Nitrogen uptake, partitioning and internal ... - Wiley Online Library

New

Phytol.

(1993), 125, 113-119

Nitrogen uptake, partitioning and internal cycling in Picea sitchensis (Bong.) Carr. as influenced by nitrogen supply PROE The Macattlay Land Use Research Institute, Craigiebuckler, Aberdeen AB9 2QJ, UK {Received 6 January 1993; accepted 12 April 1993) BY P. M I L L A R D * AND M. F.

SUMMARY

Four-year-old seedlings ol Ptcea sttclteiisis (Bong,) Carr, were grown in sand culture throughout 1989 and irrigated witb nutrient solutions containing either 1-0 mol N m^'' (Low N) or 6-0 mol N m"'' (High N), to precondition their growth and capacity for N storage. During 1990 N enriched with '^N was stipplied, either from 15 March to 27 June, or 28 June to 20 November, Recovery of unlabelled N was used to determine the storage and remobilization of N for foliage growth, and the partitioning of labelled N taken up during the two periods was tneasured. Initial growtb of trees in 1990 was unaffected by the current N supply and detertiiined only by the N supplied the previous year. High N throughout increased the number of needles grown in 1990 compared to low N-treated trees, but bad little effect on the dry weight of individual needles. When preconditioned with High N, trees responded to Low N in 1990 by a reduction in needle dry weight, without altering the number of needles produced. Low N trees supplied with High N in 1990 responded by increasing both needle tiumbers and dry weigbt, compared with trees supplied with Low N throughout, Tbe amount of unlabelled N remobilized to foliage growtb in 1990 was unaffected by the current N supply but t-eflected the atnount of N iti store, as determined by tbe N supply the previous year. The majority of N was remobilized from the 1989 foliage and none from roots. Partitioning ot labelled N taken up during 1990 altered during the year, with a greater proportion of N taken up after 28 June recovered in the roots in all treatments, due to root growth as opposed to allocation of N to storage during the autumn, since root N concentrations fell betw-een 17 June and the final har\-est on 20 November. Key words: Picea sttrlteiisis (Sitka spruee), internal c\-eling, nitrogen uptake, seasonal growth, niti-ogen supply.

INTRODUCTION T b e Storage atid seasonal intertial cycling of nitrogen (N) bas been sbovvn to be importatit for tbe sustainable growtb of evergreen trees (Miller et al., 1979; Rapp, Leclerc & Lossaint, 1979; Millaid & Proe, 1992). In conifers, N is stored duritig tbe winter in needles and remobilized in tbe spring duritig tbe growtb of new foliage, as sbowti by N budget studies (Turner, 1977; Ericsson et al., 1985, Nambiar & Fife, 1987; Heltnisaari, 1992a, b) and tbe use of ""N to quantify internal cycling directly (Millat-d & Pioe, 1992), Nitrogen budget studies bave sbowti tbat enbanced site fertility increases tbe capacity for ititertial cycling (Miller et al., 1979), tbrougb increasing needle mass atid so tbe capacity for N storage (Nambiar & Eife, 1987; Heltnisaari, 1992«), Eew studies bave considered tbe impact of nutrient supply oti tbe efficieticy of tbe processes of internal cyclitig. We found tbat tbe spring N supply bas tio

effect Oti tbe amount of N remobilized for tbe growtb of new foliage in P. sitchensis (Millard & Proe, 1992). However, we did not determine tbe effects of N supply oti tbe efficieticy of ititertial cyclitig, because all tbe trees studied bad been preconditioned with tbe satne N stipply and so bad a sitnilar amount of N iti store at tbe start of tbe experinietit. In tbe presetit study, we grew P. sitchensis witb eitber a poor or getierous N supply, to precotidition growtb and capacity for N storage during tbe wititer. Tlirougliout tbe second year trees frotn botb N treattnents were given eitber a generous or poor N supply, labelled witb '"'N in eitber tbe spritig or summer and autumn. Recovery of tbe ' ' N was used to detertiiine if tbe capacity for remobilizatioti of N in tbe spring was preconditioned by tbe size of tbe N store or depetidetit upon tbe spritig N supply, and if tbe partitiotiing of N taken up duritig tbe year cbanges to allow autumn N uptake to contribute directly to storage over tbe winter.

* To whom correspondence should be addressed. A N l ' 125

114

.--

P. Millard atid M. F. Proe

100

a. S

I

15 Mar.

20 23 27 1 Apr. May June Aug.

13 Sept.

20 Nov.

Figure 1. The effect of N supply on the d. wt of trees during 1990. The symbols represent High N/HiRh N (Q), High N/Low N (O), Low N/High N (A) atid Low N/Low N (O) and are the mean and si; of 10 replicates for the first harvest and 5 subsequently. M A T E H I A L S A N D M li T H O D S

Four-year-old seedlings of Picea sitchensis (Bong.) Carr. were planted on 15 March 1989 in fine sand in pots 60 cm in diameter and 45 cm deep. Trees were watered to field capacity every second day with a nutrient solution containing either ] - O m o l N m *' (Low N) or 6-0 mol N m"'' (High N) as NH.NO.,. Other nutrients supplied were as described by Millard & Proe (1991). Plants were arranged in a greenhouse to give five replicate blocks with 32 trees in each. During the winter the greenhouse was kept frost-free and the frecûency of watering reduced to once per week. On 15 March 1990 (while the trees were still dormant) five replicate plants from each treatment were taken for destructive harvesting. Residual N was leached from the sand in each container by the addition of 4 dm"'' deionized water. Two days later the trees were resupplied with nutrient solutions. Trees that had received High N in 1989 were given either 6-0 (High N/High N) or 1-0 (High N/Low N) mol N m"'. Similarly, those given Low N in 1989 were supplied with either 6-0 (Low N/High N) or 1-0 (Low N/Low N) mol N m"''. Destructive harvests were taken on 20 April, 23 May, 27 June, 1 August, 13 September and 20 November. Trees harvested between 20 April and 27 June and on 20 November had all their N supplied during the second year as '•'''NH,,'''^NO3, enriched with '''N to 4-9.S atom "/„. Trees sampled between 1 August and 20 November received unlabelled N until 27 June when their sand was again leached with 4 dm"'' of deionized water prior to supplying ''"'NH^'^'NO., enriched to 9-5 atom "„ '''N for the remainder of the experiment.

At each harvest trees were removed from their pots and their roots cut off. The sand from each pot was sieved and any remaining root material recovered and the bulked root systems washed. T h e remainder of the plant was separated into stem and needles from the origitnal seedling planted the previous year (designated trunk), the needles and twigs grown during 1989 (1989 foliage) and the needles and twigs produced in 1990 (1990 foliage). All samples were freczc-dried, weighed and milled before analysis. At the final harvest of 1990 all the needles from each ioliage class were separated from their twigs alter drying and weighed, before the dry weight of a subsample of 100 needles randomly selected from the bulked sample was also measured. The mean dry weight per tieedle of each tree was calculated and the mean number of needles in each age class estimated by total needle dry weight/mean needle dry weight. Total N concentrations and '"'N enrichments were determined as described by Millard & Proe (1992) and the '''N enrichment used to calculate the uptake of labelled N, as described by Millard & Nielsen (1989). RliSlILTS

Tree grozvth in relation to N sttpply The initial growth of trees in 1990 was not affected by the current N supply, but determined by the N supplied during the previous year (Fig. 1). Flowever, by 23 May and subscc]uently the Low N/High N trees had a significantly greater (P < 0-05) mass than the Low N/Low N plants (Fig. 1), due predominantly to an increase in foliage growth (Fig. 2). Growth of new foliage in the Low N/Low N trees ceased after May, while root growth continued (Fig. 2), producing a total plant mass of approximately half that of trees receiving High N during 1990 (Fig. 1). In contrast, both the roots and new foliage of the I>ow N/High N trees continued to grow throughout 1990 (Fig. 2), and at final harvest there was no significant difference between their total mass and that of the High N/High N trees (Fig. 1). Trees receiving High N in 1989 did not have their growth rate conditioned by the N supply in 1990 until after 1 August (Fig. 1). There were, however, differences in the pattern of foliage and root growth between the High N/High N and High N / L o w N trees. Growth of new foliage finished by the end of May in Fligh N/Low N trees with subsequent growth occurring predominantly in the roots (Fig. 2). In contrast growth of both roots and foliage in the High N/High N trees continued until mid September (Fig. 2). Nitrogen supply had no significant effects on either the mean dry weight of individual 1989 needles or the number of 1989 needles per tree recovered at the end of the experiment, except for the Low

Partitioning and cycling of nitrogen in Sitka spruce

15 20 23 27 1 13 Mar. Apr. May June Aug. Sept.

20 Nov.


20 Nov.

0)

D


20 Nov.


Figure 2. The elTcct of N supply on tlic growtli of roots (D) •MÂ 1990 foliage (A)SE of 10 replicates for the (irst harvest and 5 subsequently.

20 Nov.

are the meiin and

Table 1. The effect of N supply on the individual needle dry iveight {tng) and number of needles per tree grown duritig 1989 and 1990 and the dry iveight of individual leader needles at the final harvest of 1990. Values are the meati { + SE) of five replicates 1990 Leader

1990 Needles

1989 Needles

dry weight

Treatment

Dry weight

Number

Dry weight

Number

High N/High N High N/Low N Low N/High N Low N/Low N

I-1+0-2 1-2 + O-3 1-0+ 0-1 0-8+ 0-2

4600+1280 3800 + 750 1500 ±150 3600 ±630

1-3 ± 0 1 0-8+ 0-1 2-3 ±0-2 11 ±0-1

13 800 ±1180 2-3±O-2 13 5OO±318O 1-5+0-1 9 300± 1 180 3-3 ±0-4 4 400 ± 3 00 l-6±0-l

N / H i g h N trees (Table 1). These had fewer 1989 needles than those from the other treatments {P < 0-05), due presumably to their senescence during 1990. In contrast, N supply had a marked efiect upon the growth of 1990 needles. A constant supply

of High N significantly ( P < 0 - 0 1 ) increased the number of needles grown in 1990 compared to a Low N/Low N supply, but had no efiect upon the mean dr\- weight of indi\ idual needles, except those growing towards the end of tlie season on the leader

116

P. Millard and M. F. Proe Table 2. The effect of N supply on the recovery of unlabelled N {mg per tree) in plants during the spring and early summer of 1990. Values are the mean + SE) of 10 replicates in March and five replicates .subsequently Date

Treatments

Tissue

15 March

20 April

27 June

High N/High N

1990 foliage 1989 foliage Trunk Roots Total 1990 foliage 1989 foliage Trunk Roots Total 1990 foliage 1989 foliage

—

124 + 19-8 78±ll-6 54 + 7-7 122±17-1 378 ±56-4 118 + 32-6 63 ±18-7 44 + 6-4 308 ±10-3

113 + 16-7 57 + 13-5 54 + 8-9 121 ±27-6 345 ±62-5 143 ± 17-1 58 + 19-7 55 ±6-7 136 + 5-5 392 ±19-4

27 ±2-4

43 ±7-7

30 + 6-1 39 ±6-6 49 + 4-0 145 ± 10-6 30 + 6-7 27 ±3-2 29 ± 6-7 56 + 5-7 142+13-7

21 + 1-6 26 ±2-5 40 ±3-5 130±]l-8

High N/Low N

Low N/High N

Trunk Low N/Low N

Roots Total 1990 foliage 1989 foliage

Trunk Roots Total

181 ±27-3 63 + 7-1 125 ± 2 3 4 369 + 42-8 — 181 ±27-3 63 + 7-1 125±23-4 369 ±42-8 — 69 + 10-4 38 + 6-2 43 + 8-5 150 ±23-5 — 69 ± 10-4 38 + 6-2 43 ±8-5

150 ±23-5

shoot (Table 1). Trees from both the treatments preconditioned to a High N supply in 1989 produced a similar number of needles in 1990, irrespective of their current N supply. However, new needle mass in High N / L o w N trees was 10-7 + 0-76 g d.wt needles per tree, compared with 17-9+1-28 d. wt g per tree in the High N/High N trees, due to a significant ( P < 0 - 0 1 ) reduction in the mean dry weight of individual needles, including those recovered from the leader shoot ( l a b l e 1). When trees preconditioned with a Low N supply in 1989 were switched to High N for 1990, their needle growth responded by a significant {P < 0-01) increase in both the number and dry weight of individual needles, thereby producing a total d. wt of 1990 needles greater than the High N/High N trees. Individual needle mass showed a greater response than the number of needles per tree. This was particularly evident for the needles grown towards the end of the season on the leader shoots (Table 1).

83±4-2

41 ±4-5 25 + 4-6

34 ±4-0 54 + 3-7 154 + 8-5

influenced only by the amount of N provided the previous year (Table 2). Thus there were no significant differences in the recovery of unlabelled N between either the Low N/Low N and l,>ow N / High N plants or the High N/High N and High N / Low N trees. Trees preconditioned with a Low N supply remobilized 27-30 mg N tree"' for foliage growth by the second harvest on 20 April. In the l>ow N/Low N trees this unlabelled N represented 76"/,, of the total N recovered in the new foliage and 36'X, in the Low N/High N. When preconditioned with High N, trees remobilized 118-124 mg N tree ' by 20 April, accounting for 90 and 70",, of the total N content of the new foliage of the High N / L o w N and High N/High N plants, respectively. In all the treatments most N was remobilized from the 1989 foliage, and there was no evidence for a decrease in the unlabelled N content of roots or the trunk (which included the older needles). Uptake and partitiotiing of labelled N

Remobilization

of N for spring growth

The provision of labelled N to trees during 1990 allowed the recovery of unlabelled N during the spring and early summer to be used as a direct measure of internal cycling. The total amount of unlabelled N recovered in the trees from each of the treatments did not vary significantly between 15 March and 27 June ( l a b l e 2). The amount of N remobilized for the growth of new foliage in 1990 was unaffected by the current N supply and

Recovery of labelled N in the trees gave a measure of N uptake by the roots throughout 1990. Nitrogen uptake was determined by the current N supply and was unaffected by the amount provided the previous year (Fig. 3). The majority of N had been remobilized by 20 April (Table 2). Thereafter, root growth started and the rate of N uptake by the trees receiving High N in 1990 increased, only to slow down again after 27 June (Fig. 3). The rate of N uptake by trees receiving Low N in 1990 showed no

117

Partitioniitg and cyclittg of nitrogen in Sitka sprttce

except those trees receiving Low N/High N (Table 3). When trees were given labelled N between 28 June and 20 November, a significantly greater proportion {P < 0-05) was recovered in the roots than of N taken up earlier in the year except on the Low N/Low N trees (Table 3). Changes in partitioning were not due to an increased allocation of N to storage in the roots during the late summer and autumn, because the concentrations of N in the root system did not increase significantly between 27 June and 20 November in any treatment (Table 4). There was no e\-idence for N being allocated tor storage in the older needles during the period between 18 June and 20 November. N concentrations in older needles changed little, even in trees receiving Low N/High N, where the concentrations of N fell from 16-3+1-1 and 14-9 + 0-7 mg N g"' to 15-4±l-3 and 14-1+0-7 tng N g^' for the 1989 and 1988 needles, respectively.

1300

20 Nov.

15 20 23 27 Mar. Apr. May June

Figure 3. Llptake of labelled N by trees supplied with '''N throughout 1990. Values are the mean and SE of 5 replicates of High N/IIigh N ( • ) , High N/Low N (O), Low N/ High N (A) and Low N/Low N (O) trees. seasonal trends. Comparison of the High N/High N with the Low N/High N trees showed that there were significant {P < 0-05) differences in root mass during the sun-imcr, with High N/High N trees having the greater root dry weight at each harvest (Fig. 2). However, these differences in root mass did not affect the capacity for N uptake (Fig. 3). During the initial period of tree growth between 15 March and 27 June, the majority of labelled N take up was partitioned to the roots, in all treatments

D I S C I' S S 1 O N

Remobilization of N in the spring has often been estimated for evergreen trees by measuring the withdrawal of N from senescing needles (Turner, 1977; Miller et al., 1979; Baker & Attiwell, 1985). The concentratioi-i of N in the 1990 needles showed no significant change between June and November in the trees recetving High N in 1990, and increased significantly {P < 0-05) in the High N/Low N and Low N/Low N plants as foliage growth was retarded (Table 4). Such budget studies have shown the

Table 3. The effect of N supply on the partitioning of labelled N taketi up during the periods 15 Marcli-27 June and 2HJune'2O November. Data are expressed as the percentage of total labelled N taken up recovered in the roots or 1990 foliage of the trees, and are the mean { + SE) of 10 replicates in March and five replicates sttbsequently 15 March to 27 June

28 June to 20 Noven-iber

'I'rentment

Roots

1990 Foliage

Roots

1990 Foliage


43 ±4-7 55 ±5-1 28 ±2-8 59 ±4-8

37 ±5-2 30 ±5-3 56 ±3-3 26 + 4-6

51 ±0-7 74 ±4-8 42 ±4-6 60 + 2-3

26 ±0-9 17 ± 3-3 47 ±4-0 17+1-8

Table 4. The effect of N supply on the eoneentration of N {mg g ') /" the roots and 1990 needles. Values are the mean and SE of five replicates 20 No\(.'mber

27 June Treatment

Roots

1990 Needles

Roots

1990 Needles


16-4±0-71 9-2 ±0-24 14-8 ±0-92 8-8 + 0-47

26-8±2-30 11-0 ±0-17 24-7 ±2-34 10-3 ±1-35

18-3±0'91 9-1 ±1-06 13-3 ±1-44 7-8 ±0-42

22-O±2-3O 15-6 ±1-30 23-3 ±1-30 14-8 ±2-60

118

P. Millard and M. F. Proe

efficiency of the withdrawal of N during leal' senescence to be unaffected by site fertility (Chapin & Kedrowskt, 1983; Helmisaari, \^92a,b). However, it is well established that there is a reduction in the N content of old leaves, prior to the onset of senescence (e.g. Aronsson & Elowson, 1980; Nebel & Matile, 1992; Crane & Banks, 1992; Reich, Walters & Ellsworth, 1992). Nambiar & Fife (1987) showed that remobilizatioti of N from first-year tieedles provided up to 32 and 57 % of the N used for the current year's needle growth of unfertilized and fertilized P. radiata, respectively. We also found that the majority of N remobilized by P. sitchensis in the spritig came from the previous year's foliage atid was indepetident of leaf senescence. While not all evergreen species remobilize leaf N independently of senescetice (Jonasson, 1989), budget studies which relied upon measuring the difference in N content between green and senescent leaves as the only measure of internal cycling are likely to have underestimated the contribution made to the antiual detnand for N. The capacity for remobilization of stored N for spritig growth was independent of the current N supply. Instead, the size of the N store (as influenced by the N supply the previous year) determined the amount of N remobilized in the second year oi the experiment. Similarly, m a study of Pinus radiata stands grown with contrasting fertilizer and irrigatioti treatments. Crane & Banks (1992) concluded that the amount of N remobilized from the eanopy as a proportioti of the total N available for new growth was not influenced by the N status of the tree. I^'ertilization, therefore, increases the amount of N stored, but does not affect the efficiency with which stored N is subsequently cycled within the tree. The main storage site for N during the winter was in the current year's needles, with little N being remobilized in the spring from older foliage. Other studies have highlighted the importance of young needles as storage sites for N in older trees as well. Fife & Nambiar (1984) reported N storage in the current season's needles of Pinus radiata, with little capacity for N storage during their second or subsequent years. Greenway, Macdonald & Lieffers (1992) found that older needles of 32-yr-old P. mariana did not serve as nutrient storage sites in conditions of excess nutrient availability or as a greater than usual nutrient source during periods of nutrient deficiency. In our study High N stimulated foliage growth and so preconditioned the capacity for N storage, by increasing both the tiumber and size of needles grown in a season. In a study of needle growth in P. sitchensis Chandler & Dale (1990) showed that nutrient deficiency reduced the number of needles per shoot, as well as reducing the number of cells per needle, thereby reducing needle size. Roots can also store N. During root setiescence N can be withdrawn (Persson, 1979) and used to

support further root growth (Ferrier & Alexander, 1991). In a previous study we reported that P. sitchensis can remobilise N from roots in the spring to support the growth of new foliage, and that Ndeficient trees stored a greater proportion of their N reserves over winter in roots than those given a generous N supply (Millard & Proe, 1992). Since autumn uptake of N led to an increase in N concentrations in roots and the current seasoti's foliage we suggested that during this period N uptake may contribute directly to storage. The deciduous Acer pseiidoplatanits can also store significant amounts of N in their roots during winter (Millard & Proe, 1991). In the present study there was no evidence that changes in partitioning of N duritig the growing season were due to an increased allocation to storage. Root N coticentrations did not increase between 17 June and 20 November, while those of the current year's needles only iticreased sigtiificatitly when the trees received lôw N in 1990. Instead the partitioning of N taken up was dependent upon the growth of the individual tissues. There was no evidence that roots stored N during the winter as there was tio remobilisation of N from the roots in the spring. The differetice between these findings and those of our previous study tnay have beeti due to the use of seedlings in the current experiments and rootstocks in the earlier work. Escudero et al. (1992) studyitig leaf longevity in both evergreen and deciduous species concluded that nutrient stress increased leaf longevity, thereby prolonging nutrient retention and so maximizing nutrient use efficiency. However, such an adaptation in P. sitchensis would have little influetiee oti the capacity for internal cycling, sitice the tnajority of N is stored during the winter in young needles whicb are not subsequetitly used again as a store for N. Our results support the view that internal cycling is not a mechanism for adapting to low soil fertility (Chapin & Kedrowski, 1983) but a method of augmentitig the N supply to apical growing points during periods of Bushing (Nambiar & Fife, 1987). A (' K N C) W L !• D G E M \\ N I' S

We thank Sandra (j;illowiiy ;ind julic Suthcrhmcl for their skilled technical assistiincc ;ind Dr J. 13:iC()n for the '-"'N analyses. This work wiis funded by the Scottish OHice Agriculture and Fisheries Department.

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