Tree Physiology 21, 555–560
© 2001 Heron Publishing—Victoria, Canada
Vertical distribution of fine root density, length density, area index and
mean diameter in a Quercus ilex forest
B. LÓPEZ,1–3 S. SABATÉ1,2 and C.A. GRACIA1,2
1
Departament d’ Ecologia, Facultat de Biologia, Universitat de Barcelona, Avgda. Diagonal, 645-08028 Barcelona, Spain
2
Centre de Recerca Ecològica i Aplicacions Forestals (CREAF), Edifici Ciències, 08193 Bellaterra, Spain
3
Present address: CEFE-CNRS DREAM Unit, 1919, Rue de Mande, 34293 Montpellier Cedex 5, France
Received July 24, 2000
Summary We used minirhizotrons to determine the vertical
distribution of fine roots in a holm oak (Quercus ilex L.) forest
in a typical Mediterranean area over a 3-year period (June
1994–March 1997). We measured fine root density (number of
roots per unit area), fine root length density (length of roots per
unit area), fine root area index (area of roots per unit area) and
fine root mean diameter. Variables were pooled for each 10-cm
depth interval to a depth of 60 cm. Fine roots tended to decrease
with increasing depth except between 0 and 10 cm, where the
values of all fine root variables were less than in the 10-cm stratum below. Fine root vertical distribution was compared with
soil water content and soil temperature at different depths in
the soil profile.
Keywords: holm oak, minirhizotron, soil water.
Introduction
The study of fine roots, which provide the chemical and hydraulic interface between a tree and the soil, has been limited
by observational difficulties. Minirhizotrons permit observation of roots in situ with minimal disturbance to the surrounding soil (Upchurch and Ritchie 1983), and thus make it
possible to observe changes over time in the number, length,
area and diameter of fine roots without disturbing the soil or
damaging the roots.
Fine root distribution decreases with soil depth in most forest ecosystems (Persson 1983, Joslin and Henderson 1987,
Nambiar 1993, Burke and Raynal 1994). This may reflect the
distribution of nutrients returned to the soil by way of litterfall,
canopy leachates and stemflow, tropism for organic matter, or
the successional status of the forest. Other factors that may
contribute to reduced root density with depth include an increase with depth in the proportion of silt and clay, and hence
soil strength, and decreases with depth in soil fertility, organic
matter content and aeration.
In arid or semiarid areas such as the Mediterranean, where
summer and winter droughts are common and severe, soil water availability is generally lower in the uppermost soil layer
than in deeper layers (Canadell et al. 1999). This may restrict
fine root growth in the uppermost soil layers, even though nu-
trient concentrations in these layers may be higher than in
deeper horizons. In this study, we tested the hypothesis that
environmental conditions alter the vertical distribution of fine
roots of holm oak (Quercus ilex L.). Specifically, we determined the vertical distribution of fine root density (number of
roots per unit area, FRD), fine root length density (length of
roots per unit area, FRLD), fine root area index (area of fine
roots per unit area, FRAI) and fine root mean diameter (FRDi)
in a forest dominated by holm oak, a typical Mediterranean
species, over 3 years. The vertical distribution of soil water
content and soil temperature were also measured to determine
their possible relationship with fine root vertical distribution.
Materials and methods
The study was carried out in a holm oak (Quercus ilex) forest
at the Prades Experimental Complex of Catchments (PECC,
NE Spain, 41°13′ N, 0°55′ E). The climate is typically Mediterranean, with hot, dry summers, wet springs and autumns,
and mild, dry winters. Main stand-level characteristics of the
PECC are summarized in Table 1.
The main rock type in the area is schist and the soils are
Xeroschrepts (USDA Soil Taxonomy 1975), with subgroups
differing with topographic position: lithic on the upper slope
of the catchments and typic on the valley bottom. The dominant soil texture is a well-structured clay loam with a pH
around 5–6.3. Soil depth ranges between 30 and 80 cm, but
reaches 150 cm at the valley bottom. There is a high content of
coarse rock fragments in the soil profile, beginning in the shallowest horizons. The rock fragments are mainly medium-sized
shales (Table 2).
Until the 1960s, this north-facing forest was coppiced every
20–25 years to yield approximately 150 Mg wood ha –1, which
was used for the production of charcoal. This management resulted in a multi-stemmed aboveground structure with an extremely high density, reaching a maximum of up to
18,500 stems ha –1. Such densities make these forests difficult
to penetrate by wind and humans, so it has remained unaltered
during recent decades. In the experimental plots the mean
aboveground biomass of the tree layer is 103 Mg ha –1, leaf
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LÓPEZ, SABATÉ AND GRACIA
Table 1. Stand-level characteristics of the experimental area.
Altitude (m, a.s.l.)
Aspect
Mean slope (°)
Mean annual precipitation (mm)
Potential evapotranspiration (mm)
Mean annual air temperature (°C)
Stand age (years)
Dominant height (m)
Mean diameter at breast height (m)
Basal area (m 2 ha –1)
Aboveground biomass (Mg ha –1 )
Belowground biomass (Mg ha –1 )
Leaf biomass (Mg ha –1 )
Leaf area index (m 2 m –2 )
Fine root biomass (Mg ha –1 )
650–750
NE
20–25
537
1051
10
40
6.6
0.099
37.1
103.1
128
6
3.63
0.71
biomass is about 6 Mg ha –1 and net primary production is
about 10 Mg ha –1 year –1. Diameter growth rate in the PECC is
very low, averaging 0.29 mm year –1 for the period 1992–1995
(Gracia et al. 1999). Leaf net primary production is 2.5 Mg
ha –1 year –1, and mean foliar litterfall production is 2.3 Mg
ha –1 year –1, ranging between 2.2 and 5.8 Mg ha –1 year –1 depending on period, site and topographic position.
To observe fine roots, we used inflatable minirhizotrons
made from motorcyle tire inner tubes, which were developed
for use in stony soils (López et al. 1996). In April 1994, six
minirhizotrons were installed in each of two plots. The first
roots appeared after 2 months. When observations were to be
made, the minirhizotrons were deflated and removed from the
ground. Following each set of measurements, the minirhizotrons were reinstalled. Images were collected on an 8-mm videotape with an Olympus KMI Portable Video System PVS-2
connected to an Olympus OES Borescope (1-cm diameter, 90°
direction of view and a field of view of 55°). Illumination was
provided by an Olympus Multi-Function Light Source
(KMF-5 with a 100-W tungsten halogen lamp). Images were
collected every 2 cm along the minirhizotron. The software
used to analyze the images was IMAT, an image treatment
program developed by the Scientific Services of the University of Barcelona. Recorded images were digitized and the
roots manually traced with a mouse. A total of 10,313 roots
(1212 roots in 39 field campaigns between June 1994 and
March 1997) were traced. Roots were coded so that sampling
date, plot, minirhizotron, soil depth, root number and color
could be identified. Root area (RA) and perimeter (RP) were
obtained for each fine root. To estimate the lengths and diameters of the recorded fine root images, samples of fine roots
were collected from the study site at various depths and their
RA and RP measured. Regression equations were then developed relating RA and RP to fine root length (= – 0.13912 RA
+ 0.481044 RP, n = 44, r 2 = 0.95) and the log of fine root diameter (= 1.6703 + 1.4054 log(RA) – 1.6907 log(RP), n = 44,
r 2 = 0.91). Results with roots from different soil horizons were
similar and a single regression model for all layers was used.
Soil water content was measured by time domain reflectometry (TDR) (Dalton et al. 1984, Zegelin et al. 1989). In each
of two plots, a TDR probe was installed at three depths: 0–15,
0–30 and 0–50 cm. Measurements were made during each
root sampling campaign (i.e., every 2 or 3 weeks).
Thermister probes were installed at depths of 15 and 25 cm
and temperature logged every 5 min and averaged every
30 min.
Statistical analyses were performed with the SPSS statistical software package (SPSS Inc., Chicago, IL). In a MANOVA, fine root variables (FRD, FRLD, FRAI and FRDi) were
tested against three factors: plot (2 levels), minirhizotron
(6 levels per plot), and depth interval (6 levels per minirhizotron). Season was the within-subject factor. Variables were
arcsin transformed to match normality assumptions. Soil water content and soil temperature values were similarly analyzed, but data were not transformed. Soil temperature values
at 15- and 25-cm depths were compared by a two-sample
paired t-test.
Results
Soil water content
Figure 1 shows the mean soil water content for the three depth
intervals sampled. Differences between depth intervals and
between seasons were significantly different (P < 0.001), but
the pattern did not change over time (interaction was not significant). At each depth interval there were significant differences in soil water content between seasons (P ≤ 0.001). The
0–15- and 15–30-cm depth intervals had similar soil water
contents (around 6% by soil volume), whereas the 30–50-cm
depth interval had a higher value (11.5%). Among depth intervals, soil water content was highest in the 30–50-cm depth interval in all seasons (Figure 2). At all depth intervals, soil
water content was lowest in summer and highest in winter.
However, seasonal differences were greater in the 30–50-cm
Table 2. Soil characteristics at the Prades Experimental Complex of Catchments (adapted from Serrasolses 1994).
Depth (cm)
0–2.5
2.5–30
30–55
Horizon
A11
A12
Bw
Coarse gravel (%)
59.7
73.4
91.4
Fine gravel (%)
25.2
23.8
39.7
Sand (%)
20.2
41.1
26.4
TREE PHYSIOLOGY VOLUME 21, 2001
Silt (%)
25.9
12.8
22.7
Clay (%)
28.7
22.3
11.1
pH
H2 O
HCl
6.2
4.8
4.9
5.6
3.9
4.0
FINE ROOT VERTICAL DISTRIBUTION
Figure 1. Vertical distribution of soil water content (% volume) in the
0–15-, 15–30- and 30–50-cm depth intervals. Values were obtained
with TDR methodology and represent the mean ± SE of all field campaigns between June 1994 and March 1997.
depth interval than in the 0–15- and 15–30-cm depth intervals.
Soil temperature
Although the annual mean temperature at soil depths of 15 and
25 cm did not differ significantly (11.3 ± 4.8 °C at 15 cm versus 12.3 ± 5.3 °C at 25 cm), there was a significant difference
between depths in the annual variation in temperature (Figure 3). At 15 cm, the difference between the minimum temperature (2.0 °C, measured in February) and the maximum
temperature (22.9 °C, measured in July) was 20.9 °C, whereas
at 25 cm the difference was 24.4 °C (0.8 °C in February and
25.2 °C in July). There were significant monthly differences in
soil temperatures at both the 15- and 25-cm depths (P ≤ 0.001).
Fine root density
Excluding the 0–10-cm depth interval, the vertical distribution
of FRD (number of roots cm –2 ), pooled for all the field campaigns for each depth interval, decreased with increasing soil
depth until the 50–60-cm depth interval, where FRD was
higher than in the soil layer above (Figure 4a). Maximum FRD
(27% of the total FRD) was observed in the 10–20-cm depth
interval, whereas the 0–10- and 20–30-cm soil layers had similar FRD values (Table 3). Differences in FRD between depth
intervals were significant in all seasons, even though season
affected FRD in all but the 50–60-cm depth interval. Although
FRD changed with time, the vertical distribution pattern did
557
Figure 3. Monthly soil temperature at 15- and 25-cm depths at the
Prades Experimental Complex of Catchments (mean ± SE).
not (Figure 5a). At all depth intervals except the 50–60-cm
depth interval, FRD was lower in autumn than at other times of
year. Fine root density values were generally highest in summer.
Fine root area index
The vertical distribution of FRAI (mm 2 cm –2 ) fell with increasing soil depth, with the exception that the 0–10-cm horizon had lower values than the 10–20-cm horizon (Figure 4b).
The first 20 cm of soil contained 41% of total surface area, and
the first 30 cm contained 65% of total surface area. In contrast
to FRD, FRAI showed significant seasonal differences at all
depth intervals. Within a season, differences between depth
intervals were also significant (Figure 5b). Values of FRAI
were highest in spring (except in the deepest depth interval),
and lowest in autumn.
Fine root length density
Fine root length density (FRLD, mm cm –2 ) decreased with increasing depth, with the exception of the first depth interval
(Figure 4c). Almost 27% of the total FRLD was in the
10–20-cm depth interval, and 44 and 69% of the total FRLD
was in the first 20 and 30 cm of soil, respectively (Table 3).
The deepest horizon investigated (50–60 cm) contained only
6.5% of the total FRLD. Although we found significant differences in FRLD both between depth intervals within each season and within each depth interval between seasons, the
pattern of vertical distribution was similar (Figure 5c). In most
depth intervals, highest values of FRLD were found in summer and lowest values were recorded in autumn.
Fine root diameter
Except for the deepest roots, mean diameters of all fine roots
fluctuated between 0.18 and 0.29 mm (Figure 4d). Roots in the
first 30 cm of soil were, on average, thicker than roots in the
30–60-cm depth interval (0.25 ± 0.003 versus 0.15 ±
0.04 mm). Fine roots generally had larger diameters in spring
and were smallest in summer and autumn (Figure 5d).
Discussion
Figure 2. Effect of season on soil water content (% volume, mean ±
SE) in the 0–15-, 15–30- and 30–50-cm depth intervals for the period
June 1994 through March 1997. Values are within season means.
All fine root density parameters (FRD, FRLD, FRAI and
FRDi) measured in the Prades holm oak forest peaked in the
second (10–20 cm) soil horizon, whereas in most forest ecosystems fine roots are most abundant in the uppermost soil
layer and decrease in frequency continuously with depth (Jos-
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558
LÓPEZ, SABATÉ AND GRACIA
Figure 4. Vertical distribution of fine
root density, FRD (a), fine root area index, FRAI (b), fine root length density,
FRLD (c) and fine root diameter, FRDi
(d). Values are the mean ± SD for all
field campaigns within each depth interval.
lin and Henderson 1987, Burke and Raynal 1994, Hendrick
and Pregitzer 1996, Steele et al. 1997).
A further indication of the relatively deep distribution of
fine roots in the Prades holm oak stand is that the proportion of
total FRD, FRLD or FRAI in the top 40 cm of soil (around
70%) is similar to the proportions found in the top 20–30 cm
of soil in other, more northern, forest systems (63–70% of
Pinus radiata FRD (Nambiar 1983); 63% of pine-hardwood
forests FRAI (Farrish 1972); and > 69% of Picea mariana
(Mill.) BSP FRLD (Steele et al. 1997)).
Three factors seem most likely to explain the relatively low
frequency of fine roots in the uppermost 10 cm of the soil profile in the Prades forest. First is the aridity of the site, which
may cause the uppermost soil lay to desiccate more severely
than deeper layers, thereby restricting fine root proliferation.
Second, is the coarse texture of the soil, which may allow percolating water to carry mineral nutrients returned to the soil
through mineralization of litter, canopy leaching and stemflow deeper into the soil profile. Third, is temperature, which
may be sufficiently high to inhibit fine root development in the
uppermost soil layer.
Our soil water measurements were not sufficiently finely
scaled to demonstrate a gradient in water content between the
0–10- and 10–20-cm soil layers. In the 0–15- and 15–30-cm
soil layers, soil water contents were similar. However, our results do not preclude the possibility that the uppermost 10 cm
of soil was drier than the 10-cm layer beneath. Moreover, the
Table 3. Percentages of fine root density, FRD (roots cm –2 ), fine root
length density, FRLD (mm cm –2 ) and fine root area index, FRAI
(mm 2 cm –2 ) in each 10-cm depth interval.
Depth interval (cm)
FRD
FRLD
FRAI
0–10
10–20
20–30
30–40
40–50
50–60
19.74
27.36
21.81
15.82
5.79
9.71
16.35
24.97
21.03
19.06
8.74
9.80
15.40
25.99
23.81
17.55
11.03
6.21
Figure 5. Effect of season on vertical distribution of fine root density,
FRD (a), fine root area index, FRAI (b), fine root length density,
FRLD (c) and fine root diameter, FRDi (d). Values are the mean ± SD
for all field campaigns within each season.
TREE PHYSIOLOGY VOLUME 21, 2001
FINE ROOT VERTICAL DISTRIBUTION
soil at Prades, which is of colluvial origin, contains a high proportion of gravel that facilitates percolation, so it is likely that
water availability sometimes increases with soil depth within
the uppermost 20 cm of soil.
The role of mineral nutrient availability in explaining the
relatively low fine root frequency in the uppermost soil
horizon at Prades is suggested by the work of Kätterer et al.
(1995) who reported a similar vertical pattern of fine root distribution in an irrigated and fertilized Eucalyptus globulus
Labill plantation. They interpreted their finding as evidence
that nutrients were carried through the soil profile with the irrigation water, thereby promoting a deep distribution of roots.
Although we did not measure soil or water nutrient concentrations, Melià et al. (1999) and Serrasolses (1994) carried out
studies in nearby plots in the Prades forest and showed that
water collected below the forest floor had higher volume-weighted ion concentrations than water collected at
greater depths. However, they also found that water carried
solutes from the forest floor and topsoil to the deeper horizons,
and reported that plant uptake was greatest at a depth of about
30-cm, which is consistent with our finding of high fine root
density at this depth.
In addition, Serrasolses (1994) measured soil nitrogen dynamics in Prades and found that, on an annual basis, 71% of
net N mineralization takes place in the 5–20-cm soil layer. She
also reported that nitrate concentrations in percolating water
decreased with depth, probably because of plant uptake.
These findings are, therefore, consistent with the view that
mineral nutrient availability accounts for the inverted vertical
density distribution in the uppermost soil layers at Prades.
Unfortunately, our temperature data do not differentiate between the uppermost 10 and 20-cm horizons. We are unable,
therefore, to exclude the role of temperature in restricting root
proliferation near the soil surface.
Several studies have shown that fine root distribution data
obtained with minirhizotrons for the uppermost 10 cm of soil
differ from those obtained by the analysis of soil cores (Bragg
et al. 1983, Upchurch and Ritchie 1983, Vos and Groenwold
1987, Samson and Sinclair 1994). In general, it appears that
the minirhizotron observations give lower fine root densities
than soil cores (Singh et al. 1984, Van Noordwijk et al. 1985,
Kurz and Kimmins 1987, Vogt and Persson 1991, Nadelhoffer
and Raich 1992, Publicover and Vogt 1992). It is possible,
therefore, that a sampling error, due to the use of minirhizotrons, accounts for the lower observed percentage of fine roots
in the top layer of soil at Prades than in the subadjacent layer.
This question remains to be resolved as soil cores were not
taken.
Another difference between our results and the generally
observed, fine-root distribution patterns was our finding that
FRD was higher in the 50–60-cm depth interval than in the
40–50-cm depth interval (9.7 versus 5.8%, respectively). This
may reflect the existence of bedrock with few cracks at a depth
of 50 to 100 cm, which by trapping water, may have improved
water availability in the 50–60-cm depth interval relative to
the horizon immediately above.
559
Although FRD was higher in the 50–60-cm depth interval
than in the 40–50-cm depth interval, FRAI was lower, indicating that although roots in the deeper horizon are more
numerous, they are thinner, resulting in a lower total root surface area.
Except in the 50–60-cm depth interval, mean fine root diameter was between 0.18 and 0.30 mm. These values are
slightly lower than those reported by Hendrick and Pregitzer
(1992) for a northern hardwood forest (around 0.42 mm), but
similar to those measured by Roberts (1976) for a Pinus
sylvestris L. stand: 0.28 mm in the first 15 cm and increasing
with depth. However, contrary to what has been postulated for
some forest types (Roberts 1976, Hendrick and Pregitzer
1992, Fahey and Hughes 1994), the similarity in fine root diameters with increasing soil depth in the Prades holm oak forest, suggests that the structure and physiology of the fine root
do not differ across the soil profile.
Soil mineralization rates at Prades are highest during summer because of high soil temperatures (Serrasolses 1994),
which is when values of FRD and FRLD were also highest.
This finding is consistent with the view that fine root proliferation is strongly influenced by mineral nutrient availability.
If fine root production is rapid during the summer, so also is
fine root mortality (López et al., unpublished results). If mortality continues at a high rate toward the end of summer, while
the proliferation fine roots declines, this would explain our observation that values of FRD, FRLD, FRAI and FRDi were
lowest in autumn, even though soil water content was high,
soil temperatures were moderate, and leaf production, which
might otherwise create a competitive sink for photosynthates,
was minimal.
Unlike FRD and FRLD, values of FRAI and FRDi were
highest in winter. This indicates a high rate of carbon allocation to fine roots at that time of year.
Acknowledgments
We are grateful for the valuable help of Ignasi Ruiz and other students
who assisted with field work. This work was funded by the European
Commission (LTEEF-I PL93-1511) and the Regional Government of
Valencia (CEAM-Centro de Estudios Ambientales del Mediterráneo).
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