Download Lack of relationship between below

Journal of
Ecology 2003
91, 532 – 540
Lack of relationship between below-ground competition
and allocation to roots in 10 grassland species
Blackwell Publishing Ltd.
JAMES F. CAHILL JR
Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada
Summary
1 A field experiment in a native grassland in Central Alberta, Canada, tested whether
plants alter relative allocation to roots vs. shoots in response to below-ground competition, and whether the mass of a species’ root system accounts for interspecific
differences in below-ground competitive response.
2 Seedlings of each of 10 native species were transplanted into the naturally occurring
vegetation in the field at the start of the growing season. Root interactions between the
target plants and their neighbours were manipulated through the use of PVC root exclusion tubes, with target plants grown with or without potential root interactions with
their neighbours. Neighbour shoots were also tied back, forcing any target–neighbour
interactions to be below ground.
3 Below-ground competition generally reduced plant growth, with its relative magnitude
varying among species.
4 An allometric analysis indicated that competition below ground did not result in an
increase in the relative biomass allocated to roots for any of the 10 target species. This
is counter to the growth-balance hypothesis (and optimal foraging theory). Belowground competition did increase root : shoot ratios, but this was due to reduced plant
size (small plants have larger root : shoot ratios), rather than adaptive plasticity.
5 A species’ below-ground competitive ability was not related to its root system
size. Although this finding is counter to commonly made assumptions, it is supported by
other work demonstrating below-ground competition to be generally size-symmetric.
6 Despite the majority of plant–plant interactions in grasslands being below ground,
our understanding of plant competition above ground is significantly more robust.
Several wide-spread assumptions regarding below-ground competition are suspect, and
more multispecies studies such as this are required to provide a fuller picture of how
plants respond to, and compete for, soil resources.
Key-words: balanced-growth hypothesis, below-ground competition, community
ecology, growth allometry, size-symmetric competition
Journal of Ecology (2003) 91, 532–540
Introduction
Competition for soil resources is often as strong or
stronger than competition for light (Casper & Jackson
1997). Although competition reduces individual
plant growth regardless of whether it is for light or soil
resources, the mechanisms by which plants compete,
how plants respond to competition, and how the
strength of competition varies in natural communities,
is different for above- and below-ground resources
(Casper & Jackson 1997). Although we can make
sweeping statements about below-ground competition
© 2003 British
Ecological Society
Correspondence: James F. Cahill Jr (fax +1780 4929234,
e-mail [email protected]).
in general, the detail of our understanding of the ecological consequences of and morphological responses
to below-ground competition in natural communities
is limited.
For example, little is known about how plants
change biomass allocation patterns in response to
below-ground competition. Many plants respond to
shading by other plants by changing shoot architecture
and biomass allocation (Schmitt & Wulff 1993; Aphalo
et al. 1999), and can alter root : shoot ratios (Reynolds
& Antonio 1996), root architecture (Fitter & Stickland
1991) or uptake capacity (Jackson & Caldwell 1991) in
response to low soil resource availability. Plants can also
alter fine root growth in response to the presence of neighbouring plants (Gersani et al. 2001), and competition
533
Root allocation and
below ground
competition
in general can alter plant rooting depths (Wardle &
Peltzer 2003). Studies describing changes in root allocation specifically in response to below-ground competition are rare. Wilson & Tilman (1995) found
root : shoot ratios increased with below-ground
competition, inferring it to be an adaptive response.
However, increased root : shoot ratios can be due
ontogenetic shifts, rather than adaptive plasticity
(Gedroc et al. 1996; McConnaughay & Coleman 1999;
Muller et al. 2000; but see Shipley & Meziane 2002),
and increased root : shoot plasticity is not consistently
related to competitive ability (Reynolds & Antonio
1996). To date, no study has separated these aspects,
and such information is critically important to our
understanding of below-ground competition in natural
communities.
The effects of below-ground competition on individual plant growth are easily measured, and generally
vary among species (Wilson & Tilman 1995), yet little
is known about which plant traits make different species effective competitors below ground. Much as it has
been assumed that plants will increase root allocation
in response to root competition, it has also been
assumed that root system size is positively associated
with below-ground competitive ability (e.g. Tilman
1988; Wilson & Tilman 1995; Rajaniemi 2002). However,
empirical support for this idea is limited (e.g. Aerts
et al. 1991). Casper & Jackson (1997) suggest a variety
of reasons why root abundance alone may not be
a good indicator of below-ground competitive ability,
including: (i) higher root densities can result in
increased competition within a single plant’s root system; (ii) root location may matter more than amount;
(iii) mycorrhizas may be very important to resource
capture; and (iv) uptake kinetics could be crucial to
determining the outcome of below-ground competition. Evidence is also accumulating that, in contrast to
competition for light, below-ground competition is
size-symmetric (Weiner et al. 1997; Cahill & Casper
2000; Blair 2001; von Wettberg & Weiner in press). As
a result, the growth consequence of below-ground
competition should be directly, but not disproportionately, related to root system size.
In this study, I address two questions essential for a
mechanistic understanding of plant competition. (i)
Do plants alter relative allocation to roots vs. shoots in
response to below-ground competition? (ii) Does the
mass of a species’ root system account for interspecific
differences in below-ground competitive response?
These questions were investigated through measures
of root and shoot biomass of target plants in a field
experiment in a rough fescue grassland in central
Alberta, Canada. Target plants consisted of individuals
of 10 native species, grown either with or without
interactions with neighbouring roots.
Materials and methods
    
The experiment was conducted from May to August
2001 within the 3200 ha Kinsella Beef Cattle Research
Ranch, in Alberta, Canada (53° N, 111° W). The field
site has never been seeded or tilled, and is grazed annually in the fall by cattle. Vegetation is primarily graminoid, dominated by Festuca hallii, Stipa curtiseta and
Koeleria macrantha. Common forbs include Achillea
millefolium, Comandra umbellata and Solidago missouriensis. Species nomenclature follows that of Moss &
Packer (1994), except for Festuca hallii and Helianthus
petiolaris, which follow that of the USDA PLANTS
Database (USDA, NRCS 2001). Woody plants are
present (e.g. Rosa arkansana), but contribute little to
standing biomass. Over 60% of the phytomass in this
system is below ground, mostly in the upper 20 cm of
soil (Cahill, personal observation). Annual precipitation during the study year was 57% below the 27-year
average (average = 322 mm), and precipitation the
winter preceding this study was 90% below average.
Individuals of 10 native species were used as target
plants (Table 1), with seed obtained from field collections and local native seed suppliers. Seed was sown
into glasshouse flats (72 cells per flat) on 1 April (Festuca, Geum, Potentilla) and 19 April (Achillea, Galium,
Agoseris, Coreopsis, Linum, Kohleria, Helianthus), and
placed in a growth chamber (16L:8D; 20 °C). Seedlings
Table 1 Target species used during this study. Nomenclature follows that of Moss & Packer (1994), except for Festuca hallii and
Helianthus petiolaris, which follow that of the USDA PLANTS Database (USDA, NRCS 2001). Species codes are used in all
figures
© 2003 British
Ecological Society,
Journal of Ecology,
91, 532–540
Species
Species code
Family
Life history
Achillea millefolium L.
Agoseris glauca (Pursh) Raf.
Coreopsis tinctoria Nutt.
Helianthus petiolaris Nutt.
Festuca hallii (Vasey) Piper
Kohleria macrantha (Ledeb.) J. A. Schultes f.
Linum lewisii Pursh
Geum triflorum Pursh
Potentilla pensylvanica L.
Galium boreale L.
Ac
Ag
C
H
F
K
L
Ge
P
Ga
Asteraceae
Asteraceae
Asteraceae
Asteraceae
Gramineae
Gramineae
Linaceae
Rosaceae
Rosaceae
Rubiaceae
Perennial
Perennial
Annual
Annual
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
534
J. F. Cahill Jr
were thinned to one individual per cell, and all flats
were placed outside at the field site 1 week prior to
transplantation.
 
© 2003 British
Ecological Society,
Journal of Ecology,
91, 532–540
Ten 9 × 16 m blocks were established throughout a 20ha area of native grassland at the ranch. Each block was
divided into a 2 × 5 array of 10 plots (2 × 3 m each),
with 1 m separating plots and six individuals of one
randomly selected species transplanted into each plot.
Within each plot, seedlings were arranged in a 3 × 2 array,
with each seedling separated by 1 m from the nearest
other transplanted seedling. The original design of this
experiment involved each of these individuals receiving
one of six treatments (manipulating below-ground
competition, shoot competition, and potential hyphal
growth). However, the drought resulted in the shoot
competition and fungal growth treatments being abandoned during the growing season, and they will not be
discussed further. This paper deals specifically with two
of the six individuals of each of 10 species in each of 10
blocks, comparing plants grown with root interactions
with those grown without root interactions.
Root interactions between the target plants and their
neighbours were manipulated through the use of 15-cm
diameter × 20-cm lengths of PVC pipe (‘root exclusion
tubes’). On 7–9 May 2001, the exclusion tubes were
installed by digging two holes in each plot and placing
a tube into one hole (– roots treatment), but not the
other (+ roots treatment). Large roots were removed
from the excavated soil, the holes were refilled, and the
naturally occurring vegetation surrounding the holes
was left intact. On 15 May 2001, seedlings of the appropriate species were transplanted into each plot. Transplanting consisted of making a small depression in the
soil, either in the centre of the tube or in the hole without a tube, and inserting one seedling. The seedlings
were watered daily for 7 days, at which time any dead
individuals were replaced.
Root and shoot competition can have non-additive
effects on plant growth (Cahill 1999, 2002a). As this
study was specifically focused on below-ground competition, the potentially confounding effects of shoot
competition were eliminated as advocated in Cahill
(2002b). Shoot competition between neighbours and
target plants was prevented by using thin tree netting
(2 × 2 cm squares, 1 mm thick netting) to tie back the
shoots of the neighbouring vegetation. A 50 × 50 cm
square of netting was centred over each target plant,
anchored such that its centre was flush with the ground.
The four corners were then staked 15 cm above the soil
surface and the neighbouring vegetation pulled away
from the target plant and towards the netting edges.
The netting is similar in diameter to fishing line, casting
little shade (93% light penetration). Similar netting has
been used in other studies without adverse effects
on neighbouring vegetation (Wilson & Tilman 1991;
Twolan-Strutt & Keddy 1996; Cahill 1999, 2002a).
Repeated measures of morphological traits (e.g. height)
can alter the intensity of herbivory (Cahill et al. 2001),
above-ground biomass production (Hik et al. 2003),
and relative biomass allocation within a plant (Cahill
et al. 2002). As a result, non-destructive measures
were not taken during this experiment and, on 20
August 2001, all target plants were harvested. Harvest
consisted of cutting each plant at the soil surface and
extracting the root systems from the soil. Roots were
then washed free of soil, and the roots and shoots were
dried separately at 70 °C and weighed. It is not possible
to fully extract root systems from the field, particularly
when target plant roots are entangled with those of the
neighbouring vegetation (Cahill 2002b). At a minimum, the tap root (when present) and larger roots of all
target plants were recovered here. Though the excavations failed to recover some unknown proportion of
the fine roots that are likely to contribute most to root
length, they were successful in recovering the majority
of the larger roots that contribute most to root biomass
(Smit et al. 2000).

The effects of root interactions and species identity on
target plant mortality were analysed using a generalized linear mixed model (GLMM). Specifically, plant
status (living or dead) served as a binomially distributed response variable, with species identity and root
exclusion treatment as fixed effects, and block, block
× species, block × treatment, and block × species ×
treatment, as random effects in the model. All analyses
were conducted using SAS v8.0 (SAS 1999), with the
%GLIMMIX macro in PROC MIXED allowing use of
binomially distributed data (Littel et al. 1996). The
effects of root exclusion and species identity on target
plant biomass were analysed using a similar statistical
model, with the exception being that the response
variable (Ln(total biomass)) was normally distributed
and %GLIMMIX was not used.
There is no consensus on the best way to analyse
questions of plant allometry (Muller et al. 2000), and
thus I used a linear modelling approach similar to that
used in related studies (Muller et al. 2000; Shipley &
Meziane 2002). The effects of species identity and root
exclusion on the relative allocation to roots were determined using a GLMM, with Ln(root biomass) as the
response variable and Ln(shoot biomass) as a covariate. A significant root exclusion effect would indicate a
difference in relative biomass allocation to roots as a
function of below-ground competition, independent of
any allometric shift in root : shoot ratios (i.e. evidence
of adaptive plasticity). An additional analysis was conducted to determine whether there were any covariate
× fixed effect (e.g. root exclusion) interactions, which
would indicate that the root exclusion treatment alters
relative allocation to roots in a size-dependent manner.
To determine whether a species’ below-ground competitive ability was related to its root system size, a
535
Root allocation and
below ground
competition
GLM was conducted. Mean Ln(shoot biomass) for
each species served as the dependent variable (n = 10
species), the root exclusion treatment was a fixed effect,
and root system biomass served as a covariate. Root
system biomass for each species was measured as the
mean root biomass of all individuals of that species
when grown without below-ground competition. This
approach provides a measure of potential root biomass
during this experiment, rather than a theoretical
maximum that would be provided from glasshouse
studies or herbarium specimens. The strength of belowground competition is indicated as the difference in
shoot biomass between the +/– roots treatments. If this
difference changes as a function of root system size it
would indicate that below-ground competitive ability is
influenced by root system size. This would be indicated
as a significant covariate × root exclusion interaction in
the GLM. Total biomass could not be used as the
response variable in this analysis as there would have
been shared data in both axes, a factor that can cause
spurious correlations (Jackson & Sonners 1991).
Results
The root exclusion tubes were effective in preventing
neighbour root growth around the target plants and reducing root competition, as evidenced by lower neighbour
root densities (Cahill, personal observation) and higher
soil moisture (HydroSense Soil Water Measurement;
Campbell Scientific, Edmonton, Canada; mean ± SD:
exclusion tube 11.00 ± 2.64, no tube 7.65 ± 1.63, F1,9 = 22.43;
P = 0.001) inside the exclusion tubes than outside the
tubes. There was no visual evidence that the tubes restricted
target plant root growth, and the largest root system of
any target plant was 0.74 g by dry weight (41 g m−2 within
the exclusion tube) while standing root biomass outside
of the tubes was 20× higher (mean ± SD: 905 ± 350 g m−2).
,    

© 2003 British
Ecological Society,
Journal of Ecology,
91, 532–540
Mortality varied among species, but was not affected
by root exclusion or the species × root exclusion interaction (Fig. 1a; species F9,81 = 2.43, P = 0.017; root exclusion F1,9 = 0.16, P = 0.695; species × root F9,81 = 0.61,
P = 0.786). Although the species × root exclusion
treatment was not significant, visual inspection suggests that mortality of some species (e.g. Festuca) was
more strongly influenced by root exclusion than others.
Separate chi-square for each species failed to detect any
significant differences in mortality as a function of root
exclusion for any of the 10 species (all P > 0.20).
The effects of root exclusion on target plant biomass
varied among species (Table 2; Fig. 1b). Neighbour
roots reduced biomass for most species, though only
four of the 10 species showed a significant effect in
posthoc tests (Fig. 1b). For only one species (Festuca)
was there a trend towards higher biomass in the + roots
than the – roots treatment (P = 0.22).
Fig. 1 (a) Plant mortality as a function of species identity and
the root exclusion treatment. Y-values represent the proportion of target plants that were dead at the end of the study.
(b) Total plant biomass as a function of species identity and
the root exclusion treatment. Asterisks indicate significant
differences between the + roots and – roots treatment for
a given species (posthoc comparison P < 0.05). In both panels,
black colouring corresponds to the + roots treatment and
grey shading corresponds to the – roots treatment (root
exclusion).
Table 2 GLMM results for the analyses of total plant
biomass and relative biomass allocation to roots. In both
models, block was treated as a random factor, and species
identity and root exclusion treatment served as fixed effects.
As quantifying variation among blocks was not a goal of this
study, the significance of block effects is not presented. In the
latter analysis, Ln(root biomass) served as the response
variable, with Ln(shoot biomass) as the covariate. No factor ×
covariate interactions were significant (P > 0.25), meeting
that assumption of . d.f. in both analyses were calculated using Satterthwaite’s’s method (Littel et al. 1996)
Ln(total biomass)
Factor
FDF
Ln(root biomass)
P-value FDF
P-value
Ln(shoot biomass) –
–
63.221, 98.4 < 0.001
Species
8.579, 67.1 < 0.001 5.389, 93.3 < 0.001
Treatment
16.341, 81.7 < 0.001 0.731, 24.6
0.402
0.62
Species × treatment 2.989, 56.3
0.778
9,
92.9
0.006
Relative allocation to root biomass varied among
species but was not affected by root exclusion (Table 2,
Fig. 2a) nor were there any significant covariate × factor
(e.g. root exclusion treatment, species) interactions (all
× root exclusion treatment interaction (F9,94 = 0.34; P =
0.960).
536
J. F. Cahill Jr
  - 

When using average values for each of the 10 species,
root and shoot biomass were correlated across species
(F1,17 = 15.36; P < 0.01), and root interactions reduced
target shoot biomass (F1,17 = 5.68; P = 0.029; Fig. 2b),
both supporting results of prior analyses (Figs 1b and
2a). However, the size of a species’ root system had no
impact on the strength of below-ground competition,
as evidenced by homogeneity of slopes in the GLM
(root biomass × root exclusion treatment F1,16 = 0.36;
P = 0.557; Fig. 2b).
Discussion
Fig. 2 (a) Ln(root biomass) as a function of Ln(shoot
biomass) and the root exclusion treatment. Root and shoot
biomass are correlated in both treatments (+ roots R2 = 0.23,
P < 0.001; – Roots R2 = 0.48, P < 0.001), and the slope of the
lines did not differ as a function of species identity or root
exclusion treatment (Table 2). (b) Relative effects of belowground competition as a function of the target species’ root
system size. Root system size was measured as mean biomass
of those plants grown without root interactions with
neighbours. Competition can be seen as the difference in mean
shoot biomass between those plants grown with and without
root interactions. Mean root and shoot biomass were
correlated across species (+ roots R2 = 0.43, P < 0.01; – Roots
R2 = 0.52, P < 0.01), and the homogeneity of slopes indicates
the relative strength of root competition is independent of a
species’ root biomass (Ln(root) × treatment interaction,
P > 0.05). In both panels, letters indicate which species that
point represents, black colouring corresponds to the + roots
treatment and grey shading corresponds to the – roots
treatment (root exclusion). Species codes are listed in Table 1.
© 2003 British
Ecological Society,
Journal of Ecology,
91, 532–540
P > 0.25). The lack of an allocation response to belowground competition was consistent among species, as
evidenced by no significant species × root exclusion
interaction. Additionally, in separate analyses for each
of the 10 plant species, allocation to roots still did not
vary as a function of the root exclusion treatment (all
P > 0.10), nor were there any root exclusion × covariate
interactions (all P > 0.05) for any species. Although
there was no shift in biomass allocation in response
to below-ground competition when analysed using an
allometric approach, root : shoot ratios themselves
did decrease with below-ground competition (F1,19.3 =
5.34; P = 0.032). This response was consistent among
species, as evidenced by the lack of a significant species
When neighbouring roots altered target plant growth,
their effects were generally negative (Fig. 1b). Four of
the 10 target species showed a significant effect of
below-ground competition on plant growth, and 9
of the 10 species had a trend in that direction (Fig. 1b).
These results are consistent with prior studies, with
Gerry & Wilson (1995) and Cahill (2002a) finding no
evidence of facilitation through root interactions for
any of their 10 species, and Wilson & Tilman (1995),
who found only trends towards facilitative effects and
even then for only two of the eight species in their
undisturbed plots. There appear to be no widespread
net facilitative effects of root interactions in these terrestrial herbaceous plant communities, although facilitation could still occur via interactions with plant
shoots. Festuca hallii, however, had trends towards
both reduced mortality and increased growth in the
presence of neighbour roots. The consistency of these
results warrants further investigation on the nature of
biotic interactions involving this species, as it is a dominant member of this community.
    
     -

Root : shoot ratios increased with below-ground competition, though this was due to changes in plant size,
rather than an adaptive response to below-ground
competition (Table 2, Fig. 2a). Demonstrating increased root : shoot ratios with below-ground competition is not new (Wilson & Tilman 1995), though
prior studies have not differentiated between adaptive
plasticity and ontogenetic responses (sensu Gedroc
et al. 1996; McConnaughay & Coleman 1999; Muller
et al. 2000).
Variation in root allocation as a function of plant
size rather than in response to limiting resources, is
counter to the balanced-growth hypothesis, which is
built into many models of competition and community
537
Root allocation and
below ground
competition
© 2003 British
Ecological Society,
Journal of Ecology,
91, 532–540
organization (e.g. Tilman 1988; Reynolds & Pacala
1993). The balanced-growth hypothesis states that
plants preferentially allocate resources to the organs
responsible for acquiring the most limited resource
(Shipley & Meziane 2002). In this study soil resources
were limiting (Fig. 1b), and yet there was no increase in
root allocation in response to below-ground competition. Although Muller et al. (2000) also rejected the
balanced-growth hypothesis, Shipley & Meziane
(2002) found support for it in their study of 22 plant
species, and suggest four reasons to explain the differing results: (i) greater statistical power; (ii) Muller
et al. (2000) ran their study for 4 months vs. 35 days for
Shipley & Meziane (2002); (iii) Shipley & Meziane (2002)
used a more frequent, and thus temporally homogeneous, supply of resources; and (iv) there may have been
competition in the study by Muller et al. (2000). Here,
competition did not alter root allocation (Fig. 1c),
rejecting argument (iv). The fact that both this study
and that of Muller et al. reached similar answers suggests this is not due to statistical power alone. This
study was also longer than Shipley & Meziane’s (2002),
and field conditions certainly result in temporally
heterogeneous resource supply. In a greenhouse study
using a fertilization regime similar to Muller et al.
(2000), Gedroc et al. (1996) found plasticity in rootshoot allocation was greatest for very young plants,
and root : shoot ratios in low and high resource conditions converged as the plants aged. This suggests that
the age of harvest used by Shipley & Meziane (2002) is
more likely to support the balanced-growth hypothesis
than that used by Muller et al. (2000) and here. It is
clear that under certain circumstances, plants can alter
root-shoot allocation in response to environmental
conditions. The more important question that remains
is whether any such shifts in allocation, no matter how
short term, confer any advantage. This is a decidedly
more difficult question to answer, and one for which we
have little information.
Plants possess a variety of mechanisms by which
they can perceive the presence of neighbouring roots,
and neighbouring roots can influence root distributions (Mahall & Callaway 1992; Brisson & Reynolds
1994; Gersani et al. 2001). Results from this study suggest that such information does not alter the total
amount of carbon going to the root system, although it
could allow for fine-scale adjustments as to where the
roots are placed. Such a response parallels that of shoot
competition, where natural shading does not necessarily change the proportion of plant biomass that is in the
shoots, but can alter relative allocation between stems
and leaves (Casper et al. 1998). Together, these findings
suggest that whole plant allocation patterns, though
variable among species and as a function of plant size,
are not nearly as plastic as is often argued. As roots
serve functions other than resource capture (e.g. structural support and storage) it is likely that adjustments
made in response to below-ground competition are
more subtle than patterns of whole plant biomass
allocation. This argument is supported by the findings
that young plants do seem to have more biomass plasticity than do older plants (Gedroc et al. 1996), as it
is sensible that the roots of seedlings are primarily
responsible for anchorage and uptake, and not nutrient
storage. As plants mature, root weight becomes concentrated in the larger storage roots, and thus root biomass
is likely to be a reasonable indicator of below-ground
foraging effort for juvenile, but not older, plants.
     ’  
   
 - 

A species’ root system size was not a predictor of its
below-ground competitive response (Fig. 2b), and one
cannot assume that increased allocation to roots will
increase below-ground competitive ability (e.g. Wilson
& Tilman 1995; Rajaniemi 2002). What factors actually confer competitive advantage below ground are
unknown, although there is reason to believe it should
not be biomass. There is growing evidence that belowground competition is size-symmetric, with the effects
of neighbour roots on target plant growth being proportional to their abundance (Gerry & Wilson 1995;
Weiner et al. 1997; Cahill & Casper 2000; Blair 2001;
von Wettberg & Weiner in press). Under size-symmetric
competition, a plant’s relative competitive ability below
ground should be independent of its root biomass,
as found here (Fig. 2b). Comparative studies of competition in general have found contradictory results
regarding the effects of plant mass on competitive
ability (Gaudet & Keddy 1988; Wardle et al. 1998). As
there is no clear consensus on whether certain traits
make a good competitor in general, it is not too surprising that this study provides no support for the
idea that root biomass confers greater below-ground
competitive ability.
We are left with a rather interesting puzzle. We know
that species vary in their below-ground competitive
ability (Gerry & Wilson 1995; Wilson & Tilman 1995;
Twolan-Strutt & Keddy 1996; Cahill 2002a), and this is
apparently not due to differences in root allocation
(Fig. 2b). Though we can refute one potential explanation,
an understanding of what factors lead to interspecific
variation in below-ground competition is lacking. I
propose there are three main sets of plant traits that
influence a plant’s below-ground competitive ability:
• Root traits. Some traits that influence below-ground
competitive ability will be a function of the root system
itself. For example, recent work with Arabidopsis thaliana indicates that root hairs enhance competitive
ability under low, but not high P conditions (Bates &
Lynch 2001). Importantly, root hairs do not increase
anchorage (Bailey et al. 2002), indicating that a functional analysis of plant roots will require experimental
separation of the different roles of root systems (anchorage, support, uptake). Numerous other root traits have
538
J. F. Cahill Jr
© 2003 British
Ecological Society,
Journal of Ecology,
91, 532–540
been suggested or demonstrated to influence belowground competitive ability, including (but not limited
to) root proliferation (Robinson et al. 1999), root
architecture (Rubio et al. 2001), and uptake kinetics
(Caldwell et al. 1991). For the most part, studies linking
specific root traits with below-ground competitive ability
are lacking, and we know much less about the functional
ecology of roots than of leaves (Pregitzer et al. 2002).
• Shoot and whole plant traits. Above- and belowground competition interact to affect plant growth
(Cahill 1999, 2002a), and thus traits that influence
above-ground competitive ability may also alter belowground competitive ability. For example, if belowground competitive ability is somehow related to C
supply to the roots, then a plant’s ability to compete for
light (and acquire C) will influence its below-ground
competitive ability. Similarly, overall rates of water
extraction are related to competitive ability among
desert grasses (Eissenstat & Caldwell 1988). Water
extraction is not a specific trait itself, but instead is
influenced by a variety of factors including phenology,
root length and transpiration rates. Studies designed to
specifically contrast traits associated with above- and
below-ground competition are lacking, and would be a
significant step forward in our understanding of not
only the similarities and differences between these two
key ecological processes, but also the general mechanisms of plant–plant interactions.
• Traits related to other ecological processes. An individual plant’s ability to compete below ground is likely
to be determined not only by traits internal to that individual, but will also include traits related to how a plant
uses, and is used by, other species. For example, grazing
by ungulates can stimulate root growth (Frank et al.
2002), and root characteristics vary widely as a function of root order (Pregitzer et al. 2002). As a result,
grazing may alter below-ground competitive ability
through changes in root architecture and other related
root properties. As different plant species respond differently to grazing (Diaz et al. 2001), grazing could
cause increased interspecific variation in below-ground
competitive ability of the species within a community.
Such indirect effects on below-ground competition
may also involve plant–fungal interactions. Interspecific variation in mycorrhizal associations, along with
the potential for resource sharing of interconnected
individuals, can alter diversity (Hartnett & Wilson
1999), potentially through altered competitive hierarchies. Additionally, recent work indicates that
mycorrhizas can enhance the competitive ability of an
invasive species (Marler et al. 1999). There are numerous other ecological processes that are likely to influence a plant’s ability to compete for soil resources.
Although a better understanding of plant competition
is dependent upon a more active exploration of the
functional ecology of roots, it is equally important that
this work be brought to the field to allow for the determination of the potential strengths of these indirect
effects on competition below-ground.
   
There are two components to plant competition:
response and effect (Goldberg 1990). Target plant
studies, such as this one, measure the growth of individuals that are interacting with many neighbouring
plants (competitive response). Other experimental
designs determine how one species alters resource supply and the growth of other species (competitive effect).
As different traits may be associated with competitive
response and effect (Goldberg & Landa 1991), the
results here are limited to competitive response.
If the ability to extract roots from the soil differs as a
function of the root exclusion treatment, one will
recover proportionally fewer target roots in the + roots
treatment than in the – roots treatment (Cahill 2002b).
Although I found no evidence of a shift in root allocation as a function of the root treatment, it is possible
that there may have actually been increased allocation in response to below-ground competition, with
reduced root extraction in the + roots treatment
obscuring the detection of the pattern. It is therefore
important to explore the potential impact of systematic
bias in extraction efficiencies. As the magnitude of root
loss during extraction is unknown, I went back to the
raw data and artificially increased the root biomass of
the + roots target plants in 5% increments. After each
increase, I reran the GLMM looking to see at what
point the root exclusion treatment was significant in its
effects of root allocation. The root biomass of the
+ roots plants would have to increase between 25 and
30% before the root treatment term becomes significant at the P = 0.05 level. It is unlikely that over 25% of
the target root biomass went uncollected, as it is in fact
the larger, stronger and heavier roots that are most reliably recovered (Smit et al. 2000). This suggests the lack
of support for the growth-balance hypothesis found
here is real, rather than an experimental artefact. This
finding also supports my contention that if one is interested in a proxy measure of fitness in a study of belowground competition, measuring solely shoot biomass
may be sufficient (Cahill 2002b). This also appears
to satisfy Zobel & Zobel’s (2002) criteria that ‘Shoot
biomass of perennial plants could easily be used as a
sufficient proxy for root and total biomass responses
only if root/shoot allocation is predictable’.
As above- and below-ground competition interact
to affect plant growth, it was necessary to experimentally isolate the factor of interest – below-ground
competition – through the removal of shading by the
neighbouring plants. Although this is the appropriate
approach for the questions addressed here, it does leave
other questions unanswered. For example, if plants
detect the presence of neighbouring roots by piggybacking on their phytochrome system to detect shoot
competition, then this study would have prevented
them from perceiving such competition. Thus this
study clearly shows that below-ground competition
itself does not cause a shift in root allocation, though
539
Root allocation and
below ground
competition
the combined effects of root and shoot competition
may (Wardle & Peltzer 2003). Understanding both the
individual effects of above- and below-ground competition, as well the mechanisms of root–shoot interactions would seem to be a potentially fruitful way of
understanding the causes and consequences of plant–
plant interactions in natural systems.
Acknowledgements
I thank Malcolm Coupe, Josh Haag, Alexandra
Rutherford and Bryon Shore for assistance in the field,
Barry Irving for facilitating ecological research at the
Kinsella ranch, and Brenda Casper and Duane Peltzer
for comments that improved the quality of this manuscript. Financial support for this research was provided
by a research grant from the Natural Sciences and
Engineering Research Council of Canada.
References
© 2003 British
Ecological Society,
Journal of Ecology,
91, 532–540
Aerts, R., Boot, R.G.A. & van der Aart, P.J.M. (1991) The
relation between above- and belowground biomass allocation
patterns and competitive ability. Oecologia, 87, 551–559.
Aphalo, P.J., Ballare, C.L. & Scopel, A.L. (1999) Plant-plant
signaling, the shade-avoidance response and competition.
Journal of Experimental Botany, 50, 1629–1634.
Bailey, P.H.J., Currey, J.D. & Fitter, A.H. (2002) The role of
root system architecture and root hairs in promoting
anchorage against uprooting forces in Allium cepa and root
mutants of Arabidopsis thaliana. Journal of Experimental
Botany, 53, 333–340.
Bates, T. & Lynch, J. (2001) Root hairs confer a competitive
advantage under low phosphorus availability. Plant and
Soil, 236, 243–250.
Blair, B. (2001) Effect of soil nutrient heterogeneity on the
symmetry of belowground competition. Plant Ecology,
156, 199–203.
Brisson, J. & Reynolds, J.F. (1994) The effect of neighbors on
root distribution in a creosotebush (Larrea tridentata) population. Ecology, 75, 1693–1702.
Cahill, J.F. (1999) Fertilization effects on interactions between
above- and belowground competition in an old field. Ecology, 80, 466 – 480.
Cahill, J.F. (2002a) Interactions between root and shoot competition vary among species. Oikos, 99, 101–112.
Cahill, J.F. (2002b) What evidence is necessary in studies
which separate root and shoot competition along productivity gradients? Journal of Ecology, 90, 201–205.
Cahill, J.F. & Casper, B.B. (2000) Investigating the relationship between neighbor root biomass and belowground
competition: field evidence for symmetric competition
belowground. Oikos, 90, 311–320.
Cahill, J.F., Castelli, J.P. & Casper, B.B. (2001) The herbivory
uncertainty principle: visiting plants can alter herbivory.
Ecology, 82, 307–312.
Cahill, J.F. Jr, Castelli, J.P. & Casper, B.B. (2002) Separate
effects of human visitation and touch on plant growth and
herbivory in an old-field community. American Journal of
Botany, 89, 1401–1409.
Caldwell, M.M., Manwaring, J.H. & Jackson, R.B. (1991)
Exploitation of phosphate from fertile soil microsites by
three Great Basin perennials when in competition. Functional Ecology, 5, 757–764.
Casper, B.B., Cahill, J.F. & Hyatt, L.A. (1998) Above-ground
competition does not alter biomass allocated to roots in
Abutilon theophrasti. New Phytologist, 140, 231–238.
Casper, B.B. & Jackson, R.B. (1997) Plant competition underground. Annual Review of Ecology and Systematics, 28,
545–570.
Diaz, S., Noy-Meir, I. & Cabido, M. (2001) Can grazing
response of herbaceous plants be predicted from simple
vegetative traits? Journal of Applied Ecology, 38, 497–508.
Eissenstat, D.M. & Caldwell, M.M. (1988) Competitive
ability is linked to rates of water extraction; a field study of
two aridland tussock grasses. Oecologia, 75, 1–7.
Fitter, A.H. & Stickland, T.R. (1991) Architectural analysis
of plant root systems. 2. Influence of nutrient supply on
architecture in contrasting plant species. New Phytologist,
119, 383–389.
Frank, D.A., Kuns, M.M. & Guido, D.R. (2002) Consumer
control of grassland plant production. Ecology, 83, 602–606.
Gaudet, C.L. & Keddy, P.A. (1988) A comparative approach
to predicted competitive ability from plant traits. Nature,
334, 242–243.
Gedroc, J.J., McConnaughay, K.D.M. & Coleman, J.S. (1996)
Plasticity in root /shoot partitioning: optimal, ontogenetic,
or both? Functional Ecology, 10, 44 –50.
Gerry, A.K. & Wilson, S.D. (1995) The influence of initial size
on the competitive responses of six plant species. Ecology,
76, 272–279.
Gersani, M., Brown, J.S., O’Brien, E.E., Maina, G.M. &
Abramsky, Z. (2001) Tragedy of the commons as a result of
root competition. Journal of Ecology, 89, 660–669.
Goldberg, D.E. (1990) Components of resource competition
in plant communities. Perspectives on Plant Competition
(eds J.B. Grace & D. Tilman). Academic Press, New York.
Goldberg, D.E. & Landa, K. (1991) Competitive effect and
response: hierarchies and correlated traits in the early
stages of competition. Journal of Ecology, 79, 1013–1030.
Hartnett, D.C. & Wilson, G.W.T. (1999) Mycorrhizae influence plant community structure and diversity in tallgrass
prairie. Ecology, 80, 1187–1195.
Hik, D.S., Brown, M., Dabros, A., Weir, J. & Cahill, J.F.
(2003) Prevalence and predictability of handling effects in
field studies: results from field experiments and a metaanalysis. American Journal of Botany, 90, 270–277.
Jackson, R.B. & Caldwell, M.M. (1991) Kinetic responses of
Pseudoroegneria roots to localized soil enrichment. Plant
and Soil, 138, 231–238.
Jackson, D.A. & Sonners, K.M. (1991) The spectre of ‘spurious’
correlations. Oecologia, 86, 147–151.
Littel, R.C., Milliken, G.A., Stroup, W.W. & Wolfinger, R.D.
(1996) SAS System for Mixed Models. SAS Institute, Cary,
North Carolina.
Mahall, B.E. & Callaway, R.M. (1992) Root communication
mechanisms and intracommunity distributions of two
Mojave Desert shrubs. Ecology, 73, 2145–2151.
Marler, M.J., Zabinski, C.A. & Callaway, R.M. (1999)
Mycorrhizae indirectly enhance competitive effects of an
invasive forb on a native bunchgrass. Ecology, 80, 1180–
1186.
McConnaughay, K.D.M. & Coleman, J.S. (1999) Biomass
allocation in plants: ontogeny or optimality? A test along
three resource gradients. Ecology, 80, 2581–2593.
Moss, E.H. & Packer, J.G. (1994) The Flora of Alberta, 2nd
edn. University of Toronto Press, Toronto.
Muller, I., Schmid, B. & Weiner, J. (2000) The effect of nutrient availability on biomass allocation in 27 species of herbaceous plants. Perspectives in Plant Ecology, Evolution,
and Systematics, 3, 115–127.
Pregitzer, K.S., DeForest, J.L., Burton, A.J., Allen, M.F.,
Ruess, R.W. & Hendrick, R.L. (2002) Fine root architecture
of nine North American trees. Ecological Monographs, 72,
293–309.
Rajaniemi, T.K. (2002) Why does fertilization reduce plant
species diversity? Testing three competition-based hypotheses. Journal of Ecology, 90, 316–324.
540
J. F. Cahill Jr
© 2003 British
Ecological Society,
Journal of Ecology,
91, 532–540
Reynolds, H. & Antonio, C. (1996) The ecological significance of plasticity in root weight ratio in response to
nitrogen: Opinion. Plant and Soil, 185, 75–97.
Reynolds, H. & Pacala, S. (1993) An analytical treatment of
root-to-shoot ratio and plant competition for soil nutrient
and light. American Naturalist, 141, 51–70.
Robinson, D., Hodge, A., Griffiths, B.S. & Fitter, A.H. (1999)
Plant root proliferation in nitrogen-rich patches confers
competitive advantage. Proceedings of The Royal Society of
London Series B. Biology Sciences, 266, 431– 435.
Rubio, G., Walk, T., Ge, Z., Yan, X., Liao, H. & Lynch, J.P.
(2001) Root gravitropism and below-ground competition
among neighbouring plants: a modelling approach. Annals
of Botany, 88, 929–940.
SAS, Inc. (1999) SAS System for Windows. SAS Institute,
Cary, North Carolina.
Schmitt, J. & Wulff, R.D. (1993) Light spectral quality,
phytochrome and plant competition. Trends in Ecology and
Evolution, 8, 47–50.
Shipley, B. & Meziane, D. (2002) The balanced-growth
hypothesis and the allometry of leaf and root biomass allocation. Functional Ecology, 16, 326–331.
Smit, A.L., Benough, A.G., Engels, C., van Noordwijk, M.,
Pellerin, S. & van de Geijn, S.C. (2000) Root Methods: a
Handbook. Spinger-Verlag, Berlin.
Tilman, D. (1988) Plant Strategies and the Dynamics and
Structure of Plant Communities. Princeton University
Press, Princeton.
Twolan-Strutt, L. & Keddy, P.A. (1996) Above- and below-
ground competition intensity in two contrasting wetland
plant communities. Ecology, 77, 259–270.
USDA, NRCS (2001) The PLANTS Database. National
Plant Data Center, Baton Rouge, Los Angeles.
Wardle, D.A., Barker, G.M., Bonner, K.I. & Nicholson, K.S.
(1998) Can comparative approaches based on plant ecophysiological traits predict the nature of biotic interactions
and individual plant species effects in ecosystems? Journal
of Ecology, 86, 405 – 420.
Wardle, D.A. & Peltzer, D.A. (2003) Interspecific interactions
and biomass allocation among grassland plant species.
Oikos, 100, 497–506.
Weiner, J., Wright, D.B. & Castro, S. (1997) Symmetry of
below-ground competition between Kochia scoparia individuals. Oikos, 79, 85–91.
von Wettberg, E.J. & Weiner, J. (in press) Larger Triticum aestivum plants do not preempt nutrient rich patches in a glasshouse experiment. Plant Ecology.
Wilson, S.D. & Tilman, D. (1991) Components of plant
competition along an experimental gradient of nitrogen
availability. Ecology, 72, 1050–1065.
Wilson, S.D. & Tilman, D. (1995) Competitive responses of
eight old-field plant species in four environments. Ecology,
76, 1169–1180.
Zobel, M. & Zobel, K. (2002) Studying plant competition: from
root biomass to general aims. Journal of Ecology, 90, 578–580.
Received 10 September 2002
revision accepted 7 April 2003