Functional response of Quercus robur L. to taproot pruning: a 5-year case study

Effective forest management relies on high-quality seedlings that have a balanced root/shoot ratio. Various management practices in forest nurseries reduce the time required to produce seedlings and theoretically improve the ability of seedlings to cope with adverse environmental conditions (Duryea 1984). Consequently, most studies assessing the quality of seedlings used in reforestation programs have focused on either aboveground development or biomass allocation during the time period in which seedlings are grown in nurseries (Wilson and Jacobs 2006). The long-term consequences of nursery practices after seedlings are used in plantings have been overlooked.

Taproots are often pruned in forest nurseries, which mainly affects the root system but also indirectly influences shoot growth. The main response of seedlings to root pruning is the development of a dense and extensive root system, a compensatory mechanism that allows seedlings to acquire sufficient water and nutrients (Bréda et al. 2006). The ability of a plant to compensate for lost roots, however, largely depends on plant species (Peter and Lehmann 2000; Tsakaldimi and Ganatsas 2006). Other factors, such as planting density, can also affect seedling root systems (Moreno and Cubera 2008), and therefore, may also modify the effect of root pruning on water and nutrient uptake (Dong et al. 2016; Dumroese et al. 2013; Poni et al. 1992). A high stand density can contribute to the tree decline in Quercus spp. and other tree species by increasing competition for nutrients. Competition is especially enhanced on low nutrient soils (Kabrick et al. 2008). Greater competition can affect the allocation of resources to aboveground and belowground organs of seedlings (Duryea 1984; Grossnickle 2012). An increase in root number and root absorptive area due to root pruning, together with high planting densities, may result in greater competition for nutrients. The effects of root pruning and high planting densities on seedling allometry in a nursery, and on nutrient acquisition traits, however, are not well understood. It is not known if these factors have a long-term effect on specific plant organs or on whole tree growth. Determining the impact of root pruning and planting density on root traits are of particular importance because of the essential role the root plays in resource acquisition (Bonan 2008).

Plant growth is typically impacted more negatively by belowground competition than by aboveground competition (Wilson 1988; Jagodziński and Oleksyn 2009). Importantly, changing root system architecture by root pruning can alter the root/shoot ratio as well as nutrient acquisition (Clemens et al. 1999). Shifts in biomass allocation between shoots and roots (quantitative adjustment) (Enquist and Niklas 2002; Poorter et al. 2012; Shipley and Meziane 2002) enable plants to survive in resource-limited environments. Other strategies also minimize the negative effect of resource limitation. Morphological and biochemical alterations of functional traits (qualitative adjustments), such as specific leaf area (SLA) and specific root length (SRL), may also enable a plant to adapt to resource limitations (Freschet et al. 2010; Hill et al. 2006; Kerkhoff et al. 2006; Ryser and Eek 2000). Changes in root length may reduce the overlapping of roots among different plants (Valverde-Barrantes et al. 2013). Such changes, along with biomass partitioning, theoretically minimize the constraints of limited aboveground or belowground resources (Valladares et al. 2007; Van Kleunen and Fischer 2005). Poorter and Ryser (2015) suggested that organ biomass in plants is less plastic than organ morphology with respect to environmental constraints. Indeed, qualitative adjustments in SLA when light is restricted have been found to be a more effective adaptation than changes in the leaf mass fraction (LMF) (Curt et al. 2005; Freschet et al. 2013; Poorter et al. 2012). Important questions, however, still remain about the effect of management practices on root specific traits and biomass partitioning (Andersen et al. 2000; Riedacker and Poda 1977). Changes in nutrient availability have been found to affect SRL (Ostonen et al. 2007), but to a lesser extent than its effect on changes in root biomass allocation, i.e., the root mass fraction (RMF) (Freschet et al. 2013). Thus, leaves and roots exhibit contrasting patterns of adjustment (Poorter and Ryser 2015). Root competition affects the morphology of fine roots much more than biomass allocation (Curt et al. 2005), and therefore represents a long-term impact of various nursery practices. While the effects of root pruning and abiotic stresses (Dong et al. 2016) and competition between roots (Kong et al. 2016) have been studied in various tree species, the integrated responses of whole plants to management practices remain largely unknown.

Pedunculate oak (Quercus robur L.) is an economically important tree species that is widely distributed in Europe (Köble and Seufert 2001), although the future range of this species may change distinctly within the next 50 years (Dyderski et al. 2017). Poor tree survival in oak plantations has been frequently linked to restricted access to soil nutrients and the poor quality of seedlings grown in forest nurseries (Retana et al. 1999; Tsakaldimi et al. 2005; Valdecantos et al. 2006). Although root pruning is known to impact shoot growth under in vitro conditions (Harmer and Walder 1994), the effects of nursery management practices on root plasticity remain poorly understood. The effect of plant density and root pruning, however, are known to affect root system architecture and growth of red oak (Quercus rubra L.) and walnut (Juglans regia L.) (Schultz and Thompson 1990). A prior study on the capacity of the Q. robur root system to utilize soil water suggests that changes in root architecture might also have important effects on tree growth under field conditions (Zadworny et al. 2014). Despite the importance of seedling planting density and root pruning for subsequent growth, little is known about how the interaction between these factors induces alterations in biomass allocation; and consequently affects the morphology of roots and shoots in Q. robur seedlings after 1 year of growth.

The objective of the present study was to determine if taproot pruning and planting density affected the growth of Q. robur seedlings by biomass allocation and characterizing both root and shoot morphological traits in 2-, 4-, and 5-year-old seedlings. We hypothesized that (1) in response to taproot pruning, oak seedlings will allocate more resources to roots than shoots; (2) taproot pruning will modify root traits in order to optimize the acquisition of resources; (3) taproot-pruned seedlings will exhibit smaller phenotypic adjustments in LMF than in SLA; (4) RMF (a quantitative factor) will change more than SRL (a qualitative factor) in taproot pruned seedlings; and (5) tree density will affect leaf and root morphological parameters (SLA and SRL, respectively) rather than those associated with biomass allocation (LMF and RMF).

Plants alter their allocation of biomass to leaves or roots in order to reduce the effects of limited external resources (Enquist and Niklas 2002; Poorter et al. 2012; Shipley and Meziane 2002). Our initial hypothesis was that taproot pruning would increase root biomass in order to balance the acquisition of resources; however, the opposite trend was observed in the current study. Taproot pruning induced a gain in stem mass, and a lower relative root biomass. Considering the results of previous studies (Freschet et al. 2013; Poorter et al. 2012), the limited changes that were observed in SRL (which is related to resource acquisition) suggest that root morphology did not adjust to compensate for the decrease in the ability of the pruned root system to acquire nutrients. This was contrary to our expectations. The lack of a shift in biomass allocation or morphological adjustments, despite the decreased ability to acquire resources, may indicate that the limitation of nutrients was not strong enough to trigger a reaction. The higher increase in the aboveground parts of the plants, in comparison to the belowground root system, could have negative consequences for trees stability to wind storm when growing in more fertile forest stands, i.e., more frequent uprooting of taproot-pruned trees.

It is possible that the observed higher relative biomass of leaves and roots in 2-year-old seedlings, relative to older seedlings, may have been related to a phenomenon described by McConnaughay and Coleman (1999). These authors found that the biomass allocation strongly depends on plant ontogeny. We expected that greater biomass would be allocated to roots after root pruning in order to optimize the acquisition of aboveground and belowground resources. Instead, we found that root pruning decreased the relative root biomass, after the fifth season of growth, but not earlier. Given that total seedling mass at the end of the experiment was unaffected by the examined management practices, the higher relative biomass in stems in taproot-pruned seedlings than in the unpruned seedlings could reflect a strong selective growth characteristic in oak trees. In fact, well-developed stems are an attribute of the forest niche occupied by oak trees. Preferential increase of stem biomass at the expense of roots may also be advantageous when managing forests, especially since the fine root fraction remained unchanged across all of the experimental treatments. However, in our experiment, seedlings showed a temporal dynamics in the relative allocation of biomass. We assumed that after 4 years of growth, increased stem mass fraction associated with higher stem elongation at the expense of relative root mass allow shade intolerance oak seedling to compete for light, as competition for light strongly regulates light gathering, water and nutrient economy, and available for the growth carbon reserves (Gil-Pelegrín et al. 2018). Thus, steam elongation supports the production of carbohydrate reserves for the subsequent development of organs that limit the growth of, e.g., roots. The positive effect of taproot pruning on seedling growth might be particularly noticeable in fertile habitats where shallow root systems have optimal access to water and nutrients. The preferred increase of the stem biomass at the expense of the root system, however, was more pronounced at the lower density planting. At the higher density plantings, however, nutrient competition reduced this positive effect to some extent, which is most likely attributed to the effect of fine root biomass on plant productivity. Higher allocation of biomass to roots is considered to be a good predictor of successful stand development (Wu et al. 2004). The growth of different plant organs is limited equally by resources (Bloom et al. 1985) and the balance between root and stem growth depends on the availability of aboveground vs. belowground resources (Shipley and Meziane 2002, but see Reynolds and D’Antonio 1996). Q. robur, however, produces a deep root system that reaches into low levels of groundwater (Boratyński and Bugała 2000). Indeed, taproots make oak tree growth less dependent on surface soil layers that tend to dry out, and limit overexploitation of the resources present in a narrow soil profile (Cavender-Bares and Bazzaz 2000; Pierret et al. 2016). The inability of a tree species, such as Q. robur, to regenerate a pruned taproot (Ogijevskij and Popova 1954) may be essential for the optimal acquisition of nutrients and water [see Maeght et al. 2013 and literature cited therein]. Despite the response that occurred in our experimental system, a similar pattern of biomass partitioning might not occur under drought conditions or in less fertile soil, thus limiting the interpretation or extrapolation of the present findings.

No relationship was found between SLA and leaf biomass in our study. Indeed, leaf morphological adjustments rather than biomass partitioning (i.e., changes in SLA rather than LMF) could be caused by a plant responding to differences in light availability (Curt et al. 2005; Freschet et al. 2013; Freschet et al. 2015; Poorter et al. 2012). In agreement with this, SLA was higher when plants competed for light (i.e., at the high planting density) but LMF remained stable. Such adjustments might enable a plant to function properly by ensuring proper level of photosynthesis. Poorter et al. (2012) suggested that even marginal amounts of leaves, stem, and roots support plant growth. Moreover, exhibited by SSL higher than other parameters variation has important implications on a way oaks respond to higher density. A higher stem length per unit of stem biomass (i.e., a higher SSL) reflects accelerated stem elongation, which occurs to avoid shading by other plants in a low-light environment (Sasaki and Mori 1981). This alteration in SSL, therefore, may balance the aboveground acquisition of resources. When considering belowground relationships, quantitative adjustments in biomass allocation to roots have been found to be more important than qualitative adjustments (i.e., in SRL) in trees under nutrient stress (Freschet et al. 2015). This is in contrast to what has been reported for leaves (Poorter et al. 2012). Given that root biomass did not change to compensate for the lost taproot, however, we expected that generating roots with a high root length per unit biomass invested could be a strategy used to increase root absorptive surface in Q. robur. Limitations in nutrient availability should lead also to the domination of conservative root traits including low SRL (Freschet et al. 2010). SRL, which has been used as a surrogate of absorptive strategies, as a linear relationship is often expected between high SRL and enhance nutrient uptake, however, was similar in all of the treatments in our study. This apparent contradiction could have been a result of SRL being more variable than RMF among seedlings within the same group. Thus, we did not observe any pattern of root adjustment in our study. In fact, this was what was observed in all of the experimental treatments after the second and fourth growth seasons. Most likely, another explanation for the observed result comes from indirect competitive interactions involving other association that affect the way in which root traits are formed. Since Q. robur is an ectomycorrhizal species, it is plausible that colonization by different species of fungi, a parameter that was not monitored in our study, might also affect SRL (Ostonen et al. 2009; Sun et al. 2010). Since the association with ectomycorrhizal fungi occurs generally dependently of the trees density (Peay et al. 2011), mycorrhizal symbionts variability must translate into high SRL variation. Phenotypic plasticity (qualitative adjustment), however, is an adaptive response to environmental change (Freschet et al. 2013). Therefore, the additive or synergistic effects of taproot pruning and higher planting densities could make Q. robur seedlings more prone to unpredictable environmental changes than seedlings of other species (Dyderski et al. 2017).

Changes in the availability of resources, either aboveground or belowground, affect the equilibrium of biomass accumulation in roots and shoots, as well as organ morphology. Root pruning of oak seedlings increases stem biomass instead of an expected increase in root biomass. The presented results indicate that root pruning may benefit the production of oak timber and appears to be an advantageous for forestry practice. However, well-developed aboveground parts of Q. robur, with a simultaneous production of a more profuse system of shallow fine roots in response to taproot pruning root, may reduce the support and stability of mature trees, as has been shown in other tree species (Stofko and Kodrik 2008). This potential impact in oak needs to be further clarified. Given that maximum root depth is often established during the seedling stage (Hoffman and Lyr 1967), management practices which alter the structure of a root system may have irreversible, long-term effects on plant growth. In the present study, water was not limited and lack of fertilization may only result in a gradual limitation in nutrients. Thus, these abiotic factors may not have been strong enough in our study to impact the response of oak tree seedlings to root pruning. Whether or not our results also apply to tree stands with water and stronger nutrient limitations remain to be examined. This is especially important to consider since the demands of aerial portions of a plant for nutrients and water will not be met by a reduced root system. Given that anticipated changes in climate, particularly in water availability, will have striking effects on the environmental conditions to which plants are exposed (Dyderski et al. 2017), additional research should focus on determining whether or not root pruning exacerbates water and nutrient stress.