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1 Responses to spatial heterogeneity of soil nutrients were tested in 10 plant species that differ in life form and successional status, but which co-occur in the South Carolina coastal plain. The morphological responses of the root system were tested by assessing scale (represented by root mass and root length densities), precision (preferential proliferation of roots in nutrient-rich patches compared with less fertile patches) and discrimination (ability to detect and proliferate within the richest patches when patches vary in nutrient concentration). We also investigated sensitivity (growth benefits gained as spatial heterogeneity of nutrients increases, measured as total biomass).
2 Ten individuals of each species were grown in pots under four treatments that had differing nutrient distribution but the same overall nutrient addition. Plants were harvested when roots reached pot edge.
3 We observed high variation between species in scale, precision and sensitivity. No significant discrimination responses were observed, although greatest root mass density occurred at intermediate fertility levels for all species.
4 We rejected the hypothesis that scale and precision are negatively correlated. Indeed, in herbaceous species alone, scale and precision were positively correlated.
5 Sensitivity was not closely related to precision, indicating that proliferation of roots in fertile patches does not always yield growth benefits in heterogeneous soils. Further, some sensitive species had very low precision, suggesting that a positive growth response in heterogeneous environments may be related to plasticity in physiology or root life span, rather than morphology.
6 Plant life form was not correlated with precision or sensitivity. However, scale of response was greater in herbs than in woody plants, possibly because the two life forms develop root systems at different rates.
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The term ‘foraging’ has been used to describe the process by which root systems grow in the soil and thus capture nutrients ( Bray 1954). Plasticity can, presumably, increase the efficiency of resource foraging, and one of the most commonly reported plastic responses is the proliferation of roots in regions of high nutrient density ( Passioura & Wetselaar 1972; Granato & Raper 1989). Most studies of root response to fertilizer patches have examined agricultural species known to have particularly high growth rates and large demands for nutrients ( Drew 1975; Fitter 1994; Robinson 1994). More recently, plant root foraging responses in natural communities have been studied to determine whether they influence competitive interactions and succession ( Crick & Grime 1987; Jackson & Caldwell 1989; Campbell et al. 1991 ; Mou et al. 1997 ).
Three plastic responses that may be important to below-ground resource foraging are variations in scale, precision and discrimination, which depend on the morphology of root systems with respect to nutrient location. Scale (which allows nutrient capture to be monopolized by the development of an extensive root system) and precision (the tendency to proliferate roots in resource-rich patches) were negatively correlated for eight herbaceous plant species ( Campbell et al. 1991 ). Discrimination (the ability, when patches vary in fertility, to identify and to proliferate roots in patches of higher nutrient concentrations) has, to our knowledge, not yet been explicitly studied, although Jackson & Caldwell (1989) observed that some species differ in root proliferation depending on the concentration of resources within a patch.
A fourth plastic trait, sensitivity, focuses on total biomass responses to different levels of heterogeneity. A sensitive plant is one that displays increased biomass as a given amount of nutrients becomes more patchily distributed within the soil matrix. Sensitivity has been demonstrated experimentally for at least one clonal plant species (Glechoma hederacea L.); however, if enriched nutrient patches became too small, the plant responded as if the entire area was homogeneously poor ( Birch & Hutchings 1994; Wijesinghe & Hutchings 1997). We believe that understanding sensitivity may be essential for predicting whether or not plants gain fitness benefits from an increased concentration of roots in fertile patches.
Nutrient foraging patterns and individual species’ responses may be a key to competitive ability and dominance during various stages of succession. For example, Campbell et al. (1991) found that those species with the most extensive root systems (i.e. having the highest scale) were superior competitors in homogeneously fertile environments. They also found that stress tolerators had greater precision, suggesting a strategic trade-off between scale and precision. Thus, in an environment where nutrient distribution is heterogeneous, species that are highly responsive to nutrient heterogeneity may have an enhanced ability to tolerate stress or to compete with less sensitive neighbours. During a successional sequence it is possible that the relative advantage of precise foraging will change. Initially, growth will not depend on precise foraging due to low competitor density and high resource availability. However, as succession proceeds and space becomes more partitioned, greater benefits may be afforded to plants that are precise foragers.
These predictions concerning nutrient foraging effects on growth, competitive outcomes, and succession are only tentative. For instance, it is not known whether the scale vs. precision trade-off is general for plants in different communities ( Campbell et al. 1991 ), nor is it clear whether consistent patterns of plasticity or resource foraging strategies are associated with specific types of plants, such as early vs. late successional species or herbaceous vs. woody species ( Robinson 1994). Extrapolation from data sources such as the eight species used by Campbell et al. (1991) , which were all herbaceous and came from several communities, should therefore be cautious. Investigations of root foraging using species from the same community will provide greater insight into within-community interactions. Even then, arguments about the ecological significance and evolution of root foraging traits ( Grime et al. 1991 ; Jackson & Caldwell 1996; Gleeson & Fry 1997) depend on the important but often untested underlying assumption that precision leads to fitness gains in heterogeneous soil environments.
The objective of this study was to quantify root system plasticity in response to various levels of soil heterogeneity using 10 species from the same community. Scale, precision, discrimination and sensitivity were measured and analysed to answer the following questions. (i) Do these co-occurring species differ in root foraging behaviour? (ii) Are root foraging traits correlated? (iii) Does increased root proliferation within nutrient patches confer growth benefits on species? (iv) Is foraging ability related to life form?
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Analysis of the ion exchange extracts revealed significant location effects on nitrate concentration (P = 0.0001); however, depth and interaction effects were not significant (P > 0.05). In pots without plants, nutrients leached downwards with little lateral movement ( Fig. 1), although nutrient patterns might have been different in pots with plants where nutrients were not measured.
Figure 1. Nitrate concentrations at different depths and locations (negative distances represent points within the fertilized patch) in a quarterly treatment pot. Values were obtained after a 10-day incubation of ion exchange membranes in seven pots. Mean ± SD.
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At harvest, ectomycorrhizal development was observed in Pinus taeda, and root nodules were observed on both legume species (Chamaecrista nictitans and Desmodium strictum (Pursh) DC). Roots were not dissected to determine if endomycorrhizae were present; however, we assume that all but P. taeda form endomycorrhizae in natural soils.
Indices of root traits
Both measures of scale revealed significant species differences (P < 0.05) that were as large as 30-fold for root length density and sevenfold for root mass density ( Table 3).
Table 3. Root foraging and root morphology traits for 10 species of co-occurring plants from South Carolina, listed in order of greatest to least root mass density. Means (values with ± standard error) within columns with different letters are significantly different ( P < 0.05) according to Tukey’s test (SAS Institute Inc. 1996). Root mass density is based on the heterogeneous nutrient treatment only; all other parameters are based on all harvested plants. See text for methods to calculate the sensitivity index and root to shoot ratio
|Species||Root mass density (kg dry massm–3 soil)||Root lengthdensity(km m–3) ||SRL (km rootskg–1 dry mass)||Sensitivity index||Root to shootratio|
|S. nemoralis||0.116 ± 0.030a||36.6 ± 3.9a||392||–0.14||0.18|
|C. nictitans||0.087 ± 0.009a,b||35.6 ± 2.4a||483||–0.02||0.19|
|H. gentianoides||0.069 ± 0.015a,b,c||34.1 ± 4.1a||478||0.39||0.23|
|E. canadensis||0.057 ± 0.008b,c,d||28.5 ± 2.1a||411||0.45||0.41|
|D. virginiana||0.034 ± 0.010c,d|| 2.8 ± 0.6b||92||*||0.44|
|E. tomentosus||0.027 ± 0.005c,d||12.8 ± 1.2b||564||0.21||0.19|
|L. styraciflua||0.024 ± 0.004c,d|| 4.6 ± 0.5b||184||0.53||0.28|
|D. strictum||0.022 ± 0.007c,d||13.2 ± 1.4b||470||0.54||0.31|
|E. americanus||0.017 ± 0.004d|| 1.9 ± 0.4b||88||0.26||0.30|
|P. taeda||0.016 ± 0.003d|| 1.2 ± 0.1b||65||–0.19||0.23|
Patchy nutrient availability caused a shift in root mass allocation in some species but not in others ( Fig. 2). Significant treatment (H vs. Q; anova; d.f. = 1169; P = 0.016), species (d.f. = 9169; P = 0.0001) and interaction (d.f. = 9169; P = 0.028) effects on RFRMD were detected. The absence of any differences from zero for RFRMD in the H treatment indicated that root systems developed symmetrically. In the Q treatment, seven species had an RFRMD that was statistically different from zero, and of these the four with the greatest RFRMD were also statistically different from the homogeneous pots ( Fig. 2). The RFRMD in quarterly fertilized pots was used as an index of precision in our analysis of correlations between root system traits and whole plant responses (see below).
Figure 2. Precision of root growth in nutrient-rich patches for 10 plant species. Precision (RFRMD) is expressed as: fine root mass density in one quarter of a pot minus that in the opposite quarter divided by total root mass in the pot. For Q pots, this corresponds to fertilized and opposite unfertilized quarters; for H pots, this is two equally fertilized opposite quarters. In no case was the H RFRMD different from zero (i.e. no random preferential proliferation in any particular patch) at P = 0.05. **Q RFRMD is significantly different from both zero and H RFRMD (P < 0.05). *Q RFRMD is different from zero but no significant treatment effects are detected. Bars are least squares means ± SEM. Species symbols are as in Table 2.
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Evidence of discrimination was weak. The mean root mass (as a percentage of pot total) in the individual PE and PU plugs varied between 1% and 8% of the total pot root dry mass depending on species (data not shown). Significant heterogeneity of variance in these percentages (PE vs. PU) was detected in only one species, Pinus taeda (P < 0.05). In this species, however, the higher variance in the PU treatment was due to a single pot, which had an unusually large root mass in the plug with the lowest fertility level. Transplant mortality meant that only six other species could be tested. Although differences within these species were not significant, at least two of the PU plug types (i.e. low, intermediate and high fertility) within a species differed by 1.5- to fivefold (data not shown) which suggests that some discrimination may have occurred. No index of discrimination was calculated.
Many species showed a slight increase in the percentage of roots located in the plugs between the low and intermediate levels, and a large decrease between the intermediate and high levels of fertility in the PU treatment (data not shown). To examine this relationship further, we compared root mass in patches as a percentage of total root mass in the pot at the various fertilizer densities used in the experiment. Five of the seven patches (single plug collected in H, mean of three plugs for PE, and three unique plugs in PU treatments) in this comparison were the same size, but the two patches from the Q treatment were larger. To correct for these differences in size, we created a root mass density index: root mass in patch as percentage of mass in total pot divided by the volume of soil in the patch. For all eight species, the maximum root mass density index occurred at an intermediate fertility level ( Fig. 3). Some species differences were apparent; two had maximum rooting densities at around 8 kg of fertilizer m–3 soil, while three others had maximum rooting densities at less than 2 kg m–3 ( Fig. 3).
Figure 3. Index of fine root mass density (roots in patch as percentage of total pot, scaled to a m3 of soil volume to control for patch volume differences) for different rates of fertilization. Symbols represent all fertilizer densities (including no fertilizer added) in homogeneous (T) and quarterly (R) treatments, plus fertilizer densities in the plugs for the plugs equal (&U25CF;) and plugs unequal (▪) treatments. Maximum root mass density index for each species is shown as an open symbol.
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Comparisons of H vs. Q, PE vs. PU, and H vs. Q vs. PE vs. PU revealed no significant differences in biomass within any species (P > 0.05). However, when data were grouped to consider coarse nutrient heterogeneity (H and Q treatments) vs. finer scale heterogeneity (PE and PU treatments), significant species ( anova; d.f. = 8308; P = 0.0001), treatment (d.f. = 1308; P = 0.0001) and species × treatment (d.f. = 8308; P = 0.0006) effects were detected. Four species produced significantly more biomass in the finer scale treatment (P < 0.05; Fig. 4). A sensitivity index was calculated for each species by taking the difference between total biomass in fine and coarse heterogeneity treatments, and dividing this difference by mean total biomass in the fine heterogeneity treatments ( Table 3). Sensitivity scores ranged from 0.54 to – 0.19. Larger numbers represent greater stimulation of total biomass growth as soil heterogeneity becomes increasingly fine-scaled. The species with negative scores had less biomass when grown in pots with fine-scale heterogeneity than in pots with coarse-scale heterogeneity.
Figure 4. Total plant biomass in pots with fine scale (PE and PU) vs. coarse scale (H and Q) heterogeneity (least squares mean ± SE). Results were similar if PE and PU were compared to Q alone. *Significant treatment differences (P < 0.05). Species symbols are as in Table 2.
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Correlation between traits
Scale and precision were not related as hypothesized. When all species were included in analysis, the only significant correlation among root foraging traits was between the two measures of scale ( Table 4). Moreover, when woody species were excluded from analysis, we found positive correlations between both measures of scale and precision, and negative correlations between both measures of scale and sensitivity ( Table 4). When the correlations between each of the root foraging traits (scale, precision, and sensitivity) were plotted (using the most strongly related measures of scale), broad differences were apparent between woody species (for which scale was very similar) and herbs (where scale was more variable; Fig. 5).
Table 4. Pearson’s correlation coefficients (P-values for test of significance in parentheses) for relationships between foraging traits (scale, precision and sensitivity) and two other root system traits (SRL and root to shoot ratio)
| ||Root mass density (scale)||Root length density (scale)||Q RFRMD (precision)||Sensitivity index (sensitivity)||Specific root length|
|All species (n = 10 species except 9 for sensitivity) |
|Root length density||0.91 (<0.01)|| || || || |
|Q RFRMD||0.39 (0.27)||0.40 (0.25)|| || || |
|Sensitivity||–0.38 (0.31)||–0.14 (0.73)||–0.11 (0.78)|| || |
|Specific root length||0.47 (0.17)||0.73 (0.02)||0.17 (0.64)||0.21 (0.59)|| |
|Root to shoot ratio||–0.37 (0.29)||–0.37 (0.30)||–0.35 (0.32)||0.65 (0.06)||–0.40 (0.25)|
|Herbaceous species only (n = species) |
|Root length density||0.92 (0.01)|| || || || |
|Q RFRMD||0.58 (0.23)||0.76 (0.08)|| || || |
|Sensitivity||–0.78 (0.06)||–0.55 (0.25)||–0.44 (0.38)|| || |
|Specific root length||–0.62 (0.18)||–0.59 (0.21)||0.01 (0.99)||0.16 (0.16)|| |
|Root to shoot ratio||–0.40 (0.43)||–0.21 (0.69)||–0.32 (0.53)||0.74 (0.09)||–0.38 (0.46)|
Figure 5. Relationships between scale, precision and sensitivity with correlation coefficients and tests of their significance. Woody species are denoted by circles. Species codes are as in Table 2.
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For all species combined, specific root length was positively correlated with all measures of root foraging traits; however, only the correlation with root length density was significant ( Table 4). Woody plants had much smaller values for SRL and one or both measures of scale than herbs did ( Table 3). When woody plants were removed from the analysis, correlations between SRL and scale became negative, although not significant ( Table 4). For the root to shoot ratio, the strongest correlation was with sensitivity, which was nearly significant for all species combined and for herbs alone ( Table 4). Sensitive plants thus had greater proportional allocation to roots.
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We found significant differences in scale, precision and sensitivity between the species tested ( Figs 2 and 4 and Table 3). Previous studies have reported differences for scale and precision ( Campbell et al. 1991 ; Robinson 1994; Mou et al. 1997 ), although the techniques used to measure these characteristics are not always the same, and methodological differences can greatly influence conclusions drawn from such data ( Robinson 1994).
To our knowledge, no other study has clearly tested the response of multiple species to different degrees of heterogeneity. However, the effects of spatial scale of nutrient heterogeneity on total growth have been measured for Glechoma hederacea, a clonal herb. This species was able to forage successfully in large patches (25 cm × 50 cm) but responded to soils with small patches (12.5 cm × 12.5 cm and smaller) as if they were homogeneously poor ( Wijesinghe & Hutchings 1997). The surface area of the patch size when the plant could no longer detect nutrients was smaller than the size of the quarterly patch in our study.
We were unable to detect differences in discrimination between species, possibly because root proliferation was not stimulated at the highest fertility levels. All species in this experiment reached a peak rooting density at an intermediate fertilizer concentration, and proliferation dropped off at higher fertilizer concentrations ( Fig. 3). The consistency among the species in this response is suggestive that roots do indeed discriminate between patches of differing richness, as has been predicted by simulation models ( Gleeson & Fry 1997), but do not necessarily proliferate more at progressively higher levels.
Our data do not support the hypothesis that scale and precision are negatively correlated. When all species were compared, no measure of scale was negatively correlated with precision ( Table 4). Furthermore, when just herbaceous plants were compared, relatively strong, positive relationships between scale and precision were detected ( Table 4 and Fig. 5). These correlations all lack power because they compare a limited number of species (n = 10 overall, n = 6 herbs). None the less they are interesting, considering that Campbell et al. (1991) reported a negative relationship between scale and precision. The contrast in findings between our experiment and that of Campbell et al. (1991) suggests that relationships between root foraging traits may not be general across plant communities, or that the difference in methods used to measure scale and precision influences the results dramatically ( Robinson 1994).
We expected that sensitivity to the soil heterogeneity would be greater for precise than for imprecise foragers, but no such effect was detected at the fertility levels of this experiment ( Table 4 and Fig. 5). In fact, the species with the highest and lowest precision (Liquidambar styraciflua and Desmodium strictum, respectively) were the two most sensitive species. Fransen et al. (1998) found that nitrogen acquisition by plants is sometimes enhanced in heterogeneous environments, but they concluded that the enhancement was not related to root proliferation. We did not assess nutrient uptake in our experiment. None the less, our findings, plus those of other studies, call into question the benefit that species obtain from investing carbon into proliferation of roots in nutrient-rich patches, and they suggest that other mechanisms result in high sensitivity to nutrient heterogeneity.
Two mechanisms that may result in enhanced nutrient uptake without root proliferation are plasticity in root uptake kinetics and plasticity in root demography ( Jackson & Caldwell 1996; Eissenstat & Yanai 1997). Jackson et al. (1990) found that phosphate uptake rates were up to 82% greater for roots growing in nutrient-rich patches than for roots growing outside patches. Furthermore, Caldwell (1994) demonstrated that some plants increase phosphate uptake from enriched patches without significantly increasing rooting density in these patches. A field ( Pregitzer et al. 1993 ) and a glasshouse ( Gross et al. 1993 ) study provide evidence that some plants respond to nutrient patches with demographic plasticity, although the responses reported are not uniform. Pregitzer et al. (1993) reported an overall community response of increased root longevity in enriched patches compared with roots in control patches. Gross et al. (1993) found a decreased life span for roots of four herbaceous species growing in enriched patches. Together, these studies suggest that plasticity in uptake rates and root demography are also complex responses, and by measuring only total root biomass in nutrient patches we may be missing other important plastic responses.
Herbaceous plants with root systems that are small relative to other species but with large root to shoot ratios were best able to gain benefits from nutrient patches in soils. A strong negative correlation between sensitivity and scale and a strong positive correlation between sensitivity and root to shoot ratio were observed ( Table 4 and Fig. 5). However, none of these correlations was statistically significant. Additional studies with greater numbers of test species are needed to determine whether our findings can be generalized to other plant communities.
Although they ranged widely in precision, woody plants exhibited the lowest scale ( Fig. 5). Thus, life form may be a fair predictor of a root system’s scale, but not of precision. For woody plants that have a lower growth rate than many herbs, it is likely that a longer experiment and larger pots would reveal greater variability in scale.
Our intent in this study was to determine if life forms differ in nutrient foraging behaviour, but since our test species also differed with respect to dominance during succession, we were able to examine relationships between foraging traits and successional status using rank correlation ( Table 5). We found no relationship between successional status and sensitivity or precision, although early successional plants had greater scale (significantly so when measured by root length density; Table 5). This analysis is confounded by the fact that life form and successional status co-vary ( Table 1).
Table 5. Rank correlations between nutrient foraging traits and year of dominance during succession (n = 10 species, P-values given after correlation coefficients). A rank of 1 was given for species with the highest value for a trait, and for species with the earliest year of dominance during succession (see Table 1). Ties were assigned average ranks, and species that appear at year 30 or thereafter in succession were considered later successional species than those appearing during years 5–100
|Trait||r (P) |
|Root mass density (scale)||0.58 (0.07)|
|Root length density (scale)||0.75 (0.01)|
Our data provide strong evidence that current theories about foraging behaviour and trade-offs between certain traits need more testing and perhaps some rethinking. We still believe that the ability of roots to respond to nutrient patches is a key to predicting competitive interactions between individual species. However, it may be difficult to group species according to their root foraging abilities due to an apparent lack of correlation between root foraging traits and plant groups (herbs, woody species; early and late successional species). Further, more work needs to be done before we are able to suggest which traits increase fitness in heterogeneous environments. In this study we assessed morphological root system responses only, and noted no clear pattern between them and growth benefits as heterogeneity increased. More comprehensive studies that examine demographic and physiological plasticity in addition to root system morphology may be needed to reveal patterns between plant response to heterogeneity and fitness benefits.