Distribution of biomass and nitrogen among plant parts and soil nitrogen in a young Alnus incana stand

KERSTIN HUSS-DANELL' AND HELENE OHLSSON Department of Plaizt Plzysiology, UmeB University, S-901 87 UmeB, Sweden

Received June 14, 1991

HUSS-DANELL, K., and OHLSSON, H. 1992. Distribution of biomass and nitrogen among plant parts and soil nitrogen in a young Alnus incana stand. Can. J. Bot. 70: 1545 - 1549.

Grey alder, Alnus irlcana (L.) Moench, was inoculated with the local source of Frankia and planted in nitrogen-poor soil in northern (63.8"N, 20.3"E) Sweden. Each alder root system was enclosed in a cylinder that served.as an open-ended cuvette for nitrogenase activity measurements. The alders grew well, especially during the 2nd year of the study. The final leaf area in each season was more closely related to total alder biomass than final height of alders. The alders lost 17% of their total dry mass as leaf litter each year. This corresponded to 33 g dry mass and 0.67 g N per alder during the 2nd year. During the 2 years the soil N increment was 0.52 g N per alder. Leaf litter N and the increase in soil N corresponded to 27 and 17%, respectively, of the N2 fixed in the 2 years. Already at a young age, N,-fixing A. incana can apparently contribute to an improved fertility of N deficient soils.

Key words: aboveground biomass, Alrzus incana, belowground biomass, leaf litter, nitrogen content, soil N increment.

HUSS-DANELL, K., et OHLSSON, H. 1992. Distribution of biomass and nitrogen among plant parts and soil nitrogen in a young Alnus incana stand. Can. J. Bot. 70 : 1545- 1549.

Les auteurs ont inoculC des plants d'Alnus irzcarla (L.) Moench, avec une souche locale de Frankia et les ont plant& dans un sol pauvre en azote dans le nord de la Sukde (63,8"N., 20,3"E.). Le systkme racinaire de chaque plant d'aulne a CtC placC dans un cylindre qui a servi comme enceinte h extrCmitC ouverte pour la mesure de I'activitC de la nitrogknase. Les aulnes ont poussC normalement, surtout au cours de la 2C annCe de 1'Ctude. La surface foliaire observCe h la fin de chaque saison montrait une relation plus Ctroite avec la masse totale des plants qu'avec leur hauteur. Chaque annCe les plants d'aulne ont perdu 17 % de leur masse skche sous forme de litikre. Ceci correspondait h 33 g de masse skche et 0,67 g d'azote par plant au cours de la deuxikme annCe. Au cours des deux ans, l'augmentation d'azote dans le sol Ctait de 0,52 g par plant. L'azote dans la litikre et l'augmentation de l'azote dans le sol reprisentaient respectivement 27 et 17% de l'azote fixCe au cours des deux annCes. DCjh, lorsqu'il est encore jeune, le plant d'A. incana fixateur d'azote peut amCliorer la fertilitC des sols dCficients en azote.

Mots clks : biomasse aCrienne, Alrzlu irzcana, biomasse sous-terraine, litikre foliaire, contenu en azote, augmentation de l'azote du sol.

[Traduit par la rCdaction]

Introduction Alrzzls species are frequently reported to fix large amounts of

N, up to several hundred kg N . ha-' . year-', although exact measures are difficult to obtain owing to methodological limi- tations (Hibbs and Cromack 1990; Wheeler and Miller 1990). Depending on the species and location, Alnus spp. are of interest in various types of forestry. In Europe the grey alder, Alnus incana (L.) Moench, has potential for use in restoration of degenerated forest soil (Huss-Dane11 and Lundmark 1988), in biomass production (Leikola 1976; Rytter et al. 1989; Wheeler and Miller 1990), and for afforestation of exploited peat bogs (Mikola 1975).

The role of N2 fixation is primarily to provide N in a usable form for the N2-fixing organism or the symbiont's host, but the fixed N is eventually cycled into the ecosystem. Leaf litter of Alnus and other fixin^ in^ trees often, but not always, has a higher N content than neighbouring non-N2-fixing trees (Miller 1983). When A. incana leaf litter was added to a degenerated forest soil without alders, several positive effects followed (Huss-Dane11 and Lundmark 1988). The humus layer became thicker with a higher content of C and N, a higher pH, and a higher degree of base saturation.

Little information is available on the relationship between N2 fixation and the distribution of N within an alder, its leaf litter, and rhizodepositions in the field. In pot experiments indoors, nodulated young A. incana plants without a supply of

'Author to whom correspondence should be addressed.

combined N released considerably more N as shoot litter than N that accumulated in the sand (Huss-Dane11 1 9 8 6 ~ ) .

The present field experiment on a nutrient-poor soil was designed (i) to determine N2 fixation by A. incana in situ and (ii) to measure biomass and N distribution within the alders and the soil during two growing seasons. The results on bio- mass and N distribution are given here. An accompanying paper (Huss-Dane11 et al. 1992) describes how N2 fixation was calculated from whole plant nitrogenase activity by taking into account the diurnal and seasonal variation in nitrogenase activity and the relative efficiency of nitrogenase. A partial description of the experimental plot and measurements in 1987 is given in Huss-Dane11 et al. (1989).

Material and methods Experimerztal plot

The experimental plot, established in May 1987, was located at Umei University, Sweden (63.8"N, 20.3"E). The vegetation and the uppermost 0.5 m of soil was removed from an area-14 x 4 m and replaced with a fine-textured sand. Particles <0.06 mm were 27% of the soil, 0.06-0.2 mm were 48%, 0.2-0.6 mm were 20%, 0.6-2 mm were 4 % , and those 2 -20 mm were 1%. Peat was added to the uppermost 0.12 m to increase the organic content of the sand (Huss-Danell et al. 1989). At start of the experiments a total of 39 cylinders of PVC plastic were placed in the soil. Each cylinder had an inner diameter of 0.25 m, a wall thickness of 3.5 mm, and was 0.30 m deep with 0.03 m reaching above the soil surface. The cylinders were spaced 1.3 x 1 m. In each of the 33 cylinders one alder plant was planted on 4 June 1987. ThFrern.aining six cylinders

Printed in Canada / Imprim6 au Canada

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1546 CAN. J. BOT. VOL. 70. 1992

TABLE 1. Height and leaf area of Altllis incana in the experimental plot

Spring 1987 Autumn 1987 Autumn 1988

Height (m) A 0.25 k0.02 - -

B 0.27k0.02 0.54+0.04 -

C 0.31 k0 .02 0 .78k0.05 1 .34k0.07 Leaf area (m2)

A 0 - -

B 0 0.0530+0.0098 C 0 0.1423 k0.0206 0.4991 k0.0344

NOTE: A are alders harvested at planting, Spring 1987 (n = 6). B and C arc alders used for ARA rncasurcmcnts and harvested in 1987 and 1988. rcspcctivcly (11 = I I). -. not applicable. Data arc .F ? SE.

were left without plants and served as controls for studies of soil chemistry.

Plant tnaterial Seed of grey alder, A. incana (L.) Moench, was collected in 1985

from a single tree in the university area. Plants were inoculated and raised as described previously (Huss-Dane11 et al. 1989). At planting, the alders were well nodulated. Planting depth was adjusted so that a majority of the nodules were at 0.08 m depth. The Frankia inocu- lum, the local source of Frankia, fixes N, and forms spores but lacks hydrogen uptake activity in symbiosis with a number of Aln~cs species, including the provenance of A. incana used in the present study (Huss-Dane11 1991). Nitrogenase activity (acetylene reducing activity, A M ) of the intact alders was measured in 1987 and 1988 (Huss-Dane11 et al. 1989, 1992), and the yearly amount of N2 fixa- tion was calculated (Huss-Danell et al. 1992).

Plant size rneasurernents Plant height was measured at planting and at the end of each grow-

ing season. Stem base diameter was measured at the end of the grow- ing season in 1988. On each stem base two measures were taken perpendicular to each other and the mean value was calculated. Leaf area was measured by comparing each leaf with a transparent scale as detailed in Huss-Dane11 et al. (1989).

Collection of leaf litter Each of the studied alders was enclosed in a funnel-shaped leaf

litter trap of white or pale yellow nylon net (mesh size 1 mm). The opening of the trap was about 0.5 m in diameter in 1987 but larger in 1988 to avoid extensive bending of the branches. The opening was kept level with the top of the alder and the net was fastened around the stem base with a cord. The litter traps were emptied at 1- to 3-day intervals and the leaf litter was immediately dried (70°C for 24 h). The traps were operated 14 September to 8 October 1987 and 29 August to 14 October 1988. Of the leaf litter collected in 1987 only a minor part was kept for analyses and the remainder was returned to the soil surface around the stem base of the alders that were not harvested that year.

Biomass detertninations Six representative alders were harvested in connection with plant-

ing in early June 1987. Stem and branches, bursting buds plus leaves, roots, and root nodules were dried separately (70°C for 24 h). The alders used for A M measurements in 1987 and in 1988 were har- vested on 8 October 1987 and on 17 October 1988, respectively. The soil around the cuvette was excavated and the cuvette removed. The horizontal and vertical distribution of the roots were recorded. The nodulated root system was freed from soil by shaking (1987) or with a water jet (1988) and then immediately stored in a cold room for up to 10 days. Stems and branches, roots, and nodules were dried separately (70°C for 24 h).

Collection of soil sarnples The soil was sampled at planting on 4 June 1987. From each sampled

cuvette or cylinder, two samples were taken from 0- to 0.12-m depth and two samples from 0.12- to 0.25-m depth. A metal cylinder hav-

ing an inner diameter of 32 mm was used. The two samples were com- bined and immediately dried (70°C for 24 h). The sampling procedure was repeated after two growing seasons on 13 October 1988. Samples were also taken with the same metal cylinder to determine the bulk density of the soil from 0- to 0.25-m depth.

Chemical arzalyses Milled dry plant parts were analyzed for total N in a Perkin-Elmer

CHN analyzer. Soil samples were analyzed for total N (Kjeldahl-N) at the National Swedish Laboratory for Agricultural Chemistry (SLL) in Umei .

'Results

Growth of the alders During the first growing season on the experimental plot the

alders as a whole approximately doubled their height, from a mean of 0.28 m to a mean of 0.66 m (Table 1). The alders used for ARA measurements and harvested in 1987 were smaller than those used for ARA measurements and harvested in 1988. The final leaf area was on average 0.098 m2, but alders har- vested in 1987 had lower leaf area than those to be harvested 1988 (Table 1). Possibly the handling of alders during the 1987 season for measurements of ARA, leaf area, and shoot length disturbed the growth of these alders. During the second growing season in 1988, the alders approximately doubled their height again, reaching a mean height of 1.34 m (Table 1). Mean leaf area reached 0.5 m2 in 1988, which was 3.6 times as high as the preceding autumn (group C in Table 1). The stem base diameter was 19 f 1 mm (x & SE, n = 11) at the end of the 1988 season.

At the end of the first season none of the harvested alders had roots reaching deeper than the cuvette, and only half the alders had one or more roots reaching the cuvette wall (Huss- Dane11 et al. 1989). On all alders harvested in 1988, roots reached 5 0 . 2 m below the end of the cuvette and 50.15 m beyond the cuvette radius. The nodules were nearly always at the same position as they were at planting. Only on two alders were some nodules found further down on the root system, but none of the alders had nodules at the bottom of or below the cuvette.

Biomass of the alders Starting with an average dry mass (DM) of 1 g at planting,

the alders increased their DM to nearly 20 and 200 g after one and two growing seasons, respectively (Table 2). At planting the biomass was equally distributed aboveground and below- ground. After the first season more biomass was below- ground, whereas this was significantly (Mann-Whitney U-test, P <0.01) reversed after two growing seasons. Although nodule DM increased 10-fold and 60-fold after one and two growing seasons, respectively, the nodule DM as a fraction of total plant DM decreased from 10 to 3.4% during the study period. The DM distribution in stem plus branches of the current and previous year's growth was measured separately (Table 2). In the first growing season 1.2 g DM was in the current year's growth, whereas the increment in the previous year's stem and branches was 3.3 g. In the second growing season 19.2 g was in the current year's growth, whereas the increment of the previous years stem and branches was 54.8 g.

The leaf litter DM (Table 2) was 3.2 and 33.2 g in the first and second growing season, respectively. The leaf litter thus constituted 17% of total plant DM in each of the 2 years. In alders studied for ARA 1987,- thqkaf DM per unit area was on average 0.60 g m-2, whereas the alders used for ARA

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TABLE 2. Dry mass (g) of Alnus incana in the experimental plot

Plant part A B C

Bursting buds + leaves Leaves

B C

Stem + branches formed 1986 Stem + branches formed 1987 Stem + branches formed 1986- Stem + branches formed 1988 Roots Nodules Aboveground (S) Belowground (R) Whole plant Nodules as % of whole plant R:S

NOTE: A are alders harvested at planting, spring 1987 (11 = 6). B are alders used for ARA measurements and harvested in autumn 1987 (11 = 11). C are alders used for ARA measurements and harvested in autumn 1988 (11 = I I). Data are Y _+ SE for the indicated number of plants. Values in parentheses were not used in totals and ratios at bottom of table. -, not applicable; ds, determined separately; nds, not determined separately.

TABLE 3. Nitrogen content (mg) of Alnus incana in the experimental plot

Plant part A B C

Leaves Stem + branches formed 1986 Stem + branches formed 1987 Stem + branches formed 1986- 1987 Stem + branches formed 1988 Roots Nodules Aboveground Belowground Total

nds

nd s nds

7 + 1 (48) 8 + 2 (52)

15 & 3

673k53 (27) nds nds

5 8 5 k 6 3 (23) 267k21 (11) 872 k 8 7 (35) 124k11 (5)

1525k118 (61) 995k92 (40)

2520& 182

NOTE: A are alders harvested at planting, spring 1987 ( n = 6). Band C a r e alders used for ARA measurements and harvested in autumn 1987 and 1988, respectively (11 = I I). Data are .F f SE (% of total) for indicated number of plants. -, not applicable; ds, determined separately; nds, not determined separately.

measurements in 1988 had a leaf DM per unit area averaging 0.71 g . m-' in 1987 and 0.66 g . m-2 in 1988.

Nitrogen content of the alders The N content of the alders was on average 15 mg per alder

at planting (Table 3). After one growing season, the N content had increased 13 times to 194 mglalder. During the second growing season, the N content increased 13 times again to 2.52 g Nlalder. Nearly half of the N content was below- ground.

The N content of the leaf litter (Table 3) was 43 and 673 mglalder in the 2 years, or approximately 25% the total N of the alders in each of the years. The mean N percentage of DM was only 1.32 + 0.08 in 1987 but 2.09 + 0.08% DM in 1988 (x , SE, n = 22 and n = 1 1, respectively).

Nitrogen content of the soil The N content of the soil (Table 4) was initially 0.12 and

0.05 mg N g-I DM at 0-0.12 and 0.12-0.25 m depth, respectively. After two growing seasons with alders the values had increased significantly to 0.15 and 0.08 mg Nlg DM at the two depths (P 10.01, Wilcoxon matched pairs signed ranks test). The N content in soil from cylinders without alders was similar to the values recorded at start of the experiment. Each cuvette contained a soil volume of 5990 and 6400 cm3 at

TABLE 4. Soil nitrogen content (mglg DM) in the soil of the experimental plot before planting (June 1987) and after two growing

seasons (October 1988) with Alnus incana

October 1988

Soil depth Cuvettes Cylinders (cm) June 1987 with alders without alders

NOTE: Data are I f SE; number of cuvettes or cylinders is in parentheses

0-0.12 and 0.12-0.25 m depth, respectively. Thus the N increase in the soil corresponded to 520 mg N per cuvette, i.e., per alder. This calculation is based on a bulk density of 1.41 _+ 0.13 g . cm-3 (x + SE, n = 5) determined for this soil.

Discussion

The height, leaf area, and biomass of the alders differed considerably between the 2 years -studied (Tables 1 and 2). Height and leaf area were measured ionde'structively. Com-

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TABLE 5. Summary of input and recovery of N in the experimental plot planted with Alnus incana

Component g Nlalder n

Input In alders at planting Fixed 1987 Fixed 1988

Total Recovery

Alders including their leaf litter, autumn 1988

Leaf litter 1987 from alders harvested 1988

Soil N increment 1987 + 1988

Total

NOTE: Data arc .II SE; 11 = number of samplcs. Data on N fixed refcr to Huss-Danell et al. (1992).

paring the alders studied for ARA in 1987 and 1988 (groups B and C in Tables 1 and 2) their height was 2.5 times, leaf area 9.4 times, and whole plant DM 10.4 times as high in 1988 as in 1987. The leaf area measurements were thus a better indi- cator of plant biomass than height measurements. Leaves were not shed in summer. The final leaf area was thus the maximal leaf area during the growing season. As reported in an accom- panying paper, leaf area also appeared to be correlated to N2 fixation (Huss-Dane11 et al. 1992).

The root to shoot ratio (R:S) increased during the first grow- ing season, even though leaves were included in the DM at the end but were lacking at the start of the season (Table 2). A proportionally larger increment in root biomass is likely a response to the nutrient-poor soil (Elliott and Taylor 1981). During the second growing season a proportionally greater DM increment aboveground was recorded. A similar pattern of higher R:S after the first season and lower R:S after the second season was also observed when nursery-grown A. irzcana were planted on a degenerated forest soil (Huss- Danell 1986b). Data on R:S for natural old A. incana are few, but in fertilized and irrigated A. incarza the R:S was 0.20- 0.27 for stands 3-7 years old (Rytter 1989). In a 5-year-old naturally established stand of Alnus sinuata in British Colum- bia, the R:S ratio was 0.29 (Binkley 1982). It therefore seems likely that the R:S in the present study will decrease when the alders become older.

The alders lost 17% of their DM as leaf litter to the soil each year. This is within the range of the 16 to 22% of DM lost as leaf litter from the similarly aged A. irzcana planted on degenerated forest soil in northern Sweden (Huss-Dane11 1986b). The leaf litter was 22% of DM for an intensively managed 3-year-old A. incana stand on a peat bog in southern Sweden (Rytter 1989) and 13% of DM for the A. sinuata stand in British Columbia described by Binkley (1982).

With a spacing of 1 x 1.3 m, the leaf litter production of 3.2 and 33 g DM per alder amounted to 25 kg and 250 kg DM . ha-' in 1987 and 1988, respectively. In the intensively managed A. incana stand studied by Rytter (1989), the spacing was 0.5 x 0.5 m and the leaf litter production was 1400 kg D M . ha-', which corresponds to 35 g DM leaf litter per alder in the 3-year-old stand and is in close agreement with the 33 g DM leaf litter per alder in the present study. On degener-

ated forest soil in northern Sweden (Huss-Dane11 1986b) the leaf litter production was about 2 and 10 g DM per alder and 9 and 44 kg DM . ha-' in the 1st and 2nd years, respectively. However, when A. incaiza was limed at planting on the degenerated forest soil, leaf litter production increased about 2.5 times (Huss-Dane11 1986b). In a 30-year-old A. incana stand at a latitude similar to the present study, a leaf litter production of 1780 kg DM . ha-' corresponding to 760 g DM per alder was recorded (Raulo and Hokkanen 1989). Taken together these studies show a variation in amount of leaf litter per alder and that leaf litter on an area basis depends on both planting density and amount of leaf litter per alder.

The concentration of N in the leaf litter was only 1.32% DM in 1987 but 2.09% DM in 1988. In spite of the frequent empty- ing of the traps, rainfall might have leached out part of the leaf litter N in 1987. However, the N percentage calculated for stem + branches + roots + nodules was 0.99 and 1.16% in 1987 and 1988, respectively (Tables 2 and 3), indicating that the 1987 alders had a lower overall N percentage. This was possibly due to an imbalance between growth and N2 fixation during their establishment. The N percentage of the leaf litter in 1988 was similar to that found in similarly aged A. incana planted on degenerated forest soil in northern Sweden (Huss- Danell 1986b), but it was low compared with leaf litter from fertilized and irrigated A. incana soil in southern Sweden, where an N concentration of about 3 % was found (Rytter et al. 1989).

In the present study, a comparison of N content in the leaf litter (Table 3) and the calculated N2 fixation in 1987 and 1988 (Huss-Dane11 et al. 1992) shows that an amount cor- responding to 2 1 and 24 % of the N2 fixed was released as leaf litter and delivered to the soil in the 2 years. The quantities, types, and N content of the rhizodeposition are difficult to determine (Whipps 1990) and were not examined. For example some of the N released as rhizodeposition was prob- ably taken up by the alder roots. The soil N increment data presented here reflect the net addition of N to the soil.

The increase in soil N from June 1987 to October 1988 cor- responded to 520 mg N per alder. The increase was propor- tionally equal in the upper and the lower halves of the cuvette (Table 4), but the upper half had higher N content because of the addition of limed, fertilized peat at the establishment of the experimental plot. Other inputs of N to the soil, such as precipitation, were not measured nor were any N losses (leaching, denitrification) measured. However, data from cylinders without alders showed no change in N content of the soil (Table 4). Uptake of N by plants other than A. incana was negiligible at the site since only alders were planted and any weeds were removed as small seedlings.

The values of N input and N recovery in the studied system agree very closely (Table 5). The N contained in the alders at planting plus the N fixed during the 2 years amounted to a mean of 3.1 g Nlalder. In comparison, the sum of the N found in the alders harvested in 1988, their leaf litter collected in 1987, and the 1987-1988 increase in soil N averaged 3.2 g Nlalder. This comparison is, however, based on data from different alders. Two different sets of alders (B and C in Tables 1, 2, and 3) were studied for N2 fixation and harvested in 1987 and 1988, but recovered N in Table 5 refers only to alders harvested in 1988. Alders of group C had about 2.5 times the final leaf area of group B alders in the autumn of 1987. Since the amount of N2 fixed was correlated to final leaf area in both 1987 and 1988.fHussDanell et al. 1992), it

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is likely that the value of N fixed 1987 (shown in Table 5) would have been higher if it had been measured on those alders harvested in 1988. Nonetheless, even if the N2 fixation value in 1987 was 2.5 times higher, the amount of N input would still be close to the amount of N recovery reported in Table 5.

Leaf litter N and soil N increment were 26 and 16 % , respec- tively, of the N recovered in the A. incana and its soil, and 27 and 17% of the N fixed during the 2 years (Tables 3 and 5). In addition to meeting their own needs of N for growth, the young alders lost nearly half of their fixed N to the soil. Based on this experimental evidence, it appears that N2-fixing A. incana can contribute to an improved fertility of N deficient soils even in the first few years of growth.

Acknowledgements This study was financially supported by the Swedish Coun-

cil for Forestry and Agricultural Research. We thank Per-Olof Lundquist, Alf Ekblad, and Ann-Sofi Hahlin for valuable assistance and discussions.

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