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Keywords:

  • clonal plants;
  • foraging;
  • morphological plasticity;
  • patch selection;
  • root : shoot ratio

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

1  We report on an experimental investigation into the effects of contrast in patch quality and patch size upon the performance of the clonal herb Glechoma hederacea in nutritionally heterogeneous environments.

2  There were six treatments providing different degrees of patch contrast. These ranged from maximum contrast, in which patches consisted entirely of compost or sand, to homogeneity, in which all patches contained 50% of each. These were combined factorially with two patch size treatments. Overall, all treatments provided the same quantity of compost and sand, and the same area and volume of higher and lower quality patches.

3  Clones in the large-patch environments produced significantly more root biomass in both rich- and poor- quality patches than the clones in the small-patch environments. At both scales there was a decline in root biomass in the rich patches, accompanied by an increase in root biomass in the poor patches, as patch quality converged.

4  The proportion of the root biomass of clones that was located in nutrient-rich patches was greatest at high contrast and declined gradually to become equal in all patches, as contrast between patches diminished to homogeneity. This effect was independent of patch scale. There was a close match between root placement and nutrient availability in different quality patches in all treatments except that with the highest contrast.

5  At both patch scales, root : shoot ratios of clone parts in rich patches rose (and those in poor patches declined) as patch contrast increased. This species is therefore capable of morphological specialization at a local level when clones grow in heterogeneous environments. These effects were also greater at the larger patch scale.

6  The effect of patch contrast on total clone yield was significantly modified by patch scale. At lower contrast, yield was similar at both scales, whereas at higher contrast, yield was significantly greater in the large-patch treatment.

7  Although G. hederacea can match its morphology to environmental heterogeneity in some habitats, it is less able to do so when patches are small-scale and highly contrasting. These limitations cause considerable differences in the yield that can be achieved from a given quantity of resource provided in different configurations.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Spatial and temporal heterogeneity in growing conditions commonly has significant effects upon the perception of habitat quality by plants (Turkington & Harper 1979; Pearcy 1983; Chazdon et al. 1988; Lechowicz & Bell 1991; Wijesinghe & Hutchings 1997; Einsmann et al. 1999). The ubiquity of heterogeneity in natural habitats makes it likely that plasticity will have evolved enabling plants to cope with, and perhaps even to benefit from, heterogeneous rather than homogeneous environmental conditions. This may be particularly true for clonal species that distribute ramets widely in space and time. Sites occupied by connected ramets of these species often differ significantly from one another in the availability of essential resources. Several studies of clonal species have described plasticity in the form of localized morphological responses to such small-scale differences in growing conditions (Noble et al. 1979; Salzman 1985; Slade & Hutchings 1987a,b). In addition, physiological integration often protects ramets against local environmental adversity by allowing the redistribution of resources from ramets located in sites of resource abundance to ramets located where resources are scarce (Alpert & Mooney 1986; Alpert 1991; Stuefer et al. 1994).

Recent studies have shown that one of the ways in which clonal plants can respond morphologically to environmental heterogeneity is by selective placement of resource-acquiring structures in favourable habitat patches (Salzman 1985; Birch & Hutchings 1994; Robinson 1994; Wijesinghe & Hutchings 1996, 1997; Alpert & Stuefer 1997). This is expected to enhance resource acquisition in comparison with an unresponsive pattern of placement and is regarded as a manifestation of foraging behaviour (Hutchings & de Kroon 1994). Such foraging behaviour is often accompanied by localized morphological specializations that would further enhance the ability of the plant to acquire resources from habitat patches where they are abundant. Patchy distribution of light will elicit different specializations from those triggered by patchy distribution of soil-based resources because the structures used for resource capture are different in each case. For example, when light is patchy, parts of Glechoma hederacea L. clones located in high-light patches were more branched, produced more leaf area per primary ramet and allocated a significantly greater proportion of their biomass to leaves than clone parts in low-light patches (Wijesinghe & Hutchings 1996). Wijesinghe & Hutchings (1997) carried out a more complex study of the effects of patchy nutrient supply on the growth of G. hederacea. The same overall quantity of nutrients was provided to clones in a series of treatments each with a different patch size. Nutrient-rich and nutrient-poor patches occupied the same total area in all treatments. When patch size was large, clone parts located in nutrient-rich patches produced significantly more root biomass, and had a higher root : shoot ratio, than clone parts in nutrient-poor patches. However, as patch size declined, the ability to place roots selectively in high-quality patches fell significantly, and the root : shoot ratio tended to be more similar in both types of patch. Thus, the capacity of the species to forage, and the extent of its morphological specialization, depended on the scale of environmental heterogeneity.

The capacity of clonal species to forage and to exhibit morphological specialization in patchy habitats raises the possibility that yield may be altered by the pattern of resource provision. Verification of such a hypothesis requires comparisons of growth to be made when the same quantity of resources is provided in different configurations. Some support for this hypothesis, based on experiments using this approach, already exists. Birch & Hutchings (1994) observed significantly greater yield in G. hederacea clones in heterogeneous habitats than in homogeneous habitats. In addition, the study by Wijesinghe & Hutchings (1997), which provided the same quantity of nutrients to G. hederacea with heterogeneity at different spatial scales, also produced significant yield differences. Their results demonstrated that yield declined as the ability of the clone to place roots selectively in high-quality patches decreased. Some habitats were apparently perceived as homogeneous by the plant, as selective root placement did not occur in them. We therefore expect clone yield under heterogeneous conditions to be greater when the scale of environmental patchiness is perceptible to the plant, and when the difference between the quality of patches is sufficient to elicit morphological specialization.

Whereas the effects of scale of heterogeneity on clone performance have been studied experimentally, the effects of relative quality of patches (i.e. patch contrast) have not (although a modelling approach to its study has been used; Caraco & Kelly 1991). The current paper reports an experimental investigation into the effect of contrast in patch quality on the growth of G. hederacea in heterogeneous habitats. Patches of different quality were created by varying the proportions of sand and potting compost in the rooting medium, thereby altering the spatial availability of nutrients. Different treatments provided different levels of contrast in quality between patches. Overall resource supply was identical in all treatments. The different treatments provided environments ranging in quality from homogeneity (no contrast between patch types) to extreme heterogeneity (highest contrast between patch types). The different contrast treatments were also provided at different spatial scales because it has been shown previously that clone yield is dependent on patch size (Wijesinghe & Hutchings 1997). Overall, the experiment analysed growth at two patch scales and at six levels of patch contrast.

The hypotheses tested and the predictions associated with them are given below.

Hypothesis 1: foraging for nutrients, expressed as the preferential location of roots in higher quality soil patches (Hutchings & de Kroon 1994), would be greater at higher patch contrast and at larger patch scale.

We predicted that preferential location of roots in high-quality patches would be most pronounced in the treatment with the highest contrast and would decline as contrast decreased until, in the homogeneous treatment, roots would be distributed evenly throughout the substrate. In addition, we predicted that, at a given level of contrast, preferential location of roots in higher quality patches would be more pronounced in the large-patch treatment than in the small-patch treatment, i.e. that there would be a significant interaction between patch size and contrast.

Hypothesis 2: morphological specialization would be greater at higher patch contrast and at larger patch scale.

We measured morphological specialization as the local root : shoot ratios of clone parts in patches of different quality. Our prediction was that the differences between root : shoot ratios of clone parts located in rich and poor patches would be greater when contrast was higher, because higher quality patches provided more nutrients when patch contrast was greater. In addition, as G. hederacea can detect larger patches more easily than smaller patches (Wijesinghe & Hutchings 1997), we also predicted that the differences between root : shoot ratios of clone parts in patches of different quality would be higher in the large-patch treatment than in the small-patch treatment at a given level of contrast, i.e. that there would be a significant interaction between patch size and contrast.

Hypothesis 3: clone yield would be greater at higher patch contrast and at larger patch scale than at lower contrast and at smaller scale.

Because we have predicted that both selective root placement and morphological specialization would be expressed more at larger patch scale and at higher contrast (hypotheses 1 and 2), yield should be greater at the larger patch scale than at the smaller scale in all heterogeneous environments.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The species

Glechoma hederacea (Lamiaceae) is a perennial clonal herb native to the British Isles. It is common in woods, grasslands and waste places (Clapham et al. 1987). Clones consist of many ramets produced at regular intervals along slender plagiotropic stolons. A single ramet has two leaves, each borne on a petiole arising from a node on the stolon. Each node is capable of producing roots when in direct contact with the substrate. A single lateral bud is produced in the axil of each leaf and this can develop into a higher-order stolon. Despite the determinate nature of the morphology of the individual ramet, there is substantial plasticity in the growth of all its constituent structures. For example, the duration of leaf and petiole expansion can be very protracted and responsive to changes in local conditions (Birch & Hutchings 1992). Consequently, the root : shoot ratio of an individual ramet can vary over a wide range. Branching at nodes is also highly responsive to local growing conditions, being more pronounced in favourable light and soil conditions (Slade & Hutchings 1987a; Wijesinghe & Hutchings 1996).

The resources acquired by a single ramet can be redistributed within the clone by translocation, and most translocation is in an acropetal direction from older to younger ramets (Price & Hutchings 1992; Price et al. 1992). As a result, different stolon branches quickly acquire a high degree of physiological independence, despite the physical connections between them. Thus, each stolon develops into an integrated physiological unit (Watson & Casper 1984) that can respond semi-autonomously to local environmental conditions.

The experimental design

In August 1996, one G. hederacea ramet of a single genotype was transplanted into each of 60 wooden boxes of area 50 × 50 cm and depth 10 cm. The lateral dimensions of the boxes were similar to those of many naturally occurring clones (Wijesinghe & Hutchings 1997). Each box was filled with 6000 ml of washed horticultural sand and 6000 ml of John Innes potting compost. The two types of substrate were mixed in different ratios and used to create patches of different quality in each box. Each of the 60 boxes contained two types of patch. In rich patches the majority of the substrate was compost. In poor patches the majority of the substrate was sand. The patches were arranged in a chequer-board pattern (Fig. 1).

image

Figure 1. The patch size treatments. Within each treatment the rich and poor patches were of the same size and each patch type covered 50% of the total box area. Large-patch treatments contained four patches and small-patch treatments contained 16 patches. A single ramet of G. hederacea was planted in each box as indicated by the arrow. The two emerging stolons were directed towards the opposite halves of the box and allowed to root freely. Details of the quality of the rich and poor patches in different treatments are shown in Table 1.

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The experiment was a 2 × 6 factorial design, with patch size and the contrast in quality between patch types as the two main factors. There were five replicates in each size × contrast treatment combination (n = 60), set out in a fully randomized arrangement in a glasshouse. There were two patch-size treatments. In each of 30 boxes assigned to the large-patch treatment there were four 25× 25-cm patches, and in each of 30 boxes assigned to the small-patch treatment there were 16 12.5 × 12.5-cm patches (Fig. 1). The scale of the large-patch treatment corresponded with treatment T2, and that of the small patch treatment with treatment T4, of Wijesinghe & Hutchings (1997). There were six treatments in which the contrast between the quality of poor and rich patches differed. In the treatment with the highest contrast (0 : 100), the poor patches only contained sand and the rich patches only contained compost. In the treatment with no contrast (50 : 50), both the ‘poor’ and ‘rich’ patches contained compost and sand mixed in equal proportions (Table 1). There were four intermediate contrast treatments (10 : 90, 20 : 80, 30 : 70 and 40 : 60), in which the poor patches consisted of 10%, 20%, 30% and 40%, respectively, by volume of compost while their rich counterparts consisted of 90%, 80%, 70% and 60%, respectively, by volume of compost (Table 1). All treatments received the same overall volume of both compost and sand, irrespective of size of patches and contrast between patches (Table 1). The ability of the clone to grow on a standard quantity of resources, distributed over a standard area but in patches of different sizes and in patches with different levels of contrast in quality, was thus being tested.

Table 1.  The volume (ml) and percentage of sand and compost in each of the poor and rich patches of large- and small-patch environments for each patch contrast treatment. All treatments received the same total amount of substrate, i.e. 6000 ml of sand and 6000 ml of compost. Sand and compost were mixed in different ratios for each patch type to give poor and rich patches whose differential in quality was high (as in treatment 0 : 100) or low (as in treatment 50 : 50). In the large-patch treatments there were two poor and two rich patches. In the small-patch treatments there were eight poor and eight rich patches. Ten boxes were assigned to each contrast treatment, half of which were large-patch environments and the other half small-patch environments (n = 60)
Large-patch environmentSmall-patch environment
Poor patchRich patchPoor patchRich patch
Patch contrast treatmentSand ml (%)Compost ml (%)Sand ml (%)Compost ml (%)Sand ml (%)Compost ml (%)Sand ml (%)Compost ml (%)
0 : 1003000 (100)0 (0)0 (0)3000 (100)750 (100)0 (0)0 (0)750 (100)
10 : 902700 (90)300 (10)300 (10)2700 (90)675 (90)75 (10)75 (10)675 (90)
20 : 802400 (80)600 (20)600 (20)2400 (80)600 (80)150 (20)150 (20)600 (80)
30 : 702100 (70)900 (30)900 (30)2100 (70)525 (70)225 (30)225 (30)525 (70)
40 : 601800 (60)1200 (40)1200 (40)1800 (60)450 (60)300 (40)300 (40)450 (60)
50 : 501500 (50)1500 (50)1500 (50)1500 (50)375 (50)375 (50)375 (50)375 (50)

At the start of the experiment the clone in each box consisted of a single ramet with two emerging stolons, each approximately 3 cm long, one of which initially grew into a high quality patch and one into a poor quality patch (Fig. 1). The ramet was rooted half-way along one side of the box at the junction between two patches. All ramets produced by the two growing stolons were allowed to root freely within the box. The parts of stolons that grew over the edges of the box continued to elongate without their ramets rooting. Tap water was provided as necessary to keep all patches moist at all times. Plants were grown under a 12-h day/night cycle and at a temperature of 20–25 °C.

The experiment was carried out for 12 weeks, from 6 August 1996 until 29 October 1996, when the clones were harvested. The above-ground clone parts and roots in each patch, and the unrooted stolon parts, were harvested separately, dried at 80 °C to a constant weight and weighed.

Data analysis

The data were analysed using fixed-model two-way univariate analysis of variance (anova), multivariate analysis of variance (manova) or one-factor analysis of covariance (ancova). Data were normally distributed and homoscedastic. Thus, transformations were not necessary except in the case of proportions, which were angular transformed. In the presentation of the results, the statistical comparisons of the proportional distribution of shoot and root biomass between rich and poor patches in each treatment are presented for the rich patches only. The analyses for poor patches gave identical results because the data were the reciprocal of those for rich patches.

In the analysis of the proportion of clone root biomass in rich patches we used orthogonal polynomials to decompose the sum of squares of the interaction between patch size and patch contrast. This technique can be applied when the values of the independent variable (in this case patch contrast) are equally spaced and the number of replicates in each treatment combination is equal (Sokal & Rohlf 1981).

One-factor ancova was used to analyse the effects of patch size and patch contrast on shoot, root and total biomass. Patch contrast was used as the ordered independent variable. In each analysis, the slopes of linear regressions were compared for the patch size treatments. The linearity of slopes was confirmed before ancova was carried out. If the slopes were found to be homogeneous (i.e. their gradients were not significantly different), the tests for adjusted means were conducted. When the assumption of homogeneity of regression slopes is not met, the ancovaF-test and the adjustment process can produce misleading results (Huitema 1980). Therefore, if the slopes were heterogeneous, the Johnson–Neyman technique was applied to identify the values of the independent variable (patch contrast) over which values of the dependent variable (biomass) were significantly different between patch size treatments (Huitema 1980). For this test, the level of significance was set at P = 0.05. The homogeneity of regression slopes test in the one-factor ancova is analogous to the interaction test in the two-factor anova. The Johnson–Neyman technique in one-factor ancova designs with heterogeneous slopes is analogous to simple main effects tests in two-factor anova when the interaction term is significant (Huitema 1980).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Analyses of the total biomass of clones including parts outside the boxes showed that total biomass was significantly affected by patch size but not by patch contrast or by the interaction between the two (contrast; F5,48 = 0.50, P = NS; size: F1,48 = 4.55, P < 0.05; contrast × size: F5,48 = 0.99, P = NS; Fig. 2a). However, the proportion of total biomass outside the boxes was not affected by either of the two main factors (contrast: F5,48 = 0.33, P = NS; size: F1,48 = 0.47, P = NS). Also, there was no significant effect of the contrast×size interaction on this proportion (F5,48 = 0.58, P = NS; Fig. 2b). Therefore, subsequent analyses were performed only on the parts of the clones inside the box. This had the advantage of enabling comparisons of clone performance, standardized by area, to be made.

image

Figure 2. Mean (± SE) total biomass of clones including parts outside the boxes (a), and mean (± SE) proportion of total biomass outside the boxes (b), in the large- and small-patch environments at different patch contrasts.

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Total ramet production within the boxes was significantly affected by patch size (F1,48 = 6.57, P < 0.05) but not by patch contrast (F5,48 = 0.66, P = NS), nor by the interaction between the two (F5,48 = 0.76, P = NS; Fig. 3a). Ramet production in rich and poor patches was significantly affected by patch size but not by patch contrast, nor by the interaction between the two (Table 2). At high levels of contrast, more ramets were located in both rich and poor patches in the large-patch environments than in the small-patch environments (Fig. 3b).

image

Figure 3. Mean (± SE) number of ramets produced within the boxes by (a) the whole clone, and (b) by clone parts in rich and poor patches, in the large- and small-patch environments at different patch contrasts.

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Table 2.  Multivariate analysis of variance of the number of ramets of G. hederacea clone parts growing in rich and poor patches of the experimental environments. (a) Multivariate test statistics and (b) the corresponding univariate test statistics are given for the test of patch size and patch contrast and for the interactions between the two. The degrees of freedom, F-statistic and significance (at P < 0.05) are reported for each test (a)
SourceWilks’ Lambdad.f.FP
Patch size0.8702, 473.521  < 0.05
Patch contrast0.81610, 941.007NS
Patch size × patch contrast0.86310, 940.720NS
(b)
  Rich patchesPoor patches
Sourced.f.FPFP
Patch size17.032  < 0.054.145  < 0.05
Patch contrast50.809NS0.771NS
Patch size × patch contrast50.809NS0.696NS
Error48    

In the rest of this section we describe results pertaining to the interpretation of each of the three hypotheses presented in the Introduction.

Hypothesis 1: foraging

Multivariate analysis of variance revealed that the production of shoot and root biomass in rich and poor patches was significantly affected by both patch size and patch contrast, and by the interaction between the two (Table 3a). The significance of these results was caused mainly by the differences in the pattern of root production by clone parts in rich and poor patches. The univariate analyses revealed that shoot biomass in either rich or poor patches was not significantly affected by patch size or patch contrast (Table 3b). However, clones in the large-patch environments produced significantly more root biomass in both rich and poor patches than the clones in the small-patch environments (Fig. 4a). At both patch scales there was a decline in root biomass in the rich patches, accompanied by an increase in root biomass in the poor patches, as the quality of rich and poor patches converged, resulting in a significant interaction term in the manova (Table 3a). For example, in the large-patch environment, there was more than a threefold decline in root biomass located in the rich patches, and a sevenfold increase in root biomass located in the poor patches, between the 0 : 100 and the 50 : 50 patch contrast treatments, despite the area and volume of each type of patch being the same in every case. As the difference in quality between rich and poor patches declined, root biomass in the two patch types became similar in both large- and small-patch environments (Fig. 4a).

Table 3.  Multivariate analysis of variance of the biomass of shoots and roots of G. hederacea clone parts growing in rich and poor patches of the experimental environments. (a) Multivariate test statistics and (b) the corresponding univariate test statistics are given for the test of patch size and patch contrast and for the interactions between the two. The degrees of freedom, F-statistic and significance (at P < 0.05) are reported for each test (a)
SourceWilks’ Lambdad.f.FP 
Patch size0.691 4, 455.022  < 0.01
Patch contrast0.187 20, 1504.931  < 0.0001
Patch size × patch contrast0.506 20, 1501.713  < 0.05
(b)
  Shoot biomassRoot biomass
  Rich patchesPoor patchesRich patchesPoor patches
Sourced.f.FP F PFPFP
Patch size12.804NS3.111NS16.443  < 0.00015.904  < 0.05
Patch contrast50.633NS1.478NS4.266  < 0.019.794  < 0.0001
Patch size × patch contrast51.103NS1.093NS1.653NS0.680NS
Error48        
image

Figure 4. Mean (± SE) root biomass in rich and poor patches (a), and mean (± SE) proportion of root biomass in rich patches (b), in the large- and small-patch environments at different patch contrasts.

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There was no significant difference between large- and small-patch environments in the proportion of shoot biomass located in patches of different quality (anova of angular transformed data for rich patches: F1,48 = 0.0001, P = NS). However, patch contrast had a significant effect on the proportion of shoot biomass located in rich patches (F5,48 = 2.72, P < 0.05), mainly because of differences in biomass allocation between the 0 : 100 and the 50 : 50 treatments (Bonferroni multiple means comparison test at P < 0.05 level: 0 :100, 10 : 90, 20 : 80, 30 : 70, 40 : 60, 50 : 50). In the 0 : 100 contrast treatments a mean proportion (± SE) of 0.56 ± 0.02 of the total shoot biomass was located in rich patches, whereas in the 50 : 50 treatments the mean proportion of shoot biomass located in rich patches was significantly less (0.49 ± 0.01). There was no significant patch size × patch contrast interaction effect on the proportion of shoot biomass located in rich or poor patches (F5,48 = 1.19, P = NS).

The relationship between the proportion of root biomass in rich patches and patch contrast was more complex. For both patch scales, the relationship was non-linear and described by a quadratic model (Table 4 and Fig. 4b). The proportion of root biomass located in rich and poor patches was not affected by patch size. However, patch contrast had a very marked effect on the proportion of root biomass located in rich patches (Table 4 and Fig. 4b). In the treatments with the three greatest levels of contrast, rich patches contained between 0.92 and 0.86 of the total root biomass. As contrast between the two patch types diminished there was a sharp decline in the proportion of root biomass located in rich patches, to values of approximately 0.50 in the 50 : 50 treatments. Again, as for shoot biomass, there was no significant patch size × patch contrast interaction effect on the proportion of root biomass located in patches of different quality (Table 4).

Table 4.  Orthogonal polynomials of the proportion of the total root biomass of G. hederacea clones located in rich patches of the experimental environments. The data were angular transformed prior to analysis. The degrees of freedom, mean squares, F-statistic and significance (at P < 0.05) are reported
Sourced.f.MSFP
Patch size10.00050.0709NS
Patch contrast50.454366.8088  < 0.0001
ContrastLinear12.1409314.8382  < 0.0001
ContrastQuadratic10.129719.0735  < 0.0001
Residual30.00020.0294NS
Patch size × patch contrast50.00891.3088NS
Size × contrastLinear10.00380.5588NS
Size × contrastQuadratic10.00240.3529NS
Residual30.01291.8971NS
Error480.0068  

Hypothesis 2: morphological specialization

In the large-patch environments, clone parts located in rich patches produced relatively more root biomass than clone parts located in rich patches in the small-patch environments (Table 5b and Fig. 5). As the quality of rich and poor patches converged in the large-patch environments, there was a decline in root : shoot ratios of clone parts in the rich patches, from 2.27 in the 0 : 100 patch contrast treatment to 0.68 in the 50 : 50 treatment (Fig. 5). In the small-patch environments this ratio only ranged from a maximum value of 1.19 in the 10 : 90 treatment to 0.68 in the 50 : 50 treatment. While root : shoot ratios in rich patches declined as contrast fell, there was simultaneously a steady increase in root : shoot ratios in the poor patches at both patch scales (Fig. 5). All root : shoot ratios converged closely in the homogeneous 50 : 50 treatment. Consequently, there was a significant interaction between patch size and patch contrast in the manova, although the interaction terms in the univariate tests were non-significant (Table 5a). In the poor-quality patches at both patch scales, more biomass was always allocated to shoots than to roots, i.e. the root : shoot ratio was always less than one in such patches. In both large- and small-patch environments, clone parts in poor patches always had far lower root : shoot ratios than clone parts in the rich patches when the contrast between the two patch types was high (30 : 70 or greater).

Table 5.   Multivariate analysis of variance of the root : shoot ratio of G. hederacea clone parts growing in rich and poor patches of the experimental environments. (a) Multivariate test statistics and (b) the corresponding univariate test statistics are given for the test of patch size and patch contrast and for the interactions between the two. The degrees of freedom (d.f.), F-statistic and significance (at P < 0.05) are reported for each test (a)
SourceWilks’ Lambdad.f.FP
Patch size0.7542, 477.661  < 0.001
Patch contrast0.19810, 9411.736  < 0.0001
Patch size × patch contrast0.68010, 942.000  < 0.05
(b)
  Rich patchesPoor patches
Sourced.f.FPFP
Patch size115.232< 0.00016.945  < 0.05
Patch contrast56.712< 0.000111.554< 0.0001
Patch size × patch contrast51.548NS0.763NS
Error48    
image

Figure 5. Mean (± SE) root : shoot ratio of clone parts in rich and poor patches in the large- and small-patch environments at different patch contrasts.

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Hypothesis 3: clone yield

For both patch sizes, the relationship between shoot biomass and contrast was linear but the gradients were not significantly different from zero (Fig. 6a). Thus, shoot biomass was not affected by patch contrast. ancova results showed that the slopes were homogeneous and that the adjusted means (y-intercept) were not significantly different (Table 6a). Thus, shoot biomass was also not significantly affected by patch size.

image

Figure 6. The relationships between patch contrast and (a) shoot biomass (y = 10.65–0.023x for the large-patch treatment and y = 7.32 + 0.056x for the small-patch treatment), (b) root biomass (y = 13.46–0.109x for the large-patch treatment and y = 6.26 + 0.006x for the small-patch treatment) and (c) whole clone biomass (y = 24.09–0.133x for the large-patch treatment and y = 13.56 + 0.062x for the small-patch treatment) in the large- and small-patch environments. Only the slope of the regression for root biomass in the large-patch treatment was significantly different from zero (F1,28 = 5.12, P < 0.05). The linear regressions were fitted to all data points. Mean (± SE) biomass values are shown for each patch contrast treatment. In (c), values of the dependent variable to the right of the vertical broken line are not significantly different for the two patch size treatments. Values to the left of this line are significantly different (Johnson–Neyman technique, P = 0.05).

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Table 6.  Analysis of covariance of the effect of patch size on the regression of (a) shoot, (b) root and (c) total clone biomass of G. hederacea clones against patch contrast. The degrees of freedom, mean square, F-statistic and significance (at P < 0.05) are reported for each test. For each analysis, a test of homogeneity of the regression slopes was carried out first. The adjusted means were tested only if the slopes were found to be homogeneous
Sourced.f.MSFP
(a) Shoot biomass
Between slopes127.683.49NS
Within regressions567.91  
Adjusted means127.263.30NS
Error578.26  
(b) Root biomass
Between slopes158.973.67NS
Within regressions5616.09  
Adjusted means1266.2815.81  < 0.001
Error5716.84  
(c) Total clone biomass
Between slopes1167.745.30  < 0.05
Within regressions5631.63  

For the large-patch treatment, the relationship between root biomass and patch contrast was linear and the gradient was significantly different from zero, with biomass being larger at greater contrast (Fig. 6b). For the small-patch treatments this relationship was also linear, but the gradient was not significantly different from zero. ancova results showed that the two slopes were homogeneous, demonstrating that there was no significant effect of the patch size × patch contrast interaction on root biomass (Table 6b). However, the large-patch treatment produced significantly more root biomass than the small-patch treatment, i.e. the adjusted means test was significant.

For total clone yield, the relationships with patch contrast were linear for both patch sizes (Fig. 6c) but the gradients were not significantly different from zero. Thus yield was not significantly affected by patch contrast. The ancova results showed that the two slopes were heterogeneous. Therefore, there was a significant effect of patch size and of the patch size × contrast interaction on yield (Table 6c). The Johnson–Neyman technique revealed that total clone yield was significantly higher in the large-patch treatment than in the small-patch treatment at all contrasts between 35 : 65 and 0 : 100 (at the P = 0.05 level).

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The major results relating to the hypotheses of this study are as follows. (i) The proportion of the root biomass of clones that was located in nutrient-rich patches was significantly altered by patch contrast but not by patch scale (Fig. 4b). (ii) Morphological specialization, as measured by differences in root : shoot ratios of clone parts located in rich and poor patches, was greatest when clones were grown in environments with large patches and with high levels of patch contrast. Root : shoot ratio was higher for clone parts in nutrient-rich patches, at all contrast levels, and highest when patches were large rather than small (Fig. 5). (iii) Clone yield was greater at the larger patch scale than at the smaller scale in heterogeneous environments with a high degree of contrast (Fig. 6c). The greater growth was achieved primarily because of greater root production in these environments (Fig. 6b).

Preferential location of clone roots in high-quality patches is a manifestation of foraging behaviour (Hutchings & de Kroon 1994), and is expected to improve nutrient acquisition in comparison with an unresponsive pattern of root placement. It should be emphasized that roots were the responsive structures in this study. Neither ramet number nor shoot biomass responded to patch quality (Tables 2 and 3). These results conform to the definition of foraging given by Hutchings & de Kroon (1994) and bear out previous studies (Wijesinghe & Hutchings 1996, 1997) in showing that it is resource-acquiring structures (either roots or leaves), rather than ramets, that respond to the resource in heterogeneous supply. In the present study, roots were evenly distributed throughout the homogeneous (50 : 50) treatments whereas in heterogeneous treatments progressively greater proportions of root biomass were located in high-quality patches as contrast increased (Fig. 4b). Whereas we predicted that a greater proportion of roots would be located in the high-quality patches at a given level of contrast when patches were larger, this proved not to be the case, contradicting part of hypothesis 1. By using a wider range of patch sizes than those used here, Wijesinghe & Hutchings (1997) clearly demonstrated an effect of patch scale on the ability of G. hederacea to forage. They recorded substantial differences in the mean proportions of root biomass located in rich patches at the two scales used here, but high variance within treatments resulted in no significant difference in patterns of root placement by G. hederacea at these scales (see Fig. 4f in Wijesinghe & Hutchings 1997). Variance within treatments in root placement was low in the present study and the pattern of foraging was essentially identical at both patch scales (Fig. 4b).

Gersani et al. (1998) applied the marginal value theorem of Charnov (1976) to explain the distribution of roots of pea plants between habitat patches of different quality. They predicted that root biomass allocated to each patch would be proportional to the amount of nutrients it contained. Thus, if good patches contained twice as much nutrient as poor patches, root biomass in good patches should be twice that in poor patches. Both the results of Gersani et al. (1998) and those from the present study conform with this prediction. Figure 7 plots the relationship between the percentage of root biomass of G. hederacea located in rich patches against the percentage of all nutrients available in those patches. Also plotted are the expected values, assuming a precise match between root placement and nutrient availability. The 95% confidence bands around the observed data indicate that such a match was achieved in the homogeneous treatment and in all heterogeneous treatments except that with the highest level of contrast (0 : 100). We interpret this exception as indicating that there is a cost of moving across highly unfavourable habitat patches in which some ramets must root in order to gauge local habitat quality. This cost of exploration would be analogous to the costs of travelling and searching in patchy habitats identified by Charnov (1976). Where the low-quality patches contain some nutrients, the production of roots closely matches the expected response to the availability of nutrients (Fig. 7). In such conditions, the cost of exploration may be offset by the benefits of resources gained even in low-quality patches. Many natural habitats display small differences in patch quality rather than abrupt discontinuities (Lechowicz & Bell 1991; Jackson & Caldwell 1996). Thus, placement of roots by G. hederacea, at the scales used in this experiment, appears to be highly sensitive to the types of patch contrast that are likely to be encountered in the field, and foraging is equally effective at all such patch contrasts. It should be noted, however, that a close match between root placement and nutrient availability under different levels of patch contrast will be possible only if patch size can be detected by the plant (Levin 1992; Wijesinghe & Hutchings 1997). Moreover, although the proportion of roots in patches of different quality closely reflected the availability of nutrients in each patch, the absolute biomass of roots produced by the clone showed significant variation (Figs 4a and 6b). This demonstrates that, although all environments contained the same amount of nutrients, the extent to which the plant could exploit them was highly dependent on patch structure.

image

Figure 7. The relationship between the percentage of nutrients in rich patches and the percentage of root biomass in rich patches (angular transformed). The homogeneous treatment (50 : 50) is at the left and the highest-contrast treatment (0 : 100) is at the right of the horizontal axis. The data for the two patch sizes were pooled because there was no significant difference in the proportions between them (see Fig. 4b and Table 4). The broken lines are the 95% confidence limits for the quadratic relationship based on the observed data (y = –0.74 + 0.039x–0.0002x2, F2,57 = 174.48, P < 0.0001). The solid line shows the expected percentage of root biomass in the rich patches if there is a precise match between root placement and nutrient availability in patches. The solid circles represent the mean values for each level of contrast.

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Non-clonal species generally enhance their acquisition of scarce resources by adopting higher root : shoot ratios when nutrients are deficient than when they are abundant (Brouwer 1962; Aung 1974; Hunt & Nicholls 1986). However, such results have usually been based on studies of plants growing in homogeneous conditions. Several recent studies have shown that ramets of clonal species growing under heterogeneous conditions specialize morphologically to acquire locally abundant rather than scarce resources (reviewed by Alpert & Stuefer 1997). If the connections between ramets are severed, however, so that each fragment has a single root system in an essentially homogeneous location, each alters its root : shoot ratio in a manner corresponding to that of non-clonal species in homogeneous conditions (Friedman & Alpert 1991). Thus, within-clone morphological specialization only develops in heterogeneous environments when clones have physiologically integrated structures that sample different quality patches. In the homogeneous treatment in this study there was little evidence of local morphological specialization, as measured by root : shoot ratio, but as contrast increased local morphological specialization became apparent. It was greater in the larger-scale treatment at a given level of contrast (Fig. 5). Thus, the predictions of hypothesis 2 were fulfilled.

Hypothesis 3 predicted that clone yield would be greater at the larger patch scale than at the smaller scale in all heterogeneous environments. Our results show that when the contrast between good and bad patches was in the ratio of approximately 2 : 1 or greater, clone yield was higher in the large-patch treatment. At lower contrasts, yield was similar at both patch scales. Thus, hypothesis 3 was partially upheld. This hypothesis was founded on the assumption that root placement would be more selective, and morphological specialization greater, in the large-patch treatments at higher contrast. In fact, root placement responded only to patch contrast and not to patch scale (Fig. 4b), whereas morphological specialization responded to both (Table 5a and Fig. 5). Thus, a change in morphological specialization in response to both patch size and patch contrast was enough by itself to cause the differences in clone yield observed under the conditions of this experiment.

Two phenomena that are known to modify the responses of clonal plants to environmental heterogeneity are relevant in explaining these yield results. The first of these is that ramet ontogeny is responsive to local nutrient availability. Ramets of G. hederacea located in nutrient-rich patches produce roots earlier in their ontogeny than ramets in nutrient-poor patches (Birch & Hutchings 1994). Because root length increases exponentially in time, the difference in the onset of rooting will lead to much larger root systems being produced by clone parts in nutrient-rich patches (Birch & Hutchings 1994). This enables greater exploitation of the nutrients in such patches. This phenomenon is not known to be affected by patch size. The second phenomenon, which is affected by patch size, is that information gained about current conditions has a carryover effect that influences the morphology of later-produced parts of the clone. Consequently, local clone morphology does not reflect local patch quality unless patches are large enough for carryover effects to dissipate (Ackerly 1997; Hutchings 1997; Wijesinghe & Hutchings 1997). Yield will be affected by the quality of the match between local clone morphology and local growing conditions.

The consequences of carryover for clone yield in different environments might be as follows. In environments where patch contrast is low, regardless of patch scale, carryover effects will not be important because the discrepancy between patches is small and consequently the appropriate morphology for each patch type is similar. Thus, discord between morphology and patch quality will not greatly affect yield. In high-contrast environments, carryover effects will be influenced by patch size. When patches are small, carryover effects will be important, and mismatch between morphology and patch quality would be predicted to lower clone yield. When patches are large, carryover effects will decay within each patch, allowing the morphology of consecutively produced ramets to be modified until a match with patch quality is achieved (Slade & Hutchings 1987b). In large patches where nutrients are abundant, root : shoot ratios of clone parts will be high and root systems will be extensive, because of the earlier onset of rooting, resulting in the enhancement of nutrient acquisition. Thus, yield would be expected to be greater in high-contrast environments with large patches than in high-contrast environments with small patches. These predictions are borne out by our results for clone yield (Fig. 6c).

In conclusion, this study revealed (i) a close match between resource availability and the placement of resource-acquiring structures under all but the most heterogeneous conditions, and (ii) greater morphological specialization when resources were distributed in large patches with high contrast in quality. Glechoma hederacea clearly has an acute perception of the quality of its environment, and responds to it through foraging and local morphological specializations. However, while some habitats present environmental heterogeneity at spatial scales and contrasts to which the species can respond appropriately, in others it is not possible for the clone to make entirely appropriate morphological adjustments to match fluctuations in environmental quality. These limitations on the capacity of the clone to respond effectively to some heterogeneous conditions ultimately result in considerable differences in the yield that can be achieved from a given quantity of resource.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The authors thank Drs Adam Eyre-Walker and Libby John for comments on the manuscript. Two anonymous referees helped us to improve the manuscript greatly. We thank them for their perceptive comments. This research was carried out during the tenure of grant GR3/8843(ML4), awarded to M. J. Hutchings by the Natural Environment Research Council, UK.

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  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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Received 3 December 1998 revision accepted 30 March 1999