Directory UMM :Data Elmu:jurnal:T:Tree Physiology:vol17.1997:

Tree Physiology 17, 39--45
© 1997 Heron Publishing----Victoria, Canada

Responses of Picea, Pinus and Pseudotsuga roots to heterogeneous
nutrient distribution in soil
ECKHARD GEORGE,1 BETTINA SEITH,1 CHRISTOPH SCHAEFFER2 and HORST
MARSCHNER1
1

Institute of Plant Nutrition, Hohenheim University, 70593 Stuttgart, Germany

2

Physiological Ecology of Plants, Botanical Institute, University of Tübingen, 72076 Tübingen, Germany

Received November 27, 1995

Summary The spatial distribution of plant-available mineral
nutrients in forest soils is often highly heterogeneous. To test
the hypothesis that local nutrient enrichment of soil leads to
increased root proliferation in the nutrient-rich soil zone, we

studied the effects of nutrient enrichment on the growth and
nutrient concentrations of Douglas-fir (Pseudotsuga menziesii
(Mirb.) Franco), Scots pine (Pinus sylvestris L.) and Norway
spruce (Picea abies (L.) Karst.) roots. Three-year-old seedlings
were grown for 9 months in split-root containers filled with
nutrient-poor forest mineral soil, with one side supplemented
with additional mineral nutrients. Root dry weight and root
length in Scots pine and Norway spruce were increased in the
nutrient-supplemented soil compared with the nonsupplemented side, whereas root growth in Douglas-fir was unaffected by nutrient enrichment. Of the three species examined,
Norway spruce exhibited the highest root and shoot growth and
the highest nutrient demand. Specific root length (m g −1) and
the number of root tips per unit root length were not affected
by local nutrient addition in any of the species. Despite increased root growth in Norway spruce and Scots pine in nutrient-supplemented soil, their root systems contained similar
nutrient concentrations on both sides of the split-root container.
Thus, coniferous trees may respond to local nutrient supply by
increased root proliferation, but the response varies depending
on the species, and may only occur when trees are nutrient
deficient. As a response to local nutrient enrichment, increases
in root dry matter or root length may be better indicators of
pre-existing nutrient deficiencies in conifers than increases in

root nutrient concentrations.
Keywords: Douglas-fir, local nutrient supply, Norway spruce,
nutrient concentrations, root growth, root morphology, Scots
pine.

Introduction
Plants may respond to a localized nutrient supply in soil by
increasing root growth in the nutrient-rich soil zones. This
response is advantageous to plants growing in soils with high
spatial heterogeneity in nutrient distribution (Crick and Grime
1987, Jackson and Caldwell 1989), because roots in the nutri-

ent-rich soil zones can absorb more nutrients than roots growing in the nutrient-poor soil zones. Thus, a high spatial plasticity of root growth may confer a competitive advantage on plant
species in patchy soils (Jackson and Caldwell 1989).
On the other hand, a large, long-lived, and in terms of
growth, relatively nonresponsive root system may be advantageous to plants on sites where nutrients become temporarily
unavailable (e.g., during soil drying cycles) (Crick and Grime
1987, Campbell and Grime 1989). For example, the competitive ability of several arid-land grass species growing on natural soils was unrelated to the spatial plasticity of root growth
(Larigauderie and Richards 1994). Some species may possess
a high physiological plasticity, i.e., an ability to increase nutrient uptake rates in existing roots during periods of high nutrient supply (Caldwell et al. 1992). In general, no consistent

predictions can be made about the advantages and disadvantages of high spatial plasticity of root growth in patchy soils
(Hutchings and de Kroon 1994, Robinson 1994). Furthermore,
many studies on root growth plasticity have been performed in
the presence of extremely high concentrations of nutrients and
on artificial substrates where root morphology differs from that
of soil-grown plants.
The spatial distribution of nutrients in natural soils is more
heterogeneous than in cultivated soils (Cattle et al. 1994). In
forest soils, nutrient contents vary greatly over distances of a
few meters (Lechowicz and Bell 1991, Koch and Matzner
1993) or even centimeters (Hildebrand 1994), for example,
stem flow effects, gaps in the crown cover, old tree stumps, or
soil fauna activity. Therefore, the response of forest trees to
local nutrient supply is of particular interest. However, although there have been some studies of root growth plasticity
in forest trees, most studies on root growth plasticity have been
done with fast-growing grass species or agricultural crop species (Larigauderie and Richards 1994, Robinson 1994).
For coniferous tree species, detailed experiments using splitroot systems with varying local nutrient concentrations have
been described by Coutts and co-authors. Sitka spruce (Picea
sitchensis (Bong.) Carr.) root growth in a peat/sand mix increased when supplemented with nutrients (Coutts and Philipson 1976), and root growth in coarse sand increased when

40

GEORGE ET AL.

supplemented with nitrogen (N) or phosphorus (P) (Philipson
and Coutts 1977). In solution culture, root growth in lodgepole
pine (Pinus contorta Dougl. ex Loud.) seedlings increased
when supplemented with nutrients (Coutts and Philipson
1977). Local N addition to a peat /vermiculite mix also increased root growth of Douglas-fir (Pseudotsuga menziesii
(Mirb.) Franco)) seedlings, particularly when the seedlings
were N deficient (Friend et al. 1990). However, because these
studies were done with artificial rooting substrates, root
growth rates may have been higher than in natural soil.
In older, forest-grown trees, the response of root growth to
local nutrient enrichment has been studied by means of
minirhizotrons or ingrowth cores. When cores were supplemented with additional nutrients, tree root growth increased
(St. John et al. 1983) when the nutrient that was supplied was
limiting in the forest ecosystem (Raich et al. 1994).
To study whether increased root growth in nutrient-rich soil
patches occurs as a general response irrespective of plant

species or plant nutrient status, we investigated the effects of
local nutrient supply in soil on root growth and distribution of
Douglas-fir, Scots pine, and Norway spruce. We also determined the effects of local nutrient supply on root length,
morphology, and nutrient concentrations.
Materials and methods
Experimental details
Three-year-old Douglas-fir (Pseudotsuga menziesii), Scots
pine (Pinus sylvestris L.), and Norway spruce (Picea abies (L.)
Karst.) seedlings were obtained from a commercial nursery. In
December 1993, single plants were placed in split-root pots
(Figure 1) with six replicates per plant species. The commercial growth substrate (peat) and approximately 50% of the
original root mass were removed before planting. After plant-

ing, one Douglas-fir and one Scots pine seedling died, leaving
five replicates each for these species.
Mineral soil (podsolic Ranker) from a Norway spruce forest
at Ludwigsreuth (southern Germany) was used as substrate on
both sides of the split-root container. The soil was taken from
5--30 cm soil depth, mixed, air-dried to 7.3% w/w water content, and sieved (5 mm). Soil pH (H2O) was 4.5; other properties of the soil are described in Table 1. Each side of the
container was filled with 1.25 kg of mineral soil, resulting in a

bulk soil density of approximately 1.15 g cm −3. Before filling,
the soil on one side of the split-root container was supplemented with 100 mg N (NH4NO3), 20 mg P (Ca(H2PO4)2),
80 mg K (K2SO4), 40 mg Mg (MgSO4), and 53 mg Ca
(Ca(H2PO4)2 and CaSO4) per kg air-dry soil.
Seedlings were planted on top of the mineral soil (Figure 1),
so that, at harvest, the mineral soil contained only roots produced during the experiment. The upper soil layer consisted of
material (sieved to 10 mm) taken from the humus horizon of
the same site as the mineral soil. The upper layer was watered
during the first four weeks of the experiment so that the trees
could establish new roots after planting. Thereafter, only the
mineral soil was watered to increase root growth in the mineral
soil and decrease nutrient uptake from the upper soil layer.
Watering of the mineral soil layer was done continuously with
deionized water using a commercial clay cone system (Blumat, Telfs, Austria). The water content of the mineral soil was
monitored with tensiometers and maintained between 6 and
10 kPa.
Trees were placed in a greenhouse with temperatures maintained above 6 °C and with additional light (350 µmol m −2 s −1)
supplied by HQL 400 W lamps from 1400 to 2200 h. The
long-day conditions induced the onset of new shoot growth in
February 1994, two months after the beginning of the experiment. At the end of April 1994, the pots were placed outdoors

in the shade for the summer period. The soil was protected
against rainwater by plastic covers, and the plants continued to
be irrigated with deionized water.

Table 1. Chemical properties of the soil used in the experiment.
mg kg −1

Nutrient
Mineral nitrogen1

NH +4
NO −3

H2O-extractable nutrients2

Ca
K
Mg
P

3.2
3.1
0.7
< 0.6

Exchangeable nutrients3

Ca
K
Mg
P

6.3
26.4
1.1
28.5

1
2
3

Figure 1. Split-root container used in the experiment.

2.6
2.1

CaCl2 extraction.
In water/soil (2/1) extract.
0.05 N NH4Cl extraction (Ca, K, Mg) or CAL (calcium acetate-lactate) extraction (P).

ROOT RESPONSES TO HETEROGENEOUS NUTRIENT DISTRIBUTION

41

Harvest
In September 1994 (after a 9-month growth period), all trees
were harvested and their roots examined with the aid of a
microscope. Ten to 70% of the lateral roots of all plants were
ectomycorrhizal, as determined by visual observation. Scots
pine mycorrhizae showed a typical dichotomous branching.

The predominant ectomycorrhizal fungus in the mineral soil
was Thelephora terrestris Ehrh.: Fr. and, in some cases, Cenococcum geophilum Fr. A detailed identification of all fungi
associated with the roots was not done. Colonization rates
were apparently not affected by the soil nutrient supply.
After harvest, shoot and roots were divided into current-year
and older tissue. Roots in the humus top layer were treated as
older roots, although approximately 5% of the root mass in this
layer was newly formed roots. All roots in the mineral soil were
newly formed. Soil was carefully washed from roots and a root
subsample was used for element analyses. The remaining roots
were used to determine root morphology. Total root length was
estimated by the line intersect method (Tennant 1975), and the
number of root tips per cm root length was counted in five
representative subsamples. Dry weights of shoots and roots
were determined after drying at 65 °C to constant weight.
Total N in needles was measured with a Macro N analyzer
(Heraeus, Hanau, Germany), and total N in roots was measured
with an automatic nitrogen analyzer (Model 1400, Carlo Erba,
Mainz, Germany). For the determination of other elements, the
dried and ground plant samples were dry ashed at 500 °C and

dissolved in 100 mM HCl. After filtration, K and Ca concentrations were measured by flame photometry, Mg, Mn, Fe, Cu,
and Zn concentrations were analyzed by atomic absorption
spectrometry, and P was determined colorimetrically as phosphomolybdate.
Statistical analysis
Standard errors of the means were calculated. Differences
between plant species were tested for statistical significance by
analysis of variance, and differences in effects of soil nutrient
supply on root growth and root nutrient concentrations within
a plant species were tested by t-tests. When data were not
normally distributed, analyses were carried out on transformed
data. In all cases, results are reported as untransformed values.

Results
Plant growth
Distribution of newly formed roots in the two soil compartments varied with conifer species (Figure 2). Norway spruce
showed twice the amount of root growth in the nutrient-enriched soil than in the nutrient-poor soil. The growth response
of Scots pine to the locally enriched nutrient supply was less
marked than that of Norway spruce, and the Douglas-fir trees
showed no difference in root dry weight between the two soil
compartments.
Total dry weight of all current-year roots was not significantly different between plant species (P < 0.08). However,
dry weight of new roots tended to be highest in Norway spruce,

Figure 2. Dry weights of newly grown roots of three coniferous tree
species in a split-root system. Roots of the same plant were grown
either in nutrient-poor soil (L, low nutrient availability) or in nutrientrich soil (H, high nutrient availability). Values are means, vertical bars
indicate one standard error of the mean (n = 5--6). Effects of soil
nutrient supply on root growth within one species are: ns, not significant; *, significant at P < 0.05; or ***, significant at P < 0.001.

followed by Douglas-fir and then Scots pine (Table 2). In
Norway spruce, there was a larger increase in current-year
shoot growth than in belowground growth (Table 2), whereas
Scots pine and Douglas-fir produced similar amounts of new
root and new shoot biomass during the experiment. Thus, the
root/shoot dry weight ratio was approximately 0.7 in Norway
spruce, and tended to be smaller than in the other two species
(P < 0.16, Table 2).
Among species, total root length of all newly produced roots
was greatest in Norway spruce (P < 0.001, Figure 3). Both
Norway spruce and Scots pine formed greater root length in
nutrient-rich soil than in nutrient-poor soil (Figure 3), but this
effect was not observed in Douglas-fir.
Specific root lengths (m g −1) were lower in Douglas-fir than
in Norway spruce or Scots pine (P < 0.001; Figure 4), and did
not vary significantly between nutrient-poor and nutrient-rich
soil in any of the plant species. The number of root tips per
centimeter of root length was not significantly affected by soil
nutrient supply (Figure 5). Norway spruce roots had more root
tips per centimeter of root length than roots of Scots pine and
Douglas-fir (P < 0.05).
Nutrient concentrations
Concentrations of most mineral elements did not differ markedly between roots grown in nutrient-poor and nutrient-rich
soil (Table 3). However, root P and K concentrations in
Douglas-fir and root Mg concentrations in Scots pine and
Norway spruce were greater in nutrient-rich soil than in nutrient-poor soil (Table 3). Douglas-fir had the lowest root nutrient
concentrations of all three species. Root Ca concentrations
were low in all three species examined.

42

GEORGE ET AL.

Table 2. Shoot and root dry weights and root/shoot dry weight ratios of three coniferous tree species in a split-root system (n = 5--6; one SE in
parentheses). Results were calculated separately for current-year and older tissue. For roots, dry weights of roots grown in nutrient-poor soil and
of roots grown in nutrient-rich soil were added.

Douglas-fir
Scots pine
Norway spruce
F-test
P value

Shoot dry weight (g per plant)

Root dry weight (g per plant)

Root/shoot dry weight ratio

Older

Current-year

Older

Current-year

Older

Current-year

8.9 (0.5)
10.0 (1.2)
18.8 (2.6)

5.4 (0.7)
4.9 (1.6)
9.4 (1.4)

7.0 (0.6)
9.9 (2.0)
11.6 (1.2)

5.4 (0.2)
4.4 (0.8)
6.3 (0.5)

0.79 (0.04)
1.08 (0.32)
0.68 (0.10)

1.05 (0.11)
1.35 (0.37)
0.72 (0.08)

0.07

0.32

0.15

< 0.01

0.05

0.10

Figure 3. Total length of newly grown roots of three coniferous tree
species in a split-root system. Roots of the same plant were grown
either in nutrient-poor soil (L, low nutrient availability) or in nutrientrich soil (H, high nutrient availability). Values are means, vertical bars
indicate one standard error of the mean (n = 5--6). Effects of soil
nutrient supply on root growth within a species are: ns, not significant;
*, significant at P < 0.05; or ***, significant at P < 0.001.

Figure 4. Specific root length of newly grown roots of three coniferous
tree species in a split-root system. Roots of the same plant were grown
either in nutrient-poor soil (L, low nutrient availability) or in nutrientrich soil (H, high nutrient availability). Values are means, vertical bars
indicate one standard error of the mean (n = 5--6). Effects of soil
nutrient supply on specific root length within a species are not significant (ns).

Neither current- nor previous-year needles showed severe
deficiencies in any element (Table 4). In Norway spruce, concentrations of N and P were suboptimal compared with standard values for adequate nutrition (Hüttl 1990), but were not
associated with any visible deficiency symptoms. Calcium
concentrations in needles were high in Norway spruce compared with Scots pine and Douglas-fir.

ruderal plant species respond similarly to locally enriched soil
(Chapin 1980, Friend et al. 1990, Fitter 1994). The general
assumption that all plant species respond with increased root
growth in nutrient-rich soil zones may be erroneous, because
studies in which no response was observed often do not appear
in the literature (Caldwell 1994).
Root growth of Scots pine and particularly of Norway
spruce, but not Douglas-fir, was increased in the nutrient-rich
soil compartment (Figures 2 and 3). These varied responses
may reflect genetically controlled differences among tree species with ‘‘exploitive’’ (Norway spruce, Scots pine) and ‘‘conservative’’ (Douglas-fir) root growth habits (Griffin et al.
1995). Typically, tree species with finer roots (greater specific
root length) have greater root extension rates, and are more
responsive to root pruning than species with low specific root
length, because they require smaller investments in biomass to
extend the root system (Eissenstat 1991). Accordingly, among
the tree species tested, Norway spruce had the greatest specific
root length (Figure 4), and also showed the largest response to

Discussion
It is generally assumed that most plants respond to nutrientrich patches in soil with enhanced root proliferation at these
sites. This response has been shown for a range of crop species,
and also, using artificial substrates, for Douglas-fir (Friend et
al. 1990), lodgepole pine (Coutts and Philipson 1977), and
Sitka spruce (Coutts and Philipson 1976). However, it is surprising that plant species well adapted to nutrient-poor soils
should respond to locally enriched soil in the same way as

ROOT RESPONSES TO HETEROGENEOUS NUTRIENT DISTRIBUTION

Figure 5. Number of root tips per centimeter of root length of newly
grown roots of three coniferous tree species in a split-root system.
Roots of the same plant were growing either in nutrient-poor soil (L,
low nutrient availability) or nutrient-rich soil (H, high nutrient availability). Values are means, vertical bars indicate one standard error of
the mean (n = 5--6). Effects of soil nutrient supply on root growth
within a species are not significant (ns).

nutrient enrichment in the soil (Figure 2). Such a response to
local nutrient supply may indicate that Norway spruce is a
competitive species that is adapted to relatively nutrient-rich
soil (Grime 1994, Hutchings and de Kroon 1994).
Beside possible genetic differences in root growth among
tree species, the effect of enhanced nutrient supply on root
growth may depend on the nutrient demand of the plant (Jackson and Caldwell 1989). Under our experimental conditions,
Norway spruce produced more shoot dry matter than Scots
pine and Douglas-fir. Also, the root/shoot ratio was lowest in
Norway spruce (Table 2), indicating that more nutrients and
water were provided for shoot growth per unit root dry weight
in Norway spruce than in the other species. The low concentrations of N, P and Mn (Table 4) in needles indicate nutrient
deficiency, and thus, high nutrient demand, especially in Norway spruce. High demand may have driven Norway spruce to
proliferate roots in the nutrient-enriched soil. Similar evidence
suggesting a higher root growth plasticity in nutrient-deficient
plants than in nutrient-sufficient plants has been obtained for

43

trees (Friend et al. 1990), and annual plants (Drew et al. 1973),
but not for perennial grasses (Larigauderie and Richards
1994).
Within a plant, roots growing in the nutrient-rich soil compartment may have higher nutrient concentrations than roots
growing in the nutrient-poor soil compartment. For example,
differences in nutrient concentrations among roots of the same
plant have been observed shortly after large local additions of
P to the soil (Jackson and Caldwell 1992). However, within a
plant, many nutrients (including N, P, and K, but not Ca) can
be translocated in the phloem to sites of high nutrient demand,
including roots (Marschner 1995). Also, increased root dry
matter formation in nutrient-rich soil requires additional nutrients for tissue formation, because of a dilution effect. For both
reasons, a long-term increase in nutrient concentrations in
roots growing in nutrient-rich soil is unlikely, at least for
elements that can be retranslocated within the plant.
Accordingly, when tree seedlings responded to increased
local nutrient supply by increased root growth, concentrations
of the growth-limiting nutrients (N and P in Norway spruce
and Scots pine) did not increase in roots in the nutrient-rich soil
compared with concentrations in roots in the nutrient-poor soil
(Table 3). Conversely, when a nutrient was not growth limiting
(e.g., Mg), or when a species did not respond to increased local
nutrient supply with increased growth (e.g., Douglas-fir), nutrient concentrations did increase in roots growing in nutrientrich soil (Table 3). Thus, in long-term field experiments with
local nutrient addition to soil, increased root growth is a better
indicator of previous nutrient deficiency than increased root
nutrient concentrations. These results also suggest that, because of the high mobility of most nutrients in plants, and
because of nutrient cycling between shoot and roots, root
growth in the nutrient-poor soil in the split-root experiment
was not limited, in the long-term, by nutrient deficiency.
Rather, allocation of photoassimilates to the root zones may
have differed, leading to greater root growth in nutrient-rich
soil than in nutrient-poor soil. Greater carbohydrate allocation
may have been the result of a faster decrease in the cytosolic
sugar pool in metabolically active root cells (Minchin et al.
1994). With enhanced unloading of phloem solutes, growthstimulating phytohormones are also unloaded in increased
amounts (Sattelmacher and Thoms 1995).

Table 3. Nutrient concentrations in newly grown roots of three coniferous tree species in a split-root system. Roots of the same plant were grown
either in nutrient-poor soil (L, low nutrient availability) or in nutrient-rich soil (H, high nutrient availability). Effects of soil nutrient supply on
nutrient concentrations within one species are ns, not significant; *, significant at P < 0.05; or **, significant at P < 0.01 (n = 5--6; one SE in
parentheses).
Nutrient

Douglas-fir (mg gdw−1)
L

N
P
K
Ca
Mg

4.96 (0.10)
0.79 (0.03)
3.66 (0.19)
0.33 (0.01)
0.61 (0.01)

Scots pine (mg g dw−1)

H

L
ns

6.34 (0.65)
1.02 (0.09)*
5.09 (0.43)*
0.28 (0.01)**
0.66 (0.05)ns

9.91 (1.14)
1.40 (0.14)
6.06 (0.62)
0.48 (0.04)
0.77 (0.03)

Norway spruce (mg g dw−1)

H
ns

7.93 (1.14)
1.21 (0.16)ns
7.28 (0.55)ns
0.37 (0.02)ns
1.05 (0.07)**

L

H

7.50 (0.53)
1.25 (0.09)
4.21 (0.18)
0.48 (0.03)
0.73 (0.02)

7.60 (0.49)ns
1.30 (0.05)ns
3.86 (0.25)ns
0.43 (0.02)ns
1.00 (0.07)**

44

GEORGE ET AL.

Table 4. Concentrations of the macronutrients N, P, K, Mg, Ca, and Mn, and the micronutrients Fe, Cu, and Zn in previous-year and current-year
needles of three coniferous tree species in a split-root system (n = 5--6; one SE in parentheses).
Douglas-fir
Previous-year

Scots pine

Norway spruce

Current-year

Previous-year

Current-year

Previous-year

Current-year

Macronutrients (mg gdw )
N
11.38 (0.51)
P
0.91 (0.17)
K
5.76 (0.28)
Ca
7.15 (0.26)
Mg
1.41 (0.10)
Mn
0.29 (0.05)

15.12 (0.43)
1.08 (0.17)
6.63 (0.29)
4.40 (0.57)
1.90 (0.19)
0.58 (0.10)

15.28 (1.62)
1.36 (0.17)
6.58 (0.71)
5.45 (0.36)
1.18 (0.08)
0.60 (0.04)

14.88 (1.11)
1.31 (0.10)
7.62 (0.94)
2.73 (0.50)
1.03 (0.13)
0.50 (0.09)

7.18 (1.62)
1.04 (0.07)
4.34 (0.37)
12.22 (1.26)
1.60 (0.21)
0.23 (0.05)

8.43 (1.30)
0.86 (0.07)
4.85 (0.29)
7.08 (0.94)
1.50 (0.18)
0.29 (0.05)

Micronutrients (µg gdw−1)
Fe
245 (22)
Cu
3.68 (0.28)
Zn
57.6 (10.1)

117 (9)
3.32 (0.16)
71.1 (11.9)

116 (8)
3.66 (0.30)
97.1 (13.8)

89 (15)
3.85 (0.19)
59.1 (14.1)

205 (23)
2.36 (0.36)
80.8 (10.8)

114 (11)
2.35 (0.26)
50.6 (8.8)

−1

An extensive root system would be advantageous for uptake
of nutrients with low mobility in soil such as P (Theodorou and
Bowen 1993). Plants may respond to nutrient deficiency by
forming a more exploratory root system, with finer roots or
more branches or both. However, in some studies, a localized
nutrient supply had the opposite effect, and roots in nutrientrich soil were thinner (Jackson and Caldwell 1989) or more
branched (Larigauderie and Richards 1994, see also Fitter
1994) than roots in nutrient-poor soil. We found that neither
specific root length (Figure 4) nor the number of root tips per
centimeter of root length (Figure 5) was affected by local
nutrient supply. Similarly, Friend et al. (1990) found that
specific root length of Douglas-fir was not affected by local N
supply (Friend et al. 1990).
Effects of local nutrient additions on root morphology may
be transient and appear only shortly after the nutrient addition,
because of initiation of a large number of young roots. However, in the long term, effects of nutrient additions on root
longevity (Pregitzer et al. 1995) are important for overall root
morphology. In soil-grown plants, factors such as root penetration resistance and soil oxygen supply have large formative
effects on root growth, and this may be more important for root
morphology than local nutrient supply (Caldwell 1994).
The supply of a particular nutrient may have different effects
on root growth (Wikström and Ericsson 1995) and morphology
than simultaneous supply of several nutrients as in this experiment. Generalization about the formative effects of local nutrient supply on root morphology is more difficult for trees than
for annual plants, because many tree root systems are comprised of both ‘‘pioneer,’’ ‘‘extension’’ or ‘‘long’’ roots, and
‘‘fibrous,’’ ‘‘lateral’’ or ‘‘fine roots’’ (Atkinson 1983, Eissenstat
1991, Marschner et al. 1991, George and Marschner 1995). In
‘‘pioneer’’ roots, individual roots with larger diameter may
have high growth rates, whereas in ‘‘fibrous roots,’’ a high
specific root length may favor fast root extension (Eissenstat
1991). Thus, morphological effects of local nutrient supply on
tree root systems will also depend on the balance between
‘‘pioneer’’ roots and ‘‘fibrous’’ roots. This balance is determined

by a range of conditions including soil factors, plant age, and
mycorrhizal colonization of the root system.
Few data are available to quantify nutrient uptake of the
different parts of the tree root system (George and Marschner
1995). Physiological as well as morphological changes in the
root system in response to nutrient availability, for example,
increased nutrient uptake rates of roots in nutrient-rich soil,
may be important in the adaptation of plants to soils that are
heterogeneous in nutrient availability (Caldwell et al. 1992,
Hutchings and de Kroon 1994).
In our experiment, colonization of roots with ectomycorrhizal fungi appeared unaffected by the soil nutrient supply. This
may have been because root colonization was dominated by
fungal species adapted to nursery conditions, i.e., both a relatively high supply of nutrients in inorganic form and a disturbed soil. In forest-grown plants, extraradical hyphae of
mycorrhizal fungi may be more important than tree roots in
nutrient absorption from the soil, particularly when the nutrient supply is in organic form (George and Marschner 1995).
We have demonstrated that roots of coniferous tree species
can respond to an increase in local nutrient supply in soil by
increasing root dry matter growth without changing specific
root length. The effect varied with plant species (Norway
spruce > Scots pine > Douglas-fir) and was correlated with
nutrient demand of the plant (high demand > low demand).
Changes in root dry weight were a better indicator of nutrient
limitations in the system than changes in root nutrient concentrations.

Acknowledgment
We thank Sabine Kircher, Carsten Marohn, Angela Schmeisser, and
Julia Ströbele for their excellent help. This work was financed by
Projekt Europäisches Forschungszentrum für Luftreinhaltung (PEF)
in Karlsruhe, Germany.

ROOT RESPONSES TO HETEROGENEOUS NUTRIENT DISTRIBUTION
References
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