supporting those that are fixing more nitrogen with
increased resources, then cooperation will tend to
be favoured. This has been termed the ‘sanctions’
hypothesis and suggests that the reproductive suc-
cess of the rhizobium strain is contingent on the
strain’s ability to export nitrate to the host (Denison
2000; Westet al.2002a, b; Kierset al. 2003). It has
been found that legume hosts will impose fitness-
limiting sanctions (‘punishment’) to rhizobial
strains based on the actual nitrogen-fixing benefits
the strain provides (Kierset al. 2003; Simmset al.
2006). The mechanism of punishment is thought to
involve a decreased oxygen supply to nodules and
the severity of this punishment varies, depending
on the extent of cheating (Kierset al. 2006).
The nitrogen-fixing symbiosis can confer incredi-
ble advantages to both the host plant and the rhizo-
bial symbiont. For rhizobia, participating in the
symbiosis can dramatically enhance reproductive
output. A single rhizobium cell that infects a soy-
bean root can produce up to 10^10 descendents from
a single large nodule (Denison and Kiers 2004b).
For plants, the extra nitrogen from fixation can
facilitate their rapid spread across the landscape.
While free-living nitrogen fixation association may
result in approximately 0.1–25 kg/ha/year, symbi-
otic nitrogen can have fixation rates between 100
and 300 kg/ha/year (Pepper 2000). Given that the
rhizobia–legume symbioses can increase soil nitro-
gen fourfold compared with free-living nitrogen
fixers, the impact of this symbiosis on ecosystem
functioning is significant.
Some of the world’s most troublesome invaders
of natural ecosystems have been nitrogen-fixing
legumes and actinorrhizal species such asAcacia,
Albizzia, ProsopisandMyrica faya(Richardsonet al.
2000). It is believed that invading legumes are able
to alter community composition through their
modifying influence on soil nitrogen levels. Plant
species of most terrestrial ecosystems are adapted
to low-nitrogen soils (Riceet al. 2004). Nitrogen-
fixing legumes can cause a subtle, but continuous,
increase in nitrogen pools and fluxes in nitrogen-
limited ecosystems (Olde Venterinket al. 2002).
Changes in soil nutrient profiles will have direct
effects on the competitive success of species leading
to dramatic alterations in community composition
(Bobbink et al. 1998; Salaet al. 2000; Scherer-
Lorenzenet al. 2007). One clear example is invasion
by the actinorrhizalMyrica fayain a nitrogen-limit-
ed forest in Hawaii.Myrica fayacaused an influx of
18 kg nitrogen/ha/year whereas the nitrogen
amounts in the Hawaiian forest soils prior to the
introduction ofMyrica fayawas only 5.5 kg nitro-
gen/ha/year (Vitouseket al1987; Vitousek and
Walker 1989). Here, owing to a substantial increase
in nitrogen inputs,Myrica fayacould successfully
displace the nativeMetrosideros polymorpha, leading
to significant community reorganization.
Successful colonization by an alien legume spe-
cies will depend largely on its ability to find a
compatible rhizobial symbiont. Competitive exclu-
sion of species adapted to low nutrient levels by
faster growing nitrophilic species is independent of
whether it is an alien invading species or a native
species (Scherer-Lorenzenet al. 2007). Native le-
gume species, however, might be successful in reg-
ulating the community structures through their
influence on nitrogen cycling. The long-term effects
of nitrogen fixation on ecosystem functioning and
plant species composition are largely unknown
(Scherer-Lorenzenet al. 2007). Nitrogen fixation
not only influences primary productivity, but may
also have cascading effects on successional pat-
terns, community composition and disturbance re-
gimes (Riceet al. 2004). Scherer-Lorenzenet al.
(2007) suggest that the increased nitrogen availabil-
ity that nitrogen-fixing plants provide might be an
important pathway by which nitrogen-fixing inva-
ders alter community structures.
A model developed by Parker (2001) predicts
how a legume–rhizobia partnership can facilitate
the invasion of an ecosystem. The model sets a
legume invader to compete with a resident non-
mutualist plant (non-legume) in an nitrogen-limit-
ed environment. In the absence of mutualist rhizo-
bia, both the legume and the non-legume compete
for nitrogen in the soil according to Lotka–Volterra
competition dynamics. In the absence of the rhizo-
bia, legumes are assumed to be inferior competi-
tors. Both plants can coexist as long as nitrogen is
available. When nitrogen supplies are exhausted,
the non-legume excludes the inferior legume from
the community. However, when mutualist rhizobia
are introduced into the soil, they provide a benefit
to the legume host by making fixed nitrogenMUTUALISMS AND COMMUNITY ORGANIZATION 187