 272, 159e162. Kershaw, A.P., Moss, P., Van Der Kaars, S., 2003. Causes and consequences of longterm climatic variability on the Australian continent. Freshwater Biology 48, 1274e1283. Kier, G., Mutke, J., Dinerstein, E., Ricketts, T.H., Kuper, W., Kreft, H., Barthlott, W., 2005. Global patterns of plant diversity and floristic knowledge. Journal of Biogeography 32, 1107e1116. Kreeb, K.H., Whalley, R.D.B., Charley, J.L., 1995. Some investigations into soil and vegetation relationships associated with alkaline-saline soil surfaces in the Walcha area, Northern Tablelands, New South Wales. Australian Journal of Agricultural Research 46, 209e224. Kriticos, D.J., Sutherst, R.W., Brown, J.R., Adkins, S.W., Maywald, G.F., 2003. Climate change and the potential distribution of an invasive alien plant: Acacia nilotica ssp. indica in Australia. Journal of Applied Ecology 40, 111e124. Krull, E.S., Skjemstad, J.O., Burrows, W.H., Bray, S.G., Wynn, J.G., Bol, R., Spounder, L., Harms, B., 2005. Recent vegetation changes in Australia: evidence from d13C and 14C analyses of soil organic matter. Geoderma 126, 241e259. Ladiges, P.Y., Ariati, S.R., Murphy, D.J., 2006. Biogeography of the Acacia victoriae, pyrifolia and murrayana species groups in arid Australia. Journal of Arid Environments 66, 462e476. Lauchli, A., Luttge, U., 2002. Salinity: EnvironmentePlantseMolecules. Kluwer Academic Publishers. Le Houerou, H.N., 2003. Bioclimatology and phytogeography of the Red Sea and Aden Gulf Basins: a monograph (with a particular reference to the highland evergreen sclerophylls and lowland halophytes). Arid Land Research and Management 17, 177e256. Lexer, C., Fay, M.F., 2005. Adaptation to environmental stress: a rare or frequent driver of speciation? Journal of Evolutionary Biology 18, 893e900. http:// dx.doi.org/10.1111/j.1420-9101.2005.00901.x. Liphschitz, N., Waisel, Y., 1974. Existence of salt glands in various genera of the Gramineae. New Phytologist 73, 507e513. Macphail, M.K., Hill, R.S., 2001. Fossil record of Acacia in Australia: Eocene to present. In: Orchard, A.E., Wilson, A.J.G. (Eds.), Flora of Australia. Mimosaceae, Acacia Part 1, vol. 11A. CSIRO Publishing, Melbourne, pp. 13e29. Marcar, N.E., Ansari, R., Khanzada, A.N., Khan, M.A., Crawford, D.F., 2003. Performance of several tree species on a saline site in southern Pakistan. Journal of Tropical Forest Science 15, 457e468. Martin, C. San, Subiabre, M., Ramirez, C., 2006. A floristic and vegetational study of a latitudinal gradient of salt marshes in South-Central Chile. Ciencia e Investigacion Agraria 33 (1), 33e40. Martin, H.A., 2006. Cenozoic climatic change and the development of the arid vegetation in Australia. Journal of Arid Environments 66, 533e563. Maslin, B.R., 2004. Botanical Annexe. In: Crespi, B.J., Morris, D.C., Mound, L.A. (Eds.), Evolution of Ecological and Behavioural Diversity: Australian Acacia Thrips as Model Organisms. Australian Biological Resources Study and Australian National Insect Collection. CSIRO, Canberra, pp. 97e112. Maslin, B.R., Miller, J.T., Seigler, D.S., 2003. Overview of the generic status of Acacia (Leguminosae: Mimosoideae). Australian Systematic Botany 16, 1e18. McLeish, M.J., Chapman, T.W., Schwarz, M.P., 2007. Host-driven diversification of gall-inducing Acacia thrips and the aridification of Australia. BMC Biology 5, 3. http://dx.doi.org/10.1186/1741-7007-5-3. Miletto, M., Loy, A., Antheunisse, A.M., Loeb, R., Bodelier, P.L.E., Laanbroek, H.J., 2008. Biogeography of sulfate-reducing prokaryotes in river floodplains. FEMS Microbiology Ecology 64 (3), 395e406. Miller, J.T., Murphy, D.J., Brown, G.K., Richardson, D.M., González-Orozco, C.E., 2011. The evolution and phylogenetic placement of invasive Australian Acacia species. Diversity and Distributions 17, 848e860. http://dx.doi.org/10.1111/j.14724642.2011.00780.x. Molina, J.A., Casermeiro, M.A., Moreno, P.S., 2003. Vegetation composition and soil salinity in a Spanish Mediterranean coastal ecosystem. Phytocoenologia 33, 475e494. Mueller-Dombois, D., Ellenberg, H., 1974. Aims and Methods of Vegetation Ecology. John Wiley and Sons.

E.N. Bui / Journal of Arid Environments 92 (2013) 14e25 Nind, M.A.P., 1988. Age of Campaspe Formation, north Queensland. Search 19 (1), 30e32. Nix, H., 1994. Brigalow. In: Dovers, S. (Ed.), Australian Environmental History: Essays and Cases. Oxford University Press, pp. 198e233. Northcote, K.H., Skene, J.K.M., 1972. Australian Soils with Saline and Sodic Properties. CSIRO Soil Publ. No. 27. CSIRO, Melbourne. Noy-Meir, I., 1974. Multivariate analysis of the semi-arid vegetation in south-eastern Australia. II. Vegetation catenae and environmental gradients. Australian Journal of Botany 22, 115e140. Orchard, A.E., Wilson, A.J.G. (Eds.), 2001. Flora of Australia. Mimosaceae, Acacia, vol. 11B. CSIRO Publishing, Melbourne. Parida, A.K., Das, A.B., 2005. Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety 60, 324e349. Perelman, S.B., Leon, R.J.C., Oesterheld, M., 2001. Cross-scale vegetation patterns of Flooding Pampa grasslands. Journal of Ecology 89, 562e577. Pfennig, D.W., Wund, M.A., Snell-Rood, E.C., Cruickshank, T., Schlichting, C.D., Moczek, A.P., 2010. Phenotypic plasticity’s impacts on diversification and speciation. Trends in Ecology & Evolution 25, 459e467. Reed, D.N., Anderson, T.M., Dempewolf, J., Metzger, K., Serneels, S., 2009. The spatial distribution of vegetation types in the Serengeti ecosystem: the influence of rainfall and topographic relief on vegetation patch characteristics. Journal of Biogeography 36, 770e782. Reichman, S.M., Bellairs, S.M., Mulligan, D.R., 2006. The effects of temperature and salinity on Acacia harpophylla (brigalow) (Mimosaceae) germination. Rangeland Journal 28, 175e178. http://dx.doi.org/10.1071/RJ06027. Rengasamy, P., 2006. World salinization with emphasis on Australia. Journal of Experimental Botany 57, 1017e1023. Richardson, J.L., Arndt, J.L., Freeland, J., 1994. Wetland soils of the Prairie Potholes. Advances in Agronomy 52, 121e171. Rieseberg, L.H., Raymond, O., Rosenthal, D.M., Lai, Z., Livingstone, K., Nakazato, T., Durphy, J.L., Schwarzbach, A., Donovan, L.A., Lexer, C., 2003. Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301, 1211. Rogel, J.A., Silla, R.O., Ariza, F.A., 2001. Edaphic characterization and soil ionic composition influencing plant zonation in a semi-arid Mediterranean salt marsh. Geoderma 99, 81e98. Runyon, C.W., D’Odorico, P., 2010. Ecohydrological feedbacks between salt accumulation and vegetation dynamics: role of vegetation-groundwater interactions. Water Resources Research 46 (W11561), 11. Sage, R.F., 2001. Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biology 3, 202e213. http://dx.doi.org/10.1055/s-2001-15206. Sawada, H., Kuykendall, L.D., Young, J.M., 2003. Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. Journal of General and Applied Microbiology 49, 155e179. Schmiedel, U., Jurgens, N., 1999. Community structure on unusual habitat islands: quartz-fields in the succulent Karoo, South Africa. Plant Ecology 142, 57e69. Schofield, R.V., Kirkby, M.J., 2003. Application of salinization indicators and initial development of global soil salinization scenario under climatic change. Global Biogeochemical Cycles 17, 1078. http://dx.doi.org/10.1029/2002GB001935. Seddon, J.A., Zerger, A., Doyle, S.J., Doyle, S.J., Briggs, S.V., 2007. The extent of dryland salinity in remnant woodland and forest within an agricultural landscape. Australian Journal of Botany 55, 533e540. Scott, J.W., Meyer, S.E., Merrill, K.R., Anderson, V.J., 2010. Local population differentiation in Bromus tectorum L. in relation to habitat-specific selection regimes. Evolutionary Ecology 24, 1061e1080. Shaltout, K.H., El-Halawany, E.F., El-Garawany, M.M., 1997. Coastal lowland vegetation of eastern Saudi Arabia. Biodiversity and Conservation 6, 1027e1044.

25

Silburn, D.M., Cowie, B.A., Thornton, C.M., 2009. The Brigalow Catchment Study revisited: effects of land development on deep drainage determined from nonsteady chloride profiles. Journal of Hydrology 373, 487e498. Silliman, B.R., Bertness, M.D., 2004. Shoreline development drives invasion of Phragmites australis and the loss of plant diversity on New England salt marshes. Conservation Biology 18, 1424e1434. Stave, J., Oba, G., Bjora, C.S., Mengistu, Z., Nordal, I., Stenseth, N.C., 2003. Spatial and temporal woodland patterns along the lower Turkwel River, Kenya. African Journal of Ecology 41, 224e236. Stewart, R.E., Kantrud, H.A., 1972. Vegetation of Prairie Potholes, North Dakota, in Relation to Quality of Water and Other Environmental Factors. Geological Survey Professional Paper 585-D. U.S. Geological Survey, Denver. Subbarao, G.V., Ito, O., Berry, W.L., Wheeler, R.M., 2003. Sodiumda functional plant nutrient. Critical Reviews in Plant Sciences 22, 391e416. Thrall, P.H., Broadhurst, L.M., Hoque, M.S., Bagnall, D.J., 2009. Diversity and salt tolerance of native Acacia rhizobia isolated from saline and non-saline soils. Austral Ecology 34, 950e963. Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., Ferreira de Siqueira, M., Grainger, A., Hannah, L., Hughes, L., Huntley, B., van Jaarsveld, A.S., Midgley, G.F., Miles, L., Ortegua-Huerta, M.A., Townsend Peterson, A., Phillips, O.L., Williams, S.E., 2004. Extinction risk from climate change. Nature 427, 145e148. Tomar, O.S., Gupta, R.K., Dagar, J.C., 1998. Afforestation techniques and evaluation of different tree species for waterlogged saline soils in semiarid tropics. Arid Soil Research and Rehabilitation 12, 301e316. Toth, T., Rajkai, K., 1994. Soil and plant correlations in a solonetzic grassland. Soil Science 157, 253e262. United States Salinity Laboratory Staff, 1969. Diagnosis and Improvement of Saline and Alkali Soils. Agriculture Handbook No. 60, Rev. ed. United States Department of Agriculture, Washington, DC. van Dijk, D.C., 1980. Salt and Soil Reaction Patterns in the Tara Brigalow Lands, South-east Queensland. Division of Soils Divisional Report No. 47. CSIRO, Melbourne. Wardell-Johnson, G.W., Williams, J.E., Hill, K.D., Cumming, R., 1997. Evolutionary biogeography and contemporary distribution of eucalypts. In: Williams, J.E., Woinarski, J.C.Z. (Eds.), Eucalypt Ecology: Individuals to Ecosystems. Cambridge University Press, Cambridge, pp. 92e128. Whittig, L.D., Janitsky, P., 1963. Mechanisms of formation of sodium carbonate in soils. 1. Manifestations of biological conversions. Journal of Soil Science 14 (2), 322e333. Williamson, D.R., 1986. The hydrology of salt affected soils in Australia. Reclamation and Revegetation Research 5, 181e196. Wolicka, D., Jarzynowska, L., 2012. Microbiological reduction of sulphates in salty environments and mineralogical characterization of the transformation products. Geomicrobiology Journal 29 (6), 528e536. Yang, C.W., Zhao, N., Xu, C.M., Liu, B., Shi, D.C., 2012. Regulation of ion homeostasis in rice subjected to salt and alkali stresses. Australian Journal of Crop Sciences 6, 724e731. Zahran, H.H., 2001. Rhizobia from wild legumes: diversity, taxonomy, ecology, nitrogen fixation and biotechnology. Journal of Biotechnology 91, 143e153. Zhang, X.P., Harper, R., Karsisto, M., Lindstrom, K., 1991. Diversity of Rhizobium bacteria isolated from the root nodules of leguminous trees. International Journal of Systematic Bacteriology 41, 104e113. Zheng, J.F., Liu, G.R., Zhu, W.F., Zhou, Y.G., Liu, S.L., 2004. Phylogenetic clusters of rhizobia revealed by genome structures. Science in China Series C e Life Sciences 47, 268e278. Zhu, J.K., 2001. Plant salt tolerance. Trends in Plant Science 6, 66e71.