Edited by: Massimiliano Tattini, Italian National Research Council (CNR), Italy
Reviewed by: Alessio Fini, University of Milan, Italy; Lucia Guidi, University of Pisa, Italy
This article was submitted to Functional Plant Ecology, a section of the journal Frontiers in Plant Science
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Current niche models cannot explain multi-species plant coexistence in complex ecosystems. One overlooked explanatory factor is within-growing season temporal dynamism of resource capture by plants. However, the timing and rate of resource capture are themselves likely to be mediated by plant-plant competition. This study used Barley (
Niche differentiation is suggested to lead to coexistence of plants by reducing competition, either for a specific form of a resource or simultaneous demand for the same resource (
One factor which is often not included in niche models is time, more specifically the temporal dynamism of key developmental and physiological processes such as resource capture (
As well as temporal dynamism influencing competition, competition can influence the temporal dynamics of resource capture, although the extent to which these processes affect each other is unclear. As there are many aspects of temporal dynamism in plant communities that are not fully understood, temporal dynamism in resource capture may be currently unsuitable as an indicator of plant-plant competition. However, a change in the temporal dynamics of resource capture may be a wider consequence of competition or a mechanism by which plants avoid direct competition for resources.
There is in particular a lack of information on the relationship between temporal dynamism and intra-specific competition, and how the degree of relatedness of competitors might influence temporal dynamism. The genetic distance between competing individuals can influence the functional plasticity of an individual response to competition (
Here, we conducted a pot experiment with Barley (
It is expected that early and late cultivars of barley will have different temporal dynamics of nitrogen uptake and biomass accumulation, in a similar way to two species or genotypes in a natural system. The two cultivars in this study have been bred for different uses and therefore will have differing combinations of traits. Tammi has been bred for an early lifecycle (
This study aimed to understand: (1) whether early and late cultivars of barley exhibit temporal dynamics in nitrogen uptake and biomass, (2) how plant-plant competition changes the temporal dynamics of nitrogen and biomass accumulation in early and late barley cultivars, (3) how any temporally dynamic response differs with inter- and intra- cultivar competition, and ultimately (4) how this impacts on niche complementarity.
A pot-based competition study was used to investigate temporal dynamism in nitrogen uptake, using barley (
Soil was sourced from an agricultural field (Balruddery Farm, Invergowrie, United Kingdom) that had previously contained spring barley (
Seeds of both cultivars were pre-germinated in the dark on damp paper towels and planted into cylindrical 2 L pots (diameter 152 mm, height 135 mm) with five replicate pots of each of the five treatments for each planned harvest (11 harvests in total), giving a total of 275 pots. The pots were randomized to account for potential positional effects and grown in controlled environment rooms (Conviron, Isleham, United Kingdom) at a constant 15°C with an 8/16 (day/night) hour photoperiod (irradiance of 100–150 μmol m-2 s-1) and 65% relative humidity, to mimic local spring-time conditions. The pots were watered twice weekly and the soil was kept moist to avoid competition for water. Mesh screens [45 cm × 16 cm, mesh size 0.08 mm (Harrod Horticulture, Lowestoft, United Kingdom)] were inserted in those pots containing two plants to separate the plants above ground, and ensure competitive interactions only occurred below ground. Foliage was relatively upright without support and the presence of a screen – although important in ensuring above-ground competition was minimized – was unlikely to have resulted in differences in shoot development in pots with two plants compared to one.
Five randomly selected pots of each treatment were harvested every 5 days until ear formation (when grain begins to form) was observed on the early Tammi cultivar (60 days). During this period both cultivars produced flag leaves, the stage prior to grain production, when most nitrogen has already been absorbed (
To analyze temporal changes in biomass and nitrogen accumulation, the rate of each was modeled with logistic growth curves using non-linear least squares (nls) models (
C:N ratio at the final harvest (65 days after planting) was analyzed using an ANOVA test from the MASS package
The effect of a neighboring plant on a target plant’s biomass was quantified using the Relative Intensity Index (RII; Eq. 1), an index that accounts for both competitive and facilitative interactions between neighboring plants (
The land equivalent ratio (LER; Eq. 2) was used to determine if the inter-cultivar mixture (TP) overyielded when compared to intra-cultivar competition (TT or PP) (
Nitrogen (
Timing of peak nitrogen
Nitrogen uptake for both cultivars followed similar temporal dynamics, increasing until 45 days after planting, then plateauing (
Mean cumulative nitrogen
Proctor’s absolute maximum shoot nitrogen concentration was significantly lower when in competition with Tammi or Proctor compared to isolation (
Biomass accumulation increased throughout the growing period with a lag period until 31 days after planting and then rapidly increased during the remainder of the experiment (
For both Tammi and Proctor, absolute maximum accumulated biomass was significantly lower when in competition compared to isolation (
Proctor in isolation had a C:N ratio of about half that of Tammi in isolation throughout the experiment, i.e., more nitrogen relative to carbon. However, for neither cultivar were there significant differences in C:N ratio between plants in isolation compared to plants in competition at the end of the experiment [Proctor (
The significantly negative RII of final biomass indicated competitive interactions for both cultivars irrespective of whether they were in inter- or intra- cultivar mixtures. RII values also showed that Tammi and Proctor experienced a greater intensity of competition when in inter-cultivar compared to intra-cultivar competition (
Mean relative intensity index of barley (
The LER value for Tammi and Proctor in competition was 2.05 (±0.35 SE), indicating that the inter-cultivar mixture had a greater total biomass (root and shoot) than would be expected from the intra-cultivar mixtures.
This experiment aimed to detect and quantify temporal dynamism in nitrogen uptake and biomass accumulation in two barley cultivars and determine responses to inter- and intra- cultivar competition.
We found that competition significantly reduced maximum accumulated biomass and shoot nitrogen in both cultivars. Neither intra- or inter-cultivar competition impacted the timing of peak biomass accumulation in either cultivar. However, intra-cultivar competition significantly delayed peak nitrogen accumulation rate by 14.5 days in Proctor and advanced it in Tammi by 0.5 days. Relative Intensity Index values indicated that both cultivars experienced competition, with no significant difference in intensity between intra- and inter- cultivar competition. However, a positive LER value indicated that the inter-cultivar mixture overyielded when compared to the intra-cultivar mixtures.
Neither of the cultivars in this study significantly altered the temporal dynamics of peak biomass accumulation in response to a competitor. The mismatch between biomass and nitrogen accumulation dynamics in response to competition indicates biomass may not effectively measure the temporal dynamics of within-growing season resource capture, an issue previously raised by
Tammi and Proctor only demonstrated significant changes in temporal dynamism of nitrogen accumulation when in intra-cultivar competition. Tammi advanced peak accumulation rate by 0.5 days and Proctor delayed it by 14.5 days. As this only occurred in intra-cultivar competition, it suggests that this is more complex than a competition avoidance response based on a source-sink (soil – plant) relationship. If this was a simple source-sink relationship, for example, based on soil nitrogen availability (
Kin recognition has been suggested as a mechanism by which plants alter functional traits when in competition with closely related individuals (
The results of this study contrast with those of a temporal dynamism study by
In our study Proctor was the less competitive of the two cultivars, as it experienced a greater decrease in nitrogen and biomass accumulation when in competition compared to Tammi. This contrasts with the
The processes of nitrogen and biomass accumulation were temporally distinct for both cultivars. The peak rate of nitrogen accumulation was 29.0–29.5 days before peak biomass accumulation for Tammi and 16.5–27.5 days for Proctor (
Barley has been found to have temporally distinct nitrogen and biomass accumulation with a 23–24 day gap between peak nitrogen and biomass accumulation in field studies (
Competition significantly reduced the final maximum nitrogen concentration and biomass that both Proctor and Tammi were able to accumulate in intra- or inter-cultivar competition. A Proctor competitor caused a significant decrease in Tammi maximum biomass accumulation and nitrogen shoot concentration, despite not achieving the greatest biomass above or below ground. This suggests that another factor influenced the rate of nitrogen uptake. Signaling through root volatile compounds or root exudates has been found in a number of species including legumes and grasses (
The two cultivars differed in their C:N ratio by the end of the experiment. This is likely due to the earlier cultivar Tammi being more advanced developmentally than Proctor. By the end of the experiment, Tammi had begun grain production, whereas Proctor had produced a flag leaf, the stage before grain formation. However, there was no significant increase in C:N in either cultivar in response to competition. Due to selective breeding for a specific seed C:N (grain nitrogen content) with known mapped genes (
The negative RII indicated both cultivars experienced competition when grown with a neighboring plant, but no significant difference depending on the identity of the competitor. This contrasts with the positive LER value which indicated overyielding of the two cultivars when grown in inter-cultivar competition compared to intra-cultivar competition. The reason for this is unclear and may be due to the timing of the final harvest, before both cultivars had set seed. This highlights the difficulty of using multiple metrics to measure the outcome of competition, especially as the measurements were only taken at the end of the experiment, i.e., at a single timepoint. Therefore, single timepoint competition indices should be used with caution when examining the consequences of temporal dynamism of resource capture.
There is a need to understand the extent to which a species or genotype is temporally dynamic and the factors that lead to temporal dynamism in resource capture. This will allow temporal dynamism in resource capture to be included in models of coexistence, furthering our understanding of coexistence in complex plant communities.
This study demonstrates how a previously overlooked factor in plant community coexistence, within-growing season temporal dynamism of resource capture, can be measured through successive harvesting and the novel application of commonly used statistical approaches. Only peak nitrogen accumulation rate was temporally dynamic in response to competition, not biomass peak accumulation rate or shoot C:N. Therefore, we suggest that to understand the temporal dynamics of resource capture within a growing season, direct measures of mineral resources accumulated (e.g., nitrogen uptake) are important to understand the mechanisms of temporally dynamic responses to competition. By measuring shoot nitrogen accumulation rate over time, intra-cultivar competition was found to advance peak nitrogen accumulation rate in Tammi and delay it in Proctor. This suggests that temporally dynamic nitrogen uptake responses are greater in intra-cultivar competition and may be due to kin recognition. This may be mediated through root exudates and the soil microbial community, an area that requires further investigation and extension to semi-natural and natural ecosystems. Ultimately understanding the role of temporal dynamism in plant communities will lead to improved niche models of coexistence in plant communities.
The datasets generated for this study can be found in the Dryad Digital Repository.
ES, RB, JR, EP, FQB, and EACP conceived the experimental design. ES collected the data. RB, MB, JR, and ES analyzed the data. All authors wrote and/or edited the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We would like to thank Adrian Newton for his advice about the traits of the barley cultivars used in this study.
The Supplementary Material for this article can be found online at: