Tree Physiology 30, 1072–1082
doi:10.1093/treephys/tpq061
INVITED REVIEW: PART OF AN INVITED ISSUE ON TREE NUTRITION
Woody legumes: a (re)view from the South
MARK A. ADAMS,1,2 JUDY SIMON3 and SEBASTIAN PFAUTSCH1
1
Faculty of Agriculture, Food and Natural Resources, University of Sydney, Level 4, Biomedical Building, Australian Technology Park, Eveleigh,
NSW 2015, Australia
2
Corresponding author ([email protected])
3
Institute of Forest Botany and Tree Physiology, Chair of Tree Physiology, University of Freiburg, Georges-Koehler-Allee 53/54, 79110 Freiburg,
Germany
Received March 31, 2010; accepted June 8, 2010; published online July 8, 2010
Summary This review is focused on woody legumes from
the southern continents. We highlight that the evolution of the
Caesalpinioideae and Mimosoideae with old soils, with variable supplies of water and also with fire has produced a suite
of advantageous physiological characteristics. These include
good potential for nitrogen fixation and mechanisms for acquiring P. The latter includes the ability to form cluster roots
and produce extracellular phosphatase enzymes. Further,
many of the species in these subfamilies are known to
synthesize in significant amounts osmotically compatible solutes, such as pinitol and other cyclitols/polyols, that help
them cope with even severe drought conditions. In many
cases, these species regenerate prolifically after fire from
seed. Such species and their beneficial characters can now
be better exploited to help sequester carbon, provide key nutrients such as nitrogen and phosphorus for companion crops
and other plants and provide feedstocks for a range of industries, including energy industries.
Keywords: Acacia, drought, nitrogen, old soils, phosphorus,
water.
Introduction
Almost all of the progress in understanding the process of biological nitrogen fixation/diazotrophy has been stimulated by
the importance of nitrogen in agriculture. Fisher and Newton
(2004), as well as Newton (2004), provide significant insights
into the history of the subject as part of a multi-volume treatise.
They point out that, while beneficial effects of legumes in rotations with cereals were known since Greek and Roman
times, it took till 1888 for Hellriegel and Wilfarth (1888) to
build on the work of Boussingault and Lawes and Gilbert
(and others) and finally provide proof that nitrogen fixation
by legumes was due to an association with bacteria. In a recent
review of the phylogeny of legumes, Wojciechowski et al.
(2004) noted that we now recognize more than 19,400 species
worldwide. They also stated that this places legumes ‘second
only to Poaceae in agricultural and economic importance’.
Such a view is strongly justified by their widespread adoption
in agriculture: ‘Grain and forage legumes are grown on some
180 million Ha, or 12% to 15% of the Earth's arable surface’
(Graham and Vance 2003).
By comparison with the obvious impetus provided by the
importance of legumes in agriculture and research developments in the 19th century, research on woody legumes languished till well into the latter half of the 20th century.
Indeed, it is arguable that research into woody legumes only
gained any significant momentum once there were large areas
of land and soil that had been degraded by poor agricultural
practices and further areas of land that had been cleared but
ultimately proved unsuitable for agriculture. It took till well
into the 1970s and even the 1980s (e.g., Allen and Allen
1981) for there to be a significant body of research into woody
legumes. By then, we knew that diazotrophy was an energetically expensive process, requiring that N-fixing symbioses
had available to them significant supplies of phosphorus. Forestry played a role in the development of interest in woody legumes since, obviously, harvesting and fires remove nitrogen,
and such losses must be considered in relation to inputs from
nitrogen fixation—the balance between inputs and outputs of
nitrogen being perhaps one of the keys to assessing the sustainability of management (e.g., Likens et al. 1970, Johnson et al.
1982, Dyck et al. 1994).
The southern continents have played a leading role in the
development of knowledge of woody legumes. In Africa and
South America, a focus on food production and the advent of
agroforestry led to many screening studies of the suitability
of tree legumes, and their potential contributions of N, to
companion crop plants. These studies are summarized in
works by modern ‘fathers’ of agroforestry—P.K. Nair (Nair
et al. 1984, Nair 1993) and a decade later by Pedro Sanchez
(Sanchez 1995). That work continues (e.g., Aronson et al.
1992, 2002, Arredondo et al. 1998, Cervantes et al. 1998),
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WOODY LEGUMES: A (RE)VIEW FROM THE SOUTH
while much early work was captured and refined through the
creation of the International Centre for Research in Agroforestry, now the World Agroforestry Centre, and has been published under that banner (e.g., Palm 1995, Shepherd et al.
1995).
In Australia, the many and long-standing observations of
how well legumes colonize disturbed land and how quickly
they re-establish after fire led to the recognition of their importance to the N balance of forests: ‘The contribution of leguminous species is identified as critical to this balance and
demands further study’ (Baker and Attiwill 1981). However,
it was probably the issue of large areas of land requiring restoration and rehabilitation, which has been particularly acute
for large areas of old soils in the tropics and in the South more
generally, that led to a southern focus on woody legumes.
This review is focused on the woody legumes that originate
in the southern continents. The comparatively good knowledge and moderately frequent review of the legumes used
in agriculture, especially those that grow in the northern
hemisphere or wet tropics, are drawn upon for comparison,
as are some of the ecological and physiological characteristics
of woody legumes that now grow and prosper in the North or
the tropics as invasive plants. We have deliberately taken the
view that phylogeny and biogeography provide crucial contexts for the understanding of rates of N fixation, tolerance
of drought and ability to acquire phosphorus—physiological
features of this fascinating group of plants. We have not dealt
in detail with the plant–bacteria association of N-fixing symbioses in woody legumes. That subject is covered by others, in
particular by Janet Sprent and co-workers (e.g., Sprent 1995,
2003, 2005, 2007, Sprent and James 2007, Sprent et al. 2009)
and most emphatically in her recent book (Sprent 2009). It is
also well covered for the genus Acacia, in the recent report by
Brockwell et al. (2005). Nor have we attempted to cover the
basic physiology and biochemistry of nitrogen fixation per
se. That is very well described elsewhere in books (e.g., Postgate 1998), reviews (e.g., Colebatch et al. 2002) and collated
proceedings of the frequent conferences on the general topic of
nitrogen fixation at regional, national and international levels
(e.g., Dakora et al. 2008).
Phylogeny
Similarly to Sprent (2007), we have adopted the terminology
of Lewis et al. (2005) that divides the Leguminosae into three
subfamilies: Caesalpinioideae, Mimosoideae and Papilionoideae. Two aspects of the phylogeny of woody legumes are
worthy of comment in the above context. First is that their
phylogeny is not the same as that of nitrogen fixation among
angiosperms in general. Among the angiosperms, symbiotic
nitrogen fixation is not limited to the Leguminosae. Drawing
on recent papers by Wojciechowski et al. (2004) and Sprent
(2007), we note nitrogen-fixing symbioses have become
broadly distributed within the angiosperms, including a range
of non-leguminous woody genera such as Casuarina, Alnus
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and Myrica. Secondly, and more specifically with respect to
the Leguminosae, molecular data illustrate what is currently
regarded as the evolutionary pattern within the family—the
Caesalpinioideae evolved first, followed by the Mimosoideae
and then the Papilionoideae. As discussed by Sprent (2007),
nodulation is most common in the latter of the three subfamilies and least common in the first. Also, as discussed by
Sprent (2007), members of the Leguminosae that are native
to or flourish in the warm temperate to arctic regions are
mostly in the Papilionoideae, which also includes the great
majority of the forage and grain legumes. The ‘more southern’ woody legumes are mostly Mimosoideae and Caesalpinioideae, and these are the subfamilies that form the basis of
this review. Immediately, we can note that there is good empirical evidence for the poorer nodulation and N-fixation capacity of the Caesalpinioideae relative to the Mimosoideae, in
tropical forests at least (e.g., Ometto et al. 2006).
Biogeography
In an analysis of the distribution of legumes in terrestrial ecosystems, including analysis of their ecological significance,
Crews (1999) made a number of points including:
(i)
Legumes comprise an important component of canopy
trees in lowland mesic and wet tropical forests throughout the world.
(ii) Woody legumes have also been successful in drier tropical environments.
(iii) Legumes in late seral stages and woody legumes in general are notably absent in temperate regions.
Crews went on to cite dry tropical thorn-scrub communities
of Mexico, Africa and Australia as examples of his second
point, including members of the genus Acacia. While noting
that many of the Australian acacias are not ‘thorny’ in the sense
applied to African species, we concur with Crews' overall assessment that ‘potentially nodulating, woody legumes are
common and often dominant’ in many tropical ecosystems
on most continents. We would, from a southern perspective,
note that this is true for Africa and Australia and South America. Beyond this point, however, we must diverge a little from
Crews' view of legumes in temperate regions.
There are large areas of non-tropical Australia and Africa
where woody legumes, mainly of the genus Acacia Mill., are
far from absent in either late seral stage or in absolute terms—
they are either a major component of the overstorey or are the
dominant overstorey species (e.g., Johnson and Burrows
1993). Best examples include Mulga (Acacia aneura F. Muell.
ex Benth., dominates ∼1.5 × 106 km2 or ∼20% of Australia),
Myall (Acacia pendula A. Cunn. & G. Don) and Brigalow
(Acacia harpophylla F. Muell. ex Benth.) woodlands of inland
Australia. Altogether, acacias cover vast areas southwards
from the Tropic of Capricorn to at least as far as 35°S. While
it is true that much of this area is arid (e.g., <250 mm annual
TREE PHYSIOLOGY ONLINE at http://www.treephys.oxfordjournals.org
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ADAMS ET AL.
Region
Extent of Mediterranean
climate region (km2)
Legumes
(% of the total flora)
(1999), become dominant for short periods after fires. This is
a well-known phenomenon in much of the southern half of
Australia, for example, where Acacia spp. may germinate in
large numbers after fire and contribute strongly to the N budget
for up to a decade later (see May and Attiwill 2003). We will
return to this shortly.
California
Chile
South Africa
Australia
42,397
37,848
36,631
1,675,845
3.9–6.9
3.8
7.3–10.9
8.8–13.3
Ecophysiology—nitrogen fixation, phosphorus and
old soils
Table 1. Contribution of leguminous taxa to the floras of several
Mediterranean climate regions of the world. The proportion of Mediterranean climate regions to total state or country size is given in
parenthesis. Data adopted from Arianoutsou and Thanos 1996.
(10)
(5)
(3)
(22)
rainfall) to semi-arid (<350 mm), there are still large expanses
of Acacia-dominated land, well south of the tropics, that
receive up to 900 mm of annual rainfall and may reach almost
to the coast. There is almost as much Acacia-dominated land
in the band between 350 and 500 mm as there is between 250
and 350 mm. Johnson and Burrows (1993) list at least 18 identifiable Acacia open forests, woodlands and tall shrublands
(where one or more Acacia spp. is the canopy dominant).
A similar scenario is true also for southern, non-tropical
Africa. The following owes much to the work of Lewis et al.
(2005). Acacia spp. dominate large areas of Africa well
south of the equator (as well as to the north). For example,
Acacia nilotica L. and its numerous subspecies are found
throughout much of Africa and over a broad range of edaphic
conditions that include an altitudinal range of around 2000 m,
a rainfall range of 250–1500 mm. Together with Acacia karoo
Hayne (which copes with a narrower range of edaphic conditions), it is the dominant tree in large areas of savanna grassland in much of southern Africa. Likewise, Brachystegia
spp. together with Baikiaea ghesquiereana J. Léon. and
other members of the leguminous subfamily Caesalpinioideae, dominate some 2.4 × 106 km2 of Miombo woodlands
in Angola, Botswana, Burundi, Democratic Republic of
Congo, Malawi, Mozambique, Namibia, Tanzania, Zambia
and Zimbabwe.
Finally, in non-tropical America, the mesquites or algarobas
(Prosopis spp.) dominate large areas. As stated by Isomaki and
Ghandi (2004), algarobas are native to ‘the semi-arid savanna,
cerrados and caatingas of Brazil, at the edges of the desert on
the west coast of South America, on the lower slopes of the
Andes, and in many parts of the grasslands of Argentina, in
the pampas, and in Patagonia. Algarobas are, in vast areas,
the dominant tree species.’ They thrive in arid, semi-arid and
even sub-humid conditions. In Brazil, algarobas are a key part
of semi-arid vegetation that covers some 5 × 105 km2.
The point we make is that legumes are dominant elements
of the woody vegetation in much of Africa, Australia and
South America. A simple summary (Table 1) is taken from
Arianoutsou and Thanos (1996). To us, there seems little evidence of any absence of legumes in temperate parts of the
Southern Hemisphere, and, indeed, they may dominate in
large areas of the temperate and subtropical ‘South’. Where
legumes do not dominate, they may often, as stated by Crews
In a review of woody legumes, it is obvious that we might
begin any discussion of their ecophysiology with nitrogen
fixation. A strong framework is provided by Houlton et al.
(2008), who recently provided a major summary of global
patterns of N fixation. From their analysis, it is very clear that
N fixation is strongly temperature dependent, displaying a
highly normal temperature distribution with a maximum at
around 25 °C. This result accords with known biochemical
properties of many enzymes. A little more surprising was
their analysis that showed that, through enzyme activity, Nfixing plants are also able to increase the availability of P in soil.
Houlton et al. (2008) showed that the activity of phosphatase
enzymes in soil is up to three times greater when N-fixing plants
were present. Using a model to integrate these results into the
broader issues of growth and nutrient limitation, Houlton et al.
(2008) showed that it seems most likely that P released by phosphatase activity is of direct benefit to the N-fixing plants that
produced that activity.
From a Southern perspective, this model analysis represents a step forward from other models (e.g., Rastetter et al.
2001, Menge et al. 2009) because it explicitly considers the
problems of poor supplies of P in soils. By scientists studying
northern plants, this is one of the least well-understood aspects
of Australia and Africa in particular but also large parts of
South America. Old soils dominate Australia and Africa,
and P is often in chronically short supply. The ability of
woody legumes to acquire P is thus of paramount importance
to their role as N fixers.
Taking as a starting point the summaries presented in 1986
by Hayman and in 1989 by Alexander, a considerable number of both herbaceous and woody legumes were known then
to be mycorrhizal. Since then, the list has grown considerably, albeit still with a focus on herbaceous species used in
agriculture. Nevertheless, the beneficial effects of mycorrhizas on P availability and uptake by Acacia spp. and many
other woody legumes from the South are now well established for both tropical and temperate zones (e.g., Founoune
et al. 2002a, 2002b, 2002c, Duponnois and Plenchette 2003,
Giri et al. 2004, Duponnois et al. 2007). A considerable portion of our current knowledge of the beneficial effects of vesicular–arbuscular mycorrhizas on Acacia spp. is due to the
work of Drs Lynette Abbott and David Jasper at the University of Western Australia (Jasper et al. 1988, 1989a, 1989b,
Jasper 1994). They showed clearly that the availability/viability of vesicular–arbuscular mycorrhizas was a serious con-
TREE PHYSIOLOGY VOLUME 30, 2010
WOODY LEGUMES: A (RE)VIEW FROM THE SOUTH
1075
Figure 1. Growth of cluster roots and nodules of five woody legumes in a ‘choice’ experiment. All plants were container-grown in sand without
added N or P (but with other mineral nutrients supplied via solution), and lateral roots could grow out into each of four different regions. In two
regions, the sand was simply white quartz (WS), that had no inherent capacity to hold P and negligible endogenous P, or WS augmented with an
insoluble iron phytate (∼80 ppm P). In the other two, a yellow sand (YS) that had ∼2 ppm endogenous available P was either provided alone or
augmented with ash generated from native forest species (∼6 ppm P). Data presented are the masses of nodules and cluster roots growing on
lateral roots in each of the four regions. Data are recalculated from Adams et al. (2002).
straint to the success of Acacia spp. in mine rehabilitation efforts, mainly due to the need for P acquisition. Work in a
similar vein continues to highlight the importance of fungal
inoculants for successful rehabilitation of degraded soils and
mine sites, in Mediterranean climates especially (e.g., Herrera
et al. 1993, Quatrini et al. 2003).
Using the Mirbelieae as an example, Sprent (1995) noted
that: ‘This tribe, as one comes to expect of uniquely Australian plants and animals, has some very interesting features’.
Those features included both vesicular-arbuscular and ectomycorrhizal associations and the ability to form cluster
roots—yet another adaptation to low-P soils. Shane and
Lambers (2005), in a summary of much of their research into
cluster roots, noted that genera such as Viminaria, Myrica,
Acacia and Kennedia are capable of both an N-fixing symbiosis and the ability to produce cluster roots. Exactly how
widespread among woody legumes is the ability to form
cluster roots is not yet clear. What does seem clear is that
none of the woody legumes examined to date lack both
the ability to form mycorrhizal symbioses and the ability
to form cluster roots—they all have one or the other. The
more we look at the Southern flora, the greater the number
of woody legumes we find that have root specializations that
help them acquire P.
As an example, Figure 1 illustrates how, when provided with
a ‘spatially distributed choice of available phosphorus’, cluster
roots and nodules develop on lateral roots of five woody legumes from Western Australia. Quite clearly, cluster roots developed where the supplies of P were greatest. Conversely,
nodules developed most strongly elsewhere on the root system, where P supplies were low (Adams et al. 2002). Provided
the plant has adequate P and the plant has the capacity to
produce cluster roots to take advantage of spatially variable
P supplies, nodulation need not be restricted. These results
also suggest that the metabolic demands for carbon by nodules (as required for N fixation) and cluster roots (as required for P acquisition) might cause spatial separation of
root specializations and might, ultimately, limit either or both
processes.
Similarly, the potential limitation to N fixation posed by
variation in the ability of bacteria to successfully infect
woody legumes has been the subject of a very large number
of investigations, and only a broad overview is provided here.
For Africa, species from both the wet and dry topics and subtropics have been the subject of considerable scrutiny from
many researchers, including Janet Sprent loc cit. (e.g., Odee
et al. 1995, 1997, Masutha et al. 1997, Wolde-meskel and
Sinclair 1998, Bala and Giller 2001, Bala et al. 2002,
2003a, 2003b, Wolde-meskel et al. 2004). For Australia,
the reader is referred to works by Lawrie (1983), Barnet
and Catt (1991), Pérez-Fernández and Lamont (2003), Lafay
and Burdon (1998, 2001, 2007), Roughley (1987) and also
Sprent (2007). The consensus view is that there is a wide variety of nodulating bacteria, many of which are promiscuous
and capable of infecting a wide range of plants. Bradyrhizobium spp. appear particularly effective, though in many instances, identification of nodulating species is still limited
to broadly based classifications (e.g., fast- vs slow-growing).
Rates of N fixation by Southern woody legumes vary widely
(Table 2). Generally, faster rates (and greater amounts over any
given time period) of fixed N are recorded for more tropical,
mostly Mimosoid species—Albizia, Calliandra, Gliricidia,
Leucaena, Inga and Prosopis. Rates recorded for Acacia are
generally lower than those for the above genera, with the immediate caveat that most of the records for Acacia come from
drier parts of the tropics or subtropics or from temperate regions of Australia and Africa where drought (and fire) is
common. Within the Acacia data, greater amounts of fixed
N are recorded in the more productive forests, where losses
of N during fire are also greater, as is the fire-promoted
mineralization of P from biomass and litter (e.g., Adams
and Byrne 1989, Adams 1990).
The variety of methods used to make estimates of N fixation is well covered elsewhere as are the sources of error
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ADAMS ET AL.
Table 2. Annual rates of nitrogen fixed by species from the Mimosoideae subfamily of the Leguminosae from the Northern and Southern
Hemispheres. For comparison purposes, we have listed some species from the Papillionoideae at the bottom of the table.
Species
Study country
Stand age
(years)
Rate of N fixation
(kg ha−1 year−1)
Reference
Mimosoideae
Acacia alata
Acacia angustifolia
Acacia caven
Acacia dealbata
Zimbabwe
Chile
Australia
Acacia extensa
Acacia holoserica
Australia
Senegal
Acacia
Acacia
Acacia
Acacia
holostera
magnium
mearnsii
melanoxylon
Senegal
Brazil
Australia
Australia
Acacia
Acacia
Acacia
Acacia
paradoxa
pellita
pennatula
pulchella
Australia
Australia
–
Australia
Acacia senegal
Acacia vernicifula
Albizia lebbeck
Sudan
Australia
Nigeria
Albizia falcataria
Calliandra calothyrsus
Hawaii
Australia
Calliandra calothyrsus
Inga edulis
Leucaena spp.
Leucaena leucocephala
Kenya
Costa Rica
Nigeria
Malaysia
Nigeria
Puerto Rico
Tanzania
USA
Chile
2
6
2
5
50+
1–6
–
1
–
2.5
7
7
50+
7
3
–
1–13
0.3–1
4
–
1
–
–
2
1
0.6
1–2
–
–
1–4
1.5–3.5
4
1
–
–
1.6
61
9.5
12–32
50
2.1
0.1
36–108
4–11
<12
66
0.75
0.005
31.6
0.042
12
34
2.2
6
7–12
38
60–120
94
100–200
67–93
76
24
100
304
934
238
71–74
110
40
25–30
80–590
Hansen et al. 1987
Chikowo et al. 2004
Aronson et al. 2002
Adams and Attiwill 1984
May and Attiwill 2003
Pfautsch et al. 2009
Hansen et al. 1987
Peoples and Herridge 1990
Cornet et al. 1985
Peoples and Herridge 1990
Bouillet et al. 2008
Lawrie 1981
Lawrie 1981
Pfautsch et al. 2009
Lawrie 1981
Langkamp et al. 1979
Roskoski et al. 1982
Monk et al. 1981
Hingston et al. 1982
Raddad et al. 2005
Turvey and Smethurst 1983
Kadiata et al. 1996
Danso et al. 1992
Binkley and Giardina 1997
Stahl et al. 2002
Purwantari et al. 1996
Gathumbi et al. 2002
Leblanc et al. 2007
Danso et al. 1992
Peoples and Herridge 1990
Sanginga et al. 1996
Parrotta et al. 1996, 1994
Högberg and Kvarnström 1982
Shearer and Kohl 1986
Rundel et al. 1982
Urzúa 2000
Costa Rica
Costa Rica
Costa Rica
French Antilles
Nigeria
Indonesia
Sumatra
Philippines
6
1–2
1–2
8
–
1.3
1
1.5
82.5
60–160
80
147
108
700
35–38
126
Salas et al. 2001
Leblanc et al. 2007
Leblanc et al. 2007
Dulormne et al. 2003
Danso et al. 1992
Catchpoole and Blair 1990
Hairiah et al. 2000
Ladha et al. 1993
Prosopis glandulosa
Prosopis spp./Acacia caven
Papillionoideae
Erytrina lanceolata
Erytrina poeppigiana
Erytriana fusca
Gliricidia sepium
inherent to each approach. We regard most of the estimates
listed in Table 2 as conservative, while some earlier estimates
of N fixation by acacias were questioned as being ‘too large’
and due to errors associated with assay methods (such as the
acetylene reduction technique). However, when earlier results
are revisited, usually with a variety of 15N-based approaches
(e.g., Guinto et al. 2000, May and Attiwill 2003), earlier estimates are revised upwards.
Taken together with the observations of Houlton et al.
(2008), the Southern woody legumes, especially species from
the subfamily Mimosoideae, play major roles as ‘ecosystem
engineers’. Their ability to remobilize P and to fix atmospheric
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WOODY LEGUMES: A (RE)VIEW FROM THE SOUTH
N at considerable rates is of benefit to many other plants and
animals. It is arguable that, in systems where fire is common or
even prevalent, members of the Mimosoideae and perhaps the
Caesalpinioideae are truly keystone species.
Ecophysiology—coping with drought
The genus Acacia has inspired some of the most seminal and
fundamental work on the water relations of all plants. Beginning more than 50 years ago, Ralph Slatyer and colleagues
worked first to develop techniques that would yield reliable
data and then applied those to species of Acacia, most notably A. aneura (e.g., Slatyer 1960, 1961, 1962, 1965). The
history of this development is covered in some detail by
Doley (2004). Much of this work was captured in the iconic
text Plant–Soil Water Relationships published in 1967
(Slatyer 1967). One of the most striking aspects of the early
work is that the Scholander pressure chamber was not introduced till 1964 (Scholander et al. 1964). Thus, Slatyer et al.
had to use far more difficult techniques to be able to provide estimates of key aspects of water potential (including
osmotic potential)—estimates that are still used as points of
reference for researchers that have followed (see summary
by Winkworth 1973, also O'Grady et al. 2009).
The water relations of honey mesquite (Prosopis glandulosa Torr.) have been studied in some detail, particularly in
the Sonoran Desert (Nilsen et al. 1983). P. glandulosa is
largely phreatophytic, acquiring water from sources as deep
as 4–6 m below the surface. Nonetheless, it still generates
xylem pressure potentials of close to −5 MPa at midday in midsummer (Nilsen et al. 1983), when vapour pressure deficits approach 8 kPa. A key to its ability to maintain turgor is
undoubtedly its ability to generate solute (osmotic) potentials
of between 2 and 4 MPa. This is one of the notable features of
Southern woody legumes—their ability to develop significant
osmotic potentials as part of their tolerance of drought. Otieno
et al. (2005) showed that, for two African acacias—Acacia
tortilis (Forssk.) Hayne and Acacia xanthophloea Benth.—
osmotic potential at the turgor loss point accounted for almost 96% of variation in water potential at the same turgor
loss point. They went on to speculate that the accumulation
of solutes was probably responsible. Johnson et al. (1996)
recorded that Colophospermum mopane (J. Kirk ex Benth.)
J. Léon., a member of the Caesalpinioideae that is widespread in low-altitude, high-temperature regions of southern
Africa, could develop significant concentrations of pinitol
(>100 mol m−3) in foliage and especially roots in response
to drought (or salinity). Significantly, they noted that increased concentrations in roots were not due to loss of
water. Liu et al. (2008) found that pinitol content constituted
50% of phyllode total sugars in Acacia auriculiformis A.
Cunn. ex Benth. in northern Australia compared with 17%
for fructose, 20% for glucose and <10% for sucrose. These results accord closely with ‘general knowledge’ for acacias
1077
and other mimosoid legumes—they can accumulate significant quantities of pinitol and related compounds. Seigler
(2003) provides a good overview of the more general phytochemistry of Acacia spp.
Southern woody legumes can clearly become ‘conditioned’ to drought. Conditioning includes a wide range of
features in addition to osmotic adjustment, as described recently for Prosopis in Argentina by Villagra et al. (2010). As
a further example, xylem conductivity of Acacia seedlings
(Clemens and Jones 1978) can be altered by conditioning to
drought and was correlated with stomatal behaviour. Leaf
shedding is another mechanism noted as being important to
how Acacia and other woody legumes such as Senna, Anadenanthera and Machaerium spp. can adapt to and cope with
drought (e.g., Filho and Filho 2000, Gebrekirstos et al.
2006). Noting again the large area (∼20%) of Australia dominated by A. aneura, O'Grady et al. (2009) presented data that
argued for convergence of species-based physiological traits
(including Eucalyptus) within the arid and semi-arid zones,
such that general rules (e.g., for hydrological analysis) could
be applied. Even so, data for A. aneura usually marked one
of the two extremes of the recorded range (e.g., Huber values,
wood density, specific leaf area).
Ecophysiology and the future—woody legumes as exotics,
invaders and agents of rehabilitation and food and fuel
production
Looking to the future requires consideration of changing atmospheric [CO2] and its likely effects on plants. As far as we
are aware, there is still little work done on the response of
Southern woody legumes to atmospheric [CO2], and that
published by Schortemeyer et al. (1999, 2002) stands alone
for Acacia spp. Schortemeyer et al. found that both growth
and rates of N fixation by glasshouse-grown seedlings of a
range of Acacia spp. were generally increased in the presence
of increased atmospheric [CO2], albeit that plants were grown
with ample supplies of P.
Therein lies a key issue—will availability of P serve to
limit responses of Southern legumes to rising atmospheric
[CO2]? This is an open question. Binkley (2005) noted that
rates of cycling of P always seem to be greater under N-fixing
species, while Binkley et al. (2003) showed that the metabolic
responses (including rates of N fixation) to added P by the
woody legume Facaltaria moluccana (Miq.) Barneby & J.
W. Grimes (= Albizia falcataria) were far greater than the
growth responses. Binkley's evidence (and that of others)
comes mostly from areas where legumes have been planted
or introduced, so it is not that legumes have ‘selected’ those
areas of soil that have greater availability of P. It seems that
legumes in general, including woody legumes from the South,
have inherent capability to increase availability of forms of
P unavailable to other plants and to enhance N fixation as a
result (as noted above and by Houlton et al. 2008).
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This capacity also speaks to the potential of woody legumes
to succeed and even become invasive, where other plants may
fail due to poor supplies of water and P. Clearly, deliberate introductions of species from genera such as Acacia, Prosopsis,
Mimosa, Sesbania and Parkinsonia needs careful thought (e.g.,
Hughes and Styles 1989, Paynter et al. 2003, Jamnadass et al.
2005). Faye et al. (2009) noted recently that relationships
among root nodule bacteria, ectomycorrhizal fungi and cohabiting native (Faidherbia albida (Del.) A. Chev.) and introduced (Acacia holosericea G. Don) woody legumes are far
from simple and that negative effects of one association may
be offset by others. In many places, Southern woody legumes
have become ‘naturalized’ parts of the flora, and they too can
become serious pest plants (e.g., Emms et al. 2005). However,
this also provides a note of caution—interpretations that
climate alone is the cause of increased abundance of woody
legumes may well miss the obvious points that such increases
could owe as much to the ability of legumes to thrive where
other species struggle as it does to any change in climate. In
particular, the at least partial dependence of the abundance
of woody legumes on fire regimes can easily be confused or
confounded with the effects of changing climate. An example
is the honey mesquite. Most of the more than 40 species of
mesquite are native to South America (Burkhart and Simpson
1977). However, it is a highly successful woody legume in
much of the arid and semi-arid areas of both South and North
America as well as northern Africa and parts of Asia. At
present in the USA, Prosopis spp. or mesquite ‘is the dominant
woody plant on more than 38 million ha of what has been considered semi-arid southwestern grasslands’ (Van Auken 2000).
Most ecologists regard its spread into grasslands as due to
the combination of grazing and fire regimes (e.g., Wright
et al. 1976, Archer 1989, Archer et al. 1995), especially
the active suppression of fire or heavy grazing that removes
the fuel and makes fire less likely (Van Auken 2000). As
mentioned previously, availability and viability of fungal
and bacterial symbionts will continue to be important determinants of the success of efforts to (re)introduce woody
legumes as part of rehabilitation or restoration programmes
(e.g., Murray et al. 2001, Bell et al. 2003, Thrall et al. 2005,
2007). The many advantages over other plants enjoyed by
woody legumes from the South and their association with
and responses to fire make assigning causality to their spread
a hazardous occupation.
All of the above also suggest that effort to better understand the physiology of the Southern woody legumes will
be rewarded—they will play a major role in land rehabilitation and carbon sequestration strategies. Using their ability
to fix nitrogen and acquire phosphorus, they can contribute
strongly to soil carbon. Their capacity to accumulate cyclitols to very significant concentrations as part of coping with
drought is largely unexplored. We believe this last trait offers great potential. For example, SoyOyl® is a trademark
product of Dow Chemical that is based on the cyclitols produced by soy beans. SoyOyl® has countless applications
and is now widely used in plastics and other industries. A
combination of useful physiological traits make Southern
woody legumes literally ‘biofactories’.
Conclusions
This review has focused on the woody legumes of the South,
especially genera such as Acacia and Prosopis, that have
proved to be remarkable for their adaptability to old soils,
drought and fire, as much in the North as in the South. While
many of the genera in the subfamilies Mimosoideae and Caesalpinioideae are not always nodulated and do not always
show evidence of N fixation, under the right conditions,
many of their species will nodulate and fix atmospheric N,
often at rates approaching those measured for legumes from
the Papilionoideae that are more frequently used in agricultural systems. Insofar as we have looked, species of the Mimosoideae and Caesalpinioideae subfamilies show clear
adaptations that aid their acquisition of P from soils that frequently lack plant-available P.
Given the increasingly clear economic importance of nitrogen fixation, the ecological significance of woody legumes in
the South (and the North) and the still poor general level of
knowledge of these remarkable plants, there is an urgent need
for further research. Perhaps, the first priority should be the
processes that facilitate their acquisition of N and P under
often harsh edaphic conditions. A second priority might be
investigations as to why the Caesalpinioideae are generally
so poor at producing nodules and into their rates of N fixation. In evolutionary terms, it seems odd that they seemingly
cannot fix N, yet can be so common or even dominant in
areas/regions where N could become a limiting element
(most likely due to fire).
Finally, given changing climates (especially potential reductions in rainfall in large parts of southern Africa and
Australia and South America) and atmospheric [CO2], the
mechanisms by which the Mimosoideae and Caesalpinioideae adapt to drought and fire deserve far more attention.
As a side benefit, we might elucidate further the processes
responsible for their accumulating large quantities of cyclitols (e.g., pinitol) and their adaptation to use as feedstocks
for biofuels and even their use as ‘biofactories’. We concur
with and extend the understated plea of Sprent et al.
(2009) for greater investment in research in African legumes. We agree that there is an urgent need to develop
African legumes for Africa and Australian legumes for
Australia and South American…
Funding
Funding to support the preparation of this article was provided by
the Australian Research Council.
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