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Functional
Ecology 2001
15, 748 –753
Root and leaf production, mortality and longevity in
response to soil heterogeneity
Blackwell Science Ltd
M. PÄRTEL† and S. D. WILSON
Department of Biology, University of Regina, Saskatchewan S4S 0A2, Canada
Summary
1. Patches of fertile soil support concentrations of roots, but whether this reflects
increased production or increased longevity is not known. We examined the production and longevity of roots of the grass Festuca rubra in response to soil heterogeneity.
We also explored the extent to which root dynamics reflect shoot responses to heterogeneous soils.
2. Root and leaf dynamics were followed in pots of heterogeneous or homogeneous
soils containing the same total amount of nutrients. Digital minirhizotron images of
roots and leaves were collected weekly.
3. Root length was significantly greater in homogeneous than heterogeneous soils.
This was caused by significantly larger root production but shorter life span. In contrast, soil heterogeneity had no effect on leaf production or longevity.
4. Within heterogeneous pots, root and leaf production were strongly concordant,
both being significantly greater in fertilized patches. More roots died in fertilized
patches, but leaf mortality was not affected. Longevity of neither roots nor leaves was
affected by the location of a fertile patch.
5. Spatial variation in production of roots and shoots in response to nutrient patches
was concordant. Roots and shoots, however, showed independent responses to the
presence of within-pot heterogeneity. A decrease in total root length in heterogeneous
soils was a counterintuitive result of decreased production and increased longevity.
Key-words: Festuca rubra, root and leaf appearance, root and leaf disappearance, root and leaf turnover, soil
nutrient patchiness
Functional Ecology (2001) 15, 748 –753
Introduction
There is much evidence that plant roots can proliferate in nutrient-rich patches (Caldwell & Pearcy 1994;
Hutchings, John & Stewart 2000; Robinson 1996), but
whether this proliferation results from increased productivity or increased longevity has received less attention. Both the production and mortality of roots in
Michigan old-field species followed for 9 days increased in nutrient-rich patches, resulting in little net
change in root number (Gross, Peters & Pregitzer
1993). But root production and mortality can have
independent responses to environmental changes such
as elevated atmospheric CO2 (Pregitzer et al. 1995) or
soil temperature (Fitter et al. 1999), suggesting that they
may also have independent responses to soil patches.
Root and leaf longevity are generally greater in
nutrient-poor habitats (Kikuzawa 1995; Pregitzer
© 2001 British
Ecological Society
†Author to whom correspondence should be addressed.
Present address: Institute of Botany and Ecology, University of Tartu, Lai 40, Tartu 51005, Estonia. E-mail:
[email protected]
et al. 1995; Ryser 1996). Roots of some herbaceous
species lived longer in relatively dry soils in Italy than
in relatively wet soil in Britain (Watson et al. 2000).
Tree roots lived longer in a warmer and dryer southern
stand relative to a cooler northern stand in Michigan
(Hendrick & Pregitzer 1993), and during dry years
compared to wetter ones in Alaska (Ruess, Hendrick
& Bryant 1998). No differences were found in leaf
longevity between two altitudes in the Alps (Diemer,
Körner & Prock 1992). Soil resource availabilities
influence root longevity, but we know of no studies of
the response of longevity to soil heterogeneity.
Early studies of root longevity, using tags (Weaver &
Zink 1946) or estimates of changes in annual root biomass (Dahlman & Kucera 1965), focused on relatively
large roots. The majority of root biomass, turnover
and activity occurs in fine roots (Eissenstat & Yanai
1997), which were not included in these measures.
Similarly, little is known about the concordance of
root and shoot activity in response to heterogeneity. In
grasslands, below-ground biomass may be either more
(Pechácková et al. 1999) or less heterogeneous (Titlyanova et al. 1999) than shoot mass. These studies agree
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dynamics and soil
heterogeneity
that some species have well correlated distributions of
above- and below-ground mass, whereas other species
do not. Seedling root and shoot biomasses of two tree
species were not spatially correlated at the scale of
0·5 m (Mou et al. 1995). It is not clear how precisely
root and shoot production can follow small-scale
patchiness in soil fertility. Shoot distribution patterns
may be less influenced than roots by soil heterogeneity,
as roots can transport nutrients to shoots from rich
patches (de Kroon & Hutchings 1995; Stuefer, de
Kroon & During 1996), but there are no comparisons
of similarities between roots and shoots in terms of the
dynamics of their responses to patches.
Our objective was to examine the effects of heterogeneity on root and leaf dynamics simultaneously, in a
comparable and spatially explicit manner. Specifically,
we tested whether: (i) the production, mortality and
longevity of roots and leaves differ between homogeneous and heterogeneous soils; and (ii) root and
leaf production, mortality and longevity show similar
spatial responses to nutrient patches.
Materials and methods
© 2001 British
Ecological Society,
Functional Ecology,
15, 748 –753
We followed root and leaf dynamics of the grass Festuca rubra L. in heterogeneous and homogeneous soils.
Festuca rubra is a circumpolar species, common at
intermediate soil fertility and moisture in Eurasia and
Northern America.
Festuca was grown in pots (14 × 14 cm, 11 cm deep)
in a greenhouse in Regina, Canada. Clear plastic tubes
(6 cm diameter) were installed horizontally 4 cm
beneath and above the soil surface to allow access by a
digital camera (Bartz Technology, Santa Barbara,
CA). Tubes were used to study both roots and leaves
in order to obtain comparable results for below- and
above-ground responses. Wire mesh (1 × 1 cm) surrounded above-ground tubes, 4 cm from the tube, in
order to reduce leaf movement. Pots were arranged
in three rows of six pots each, with one tube placed
through, and another over, each row. Tubes running
through the pots were wrapped with black electrical tape
in spaces between pots to prevent light penetration.
All pots were filled with nutrient-poor soil (4 : 1 : 1
sand, peat, and dried and sieved local soil; the local soil
provided micro-organisms as Festuca rubra is a mycorrhizal species, Harley & Harley 1987). Pots containing
homogeneous soils were evenly spread with slowrelease fertilizer (10 g m–2 each of N, P and K) and covering it with 5 mm soil. Pots containing heterogeneous
soil received the same amount of fertilizer, but it was
concentrated in one-third of each pot, located at one
side of the pot. The fertilized patch was oriented at
right angles to the tubes so that the tubes crossed both
fertilized and unfertilized patches. There were nine
replicates of both treatments, arranged in a completely
randomized design. Nutrient heterogeneity in natural
vegetation is on similar scales (10 cm, Kleb & Wilson
1997; 20 cm, Farley & Fitter 1999).
Local commercial Festuca seeds (United Grain
Growers Ltd, Saskatchewan, Canada) were sown in
February 2000 and thinned immediately after germination to obtain 20 plants evenly dispersed over the
pot. Pots were watered to field capacity, illuminated
for 16 h daily (six 400 W daylight lamps), and kept
at 25 °C.
We collected eight contiguous digital images (each
13·5 mm wide, 18 mm tall; the strip of images was
centred in the pot) from each pot each week for 11
weeks, starting one week after sowing. Nutrient pulses
in a woodland in Great Britain persist for less than
4 weeks (Farley & Fitter 1999), suggesting that the
length of our study was relevant to natural patterns of
heterogeneity.
Root images were taken from the upper surface of
buried tubes. Leaf images were taken from the side of
the tubes over pots. The same location within a tube is
referred to as a window; one image was collected from
each window each week. The position of each window
was fixed using a mechanically indexed handle.
Each week in each window, the lengths of living
roots and leaves were measured. As a rule, leaves were
vertical across the window (18 mm), and their length
was determined by counting and multiplication. By
comparing images from two contiguous weeks, the
lengths of roots and leaves that were newly produced and newly dead (‘production’ and ‘mortality’)
were determined. A root was considered dead if it
was black, disintegrated or not visible (Hendrick &
Pregitzer 1992). A leaf was considered dead if it was
brown. Root and leaf length, production and mortality
were determined for each pot weekly, and the effects of
heterogeneity, time and their interaction were tested
using repeated-measures .
Root longevity was measured for each window as
the life span of the largest white root >2 mm long
found in the first week’s cohort. Leaf longevity was
measured for each window as the number of weeks
between the appearance of the first live leaf and the
first dead leaf. We were unable to assess individual
leaf mortality, as was done for roots, because leaves
moved despite the mesh. Although it is possible that
the leaf that died may have appeared after the first leaf,
causing an underestimation of longevity, we expected
older leaves to die before young leaves on average.
Kolmogorov–Smirnov statistics were used to test for
differences between root and leaf longevity distributions in homogeneous and heterogeneous soils. Mean
root and leaf longevity were calculated for each pot
across all eight windows.
Within the pots, root and leaf production and mortality during the experiment, and root and leaf longevity, were also determined separately for each of the
eight windows. In the heterogeneous pots, five windows were associated with soil without fertilizer, and
three were associated with soil that received fertilizer.
Split-plot  tested for differences in productivity, mortality and longevity between heterogeneity
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M. Pärtel &
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Fig. 1. Length of living roots and leaves during the experiment (mean ± 1 SE).  effects: H, heterogeneity level;
T, time. *P < 0·05; **P < 0·01.
treatments (main plot effect) and among window
locations (subplot effect). In cases where both roots
and leaves varied significantly across locations in the
heterogeneous soils, Kendall’s coefficient of concordance was used to test whether the spatial distribution
of these variables was similar between roots and leaves.
Results
© 2001 British
Ecological Society,
Functional Ecology,
15, 748 –753
Both root and leaf length were significantly higher in
homogeneous soils (Fig. 1). The interaction between
heterogeneity and time was significant because differences between treatments increased during time.
Weekly root production was significantly less in
heterogeneous than in homogeneous soils (Fig. 2a).
Weekly leaf production was also less in heterogeneous
soils, but not significantly so (Fig. 2a). Weekly mortality of roots and leaves did not vary between heterogeneity treatments for either roots or leaves (Fig. 2b).
Weekly production of roots and leaves were less at the
beginning and at the end of the experiment (Fig. 2a),
and root mortality increased during the experiment,
but shoot mortality was constant (Fig. 2b).
Approximately 50% of first-cohort roots in heterogeneous soils lived for 6–8 weeks, whereas 50% of
first-cohort roots in homogeneous soil lived for only
2 –3 weeks (Fig. 2c). No leaves died during the first
3 weeks, after which survival decreased steadily in
both homogeneous and heterogeneous soils, and 50%
of the leaves lived for 7–8 weeks. Mean root longevity was significantly longer in heterogeneous soil, but
mean leaf longevity did not differ significantly between
treatments (Fig. 3c).
Total root production during the experiment was
significantly less in heterogeneous soil (Fig. 3a). Total
leaf production did not vary with soil heterogeneity,
nor did the total mortality of roots or leaves (Fig. 3b).
The total cumulative dynamics during the experiment
reflected the weekly pattern. During the experiment,
about 60% of the roots disappeared on average. In
Fig. 2. For root and leaf, (a) weekly production
(mean ± 1 SE), (b) mortality and (c) longevity distribution
during the experiment in homogeneous and heterogeneous
soils.  effects: H, heterogeneity level; T, time. D values
are for the Kolmogorov–Smirnov test for differences between
heterogeneity levels. **P < 0·01; ***P < 0·001.
contrast, fewer than 10% of the leaves disappeared during the experiment.
In heterogeneous pots, root and leaf production
were both significantly higher in the fertilized side of
the pot (Fig. 3a), and spatial variation in production
was significantly concordant between roots and leaves
(Kendall’s W = 0·81, P < 0·001). In homogeneous
pots, root or leaf production did not vary significantly
across the pot. In heterogeneous pots, root mortality
was significantly higher in the fertilized side of the pot
(Fig. 3b), but leaf mortality was not affected by the fertility gradient. In homogeneous pots, root mortality
was higher in the middle of the pots. Neither root nor
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heterogeneity
Fig. 3. For root and leaf, (a) production (mean ± 1 SE), (b)
mortality and (c) longevity within heterogeneous and
homogeneous pots with the same amount of fertilizer. Dark
columns indicate the patch receiving fertilizer.  effects:
H, heterogeneity level; L, location within pot. *P < 0·05;
***P < 0·001.
leaf longevity varied significantly within heterogeneous or homogeneous pots (Fig. 3c).
© 2001 British
Ecological Society,
Functional Ecology,
15, 748 –753
Discussion
Heterogeneity significantly reduced root production
but increased root longevity. This increased net root
length in homogeneous soils. Our results show that
differences in root mass between heterogeneous and
homogeneous soils can be caused by changes in root
production and turnover.
Previous studies of responses to heterogeneity have
focused on the response of physiologically integrated
ramets. Root and shoot biomasses of the clonal plant
Glechoma hederaceae were higher in coarse-scaled
heterogeneous soils than in fine-scaled heterogeneous
soils (Wijesinghe & Hutchings 1997). Fransen, de
Kroon & Berendse (1998) studied five grass species
(including Festuca rubra) in an experiment where a single plant grew into homogeneous or heterogeneous
conditions with the same amount of total nutrients.
No species showed differences in root mass between
heterogeneous and homogeneous soils, and only one
species (Anthoxanthum odoratum) produced more
above-ground mass under heterogeneous conditions.
Both these examples contrast with our results of significantly reduced root production in heterogeneous soils
(Figs 2a and 3a). The difference lies in the response
variable considered: we examined a population response, whereas the examples above addressed integrated ramets. Lessons from integrated ramets may
not apply to population-level responses.
Many roots died during our experiment (60%,
Figs 2b and 3b). Using rhizotrons in a heathland,
Aerts, Bakker & Caluwe (1992) found that the proportion of roots that died within a year were 25% for Calluna vulgaris, 35% for Deschampsia flexuosa and 67%
for Molinia caerulea. A rhizotron study showed that
up to 80% of roots of different herbaceous species
died within 21 days (Watson et al. 2000). In contrast,
early studies of prairie root dynamics reported that
only ≈25% of roots died within a year (Dahlman &
Kucera 1965; Weaver & Zink 1946). These early studies, however, considered only large roots, which are
usually much longer-lived than small roots (Eissenstat
& Yanai 1997).
In contrast to roots, leaf mortality was much smaller
(10%) and this did not differ between heterogeneous
and homogeneous soils (Figs 2b and 3b). No differences were found between leaf longevity on homogeneous and heterogeneous soils (Figs 1c and 3c). Our
mean leaf longevity was 4–8 weeks, similar to a study
of 29 herbaceous species in central Europe, where
mean leaf longevity was 10 weeks (Diemer et al. 1992).
Similar results were reported for 14 herbaceous species
in northern America, where the mean leaf longevity
was 9 weeks within a range of 4–14 weeks (Craine
et al. 1999).
Root production and mortality were greater in fertilized patches (Fig. 3a,b), similar to the results of Gross
et al. (1993) and Hodge et al. (1999b). In an experiment with the grass Lolium perenne, however, only root
production, and not mortality, was increased by fertilizer addition (Hodge et al. 1999a). Our experiment
showed concordant responses of root and leaf production in response to a fertile patch, as has been
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described for root and shoot mass of several grassland
species in the field (Pechácková et al. 1999; Titlyanova
et al. 1999). The only parameter that varied significantly within homogeneous pots was root mortality.
More roots died in the centre of the pot than at the
edges (Fig. 3b), probably due to greater competition.
In general, plant tissue longevity increases with
decreasing soil fertility (Eissenstat & Yanai 1997;
Kikuzawa 1995; Pregitzer et al. 1995; Reich, Walters
& Ellsworth 1992; Ryser 1996), but we found no difference in root or leaf longevity between fertilized
and unfertilized patches in the heterogeneous pots
(Fig. 3c). In contrast, longevity was significantly
greater in heterogeneous than homogeneous soils
(Figs 2c and 3c). This suggests that a seedling’s first
roots are important for integrating a heterogeneous
environment, forming a structural framework for the
root system to detect rich patches in space and in time
(Eissenstat & Yanai 1997).
In conclusion, root and leaf production showed concordant spatial responses to a fertile patch, but roots
and leaves had distinct responses to the presence of
heterogeneity. Root production decreased and longevity increased in heterogeneous relative to homogeneous soils, whereas leaf dynamics were unaffected by
heterogeneity. The production and death of roots in
response to heterogeneity cannot be inferred with
certainty from patterns of final length in either shoots
or roots.
Acknowledgements
We thank Peter Ryser and two anonymous referees for
valuable comments. Financial support was from a
NATO Science postdoctoral fellowship to M.P. and a
Natural Sciences and Engineering Research Council
of Canada grant to S.D.W.
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© 2001 British
Ecological Society,
Functional Ecology,
15, 748 –753
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Received 13 March 2001; revised 21 June 2001; accepted
21 June 2001