The fate of 15N-labelled nitrogen deposition in coniferous forest ecosystems

F0res;~;olog-j Management ELSEVIER

Forest Ecology

and Management

101 (1998)

19-27

The fate of ‘“N-labelled nitrogen deposition in coniferous forest ecosystems Albert Tietema a,* , Bridget A. Emmett b, Per Gundersen ‘, 0. Janne Kjonaas d, Chris J. Koopmans a-1 A Landscape

and Environmental ’ Danish

Research Group, Uniuersit?, of Amsterdam, Nieuwe Prinsengracht 130, 1018 VZ Amsterdam. b Institute of Terrestrial Ecology, UWB Deiniol Road, Bangor L.57 ZUP, UK Forest and Landscape Research Institute, H@sholm Kongevej Il. 2970 H@rsholm, Denmark ’ Norwegian Forest Research Institute. H@gskoleL:eien 12. 1432 A’s, Norway Accepted

11 March

Netherlands

1997

Abstract As part of four European ecosystem manipulation experiments in coniferous forests, field-scale 15N tracer experiments have been carried out. The experiments involved a year-long addition of 15NH: and/or ‘“NO; to throughfall at experimental plots with different N inputs. The fate of this applied 15N in the important ecosystems pools (trees. ground vegetation, forest floor and mineral soil), as well as in drainage was measured. About lo-30% of added “N was taken up by the trees and IO- 15% was retained in the mineral soil. Both retention efficiencies were found to be constant with N input. The part of 15N retained in the organic layer was relatively high (20-45% of applied) at low N inputs (O-30 kg N ha-’ yr- ’ 1 but low (lo-20%) at high N inputs (30-80 kg N ha- ’ yr- ’ 1. An inverse relationship between N input and the loss of 15N in drainage was found: drainage losses increased as a function of N input. These results suggest that increased N inputs exceed the capacity of the microbial population to retain throughfall-N in the organic layer, with the result that N leaching increases. 0 1998 Elsevier Science B.V. Kew,ords:

“N

tracer;

Coniferous

forest ecosystem;

NITREX;

Nitrogen;

1. Introduction Increased atmospheric nitrogen (N) input to forest ecosystems has been hypothesized as a major contributor to forest damage in large parts of Europe (Nihlgird, 1985; Aber et al., 1989; Schulze and Freer-Smith, 19911. In order to study the impact of

- Corresponding author. Tel.: + 3 l-20-525-7458: 525-74-3 1; e-mail: [email protected] ’ Present address: Michael Fields Agricultural Troy, WI 53120. USA. 0378-l 127/98/$19.00 0 1998 Elsevier PII SO378-I 127(97)00123-O

fax: + 3 l-20Institute,

East

Science B.V. All rights reserved.

Soil retention

changed N inputs, field-scale ecosystem manipulation experiments with N deposition have been carried out at several sites in Europe as part of NITREX (NITRogen saturation Experiments). NITREX studies the factors and processes affecting N saturation by means of field experiments in eight coniferous forests along a N deposition gradient in north-west Europe (Disc and Wright, 1992; Wright and Van Breemen, 1995). Nitrogen is experimentally added to throughfall at sites with low to moderate N deposition (3-20 kg N ha-’ yr- I), whereas at sites with high N deposition (up to 60 kg N ha-’ yr- t) N is

removed from throughfall by roofs and ion-exchange systems (Disc and Wright, 1992). One of the key questions within NITREX is how changes in N deposition affect N cycling in the ecosystem. In order to address this question, fieldscale “N tracer experiments have been carried out in most NITREX experiments (Kjonaas et al., 19931. This paper summarizes some important results on the short-term fate of ‘5N-labelled throughfall at four sites receiving different levels of N deposition.

2. Material

and methods

2. I. Sites The studied sites are located at Klosterhede (Denmark), Aber (Wales, United Kingdom) and at Speuld and Ysselsteyn (Netherlands). The dominant tree species are Norway spruce (Piceu ubirsl, Sitka spruce (Picea sitchensis), Douglas fir ( Pseudotsugu men:iesii) and Scats pine (Pinus syh,estris), respectively. Ground vegetation is present in two of the forests: Deschampsia ,flexuosa and mosses at Klosterhede and Rubus sp., Dryopteris dilatatu, Molinea caerulea, D. jlexuusa and several kind of mosses at Ysselsteyn. All soils are podzolic. The sites cover a range of atmospheric N inputs from relatively moderate in Denmark and Wales (lo-25 kg N ha-’ yr- ’ in throughfall) to extremely high N

Table

deposition in the Netherlands (50-60 kg N ha -’ yr ’ 1. Additional site information is given in Table ! and by Dise and Wright ( 199’2).

At these four sites, field-scale manipulation cxperiments with nitrogen deposition have been carried out as part of NITREX. At Klosterhede and Aber. the impact of increased nitrogen deposition was studied by N addition experiments. Additional N was sprayed weekly (Aberl or monthly (Klosterhedel to experimental plots. At Aber three levels of N addition were implemented: N was applied as NaNO, at 35kgNha-’ yr ‘(SN3Slor75kgNha~‘yr~! (SN75), or as NH,NOI at 35 kg N ha. ’ yr ’ (AN351. At Klosterhede a total input of 55 kg N ha- ’ yr ’ was simulated by adding 35 kg N ha ! yr as NH,NO;. At the two Dutch sites. the re. versibility of nitrogen saturation was studied by removing nitrogen from throughfall by means of a roof underneath the canopy. Natural throughfall (45-55 kg N ha ’ yr ’ 1 was replaced by an artificial throughfall solution containing very low amounts of N ( < 5 kg N ha- ’ yr ’ 1 and sulphur (Sl, which was sprayed automatically in parallel to natural rain event:, to the experimental plots underneath the roof. The plot size and the replication differed between the sites. The Klosterhede site had three replicated control plots and one N addition plot of 15 ‘x: 15 m. Ai

I

Site characteristics Dose and Wright. available (l-6 yr) ’

1992; Gundersen,

1908). Data on N concentrations

Klosterhede Mean annual temperature (“C) Annual precipitation (mm) Soil classification Tree species Stand age in 1995 (yr) Stand density (trees ha- ’ 1 Bulk precipitation (kg N ha - ’ yr- ’ ) Throughfall (kg N ha-’ yr- ’ ) Leaching below rooting zone (kg N ha- ’ yr- ’ ) Current year needles f%N) Organic layer (%N) Mineral soil (O-30 cm) (%N)

9.0 860 Haplic Piceu

(DK)

Podzol uhirs

and tluxes are average

Aber (UK)

Speuld (NI.)

8.8 1850

9.3

Ferric Stagnopodzol

7s

Piceu 3s

860 9 ‘3 0.6 1.4 I .4 0.07

2020 II 1s 9 1.x 1.8 0.4

sirchensis

values of a> many years as Yxseisteyn

750 Ortic Podzol Pxwdotsugcl 35 800 23 50 29

1.7 2.0 0.08

mw:imii

__.. (NL)

A. Tietema et al./Forest

Ecology

and Marlagement

Aber, treatments were replicated three times on plots of 15 X 15 m. No replications were included at Speuld and Ysselsteyn and the plots measured 10 X 10 m. More details on general experimental set-up in all these sites can be found for Klosterhede in Gundersen and Rasmussen (19951, for Aber in Emmett et al. (1995a,b) and for Speuld and Ysselsteyn in Boxman et al. (1995).

During one year from spring 1992 to spring 1993, “N was added to the throughfall solutions that were sprayed to the experimental plots (Table 2). The tracer was added to the throughfall solution as enriched lSNHi5N0, at Klosterhede, ‘5NHi5N0, and Na’“N0, at Aber and (‘5NH4)2SO;1 at Speuld and Ysselsteyn. The final enrichments of 15N in throughfall ranged from about 2000%0 on the high deposition plots to a maximum of about 80000%~~ on the low deposition plots. The enrichments of “N (6 “N) are expressed as parts per thousand difference from a standard: \ample/R\ta”dard

-

1) *

21

Ecosystem pools and fluxes were sampled to determine the fate of the applied “N at the end of the 1Zmonth addition period. At the Dutch sites, sampling was carried out 9 and 21 months after the start of the addition. The measured pools included trees (sampled as current year and older needles, current year and older twigs, branches, sapwood, heartwood, bark, coarse and fine roots), ground vegetation, the organic layer and the mineral soil (sampled in layers from 0 to 25 cm and 25 to 50 cm soil depth). To quantify the loss of applied 15N by drainage, soil water was sampled below the rooting zone, bulked in proportion to volume collected over three or six months, and analyzed for total NH: and NO,, and 15NHl and 15NO;. Soil water fluxes were calculated by soil hydrological models calibrated to fit measured tensiometer values. The partitioning of added ‘“N was estimated according to a mass balance equation (Nadelhoffer and Fry, 1994):

2.3. 15N tracer experiments

6”N=(R

I01 (19981 19-27

m,,,, = m,( 6 “N, - 6 l5Ni)/(

s15Nlah - 615N,)

where, fnlab = mass of 15N-labelled compound incorporated into the N pool; m, = final mass of the ecosystem N pool; 6 15Nf = final j5N abundance of the ecosystem N pool; S I5Ni = initial I5N abundance in the ecosystem N pool; 6 “Nlab = “N abundance of the labelled N additions. Emmett et al. (1998) give a detailed description of sampling procedures, sample preparation and ‘“N

1ooWl

;here RsTa’+ and Rstandard are the ratios between N and N of the sample and standard, respectively. The standard used is atmospheric N?, with a 15N:‘“N ratio of 1:272 (Hauck et al., 1994).

Table 2 Characteristics of the “N tracer addition experiments. The N fluxes in throughfall and drainage are given for the 12 months of 15N addition (Spring 1992-Spring 1993), except for Speuld and Ysselsteyn, where the two numbers are fluxes in the first 9 and 21 months after the start of the I Z-months addition Site

Klosterhede

Treatment

Control

Period of “N addition Addition as: Total N in throughfall during Ifi N addition (Kg N ha’ ) Calculated 6 15N in throughfall (%) Total N in drainage (kg N ha- ’ )

April

Aber High

1992-April

“NH15N0 2;

81600

AN35 1993 April

3 55

2530 0

Speuld

2.4

SN35 1992-April

“NH’5N04 51

2380 51

3

SN75

1993 NalSNO 51

2178 72

Low May

?

Ysselsteyn High

1992-May

Low 1993 May

High 1992-May

Na15N0 3 91

(“NH,),SO, 4

2181

39000

2870

43 000

3360

l/5

34/61

23/38

36/59

102

44

(‘5~~,)z~~, 6

1993

53

22

A. Tietrma

et al. / Forest

Ecology

and Mantrgement

analysis at the four sites. A cross-laboratory comparison of reference samples at the natural abundance level (Emmett et al., 1998) included also enriched samples of branches (average S ‘5N:37.0%o). needles (84.7%0) and forest floor (24.3%0). The results indicated a maximum difference between the laboratories ranging from 1.0%0 in the forest floor sample to 2.7%0 in the branch sample. These differences between the laboratories were considered small enough to allow a comparison of “N retention rates between the sites, because retention rates of one particular site were all calculated relative to the input of which the enrichment was determined by the same laboratory. A detailed presentation and discussion of the fate of 15N in the specific vegetation and soil compartments at Speuld and Ysselsteyn can be found in Koopmans et al. (1996), at Klosterhede in Gundersen (1998), while for Aber results will be presented in due course. Here the results on “N retention in trees, ground vegetation, organic layer and mineral soil (O-25 cm) and on 15N loss by drainage at all four sites are discussed.

are generally within the range of recoveries found in field scale tracer applications (Mugasha and Pluth. 1994: Preston and Mead. 1994; Buchmann et al., 1995). Deviations from complete recovery of added 15N can be explained by uncertainties in the total N pool sizes and flux estimates, and in 15N abundances in the different pools and fluxes. The largest contribution to uncertainty in ‘“N recovery in field-scale tracer experiments in forests is caused by the total pool sizes. Only the Aber experiment had replicated plots allowing a statistical analysis of recovery data. However, pool sizes of mass were assumed similar for all treatments because of high variability between the plots. As a result. calculated coefficients of variation of total lSN recovery at Aber. ranging from 9%’ (SN35) to 20% (AN351 of applied lSN. only signified variation in total N concentrations and lSN abundances. Another explanation for incomplete recovery is that at some of the sites not all possible N sinks were investigated or given in Table 3. The “N budget at the Dutch sites did not include roots and the mineral soil below 25 cm. Considering the low root biomass at the Dutch sites compared to the other sites (Gundersen et al., 1998), roots are not considered an important sink of 15N in these sites. The mineral soil between 25 and 70 cm soil depth at the Dutch sites retained S- 10% of applied ltiN (Koopmans et al.. 1996). The lower part of the mineral soil

3. Results and discussion Total recoveries of the applied 15N varied between 65 and 105% (Table 3). These recovery rates

Table 3 Retention 1 Z-month

of the added “N addition

llN

as a percentage

added.

The time of sampling

is given

in months

after the start of the ___-

Klosterhede

Site Treatment Total N in throughfall during N addition (kg N ha-’ ) Time of sampling (months) Trees” (%) Ground vegetation (%) Organic layer (% ) Mineral soilb (c/c) Drainage (‘% 1 Total recovery (‘2)

of the total amount

IO1 CIWYJ 1%27

”

Aber

Speuld

Control

High

AN35

SN3S

SN75

20

55

51

51

91

12 32 13 26 I? 0 81

I? 47 3 16 17 4 82

12 32 NP 47 I 25 10.5 (31J

I? 32 NP 17 15 35 99 (9)

12 20 NP II 15 so 97(10)

“Speuld and Ysselsteyn: only aboveground. hKlosterhede: O-30 cm soil depth: Aber, Speuld and Ysselsteyn: O-25 cm. Numbers between brackets are standard deviations (n = 3) of total “N recovery explanation. NP = Not present.

Ysselsteyu

Low

Low

3.5

1.4

Y IS NP 51 70 ? 91

71 33 NP -22 15 7 72

assuming

High

High

35

44

Y ii NP 26 Y IY 67

21 79 NP 15 IS 33 92

constant

Low 3.7 Y 3 NP 1Y 37 h X6

.-_--_ Low High 6. I ?I 10 NP 46 15 IO 81

Hugh

iI

53

0 i NP 2x 20 I2 tJ5

21 i7

NP 71 I(’ !7 bh

total pool sizes. See text for t’urther

A. Tietema et al./ Forest

Ecology

was not considered in this integrative study to keep the compartments as comparable as possible between the sites. Gaseous 15N losses were not measured, nor the drainage of dissolved organic 15N (DON). Denitrification rates are probably small in all sites; estimated N,O emission rate is 0.5 kg N ha-’ yr-’ at the control plot at Aber, rising to 3 to 4 kg N ha-’ yr ~’ in the N addition plots (Emmett et al., 1995~). Leaching of DON, however, can be a significant output of N. In the control plot at Klosterhede, DON leaching losses are small (0.5 kg N ha-’ yr~ ‘1 but about five times as much as NO;-N leaching (Gundersen et al., 1998). At Ysselsteyn, DON leaching amounts to 9.4 kg N ha-’ yr-‘, which is about 15% of total N leaching (Koopmans et al., 1996). The trees retained between 3 and 42% of added lSN. At the two Dutch sites a relatively low amount of 15N was retained by the trees after 9 (Speuld and Ysselsteyn) and after 21 months (Ysselsteyn). The low retention after 9 months can be explained by the difference in sampling date compared to the other sites: the Dutch sampling in February did not include the start of the second growing season in contrast with the samplings in April and May at the other sites. The low 15N retention after 21 months at Ysselsteyn can be attributed to a low tree biomass at Ysselsteyn of less than 50% of tree biomass at the other sites and a low N demand of the trees in that site, as indicated by storage of excess nitrogen as arginine in the needles (Pietila et al., 1991; Boxman et al., 1995, 1998). Ground vegetation at Klosterhede, which consists of D. jlexuosa and mosses,was a significant sink of “N; a maximum of 13% of 15N was retained in the control plot. compared to only 3% in the high-N plot. At Ysselsteyn, ground vegetation consisted mainly of ferns (D. data). At the time of sampling in February. no above-ground parts of these ferns were present. Sampling of the above-ground biomass in August (16 months after the start of the application) showedthat the above-ground parts of the ferns had retained l-2% of the applied 15N(Koopmans et al., 1996). Buchmann et al. (1996) measuredcomparable ‘“N retention rates (9% and 15%) in the ground vegetation of a 15-year-old P. abies stand in Germany 8 months after a single dose application of ‘“NH: and 15NO;, respectively. However, in their experiment the ground vegetation was a much larger

and Management

101 (1998)

19-27

23

sink for the label than the trees (3 and 7%, respectively), indicating the high N competition between these two members of the plant community (Buchmann et al., 1996). Retention of 15N in the organic layer ranged between 11 and 47% (Table 3). Highest retention rates of 40 to 50% were all found in “NH:-addition experiments: at Aber (AN351 and in the low N deposition plots at Speuld (only after 9 months) and Ysselsteyn. The organic layer is one of the important pools capable of retaining large amounts of N. This retention is mainly biological: microbes immobilize inorganic N for assimilationof biomassor incorporation into polymerized decomposition products (Fog, 1988). Part of this 15Nis expected to be immobilized in freshly fallen litter; throughfall-N is one of the main sources of this N immobilized in relatively N-poor organic matter (Van Vuuren and Van der Eerden, 1992; Tietema and Wessel, 1994; Downs et al., 1996). From litter bag data of Koopmans et al. (19971, we calculated that at 9 months only about 15% of the retention in the whole organic layer had been retained in fresh needle litter. This meansthat in both Dutch sites about 85% had been retained in older, N-rich litter, illustrating the large exchange capacity in that organic pool causedby simultaneous immobilization and mineralization of inorganic N (Stams et al.. 1990; Emmett and Quarmby, 1991). Lower retention rates in the organic layer were found in the SN35 (NaNO, addition at 35 kg N ha-’ yr- ’ > treatment at Aber (17%) compared to the AN35 (NH,NO, addition at 35 kg N ha-’ yr~ ‘1 treatment (47%). Also in the P. abies stand studied by Buchmann et al. (1996) a higher retention of 15NH: (63% of applied) than of “NO; (46%) was found in the organic layer. These results can be explained by a preference of microbes to take up NH: insteadof NO, and/or by adsorptionof NH,’ by cation exchange. The first explanation agreeswith the results from laboratory incubations using ‘“N with samplesof the organic layer of the NITREX sites: gross NO; immobilization by microbes in theseacid soils is negligible comparedto grossNH: immobilization (Tietema, 1998). Variation in “N retention in the mineral soil was relatively low; at 12 and 21 months after the start of the application between 1 and 17% of applied 15N was found in the upper 25 or 30 cm of the mineral

soil. Loss rates of inorganic “N by drainage ranged from nearly zero in the control plot at Klosterhede to SO% of at the SN7S (NaNO, addition at 75 kg N ha- ’ yr- ‘) treatment at Aber. Considering the fact that 15N retention in the mineral soil and the amount lost by drainage depend on retention higher in the soil profile (in the organic layer and in the vegetation assuming that the vegetation takes up all its N from the organic layer), these retention and drainage loss rates can be better evaluated as a percentage of the amount of 15N that actual reaches the mineral soil. This calculation assumes that the non-recovered 15N can be explained by unmeasured fluxes leaving the ecosystem from the mineral soil. The 105% recovery in the AN35 plots at Aber was excluded from this calculation. The partioning of this added-‘“N not retained in the organic layer and vegetation. between mineral soil and drainage showed large differences between sites. In the two SN treatments at Aber only 20-30% was retained in the mineral soil, while about 70% was lost in drainage (Table 4). In contrast, at Klosterhede 40-450/o was retained in the mineral soil, and only O-l 1% was leached out of the system. This difference between Aber and Klosterhede can be explained by a difference in N status (Gundersen et al., 1998): the C:N ratio of the top 30 cm at Klosterhede (30) is much higher than at Aber (I 8), signifying a relative N shortageat the first site. At the Dutch sites. the 15N partitioning after 21 months varied per treatment: in the low N treatments more j5N was retained in the mineral soil. while in the high N treatments more of the ‘“N was leached out of the ecosystem.

Table 1 Partioning of added “N that passed the organic layer, assuming sampling is given in months after the start of the I?-month “N

This data set allows evaluation of the differences in the fate of 15N in these forests at different N inputs. A comparison of the low and high N treatments at Speuld and Ysselsteyn, the control and high N treatment at Klosterhede and the SN35 and SN75 treatments at Aber, shows how a decreaseand an increase in N deposition affects N cycling. The results of this analysis are summarized in Fig. 1. in which the arrows illustrate the change in “N retention in trees. organic layer and mineral soil and in 15N loss by drainage as a result of the changesin N inputs. Retention of added-N in the organic layer and loss by drainage showed comparable trends at all sites in responseto changesin N inputs (Fig. I). An increasein N input at Klosterhede and Aber resulted in decreasedretention. while a decreasein N inputs in the Dutch sites led to increasedretention in the organic layer. With respect to the “Iv loss b} drainage the opposite effect was found: lossesof “N are low at low N inputs and high at high inputs. Retention of 15Nin trees showed variable changesas a result of changed input. An average retention rate of 22%:f 10% of added “N was found in the tree compartments of all sites and treatments. Retention efficiency in the mineral soil seemed constant at all sites (13% rt 3%) and thus independent of N input (Fig. I ). These resultsgive an indication of the partitioning of throughfall-N as a function of the total amount of N in input. Independently of the amount of N in throughfall, IO-30% 01‘thar amount is taken up by the trees and IO---IS% is retained in the mineral soil. The percentage of throughfall N retained in the

that the vegetation addition

took up all its liIv

from

Klosterhede

Treatment

Control

High

SN.35

SN75

Low

High

Total N in throughfall during “N addition (kg N ha- ’ ) Time of sampling (months) Amount of ‘“N that passed the organic layer (“/ of total applied) Retention by mineral soil” (‘3, of amount that passed the organic layer) Loss in drainage (‘Z of amount that passed the organic layer)

20 I3 30 40 0

5s 12 34, 1s II

51 I? 51 ‘9 69

91 12 69 21 71-

1.4 21 4s 37 s

31 II 56 27 5’)

O-30

cm soil depth; Aber.

Speuld and Ysselsteyn:

O-15

cm.

layer. The tune of _--. Ysselsteyn

Site

“Klosterhede:

Aber

the organic Speuld

I,ow

High

-..

A. Tietema et al./ Foresi

Ecology

and Management

101 (1998)

19-27

25

Trees

Mineral

soil

Drainage

v

0

20

40

60

80

N In throughtall

0

100

20

40

q

80

60

100

(kg N ha” y”)

Fig. I. The fate of added “N expressed as percentage of total amount applied. as a function of N input. Given is the retention of 15N in trees, organic layer and mineral soil (O-25 cm) and the loss in drainage. The arrows indicate the change in retention as a result of the treatment: either an increased N input at Aber (SN35 and SN75) and Klosterhede (control plot and N addition plot) or a decreased N input at Speuld and Ysselsteyn (high and low N plot).

organic layer is relatively high (20-45%) at N inputs at low N inputs (O-30 kg N ha-i yr- ‘) and low (lo-20%) at high N inputs (30-80 kg N ha-’ yr- ‘1. This would mean that the microbes responsiblefor the retention 15N are strong competitors for the inorganic N supply in throughfall and that there is a limitation in their demandof throughfall-N. Another explanation could be that at low N input the contribution of cation exchange to total retention in the organic layer is higher than at high N input due to a saturation of exchange sites. In the N limited site at Klosterhedecation exchange is a significant pathway of N retention (Gundersen and Rasmussen,1995). whereas unpublished “N enrichments in KC1 extracts of the organic layer at the Dutch sites indicate that in these N saturated sites only a very small proportion (2-7%) of total retained 15N in the organic layer was adsorbed or in soil solution. The amount of throughfall-N in drainage is the result of the retention in the other three compartments.As the trees and the mineral soil retention efficiencies are virtually independent of N input, the relation between “N loss in drainage and N input is complementary to the relation of retention in the organic layer and N input.

In a comparable study, Nadelhoffer et al. (1995) applied i5NO; with 28 and 56 kg N ha-’ yr-’ to a hardwood forest in the north eastern USA. In contrast to our results, they found that NO; retention efficiencies were relatively constant with 25% on the high N plot and 25-30% on the low N plot in the -?s.

20

a c z a 5

3 Aber

Organic Layer 15

0 Klostethede V Speuld A YSSelSteyn

-

0

20

40 N in throughfall

60

80

100

(kg N ha ’ y ‘)

Fig. 2. The absolute amount of throughfall-N (in kg N ha- ’ yr- ’ ) retained in the organic layer, as a function of N input. The arrows indicate the change in retention as a result of the treatment: either an increased N input at Aber (SN35 and SN75) and Klosterhede (control plot and N addition plot) or a decreased N input at Speuld and Ysselsteyn (high and low N plot).

above-ground biomass, organic layer and O-5 cm of the mineral soil. They suggested that the potential of retaining NO,; was stimulated by increased biological activity as a result of the increased N input. This might have been true for the trees at our sites, but not for the organic layer, as that retention efficiency clearly decreased at higher N inputs. This changed retention efficiency of throughfall-N (as a percentage of total throughfall-N) should clearly be distinguished from the changes in the absolute amount of throughfall-N retained (Fig. 2). For instance, an increasing absolute amount of throughfallN is retained in the organic layer at higher N input. The graph clearly shows a maximum of about 10 kg throughfall-N ha-’ yr ’ retained in the organic layer in these four sites (Fig. 2).

4. Conclusion The results presented in this paper agree well with the nitrogen saturation concept (Aber et al., 1989; Aber, 1992). in which N leaching, indicative of a N saturated ecosystem, is attributed to the exceedance of the N demand by biological sinks. The complementary behavior of microbial N retention and leaching as a result of changed N inputs indicates that the organic layer is the biological sink that is being affected by changes in N input. Obviously, at increased N inputs the retention capacity of the microbial population was exceeded. which eventually resulted in increased N leaching. These findings also agree with the hypothesized ‘cascade of response’ to manipulation of N deposition (Tietema et al.. 199.5). This concept describes the sequence of ecosystem response to manipulation as a function of site characteristics, type of manipulation. pool size of the various ecosystem compartments and the degree of interaction between compartments and manipulated phase. Field measurements have indicated that in most NITREX sites run-off and drainage have responded to the changed N inputs (Bredemeier et al., 1998). Partly, this reponse is purely hydrological, if episodes of high water flow contribute to changed nitrate leaching. Microbial N transformations are influenced in most sites (Gundersen et al., 1998), whereas the responses in vegetation are mainly still restricted to one or two sites (Boxman et al., 1998). As the manipulations at the NITREX sites involve N inputs

in throughfall, the results of the “N tracer experiments strongly support the findings that the microbial population and the drainage losses are the first ecosystem compartments to be affected.

Acknowledgements The contributions of Knute Nadelhoffer. Nina Buchmann and Douwe van Dam during the whole course of the 15N experiments are greatly acknowledged. This study was made possible by the financial support of the Commission of European Communities (EV5V-CT930264 and EV5V-CT940436) and by various national funding agencies.

References Aber. J.D.. 1992. Nitrogen cychng and nitrogen saturation in temperate forest ecosystems. Trends in Ecology and Evolution I. 120-223. Aber. J.D., Nadelhoffer, K.J.. Streudler, P., Melillo. J.. 1989. Nitrogen saturation in northern forest ecosystems. Bioscience 39. 37X-386. Boxman. A.W.. Van Dam, D.. Van Dijk. H.F.G.. Hogervor?t. R.F., Koopmans. C.J.. 199.5. Ecosystem responses to reduced nitrogen and sulphur inputs into two coniferous forest stands in the Netherlands. Forest Ecology and Management 71. 7.-29. Boxman. A.W., Blanck. K., Emmett, B.A., Gundersen, P.. Hogerworst. R.F., Kjonaas. O.J., Persson. H., Stuanes. A.O., 1998. Cross-site comparison of vegetation and soil fauna response to experimentally changed nitrogen inputs in coniferous ecosystems in the EC-NITREX project. Forest Ecology and Management 101 (l-3). Bredemeier. M., Blanck. K.. Xu. Y.-J., Tietema, A., Boxman. A.W.. Emmett. B., Moldan. F.. Gundersen. P., Schleppi. P.. Wright, R.F.. 1998. input-output budgets at the NITREX sites. Forest Ecology and Management 101 (l-3). 57-64. Buchmann, N., Schulze, E.-D., Gebauer, G., 1995. ‘rN-ammonium and “N-nitrate uptake of a IS-year-old P&a u&s plantation. Oecologia 102, 361-370. Buchmann. N.. Gebauer, Ci., Schulze. E.-D.. 1996. Partitioning of “N-1abelled ammonium and nitrate among soil, litter, belowand above-ground biomass of trees and understory in a 15. year-old Picea a&es plantation. Biogeochemistry (in press). Dise, N.B.. Wright. R.F. (Eds.), 1992. The NITREX project (Nitrogen saturation experiments). Ecosystem Research Report, 2. Commission of the European Communities, Brussels. Downs. M.R., Nadelhoffer, K.J.. Melillo. J.M.. Aber. J.D.. 1996. Immobilization of a ‘sN labelled nitrate addition by decomposing forest litter. Oecologia 105. 131-150.

A. Tietema et al. /Forest

Ecology

Emmett, B.A., Brittain, A., Hughes, S., GBrres, J., Kennedy, V., Norris, D., Rafarel, R.. Reynolds, B., Stevens, P.A., 1995a. Nitrogen additions (NaNO, and NH,NO,) at Aber forest. Wales: I. Response of throughfall and soil water chemistry. Forest Ecology and Management 71, 45-59. Emmett, B.A.. Brittain, A., Hughes. S., Kennedy, V.. 1995b. Nitrogen additions (NaNO, and NH,NO,) at Aber forest, Wales: II. Response of vegetation and soil. Forest Ecology and Management 71, 61-73. Emmett. B.A., Stevens, P.A., Reynolds, B., 1995~. Factors influencing nitrogen saturation in Sitka spruce stands in Wales UK. Water, Air, Soil Pollut. 85, 1629-1634. Emmett. B.A.. Kjonaas, O.J., Gundersen, P., Koopmans, C.J., Tietema, A.. Sleep, D., 1998. Natural abundance of ‘sN in forests along a nitrogen deposition gradient. Forest Ecology and Management 101 (l-31, 9-18. Emmett, B.A.. Quarmby, C., 1991. The effect of harvesting to the organic intensity on the fate of applied ‘5N-ammonium horizons of a coniferous forest in N-Wales. Biogeochemistry 15. 47-63. Fog. K.. 1988. The effect of added nitrogen on the rate of decomposition of organic matter. Biological Reviews 63, 433462. Gundersen. P., 1998. Effects of enhanced nitrogen deposition in a spruce forest at Klosterhede, Denmark, examined by NH,NO, addition. Forest Ecolology and Management 101 (l-3), 251268. Gundersen, P.. Emmett, B.A., Kjonaas, O.J., Koopmans. C.J.. Tietema, A., 1998. Impact of nitrogen deposition on nitrogen cycling in forests: a synthesis of NITREX data. Forest Ecololy and Management 101 (l-31, 37-55. Gundersen, P., Rasmussen, L., 1995. Nitrogen mobility in a nitrogen limited forest soil at Klosterhede, Denmark, examined by NH,NO, addition, Forest Ecology and Management 71, 75-88. Hauck, R.D., Meisinger, J.J., Mulvaney, R.L.. 1994. Practical considerations in the use of nitrogen tracers in agricultural and environmental research. In: Weaver, R.W.. Angle, J.S., Bottomley, P.S. (Eds.). Methods of soil analysis, Part 2: Microbic logical and biochemical properties. Soil Science of America. Madison, WI. USA. Kjonaas. O.J.. Emmett, B.A., Gundersen, P., Koopmans. C.J.. Tietema, A.. 1993. ‘sN approach within NITREX; II. Enrichment studies. In: Rasmussen, L.. Brydges, T., Mathy, P. (Eds.1. Experimental manipulations of biota and biogeochemical cycling in ecosystems EC. Ecosystems Research Report 4, pp. 235-237. Koopmans, C.J.. Tietema, A., Boxman, A.W., 1996. The fate of 15N enriched throughfall in two coniferous forest stands at two nitrogen deposition levels. Biogeochemistry 34. 19-44. Koopmans. C.J., Tietema, A., Verstraten, J.M.. 1997. The impact

and Management

101 (1998)

19-27

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of experimentally reduced N deposition on litter decomposition in two nitrogen saturated forest ecosystems. Soil Biology and Biochemistry (in press). Mugasha, A.G., Pluth, D.J., 1994. Distribution and recovery of lSN-urea in a tamarack/black spruce mixed stand on a drained minerotrophic peatland. Forest Ecology and Management 68. 353-363. Nadelhoffer. K.J., Fry, B., 1994. Nitrogen isotope studies in forest ecosystems. In: Lajtha, K., Michener, R. (Eds.), Stable Isotopes in Ecology and Environmental Science. Blackwell, Oxford, pp. 22-44. Nadelhoffer, K.J., Downs, M.R.. Fry, B., Aber, J.D., Magill, A.H., Mellilo, J.M., 1995. The fate of ‘5N-labelled nitrate additions to a northern hardwood forest in eastern Maine USA. Oecologia 103, 292-301. NihlgCd. B., 1985. The ammonium hypothesis - an additional explanation to the forest dieback in Europe. Ambio. 14, 2-8. Pietill, M., Lahdesmlki. P.. Pietilainen. P.. Ferm, A., Hytonen, J., Patill, A.. 1991. High nitrogen deposition causes changes in amino acid concentrations and protein spectra in needles of Scats pine (Pinus s$restris). Environmental Pollution 72. 103-l 15. Preston, CM., Mead, D.J., 1994. Growth response and recovery of “N-fertilizer one and eight growing seasons after application to lodgepole pine in British Columbia. Forest Ecology and Management 65, 219-229. Schulze. E.-D., Freer-Smith. P.H., 1991. An evaluation of forest decline based on field observations focused on Norway spruce Picea a&es. Proc. R. Sot. Edinburgh 97, 155-168. Stams, A.J.M.. Lutke Schipholt, I.J., Mamette, E.C.L., Beemsterhoer, B., Woittiez, J.R.W.. 1990. Conversion of lSN-ammonium in forest soils. Plant and Soil 125. 129-134. Tietema, A., 1998. Microbial carbon and nitrogen transformations in litter from coniferous forest ecosystems along an atmospheric nitrogen input gradient. Forest Ecology and Management 101 (l-31. 29-36. Tietema. A., Wessel, W.W., 1994. Microbial activity and leaching during initial oak leaf litter decomposition. Biology and Fertility of Soils 18, 49-54. Tietema, A., Wright, R.F.. Blanck, K., Bredemeier, M., Emmett, B.A., Gundersen, P.. Hultberg, H., Kjiinaas, O.J., Moldan, F., Roelofs. J.G.M., Schleppi, P., Stuanes. A.O.. van Breemen, N.. 1995. NITREX: the timing of response of coniferous forest ecosystems to experimentally-changed nitrogen deposition. Water, Air. Soil Pollut. 85, 1623-1628. Van Vuuren. M.M.I., Van der Eerden, L.J., 1992. Effects of three rates of atmospheric nitrogen deposition enriched with “N on litter decomposition in a heathland. Soil Biology and Biochemistry 24. 527-532. Wright, R.F., Van Breemen. N., 1995. The NITREX project: an introduction. Forest Ecology and Management 7 1, l-5.