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Keywords:

  • Avena sativa;
  • activated carbon;
  • pot partitions;
  • root exudates;
  • root interactions;
  • self-inhibition;
  • self/non-self discrimination;
  • substrate volume;
  • tragedy of the commons

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • 1
    It has been claimed that, compared with plants grown without competition, plants competing for a common pool of soil-based resources overproduce roots at the expense of reproduction (known as the tragedy of the commons). However, experiments on this phenomenon have manipulated not only the presence/absence of neighbours, but also substrate volume. Restricted substrate volume can itself affect plant growth, possibly through chemical self-inhibition of root growth. We conducted an experiment with oats (Avena sativa) to examine whether the experimental design used in previous studies on the tragedy of the commons in root competition might have confounded the effects of detection of neighbours and substrate volume.
  • 2
    Six treatments combined two factors, namely the presence or absence of activated carbon, and either the presence of a plastic or a mesh partition, or the absence of a partition, between two plants in a pot. Activated carbon was used to adsorb root exudates and reduce their potential effects on root growth. In a seventh treatment, plants were grown alone in pots with half the substrate volume replaced by gravel, to fragment the distribution of available resources.
  • 3
    We observed no tragedy of the commons in a comparison of the performance of plants grown with and without partitions; plants performed equally well in the presence and absence of root competition.
  • 4
    In the treatment with gravel, plants displayed reduced tillering and shoot growth per unit root mass, and an earlier switch to reproduction.
  • 5
    Pot partitioning was associated with inhibition of root growth that was mediated by root exudates. When activated carbon was present, plants in partitioned pots performed better than plants growing with a root competitor.
  • 6
    We conclude that two processes could determine plant growth in the experimental design used in studies of the tragedy of the commons: (i) greater root self-inhibition in the more limited space of partitioned pots, and (ii) inefficient root placement in larger substrate volumes in unpartitioned pots that are shared with roots of a competitor. These findings provide a new challenge for experimental designs attempting to demonstrate the role of self/non-self discrimination in root competition.

Introduction

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

Recent studies on root competition have shown that, compared with plants grown without below-ground competition, plants competing for a common pool of soil-based resources allocate more mass to roots at the expense of reproduction (Gersani et al. 2001; O’Brien et al. 2005). This phenomenon has been described as a ‘tragedy of the commons’ (after Hardin 1968). The production of extra roots potentially confers a selective advantage to a plant by allowing capture of more nutrients and water at the expense of its competitors. If competitors adopt the same strategy, however, an increase in root production may not benefit any plant, and all have to pay the costs of producing additional roots and of having fewer resources to devote to reproduction (Zhang et al. 1999; Gersani et al. 2001). Unless plants cooperate and actively prevent invasion by non-cooperators, the overproduction of roots in the presence of root competitors appears to be the only evolutionarily stable strategy (Zhang et al. 1999; Gersani et al. 2001). Thus, the tragedy of the commons should be a widespread phenomenon.

The tragedy of the commons can only arise if plants can detect and discriminate between their own roots and the roots of their neighbours (self/non-self discrimination). Currently, there is little understanding of how plants might do this. Root-mediated allelopathy and non-toxic signals that are elicited when root contact occurs could be important in the detection of the roots of neighbours, but they have been shown to decrease root growth rather than cause overproduction of roots (Mahall & Callaway 1992, 1996; Ridenour & Callaway 2001). Physiological coordination among roots of the same plant may play a significant role in allowing differentiation between self and non-self roots (Falik et al. 2003; Gruntman & Novoplansky 2004). The genetic identity of competitors has also been shown to determine the responses of plant roots to the roots of neighbours (Mahall & Callaway 1996; de Kroon et al. 2003).

Experiments on the reactions of plants to root competition often involve treatments that provide a constant volume of substrate and amount of nutrients per plant (Gersani et al. 2001; Maina et al. 2002; Falik et al. 2003; O’Brien et al. 2005; Falik et al. 2006). However, this results in plants that share rooting space with a neighbour potentially having access to twice as much substrate as plants grown without a neighbour. Thus, the effects of the presence of neighbours may be confounded with the effect of changing the rooting volume potentially available to each competitor (Schenk 2006). There is much evidence that the volume of substrate to which a plant has access may have significant effects on its yield (Taylor & Aarssen 1989; Gurevitch et al. 1990; McConnaughay & Bazzaz 1991, 1992; NeSmith & Duval 1998; McPhee & Aarssen 2001; Holzapfel & Alpert 2003; O’Brien et al. 2005; Schenk 2006; Hess & de Kroon 2007). For example, McConnaughay & Bazzaz (1991) showed that plants provided with a fixed amount of nutrients achieved greater vegetative growth when provided with larger substrate volumes. Species differed in sensitivity of growth and allocation to reproduction in response to volume of substrate available. Reassessment of the data from previous studies on the tragedy of the commons and self/non-self root discrimination has shown that some of the results could indeed be attributed to differences in substrate volumes provided in different treatments (Hess & de Kroon 2007).

The effects of substrate volume and space partitioning on plant growth, and the mechanisms involved, are still not fully understood. Changes in root architecture, morphology and hormone production have been proposed as causes of reduced resource acquisition when rooting volume is smaller, resulting in lower plant performance (Hameed et al. 1987; McConnaughay & Bazzaz 1991, 1992; Kharkina et al. 1999). Physical contact between different roots of a single plant may be important in coordinating root growth and function, and this may be disrupted by physical obstacles (Holzapfel & Alpert 2003). One proximate mechanism behind responses to the presence of inert obstacles in the soil was reported by Falik et al. (2005); reduced growth of roots towards physical obstacles (lengths of nylon string) was caused by sensitivity of roots to their own allelopathic exudates accumulating in the vicinity of obstacles.

Another possible cause of the apparent tragedy of the commons in root competition is use of the average mass of groups of plants as an equivalent of absolute mass of individual plants (Laird & Aarssen 2005). If there is a decelerating relationship between substrate volume and plant mass, and greater inequality in total mass of plants grown with competitors than of plants grown alone (due to size-asymmetric competition; Weiner 1990; Schwinning & Weiner 1998; Cahill 2002), average mass per individual will be lower for plants grown with competitors than for plants grown alone (see Fig. 1 in Laird & Aarssen 2005). Due to shoot/root growth allometry, a decrease in average plant size can also produce lower shoot to root ratios. Laird & Aarssen (2005) suggested that this would make the observed tragedy of the commons a mathematical inevitability of size-asymmetric competition rather than the result of a biological process.

We conducted an experiment with oats (Avena sativa L.) to examine whether the experimental design used in previous studies on the tragedy of the commons in root competition might have confounded the effects of self/non-self discrimination and substrate volume. We used similar treatments to those used in previous studies on the tragedy of the commons, namely two plants sharing the whole substrate (‘root competition’ treatment) and two plants with root systems separated by a solid partition, i.e. each having access to half of the substrate (‘no root competition’ treatment). In addition, we used several treatments that were not used in previous studies to examine mechanisms that could be involved in root communication, and in any responses of plants to changes in available substrate volume. These treatments involved (i) mesh partitions, which permitted the movement of resources and root exudates from one side of the partition to the other while preventing direct contact between roots of different plants, and (ii) the addition of activated carbon. Activated carbon adsorbs organic root exudates from the growth medium, reducing possible effects on root growth (Mahall & Callaway 1992; Ridenour & Callaway 2001).

A key challenge in studying the tragedy of the commons is to discriminate between active neighbour recognition and the effects of a neighbour on resource uptake. Even if the amount of resources and substrate volume per plant are kept constant in all treatments, the acquisition of resources by a competitor's roots creates depletion zones and thus generates a more heterogeneous pattern of resource distribution than when plants are grown alone. Importantly, remaining nutrients will be distributed throughout twice as large a volume as in the treatment without root competition. If root systems of competitors overlap, nutrient uptake per unit of root length may be lower as there will be less resource in substrate already occupied by a competitor. This aspect of nutrient uptake in the presence of neighbours has been largely overlooked in previous studies on the tragedy of the commons, although soil heterogeneity can significantly affect plant growth (Ryel & Caldwell 1998; Wijesinghe et al. 2001; Hutchings et al. 2003). We did not measure nutrient uptake efficiency directly in our study, but attempted to examine the effects on plant growth and development of substrate fragmentation and distribution of nutrients throughout a larger substrate volume. To do this, we grew single plants in pots of the same size as in other treatments, but replaced half of the substrate with fine gravel.

These treatments allowed us to test several hypotheses (Table 1). Studies on the effects of substrate volume show that restricting rooting space (as in ‘no root competition’ treatments) causes a reduction in root growth and affects biomass allocation and above-ground growth. However, the need to explore larger substrate volumes to acquire the same amount of resources in the ‘root competition’ treatment as in the ‘no root competition’ treatment may make growth in larger volumes less efficient. Thus, these two processes could act in opposition. It is difficult to predict their overall effect; depending on their relative importance in a particular study we might observe an increase, a decrease, or no effect on plant performance in the ‘no root competition’ treatment compared with the ‘root competition’ treatment. As in previous studies on the tragedy of the commons in root competition, we have examined root, shoot and total mass of plants, and the allometric relationship between shoot and root mass in different treatments, to test our hypotheses. We did not examine reproductive output. Total plant mass is a good measure of reproductive performance of agricultural oats as the relationship between seed yield and total mass of oats is very strong and scarcely influenced by growing conditions (Semchenko & Zobel 2005). We also compared size inequalities between plants in different treatments to control for the possibility that plants grown with root competition exhibit greater size inequality than plants grown without root competition (hypothesis 7 in Table 1), which would support Laird & Aarssen's (2005) suggestion that the tragedy of the commons could be a mathematical consequence of size-asymmetric competition. In a study by McConnaughay & Bazzaz (1991) on Setaria faberii, decreased tiller production and early flowering were observed in plants grown in smaller rooting volumes. We examined differences in numbers of tillers, numbers of leaves on the main shoot, and the emergence of the flag leaf (the final leaf on the shoot), which occurs at the same time as panicle formation in grasses (e.g. Counce et al. 2000), to estimate the effect of substrate fragmentation on vegetative growth and the timing of reproduction.

Table 1.  List of hypotheses and the specific comparisons that were used to test them. Details of treatments used in the study are presented in Fig. 1
No.HypothesisCritical testNotes
  • *

    Activated carbon was expected to adsorb organic root exudates in the growth medium and reduce any effects on root growth. In partitioned pots, activated carbon was added to reduce possible effects of root self-inhibition in smaller substrate volumes.

1When given equal amounts of nutrients and volumes of substrate per plant, plants experiencing root competition will produce the same root mass and total yield as plants growing without root competition‘No carbon, no partition’ vs. ‘no carbon, plastic partition’The absence of a partition in the first treatment allowed root competition between the two plants in a pot
2Fragmentation and dispersal of below-ground resources throughout larger substrate volumes will result in the reduction of growth and/or changes in the development of plants‘Gravel’ vs. ‘carbon, plastic partition’*The same amount of below-ground resources was distributed over twice as large a volume in the ‘gravel’ treatment as in the ‘carbon, plastic partition’ treatment. These represented fragmented and homogeneous distribution of below-ground resources, respectively
3Plants will exhibit changes in growth and/or biomass allocation in response to the presence of neighbour's root exudates in the substrate‘No carbon, no partition’ vs. ‘carbon, no partition’* 
4Partitioning of rooting volume results in self-inhibition of root growth due to concentration of inhibitory root exudates‘No carbon, mesh partition’ and ‘no carbon, plastic partition’ vs. ‘carbon, mesh partition’ and ‘carbon, plastic partition’, respectively* 
5Physical contact between root systems of different plants will change their growth and/or biomass allocation pattern‘Carbon, mesh partition’ vs. ‘carbon, no partition’*Treatment ‘carbon, no partition’ allowed root system overlap and root contact between the two plants in a pot, whereas treatment ‘carbon, mesh partition’ did not
6Resource acquisition by the roots of a neighbour will change plant growth and/or biomass allocation pattern‘Carbon, mesh partition’ vs. ‘carbon, plastic partition’*Treatment ‘carbon, mesh partition’ allowed the movement of resources between the two halves of a pot, whereas treatment ‘carbon, plastic partition’ did not
7Plants grown with root competition exhibit greater size inequality than plants grown without root competitionThe significance of the interaction between the ‘partition’ factor and the factor denoting an individual as smaller or larger than its neighbour (‘size category’)Significant interaction would indicate a significant effect of the presence of a neighbour's roots (no partition vs. mesh or plastic partition) on the symmetry of competition, supporting Laird & Aarssen's (2005) suggestion that the tragedy of the commons can be a mathematical consequence of size-asymmetric competition

Materials and methods

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

experimental design

Seeds of spring oats (Avena sativa L., variety Dala) were sown in trays of moist perlite on 28 November 2005. Nine days later, seedlings of equal size were transplanted into square plastic pots (15 cm × 15 cm × 20 cm deep) filled with potting sand. Seedlings were planted in the positions shown in Fig. 1. Seven treatments were used in the experiment. Six treatments combined two factors, namely the addition or absence of activated carbon and the presence or absence of a partition. In treatments with carbon addition, activated carbon was added at the rate of 20 mL of C powder to 1 L of potting sand. In treatments with partitions, the partitions were placed diagonally across the pots and half way between the two plants in a pot (Fig. 1). The edges between the pots and the partitions were sealed with silicon. Two types of partition were used: mesh partitions (PermatexTM Supercover Standard Ground Cover (GC) 95, Fargro Ltd, Littlehampton, UK), which allowed movement of soluble resources and root exudates between the two sides of the pot, but prevented contact between the roots of different plants, and solid plastic partitions (1 mm thick acrylic glass, Wickes Ltd, Northampton, UK), which prevented contact between the roots of different plants and also prevented movement of resources and root exudates between the two sides of the pot.

image

Figure 1. Experimental design. The experiment had seven treatments. Six treatments represented a 2 × 3 factorial design, with the addition of activated carbon as one factor (two levels: ‘no carbon’ and ‘carbon’) and pot partitioning as the other factor (three levels: ‘no partition’, ‘mesh partition’ and ‘plastic partition’). In these treatments, two seedlings were placed at equal distances from each other and the pot wall (indicated by arrows; a = 7 cm). In treatments with partitions, these were placed diagonally and equidistant from the plants. Letters ‘C’ indicate the presence of activated carbon in the substrate. In the seventh treatment (‘gravel’), single plants were grown in pots with half of the substrate volume replaced with gravel (indicated by black dots). In the half of the pot where the seedling was located, a mixture of one part gravel to two parts potting sand was used. In the other half of the pot, a mixture of two parts gravel to one part potting sand was used. See ‘Methods’ for further detail.

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In the seventh treatment (‘gravel’), plants were grown alone in pots of the same size with half of the substrate volume replaced with gravel (washed and graded lime-free quartzite grit, nominal size 4 mm, William Sinclair Horticulture Ltd, Lincoln, UK). The sand and gravel were thoroughly mixed to minimize empty spaces between gravel particles that could affect substrate porosity and water retention (Stephens et al. 1998; Fiès et al. 2002). The position of the single seedling in this treatment was the same as for one of the plants in the other treatments. We assumed that, in treatments with two plants growing in pots without a partition, the roots of each plant would experience more obstacles and resource-depleted substrate patches, as caused by the competitor's roots, when growing into the opposite half of the pot. To simulate this change in density of available space and resources for root growth, a mixture of one part gravel to two parts potting sand was used in the half of the pot into which the seedling was transplanted. A mixture of two parts gravel to one part potting sand was used in the other half of the pot (Fig. 1).

Each treatment was replicated 20 times. The pots were placed in a glasshouse with a 16-hour day/8-hour night cycle and a temperature of 18–20 °C. Positions of pots were randomized within the glasshouse every week, and all pots were closely spaced so that all plants experienced a similar level of above-ground competition. Pots were surface-watered to keep the substrate moist at all times. The pots were fertilized with 25 mL of 10% Hoagland's solution per plant on 15 December, 22 December, 27 December 2005 and 2 January 2006. Above- and below-ground parts of each plant were harvested separately on 13–14 January 2006. The number of shoots, the number of leaves on the main shoot and the presence or absence of the flag leaf on the main shoot were recorded. Shoots and roots of each plant were dried separately at 75 °C for 48 hours and weighed. In pots with two plants, every individual was recorded as larger or smaller than its competitor depending on its total dry weight.

statistical analysis

The list of hypotheses and critical comparisons that were used to test them are presented in Table 1. We used a general linear mixed model (except in testing hypothesis 2, see below) to test for the effects of pot partitioning (fixed factor with three levels: no partition, mesh partition and plastic partition), the addition of activated carbon to the substrate (fixed factor with two levels: activated carbon present or absent), size inequalities between individuals within a pot (fixed factor with two levels: smaller individual and larger individual) and interactions between these factors. Root, shoot and total dry mass of each individual were used as dependent variables. Pot, nested within treatment, was included in the model as a random factor to take into account the interdependence of the growth of two plants within a pot.

Hypothesis 2 was tested using one-way anova with treatment as a fixed factor and root, shoot and total mass, number of shoots and the number of leaves on the main shoot as dependent variables. Treatment ‘no carbon, no partition’ was included in the analysis for general comparison, although it was not needed to test this hypothesis. Average values per individual were used as response variables in treatments with two plants in a pot. A generalized linear model (binomial distribution and logit link function) was used to estimate the effect of treatment on the proportion of plants that had produced the flag leaf on the main shoot by the end of the experiment.

We used a one-way ancova to examine the effects of different treatments on biomass allocation between shoots and roots, with shoot mass as a dependent variable, treatment as a fixed factor and root mass as a covariate. Test of homogeneity of slopes revealed no differences in slopes between the treatments, satisfying an assumption of ancova. To equalize sample sizes in the treatment with only one plant in a pot (‘gravel’) and in the other treatments, average values were used in treatments with two plants in a pot. Means of shoot mass adjusted for the mean values of the covariate (root mass) were calculated to present differences in shoot/root mass allocation between treatments (see Steel & Torrie 1980; Sokal & Rohlf 1995 for details).

Dependent variables were ln-transformed before analysis when necessary to improve normality of residuals and homogeneity of variances.

Results

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

In treatments without carbon addition, plants attained similar root, shoot and total mass in pots without partitions and in pots with partitions (Fig. 2). The allocation pattern between roots and shoots was also very similar among these treatments (Fig. 3). Thus, given the amount of nutrients and substrate volume used in our experiment, no tragedy of the commons was observed: plants performed equally well in the presence and absence of root competition (hypothesis 1 supported).

image

Figure 2. Effects of pot partitioning and activated carbon addition on the root, shoot and total dry mass of individual plants. Error bars denote 95% confidence intervals for the mean. Different letters indicate significant differences between means (P < 0.05, Tukey test).

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image

Figure 3. Mean shoot mass after adjusting for the variation in the covariate means (root mass) over seven treatments in one-way ancova. This figure shows differences in shoot mass between different treatments that could not be attributed to corresponding differences in root mass, i.e. it reflects differences in the biomass allocation between shoots and roots in different treatments. Six treatments represented a combination of (i) pot partitioning (plastic or mesh partition, or no partition), and (ii) the addition or absence of activated carbon: NN = no carbon, no partition; NM = no carbon, mesh partition; NP = no carbon, plastic partition; CN = carbon, no partition; CM = carbon, mesh partition; CP = carbon, plastic partition. In treatment ‘G’ (gravel), half of the volume of substrate was replaced with gravel. Error bars denote 95% confidence intervals for the mean. Bar colours match those in Fig. 2, except for the treatment ‘gravel’. The effects of treatment and covariate were significant at P < 0.0001. Different letters indicate significant differences between means (P < 0.05, Tukey-Kramer test).

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Plants grown in substrate that was fragmented by gravel produced less shoot mass per unit of root mass, less total mass and fewer shoots, than plants grown in homogeneous substrate in the treatment ‘carbon, plastic partition’ (hypothesis 2 supported; Fig. 3, Table 2). The main shoots of plants in treatment ‘gravel’ developed further by the end of the experiment (as indicated by the number of leaves) than plants grown in homogeneous substrate (Table 2). Plants grown with a root competitor (‘no carbon, no partition’) exhibited intermediate morphology (Table 2). In addition, the proportion of plants that produced the flag leaf on the main shoot by the end of the experiment was 45% for plants grown in treatment ‘gravel’ compared with only 5% for plants grown in homogeneous substrate (treatment ‘carbon, plastic partition’) and 10% for plants grown with a root competitor (effect of treatment significant, P = 0.0094), indicating a faster switch to reproduction in the ‘gravel’ treatment.

Table 2.  Means for the number of shoots, the number of leaves on the main shoot, and root, shoot and total dry mass per individual in three different treatments. Standard errors are shown in parentheses. Means with the same letter are not significantly different (P > 0.05, Tukey test within one-way anova). Treatment ‘gravel’: single plants were grown in pots with one half of the pot volume replaced by gravel. Treatment ‘carbon, plastic partition’: two plants were grown in a pot with a plastic partition between them and activated carbon added to the substrate. Treatment ‘no carbon, no partition’: two plants were grown in a pot without a partition
TreatmentNo. shootsNo. leavesRoot mass (g)Shoot mass (g)Total mass (g)
Gravel1.5 (0.18) a5.9 (0.15) b0.149 (0.013) a0.269 (0.018) a0.419 (0.028) a
No carbon, no partition2.3 (0.18) b5.3 (0.15) ab0.189 (0.013) ab0.371 (0.021) b0.560 (0.032) b
Carbon, plastic partition3.2 (0.22) c5.2 (0.21) a0.229 (0.014) b0.493 (0.023) c0.722 (0.035) c

The addition of activated carbon to the substrate did not significantly change plant mass or allocation pattern between roots and shoots in the treatments without a partition (hypothesis 3 not supported; Figs 2 and 3). However, the performance of plants grown in pots with plastic or mesh partitions benefited considerably from the presence of activated carbon (hypothesis 4 supported; significant interaction between pot partitioning and the addition of activated carbon, Table 3, Fig. 2). Greater allocation to shoots was also observed in treatments with partitions and activated carbon (Fig. 3). Notably, when activated carbon was added to the substrate, plants in pots with plastic partitions performed significantly better than plants growing without a partition and having access to the whole volume of a pot (‘carbon, plastic partition’ vs. ‘carbon, no partition’; Fig. 2).

Table 3.  Results of general linear mixed models for the effects of treatment on root, shoot and total mass. The statistical significance of the effects of pot partitioning and the addition of activated carbon to the growth medium is presented. A factor denoting an individual as smaller or larger than its competitor within a pot (‘size category’) was included in the model to test for the effects of experimental treatment on the symmetry of competition. Pot was included in the models as a random factor (results not shown). Significant effects (P < 0.05) are shown in bold. d.f.: numerator, denominator
Effectd.f.Ln (root mass)Shoot massTotal mass
Carbon1,114 0.0274<0.0001<0.0001
Partition2,114 0.0374 0.0879 0.0727
Carbon × partition2,114 0.0277 0.022 0.0253
Size category1,114<0.0001<0.0001<0.0001
Size category × carbon1,114 0.4082 0.1734 0.1793
Size category × partition2,114 0.2563 0.5715 0.5085
Size category × carbon × partition2,114 0.1657 0.8347 0.7042

The absence of root contact between plants or resource movement between the two halves of a pot had a slightly positive but statistically insignificant effect on plant mass (treatments ‘carbon, mesh partition’ vs. ‘carbon, no partition’, and treatments ‘carbon, mesh partition’ vs. ‘carbon, plastic partition’, respectively; Fig. 2; hypotheses 5 and 6 not supported for mass). However, plants separated by a mesh partition exhibited greater allocation to shoots than plants grown without partitions (Fig. 3; hypothesis 5 supported for biomass allocation).

The size differences between the two plants in a pot were not affected by the presence of the roots of a competitor in a plant's rooting space (interactions between size category and treatments were not significant, Table 3). Thus, the symmetry of competition did not differ between treatments (hypothesis 7 not supported).

Discussion

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

In a comparison of the performance of plants grown in pots with and without partitions, we observed no tragedy of the commons (hypothesis 1 supported); there was no overproduction of roots or changes in overall growth and biomass allocation of plants in a treatment with root competition (‘no carbon, no partition’) compared with a treatment without root competition (‘no carbon, plastic partition’). However, additional treatments in our experiment showed that plant growth in the presence or absence of root competition could be affected by factors other than neighbour recognition, namely the restriction of root growth by partitioning of pots and differences in the distribution of available nutrients within a pot.

The treatments combining pot partitioning and the addition of activated carbon revealed a confounding effect of root self-inhibition in restricted rooting volume. The addition of activated carbon to pots without partitions did not change the mass of plants or the allocation pattern between roots and shoots, indicating that root exudates were not involved in the reactions of plants to the presence of competitors (hypothesis 3 not supported). However, the performance of plants grown in pots with plastic or mesh partitions was significantly greater when activated carbon was added to the substrate, despite there being no change in nutrient availability or substrate volume. This implies that space partitioning caused chemical inhibition of root growth that was alleviated by the addition of activated carbon to the rooting space (hypothesis 4 supported). Thus, effects attributed to the presence of competitors in previous studies (Gersani et al. 2001; Maina et al. 2002; Falik et al. 2003; O’Brien et al. 2005) may be confounded with the effect of reducing rooting space in control ‘no root competition’ treatments, which may cause self-inhibition of root growth. Schenk (2006) has also suggested that plants might respond not to the presence of competitors but to the soil volumes potentially available for rooting, which might affect the intensity of self-inhibition among roots.

The addition of activated carbon was also associated with effects on shoot growth and shoot/root allocation. Carmi & Heuer (1981) have shown that shoot growth of plants grown in small substrate volumes was regulated through changes in biosynthesis of hormones in roots, and that the reduction of plant growth in restricted rooting space was not caused by mineral or assimilate deficiency or water stress. However, they could not identify a specific stress that caused a reduction in hormone synthesis in root systems confined to smaller rooting volumes. Our results suggest that greater accumulation of self-inhibitory compounds in smaller rooting volumes may be involved in the regulation of overall plant growth.

Interestingly, when self-inhibition of root growth was removed by adding activated carbon to the substrate, plants in partitioned pots performed better than plants growing with a competitor and having free access to the competitor's rooting space (Fig. 2). Direct competition for limiting resources within intermingled root systems of competitors is thought to be energetically inefficient (Schenk et al. 1999). Reduced root system overlap between neighbours compared with that predicted from symmetrical root growth has been observed in a variety of species and is believed to increase the fitness of competitors (Mahall & Callaway 1992, 1996; Schenk et al. 1999; de Kroon et al. 2003). In our experiment, the absence of a partition between competitors allowed the possibility of overlap between the root systems of different plants. We suggest that the poorer growth in the treatment without a partition (‘carbon, no partition’) compared with partitioned treatments (‘carbon, mesh partition’ and ‘carbon, plastic partition’) could be caused by lack of a mechanism to detect and avoid overlap with the root system of a competitor. Due to the physical presence of a competitor's roots and depletion zones created by them, each plant should have experienced a more heterogeneous distribution of available resources than plants grown without root competition. Moreover, the roots of each plant would need to explore a greater volume of substrate to acquire the same amount of resources as in the partitioned treatments with more limited space. We attempted to simulate these effects in the treatment where substrate was highly fragmented by the addition of gravel. Significant differences in growth, development and biomass allocation were observed between plants grown in homogeneous substrate (‘carbon, plastic partition’) and plants grown in highly fragmented substrate where the same amount of nutrients was spread over the whole volume of a pot (‘gravel’; hypothesis 2 supported). Reduced shoot growth per unit of root mass in treatment ‘gravel’ (Fig. 3) suggested that the amount of nutrients acquired per unit of root mass might be lower in plants grown in the mixture of gravel and sand than in plants grown in homogeneous substrate. Similarly, McConnaughay & Bazzaz (1992) observed a significant reduction in growth of plants in soil fragmented by wire, even though the wire constituted only 2% of the total substrate volume. Self-inhibition of root growth close to gravel particles may also have contributed to changes in plant growth in the gravel treatment (Falik et al. 2005).

We attempted to examine the role of root exudates, physical contact and resource movement between root systems in communication that would lead to changes in plant growth and biomass allocation. We observed no significant effect of any of these factors on growth (hypotheses 3, 5 and 6 not supported). However, we could not eliminate root contact between different plants without also preventing overlap between their root systems (‘carbon, no partition’ vs. ‘carbon, mesh partition’). Thus, the effect of neighbour recognition via root contact could be confounded with the effect of overlap between root systems and inefficient foraging for nutrients in unpartitioned pots compared with partitioned pots.

The size differences between the two plants in a pot were not affected by whether or not their root systems could overlap and compete. Thus, symmetry of competition did not differ between treatments with and without root competition, and we were able to dismiss hypothesis 7 arising from the proposal of Laird & Aarssen (2005) that the tragedy of the commons can be a mathematical consequence of size-asymmetric competition. As in other studies on the tragedy of the commons, plants in all treatments experienced a similar level of above-ground competition. This was probably the main determinant of the degree of size-asymmetry independent of the presence or absence of root competition.

In conclusion, our results show that two distinct processes can be involved in the determination of root growth and plant performance in the experimental design used in this study: greater root self-inhibition in the more limited space of partitioned pots, and inefficient root placement in larger substrate volumes of unpartitioned pots that are shared with roots of a competitor. We suggest that the action of these processes may also explain some of the results of recent studies on root competition (Gersani et al. 2001; Maina et al. 2002; Falik et al. 2003; O’Brien et al. 2005). Our study does not show that the tragedy of the commons in root competition does not exist, but demonstrates that it is not the only possible explanation of the observed phenomenon. However, there are currently no studies demonstrating the proximate mechanisms involved in self/non-self root discrimination that leads to overproduction of roots (Falik et al. 2003; Gruntman & Novoplansky 2004), nor is there evidence to identify the selective pressures that would lead to the tragedy of the commons in root competition.

Acknowledgements

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

We gratefully acknowledge technical assistance from Martyn Stenning and statistical advice from Jaan Liira. This study was supported by the University of Sussex and a postgraduate studentship awarded to M.S. by Archimedes Foundation. The manuscript has greatly benefited from the constructive criticism of three anonymous referees.

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