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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).
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
|1||When 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|
|2||Fragmentation 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|
|3||Plants 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’*|| |
|4||Partitioning 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*|| |
|5||Physical 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|
|6||Resource 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|
|7||Plants grown with root competition exhibit greater size inequality than plants grown without root competition||The 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|
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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).
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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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
|Treatment||No. shoots||No. leaves||Root mass (g)||Shoot mass (g)||Total mass (g)|
|Gravel||1.5 (0.18) a||5.9 (0.15) b||0.149 (0.013) a||0.269 (0.018) a||0.419 (0.028) a|
|No carbon, no partition||2.3 (0.18) b||5.3 (0.15) ab||0.189 (0.013) ab||0.371 (0.021) b||0.560 (0.032) b|
|Carbon, plastic partition||3.2 (0.22) c||5.2 (0.21) a||0.229 (0.014) b||0.493 (0.023) c||0.722 (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
|Effect||d.f.||Ln (root mass)||Shoot mass||Total mass|
|Partition||2,114|| 0.0374|| 0.0879|| 0.0727|
|Carbon × partition||2,114|| 0.0277|| 0.022|| 0.0253|
|Size category × carbon||1,114|| 0.4082|| 0.1734|| 0.1793|
|Size category × partition||2,114|| 0.2563|| 0.5715|| 0.5085|
|Size category × carbon × partition||2,114|| 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).
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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.