Research

Root structurefunction relationships in 74 species: evidence of a

root economics spectrum related to carbon economy
Catherine Roumet1, Marine Birouste1, Catherine Picon-Cochard2, Murielle Ghestem3, Normaniza Osman4,
Sylvain Vrignon-Brenas2, Kun-fang Cao5 and Alexia Stokes3
Centre dEcologie Fonctionnelle et Evolutive, UMR 5175, CNRS Universit
e de Montpellier Universit
e Paul Val
ery Montpellier EPHE, 1919 Route de Mende, 34293 Montpellier Cedex

5, France; 2INRA, UR 874, UREP, Grassland Ecosystem Research, 5 Chemin de Beaulieu, 63039 Clermont-Ferrand, France; 3INRA, UMR AMAP, Boulevard de la Lironde, 34398
Montpellier Cedex 5, France; 4Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia; 5State Key Laboratory for Conservation and Utilization of Subtropical
Agro-bioresources, and College of Forestry, Guangxi University, Nanning Guangxi 530004, China

Summary
Author for correspondence:
Catherine Roumet
Tel: +33 4 67 61 32 40
Email: catherine.roumet@cefe.cnrs.fr
Received: 6 August 2015
Accepted: 25 November 2015

New Phytologist (2016)

doi: 10.1111/nph.13828

Key words: economics spectrum, eudicots,

fine-root traits, graminoids, nitrogen, plant
diversity, root decomposability, root
respiration.

Although fine roots are important components of the global carbon cycle, there is limited

understanding of root structurefunction relationships among species. We determined

whether root respiration rate and decomposability, two key processes driving carbon cycling
but always studied separately, varied with root morphological and chemical traits, in a coordinated way that would demonstrate the existence of a root economics spectrum (RES).

Twelve traits were measured on fine roots (diameter 2 mm) of 74 species (31 graminoids
and 43 herbaceous and dwarf shrub eudicots) collected in three biomes.

The findings of this study support the existence of a RES representing an axis of trait variation in which root respiration was positively correlated to nitrogen concentration and specific
root length and negatively correlated to the root dry matter content, lignin : nitrogen ratio
and the remaining mass after decomposition. This pattern of traits was highly consistent
within graminoids but less consistent within eudicots, as a result of an uncoupling between
decomposability and morphology, and of heterogeneity of individual roots of eudicots within
the fine-root pool.

The positive relationship found between root respiration and decomposability is essential
for a better understanding of vegetationsoil feedbacks and for improving terrestrial biosphere models predicting the consequences of plant community changes for carbon cycling.

Introduction
Fine roots, traditionally defined as all roots 2 mm in diameter,
play a key role in the carbon (C) economy at both the plant and
ecosystem level, as c. 40% of the net C fixed by photosynthesis is
allocated to fine roots (Jones et al., 2009). This C is used in the
maintenance of existing fine roots and in the construction of new
roots which are involved in the acquisition of additional
resources. Part of the C allocated to fine roots is released as CO2
back to the atmosphere either during their life through respiration (Warembourg et al., 2003; Jones et al., 2009) or after their
death through root decomposition. Understanding variations in
fine-root respiration and decomposition among species is of
paramount importance for global change science and plant ecology, because the CO2 efflux from these two processes is a critical
and uncertain component of plant, ecosystem and global C budgets (Reich et al., 2008). While the decomposition rate of species
is influenced by climate and the decomposer community, there is
evidence that the decomposition rate measured in standard conditions (decomposability) is strongly driven by functional traits
and consistently correlated with a species ecological strategy
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(Cornwell et al., 2008). Fine-root decomposability and respiration rates are both influenced by chemical and morphological
traits (Reich et al., 2008; Makita et al., 2012; Picon-Cochard
et al., 2012 for respiration; Silver & Miya, 2001; Hobbie et al.,
2010; Freschet et al., 2012 for decomposability), but have always
been studied in isolation from each other. It is thus not known if
root respiration rate, decomposability, and morphological and
chemical traits vary in a coordinated way that would demonstrate
the existence of a root economics spectrum (RES) related to the
C economy across species and functional groups.
Compared with the major advances made concerning leaf
functioning, little effort has been made to understand variations
in the root C economy among species. At the leaf level, a suite of
correlated traits known as the leaf economics spectrum (LES) has
been identified in which high photosynthetic and respiration
rates were observed in species with short-lived leaves possessing a
high specific leaf area and nitrogen (N) concentration. The converse was observed for thick, dense, N-poor and long-lived leaves
that conserved resources efficiently (Wright et al., 2004). Recent
studies demonstrated that traits characterizing leaf economics also
influenced leaf decomposability (Santiago, 2007; Bakker et al.,
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2011; Freschet et al., 2012). Whether such an RES exists is still a

matter of debate and remains elusive (Freschet et al., 2010;
Mommer & Weemstra, 2012; Chen et al., 2013; Bardgett et al.,
2014; Reich, 2014; Valverde-Barrantes et al., 2015). In analogy
to the LES, if an RES exists among species, it should represent a
manifold of covarying root traits, that is, a root trait syndrome,
highlighting a trade-off between resource acquisition and conservation, in which fine roots with high N concentration and specific root length (SRL) should have high respiration and nutrient
uptake rates. These traits might be associated with a short life
span and low dry matter content and could enhance decomposability. At the opposite end of the spectrum, species with thick,
N-poor roots are expected to have a long life span and low respiration and decomposability, thus leading to low CO2 release to
the atmosphere. Experimental evidence of such an acquisition
conservation trade-off for fine roots across species is missing as a
consequence of the scarcity of data related to root functioning
and in particular with regard to resource acquisition and life
span. Recent multivariate comparative root studies have generally
focused on covariation of morphological and chemical fine-root
traits (Chen et al., 2013; Fort et al., 2013, 2015; Kong et al.,
2014; Prieto et al., 2015), but how these syndromes are related to
root functioning remains poorly understood. In a recent review,
Reich (2014) suggested the existence of an RES representing a
trade-off between root growth and persistence in fine roots. This
conclusion was derived from two sets of independent data: first,
root N concentration was correlated both with root respiration
(positively) and with root life span (negatively), and second, N
concentration was related to root morphological traits. Other
authors consider that there is not enough evidence for such an
RES, because of strong inconsistencies among studies (Mommer
& Weemstra, 2012; Chen et al., 2013) and functional groups.
For example, in herbaceous species, most studies have shown that
root N concentration is correlated with morphological traits
(Craine et al., 2005 and Picon-Cochard et al., 2012 for grasses;
Tjoelker et al., 2005 for grasses and forbs) but this was not confirmed in woody species (Withington et al., 2006; Chen et al.,
2013; Valverde-Barrantes et al., 2015). Similarly, root life span
has been found to be negatively related to root N concentration
and SRL (Tjoelker et al., 2005; Withington et al., 2006; McCormack et al., 2012; Reich, 2014), but positively related to root
diameter (McCormack et al., 2012; Pilon et al., 2013) although
this result was not confirmed by Tjoelker et al. (2005) and
Withington et al. (2006). The development of a unified framework toward an RES might suffer from a lack of homogeneity in
fine-root sampling methods between studies. Because it is now
recognized that fine-root structure and function vary among fineroot orders both within (Pregitzer et al., 2002; Guo et al., 2008;
Valenzuela-Estrada et al., 2008; Comas & Eissenstat, 2009;
Picon-Cochard et al., 2012; McCormack et al., 2015) and across
species (McCormack et al., 2012), the comparison of results
obtained with contrasting sampling methods might bias general
patterns of root traits. This issue is particularly relevant for the
comparison between woody and nonwoody species, since root
traits are commonly measured on first-order roots in woody
species and on roots < 2mm in herbaceous species (G. Freschet
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et al., unpublished). Another explanation of the lack of evidence

for an RES might be the absence of studies considering a large
number of species on which morphological, chemical and, in particular, physiological traits are measured simultaneously using
standardized methods.
The objective of our study was to investigate, in a large number of species from different biomes, general relationships
between fine-root structure and two processes involved in the
global C budget: root respiration and decomposability, in order
to test whether an RES exsits. We also aimed to examine whether
patterns of root traits differed between graminoids and eudicots.
Graminoids and eudicots are often considered as contrasting
functional groups because they differ in many aspects, such as
root morphology and anatomy. Roots of graminoids are fibrous,
with no secondary growth, and they generally have thin and Npoor roots compared with eudicots (Craine et al., 2001; Roumet
et al., 2006, 2008). Whether these differences translate into a disparity in root function and whether structurefunction relationships are consistent across functional groups remain untested.
We collected fine roots of 74 species (mostly herbaceous and
dwarf shrub species) at six sites from three climatic zones, that is,
Mediterranean, temperate and tropical. Fine roots are defined in
our study as all nonwoody roots (except rhizomes and tap roots)
with a diameter 2 mm. We selected fine roots 2 mm because
in herbaceous species most roots 2 mm are considered as
absorptive (McCormack et al., 2015). In addition, it was logistically impossible to dissect roots into individual root orders and
obtain enough material per root order to measure respiration,
decomposition and chemical composition, as all these analyses
require significant amounts of root material. Using standardized
methods, we measured specific root respiration (RR) rates and
decomposition in controlled conditions (termed decomposability
hereafter) together with four fine-root morphological traits (SRL,
diameter, proportion of very fine roots with a diameter 0.2 mm
and dry matter content, which is a proxy of tissue density;
Birouste et al., 2014) and six chemical traits (N, C, water-soluble
compound, hemicellulose, cellulose and lignin concentrations).
We hypothesized that: (1) an RES exists in which species that
possess thinner roots with a high SRL and a low dry matter content have high N and water-soluble compound concentrations
and high respiration and decomposition rates, whereas the opposite pattern is expected for species with thick, dense roots, which
are rich in structural compounds such as lignin and cellulose; (2)
eudicots and graminoids show opposite patterns along the RES
because eudicots are known to have N-rich roots with a high SRL
and a lower tissue density compared with graminoids (Craine
et al., 2001; Roumet et al., 2008; G. Freschet et al., unpublished);
(3) respiration and decomposability covary and are driven by
similar traits.

Materials and Methods

Species and sites
The study was conducted on 74 C3 species, mostly herbaceous
and dwarf shrub species (see Supporting Information
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Table S1). Species originated from six sites in France and
China representing three major terrestrial biomes, temperate,
Mediterranean and tropical (Table S2). Species were harvested
in temperate, montane conifer forest and prairie (Chamrousse,
Alps, France (FR-Ch)), temperate upland perennial grassland
(Saint-Genes Champanelle, central France (FR-Sg)), temperate
montane farmland mixed with noncrop species (Daxingdi,
western Yunnan, China (CH-Da); Ghestem et al., 2014),
Mediterranean rangelands (Montpellier and La Fage, southern
France (FR-Mo and FR-Lf, respectively)), and tropical rangelands (Xishuangbanna, southern Yunnan, China (CH-Xi)).
Species were chosen in order to represent a large range of traits
within graminoids (monocots) and eudicots. Species included
23 botanical families, 31 graminoids and 43 eudicots, which
have contrasting life forms (as described by Raunkiaer, 1934):
16 therophytes (annuals), 46 hemicryptophytes (herbaceous
perennials), eight chamaephytes (dwarf shrubs < 20 cm height)
and four phanerophytes (two shrubs and two climbers). Species
included seven N2-fixing species (all Fabaceae); tree species
were not considered in this study. Eight to 23 species were
harvested at each site.
Plant harvest and root processing
Plants were harvested between June 2010 and May 2011, during
the peak of aboveground vegetative growth, in natural areas
(CH-Da, CH-Xi and FR-Ch), in common gardens where
species were grown in monocultures (FR-Sg and FR-Lf) or in a
pot experiment (FR-Mo). When harvested in the field, root systems of 2050 well-developed individuals per species were carefully dug out with a pickaxe or spade to a depth of 15 cm and
were immediately put in containers filled with water. When
grown in common gardens, four to eight randomly distributed
soil cores (510 cm diameter 9 15 cm depth) per species community were collected between two healthy plants and placed in
a plastic bag. After harvest, root systems and soil cores were
transferred to the laboratory, where they were meticulously
washed and sorted under water. We selected fine roots only,
defined in this study as nonwoody roots with a diameter
2 mm. Tap roots, rhizomes, dead roots and all roots with a
diameter > 2 mm were discarded. For each species, fine roots
from all individuals (or soil cores) were kept in water and pooled
together until c. 50 g of fresh fine-root biomass was obtained for
each species, that is, the biomass needed for further analyses.
Subsamples of this composite sample were then used for measurements of root respiration and decomposition, root morphology and chemical composition. For the measurement of
respiration rate, eight subsamples (the fresh biomass of each was
c. 36 g) were used within the 30 min following root washing.
These same samples were then destined for the measurement of
root decomposition. Eight additional subsamples (the fresh
biomass of each was c. 0.15 g) were put aside in water, at 4C,
and were used for the measurement of morphological root traits
within 13 min following root washing. Four more subsamples
(each weighing c. 3 g FW) were dried at 40C for 5 d before the
measurement of chemical traits.
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Research 3

Specific root respiration

After washing, fine roots of the eight subsamples to be used for
respiration measurements were carefully removed from water,
blotted between two sheets of tissue paper to remove excess water,
and then placed in a soil respiration chamber (Li6400-09; LiCor,
Lincoln, NE, USA) to measure root respiration using an infrared
gas analyser (Li6400; LiCor). A thermocouple (6000-09TC;
LiCor) placed below the root sample recorded temperature. In
order to measure root respiration at the same temperature for all
species and sites, measurements were performed in airconditioned or heated rooms, depending on the site. When necessary the respiration chamber was placed on a heating plate. For
all species, the average temperature inside the respiration chamber was 24.3  0.1C (mean  SE; n = 490). Averages of three to
eight measurements of root respiration (lmol m2 s1) were used
for each subsample. At the end of the respiration measurements,
roots were spread on filter paper, air-dried for at least 1 wk and
then weighed to determine their air-dried mass. Four subsamples
per species of these air-dried roots were selected, weighed, ovendried for 48 h at 60C and weighed again. The air-dried
mass : dry mass ratio was used to calculate the specific root respiration by root dry mass (RDM; nmol g1 s1). The remaining
air-dried roots from all sites were transferred to the Centre
dEcologie Fonctionnelle et Evolutive (CEFE, Montpellier,
France) and stored in the dark until decomposability measurements were carried out.
Root morphological traits
Morphological traits were measured on eight samples per species.
Washed roots (which were kept in water in order to ensure full
hydration) were pressed between two sheets of blotting paper to
remove excess water and were then weighed to determine their
Root Saturated Mass (RSM) before staining with methylene blue
(5 g l1) to increase contrast during scanning. Roots were then
rinsed, placed onto a mesh tray filled with distilled water and
spread out to avoid any overlap between roots. The mesh tray
with roots was removed from the water, an acetate sheet was
pressed onto the mesh and flipped over allowing the roots to be
transferred to the acetate sheet, which was then placed on the
scanner. (Roumet et al., 2008; Birouste et al., 2012). Samples
were scanned as greyscale images at a resolution of 400 dpi using
a scanner equipped with a transmitted light source to avoid shadows (Epson Expression 1680; Epson, Ontario, Canada). All
scanned roots were then oven-dried for 48 h at 60C and
weighed to determine their RDM. Digital image analysis software (WINRHIZO PRO, v.2009c; Regent Instruments, Qu
ebec,
Canada) was used to determine mean diameter (D) and the distribution of root length (L) in different diameter classes (from 0
to 2 mm, with a 0.1-mm-diameter interval) of all samples from
the 74 species. Fig. S1 shows that the fine-root samples selected
for the 74 species were very homogeneous in terms of root diameter distribution as for all species 90% of the root length had a
diameter between 0.1 and 0.4 mm. SRL (m g1) was calculated
as the ratio L : RDM, root dry matter content (RDMC; mg g1)
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as the ratio RDM : RSM and percentage of very fine roots (VFR)
as the percentage of root length with a diameter 0.2 mm. This
latter trait is useful to measure as it mirrors the distribution of the
finest roots, which have the highest foraging capacity and the
highest branching intensity (Pages & Picon-Cochard, 2014).
Root chemical composition
For each species, determination of root chemical composition
was conducted on the four subsamples reserved for chemical
analyses. C and N concentrations were determined on ground
material using an elemental analyser (CHN model EA 1108;
Carlo Erba Instruments, Milan, Italy). Concentrations of
water-soluble compounds, hemicelluloses, cellulose and lignin
were obtained following the Van Soest method (Van Soest,
1963) and using a fiber analyser (Fibersac 24; Ankom, Macedon, NJ, USA).
Root decomposability
We experimentally examined the influence of root traits on
decomposition rate under standardized conditions (i.e. decomposability) by keeping all other environmental factors constant
(soil, decomposer community, temperature and humidity). Root
decomposability of the 74 species was measured at the CEFE
(Montpellier, France) according to Taylor & Parkinsons (1988)
protocol, modified by Ibrahima et al. (1995). In January 2012,
for each species, eight air-dried root samples (500  0.1 mg) were
enclosed in a nylon root decomposition bag (Northern Mesh,
Oldham, UK) (12 9 8 cm; 2-mm mesh) and stapled. Roots of all
species were incubated for 12 wk in microcosms under controlled
conditions.
The microcosm type used comprised a polyvinylchloride pipe
(15 cm diameter and 15 cm tall), fitted with a lid and a sealed
bottom. A grid, 2 cm above the bottom, divided the chamber
into two unequal parts: a usable space of 1.5-l capacity in which
1.0 kg of soil was placed and a drainage compartment of 300 ml.
The soil (pH 8.2; C concentration 13.9 g kg1; N concentration 1.32 g kg1; phosphorus (P) concentration 0.03 g kg1) was
a 3 : 1 mixture of a clay loam soil from a common garden experiment at the CEFE (Montpellier, France) and the surface organic
horizon soil from a nearby area, respectively. In each microcosm,
a root decomposition bag was buried horizontally in the soil, at
3 cm depth. The microcosms were kept in the dark at
22  0.01C throughout the experiment, covered with a nonsealing plastic lid to avoid evaporation losses. Microcosms were
watered once a week with distilled water to maintain soil humidity at 80% of field capacity. Twelve weeks after the beginning of
the incubation, the bags were removed from the microcosms.
Upon harvest, bags were opened; soil particles were carefully
removed from the samples by washing roots with water using a
sieve with a 0.2-mm mesh to prevent loss of root fragments.
Washed roots were oven-dried for 48 h at 60C and weighed to
determine the RDM after incubation (Rootmasst ). Corrections for
inorganic contaminants (mainly soil particles) were made after
sample combustion at 550C (3 h at 350C then 3 h at 550C)
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in a muffle furnace (LE14; Nabertherm, Lilienthal, Germany) in

order to determine the root biomass on an ash-free basis
(Rootashmasst ). The percentage of remaining mass (RM; %) after
incubation was calculated as:
RM Rootmasst  Rootashmasst =Rootmassi  Rootashmassi
 100
with Rootashmassi the initial root ash-free biomass.
Data analyses
For all the variables measured, the distribution of values was
tested for normality (Shapiro-Wilk test; a = 0.05) and logtransformed when necessary. We focused our analyses on differences between graminoids and eudicots. We performed a general
linear mixed model (GLMM) for each measured trait using all
replicates. Fixed factors included class (graminoids or eudicots),
biome (temperate, Mediterranean or tropical), growing conditions (field, common garden or pot), and their interactions;
species was nested within sites as a random factor. The effects of
life form and N2-fixing capacity were not included in the GLMM
because of unbalanced numbers of species among groups, biomes
and growing conditions. Bivariate correlations among traits were
evaluated using Pearsons correlation coefficients. Principal component analyses (PCAs) were conducted with the eight most
important root variables: RR, RM, root nitrogen concentration
(RNC), water-soluble compound concentration (Sol), SRL,
diameter, RDMC, and lignin : N ratio. PCAs were performed for
all species, and for graminoids and eudicots separately, using the
mean of each trait per species. The KaiserMeyerOlkin (KMO)
test for sampling adequacy and Bartletts sphericity were first used
to assess the appropriateness of using PCA. Finally, one-way
ANOVAs were conducted on the scores of species on axes 1 and
2 of the PCA to test for differences between graminoids and eudicots and among life forms at the multivariate level. GLMM and
PCA statistical analyses were performed with the open-source statistical environment R, version 2.13.0 (R Development Core
Team, 2013) using the packages lme4 and ade4.

Results
Fine-root respiration and remaining mass
Fine-root respiration rates showed 18-fold variation among
species, ranging from 1.89 nmol CO2 g1 s1 (Dactylis
glomerata, FR-Mo) to 34.6 nmol CO2 g1 s1 (Daucus carota)
(Table S3). Fine-root respiration rates were significantly higher
for eudicots (9.43 nmol CO2 g1 s1) compared with graminoids
(8.32 nmol CO2 g1 s1) (Table 1). This pattern was similar
across biomes (no significant interaction between class and
biome), but was stronger in species grown in pot and field conditions compared with those from common gardens (significant
interaction between class and growing conditions). Overall, root
respiration was significantly correlated with six of the 12 traits
studied (Table 2): respiration rate was correlated positively with
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Research 5

Table 1 Means, SEs and results of general linear models (GLMs) for fine-root traits ( 2 mm) measured on 31 graminoids and 43 eudicots

Root traits

Graminoids
mean  SE

Root respiration (nmol CO2 g1 s1)

Remaining mass (%)
Specific root length (m g1)
Mean diameter (mm)
Very fine roots 0.2 mm (%)
Root dry matter content (mg g1)
C conc. (mg g1)
N conc. (mg g1)
C : N ratio
Water-soluble conc. (mg g1)
Hemicellulose conc. (mg g1)
Cellulose conc. (mg g1)
Lignin conc. (mg g1)
Lignin : N ratio

454
435
399
399
399
449
308
308
308
251
251
251
251
234

8.32  1.06
46.4  3.07
155.0  22.1
0.33  0.02
49.52  4.15
231.00  6.13
412.7  5.40
10 .49  0.87
50.85  5.02
205.0  9.0
381.4  9.0
331.0  6.0
82.5  4.5
10.52  1.16

Eudicots
mean  SE

Class
v2 (P)

Biome
v2 (P)

Growth
cond
v2 (P)

Biome 9
class
v2 (P)

Growth
cond 9 class
v2 (P)

9.43  1.23
37.5  2.57
99.89  20.9
0.46  0.02
16.97  2.15
257.1  10.8
416.8  3.83
12.01  0.91
41.58  2.57
378.4  18.2
223.6  10.1
258.8  10.1
139.3  8.9
13.72  1.13

14.17***
21.80***
15.81***
11.49***
29.86***
0.56ns
0.41ns
11.88***
13.14***
30.08***
50.58***
17.04***
7.38**
2.91ns

59.57***
9.87**
3.73ns
11.65**
32.14***
1.11ns
0.04ns
3.76ns
11.68**
1.68ns
4.91ns
0.62ns
5.80ns
6.68*

55.93***
17.95***
13.38**
36.78***
39.56***
2.60ns
0.59ns
15.09***
35.81***
21.82***
18.06***
0.49ns
4.65ns
12.44**

5.37ns
1.18ns
4.80ns
3.37ns
2.69ns
6.17*
0.32ns
4.15ns
3.33ns
8.76*
1.32ns
3.84ns
5.92ns
9.44**

9.58**
4.59ns
11.71**
7.53*
2.59ns
3.86ns
0.52ns
14.24***
12.72**
1.54ns
0.05ns
1.90ns
3.96*
9.50**

Remaining mass refers to the root mass remaining after 12 wk of incubation in standard conditions. v and P-values indicate the results of the GLM with
class (graminoids and eudicots), biomes (tropical, temperate and Mediterranean), growing conditions (field, common garden and pot) and their interactions
as fixed factors and species nested in site as a random factor. *, P < 0.05; **, P < 0.01; ***, P < 0.001; ns, not significant. C, carbon; N, nitrogen; conc., concentration; cond, conditions.
Table 2 Pearsons regression coefficients between root respiration rate (nmol CO2 g1 s1), or remaining mass (%), and root traits
Root respiration

Remaining mass

Root traits

All species
(n = 73)

Graminoids
(n = 31)

Eudicots
(n = 42)

All species
(n = 73)

Graminoids
(n = 31)

Eudicots
(n = 42)

Remaining mass (%)

Specific root length (m g1)
Mean diameter (mm)
Very fine roots 0.2 mm (%)
Root dry matter content (mg g1)
C conc. (mg g1)
N conc. (mg g1)
C : N ratio
Water-soluble conc. (mg g1)
Hemicellulose conc. (mg g1)
Cellulose conc. (mg g1)
Lignin conc. (mg g1)
Lignin : N ratio

0.63***
0.46***
0.35**
0.19ns
0.48***
0.02ns
0.50***
0.49***
0.08ns
0.02ns
0.10ns
0.01ns
0.37**

0.67***
0.53**
0.54**
0.69***
0.40*
0.26ns
0.63***
0.63***
0.26ns
0.09ns
0.44*
0.29ns
0.63***

0.60***
0.53***
0.36*
0.02ns
0.53***
0.19ns
0.37*
0.35*
0.15ns
0.14ns
0.20ns
0.02ns
0.23ns

0.25*
0.19ns
0.03ns
0.15ns
0.03ns
0.43***
0.42***
0.34**
0.12ns
0.38**
0.20ns
0.49***

0.72***
0.80***
0.68***
0.29ns
0.21ns
0.81***
0.79***
0.27ns
0.37*
0.02ns
0.32ns
0.79***

0.20ns
0.01ns
0.18ns
0.20ns
0.09ns
0.07ns
0.06ns
0.41**
0.10ns
0.38*
0.52***
0.48**

Pearsons coefficients are given for all species, for graminoids and for eudicots; *, P < 0.05; **, P < 0.01; ***, P < 0.001; ns, not significant. C, carbon;
N, nitrogen; conc., concentration.

SRL (Fig. S2a) and RNC (Fig. S2d) and negatively correlated
with root diameter (Fig. S2b), RDMC (Fig. S2c), and C : N and
lignin : N (Fig. S2e) ratios. Surprisingly, the concentration of
water-soluble compounds or fibre compounds did not influence
fine-root respiration. Patterns were similar within graminoids
and eudicots except for two traits; the proportion of VFR (diameter 0.2 mm) and the lignin : N ratio were both correlated with
respiration rates in graminoids but not in eudicots (Table 2).
Correlation coefficients between respiration rate and traits were
generally greater in graminoids compared with eudicots.
The remaining mass of fine roots after 12 wk of incubation
showed 15-fold variation among species and ranged from 5.3%
for Astrantia minor to 79.4% for Trichophorum cespitosum
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(Table S3). Remaining mass was significantly higher for

graminoids (46.4%) as compared with eudicots (37.5%), indicating that roots of graminoids decomposed slightly more slowly
than those of eudicots (Table 1). This pattern was similar regardless of biome and growing conditions. Across all species, remaining mass was more influenced by chemical traits than by
morphological traits (Table 2). Remaining mass diminished significantly with increasing SRL (Fig. S2f), RNC (Fig. S2i) and
water-soluble compound concentration and increased significantly with increasing cellulose concentration and C : N and
lignin : N ratios (Fig. S2j). Fine-root remaining mass of
graminoids and eudicots was not influenced by the same traits.
Within graminoids, remaining mass was driven both by chemical
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and by morphological traits; it increased with decreasing SRL or

with increasing root diameter. Within eudicots, the remaining
mass could not be predicted by any morphological traits nor by
RNC or C : N ratio (Table 2). The only traits explaining the variation in remaining mass among eudicots were water-soluble compound, cellulose and lignin concentrations and the lignin : N
ratio (Table 2).
Fine-root respiration and remaining mass were negatively correlated overall and within each functional group (Fig. 1; Table 2),
suggesting that roots characterized by a high metabolic rate also
decomposed more rapidly.
Root trait syndrome
Overall, root respiration, remaining mass, and chemical and morphological traits were strongly correlated to each other (Fig. 2a).
The PCA conducted on the eight most important traits captured
60.8% of the variance in the first two axes with 39.2% on the first
component (PC1) (Fig. 3a; Table S4). PC1 was negatively related
to SRL, RR and RNC and positively related to lignin : N ratio,
RM, D and RDMC. The ANOVA conducted on species PCA
scores indicated that PC1 discriminated between plant life forms,
with a continuum from therophytes and hemicryptophytes at the
negative end of PC1 to chamaephytes and then phanerophytes at
the positive end of PC1 (Fig. 3b). Therophytes and hemicryptophytes were characterized by higher SRL, RNC and root respiration and phaneropytes by higher D, RDMC, lignin : N ratio and
RM. The second PC (PC2) explained 21.6% of the variation and
was negatively related to the concentration of water-soluble compounds and D and positively related to RM. PC2 strongly discriminated graminoids from eudicots (Fig. 3c). Graminoids were
all at the positive end of PC2 and had low water-soluble compound concentration and very fine roots with high SRL and
lignin : N ratio and decomposed slowly (high RM). Eudicots

Fig. 1 Relationship between fine-root respiration and remaining mass for

74 species. Data are shown for graminoids (closed circles) and eudicots
(open circles). Respiration is expressed on a logarithmic (base10) basis. The
regression line is drawn for all species pooled. See Table 2 for Pearsons
regression coefficients.
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were found mostly on the negative side of PC2, with thicker fine
roots which had higher concentrations of water-soluble compounds and lignin. Life forms did not vary significantly along
PC2 (Fig. 3b).
The PCAs conducted within each group explained 73.9% of
the variation for graminoids (Fig. 4a; Table S4) and 60% for
eudicots (Fig. 4b; Table S4). Within each group, the PCA yielded
nearly the same pattern of trait correlations as for the total data
set (Fig. 3a), except for RDMC and D. Within graminoids, PC2
was related to the concentration of water-soluble compounds and
RDMC, whereas in eudicots, as for the whole set of data, PC2
was related to water-soluble compound concentration and D.
The percentages of the variance explained by the two first PCs
(Fig. 4a,b) were much higher in graminoids than in eudicots
(56% and 34.7%, respectively). Similarly, the number and
strength of the correlations among traits (Fig. 2b,c) were higher
in graminoids compared with eudicots. For eudicots, this result
was largely attributable to a lack of positive relationships between
traits related to root fineness (D and VFR) and other chemical
and physiological traits.

Discussion
Evidence of a root economics spectrum
Our study yielded two major results: we identified a manifold of
covarying traits that revealed strong links between root morphology, chemistry and two processes involved in the C economy
(respiration and decomposability); and we demonstrated that
root respiration was negatively correlated with the remaining
mass. Taken together, these results on 74 species support the existence of an RES based on the C economy and represented by axis
1 of the PCA (Fig. 3). Axis 1 represented a continuous distribution of life forms from herbaceous species (therophytes and
hemicryptophytes) to dwarf shrubs (chamaephytes) and shrubs
(phanerophytes). Herbaceous species that occupy frequently disturbed environments possessed root traits facilitating a resource
acquisition strategy because of a higher metabolic activity (high
respiration rate), high RNC and high foraging ability (high SRL).
At the opposite end of the RES, shrubs, which are more slowgrowing, had a more conservative strategy with thicker roots,
high RDMC and a high lignin : N ratio, which probably contributed to greater longevity, greater stress and herbivore
tolerance and lower decomposability.
Contrary to our hypothesis, graminoids and eudicots did not
show opposite patterns along axis 1, but differed along axis 2.
Roots of graminoids were poorer in water-soluble compounds
and lignin, but richer in hemicellulose and cellulose compared
with eudicots. Graminoids possessed thinner roots and decomposed slowly compared with eudicots, as previously reported for
fine roots (Birouste et al., 2012) and leaves (Cornelissen &
Thompson, 1997; Cornwell et al., 2008). These differences
might be attributable to the particular anatomy of graminoids,
characterized by the absence of secondary growth and by a high
proportion of recalcitrant tissues, such as xylem (Wahl & Ryser,
2000; Hummel et al., 2007; Vogel, 2008) and lignified xylem
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(a) All species

Chemical traits

RNC

C:N

Solubles

Lignin : N

Functions
Root
respiration

Remaining
mass

SRL

RDMC

VFR

Morphological traits
Acquisitive
traits

Diameter

Root economics spectrum

(c) Eudicots

(b) Graminoids

RNC

C:N

Solubles

RNC

Lignin : N

Root
respiration

Remaining
mass

SRL

RDMC

VFR

Conservative
traits

Diameter

C:N

Solubles

Lignin : N

Root
respiration

Remaining
mass

RDMC

SRL

VFR

Diameter

Fig. 2 Positive (red lines) and negative (blue dotted lines) correlations between fine-root traits (diameter 2 mm), calculated for (a) 74 species, (b) 31
graminoids and (c) 43 eudicots. RNC, root nitrogen concentration; solubles, water-soluble compound concentration; SRL, specific root length; VFR, very
fine roots (diameter 0.2 mm); RDMC, root dry matter content; C : N, ratio between carbon and nitrogen concentrations. For clarity, chemical traits are at
the top, root functions (respiration and remaining mass) in the middle and morphological traits at the bottom of the diagram. Root traits related to the
acquisition syndrome (RNC, solubles, respiration, SRL and VFR) are on the left side of the diagram, and traits related to resource conservation or
persistence (C : N and lignin : N ratios, remaining mass, RDMC and diameter) are on the right side. Line thicknesses indicate the magnitude of P-values:
thick lines, P < 0.001; medium lines, P < 0.01; thin lines, P < 0.05.

rings (Lindedam et al., 2009) whose cell walls are mainly composed of cellulose and hemicelluloses (Vogel, 2008). Despite
these differences, within graminoids and within eudicots, the pattern of some core traits was similar to the pattern reported for the
whole data set. In both groups, root respiration was positively
related to SRL and RNC and negatively correlated with RM and
RDMC. The percentage of the variance explained by axis 1, as
well as the number and strength of correlations among traits,
were, however, greater for graminoids than for eudicots (Figs 2,
4). This result was explained by the decomposability of eudicots
which was unrelated to morphological traits and RNC, as previously reported by Birouste et al. (2012), as well as by the
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contrasting roles of root diameter in the two groups. In

graminoids, root diameter was strongly and negatively related to
traits involved in resource acquisition and positively related to
traits involved in resource conservation, whereas this was not the
case for eudicots. Therefore, for eudicots, average root diameter
is not part of the RES and is not a useful trait to differentiate
species strategy as already reported for tree species (McCormack
et al., 2015). This result is probably attributable to the heterogeneity of the eudicot group, including 20 taxonomical families
that differed in life forms, nutrient acquisition strategy, or root
system types. In addition, roots of eudicots underwent secondary
(radial) growth that influenced root functioning (McCormack
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Fig. 3 Principal component analysis of eight

fine-root traits in 74 species. (a) Traits and (b,
c) species projections according to (b) their
life form (Th, therophytes; He,
hemicryptophytes; Ch, chamaephytes; Ph,
phanerophytes) and (c) their class
(graminoids and eudicots). Labels represent
the centroid values for each life form and
each class. F-values were obtained from an
ANOVA testing the effect of lineage or life
form on species scores on PC1 and PC2. **,
P < 0.01; ***, P < 0.001; ns, nonsignificant.
RR, root respiration; RNC, root nitrogen
concentration; SRL, specific root length; RM,
remaining mass; D, mean diameter; RDMC,
root dry matter content; Lig : N,
lignin : nitrogen ratio; Sol., concentration of
water-soluble compounds.

Fig. 4 Principal component analysis of eight

fine-root traits in (a) 31 graminoids and (b)
43 eudicots. RR, root respiration; RNC, root
nitrogen concentration; SRL, specific root
length; RM, remaining mass; D, mean
diameter; RDMC, root dry matter content;
Lig : N, lignin : nitrogen ratio; Sol.,
concentration of water-soluble compounds.

et al., 2015). The pool of roots considered in this study (Fig. S1)
could have included both absorptive (first-order roots) and transport (higher order roots with secondary growth) roots that would
have biased the results as compared with graminoids, which are
composed of homogeneous root axes without secondary growth.
Therefore, the range of fine-root morphology and chemistry in
eudicots is much greater compared with the graminoid group, as
indicated by the lower coefficient of variation observed for traits
of graminoids (data not shown).
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In conclusion, our study on 74 herbaceous and dwarf shrub

species supports the existence of an RES in which root respiration
was positively related to SRL and RNC and negatively correlated
with RM and RDMC, both within and among graminoids and
eudicots. Recent studies on tree species in which root N concentration was not correlated with morphological traits (Chen et al.,
2013; Valverde-Barrantes et al., 2015) did not support the existence of an RES. However, in these studies, traits were measured
on first-order roots. In herbaceous species, where traits are
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traditionally measured on roots 2 mm, there is much evidence
of a coupling between morphological and chemical traits (Craine
et al., 2005; Tjoelker et al., 2005; Roumet et al., 2006; Freschet
et al., 2010; Picon-Cochard et al., 2012; Fort et al., 2013), and
between root traits and functions such as root respiration (Reich
et al., 2008; Picon-Cochard et al., 2012) or life span (Van Der
Krift & Berendse, 2002). These inconsistencies among studies
might reflect different patterns of traits between herbaceous and
tree species which are often studied separately. The disparity in
results may also be attributable to a lack of standardized root
sampling methods enabling comparisons among studies (McCormack et al., 2015). It would thus be necessary to investigate
whether an RES exists in a larger number of species world-wide
and with standardized methods. Future research should also focus
on whether major plant lineages are functionally distinct at the
root level, as recently demonstrated for leaves (Cornwell et al.,
2014).
Root respiration and decomposability
The fine-root respiration rate, which represents metabolic activity, was influenced both by chemical traits (RNC, C : N and
lignin : N) and by morphological traits (SRL, diameter and
RDMC) and this pattern was similar between graminoids
and eudicots. The positive relationship between root respiration
and RNC is consistent with previous studies, which reported a
common respirationN relationship across different taxonomic
groups (Reich et al., 2008). Interestingly, the range of variation
in RNC (0.292.23 mmol g1) and respiration rates (1.89
34.6 nmol g1 s1) covered by our 74 herbaceous and dwarf
shrub species represents 67% and 45%, respectively, of the ranges
reported by Reich et al. (2008) for 744 observations on woody
and herbaceous species (Fig. S3). In addition, the slope of the
root respirationRNC relationship is consistent between the two
data sets. This relationship is associated with the concentration of
key enzymes that drive expensive metabolic processes such as
uptake, assimilation and transport of nutrients (Reich et al.,
2008). Surprisingly, the root respiration rate was not related to
the water-soluble compound concentration. One explanation is
that water-soluble compounds do not represent only carbohydrates (i.e. the primary compounds metabolized during the respiration process; Atkin et al., 2000), but a mixture of molecules, or
that respiration, which was measured on excised roots in our
study, was linked to maintenance rather than to growth respiration. Fine-root respiration rate was also influenced by morphology and increased with increasing SRL, in agreement with
previous studies (Tjoelker et al., 2005; Makita et al., 2012), and
decreased with increasing root diameter and RDMC. At the
interspecific level, thinner roots are thus metabolically more
active than thicker roots, as a result of their involvement in water
and nutrient uptake, as demonstrated among root orders within a
species (Jia et al., 2013; Rewald et al., 2014). Among species, root
diameter has been reported to increase linearly with stele diameter (Wahl & Ryser, 2000; Hummel et al., 2007; Guo et al., 2008;
Kong et al., 2014) and the lignin : N ratio (this study). As a consequence, thicker roots have a higher transport capacity but lower
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metabolic activity, as previously shown by Picon-Cochard et al.

(2012) for 13 grass species and by Jia et al. (2013) for two tree
species.
The drivers of fine-root decomposability were less obvious
than those of respiration because they differed between
graminoids and eudicots. Decomposability was driven by both
chemical and morphological traits in graminoids, but only by the
lignin : N ratio in eudicots. The lack of a general pattern across
the two groups suggested that decomposability is a much more
complex process than respiration, depending both on root traits
and on the interaction with the standard microbial community
during the incubation. In agreement with meta-analyses on root
decomposition (Silver & Miya, 2001; Zhang et al., 2008), this
study emphasizes that the lignin : N ratio is a valuable predictor
for root decomposability overall and within each group of
species. In particular, lignin controls decomposition rates
through its resistance to enzymatic attack, while N is an essential
and limiting element for the metabolism of microbial decomposers (Berg & McClaugherty, 2008).
Although root respiration and decomposability were not
driven by the same traits, the two processes were significantly and
negatively correlated overall and within each group, suggesting
that roots characterized by a high metabolic rate also decomposed
more rapidly, and thus potentially released together more CO2 to
the atmosphere. This connection between root respiration (a key
component of the plant C economy) and decomposability (a key
component of the soil C cycle) is crucial both for understanding
vegetationsoil feedbacks (Cornwell et al., 2008) and for improving terrestrial biosphere models predicting the consequences of
plant community changes for C cycling (Warren et al., 2015).
The understanding of the role of these processes in global C
cycling, however, requires further determination of root turnover
rates and of diurnal and seasonal variations in root respiration.
Limits and perspectives
Despite using standardized methods, the correlation coefficients
between root structure and function remained lower than those
reported in the leaf economics spectrum (Wright et al., 2004;
Cornwell et al., 2014). This result may be attributable to the
heterogeneity of the growing conditions at the different sites
which impacted root trait values, but also to the heterogeneity of
the fine-root pool considered, which comprised different root
orders that differed in structure and function (Pregitzer et al.,
2002; Guo et al., 2008; Valenzuela-Estrada et al., 2008; PiconCochard et al., 2012; Rewald et al., 2014). Within the fine-root
pool, the proportion of biomass allocated to absorptive roots (i.e.
the most distal roots, which are the analogues of leaves) varies
among species. For example, it may represent from 10% to 58%
of roots 2 mm in woody species, but from 60% to 100% in
herbaceous species (McCormack et al., 2015). In our study,
where 80% of the species were herbaceous, and where 90% of
root length had a diameter < 0.5 mm, this bias may be low. To
improve the consistency of the RES, it would be necessary to
adopt the functional approach proposed by McCormack et al.
(2015), consisting of selecting only absorptive roots. This
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approach is particularly important for broad interspecific comparative studies including tree and herbaceous species. Nevertheless, the methodology remains challenging for herbs that have
very fine and breakable roots and for which there is no clear evidence in the literature of which orders are absorptive. Another
potential cause of weaker correlations for fine roots than for
leaves is the complex nature of absorptive roots which perform
multiple functions simultaneously (e.g. exudation, water and
nutrient uptake, and symbiosis with N2-fixing bacteria or mycorrhizal fungi). These functions may be controlled positively or
negatively by similar traits and thus have to face conflicting
demands.
Conclusions
This study on 74 herbaceous and shrubby species from contrasting biomes is original as we measured simultaneously, and using
the same methods, a large number of root traits, including two
processes that have a major impact on plant and soil C cycling.
Our study highlights the existence, at the interspecific level, of
strong covariations among morphological and chemical traits that
influence root functioning. We demonstrated an RES, in which
root respiration is tightly correlated to SRL, RNC, RDMC and
root decomposability, which is of fundamental importance to
better understand the role of fine roots in soil C storage and CO2
release. This study needs, however, to be extended to other phylogenetic lineages world-wide and also to other root functions. In
particular, a next step for a better understanding of root functioning and trade-offs would be to consider root life span and water
and nutrient acquisition, as well as to determine whether the RES
reflected aboveground trade-offs between function and structure.

Acknowledgements
This study was funded by the Fondation pour la Recherche sur la
Biodiversit
e (FRB, France) through the projet innovant
RESPIRS, AAP-IN-2009-046), INRA (Jeune Equipe), and the
Agence Nationale de la Recherche (projects O2LA ANR-09STRA-09 and Ecosfix ANR-10-STRA-003-001). M.B. was
financed by the Agence de lEnvironnement et de la Ma^trise de
lEnergie (ADEME) and the Centre International d
etudes
sup
erieures en sciences agronomiques (Montpellier SupAgro).
Bursaries are gratefully acknowledged for M.G. (AgroParis Tech,
France; FCPR programme) and N.O. (University of Malaya,
Malaysia). Thanks are due to Ivan Prieto for statistical advice, to
the Town Hall and Forest Office of Daxingdi, Township,
Nujiang Prefecture, and Xishuangbanna Tropical Botanical
Garden, Chinese Academy of Sciences, Yunnan, China, for access
to field sites, to the staff of the CEFE experimental field (France),
of the Plateforme dAnalyses Chimiques en Ecologie (technical
facilities of the Labex Centre M
editerran
een de lEnvironnement
et de la Biodiversit
e) and of the INRA-UREP laboratory, where
morphological and chemical analyses were performed. We thank
F. Pailler (INRA, France), A. Blanchard, J. Goldin and D.
Delgueldre (CEFE, France), Yun-Hong Tang (XTBG, China),
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S. Revaillot, P. Pichon and A Augusti (INRA-UREP, France) for

technical assistance.

Author contributions
C.R., C.P-C. and A.S. designed the study, A.S., C.P-C., C.R.,
M.B., M.G., N.O. and S.V-B. performed analyses, A.S., C.P-C.,
C.R. and K-f.C. provided materials and methods, C.R. wrote the
first draft of the manuscript, and A.S., C.P-C. and K-f.C. contributed substantially to revisions.

References
Atkin OK, Edwards EJ, Loveys BR. 2000. Response of root respiration to
changes in temperature and its relevance to global warming. New Phytologist
147: 141154.
Bakker MA, Carre~
no-Rocabado G, Poorter L. 2011. Leaf economics traits
predict litter decomposition of tropical plants and differ among land use types.
Functional Ecology 25: 473483.
Bardgett RD, Mommer L, De Vries FT. 2014. Going underground: root traits as
drivers of ecosystem processes. Trends in Ecology and Evolution 29: 692699.
Berg B, McClaugherty C. 2008. Plant litter: decomposition, humus formation,
carbon sequestration. Berlin, Germany: Springer-Verlag.
Birouste M, Kazakou E, Blanchard A, Roumet C. 2012. Plant traits and
decomposition: are the relationships for roots comparable to those for leaves?
Annals of Botany 109: 463472.
Birouste M, Zamora-Ledezma E, Bossard C, P
erez-Ramos IM, Roumet C.
2014. Measurement of fine root tissue density: a comparison of three
methods reveals the potential of root dry matter content. Plant and Soil
374: 299313.
Chen W, Zeng H, Eissenstat DM, Guo D. 2013. Variation of first-order root
traits across climatic gradients and evolutionary trends in geological time.
Global Ecology and Biogeography 22: 846856.
Comas LH, Eissenstat DM. 2009. Patterns in root trait variation among
25 co-existing North American forest species. New Phytologist 182:
919928.
Cornelissen JHC, Thompson K. 1997. Functional leaf attributes predict litter
decomposition rate in herbaceous plants. New Phytologist 135: 109114.
Cornwell W, Cornelissen J, Amatangelo K, Dorrepaal E, Eviner V, Godoy O,
Hobbie S, Hoorens B, Kurokawa H, P
erez-Harguindeguy N et al. 2008.
Plant species traits are the predominant control on litter decomposition rates
within biomes worldwide. Ecology Letters 11: 10651071.
Cornwell WK, Westoby M, Falster DS, Fitzjohn RG, OMeara BC, Pennell
MW, Mcglinn DJ, Eastman JM, Moles AT, Reich PB et al. 2014.
Functional distinctiveness of major plant lineages. Journal of Ecology 102:
345356.
Craine JM, Froehle J, Tilman DG, Wedin DA, Chapin FS. 2001. The
relationships among root and leaf traits of 76 grassland species and relative
abundance along fertility and disturbance gradients. Oikos 93: 274285.
Craine JM, Lee WG, Bond WJ, Williams RJ, Johnson LC. 2005. Environmental
constraints on a global relationship among leaf and root traits of grasses. Ecology
86: 1219.
Fort F, Cruz P, Catrice O, Delbrut A, Luzarreta M, Stroia C, Jouany C. 2015.
Root functional trait syndromes and plasticity drive the ability of grassland
Fabaceae to tolerate water and phosphorus shortage. Environmental and
Experimental Botany 110: 6272.
Fort F, Jouany C, Cruz P. 2013. Root and leaf functional trait relations in
Poaceae species: implications of differing resource-acquisition strategies. Journal
of Plant Ecology 6: 211219.
Freschet GT, Aerts R, Cornelissen JHC. 2012. A plant economics spectrum of
litter decomposability. Functional Ecology 26: 5665.
Freschet GT, Cornelissen JHC, van Logtestijn RSP, Aerts R. 2010. Evidence of
the plant economics spectrum in a subarctic flora. Journal of Ecology 98: 362
373.

2016 CNRS
New Phytologist 2016 New Phytologist Trust

New
Phytologist
Ghestem M, Cao K, Ma W, Rowe N, Leclerc R, Gadenne C, Stokes A. 2014. A
framework for identifying plant species to be used as ecological engineers for
fixing soil on unstable slopes. PLoS ONE 9: e95876.
Guo D, Xia M, Wei X, Chang W, Liu Y, Wang Z. 2008. Anatomical traits
associated with absorption and mycorrhizal colonization are linked to root
branch order in twenty-three Chinese temperate tree species. New Phytologist
180: 673683.
Hobbie SE, Oleksyn J, Eissenstat DM, Reich PB. 2010. Fine root
decomposition rates do not mirror those of leaf litter among temperate tree
species. Oecologia 162: 505513.
Hummel I, Vile D, Violle C, Devaux J, Ricci B, Blanchard A, Garnier E,
Roumet C. 2007. Relating root structure and anatomy to whole-plant
functioning in 14 herbaceous Mediterranean species. New Phytologist 173:
313321.
Ibrahima A, Joffre R, Gillon D. 1995. Changes in litter during the initial
leaching phase: an experiment on the leaf litter of Mediterranean species. Soil
Biology and Biochemistry 27: 931939.
Jia S, McLaughlin NB, Gu J, Li X, Wang Z. 2013. Relationships between root
respiration rate and root morphology, chemistry and anatomy in Larix gmelinii
and Fraxinus mandshurica. Tree Physiology 33: 579589.
Jones DL, Nguyen C, Finlay RD. 2009. Carbon flow in the rhizosphere: carbon
trading at the soilroot interface. Plant and Soil 321: 533.
Kong D, Ma C, Zhang Q, Li L, Chen X, Zeng H, Guo D. 2014. Leading
dimensions in absorptive root trait variation across 96 subtropical forest species.
New Phytologist 203: 863872.
Lindedam J, Magid J, Poulsen P, Luxhi J. 2009. Tissue architecture and soil
fertility controls on decomposer communities and decomposition of roots. Soil
Biology and Biochemistry 41: 10401049.
Makita N, Kosugi Y, Dannoura M, Takanashi S, Niiyama K, Kassim AR, Nik
AR. 2012. Patterns of root respiration rates and morphological traits in 13 tree
species in a tropical forest. Tree Physiology 32: 303312.
McCormack LM, Adams TS, Smithwick EAH, Eissenstat DM. 2012. Predicting
fine root lifespan from plant functional traits in temperate trees. New
Phytologist 195: 823831.
McCormack LM, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D,
Erik A, Iversen CM, Jackson RB. 2015. Redefining fine roots improves
understanding of below-ground contributions to terrestrial biosphere processes.
New Phytologist 207: 505518.
Mommer L, Weemstra M. 2012. The role of roots in the resource economics
spectrum. New Phytologist 195: 725727.
Pages L, Picon-Cochard C. 2014. Modelling the root system architecture of
Poaceae. Can we simulate integrated traits from morphological parameters of
growth and branching? New Phytologist 201: 149158.
Picon-Cochard C, Pilon R, Tarroux E, Pages L, Robertson J, Dawson L. 2012.
Effect of species, root branching order and season on the root traits of 13
perennial grass species. Plant and Soil 353: 4757.
Pilon R, Picon-Cochard C, Bloor JMG, Revaillot S, Kuhn E, Falcimagne R,
Balandier P, Soussana JF. 2013. Grassland root demography responses to
multiple climate change drivers depend on root morphology. Plant and Soil
364: 395408.
Pregitzer KS, Deforest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL.
2002. Fine root architecture of nine North American trees. Ecological
Monographs 72: 293309.
Prieto I, Roumet C, Cardinael R, Dupraz C, Jourdan C, Kim JH, Maeght JL,
Mao Z, Pierret A, Portillo N et al. 2015. Root functional parameters along a
land-use gradient: evidence of a community-level economics spectrum. Journal
of Ecology 103: 361373.
R Development Core Team 2013. R: a language and environment for statistical
computing. Vienna, Austria: R Development Core Team.
Raunkiaer C. 1934. The life forms of plants and statistical plant geography. Oxford,
UK: Oxford University Press.
Reich PB. 2014. The world-wide fast-slow plant economics spectrum: a traits
manifesto. Journal of Ecology 102: 275301.
Reich PB, Tjoelker MG, Pregitzer KS, Wright IJ, Oleksyn J, Machado JL.
2008. Scaling of respiration to nitrogen in leaves, stems and roots of higher
land plants. Ecology Letters 11: 793801.

2016 CNRS
New Phytologist 2016 New Phytologist Trust

Research 11
Rewald B, Rechenmacher A, Godbold DL. 2014. Its complicated: intraroot
system variability of respiration and morphological traits in four deciduous tree
species. Plant Physiology 166: 736745.
Roumet C, Lafont F, Sari M, Warembourg F, Garnier E. 2008. Root traits and
taxonomic affiliation of nine herbaceous species grown in glasshouse
conditions. Plant and Soil 312: 6983.
Roumet C, Urcelay C, D
az S. 2006. Suites of root traits differ between annual
and perennial species growing in the field. New Phytologist 170: 357368.
Santiago LS. 2007. Extending the leaf economics spectrum to decomposition:
evidence from a tropical forest. Ecology 88: 11261131.
Silver WL, Miya RK. 2001. Global patterns in root decomposition: comparisons
of climate and litter quality effects. Oecologia 129: 407419.
Taylor B, Parkinson D. 1988. A new microcosm approach to litter
decomposition studies. Canadian Journal of Botany 66: 19331939.
Tjoelker MG, Craine JM, Wedin D, Reich PB, Tilman D. 2005. Linking leaf
and root trait syndromes among 39 grassland and savannah species. New
Phytologist 167: 493508.
Valenzuela-Estrada LR, Vera-Caraballo V, Ruth LE, Eissenstat DM. 2008. Root
anatomy, morphology, and longevity among root orders in Vaccinium
corymbosum (Ericaceae). American Journal of Botany 95: 15061514.
Valverde-Barrantes OJ, Smemo KA, Blackwood CB. 2015. Fine root
morphology is phylogenetically structured, but nitrogen is related to the plant
economics spectrum in temperate trees. Functional Ecology 29: 796807.
Van Der Krift TAJ, Berendse F. 2002. Root life spans of four grass species
from habitats differing in nutrient availability. Functional Ecology 16: 198
203.
Van Soest PJ. 1963. Use of detergents in the analysis of fibrous feeds. II. A rapid
method for the determination of fiber and lignin. Journal of the Association of
Official Analytical Chemists 46: 829835.
Vogel J. 2008. Unique aspects of the grass cell wall. Current Opinion in Plant
Biology 11: 301307.
Wahl S, Ryser P. 2000. Root tissue structure is linked to ecological strategies of
grasses. New Phytologist 148: 459471.
Warembourg FR, Roumet C, Lafont F. 2003. Differences in rhizosphere carbonpartitioning among plant species of different families. Plant and Soil 256:
347357.
Warren JM, Hanson PJ, Iversen CM, Kumar J, Walker AP, Wullschleger SD.
2015. Root structural and functional dynamics in terrestrial biosphere models
evaluation and recommendations. New Phytologist 205: 5978.
Withington JM, Reich PB, Oleksyn J, Eissenstat DM. 2006. Comparisons of
structure and life span in roots and leaves among temperate trees. Ecological
Monographs 76: 381397.
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F,
Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M et al. 2004. The
worldwide leaf economics spectrum. Nature 428: 821827.
Zhang D, Hui D, Luo Y, Zhou G. 2008. Rates of litter decomposition in
terrestrial ecosystems: global patterns and controlling factors. Journal of Plant
Ecology 1: 8593.

Supporting Information
Additional supporting information may be found in the online
version of this article.
Fig. S1 Distribution of root length in different diameter classes
(from 0 to 2 mm, with a 0.1-mm diameter interval) of fine roots
sampled for the 74 species studied.
Fig. S2 Relationships between (A) fine-root respiration, (B)
remaining mass, and fine root traits of 74 species.
Fig. S3 Relationships between fine-root respiration and root
nitrogen concentration.

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Table S1 List of species studied and their characteristics

Table S2 Description of sites and growing conditions where the
species were harvested
Table S3 Means, SE and number of replicates of the 12 traits
measured on fine roots ( 2 mm) of 74 species

Table S4 Principal component analysis of eight root traits from

74 species
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