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Plant and Soil
An International Journal on Plant-Soil
Relationships
 
ISSN 0032-079X
 
Plant Soil
DOI 10.1007/s11104-012-1493-z
Soil microbial biomass and the fate of
phosphorus during long-term ecosystem
development
Benjamin L.?Turner, Hans Lambers,
Leo M.?Condron, Michael D.?Cramer,
Jonathan R.?Leake, Alan E.?Richardson &
Sally E.?Smith
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REGULAR ARTICLE
Soil microbial biomass and the fate of phosphorus
during long-term ecosystem development
Benjamin L. Turner & Hans Lambers &
Leo M. Condron & Michael D. Cramer &
Jonathan R. Leake & Alan E. Richardson &
Sally E. Smith
Received: 4 May 2012 /Accepted: 5 October 2012
# Springer Science+Business Media B.V. (outside the USA) 2012
Abstract
Background Soil phosphorus availability declines
during long-term ecosystem development on stable
land surfaces due to a gradual loss of phosphorus in
runoff and transformation of primary mineral phos-
phate into secondary minerals and organic com-
pounds. These changes have been linked to a
reduction in plant biomass as ecosystems age, but the
implications for belowground organisms remain
unknown.
Methods We constructed a phosphorus budget for the
well-studied 120,000 year temperate rainforest chro-
nosequence at Franz Josef, New Zealand. The budget
included the amounts of phosphorus in plant biomass,
soil microbial biomass, and other soil pools.
Results Soil microbes contained 68?78 % of the total
biomass phosphorus (i.e. plant plus microbial) for the
majority of the 120,000 year chronosequence. In con-
trast, plant phosphorus was a relatively small pool that
occurred predominantly in wood. This points to the
Plant Soil
DOI 10.1007/s11104-012-1493-z
Responsible Editor: Nico Eisenhauer.
B. L. Turner (*)
Smithsonian Tropical Research Institute Apartado,
0843-03092 Balboa, Ancon, Republic of Panama
e-mail: TurnerBL@si.edu
B. L. Turner : H. Lambers : M. D. Cramer :
A. E. Richardson
School of Plant Biology, The University
of Western Australia,
35 Stirling Highway,
Crawley, Western Australia 6009, Australia
L. M. Condron
Agriculture and Life Sciences,
PO Box 84, Lincoln University,
Lincoln 7647 Canterbury, New Zealand
M. D. Cramer
Department of Botany, University of Cape Town,
University Private Bag,
Rondebosch 7700, South Africa
J. R. Leake
Department of Animal and Plant Sciences,
University of Sheffield,
Alfred Denny Building, Western Bank,
Sheffield S10 2TN, UK
A. E. Richardson
CSIRO Plant Industry,
GPO Box 1600, Canberra, Australian Capital Territory
2601, Australia
S. E. Smith
School of Agriculture, Food and Wine,
The University of Adelaide,
Adelaide, South Australia 5005, Australia
Author's personal copy
central role of the microbial biomass in determining
phosphorus availability as ecosystems mature, yet also
indicates the likelihood of strong competition between
plants and saprotrophic microbes for soil phosphorus.
Conclusions This novel perspective on terrestrial
biogeochemistry challenges our understanding of
phosphorus cycling by identifying soil microbes
as the major biological phosphorus pool during
long-term ecosystem development.
Keywords Chronosequence . Franz Josef . Microbial
biomass . Phosphorus . Soil
Introduction
On stable land surfaces, and in the absence of major
disturbance, phosphorus availability declines during
ecosystem development over thousands to millions
of years (Walker and Syers 1976; Crews et al. 1995).
This occurs through a combination of chemical trans-
formations of soil phosphorus (Walker and Syers
1976; Parfitt et al. 2005; Turner et al. 2007) and its
loss in runoff at a greater rate than it is replenished by
bedrock weathering or dust deposition from the atmo-
sphere (Hedin et al. 2003). These changes have been
linked to a reduction in plant biomass as ecosystems
age, termed forest retrogression (Wardle et al. 2004),
and appear to be a consistent property of ecosystems,
because the same pattern has been observed in chro-
nosequences that have developed under a range of
climate conditions and on different geological sub-
strates (Peltzer et al. 2010). The trend towards biolog-
ical phosphorus limitation as soils age therefore
provides a strong conceptual framework within which
to evaluate the effects of long-term changes in nutrient
availability on biological communities.
Although previous studies have revealed the impor-
tance of phosphorus in regulating forest biomass
(Wardle et al. 2004) and diversity (Wardle et al.
2008; Wassen et al. 2005), the implications of the
decline in phosphorus availability during ecosystem
development for belowground microbial communities
remain poorly understood (Peltzer et al. 2010). This is
of significance because the soil microbial biomass
(including saprotrophs and mycorrhizal fungi) plays
a central role in the cycling and availability of phos-
phorus in soils (Richardson and Simpson 2011).
Despite this, the microbial phosphorus pool is often
assumed to be quantitatively small, because most
measurements have been made on agricultural soils
that are enriched in phosphorus (Cleveland and
Liptzin 2007). Although a few studies have included
microbial biomass in whole-ecosystem phosphorus
budgets (e.g. Halm et al. 1972; Chapin et al. 1978),
this has not been attempted previously for a long-term
retrogressive chronosequence.
To address this gap, we constructed a whole-
ecosystem phosphorus budget for the 120,000 year
Franz Josef post-glacial chronosequence, New
Zealand. The budget included estimates of phosphorus
in plant biomass, soil microbial biomass, and other
soil pools. Our aim was to determine for the first time
how phosphorus pools in plants, microbes, and soils,
vary during ecosystem development.
Methods
The Franz Josef post-glacial chronosequence is well
studied (Walker and Syers 1976; Parfitt et al. 2005;
Wardle et al. 2004; Richardson et al. 2004; Turner et
al. 2007) and patterns of soil phosphorus and forest
biomass are representative of chronosequences more
broadly (Peltzer et al. 2010). Briefly, the Franz Josef
chronosequence consists of a series of post-glacial
schist outwash surfaces up to 120,000 years old on
the west coast of the South Island of New Zealand.
Mean annual temperature is 10.8 ?C and annual rain-
fall varies from ~6.5 m on young soils in the glacial
valley to ~3.5 m on the older sites nearer the coast
(Richardson et al. 2004). The sites support mixed
conifer?angiosperm forests, with young sites dominat-
ed by evergreen angiosperms and older sites support-
ing an increasing proportion of conifers in the
Podocarpaceae (Richardson et al. 2004). The two old-
est sites have experienced at least one glacial?inter-
glacial cycle, with deposition of infertile quartz silt
loess during the last glaciation (Almond et al. 2001).
Despite this, the sequence represents a clear age-
related nutrient gradient that influences both above
and below-ground biological communities (Allison et
al. 2007; Richardson et al. 2004; Wardle et al. 2004;
Williamson et al. 2005).
We calculated a phosphorus budget for four key
stages of the chronosequence: 5 years, 1000 years,
12,000 years, and 120,000 years. Note that the age
of the oldest stage of the sequence (120,000 years)
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was revised from the original 22,000 years reported by
Walker and Syers (1976) based on reinterpretation of
landforms (Almond et al. 2001). For each stage we
calculated the amount of phosphorus on an area basis
(g P m-2) contained in plant biomass, soil microbial
biomass, and other soil pools. Soil phosphorus pools,
including phosphorus in stones, primary mineral phos-
phate (apatite), organic phosphorus, and secondary
mineral phosphate, were calculated to 75 cm depth
using values from Walker and Syers (1976) and bulk
density values for each horizon from Stevens (1968).
Phosphorus in plant biomass was calculated for above-
ground wood, roots, and leaves using published val-
ues. Foliar phosphorus was estimated from leaf
phosphorus concentrations across the chronosequence
(Richardson et al. 2005) and specific leaf area
(Whitehead et al. 2005) and leaf area index (LAI)
derived from normalized difference vegetation index
values (NDVI; Whitehead et al. 2005) using an LAI?
NDVI relationship established for New Zealand for-
ests (Coops et al. 2002). Phosphorus in aboveground
wood was estimated from vegetation height (H)
(Richardson et al. 2004; Wardle et al. 2004) converted
to wood biomass using (2.8+0.4H)2 (Lefsky et al.
1999) and a global average of wood phosphorus con-
centration (0.0075 %; Chave et al. 2009) that was
similar to values for native New Zealand trees
(Levett et al. 1985). Belowground plant biomass was
estimated as a fixed proportion (20 %) of aboveground
biomass (White et al. 2000), with phosphorus content
calculated using a mean root phosphorus concentra-
tion (Vitousek and Sanford 1986); this measure for
coarse plus fine roots gave a similar, but slightly
lower, estimate of belowground phosphorus than us-
ing phosphorus concentrations for fine roots sampled
along the Franz Josef chronosequence (Holdaway et
al. 2011). The estimate of vegetation phosphorus was
most sensitive to the 50-fold variation in canopy
height across the chronosequence rather than to possi-
ble variation in individual parameters.
We added new measurements of soil microbial
phosphorus in the top 10 cm of the mineral soil and
the organic horizon (where present). This is presum-
ably the region that contains the majority of the mi-
crobial biomass (e.g. Fierer et al. 2003), although the
oldest soil along the sequence contained relatively
high carbon concentrations in deeper parts of the pro-
file (Stevens 1968), raising the possibility that micro-
bial phosphorus was underestimated at this site. Five
replicate soil samples were taken at each site over 3 days
in the southern hemisphere winter. Soils were sieved
<4 mm, small stones and fine roots were removed
manually, and the samples were stored at 4 ?C prior to
analysis. Microbial phosphorus was determined for nine
sites along the chronosequence ranging from 60 to
120,000 years, including the four sites for which the
whole-ecosystem budgets were calculated. For the sur-
face mineral soil we measured microbial phosphorus
directly by chloroform fumigation with phosphorus de-
tection by molybdate colorimetry (Brookes et al. 1982).
Values were corrected for phosphate sorption to soil
during the extraction and for microbial phosphorus not
recovered by fumigation (i.e. using a kp factor) (Brookes
et al. 1982). In the same soils we also determined
microbial carbon and nitrogen by standard procedures
involving chloroform fumigation and extraction in
0.5 M K2SO4 with carbon and nitrogen detection by
TOC?TN analyzer (Shimadzu, Columbia, MD) and ap-
propriate corrections for unrecovered biomass (Brookes
et al. 1985; Vance et al. 1987).
Chloroform fumigation does not release phospho-
rus from non-microbial soil organic matter (Brookes et
al. 1982), although leaf fragments and fine roots can
contribute (Sparling et al. 1985). As this could lead to
an overestimation of microbial phosphorus in soil
organic horizons, we used total phospholipid fatty acid
(PLFA) concentrations measured in both mineral soil
(0?10 cm) and organic horizons (methodology and
data reported in Allison et al. 2007) to estimate micro-
bial phosphorus in the organic horizon using the
PLFA-to-microbial-carbon ratio of the mineral soil.
This assumes a close relationship between total
PLFA and microbial carbon concentrations deter-
mined by fumigation extraction (e.g. Fierer et al.
2003), and a constant microbial carbon to phosphorus
ratio between organic and mineral horizons at a site
(e.g. Sparling et al. 1994).
We corrected the original organic phosphorus val-
ues presented in Walker and Syers (1976) by subtract-
ing the amount of microbial phosphorus, based on the
assumption that most microbial phosphorus in unman-
aged soils occurs in organic forms (Magid et al. 1996).
Microbial phosphorus concentrations were too low to
measure on the youngest soil, so these were estimated
from microbial phosphorus data for a 60 year old site,
assuming a constant total organic carbon-to-microbial
phosphorus ratio (as observed from the positive linear
relationship between total carbon and microbial
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phosphorus in surface soils along the sequence). Total
organic carbon concentrations for all samples along
the sequence were reported previously (Allison et al.
2007).
Results
There was a rapid depletion of primary mineral
phosphate in both stones and the fine earth fraction
(< 2 mm), and a parallel accumulation of phospho-
rus in secondary minerals and organic compounds
(Fig. 1, Table 1). Only a small proportion of the
total profile weight of phosphorus was in the or-
ganic horizon at any site (? 4 %; Table 2).
Ecosystem phosphorus in organic forms, including
dead soil organic matter, plants, and microbes, in-
creased from < 1 % of the total phosphorus in the
youngest soil (5 years) to > 40 % in the oldest soil
(120,000 years). These changes confirm a progressive
switch from a system dominated by dissolution of inor-
ganic phosphorus in primary minerals driven by weath-
ering, to mineralization of organic phosphorus driven by
biological processes. Particularly striking, although not
widely recognized, is the rapid decline of the stone
fraction and its contribution to phosphorus availability
during ecosystem development through weathering and
the release of primary mineral phosphate.
For living tissue, phosphorus in plant biomass con-
stituted a relatively small pool throughout the sequence
(0.5?4.9 g P m-2; Fig. 1; Table 1). Plant phosphorus
was mostly contained in woody tissue in the late
phosphorus-limited stages of the chronosequence
(Table 1). In contrast, the soil microbial biomass
contained 3.9?10.3 g P m-2 in mature soils, which
represented 68?78 % of the total biomass phosphorus
(Fig. 1; Table 1). Microbial phosphorus was therefore
several times greater than phosphorus in vegetation for
the majority of the 120,000 year chronosequence. The
organic horizon contained only ~8 % of the total micro-
bial phosphorus in the 1000 and 120,000 year soils, but
26 % in the 12,000 year soil, reflecting the thickness of
the organic horizon at this site (Table 2).
Aside from the early stages of the chronosequence,
microbial nutrient concentrations in mineral soil var-
ied little over 120,000 years of ecosystem develop-
ment (Fig. 2). For soils between 500 and 60,000 years
old, microbial carbon, nitrogen, and phosphorus con-
centrations were ~1500 mg C kg-1, ~300 mgN kg-1,
and ~150 mg P kg-1, respectively (Fig. 2).
Concentrations of all microbial nutrients were lower
in younger soils, and there was a small decline in
microbial phosphorus in the oldest soil (Fig. 2c).
The relatively consistent concentrations of nutrients
in microbial biomass resulted in stable carbon to ni-
trogen and carbon to phosphorus ratios for the major-
ity of the sequence (Fig. 2d). For all soils between 130
and 60,000 years, mean microbial carbon to phospho-
rus molar ratios were ~30 and microbial nitrogen to
phosphorus molar ratios were ~5 (Fig. 2d). Ratios
were higher in young (60 year) and old (120,000 year)
soils (Fig. 2d).
Discussion
Previous studies of ecosystem development have
revealed the importance of total phosphorus in regu-
lating plant biomass (Wardle et al. 2004), as well as
the increasing importance of organic phosphorus as
soils age (Walker and Syers 1976; Turner et al. 2007),
but have not recognized the quantitative significance
of the soil microbial phosphorus pool. This is perhaps
because measurements have been made on agricultural
systems, where microbial biomass typically
contains < 5 % of the total soil phosphorus
(Brookes et al. 1982; Cleveland and Liptzin 2007).
The remarkable finding that soil microbial bio-
mass contains much more phosphorus than plant
biomass for the majority of the 120,000 years of
ecosystem development at Franz Josef is linked to
the disparity between the concentrations of phos-
phorus in plant and microbial tissues. For example,
the mean phosphorus concentrations (dry weight
basis) for soil microbes were reported to be
5.4 mg P g-1 in fungi and 19 mg P g-1 in bacteria
(Brookes et al. 1982). In contrast, the global aver-
age phosphorus concentration in wood is approxi-
mately 0.08 mg P g-1 (Chave et al. 2009), which
is similar to values reported for New Zealand
broadleaf?podocarp forests (Levett et al. 1985).
For live leaves, community-level phosphorus con-
centrations range between 0.5 and 1.6 mg P g-1
along the Franz Josef chronosequence, with the lowest
concentrations on the oldest sites (Richardson et al.
2004). Microbes therefore contain substantially greater
phosphorus concentrations than plants throughout the
sequence.
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Concentrations of carbon, nitrogen, and phospho-
rus in microbial biomass varied little along the chro-
nosequence, although there was evidence for a decline
in microbial phosphorus in the oldest soil, perhaps
attributable to the previously reported increase in the
fungal to bacterial ratio in the late stages of the
Fig. 1 Changes in ecosys-
tem phosphorus pools along
the 120,000-year Franz
Josef soil chronosequence,
New Zealand. The area of
each scale box represents the
amount of phosphorus in the
respective pool on an area
basis to 0.75 m depth (g P
m-2). Note the central role of
the microbial biomass in the
system; its representation as
a triangle emphasizes the
three axes of interactions
and transfers between the
other major pools, including
with plants via mycorrhizal
fungi (the apex of the trian-
gle), weathering of mineral
phosphorus (the left-facing
point of the triangle) and
mineralization of organic
phosphorus (the right facing
point). Bar graphs show
(from left to right) organic
phosphorus (i.e. phosphorus
in soil organic matter,
microbes, and vegetation) as
a percentage of the total
ecosystem phosphorus, mi-
crobial phosphorus as a per-
centage of the soil organic
phosphorus (i.e. phosphorus
in organic matter and
microbes), and microbial
phosphorus as a percentage
of the total biomass phos-
phorus (i.e. phosphorus in
microbes and vegetation)
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sequence (Allison et al. 2007). Wardle and Ghani
(1995) also observed that microbial biomass in mineral
and organic horizons determined by substrate-induced
respiration increased early on in the sequence and de-
clined in the oldest soil, a similar pattern to that reported
here for microbial carbon and nitrogen determined by
fumigation?extraction. The stable microbial nutrient
concentrations are consistent with the recent suggestion
that microbial element stoichiometry is constrained
across ecosystems worldwide (Cleveland and Liptzin
2007). For example, the global mean (? standard error)
microbial carbon to phosphorus molar ratio in forest
soils is 74.0?6.2, while the mean microbial nitrogen to
phosphorus molar ratio is 8.9?0.8 (data from Table 1 in
Cleveland and Liptzin 2007). For all soils along the
Franz Josef chronosequence, the mean microbial carbon
to phosphorus molar ratio was 36.2?2.8 and the mean
microbial nitrogen to phosphorus molar ratio was 5.9?
0.7. Although there are few comparable data on soil
microbial nutrients in the Franz Josef region, a study
of organic and surface mineral soils supporting native
Nothofagus forest in New Zealand reported microbial
nitrogen to phosphorus molar ratios < 5 (Sparling et al.
1994). Our values therefore indicate that the microbial
biomass along the Franz Josef chronosequence is rela-
tively rich in phosphorus compared to forest soils world-
wide, but is similar to at least one other site under native
forest in New Zealand. This hints at persistent nitrogen
limitation of soil microbes throughout ecosystem devel-
opment in New Zealand temperate rain forests.
There have been three previous assessments of
microbial phosphorus concentrations along soil chro-
nosequences. Lajtha and Schlesinger (1988) studied a
sequence of Aridisols ranging in age from ~1000
to > 25,000 years old in the Basin and Range
physiographic province in the Southwestern United
States. However, microbial phosphorus concentrations
determined by chloroform fumigation and anion-
exchange resins were small and variation along the
sequence was not reported. Torn et al. (2005) studied a
series of soils developed on basaltic lava on the
Hawaiian Islands ranging from 300 to 4.1 million years
old. Microbial phosphorus concentrations peaked after
150,000 years in both organic and mineral soil horizons,
Table 1 Phosphorus pools (g P m-2) in plants and soils along the Franz Josef post-glacial chronosequence, New Zealand
Surface
agea
Profile
numberb
Plant biomass P Soil (profile to 75 cm including the organic horizon)
Years
Wood Leaf Root Total Total
Pc
Total P
(>2 mm)
Total P
(<2 mm)
Apatite
(<2 mm)
Secondary P
(<2 mm)
Organic P
(<2 mm)d
Microbial P
(<2 mm)
5 I 0.07 0.34 0.10 0.51 1292.0 1177.0 115.0 108.0 5.2 1.7 0.14
1000 LW1 1.17 0.41 1.04 2.62 753.0 558.0 194.2 109.6 31.1 46.8 6.66
12000 M1 2.48 0.25 2.18 4.90 229.0 59.0 169.6 19.5 90.4 49.4 10.31
120000 Ok2 0.49 0.19 0.45 1.13 76.0 18.0 58.0 0.0 25.7 28.4 3.89
a Year five is equivalent to year zero in Walker and Syers (1976)
b Profile numbers are from Stevens (1968)
c Including stones >2 mm
d Soil organic phosphorus does not include microbial phosphorus
Table 2 Proportional distribu-
tion of total and microbial phos-
phorus by organic versus
mineral soil horizons for four
key stages along the Franz Josef
chronosequence, New Zealand
Surface age Total P (% of total profile P) Microbial P (% of microbial P in profile)
Years Organic horizon Mineral soil Organic horizon Mineral soil
5 0 100 0 100
1000 0.6 99.4 7.4 92.6
12000 4.0 96.0 26.4 73.6
120000 1.9 98.1 8.0 92.0
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and then declined in older soils. However, values were
not corrected for phosphate fixation, which might have
contributed to the low values on the oldest and presum-
ably most strongly phosphorus-fixing soils, particularly
given the long fumigation times used in that study (36?
48 h). Lagerstr?m et al. (2009) studied microbial bio-
mass in soils along the Swedish Islands sequence, in
which fire frequency is determined by island size,
resulting in ?younger? soils on larger islands that
burn less frequently and ?older? soils on small
islands that burn rarely. Microbial phosphorus con-
centrations were between 298 and 545 mg P kg-1,
with highest concentrations on intermediate-sized
islands, and microbial nitrogen to phosphorus ratios
were < 4 on a molar basis. Together with our data
for the Franz Josef chronosequence, these results
suggest a consistent pattern of change in microbial
phosphorus during pedogenesis under a range of
geological and climatic conditions.
The studies discussed above did not determine
pools of phosphorus in microbes and plants, so we
cannot assess whether the dominance of the microbial
phosphorus pool observed at Franz Josef also occurs
along other chronosequences. However, the generality
of the phenomenon is hinted at by a simple calculation
based on global estimates of plant and microbial phos-
phorus. Combining the global estimate of soil micro-
bial carbon of 13.9 Gt (Wardle 1992, p. 341) with the
global mean carbon to phosphorus ratio in microbial
biomass of 23.1 on a mass basis (Cleveland and Liptzin
2007) yields a global microbial phosphorus estimate of
0.60 Gt. Comparing this with the global estimate of
plant phosphorus of 0.39 Gt (Wang et al. 2010)
indicates that the global microbial phosphorus pool
is 54 % greater than the global plant phosphorus
pool and accounts for 60 % of the total biomass
phosphorus. Although this calculation requires further
verification, it does suggest that our findings are
broadly applicable to ecosystems worldwide.
The quantitative importance of the microbial phos-
phorus pool in even moderately aged ecosystems indi-
cates that microbes must play a far greater role than
previously recognized in regulating phosphorus dynam-
ics during ecosystem development. First, microbes,
including symbiotic mycorrhizal fungal associations
with plant roots, promote phosphorus availability
through apatite weathering (Blum et al. 2002; Smits et
al. 2012) and recycling from decaying organic matter
(Magid et al. 1996; Smith and Read 2008). Phosphorus
sequestered in microbial tissue subsequently becomes
available to other microbes and plants following cell
death. The large size of the microbial phosphorus pool,
coupled with the rapid turnover time of soil microbial
phosphorus (i.e. ~40 days for temperate agricultural
soils; Kouno et al. 2002), suggests that it is an increas-
ingly important source of plant-available phosphorus as
soils age.
Second, microbes determine the long-term fate of
phosphorus in ecosystems by influencing the rate of
soluble phosphorus loss in runoff. Microbes conserve
phosphorus by converting it into organic forms in their
tissue, particularly during the early period of pedogen-
esis when there is greatest overall loss of phosphorus
a
M
ic
ro
bi
al
 C
 (m
g 
C 
kg
-
1 )
0
1000
2000
c
M
ic
ro
bi
al
 P
 (m
g 
P 
kg
-
1 )
0
100
200
300
d
Soil Age (Years)
101 102 103 104 105 106
El
em
en
t r
at
io
 (m
o
la
r)
0
20
40
60 Microbial C:P
Microbial N:P
b
M
ic
ro
bi
al
 N
 (m
g 
N 
kg
-
1 )
200
400
Fig. 2 Soil microbial carbon (a), nitrogen (b), and phosphorus
(c), and the molar ratios of carbon and nitrogen to phosphorus
(d) in mineral soil (0?10 cm) at nine sites along the Franz Josef
chronosequence, New Zealand. Values are the mean ? standard
error of five replicate samples at each site
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from the ecosystem. However, microbes may promote
phosphorus loss by enhancing weathering (see above)
and via leaching of organic phosphorus; many organic
phosphorus compounds are more mobile in soil than
inorganic phosphate (Frossard et al. 1989) and are
released from microbial cells following cycles of wet-
ting and drying or freezing and thawing (Turner and
Haygarth 2001; Blackwell et al. 2010).
Finally, the disparity between the amounts of phos-
phorus in plants and microbes in the late stages of the
Franz Josef chronosequence indicates the likelihood of
intense competition for available phosphorus between
autotrophs and saprotrophs in mature soils. This might
be expected to increasingly influence the composition
of plant communities through time by favoring species
with root symbiotic associations adapted to acquire
phosphorus from the organic and recalcitrant inorganic
forms of phosphorus that dominate the total phospho-
rus pool in strongly-weathered soils (Lambers et al.
2008; Turner 2008). For example, plants species form-
ing arbuscular mycorrhizas, typical of the majority of
land plants and adapted to efficiently scavenge soluble
phosphate (Smith and Read 2008), would be expected
to decline as ecosystem development proceeds. In
contrast, plant species capable of forming ericoid my-
corrhizas, which can use a variety of organic phospho-
rus forms including nucleic acids (Leake and Miles
1996), or plant species that form cluster roots, which
are extremely efficient at acquiring phosphorus from
infertile soils (Lambers et al. 2008), would be
expected to increase in abundance on old soils where
competition for phosphorus with microbes is intense.
This is consistent with the abundance of members of
the Ericaceae and Proteaceae on ancient landscapes,
such as the kwongan of Western Australia and the
fynbos of South Africa (Lambers et al. 2010).
Furthermore, the progressive loss of phosphorus from
soils as ecosystems age may have driven plants and
mycorrhizas to evolve more effective mechanisms of
mineral weathering and phosphorus recycling. For ex-
ample, there is evidence that mineral weathering has
progressively increased with advancement from arbus-
cular mycorrhizal to later independently-evolved ecto-
mycorrhizal fungi, and from gymnosperm to angiosperm
hosts with both fungal groups (Quirk et al. 2012). This
has far-reaching consequences for global biogeochemi-
cal cycles, including feed-backs between the geosphere
and atmosphere via the geochemical carbon cycle over
multi-million year timescales (Taylor et al. 2009).
In summary, our results indicate that microbial
biomass can be the dominant biotic phosphorus pool
for > 100,000 years of ecosystem development, far
exceeding the amount of phosphorus in vegetation.
This finding challenges our understanding of phos-
phorus cycling in natural systems and provides a
novel framework for understanding plant?microbe
interactions in space and time. The results are likely
to apply broadly to ecosystems worldwide given the
similarity of changes in phosphorus during pedogen-
esis in contrasting ecosystems (Parfitt et al. 2005;
Peltzer et al. 2010; Turner et al. 2012). They also
have important implications for the development of
sustainable agronomic systems in light of the
impending depletion of rock phosphate reserves for
fertilizer production worldwide (Cordell et al. 2009).
Acknowledgements This manuscript is a product of an ARC?
NZ Network for Vegetation Function workshop held at the
University of Western Australia. We thank V.J. Allison, S.J.
Davies, A.E. Herre, E. Lalibert? and P. Thrall for their
contributions.
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