Salt tolerance screening of selected Australian woody species — a review

Forest Ecology and Management 139 (2000) 1±19

Salt tolerance screening of selected Australian woody species Ð a review S.R. Niknama,b, Jen McComba,* a

b

School of Biological Sciences and Biotechnology, Murdoch University, Murdoch, WA 6150, Australia Plant Science, Faculty of Agriculture, The University of Western Australia, Nedlands, WA 6907, Australia Received 25 May 1999; accepted 21 November 1999

Abstract This review critically evaluates the strategies for selection of salt tolerant woody Australian species for land reclamation. There is evidence that in selecting material to screen, provenances from saline areas will show higher levels of salt tolerance than those from non-saline areas. However, there are suf®cient numbers of exceptions to justify inclusion in trials of some material from non-saline areas. Because of the complexity and long term nature of ®eld trials, large numbers of species and provenances have been screened as juvenile plants (up to 1 year old) in the glasshouse. For very few of these, has the match between performance in glasshouse and ®eld been checked. In Eucalyptus, the genus for which most species have been screened, the assessment of salinity tolerance is the same in the ®eld and glasshouse for 20 species, three appear more tolerant in the ®eld than the glasshouse and ®ve are less tolerant in the ®eld than would be expected from glasshouse results. For 13 eucalypt species there are con¯icting results between different glasshouse and/or ®eld trials. A similar picture emerges for Melaleuca, Acacia and Casuarina though in these genera fewer species have been tested in both glasshouse and ®eld. Glasshouse trials have a role where speci®c information is needed from juvenile plants such as the ability of a species to exclude salt from the leaves, or performance under controlled conditions of waterlogging or saline waterlogging. However, as the objective of most experiments is to identify superior salt tolerant lines for the ®eld, despite the complexity and cost, well designed and monitored ®eld trials are the ultimate test. Researchers are also encouraged to consider inclusion of appropriate standard lines of Eucalyptus camaldulensis and E. occidentalis to enable better comparisons between trials. # 2000 Elsevier Science B.V. All rights reserved. Keywords: Salinity; Selection; Eucalyptus; Melaleuca; Acacia; Casuarina

1. Introduction Secondary salinisation is affecting millions of hectares of land around the world mainly due to clearing of forests and shrub lands for agriculture and also due to excessive irrigation. Although estimates of the *

Corresponding author. Tel.: ‡61-89360-2336; fax: ‡61-89360-6303 E-mail address: [email protected] (J. McComb).

extent of the areas affected by salinity vary, it is clear that some of the worst affected areas are Africa, southwest Asia, Australia and central America (Dudal and Purnell, 1986; Ghassemi et al., 1995). In Australia, before European settlement there were large areas of natural primary salinity, but secondary salinity was detected within the ®rst 100 years of settlement (Wood, 1924; Scho®eld et al., 1988). Recent studies estimate that 4 million hectares of land are affected in Australia (Williamson, 1990; Robertson, 1996;

0378-1127/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 9 9 ) 0 0 3 3 4 - 5

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Scho®eld, 1997). Most of the dry-land salt-affected areas are in Western Australia and it has been predicted that in this state alone, the total area affected could rise to 3.3 million hectares in the next 15 to 25 years (Ferdowsian et al., 1996). Tree planting has an important role for the control of salinity in both recharge and discharge areas. The commercial impact of planting trees in these two types of areas is different because recharge areas are usually productive agricultural lands while discharge areas have lost the most valuable agricultural species. The types of trees required in these areas differs as trees with high rates of transpiration are desirable in the recharge areas, and salt and waterlogging tolerance are essential in discharge areas. Many tree species that are salt-waterlogging tolerant will provide fodder, shade shelter and windbreaks; there are fewer that will yield products of commercial value such as oil, lumber and paper pulp. It is more likely that species that provide commercial timber will be found for areas with lower ranges of salinity (up to 8 dSmÿ1 Ecse), while in more extreme salinity, the land care value of establishing species such as Melaleuca or Casuarina is more important than commercial return. Compared with annual agricultural crops, trees have a higher water use and can therefore lower the raised water tables of cleared areas and so reduce salt discharge into streams. Experimental reforestation in catchments in the southwestern Australia has shown that plantations can dramatically reduce ground water levels and salt discharge from catchments in the 800± 900 mm rainfall zone. A study of the impact of reforestation on ground-water levels over 11 years at one site showed that beneath reforestation, groundwater level decreased by 6 m while under pasture it increased by 2 m (Bari and Boyd, 1994). A similar study showed that salt discharge was reduced to 10% of that predicted without reforestation (Scho®eld et al., 1989). As dense plantations use more water than the original native vegetation on a per unit area basis, it is not necessary to revegetate all of an agricultural area with trees to achieve a signi®cant reduction in the level and salinity of ground water. The water uptake of plantation Eucalyptus camaldulensis so far exceeded the 432 mm of annual rainfall at Wubin in Western Australia that it was estimated that reforestation of 37% of the lower catchment would be suf®cient to prevent further rise of ground water (Marshall et al.,

1997). The area of tree plantation required to restore hydrological balance varies with annual rainfall (Scho®eld and Ruprecht, 1989). The effectiveness of tree plantations in discharge areas is not clear-cut. Some experimental plantations of mixed species have not reduced the extent of salt scalds over a period of 15 years (Greenwood et al., 1994). Whether or not the plants will remove more water than would have been lost from a bare surface depends on the subsurface hydrology, as well as plant factors such as canopy shape and density and partitioning of water uptake between recharge and ground water (Thorburn, 1996; Cramer et al., 1999). If lowering the water table is a priority, it is necessary to monitor the ground water as some trees may survive in saline areas, and possibly ful®ll a role in providing shelter or increasing biodiversity, but not lower the water table. To select tree genotypes tolerant of salinity, an obvious method would appear to be to clone trees surviving and growing in saline areas. This strategy is rarely feasible, as for many tree species, and particularly eucalypts, it is usually very dif®cult to root cuttings from mature trees (McComb et al., 1996). Cultures from the crowns of mature trees may take years to stabilise in vitro and many lines never regain the ability to root (McComb and Bennett, 1986). Tissue cultured plants from explants of mature trees may also have problems with topophysis or plagiotropism. There are techniques for making it easier to clone from mature trees, such as felling the tree and taking explants from basal coppice, or repetitive grafting onto juvenile root-stocks (McComb et al., 1996) but they have rarely been applied to mature, salt tolerant trees. One example of success in cloning from mature trees is from the Victorian Department of Conservation and Natural Resources. Clones have been established directly from mature trees of salt tolerant E. camaldulensis (Morris, 1995). These clones performed well in areas of similar climate and soil to the parent trees, under both saline irrigation and dryland salinity conditions. A commonly employed approach has been to collect seed from a number of provenances thought to be salt tolerant and, using glasshouse screening of the seedlings, identify the most salt tolerant provenances. Where cloning protocols are available, genotypes showing the highest salt tolerance are cloned for ®eld

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planting. It is apparent from this review that relatively little work has been done to follow up ®eld trials and compare the performance of trees in the glasshouse and ®eld to prove that the glasshouse screening has in fact resulted in the selection of the most salt tolerant lines. This review will assess screening methods for salt tolerance and the evidence that glasshouse screening of juvenile plants identi®es lines that have superior salt tolerance as mature trees in the ®eld. 2. Mechanisms of salt tolerance The mechanisms adopted by salt tolerant plants have been reviewed extensively (Greenway and Munns, 1980; Levitt, 1980) and Allen et al. (1994b) and Bell (1999) have summarised the information in relation to salt tolerant trees. It is only necessary to brie¯y summarise their conclusions. Tolerant species use more than one strategy for avoidance or tolerance of salt stress. Most important is to keep the levels of ions in young leaves and shoot apices low. This is achieved by exclusion of ions at the point of uptake, and/or reduction of translocation of ions to the shoot. An ability to maintain ion exclusion from young shoots under hypoxic conditions of waterlogging is also vital. As the concentration of salt is increased, the most important mechanism giving rise to salt tolerance may change. At low to moderate salt levels, ion exclusion may be operational. However, there will be a salt level at which this mechanism will no longer be effective and salt uptake occurs. Only species that have some tolerance mechanism will survive these higher levels. Tolerant species may have mechanisms of compartmentalisation of ions in vacuoles, or deposition into bark, ray cells, tracheid walls and lumens, or older senescent leaves. Also important is the ability of the plant to continue water uptake in the presence of high salt concentrations. Different E. camaldulensis clones have been found to have different mechanisms of tolerance. Some have high growth and high water transport rates, but strong stomatal control of water loss during stress; others have slower growth and maintenance of stomatal conductance during stress, but tolerance of high tissue levels of Na‡ (Farrell et al., 1996). E. grandis tolerates low to medium levels of soil salinity through exclusion mechanisms, but once these break down the tissues

3

are very sensitive to salt. Sun and Dickinson (1993) found E. grandis to be the most tolerant of 16 eucalypts they tested at 50, 100 and 150 mM NaCl, but the plants died at 200 mM NaCl. E. maculata on the other hand, showed less tolerance than E. grandis at the lower salt levels but survived at 200 mM salt. Species that have salt excretion mechanisms such as salt glands are not appropriate for planting in saline areas when the objective is to reduce soil salinity. In these species, salt uptake and excretion results in redeposition of salt, as salt is washed from leaves or the leaves abscise. There are few tree species in this category. Tamarix is a species with salt excretion from the shoots that has been tested. In a saline area in Kerang T. articulata had a chlorine content of 65.8 mg g dwÿ1 in the foliage compared with 8 mg g dwÿ1 for E. camaldulensis growing on the same site (Morris, 1984). Tamarix may be inappropriate for planting in Australia as it has recently shown an explosive spread as an environmental weed along river courses in arid areas (Grif®n et al., 1989). Planting of woody shrubs with salt glands such as Atriplex is justi®ed on the basis of the fodder they produce and the lowering of the water table, not solely on the expectation that they will ameliorate the salinity of an area (Davidson and Galloway, 1991). 3. Genetic control of salt tolerance If it could be shown that salt tolerance is under strong genetic control, we could be more con®dent that resistance to salt in glasshouse trials will be correlated to ®eld performance. Interspeci®c genetic variation for salt tolerance has been found in many genera including Acacia, Eucalyptus, Melaleuca, Prosopis and Casuarina, but is perhaps best documented for Eucalyptus species (Blake, 1981; Sun and Dickinson, 1993; Bell, 1999). Intraspeci®c variation in tolerance to the combination of salinity and waterlogging has been reported in species from these genera and from gymnosperm species (e.g. Taxodium distichum) (Sands, 1981; Saur et al., 1995; Allen et al., 1996). This variation is hardly surprising. It is however surprising to ®nd reports of within-cultivar variation in salt tolerance in lucerne (Noble et al., 1984). Despite considerable genetic variability in salt tolerance in tree species, there has been little progress in

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assessment of level of heritability or identi®cation of genes controlling salt tolerance. Studies in annual crops (Mishra et al., 1988; Dvorak et al., 1992) suggest that salt tolerance is a complex multigenic trait. There is evidence that, in several temperate forage legumes, moderate to high heritability exists for salt tolerance (Noble and Rogers, 1994). In rice, tomato and wheat there is either dominance or overdominance for tolerance (Moeljopawira and Ikehashi, 1981; Subbarao and Johansen, 1994), while in soybeans Clÿ exclusion is under the control of a dominant gene (Able, 1969). Citrus and Vitis are amongst the few woody plants in which inheritance of salt tolerance has been evaluated. In Citrus the inheritance of Na‡ and Clÿ exclusion is independent and both are polygenic (Sykes, 1992), while in Vitis Clÿ exclusion was originally thought to be under the control of a dominant gene (Newman and Antcliff, 1984; Sykes, 1987) but polygenic control is now favoured (Sykes, 1992). One piece of evidence from E. camaldulensis (Bell et al., 1994) is that open pollinated seedlings from a salt tolerant tree in an orchard of salt tolerant lines showed an even higher level of tolerance than the female parent. In contrast Oddie and McComb (1996) found in controlled crosses between salt tolerant E. camaldulensis clones that the level of salt tolerance in the F1 was intermediate between the two parents. A possible explanation is the difference in male parentage in the two trials. Marcar et al. (1996) reported within provenance high narrow-sense heritability (h2) for shoot and root dry weights of E. grandis and E. globulus over all treatments of salt, waterlogging and saltwaterlogging (Marcar et al., 1995, 1996). It seems possible that the inheritances of ability to exclude Na‡ and Clÿ are independent, as are those of the ability to tolerate high levels of ions. It is not known whether or not combinations of the genes for these traits give additive salt resistance. The possibilities have yet to be explored of crossing salt tolerant species such as E. sargentii and E. spathulata (Van der Moezel and Bell, 1990) or including in breeding programs, trees with traits complementary to salt tolerance such as cold tolerance and early vigour (Munns and Richards, 1997). For Eucalyptus species, salt tolerance and frost tolerance appear related (Marcar, 1989). The possibility of using DNA markers to detect salt tolerance at a young age and without the need to

expose the plants to salinity is a new and exciting prospect. To identify appropriate markers, segregating progenies from crosses between salt tolerant and salt sensitive parents, and the parents themselves are required. Markers that identify plants that exclude salt at low concentrations, may well be different from those that distinguish plants that survive high salt concentrations. DNA studies of salt tolerance in woody species are scarce. However in herbaceous species Ding et al. (1998) found a major gene for salt tolerance on chromosome 7 in rice, while Foolad and Chen (1998) reported polygenic control of salt tolerance in tomatoes at the germination stage. 4. Choice of provenances to screen for salt tolerance Natural selection has resulted in development of salt tolerant species and of ecotypes within species. It is logical to expect best results from selection trials for salt tolerance from species that grow naturally in saline environments, and within a species, from progeny of plants growing in the most extreme saline conditions. This strategy has been used by many workers (Bell et al., 1994) and the expectation that these starting materials will give the highest levels of salt tolerance has usually been met, but not always. Studying the intraspeci®c variation in three provenances of E. camaldulensis, Sands (1981) found greater salt tolerance and survival in seedlings from more saline sites. In a glasshouse study, Van der Moezel and Bell (1987b) found highest salt tolerance of Melaleuca cymbifolia and E. halophila from provenances collected from areas close to the edge of salt lakes in the mallee region 50 km north of Esperance, W. Australia Similarly, germination of seed from Melaleuca thyoides from plants growing on saline land (ECˆ2.6 mSmÿ1) in this area was less depressed by salinity than seeds from plants from non-saline habitats (ECˆ0.2 mSmÿ1) (Van der Moezel and Bell, 1987a). The ®ndings of Fox et al. (1990) suggest that E. camaldulensis from ¯ood plain sites may be more salt tolerant than those from creek lines. However, exclusion of non salt-tolerant species or provenances may preclude identi®cation of valuable genetic material. Van der Moezel et al. (1989) found the highest intraspeci®c variation in salt tolerance in Casuarina

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species that were considered to have low salt tolerance. Clearly this high variability could be useful in breeding programs. Clemens et al. (1983) found similar levels of salt tolerance in glasshouse trials of C. cunninghamiana, a species that grows naturally around freshwater streams, and C. glauca, which is found in saline habitats. The salt tolerance of Acacia redolens and A. patens provenances did not match up with their origin from saline and non-saline habitats (Craig et al., 1990). Allen et al. (1994a) reported that, when tested at high salinity, seedlings of baldcypress (Taxodium distichum) collected from trees naturally inundated with saline water (0.4 to 15.3 glÿ1 NaCl) showed greater total biomass, leaf area, and tolerance index values than families from trees 80 km away, inundated with freshwater. However, at lower salinity levels, seedlings from freshwater sources grew better (Pezeshki et al., 1995). Thus there is clear evidence that when selecting material to screen for salt tolerance the bulk of genotypes should be from salt tolerant species growing in saline areas, but inclusion of some species or provenances not known to be salt tolerant is justi®ed. 5. Choice of screening in the glasshouse or in the field 5.1. Field In the ®eld there are ¯uctuations of salinity both seasonally and spatially. There is the problem and cost of hydrological evaluation and extensive soil sampling of an area. Variation in salinity occurs due to rainfall, changes in ground water depth and salinity, dykes, surface and basement rock topography, soil type, composition, fertility and structure. For example, in the salt affected areas of the wheat belt of Western Australia, there is often a duplex soil. Davidson et al. (1991) demonstrated a strong positive relationship between Atriplex productivity and increasing depth of sand over clay in salt-affected duplex soils in Western Australia. One might reasonably expect a similar response from tree species. Because of these factors, and because roots of some plants may escape salinity by capturing pockets of fresh water or opportunistically using seasonal input of fresh water, evaluating lines in the ®eld is very

5

dif®cult. The high environmental variation in salinity usually exceeds the genetic variation (Subbarao and Johansen, 1994). For many species, it is now possible to use clonal lines for ®eld-testing and replicate the same genotype over the area. This may reduce the problem of variation to some extent. It has been suggested that one solution to the problem of variable soil salinities in drier areas is saline irrigation (Ra®q et al., 1994). Hamlet and Morris (1996) have applied this but in many circumstances the cost may be prohibitive, and for long term ®eld trials there will be the problem of salt build up in the soil. In many salt affected areas, a raised water table is the main reason for salinity. Many experimental ®eld sites will be on a slope and the gradient of waterlogging imposes constraints on experimental design. Clearly it is important to screen for salt and waterlogging tolerance together, as the degree of salt tolerance and the relative salt tolerance of different lines can change depending on soil aeration (Marcar, 1993; Bell et al., 1994). Saline waterlogging results in a decreased ability to exclude Na‡ and selectivity of K‡ over Na‡ (Kriedemann and Sand, 1984; Barrett-Lennard, 1986). Craig et al. (1990) reported signi®cant increases in mortality of Acacia plants when combined treatments of salinity and waterlogging were applied. They found the two species, A. aff. lineolata and A. mutabilis subsp. stipulifera, to be highly tolerant to combined salt and waterlogging treatments. Conner (1994) also reported the combined detrimental effect of salinity and waterlogging on baldcypress seedlings. Van der Moezel et al. (1991) found that those Eucalyptus and Melaleuca species with highest tolerance to non-saline waterlogging showed more tolerance to saline waterlogged conditions. In eucalypts, the detrimental effect of waterlogging alone was greater than of low to moderate levels of salinity alone. However, the combination of salinity and waterlogging depressed survival of most species to below that of waterlogging alone. Amongst 40 eucalypt species, the relative growth of 34 in saline waterlogging was below that in waterlogged conditions; it was equal in ®ve species and better in only one provenance of a mallee form of E. salicola. One strategy for survival in waterlogged soil is the production of adventitious aerenchymatous roots (Barrett-Lennard, 1986; Marcar, 1993) or aerenchyma in the stem (Blake and Reid, 1981). E. camaldulensis

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and Casuarina obesa have the ability to produce aerenchymatous roots under conditions of freshwater ¯ooding, but this ability may be lost as salinity levels are increased (Van der Moezel et al., 1988). The presence of such roots is rarely scored, as by the end of a saline waterlogging trial in the glasshouse the plants are dead and dying and the pots a mass of algae and bacteria. Uptake of ground water by plant roots may increase the salinity of the ground water or the soil around the roots due to exclusion of salt or the ability of some species to sequester salt in the roots which protect the leaf tissue from toxic levels of ions. The increase salinity in the root zone can be deleterious to plant growth, but in many situations it is compensated by discharge of ground water into streams and leaching down of the salt front during the wet season. At present, there are regrettably few data on the partitioning by plants of water uptake between surface and ground water, and on ground water and salinity changes under tree plantations. However, it is an area of active research, as is the construction and validation of models of salt changes in the soil as a result of tree planting (Silberstein et al., 1997). Without periodic monitoring of the prevailing soil and water salinities it is not possible to know the conditions under which trees in a ®eld trial are growing (or dying). Such data are expensive to obtain and are usually only given for conditions that prevailed at the beginning of a ®eld trial. In all salinity experiments, it is desirable to have a non-saline control treatment, to determine the inherent variation and provide a relative basis for the plant's growth and development (Subbarao and Johansen, 1994). In ®eld conditions, it is usually dif®cult to ®nd an area that can be allocated to screening of control plants. It is perhaps impossible to hope to ®nd control areas that are waterlogged but not saline, but few ®eld trials even include control trees in the same environment in areas neither saline nor waterlogged. Exceptions are the trials reported by Pepper and Craig (1986) and Biddiscombe et al. (1985) both of which included an upslope, less saline plot for comparison with the saline plots, and the irrigated trial of Hamlet and Morris (1996) which included a comparison of plants irrigated with water at 0.2 and 10 dSmÿ1 salt. Evaluation of salt tolerant trees in control and saline areas would be a useful way of ranking lines, but it has

mainly been applied in glasshouse studies and horticultural woody species (Maas and Hoffman, 1977). One advantage of a ®eld trial is that the experiment provides early information on other important factors such as suitability of a provenance to the climatic conditions and susceptibility to prevalent insects and diseases. However data from the ®rst few years indicates only initial survival, not long term tolerance. There are many reports of salt tolerance assessed after two or less years growth in the ®eld. These are of limited value as the few long term trials that have been reported often reveal that some species grow well for 5±8 years then die (e.g. Donaldson et al., 1983). Other problems associated with ®eld trials include unpredictable circumstances such as strong winds, bush ®res, extreme temperatures, frosts, damage from insects and other animals and ¯ood. Trials which are established with the best of intentions are not remeasured when mature due to changes in staff, loss of paper records or markers in the ®eld. It is not hard to appreciate why screening for salt tolerance is done mainly in the glasshouse rather than the ®eld. 5.2. Glasshouse The plethora of dif®culties associated with screening plants in the ®eld makes glasshouse screening appear most attractive. Large numbers of seedlings can be grown in a small area, and conditions of water, nutrient and temperature can be controlled. Saline ®eld sites are often distant from research laboratories so glasshouse work allows savings on travel costs. To simulate the ®eld conditions in the glasshouse, decisions have to be made about medium, the type of salt to use, the regime of increasing salt levels and the imposition of waterlogging. In most glasshouse experiments, screening for salt tolerance has been carried out by adding NaCl to increase the salt level of the medium. This is valid as in Australia, NaCl dominates other salts in the root zone of salt affected plants (Noble and Rogers, 1994). In America sulfates and selenium salts may be important. Compounds such as Na2SO4, K2SO4, MgCl2, MgSO4 and KCl have been included in some glasshouse experiments (Subbarao and Johansen, 1994) (Tables 1 and 2). In glasshouse experiments whether to impose sudden or gradual increases in the level of salt is a factor

Table 1 A selection of papers showing the parameters used in screening salt tolerance of trees in the glasshouse Age of plant

Mediuma

Maximum salt levelb

Duration of trial

Parameters assessed

Ref.

Eucalyptus (6 spp.) and Melaleuca (6 spp.)

3.5-month-old seedlings

Soil C and S

15 weeks

Survival and height

Van der Moezel and Bell, 1987b

Eucalyptus (6 spp.) and Casuarina (1 spp.) Eucalyptus (19 spp.) and Melaleuca (19 spp.)

4.5-month-old seedlings 4.5-month-old seedlings

Soil C,S,W and SW Soil C,S,W and SW

11 weeks

Van der Moezel et al., 1988 Van der Moezel et al., 1989

5-week-old seedlings 6-week-old seedlings 6±12-month old plants

Solution culture S Sand S

5 weeks for Eucalyptus, 11 weeks for Melaleuca 5 weeks

Survival, height, Na‡, Clÿ in leaves Tolerance indexˆsurvival %  relative growth %

Eucalyptus (51 spp.)

Gradual increase of 15:1 NaCl:CaCl2 to 72 (Melaleuca) and 80 mScmÿ1 (Eucalyptus) Gradual increase of 10:2:1 NaCl:MgSO4:CaCl2 to 42 mScmÿ1 Gradual increase of 10:2:1 NaCl:MgSO4:CaCl2 to 35 (Eucalyptus ) and 63 mScmÿ1 (Melaleuca) Gradual increase of NaCl to 400 mM 200 mM NaCl

LD50

Blake, 1981

2 months

Height, leaf size and number

Soil

Up to 950 mM

5 weeks

Survival

Sun and Dickinson, 1993 Morris et al., 1994

3-month-old plants 4±5-month-old plants 2-month-old seedlings

Sand S

400 mM NaCl

3 months

Sand C,S,W and SW Soil C and S

Gradual increase of NaCl to 150 (exp 1) and 100 mM (exp 2) Gradual increase of 65:18:8.5:8.5 NaCl, Na2SO4, CaCl2 and MgSO4 to 1250 mM Gradual increase of 16:3:1 NaCl:MgSO4:CaCl2 to 1200 mM for S and 500 mM for SW To 400 mM NaCl (germination experiment) to 150 mM NaCl (plants) Gradual increase Na:Mg:Ca 10:2:1 to 56 mScmÿ1 Gradual increase of NaCl to 650 mM

28 days (exp. 1) 25 days (exp. 2) 14 weeks

Dry weight, Na‡ and Clÿ in leaves, stems and roots Height, fresh and dry wt, Na‡ and Clÿ in leaves, water relations Height, LD50

Eucalyptus (16 spp.) and other genera Eucalyptus (14 spp.), Acacia (2 spp.), Casuarina (2 spp.), Melaleuca (3 spp.) and 3 other genera Eucalyptus (1 spp.) Eucalyptus (4 spp.) Acacia (27 spp.) Acacia (9 spp.)

3-month-old seedlings

Sand C,S,W and SW

Casuarina (11 spp.)

germination and 10-month-old plants 4-month-old plants 4-month-old plants

Sand S

Casuarina (5 spp.) Casuarina (9 spp.)

Sand C,S,W and SW Solution culture S

Sands, 1981 Marcar, 1993 Aswathappa et al., 1987

12 weeks for S and 7 weeks for SW

Survival, height, DW, Na‡ in phyllodes

Craig et al., 1990

21 days

Growth; Na‡ Clÿ and K‡ in shoot and root

Clemens et al., 1983

12 weeks

Survival, relative growth

21 weeks

Survival, height, fresh and dry weight

Van der Moezel et al., 1989 El-Lakany and Luard, 1982

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Species

a The conditions of the media were C control- free draining soil or aerated solution culture; S free draining pots watered with saline solutions, or aerated saline liquid cultures; W fresh waterlogging; SW saline waterlogging. b electrical conductivity measurements can be approximated to NaCl concentrations as follows (1 dSmÿ1ˆ1 mScmÿ1  11 mM NaCl).

7

8

Table 2 A selection of papers showing the parameters used in screening salt tolerance of trees in field experiments Species

Salt level ÿ1

Duration of trial

Parameters

Ref.

5 salinity classes from 0.75 to >1.75 mScm

18 months

Height and survival

Dunn et al., 1994

3 salinity classes <0.6 to >1.1 mScmÿ1

3 and 24 months

Soil salinity from 1.6 to 46.7 mScmÿ1

8±10 years

Survival, height, crown features Survival and growth

Eucalyptus (22 spp.), Casuarina (1 spp.) and 6 other genera

3 rainfall zones, max. Cl conc. of 2000±5500 mglÿ1

15 months 5, 7 and 15 years

Survival, height, leaf area and crown volume

Eucalyptus (12 spp.), Casuarina (1 spp.), Acacia ( 2 spp.), Melaleuca (2 spp.) and 3 other genera

Irrigation with water at 2±13.3 mScmÿ1, groundwater containing 25000±35000 ppm total dissolved salts (approx. equiv. 430±600 mM NaCl) 4 locations EC range (7±17), (9±48), (17±28), (6±11) mSmÿ1. Irrigation with water of 0.2±5 mScmÿ1 and in one location 10 mScmÿ1 5±40 mScmÿ1 (0±30 cm) max of 19 mScmÿ1 (>30 cm) control plot 0.1±3.6 mScmÿ1 (0±30 cm) max of 1.7 mScmÿ1 (>30 cm) depth EC 7±35 mScmÿ1

3 and 10 years

Survival, height, foliar Clÿ, weighted survival index

Sun and Dickinson, 1995a,b Donaldson et al., 1983 Biddiscombe et al., 1981, 1985; Greenwood et al., 1994, 1995 Morris, 1984; Morris et al., 1994

18±24 months

Height, diameter, EC50

Hamlet and Morris, 1996

8 years

Survival, height, vigour

Pepper and Craig, 1986

6±8 years

Survival and growth

Singh et al., 1994

0.5±4.6 mScmÿ1

16 months

Survival, height

7 sites in SE Queensland, up to >20 dSmÿ1 (Ecse) 0.3 to 2.9% total soluble salts (approx. equiv. 50±500 mM NaCl)

2±9 years

Survival, height (summary data given) Survival, height and diameter

Hussain and Gul, 1991 House et al., 1998

Eucalyptus (4 spp.) Eucalyptus (12 spp.)

Eucalyptus (2 spp.), Acacia (5 spp.), Casuarina (4 spp.) and 19 other genera Eucalypyus (4 spp.), Acacia (12 spp.), Casuarina (3 spp.) and other genera Eucalyptus (14 spp.), Acacia (12 spp.), Casuarina (2 spp.), Melaleuca (6 spp.) and other genera Eucalyptus (4 spp.), Casuarina (4 spp.), Acacia (6 spp.), Melaleuca (4 spp.) and other genera

3 years

Hafeez, 1993

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Eucalyptus (8 spp.), Casuarina (2 spp.), Melaleuca (1 spp.) and 1 other genus Eucalyptus (4 spp.), Casuarina (4 spp.), Acacia (2 spp.), Melaleuca (4 spp.) Eucalyptus (55 spp.) and 33 other genera

S.R. Niknam, J. McComb / Forest Ecology and Management 139 (2000) 1±19

to be considered. In the ®eld the plants are likely to be exposed to gradually increasing salinity levels as the dry season progresses so the usual decision is to expose the plants to small (around 50 mM NaCl per week) stepwise increments in salt in the glasshouse. It is considered that exposing plants to sudden high concentration of salt may not only be arti®cial, but also may adversely affect or mask the initiation of adaptive responses. Screening for salt tolerance has been carried out in a number of media including nutrient solutions, soil and washed sand to which nutrient solution is added. If free-draining pots are irrigated with saline solutions it is possible that as soil moisture changes, plants will experience higher levels of salinity around their roots than is provided in the watering solutions. Some ¯uctuations will occur even if care is taken to thoroughly ¯ush pots each day (Marcar, 1993). Screening of plants for combined salt and waterlogging stress in the glasshouse has mostly been conducted in soil medium. This mimics some ®eld condition more closely than any other method especially when factors such as toxicity of reduced ions and redox potential of soil are considered. However it is rare for experiments to include more than one soil type and soil structure is destroyed in pot trials. Accumulation of plant hormones such as ethylene, which play an important role in responses of plants to waterlogging, may also occur in ¯ooded soil. In stirred nutrient solution with high levels of convection, accumulation of plant hormones may be quite different to the situation in soil. However, one major advantage of using nutrient solutions instead of soil medium is the possibility of close observations of root growth and damage. The major drawback to screening in the glasshouse is that only juvenile plants can be used. Finally the glasshouse environment does not test the very factors that may cause plants to die in ®eld trials, lack of ability to withstand hot drying winds, failure to root at depth, or wind throw from shallow rooting. 6. Factors to consider when screening juvenile plants for salt tolerance The ideal screening procedure involves exposing experimental plants to saline conditions throughout their entire life cycle. This has been successfully

9

applied to seed-yielding annual agricultural crops such as barley and rice (Epstein and Norlyn, 1977; Subbarao and Johansen, 1994). Even with annuals, screening over the entire life cycle is unusual and screening for just a few weeks is commonly used to evaluate the level of salt tolerance for a species or cultivar. Initially one must choose the age of the seedling when it is appropriate to impose the salt treatments. Direct seeding into saline soil is not recommended (Bell, 1999) and screening of seeds for germination in saline solutions has little practical application. It is usual for germination even of halophytes to be depressed at all levels of salt (Van der Moezel and Bell, 1987a). Few species of Casuarina, Eucalyptus and Melaleuca germinate at 200 mM NaCl (Sands, 1981; Clemens et al., 1983; Van der Moezel and Bell, 1987a). In addition, there may be no correlation between tolerance at germination and at later stages of seedling growth. For example, Allocasuarina torulosa which showed high salt tolerance at germination was one of the less tolerant species when 4-month old plants were screened (Clemens et al., 1983) and in eucalypts no correlation was found between sensitivity to salt at germination and at 4 months old (PearcePinto et al., 1990). Experiments rarely use very young seedlings. While seedlings as young as 3±6 weeks old have been used, it is more common to use plants 3±6 months old (Tables 1 and 2). The rationale is that plants will be of this age before they are planted in the ®eld. In glasshouse screening of trees, it is only possible to expose plants to salt for a short period during their juvenile phase of growth. Knowledge of the differences between the juvenile and mature growth phases raises concern about whether we can be con®dent that the salt tolerance of juvenile woody plants will correlate with the salt tolerance of mature trees. There are differences between juvenile and mature trees at the morphological, physiological, biochemical, histological and ultrastructural levels. There are variations in the relative proportion of each organ as a percentage of the total biomass, and branching pattern, leaf shape, type of bark, and stem spininess may differ in juvenile and mature trees. Physiological changes in maturity include the ability to ¯ower, reduced ability of cuttings to produce roots, and differences in organogenesis and other traits in tissue culture (Bonga,

10

S.R. Niknam, J. McComb / Forest Ecology and Management 139 (2000) 1±19

1982). Biochemical differences include the synthesis of new compounds in heartwood (Hillis, 1987), and at the histological level there are changes in shape, proportions and sizes of xylem elements and of cells at the shoot apex. There are even differences at the sub-cellular level, as cells from mature trees are observed to have more polyribosomes and a higher level of methylation of DNA (Bonga, 1982). All of these changes are recorded on above ground organs, which is hardly surprising in view of the inaccessibility of roots. A mature tree has a diversity of root types. They include long-lived deep sinker roots and short lived, highly branched, often mycorrhizal surface roots. Deep roots, which are dif®cult to study, are the types most likely to encounter salinity. Whether or not the apices of these roots have undergone maturity changes similar to those seen in a shoot apex is not known. There is some evidence that surface roots from mature and juvenile plants may differ, as for some species different strains of mycorrhizal fungi are known to infect roots of juvenile and mature plants (Mason, 1975). On the other hand a mature tree in the ®eld may explore a wide area with its roots, avoid areas of salinity and pick up pockets of relatively fresh water. Ramets from such a tree would not necessarily show salt tolerance under glasshouse testing. Thus there are reasons to suspect that exposing roots of 6-month-old plants to salinity may evoke different responses to those expressed in mature roots or seen in a large tree in the ®eld. 7. Parameters that have been used to assess salt tolerance of woody plants under either glasshouse or field conditions Growth and/or survival are most commonly scored. These characters are a culmination of the various physiological mechanisms, which are responsible for tolerance (Noble and Rogers, 1992). Also frequently measured are leaf damage and the levels of sodium and chloride in the leaves. In the ®eld the crown volume may be a more informative parameter then height. Less frequently, photosynthesis, stomatal conductance and transpiration, or relative water use are scored (Greenwood et al., 1995). Marcar (pers. com.) has suggested that the availability of mini-

calorimeters (Criddle and Hansen, 1997) may provide a fast and sensitive tool to measure response to salt. The salt concentration for LD50 has been used by Blake (1981), and the soil salt level at which growth is reduced to 50% of control levels of growth (EC50) is a useful measure when control values are available (Hamlet and Morris, 1996). The validity of selection criteria may also vary with the degree of salinity and the application for which salt tolerant trees are required (Craig et al., 1990). According to Epstein et al. (1980), at low to moderate salinity levels, salt exclusion is the main adaptive strategy, and this is re¯ected in growth and yield. At high salinities, ion toxicity is the primary cause of plant death so survival is the main criterion (Levitt, 1980). The experimenter is thus faced with a choice Ð to hold the salinity at a moderate level and assess the ability of the plant to exclude Na‡ and Clÿ ions, or to increase the salinity to higher levels and select plants which better tolerate the ion concentrations once exclusion mechanisms have broken down (and risk killing the plant). The mechanisms giving optimal performance under moderate and high salinities may be different, but selection protocols rarely consider this during the selection process, or when matching selected lines to ®eld conditions. Another problem is how to interdigitate the different scores that are obtained for survival, relative growth, and the highest salinity tolerated by individuals within a provenance. In order to give an overall quantitative score, Van der Moezel et al. (1991) utilised a `tolerance index' which is the multiple of survival (%) and mean relative growth (%). Pepper and Craig (1986) derived a `health and vigour index' and a `survival index' from comparisons between control and saline plots in the ®eld, and this concept could also be used for plants in glasshouse trials. Morris et al. (1994) devised a `weighted survival index' which was the summation of the survival of the trees in each of the ®ve salinity classes found over their experimental site. Maas (1993) has suggested using the threshold value of salinity above which yield is depressed, as well as the slope of the regression of relative growth against soil salinity. For some herbaceous plants the adaptive physiology for salt tolerance includes a low growth rate which is relatively little affected by salinity. Such species show up well when experiments are assessed on the basis of

S.R. Niknam, J. McComb / Forest Ecology and Management 139 (2000) 1±19

relative growth rate. However, their actual productivity at a particular level of salt may be considerably less than a more salt sensitive accession whose growth, although dramatically reduced by the presence of salt, is still greater than that of the slow-growing, tolerant line. Also as the objective of planting trees in saline areas is frequently to lower the water table, the absolute volume of the crown and water loss are more important then relative depression of growth rates or crown volumes; i.e. a species with small biomass, which is little affected by salt, may not be as valuable as a larger species which has a marked reduction of growth in saline areas. 8. Correlations between salt tolerance at the juvenile stage and at maturity There is little information on this issue (Allen et al., 1994b; Marcar et al., 1995). Amongst herbaceous plants such as lettuce, early screening for salt tolerance was reliable for assessing salt tolerance at later stages of development (Shannon et al., 1983). Noble and Rogers (1994) reached similar conclusions for temperate forage legumes. In general, agricultural crops are more salt sensitive at the seedling stage than at later stages of growth (Francois and Maas, 1994). As mentioned above, most woody species show no salt tolerance at germination, low tolerance at the seedling stage, but greater tolerance to salinity at 4± 6 months of age. One reason for higher tolerance of older plants could be a gradual adaptation of the plants to the presence of salt (Subbarao and Johansen, 1994). For most species this rule of thumb is without quantitative data. There is a tacit assumption that as trees age their salt tolerance will continue to increase so that selection at the juvenile stage will underestimate salt tolerance. This may not be justi®ed. Early growth in the ®eld may utilise relatively fresh surface water and only as the trees age must they tap into more saline ground water. The best documented ®eld trial in which a large number of species has been observed for an extended time period is in California (Donaldson et al., 1983). Even after 8±10 years of satisfactory growth some species died. After 10 years only 17 of the original 55 species were showing acceptable survival and growth. Whether this re¯ects different species having different mechanisms of tolerance at different

11

stages of maturity, or whether it is a result of changes in soil and water salinity is not known, as soil and water were not monitored. More information is clearly needed on the relative level of salt tolerance of young seedlings, juvenile plants, saplings and mature plants in the ®eld. 9. Evidence of correlation between salt tolerance as assessed in the glasshouse and in the field It is dif®cult to ®nd published reports of good experiments designed to test for correlations between salt tolerance in glasshouse trials and ®eld trials. The ideal trial would include the same lines in the glasshouse and the ®eld, and the glasshouse trial would match the ®eld site by including waterlogging if this was present. There appears to be no information of this sort in the published literature at the level of genotype, and few papers at the level of provenance. Most information is based on experiments at the species level. For the purpose of comparisons between glasshouse and ®eld results data from the genera Eucalyptus, Melaleuca, Casuarina and Acacia provide most information (Tables 1 and 2). The variability of the range of salinity between ®eld sites makes it dif®cult to compare between trials so for this review species have been grouped very broadly into those with High, Medium or Low tolerance. Some publications which provide useful general information on the performance of trees in the ®eld have been excluded from this analysis as the ®eld conditions or the parameters measured for the trees have not been given in suf®cient detail (e.g. Firman, 1968; Gill and Abrol, 1991). There are over 500 species of Eucalyptus described in the Flora of Australia (Chippendale, 1988) and around 166 have been screened for salt tolerance (Tables 1 and 2). Most species have been screened only in the glasshouse, or only in the ®eld so comparisons between glasshouse and ®eld are impossible. There is consistency in the level of salt tolerance between glasshouse and ®eld trials for 20 species (Table 3A). Most of these are tolerant but E. botryoides, E. cloeziana, E. stricklandii and E. intermedia have been assessed as sensitive to salt in both the glasshouse and ®eld. There is a number of species for which assessments in the glasshouse and ®eld are contradictory.

12

S.R. Niknam, J. McComb / Forest Ecology and Management 139 (2000) 1±19

Table 3 Comparisons between glasshouse and field testing for salt tolerance in Eucalyptus species A. Species for which the same level of salt tolerance has been recorded from glasshouse and field tests E. agrophloia Highly tolerant in glasshouse (Sun and Dickinson, 1995a) and in the field (House et al., 1998) E. botryoides Sensitive in glasshouse (Blake, 1981) and in the field (Donaldson et al., 1983; Morris et al., 1994) E. citriodora Moderately tolerant in glasshouse (Sun and Dickinson, 1993) and in the field (Gill and Abrol, 1991) E. blakelyi Tolerant in glasshouse (Blake, 1981) and in the field but poor form and vigour (Donaldson et al., 1983) E. cloeziana Sensitive in the glasshouse (Sun and Dickinson, 1995a) and in the field (House et al., 1998) E. goniantha Moderately tolerant in glasshouse (Van der Moezel and Bell, 1987b), survived 8 but not 10 years in the field (Donaldson et al., 1983) E. grandis Moderately tolerant in glasshouse (Sun and Dickinson, 1993) and the field (Dunn et al., 1994) E. grossa Highly tolerant in glasshouse (Blake, 1981) and the field (Donaldson et al., 1983) E. intermedia Sensitive in glasshouse (Sun and Dickinson, 1993) and field (Dunn et al., 1994) E. intertexta Tolerant in glasshouse (Van der Moezel et al., 1991), survived 8 but not 10 years in the field (Donaldson et al., 1983) E. largiflorens Highly tolerant in glasshouse (Blake, 1981; Morris et al., 1994) moderately to highly tolerant in the field (House et al., 1998; Morris, 1984) E. leucoxylon Moderately tolerant in glasshouse (Blake, 1981; Van der Moezel et al., 1991), moderately to highly tolerant in the field (Biddiscombe et al., 1981, 1985; Greenwood et al., 1994; Morris, 1984; Morris et al., 1994) E. loxophleba Moderately tolerant in glasshouse (Van der Moezel et al., 1991) and field (Biddiscombe et al., 1981; Pepper and Craig, 1986) E. microtheca Highly tolerant in glasshouse (Van der Moezel et al., 1991) and field (Donaldson et al., 1983) E. moluccana Highly tolerant in glasshouse (Sun and Dickinson, 1993) and field (Dunn et al., 1994) E. raveretiana Highly tolerant in glasshouse (Van der Moezel et al., 1991) and field (Dunn et al., 1994) E. sargentii Highly tolerant in glasshouse, moderately to highly tolerant in field (Greenwood et al., 1994, 1995; Sun and Dickinson, 1993; Pepper and Craig, 1986) E. sideroxylon Moderately to highly tolerant in glasshouse (Blake, 1981; Van der Moezel et al., 1991) highly tolerant in the field (House et al., 1998) E. stricklandii Sensitive in glasshouse (Blake, 1981) survived in field with poor form for 8 but not 10 years (Donaldson et al., 1983) E. tereticornis Highly tolerant in glasshouse (Blake, 1981; Marcar, 1993; Van der Moezel et al., 1991) and field (Dunn et al., 1994; Sun and Dickinson, 1995b) B. Species showing higher tolerance in the field than the glasshouse E. aggregata Sensitive in glasshouse (Blake, 1981), survived 10 years in the field but with poor form and vigour (Donaldson et al., 1983) E. albens Sensitive in glasshouse (Blake, 1981), survived 10 years in the field but with poor form and vigour (Donaldson et al., 1983) E. tetraptera Moderately tolerant in glasshouse (Blake, 1981) highly tolerant in the field (Donaldson et al., 1983) C. Species showing less tolerance in the field than the glasshouse E. brockwayi Moderately tolerant in glasshouse (Morris et al., 1994) sensitive in field (Morris et al., 1994) E. caesia Moderately tolerant in the glasshouse (Blake, 1981) sensitive in field (Donaldson et al., 1983) E. dundasii Moderately tolerant in the glasshouse (Morris et al., 1994) sensitive in field (Morris et al., 1994) E. largiflorens Highly tolerant in glasshouse (Blake, 1981; Morris et al., 1994), moderately tolerant in field (Morris et al., 1994) E. tessellaris Moderately tolerant in the glasshouse (Blake, 1981) sensitive in the field (Sun and Dickinson, 1995b)

Some eucalypt species scored as salt sensitive in the glasshouse survived for long periods in the ®eld even though form and vigour were low (Table 3B). The reverse is the case for ®ve other species scored as more tolerant in the glasshouse than in the ®eld (Table 3C). Finally there are eucalypt species for which the results are variable (Table 4). It might be reasonable to expect that as more trials of a species are done the

more likely it is that a provenance will be included that lies at the extreme of the species' salt tolerance, or that a ®eld trial will include a provenance badly matched to local conditions. However, the number of mismatches of results from the ®eld and glasshouse highlights the importance of ®eld trials, particularly for species for which there is only a single record of a glasshouse test.

S.R. Niknam, J. McComb / Forest Ecology and Management 139 (2000) 1±19

13

Table 4 Eucalyptus species for which the level of salt tolerance varies in the glasshouse and/or the fielda Eucalyptus species

Glasshouse trials

astringens camaldulensis cladocalyx globulus incrassata kondininensis lesoufii maculata occidentalis platypus robusta rudis spathulata

Ms Hs Ms M-Hs Hs Ls Ls Ls Ls

G

b

G

Hs.Hsw

Hs

G

d

G

e

f

G

Ls.Hsw

Hs

G

g

G

h

Hs.Lsw

Ms Ms.Lw

Ms

Field trials

c

Hs.Lsw Hs.Lsw Hs

Hs

Hs Hs.Lsw

Fi,j,k

F

i,j,k

M H H M

M H

l

H H

Hs.Lsw

M

Hs.Hsw Ls

H H H L

M H L

L

H

Hs.Msw Hs.Hsw

F

M H M M H H

Fd,m F H

L H L

n,g

F

o

H

p

F

L

q

F H

r

F

s

L-H

L

L

M

H M M

F

H H L L H

H H

H

a

Lˆlow tolerance, Mˆmoderate tolerance, Hˆhigh tolerance. For glasshouse trials sˆsalt, swˆsaline waterlogging, wˆwaterlogging. Blake, 1981. c Marcar, 1993. d Sun and Dickinson, 1993. e Van der Moezel and Bell, 1987b. f Van der Moezel et al., 1988. g Morris et al., 1994. h Van der Moezel et al., 1991. i Biddiscombe et al., 1981. j Biddiscombe et al., 1985. k Greenwood et al., 1994. l Donaldson et al., 1983. m Sun and Dickinson, 1995a. n Morris, 1984. o Dunn et al., 1994. p Pepper and Craig, 1986. q Hamlet and Morris, 1996. r Hafeez, 1993. s House et al., 1998. b

E. astringens was assessed as moderately tolerant in the glasshouse, and although it showed good early growth in the ®eld in Western Australia, in a Victorian ®eld trial all trees had died by Year 9. E. camaldulensis has been scored as highly tolerant in most glasshouse trials, but in one it was shown to be relatively susceptible to salt, but to tolerate waterlogging or salt waterlogging. In the ®eld, it has performed as moderately or highly tolerant to salt in most trials (refs. in Table 4 and Fox et al., 1990, Gill and Abrol, 1991; Singh et al., 1994) but in others was recorded as surviving but with poor form, or to be sensitive to salt. Morris (1995) showed very clearly the importance of matching clones to sites as in Victoria, salt tolerant E. camaldulensis

clones derived from other states grew poorly and died back after 5 years, whilst those selected from amongst local trees performed far better. E. cladocalyx was also assessed as moderately tolerant in the glasshouse and while in the ®eld in Western Australia it was highly tolerant in Victoria it was susceptible. E. globulus was reported to be highly tolerant from a glasshouse trial while in the ®eld it showed low tolerance in an irrigated ®eld trial and low to moderate tolerance in a ®eld site in Western Australia. E. incrassata displayed high tolerance to salt in a glasshouse trial as well as in the ®eld in California but in Victoria it showed low survival but good height of the survivors. For E. kondininensis, there are reports of both high

14

S.R. Niknam, J. McComb / Forest Ecology and Management 139 (2000) 1±19

and low salt tolerance in the glasshouse while in the ®eld, it showed moderate tolerance. E. lesou®i has given con¯icting results under glasshouse conditions. The results for E. maculata are similar with one report of low, and another of moderate tolerance in the glasshouse while in the ®eld in Western Australia the trees showed high tolerance. In California they grew for 8 years but died by Year 10. E. occidentalis has one report of low tolerance in the glasshouse which is in con¯ict with other glasshouse and ®eld reports of high tolerance. A report of low tolerance of E. platypus for salt in the glasshouse is not matched by moderate to high tolerance in the ®eld. For E. robusta there are reports of moderate to high tolerance in the glasshouse while the species in the ®eld was susceptible in two studies and at best moderately tolerant in others (growing for 8 years before dying by Year 10). In the one report of high tolerance of E. robusta in the ®eld, the plants were only 2 years old. In E. rudis reports of salt tolerance in the glasshouse and the ®eld in California and Pakistan con¯ict with the poor performance of the species in the ®eld in Western Australia. E. spathulata is another species for which reports of tolerance to salt or saline waterlogging in the glasshouse vary, and in the ®eld it shows from low to high tolerance. Some 25 species of Melaleuca have been screened (Tables 1 and 2) and many species show higher salt tolerance than eucalypts in the glasshouse. There are few published data on the ®eld performance of different species. M. lanceolata performed well under both salinity and saline waterlogging in the glasshouse (Van der Moezel et al., 1991) and in the ®eld was amongst the better species tested (Morris, 1984; Hafeez, 1993; Morris et al., 1994). M. bracteata showed moderate tolerance in the glasshouse under salinity, but performed poorly under saline waterlogging (Van der Moezel et al., 1991). It showed good survival in ®eld trials conducted by Dunn et al. (1994), Sun and Dickinson (1995b) and House et al. (1998) and was the best of four Melaleuca species tested in Pakistan (Hafeez, 1993). M. armilaris was reported to be less tolerant in the ®eld than would be expected from glasshouse results (Morris, 1984, Morris et al., 1994). M. cajuputi was amongst the least tolerant melaleucas screened in the glasshouse by Van der Moezel et al. (1991) but, based on 2-year old plants, was scored as moderately tolerant in the ®eld by

House et al. (1998). M. leucadendra was amongst the least tolerant species screened by Van der Moezel et al. (1991) Ð plants were almost totally killed under saline conditions and completely killed under saline waterlogging. Similarly it did not survive in the ®eld in Pakistan (Hafeez, 1993). In contrast, in conditions of high salinity in the ®eld in Queensland it showed 75% survival and only a 25% reduction in growth compared with growth at low salt (Sun and Dickinson, 1995b; House et al., 1998). Thus the few comparisons between glasshouse and ®eld trials for Melaleuca species rarely show consistency. The results of glasshouse screening however, would indicate that there is a large number of potentially salt tolerant species that remain to be ®eld-tested. At least 48 species of Acacia have been screened (Tables 1 and 2), but few of these have been tested both in the ®eld and glasshouse. A. stenophylla, A. saligna and A. salicena have been shown to be highly tolerant in the glasshouse and tolerant to highly tolerant in the ®eld (Aswathappa et al., 1987; Gill and Abrol, 1991; Hussain and Gul, 1991; Hafeez, 1993; Singh et al., 1994; Morris et al., 1994; Sun and Dickinson, 1995b, House et al., 1998), with some variation between provenances shown by Sun and Dickinson (1995b). A. auriculiformis was highly tolerant in the glasshouse (Aswathappa et al., 1987) while in the ®eld it was reported to be tolerant in most trials (Hafeez, 1993; Sun and Dickinson, 1995b) but moderately susceptible in others (Singh et al., 1994; House et al., 1998). A. aulococarpa was less tolerant than A. auriculiformis in a glasshouse trial (Aswathappa et al., 1987) and also showed less survival and growth than this species in the ®eld (Sun and Dickinson, 1995b). A. ampliceps showed high tolerance in glasshouse trials (Aswathappa et al., 1987; Craig et al., 1990) and also in one ®eld trial in Pakistan (Hussain and Gul, 1991) while in another ®eld trial in Pakistan it was amongst the worst species with only 15% survival (Hafeez, 1993). A. victoriae showed moderate tolerance in the glasshouse (Aswathappa et al., 1987) but poor survival and growth in the ®eld (Hussain and Gul, 1991; Hafeez, 1993). A. ¯oribunda and A. pendulata are also species less tolerant in the ®eld than would have been predicted from glasshouse results (Morris, 1982; Aswathappa et al., 1987; Morris et al., 1994). Thus for Acacia of the few species for which there are comparative data, four show good correlation between

S.R. Niknam, J. McComb / Forest Ecology and Management 139 (2000) 1±19

glasshouse and ®eld screening and ®ve species are less tolerant in the ®eld than would have been expected from the glasshouse results or show variable ®eld results. Further, results from the glasshouse suggest that for some species there is no correlation between resistance to salt and to salt waterlogging and thus extrapolation from glasshouse trials done under aerated conditions to waterlogged ®eld sites is not possible. For example in a glasshouse trial A. cyclops and A. brumalis had no deaths in salt (up to 1200 mM) but showed 100% deaths in salt waterlogging at 500 mM salt (Craig et al., 1990). Twelve species of Casuarina and Allocasuarina have been screened (Tables 1 and 2) with most salt tolerant species being identi®ed in Casuarina except for Allocasuarina littoralis (Clemens et al., 1983). The salinities tolerated by these species are higher than for eucalypts and comparable with the levels tolerated by Melaleuca species. There is consistency in reports from glasshouse and ®eld for the high tolerance of C. cunninghamiana, C. glauca, C. obesa and C. equisetifolia (Biddiscombe et al., 1981; El-Lakany and Luard, 1982; Clemens et al., 1983; Van der Moezel et al., 1988; Hafeez, 1993; Dunn et al., 1994; Sun and Dickinson, 1995a,b; House et al., 1998). There is, however, some variability. The high salt tolerance of C. cristata in the ®eld (equivalent to C. cunninghamiana) (Morris et al., 1994; Sun and Dickinson, 1995b) would not have been predicted as in the glasshouse, it was ranked only as moderately tolerant (El-Lakany and Luard, 1982) or moderately sensitive (Clemens et al., 1983). Although C. cunninghamiana and C. glauca showed similar levels of tolerance in the ®eld trial reported by Sun and Dickinson (1995b); Dunn et al. (1994) reported the two species to be similar (100% survival) at intermediate salt levels but at high salt all the C. glauca plants died where 71% of C. cunninghamiana survived. The only work that has attempted to match up glasshouse and ®eld performance of the same lines of Eucalyptus, Acacia, Melaleuca and Casuarina is found in an unpublished report by Morris et al. (1994). They assessed several species in free-draining pots in the glasshouse and under saline irrigation in Kerang, Victoria. Species rankings using four different parameters in the ®eld were signi®cantly different from one another and from the glasshouse rankings. When all four ®eld rankings were combined the match

15

between ®eld and glasshouse was reasonable for 10 of the 13 species. On a species level, researchers tend to accept that a glasshouse trial has been validated when there is a good correlation for salinity tolerance in glasshouse and in ®eld. When there is not a good correlation, researchers tend to explain this away as a result of intraspeci®c variation for tolerance, testing of different provenances in the ®eld and the glasshouse, inappropriate salinity levels, or a mismatch of provenances to environmental conditions. Future studies clearly need to look more critically at all the other factors that differ between the plant material being tested and the environmental conditions that prevail in the glasshouse and the ®eld to decide the relative effort and value to place on glasshouse and ®eld screening. 10. Conclusions The ideal experiment has yet to be designed for assessing the validity of a glasshouse screening of juvenile trees in relation to their subsequent performance in the ®eld. We suggest that clonal material is highly desirable. In the glasshouse trial, some clonal replicates should be tested for their ability to exclude salt at moderate salt levels, and others used to determine survival under high levels of salinity. A comparison with the growth of the same genotypes under control conditions would allow assessment of the reduction in productivity. Depending on whether material is intended for waterlogged or free draining areas, the glasshouse trial should match these conditions. At the conclusion of the glasshouse screening, lines should be ranked from most to least resistant using data on survival and growth. Clones of all lines should then be planted in the ®eld under different levels of soil salinity in a well-replicated design to overcome the mosaic of ®eld conditions that usually exists. Inclusion of a control plot under non-saline conditions is highly desirable. To test lines under different salinities in the ®eld it may be possible to use irrigation water with different levels of salinity for different trial areas. This will be most effective in areas of low rainfall and would not be appropriate in areas of high water table. Several different parameters should be

16

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used to assess the plants in the ®eld; survival, height and maximum salinity tolerated appear to be a minimum. Foliar chloride and sodium levels, and assessment of canopy size and water loss are the next most important. At present a trial that conforms to these requirements is being established near Deniliquin (New South Wales), using over 550 clonal lines from 10 control pollinated families of Eucalyptus camaldulensisglobulus and E. camaldulensisgrandis (Dale pers. com.). Five ramets per genotype will be tested under glasshouse conditions and another ®ve ramets per genotype in each of two ®eld irrigation treatments; fresh (control), and low to moderate salinity (2± 8 dSmÿ1). This will allow comparisons to be made between glasshouse and ®eld, and juvenile and mature plants. It would seem desirable for experimenters in either ®eld or glasshouse to include one or more common `standard' lines. This would facilitate comparisons between successive experiments and between different ®eld locations although there could be interactions between the standard line and ®eld conditions. Possibly lines to include would be E. camaldulensis (provenances from Lake Albacutya, Victoria, and Silverton, New South Wales) and E. occidentalis (provenances from Grass Patch and Borden, both in Western Australia). Seed is available from the Australian Tree Seed CSIRO Canberra, ACT, Australia. Assessment of survival and growth of trees in the ®eld has to continue for many years. Until comparisons of this nature have been carried out the superiority of plants selected for salt tolerance as seedlings under glasshouse conditions remains uncertain for many species. The de®nitive experiments remain to be done. They will be costly and long term. Acknowledgements Preparation of this review was supported by the XylonovA syndicate. References Able, G.H., 1969. Inheritance of the capacity for chloride inclusion and chloride exclusion by soybeans. Crop Sci. 9, 697±698.

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