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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.
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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 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 (Pecháckováet al. 1999) or less heterogeneous (Titlyanova et al. 1999) than shoot mass. These studies agree 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
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 slow-release 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 anova.
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 anova tested for differences in productivity, mortality and longevity between heterogeneity 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.
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 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 leaf longevity varied significantly within heterogeneous or homogeneous pots (Fig. 3c).
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 described for root and shoot mass of several grassland species in the field (Pecháckováet 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 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.
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.