Structural Adaptations for Overcoming Light Limitation
3.2 Effect of growth properties under carbohydrate restriction
The data generated by the 4-factorial design of treatment combinations is presented in Table 7.1. Three treatments were unable to overcome photosynthetic limitation during early spring, namely the control simulation, the simulation with only the etiolation property added to growth and the simulation with only the non-linear blade mass growth added to growth.
All other simulations survived through to the completion of floral growth and natural senescence but with different levels of success, as demonstrated by the maximum live masses achieved. This included the two simulations with only increased proportional winter root live mass and surviving live photosynthetic surface respectively, but growth in both of these simulations was extremely poor, indicating that the plants were severely limited by photosynthetic production.
Simulations in which two of the properties were included improved growth substantially, except for the combination of non-linear blade mass growth and increased proportional winter root live mass. This indicates that etiolation and surviving live photosynthetic surface each provided a greater benefit in combination with other properties, and together provided sufficient benefit to completely overcome resource restriction. All other 2-property strategies experienced substantial growth restriction caused by carbohydrate limitation, indicated both by poor growth and greater shoot growth than root growth.
Table 7.1 Maximum live masses achieved in the second spring by simulated single- tiller ramets in a 4-factorial experiment with etiolation (E), non-linear blade mass growth (B), greater proportional winter root mass (R), and surviving residual live photosynthetic surface (L)
Treatment Variable Blade mass (g) Shoot mass (g) Root mass (g)
Non-restricted values
Control E B R L E+B E+R B+R L+E L+B L+R E+B+R L+E+B L+E+R L+B+R L+E+B+R
0.115 (E: 0.199)*
0.007 0.009 0.007 0.025 0.045 0.098 0.058 0.021 0.184 0.040 0.055 0.152 0.162 0.188 0.058 0.165
0.659 (E: 0.881)
0 0 0 0.150 0.243 0.700 0.289 0.160 0.848 0.269 0.301 0.791 0.828 0.891 0.406 0.857
0.756 (E: 1.003)
0 0 0 0.075 0.124 0.564 0.123 0.074 0.966 0.155 0.168 0.900 0.943 0.988 0.274 0.950
• maximum live mass achieved with etiolation
Simulations that combined three properties included were all capable of substantial growth in spring, except the treatment without etiolation (L+B+R), indicating that etiolation played the most substantial role in spring regrowth, but that it required at least one of the other properties to increase the temporal growth efficiency during early spring regrowth. The simulation in which surviving live photosynthetic surface was excluded (E+B+R), also grew substantially. This indicates that single-tiller ramets were able to overcome carbohydrate limitation in spring with the combination of the three growth properties in the absence of surviving live photosynthetic surface. However it is important to note that this E+B+R combined strategy was subject to carbohydrate limitation throughout the period of blade expansion in the second spring (Figure 7.5).
Only the E+B+R+L combined strategy was not restricted by carbohydrate limitation during this period (Figure 7.5). Therefore it is clear that maintaining some photosynthetic surface through winter has a strong positive effect on net carbohydrate balance.
4 DISCUSSION
The combined evidence indicates that bunchgrass ramets with little or no live photosynthetic material can regrow new photosynthetic surface sufficiently to overcome light limitation in closed swards, even though their potential to store carbohydrate reserves is fairly restricted. They do this through a series of complementary structural properties.
The simulations demonstrated that tillers could overcome resource depletion without surviving residual photosynthetic surface, and that the most important property was etiolation, confirming a large body of empirical evidence linking this property to light foraging (Hutchings & de Kroon 1994). However, etiolation on its own was not sufficient to overcome the resource limits. Combining sigmoidal blade mass growth with etiolation was an effective strategy because the non-linear increase in blade mass with extension improved temporal resource-use efficiency by allowing the tiller to reach higher into the canopy for a lower nutrient cost. These properties combined with disproportionate resource allocation between roots and shoots allowed single-tiller ramets to overcome light restriction sufficiently to avoid death, indicating that temporal resource-use efficiency is a probable strategy employed by bunchgrasses to avoid death in moribund swards. Leaf etiolation and non-linear blade mass growth combined with disproportionate allocation between roots and shoots were, however, not sufficient to overcome light limitation during the second growing
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Figure 7.5 Comparison of carbohydrate retained in the AVC at the end of each iteration for the simulated single-tiller ramet that did not maintain live photosynthetic surface through winter, E+B+R (a), and that which did retain live photosynthetic material through winter, E+B+R+L (b).
(Environmental conditions: Plant activity during the growing and non-growing season as defined in Section 4.3 of Chapter 4. Growing season proceeds from Yearday 1 to Yearday 242 of each year. Soil nitrogen is not limiting to growth.)
season, and consequently growth was still substantially reduced in the absence of the other considered structural adaptations.
The importance of sigmoidal blade mass growth to temporal resource-use efficiency during light foraging does not appear to have been considered previously. There is evidence that etiolated blades have a lower mass-to-area ratio than non-etiolated blades (Givnish
1988; Mojzes, Kalapos & Viragh 2003), suggesting that etiolation does itself lead to greater resource-use efficiency through changes in leaf allometry. This property was ignored for the present study because there is no clear data on how etiolation affects the mass-to length ratio of bunchgrass leaves, nor any corroborative data on whether comparable leaves grown in sun and shade have the same net mass, in which case changes in leaf allometry would certainly increase resource efficiency. To the contrary, there is evidence of increased allocation to leaves relative to other shoot organs under shaded conditions (e.g. Rice &
Bazzaz 1989), which suggests that leaves on shaded plants are heavier than light-grown plants. Given the length and upright growth of leaves of bunchgrasses, it is improbable that bunchgrasses could afford the loss of tensile strength in individual leaves growing through closed swards that would result from a change in the mass-to-length ratio. This suggests that sigmoidal blade mass growth, although only a temporal effect, provides a real benefit to bunchgrass tillers growing through closed canopies.
The temporal resource efficiency demonstrated here arises from the combined effects of structural adaptations and disproportionate resource allocation. The combined effects were demonstrable because the TILLERTREE model considers both bunchgrass architecture (phytomer object arrangement and growth) and resource allocation explicitly.
Most previous models have been unable to consider these interactions because either they concentrated on disproportionate resource allocation and did not consider structure sufficiently explicitly (e.g. Reynolds & Chen 1996; Herben & Suzuki 2002), or they considered structure explicitly and avoided resource allocation (e.g. Prusinkiewicz &
Lindenmayer 1990).
The combined evidence indicates that Themeda triandra plants are carbohydrate- limited during spring regrowth even if they maintain some live photosynthetic material over the non-growing period, and only the simulation which included all four structural adaptations (etiolation, non-linear blade mass growth, increased root mass survival, and survival of residual live photosynthetic surface) overcame carbohydrate limitation during spring regrowth (Figure 7.5). That said, survival of live photosynthetic material over winter did improve the growth response. These results have significance for the seasonal growth of
bunchgrasses, as they suggest that seasonal growth in non-defoliated bunchgrass swards will depend strongly on the amount of live photosynthetic surface maintained over the previous non-growing season. If the amount is small, then carbohydrate limitation will be severe and initial regrowth will be slow, while if it is large then carbohydrate limitation will be less restrictive and initial regrowth will be more rapid. This in turn will affect the bunchgrass swards' ability to capture soil nitrogen, which is greatest at the beginning of the growing season in humid grassland communities (Blair et al. 1998), which will affect the subsequent growth potential of the bunchgrasses, as nitrogen is the most limiting nutrient to growth. Environmental conditions that might cause substantial desiccation of live photosynthetic surface include frost and severe drought (Walters et al. 2002). In environments subjected to varying degrees of winter frost, such as the Southern Tall Grassveld (Acocks 1953), this means that growth in non-defoliated swards in any given growing season could be dependent on the severity of frost in the previous winter, which would determine the amount of surviving residual biomass. Thus seasonal productivity is temporally dependent on events that occur prior to the season and productivity cannot be estimated from within-season rainfall alone.
The simulations indicate that there would certainly be a benefit from increased root survival through winter because additional carbohydrate can be assigned to shoot growth in spring both from storage and root dieback, even if the concept of root dieback during spring seems unlikely as a growth strategy. One trade-off of such a strategy would be the reduction in nitrogen absorbed while resources are allocated to shoot growth. This might prove too expensive in a humid grassland community where nitrogen is very restrictive to potential growth across the entire season (Knapp et al. 1998) even if it is non-limiting during spring (Bausenwein et al. 2001, Lamaze et al. 2003). It may be that root dieback occurs on some structures while other roots start to grow during spring. The model is unable to assess this effect presently because it treats roots as an amorphous mass.
The benefit given by greater root survival through winter indicates that increased biomass survival over winter increases the subsequent spring growth of bunchgrasses because more resources are available for early spring regrowth, which increases the ability to capture soil nitrogen in spring and therefore promotes seasonal growth. This provides a probable explanation for the noted positive relationship between biomass production in a given year and biomass production in the next year (O'Connor, Haines & Snyman 2001):
greater biomass accumulation in the present year will increase biomass survival over the
subsequent winter, thereby increasing resource availability for growth in the subsequent growing season.
The simulations indicate that bunchgrasses overcome light limitation at the start of spring through maximum allocation to the first emerging blade. This indicates that properties of phytomer growth in early spring and phytomer survival through winter are critical to the behaviour. These properties are understudied. Of interest here is the growth and dieback of leaf blades during unfavourable growth periods. Critically, assuming that dormancy in C4 grasses is imposed by environmental conditions, what are the effects of unfavourable growth periods on phytomer development? Do these periods induce growth phase change (e.g. induction of the plateau phase)? Do unexpanded phytomer numbers accumulate during these periods? The latter would cause simultaneous growth of multiple blades when conditions for growth become favourable once again, which might place additional stress on regrowth during spring.
The present chapter considers the growth of a single-tiller ramet only. Once secondary tiller recruitment is incorporated, the demand for resources will increase and the increased growth will further reduce photosynthetic efficiency as the LAI increases. This effect is described in Chapter 8, and it is demonstrated that multi-tiller growth further compromises the total growth of individual reproductive tillers.
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