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- Materials and Methods
Deciduous trees recycle nitrogen from one plant tissue to another, facilitating the storage of N to be remobilized for new growth in the following year (Millard, 1996). This uncouples growth from current (external) N supply, and so enables growth to occur before mineralization makes external N available to the plant (Millard & Nielsen, 1989; Millard & Proe, 1992). In deciduous trees the main periods of N translocation are in the spring and during leaf senescence in the autumn. Nitrogen uptake during the growing period is used predominantly for new shoot and leaf growth, although uptake during leaf senescence can be allocated directly to storage (Weinbaum et al., 1984; Millard & Proe, 1991). During leaf senescence, N is withdrawn from the leaves (Thomas & Stoddart, 1980) and translocated to be stored in the roots, woody stem and bark during the dormant period (Gelrum, 1980; Nsimba-Lubaki & Peumans, 1986; Stepien et al., 1992; Millard et al., 2001). In the following spring, this stored N is remobilized for new leaf and shoot growth (Millard, 1996) and can contribute significantly to sapling growth and fitness (May & Killingbeck, 1992).
Nitrogen remobilization by silver birch is a source-driven process because the amount remobilized depends on the size of the storage pool and is unaffected by sink strength (Millard et al., 1998). However, while the effect of N availability on N remobilization in trees is well understood, other biotic and abiotic factors that may influence N uptake, withdrawal and remobilization are only partly understood.
Herbivory can influence internal N cycling through the removal of N, and thus a reduction in the amount of N available for storage (Millard et al., 2001). The effect is species-specific, and depends on the timing of herbivory because of the low N concentrations in browsed tissues during winter dormancy. Millard et al. (2001) found no effect of simulated mammalian browsing on the amount of N remobilized in Betula pendula saplings because the N storage sites are in tissues that remain unbrowsed. Moreover, fast-growing deciduous species such as B. pendula are generally able to compensate for the loss of tissue (and N) caused by herbivory (Hester et al., 2004, 2006).
Plant responses to competition may also be mediated by the effects on internal N cycling of interactions with other plants. Such interactions can influence all plant life-cycle stages, and can reduce resource availability and thus growth and development (Grace & Tilman, 1990; Tilman, 1997). Trees in temperate systems normally experience both intra- and interspecific competition, often resulting in growth inhibition (Berkowitz et al., 1995) and changes in morphology (Aphalo et al., 1999). It seems likely that interactions with other plants will also influence the pattern of internal nutrient cycling, because of the effects of resource limitation and the growth responses of the plant to competition. However, despite these factors being fundamentally important influences on plant development and growth in natural systems, the effects of competition on internal N cycling, and possible interactions with herbivory, have not been studied as far as we can ascertain.
In this experiment we measured the effects of competition (belowground or above- and belowground) and simulated herbivory on the internal N cycling of Betula pubescens saplings. Saplings were subjected to competition from either Molinia caerulea or Calluna vulgaris and simulated mammalian browsing at either bud-burst or pre-leaf senescence. Competition effects were separated to enable the relative contribution of above- and belowground processes to be quantified. Betula pubescens is a temperate deciduous tree; M. caerulea is a temperate deciduous grass; and C. vulgaris is an evergreen woody shrub. These three species are widespread throughout Europe and are found in many heath and woodland systems (Gimingham, 1960; Atkinson, 1992; Taylor et al., 2001). They often co-occur, and provide an interesting and ecologically important model system for studying plant interactions because of differences in their life-history traits. The aims of this study were to test the hypothesis that reductions in sapling size, caused by competition and herbivory, will reduce the sink strength for N during autumn nutrient withdrawal, and reduce N-storage capacity and hence the amount of N remobilized during the following spring. Specifically, this study aimed to determine whether reductions in B. pubescens sapling size, caused by competition with C. vulgaris or M. caerulea and simulated browsing, result in: (1) a reduction in leaf N withdrawal during senescence because of a reduction in the sink for withdrawn N; and/or (2) a reduction in the size of the potential N store and therefore in the amount of N remobilized in the spring.
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Nitrogen withdrawal during leaf senescence has been shown to be influenced by a number of factors, including summer temperature (Nordell & Karlsson, 1995), leaf N content and time of leaf senescence. However, we are not aware of any studies that have shown a difference in leaf N withdrawal caused by the effects of competition. Mineral nutrient transport in plants is highly dependent on source–sink relationships (Marschner, 1995). Nambiar & Fife (1991) found that shoot production (sink strength) was closely related to nutrient withdrawal from Pinus radiata needles. Furthermore, Chapin & Moilanen (1991) considered the rate of phloem transport (source–sink interactions) to be the most important factor controlling nutrient resorption efficiency in Betula papyrifera. We found close relationships between sapling size and N uptake and remobilization. Additionally, the effect of competition on N uptake, withdrawal and remobilization closely followed the effects of competition on sapling dry mass. Therefore it is likely that the differences in N withdrawal and remobilization were the result of the effect of competition on sapling size. In birch trees, N is stored in the roots, bark and old wood (Millard et al., 1998). A reduction in sapling size will also result in a reduction in the size of these tissues (Millard et al., 2001). Consequently, the sink strength in the autumn could be reduced, reducing the proportion of available N that is withdrawn from the leaves. Additionally, the source strength for remobilized N in spring will also be reduced, resulting in a reduction in the amount of N remobilized.
Nordell & Karlsson (1995) found that variation between individuals (genetic variation) was the largest source of variation in leaf N withdrawal of B. pubescens ssp. czerepanovii. However, in the present study it is differences in sapling size that account for most of the variation in N withdrawal and remobilization. These apparently conflicting results can be explained by the ontogenetic stages of birch studied. Nordell & Karlsson (1995) studied adult trees while we studied saplings. Furthermore, the trees that Nordell & Karlsson (1995) studied differed in height by a factor of c. 1.5, whereas the final dry mass of the trees that we studied differed by a factor of 10–14. It appears that in our study the size of saplings was more important in determining leaf N withdrawal because of the relatively large variation in sapling dry mass.
Effects of competition
The reduction in growth and N uptake was caused by a negative effect of belowground interactions. This indicates that acquisition of N by competing plants reduced N availability for the saplings. Weih & Karlsson (1999) found that intraspecific competition reduced N concentration, productivity and uptake in B. pubescens ssp. czerepanovii. However, this effect was caused by a reduction in soil temperature and N uptake caused by aboveground competition. These differing results suggest that competitive effects on N uptake are dependent on a number of factors, the importance of which depends on the specific situation, including species, temperature and soil N availability. Furthermore, in the present study M. caerulea shoots increased growth and N uptake. Facilitation is a well documented (although apparently less common) result of plant interactions (Callaway & Walker, 1997; Callaway et al., 2002; Bruno et al., 2003). Aboveground facilitative interactions can be attributed to reducing temperature, water or nutrient stress (Callaway, 1995; Bruno et al., 2003). However, the mechanism in the present study is not clear and could conceivably be attributed to any one, or any combination of these.
The efficiency of N withdrawal from leaves before abscission can be defined in terms of the percentage of N removed (withdrawal efficiency), or the final level to which the plant is able to decrease leaf N (withdrawal proficiency) (Killingbeck, 1996). Withdrawal efficiency is highly dependent on the N content of leaves pre-senescence, whereas withdrawal proficiency is a measure of the ultimate ability of the plant to withdraw N. We found similar patterns in both withdrawal efficiency and proficiency. Saplings growing in M. caerulea or with no competition had both a greater N resorption efficiency and proficiency than those growing with C. vulgaris (they withdrew a greater proportion of leaf N and decreased the N content of abscised leaves to a greater extent). Killingbeck (1996) considered that woody perennials could potentially reduce the N concentration of abscised leaves to 0.3% (potential resorption proficiency). Chapin & Kedrowski (1983); Chapin & Moilanen (1991); and Escudero et al. (1992) measured the resorption potential of birch to be 0.50, 0.88 and 0.65%, respectively. The range of N concentrations in abscised leaves in our study was 0.78–2.79%. This suggests that some saplings achieved close to their ultimate resorption potential, while others achieved considerably below their potential. The efficiency of N withdrawal was also lower than may be expected for woody perennials (Aerts, 1996). Additionally, in a review of 60 studies Aerts (1996) found little evidence that N-resorption efficiency was related to N availability or leaf N content. It seems likely that, in the present study, differences in sapling size caused by the effects of competition, and therefore source–sink interactions, are the main driving mechanism determining N withdrawal and remobilization.
Nitrogen remobilization in the spring has been shown to be dependent on the amount of N in store (source strength). For example, Dyckmans & Flessa (2001) found that the amount of N remobilized for leaf growth in Fagus sylvatica saplings was strongly influenced by the previous year's N supply. Additionally, Millard & Proe (1992) showed that N remobilization in Acer pseudoplatinus was dependent on the previous year's N supply, and therefore the amount of N in store, and independent of the current year's N supply. Larger saplings will have a larger capacity for N storage. We conclude from this that the effect of competition on N remobilization was caused by the effects of competition on sapling size, and thus their ability to store N.
Effects of browsing
Fast-growing species are generally able to compensate for tissue loss caused by herbivory (Millard et al., 2001). Moderate levels of simulated browsing (50% of shoots) have also been shown to have little effect on N remobilization in B. pubescens (Millard et al., 2001). Additionally, Karlsson & Weih (2003) found that mature B. pubescens ssp. czerepanovii trees were able to compensate for severe defoliation within 2 yr of damage. In this study, we also found little effect of simulated browsing on sapling dry mass one growing season after the damage occurred. Furthermore, there was no significant effect of browsing on N uptake, withdrawal or remobilization. This corresponds with the response of B. pendula saplings (Millard et al., 2001), and is likely to be caused by the main storage tissues remaining undamaged. However, a delayed negative response to browsing cannot be ruled out. Weih (2000) found that B. pubescens ssp. czerepanovii seedlings exhibited a response to various environmental variables that was delayed until two seasons after treatments were imposed. The compensation for damage that the saplings in our study exhibited could potentially reduce their fitness for following growing seasons.
It has been suggested that the ability of plants to compete would be reduced by herbivory, but there was no evidence of this under the moderate levels of browsing applied in this study. This result concurs with that of Karlsson et al. (2005), who found no interaction between competition and herbivory in B. pubescens ssp. czerepanovii. We believe that these results are caused by the ability of birch saplings to compensate for such damage, with no further negative effect on their competitive ability.