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Recovery of 15N-urea 10 years after application to a Douglas-fir pole stand in coastal British Columbia
Forest Ecology and Management 256 (2008) 694–701
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Recovery of 15N-urea 10 years after application to a Douglas-fir pole stand in coastal British Columbia Donald J. Mead a, Scott X. Chang b, Caroline M. Preston c,* a
P.O. Box 6, Collingwood, New Zealand Department of Renewable Resources, 442 Earth Sciences Building, University of Alberta, Edmonton, Alberta, Canada T6G 2E3 c Pacific Forestry Centre, Natural Resources Canada, 506 West Burnside Road, Victoria, BC, Canada V8Z 1M5 b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 14 December 2007 Received in revised form 13 May 2008 Accepted 17 May 2008
The long-term fate of fertilizer N in forest ecosystems is poorly understood even though such information is critical for designing better forest fertilization practices. We studied the distribution and recovery of 15 N (4.934 atom% excess)-labelled fertilizer (applied as urea at 200 kg N ha 1) 10 years after application to a 38–39-year-old Douglas-fir (Pseudotsuga menzeisii (Mirb.) Franco) stand in coastal British Columbia. The urea was applied in the spring (May 1982) or fall (November 1982). Sampling was conducted in October 1992, and we found that after 10 years, there were few differences between the fall and spring fertilizer applications in total N and 15N distribution within the tree and forest ecosystem. On average total fertilizer-N recovery was 59.4%; about 14.5% of the applied-N was recovered in the trees including coarse roots, with foliage containing 41% of the labelled-N recovered in the aboveground tree biomass. Tissue 15N remained mobile and could be transferred to new growth. Soil recovery was 39.8%, which had decreased from 57.0% at a previous 1-year sampling, with an average loss of 3.0% per year from the mineral soil and 3.7% from the litter layers. However, it appears that there was little continuing tree uptake. While short-term effects of fall vs. spring urea application were previously reported, there were no long-term effects on either stand productivity or fertilizer use efficiency, suggesting that if fertilization is properly done, timing of fertilization is not a critical issue in terms of maximizing fertilizer use efficiency for the coastal Douglas-fir forest we studied. Our results also highlight the high capacity of this ecosystem to retain externally applied inorganic N over the long-term, the importance of maximizing nitrogen uptake in the first year, and also of the continuing need to develop new approaches to overcome the generally low efficiency of forest N fertilization. Crown Copyright ß 2008 Published by Elsevier B.V. All rights reserved.
Keywords: Pseudotsuga menzeisii Fertilization 15 N Long-term change N budget N distribution
1. Introduction Nitrogen fertilizer, usually as urea, is frequently applied to midrotation stands of Douglas-fir (Pseudotsuga menzeisii (Mirb.) Franco) in western North America and typical responses for Ndeficient stands are 2–4 m3 ha 1 year 1 for 8–15 years (Chappell et al., 1991). This practice is based on substantial research into estimating growth responses and intensive studies on nutrient cycling and other ecosystem processes over a wide range of sites (Chappell et al., 1991; Mitchell et al., 1996). The application of N fertilizers to late-rotation Douglas-fir stands is less common but is considered more attractive financially if a positive growth
* Corresponding author. Tel.: +1 250 363 0720. E-mail address: [email protected] (C.M. Preston).
response can be established because of the fewer number of years the investment has to be made to realize a return (Bevege, 1984). However, there has been relatively little effort in estimating fertilizer-N uptake and its long-term fate in Douglas-fir ecosystems using labelled-N. Such information is often critical in establishing the effectiveness of the fertilization program and the efficiency of N fertilization (Chang et al., 1996). There have been three short-term studies, two with young Douglas-fir trees and the other in an older Douglas-fir stand (see below), where 15N was used to quantify fertilizer-N uptake or its fate in the ecosystems. Two years after applying urea at 224 kg N ha 1 to 7- and 9-year-old stands on two fertile sites in coastal Washington, Heilman et al. (1982) recovered 30 and 38% of the fertilizer-N in the trees and soils, respectively. They did not find consistent differences between spring and fall applications. The application of 200 kg N ha 1 as urea on snow, under a 13-year-old Douglas-fir stand in the interior of British Columbia resulted in 6, 11, and 33% being recovered in the trees,
0378-1127/$ – see front matter . Crown Copyright ß 2008 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2008.05.022
D.J. Mead et al. / Forest Ecology and Management 256 (2008) 694–701
understory and soil, respectively, after 1 year (Preston et al., 1990). The third experiment was established to understand the processes that occur when urea is applied to forest floor of a 38–39-year-old Douglas-fir stand and how these might differ between fall and spring applications (Nason et al., 1988; Nason, 1989). The results showed greater urea volatilization in the spring than the fall (see later), and after 1 year 57.0% of the applied-N was found, on average, in the soil. A major long-term 15N study with trees was undertaken with lodgepole pine (Pinus contorta Dougl. var. latifolia Engelm.) in interior British Columbia (Preston and Mead, 1994). In this study the distribution from the application of 100 kg N ha 1 as 15N-urea, 15 NH4NO3 and NH415NO3 in the ecosystem was compared 1 and 8 years after application to 11-year-old trees. The results showed that uptake was largely complete after 1 year, and that urea and NH4+ uptakes were similar and considerably higher than from NO3 . There was also evidence of plants outside the plots utilizing the labelled-N and there was a continuing loss of fertilizer-N from the ecosystem. Similar results were obtained in another 15N study that compared fertilizer 15N recovery 2 and 6 years after application to newly planted western redcedar (Thuja plicata Donn.), western hemlock (Tsuga heterophylla (Raf.) Sarg.), and Sitka spruce (Picea sitchensis (Bong.) Carr.) stands in coastal British Columbia (Chang and Preston, 2000). The latter study did not find significant differences in fertilizer-N uptake between the 2- and 6year measurements. Whether labelled fertilizer N is retained or continuously lost from the forest ecosystem thus appears to be site-specific, and long-term studies will help clarify the mechanisms involved in controlling the dynamics of applied-N. The objective of this study was to compare the long-term recovery and ecosystem distribution of 15N-urea applied at 200 kg N ha 1 in the spring or fall to a 38–39-year-old Douglasfir stand. The study was made 10 years after the fertilizer had been applied by Nason et al. (1988) as summarized above. In the initial study, Nason et al. (1988) reported that volatilization losses were higher in the spring than in the fall (14% vs. <1% of applied-N, respectively), although part of the volatilized ammonia was able to be utilized by plants. Furthermore, N moved down the soil profile faster when applied in the fall. Both of these results were related to throughfall patterns shortly after the urea was applied. Nason et al. (1990) also reported that foliar N concentration in current foliage was increased by 19% after 6 months when urea was applied in the spring; with the fall application the same response was measured the following fall. 2. Methods 2.1. Site and experimental design The site and experimental design have been described in detail by Nason (1989) and Nason et al. (1988, 1990). The experiment is located 14 km northwest of Nanaimo on the east side of Vancouver
695
Island at 300-m elevation. The area falls into the Very Dry Maritime Coastal Western Hemlock biogeoclimatic Subzone (CWHxm), previously designated at the time of establishment as the Wetter Coastal Douglas-fir Biogeoclimatic Subzone (Klinka et al., 1991). The climate has cool wet winters and warm summers that are often droughty between mid-July and October. Annual precipitation is 900–1400 mm with the main rainfall being between November and April. Nason et al. (1988) provided details of the temperature and throughfall under the stands immediately after the application of the urea treatments, during the time ammonia volatilization was being measured. The slope of the study site is <5% and the soil, a Typic Haplorthod (Soil Survey Staff, 1975), is well-drained, 75–125-cm thick gravelly loamy sand till overlying basaltic bedrock. The basic soil properties for the LFH and 0–10 cm mineral soil were not significantly different between the spring- and fall-applied urea treatments (Table 1). The forest floor had 354 and 389 g kg 1 of organic C (see below for a description of the methods of analyses), and C:N ratio of 46 and 50, respectively, in the spring and fall treatments. Those organic C concentrations are typical for representative organic horizons in coastal forest ecosystems in the Pacific Northwest (Chang et al., 1996). Organic C concentrations in the 0–10 cm mineral soil layer were much lower. The 15N abundance in the forest floor was also much greater than in the 0– 10 cm mineral soil but in both cases the abundance was greater than the natural abundance (Table 1), indicating that the organic and mineral soil layers were still highly 15N-enriched 10 years after the 15N-labelled fertilizer application. Associated with the high organic C concentration was the high nutrient (total N, NH4+-N, P, K, Ca and Mg) concentrations and cation exchange capacity in the forest floor as compared with the mineral soil. At the time the trial was established the LFH layer was 1–3-cm thick and the A horizon had a pH of 4.6 (Nason et al., 1988). At the time of the trial establishment the 38–39-year-old Douglas-fir stand had a stocking of about 1050 stems ha 1 and a site index of 27 m at 50 years (Table 2). The patchy understory, with cover ranging from 20 to 55%, was dominated by salal (Gaultheria shallon Pursh.) with minor components of Oregon grape (Mahonia nervosa (Pursh.) Nutt.) and bracken fern (Pteridium aqualinum (L.) Kuhn). The original fertilization experiment consisted of five treatments, of which three are the subject of this paper: 1. Control—no fertilizer application, 2. 200 kg N ha 1 as urea applied in the spring, 3. 200 kg N ha 1 as urea applied in the autumn. There were three replications in a completely randomized design. Individual plots were 11 m 11 m (0.0121 ha) and were separated by at least 10 m to prevent cross-contamination. The urea granules of about 5-mm diameter were enriched with 4.934 atom% excess 15N and were uniformly applied to the spring
Table 1 Basic soil properties of the spring- and fall-applied urea treatments at Nanaimo (means with S.E.s in brackets) Treatment
LFH Spring Fall
C (g kg
1
)
N (g kg
1
)
N abundance (%)
NH4+-N (mg kg 1)
P (avail) (mg kg 1)
K (ex) (mg kg
15
1
)
Ca (ex) (mg kg 1)
Mg (ex) (mg kg 1)
CEC (cmol+ kg
102 (4.1) 122 (13.6)
354 (16.3) 389 (22.5)
7.77 (0.61) 7.80 (0.63)
0.8670 (0.0472) 0.8770 (0.0314)
6.4 (1.40) 9.4 (2.43)
53 (6.3) 55 (11.8)
1086 (159.7) 1363 (56.6)
6376 (189.0) 6866 (847.3)
507 (50.7) 641 (126.7)
0–10 cm mineral soil Spring 31 (10.5) Fall 67 (19.7)
0.82 (0.29) 1.25 (0.36)
0.5868 (0.0471) 0.6370 (0.0405)
1.6 (0.20) 1.2 (0.28)
30 (10.9) 26 (10.8)
83 (22.0) 216 (65.5)
973 (390.8) 588 (46.9)
72 (22.0) 73 (11.1)
Fertilization was in May and November 1982, and sampling in October 1992.
17.9 (4.4) 27.2 (5.6)
1
)
D.J. Mead et al. / Forest Ecology and Management 256 (2008) 694–701
696
Table 2 Douglas-fir stand characteristics at the start of the Nanaimo experiment compared to the T2F2 thinning/fertilizer treatment at Shawnigan Lake experiment from where the biomass regression equations were obtained (Mitchell et al., 1996)
Site index age 50 years (m) Stocking (stems ha 1) Mean D.B.H. (cm) Basal area (m2 ha 1) Mean height (m) Mean foliage N (mg g 1)a
Nanaimo experiment
Shawnigan T2F2
27 1054 20.9 35.2 18.7 10.9
25 915 22.0 34.8 19.4 9.1
Both stands are the same age. a At least 9 years after fertilizer was applied.
treatment on 21 May 1982 and to the fall treatment on 26 November 1982. 2.2. Tree uptake methodology In October 1992, about 10 years after the fertilizer was applied, all urea-treated plots and two control plots were sampled to determine tree uptake of fertilizer N based on 15N enrichment. In each treated plot two trees were climbed and a branch sampled at whorl 6 (first formed at age 43 years), whorl 9 (age 40 years) and whorl 15 (age 34 years). In the laboratory these branches were divided into foliage and branches by issue age, with five annual foliage ages being available. Foliage and branch material formed before age 43 years were bulked. This sampling pattern resulted in five foliage samples from whorl 6 and six elsewhere. Their dry weights were recorded. Wood cores and bark plugs were collected at six points along the stem, at whorls 6, 9 and 15, immediately below the live crown, at mid-bole, and at breast height. In each control plot only one tree was sampled to obtain background 15N enrichment data. To estimate the aboveground biomass, we used biomass equations (Table 3) for 42-year-old trees of the T2F2 (heavy thinning with two-thirds of basal area removal and heavy fertilization with application of 448 kg N ha 1 as urea) treatment at the Shawnigan Lake Douglas-fir fertilization-thinning experiment (Mitchell et al., 1996). The equations from this experiment and treatment were used because the stand characteristics were similar to the experimental area in terms of stocking, site index, growth rates and foliar N levels (Table 2). Both experiments had been fertilized with urea and were on shallow glacial till underlain by basalt and at 300-m altitude, although Shawnigan Lake is in a dryer climatic zone (Mitchell et al., 1996). The equations were used to estimate the biomass of trees with mean diameter and the basal area ratio method was employed to obtain individual plot biomass estimates (Madgwick, 1994). As the Nanaimo experimental plots were not measured annually it was sometimes necessary to estimate mean plot diameters for given ages by interpolating between measurement years. Table 3 Equations used to estimate the biomass of various components (obtained from Mitchell et al., 1996) Component Foliage Live branches Stem wood Stem bark
a
b 4.092 4.439 1.689 3.438
2.092 2.491 2.132 2.088
The equations take the form: ln (B) = a + b(ln D), where B is the biomass (kg dry weight) and D is the diameter at breast height (cm); all equations were reported to be highly significant, with the probabilities of F-tests exceeding 0.01 for all biomass components.
Foliar biomass tends to be stable after crown closure as the study at Shawnigan Lake clearly illustrated (Mitchell et al., 1996). As the Shawnigan equations were for trees of age 42 years, the foliage biomass in individual plots at Nanaimo was estimated for this age and these were used for the age 49-year calculations of total N and 15N recovery. Applying the equation to mean diameters at age 49 years would result in excessively high amounts of foliage. Live branch biomass increases with age, unlike foliage biomass (Mitchell et al., 1996). Thus the equation in Table 3 was applied to the diameters at age 49 years to obtain branch biomass and subsequently total N and 15N recovery. Dead branches were ignored as the trees had largely self-pruned. As a statistical analysis revealed that there was a gradient in total N and 15N concentrations (expressed as percent N derived from the fertilizer (%NDFF, Mead and Preston, 1994)) in wood and bark down the tree trunks (see Section 3) it was necessary to weight the chemical analysis means according to the proportion of the trunk they represented. Three stem sections were recognised: 1. The upper 12 years of growth which contained 2% of the biomass, represented by the wood samples collected at whorls 6 and 9. 2. The mid-section of the stem containing the same number of annual sections (between mean tree heights at stand ages 22 and 34 years) and representing 10% of the wood biomass. This proportion was represented by the cores collected at whorl 15 and below the live crown. 3. The lower bole of the tree (to height at age 22 years) that contains 88% of the biomass. The cores taken at mid-bole and at breast height represented this section. The proportions were obtained using mean plot heights in the relevant years and from average taper. Fine roots of the Douglas-fir and understory were sampled directly (see below). Coarse root biomass of Douglas-fir was estimated using published equations for softwoods that relate root biomass to aboveground biomass (Kurz et al., 1996). As these coarse roots were not sampled for analysis, the N and 15N recoveries were estimated using the mean, for that treatment, of all stem and branch total and labelled-N concentrations. The resulting 15 N root recovery was similar to Mead and Pritchett (1975) where roots were excavated and analyzed. 2.3. Soil and fine root sampling Forest floor (LFH) as well as mineral soil samples were collected from 20 cm 20 cm quadrats. The forest floor samples were excavated down to the mineral soil surface and the mineral soil was then excavated by 10 cm intervals to 40 cm. For each treated plot, four LFH quadrats were sampled, of which two were further excavated for mineral soil sampling. For control plots, one quadrat and pit were sampled. In the laboratory, the total fresh weights of the forest floor and mineral soil samples were determined. Then the fine roots (4 mm) were manually separated from the samples, washed and weighed. Tree and understory roots were not separated. Soil moisture content was determined gravimetrically. This allowed the bulk density of the forest floor and mineral soil to be calculated for converting the N concentration data to content. 2.4. Understory vegetation and woody debris sampling Aboveground understory vegetation and woody debris were sampled from two 1 m 1 m quadrats within each treated plot, and similarly from one quadrat for each control plot. Understory vegetation was separated into salal and other understory species.
D.J. Mead et al. / Forest Ecology and Management 256 (2008) 694–701
2.5. Sample preparation and chemical analyses All plant and woody debris samples were dried at 70 8C, weighed and then coarse-ground, subsampled and fine-ground (to 20-mesh in a Wiley mill) for chemical analysis. Total C was determined by combustion using a LECO CR12 carbon analyzer. Available P was determined by the Bray 1 method utilizing an acid fluoride extractant and subsequent colorimetric analysis for phosphate-P. Exchangeable Ca, Mg and K were determined on unbuffered ammonium chloride leachates of the soil by inductively coupled plasma emission spectrometry using an ARL 3410 Sequential Plasma system. Cation exchange capacity (CEC) was determined on the extracted soil using the alcohol wash, NaCl replacement procedure with subsequent distillation and titration to quantify retained ammonium ions. As previously described in more detail (Chang and Preston, 2000; Preston et al., 1990), soil and plant samples were analyzed for total N and 15N concentrations using Kjeldahl digestion and steam distillation. The NH4+-N collected into boric acid was titrated, then converted into N2 gas and analyzed using a Vacuum Generators Sira 9 isotope-ratio mass spectrometer. 2.6. Statistical analyses The analysis of variances of biomass, N contents and N uptake estimates for the treatments sampled in 1992 were made using either SYSTAT (Systat Inc., 1986) or by SAS (SAS Institute Inc., 1989), while soil and understory data were analyzed using the SPSS software (SPSS Inc., Chicago, IL, USA, v.14). Where appropriate, as with sampling within the trees or down the soil profile, a split-plot model was used. Tukey’s HSD test was used for testing differences among foliage and branch ages. Statistical significance at a = 0.05 was used as the decision criterion, unless otherwise noted. 3. Results 3.1. Labelled-N distribution in the trees The ANOVA of crown samples, taken 10 years after the fertilizer was applied, for N concentration and nitrogen derived from the fertilizer (%NDFF) did not reveal differences between the spring and fall applications (Table 4). Foliar N concentration was generally higher in younger foliage and in the upper part of the crown (Table 4), although the difference between whorls was smaller for the fall treatment (0.05%) compared to the spring treatment (0.20%). The age whorl interaction resulted from younger and older foliage age classes following different trends with whorl number. The N concentration of branch woody material had significant treatment age whorl and treatment whorl interactions (Table 4) due to the treatments showing different patterns between whorls, for different aged branch material. On average, N concentrations were higher in the lower than in the upper whorls, and in the younger branches than in the older ones; the N concentration in the oldest and thickest branch material was 35% of that in the youngest twig material (Table 4). The distribution pattern of %NDFF was simpler than for N concentrations, there being no significant interactions. For foliage, the age differences dominated (Table 4), with older foliage having higher enrichments than younger foliage. This trend contrasts with total N concentration. A similar pattern is apparent in branches, but there branch whorl is also important with the branches lower in the crown having higher levels of N and lower levels of %NDFF. The youngest age of branch material had higher %NDFF levels than older branchwood (Table 4).
697
Table 4 ANOVA degrees of freedom (d.f.) and probabilities for foliage and branch N concentrations and 15N derived from the fertilizer (%NDFF), together with the whorl and age means Source
d.f.
Foliage (probability)
N (mg g Treat. (T) Whorl (W) TW Age (A) AT AW ATW Whorl 6 vs. whorl 9, 15 Whorl 9 vs. whorl 15
1 2 2 5 5 9 9 1 1
1
)
0.833 0.001 0.007 0.001 0.953 0.001 0.076 nt nt
Foliage N (mg g Means Whorl 6 9 15 Age 1 2 3 4 5 6
d.f.
%NDFF 0.180 0.080 0.453 0.001 0.227 0.261 0.655 nt nt
Branches (probability) N (mg g
1 2 2 5 5 10 10 1 1
0.570 0.001 0.141 0.001 0.001 0.001 0.004 0.001 0.001
1
)
%NDFF 0.252 0.016 0.545 0.001 0.645 0.685 0.658 0.010 0.090
Branches 1
)
1
%NDFF
N (mg g
)
%NDFF
11.5 11.0 10.2
8.98 9.08 8.64
4.5 4.9 5.1
7.98 7.68 7.38
11.1a 11.8b 11.7ab 11.1a 9.9c 9.1d
8.48c 8.50c 8.91bc 9.11ab 9.14ab 9.44a
7.0a 5.8b 5.0c 4.7c 4.1d 2.5e
8.30a 7.65b 7.69b 7.54b 7.35b 7.54b
Probabilities highlighted in bold are significant at P 0.05. nt, not testable due to imbalance in number of age classes. Means followed by the same letters (a,b,c) are not significantly different at P = 0.05 by Tukey’s test.
The N concentrations for stem wood and bark samples were highest at the top of the tree and lowest below the crown, and lower in the wood than in the bark (Table 5). The %NDFF in stem wood and bark followed a similar trend except that whorl 6 and 9 samples, that grew after the urea were applied, had similar levels. Bark had higher %NDFF levels than wood at whorl 15 and in samples taken from below this height. 3.2. Nitrogen recovery in the trees Ten years after the urea was applied 14.5% of the applied-N was recovered in the trees. There were no significant treatment differences in aboveground biomass, N content or fertilizer recovery (Tables 6 and 7). Foliage contained 41% of the labelledN recovered in the trees (excluding fine roots), whereas it contained 30% of the N content and made up only 4% of tree biomass. This emphasises the importance of N retranslocation within the tree as well as the biological functions of foliage. Branches, which made up 12% of dry weight, had 28 and 32% of the N and labelled-N, respectively. The stem dominated the weight but contained less labelled-N than either of these crown components. Only 10% of the fertilizer-N in the trees was estimated to be in coarse roots. 3.3. Understory and soil Fine root biomass in both the forest floor and mineral soil sampled 10 years after the treatments were applied was not affected by the timing of fertilizer application (Table 8). The variations for most parameters we measured were high, and in particular the amount of fine roots in the mineral soil appears excessive for the fall application.
D.J. Mead et al. / Forest Ecology and Management 256 (2008) 694–701
698
Table 5 ANOVA degrees of freedom (d.f.) and probabilities for wood and bark samples for N concentrations and 15N derived from the fertilizer (%NDFF), together with location means Source
d.f.
N (mg g 1 5 5 1 1 1 1 1
0.881 0.001 0.333 0.001 0.001 0.001 0.833 0.674
N (mg g
Biomass (t ha Spring Fall P value
Bark 1
)
%NDFF
N (mg g
0.323 0.001 0.092 0.001 0.541 0.001 0.001 0.753
0.742 0.001 0.474 0.001 0.001 0.001 0.030 0.164
Wood
Means Location Whorl 6 Whorl 9 Whorl 15 Below live crown Mid-bole Breast height
Treatment
Probability Wood
Treat. (T) Location (L) TL Whorl 6 vs. others Whorl 6 vs. whorl 9 Mid vs. lower Whorl 15 vs. blc* mb* vs. bh*
Table 8 Root and understory aboveground biomass in a urea fertilization experiment near Nanaimo, British Columbia, about 10 years after treatment (stand age 49)
1
)
%NDFF 0.506 0.001 0.832 0.001 0.586 0.001 0.254 0.026
)
1.25 1.08 0.46 0.45 0.35 0.33
%NDFF
N (mg g
8.16 8.35 5.46 3.94 2.03 1.93
5.05 4.22 3.45 3.06 1.85 1.61
1
)
Fine root in mineral soil
Salal
Other understory
1.9 (1.16) 1.1 (0.45) 0.562
12.2 (3.01) 39.9 (21.17) 0.264
1.3 (0.55) 2.6 (0.29) 0.110
0.2 (0.12) 0.4 (0.27) 0.500
1
)
Means, with S.E.s in brackets, together with ANOVA treatment probabilities (P).
labelled-N was recovered in understory biomass, fine roots and coarse woody debris, compared to 17% in the LFH and 23% in mineral soil to 40 cm depth. Recoveries of 15N fertilizer in mineral soil and fine roots decreased with depth (Fig. 1), with most of the 15 N remaining found in the LFH and 0–10 cm layers.
Bark 1
Fine root in LFH
%NDFF
3.4. Total recovery of labelled urea At the end of 10 years we were able to account for 60.2 5.25% (mean S.E.) and 58.6 12.0% of the 15N-urea that was applied (Tables 7 and 9) in the spring and fall applications, respectively. Total recovery in the forest ecosystem was not affected by the timing of urea application (P = 0.911).
8.28 8.01 8.32 7.76 5.86 4.71
4. Discussion
Probabilities highlighted in bold are significant at P 0.05. *blc, mb and bh are below live crown, mid-bole and at breast height, respectively.
4.1. Fertilizer-N distribution within the trees Total N contents in kg N ha 1 in any of the components (woody debris, the forest floor, mineral soil, roots in both the forest floor and mineral soil, and understory vegetation) were not affected by the timing of fertilizer application (Table 9). In terms of total fertilizer-N recovery, the only possible difference was with understory vegetation (P = 0.080), which was higher in the fall than in the spring application treatment. Overall, only 5% of the
Branches and foliage had different patterns of %NDFF and total N concentration (Table 4). Branchwood N concentration tended to be higher in lower than in upper crown branches, but on average was highest in current branchwood, although the significant interactions suggest that this oversimplifies the picture. Of greater importance is that %NDFF was highest with upper branchwood and that current branchwood had a higher level than 2–6-year-old
Table 6 Douglas-fir biomass and N content, by components and treatment, at stand age 49 years, together with standard errors (in parentheses) and ANOVA treatment probabilities (P) Foliage Biomass (t ha 1) Control Urea spring Urea fall Mean P value N content (kg ha Control Urea spring Urea fall Mean P value
1
Branches
Stem bark
Stem wood
Aboveground
Coarse roots
9 (1.3) 13 (1.1) 11 (1.1) 11.1 0.135
29 (4.4) 41 (3.6) 36 (3.6) 35.3 0.181
21 (3.2) 31 (2.6) 27 (2.6) 26.3 0.163
142 (21.0) 205 (17.2) 177 (17.2) 174.5 0.163
201 (29.7) 290 (24.3) 250 (24.3) 247.3 0.162
42 60 53 51.7 na
95 (18.0) 145 (14.7) 121 (14.7) 120.5 0.189
89 (16.9) 130 (13.8) 117 (13.8) 111.9 0.264
40 (7.6) 59 (6.2) 53 (6.2) 50.7 0.268
51 (11.2) 77 (9.1) 65 (9.1) 64.0 0.282
275 (50.8) 410 (41.5) 356 (41.5) 347.2 0.215
40 58 52 49.7 na
)
na, not appropriate. Table 7 Recovery of applied nitrogen in the trees 10 years after treatment (stand age 49 years) by component and treatment, together with standard errors (in brackets) and ANOVA treatment probabilities (P)
% recovery Spring Fall Mean P value
Foliage
Branch
Stem bark
Stem wood
Aboveground
Coarse roots
Total tree
6.1 (0.57) 5.8 (0.57) 5.9 0.740
4.6 (0.37) 4.6 (0.37) 4.6 0.978
1.5 (0.27) 1.6 (0.27) 1.6 0.796
0.9 (0.09) 0.8 (0.09) 0.8 0.322
13.1 (1.20) 12.8 (1.20) 13.0 0.864
1.5 1.5 1.5 na
14.6 14.3 14.5 na
na, not appropriate.
D.J. Mead et al. / Forest Ecology and Management 256 (2008) 694–701
699
Table 9 Total N content and recovery of applied-N in woody debris, mineral soil (0–40 cm), fine roots and understory in a urea fertilization experiment near Nanaimo, British Columbia, about 10 years after treatment (stand age 49) Treatment Total N (kg ha Spring Fall P value % recovery Spring Fall P value
Woody debris
LFH
Mineral soil
Roots in LFH
Roots in mineral soil
Understory
Total
15 (4.7) 11 (1.7) 0.396
361 (93.6) 320 (73.4) 0.745
1480 (281.3) 1104 (134.4) 0.294
6 (3.9) 4 (1.6) 0.575
47 (8.6) 112 (48.4) 0.258
10 (4.8) 19 (2.2) 0.189
1920 (206.8) 1568 (242.0) 0.331
1
)
0.43 (0.21) 0.36 (0.09) 0.770
17.8 (4.05) 16.0 (4.55) 0.778
25.0 (9.50) 20.8 (6.50) 0.736
0.27 (0.13) 0.23 (0.09) 0.845
1.8 (0.48) 4.8 (1.67) 0.166
0.5 (0.25) 1.2 (0.15) 0.080
45.8 (5.85) 43.4 (12.40) 0.866
Means, with S.E.s in brackets, together with ANOVA treatment probabilities (P).
branchwood. Crown stem wood and bark also had higher %NDFF compared to the lower bole (Table 5). In contrast, foliage N levels were higher on upper crown branches, and in younger than older foliage (Table 4), while %NDFF was not influenced by branch position in the crown, but was higher in older than young foliage. Mead and Preston (1994) found a similar pattern with foliage N and %NDFF for lodgepole pine sampled 8 years after the fertilizer was applied. These patterns suggest that the higher %NDFF in older foliage largely, but not completely, reflects the levels of 15N enrichment in available N to the tissue when these were formed, whereas the lower total N in old foliage illustrates the retranslocation out of the foliage as it ages. One-year-old needles can take up additional N from the soil or from retranslocation from current needles (Mead and Preston, 1994; Fife and Nambiar, 1984) but these effects are very much smaller for older needles. The %NDFF levels in branches, wood and bark within the crown, particularly that formed since the fertilizer was applied, appear stable, but these data hide the retranslocation that occurs as these tissues die. Woody tissues
largely formed before the fertilizer was applied, such as lower branches and lower bole samples, have lower 15N enrichments. The 15 N enrichments indicate that movement of fertilizer N to those pre-fertilization woody tissues occurred, a finding also supported by Mead and Preston (1994), Hart and Classen (2003) and Elhani et al. (2003). Looking at recently formed foliage, branches, stem wood and bark, the %NDFF values are remarkably similar, being 8.5, 8.3, 8.3 and 8.2%, respectively. This is an indication of the high mobility of N to tissues formed within the same year. Salal had a slightly higher labelling (11.9%) than the minor understory (6.2%) while fine roots from 0 to 10 cm averaged 9.8%. The current %NDFF values in the LFH and in the 0–10 cm of mineral soil are 10.1 and 4.0%, respectively, which ties closely with the current %NDFF levels in the trees and understory. The change of %NDFF with time illustrates the initial pulse of fertilizer N that went into trees, followed by a gradual decline since that time (Fig. 2). The long-term study in lodgepole pine also found a decrease with time in age sequences of foliage taken from either stem or branch needles (Mead and Preston, 1994). In the lodgepole pine study, foliage was retained for 12 years and the highest 15N enrichment was found in needles that were current or 1-year-old at time of fertilization, but older foliage also contained some fertilizer-N. Nason et al. (1990) also found that nitrogen increased in both current and 1-year-old foliage at Nanaimo following the application of urea, and other studies have reported a similar response in foliage existing at the time the N was applied (Heilman et al., 1982; Mead and Pritchett, 1975; Thomas and Mead, 1992). 4.2. Spring vs. fall urea application We found no differences in Douglas-fir stand biomass, N content or fertilizer-N recovery between urea applied in the spring and fall (Tables 6 and 7). The result agrees with Heilman et al.
Fig. 1. Percent of fertilizer-N recoveries in: (a) mineral soil and (b) fine roots by depth. Error bars are standard errors.
Fig. 2. Change in percent nitrogen derived from the fertilizer (%NDFF) with time for current foliage. The fall 1982 and 1983 data are from Nason (1989).
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(1982) who found inconsistent differences at 2 years between spring- and fall-applied urea in young stands of Douglas-fir. Nason et al. (1988), in this study, found that the volatilization from the urea applied in the spring was 14% of that applied, compared to 0.7% for fall-applied urea. However, they also found that some of this volatilized ammonia was able to be recaptured by Douglas-fir seedlings, so the percentage lost to the ecosystem might have been smaller. Nevertheless, samples of 1-year-old foliage taken 11 and 15 weeks after the fertilizers were applied had significantly higher %NDFF for fall-applied (16%) than for springapplied urea (12%) (Nason, 1989). Heilman et al. (1982) also found higher %NDFF levels in 1-year-old foliage when N was applied in the fall. In the first 2 years the fertilizer-N in the soil was also higher in the fall than in the spring treatment (Nason et al., 1988; Nason, 1989). In the first 3 weeks, the application in the fall was followed by 195 mm of throughfall compared to 6 mm for the spring application. This resulted in less volatilization in the fall application and greater movement of fertilizer-N from the organic horizons down into the mineral soil (Nason et al., 1988). Taken together, this information suggests that the fall application may have resulted in slightly more fertilizer-N being available to plants, but this was not detectable 10 years later. Based on the initial needle N concentrations (around 11 mg g 1 in the fall) and the site index (27 m at 50 years) (Table 2; Nason et al., 1990) a growth response would have been expected on this site (Brix, 1983; Hopmans and Chappell, 1994; Carter et al., 1998). Furthermore, Nason et al. (1990) found that N concentration in current foliage was increased by about 19%. However, like tree biomass measurements (Table 6), tree volume measurements did not detect a significant response to urea fertilizers (Van den Driessche, pers. comm.). There are several explanations for this apparent non-response. First, the volume response could have been missed as tree form was not measured (Bevege, 1984). Second, the experiment had low replication which may have made detection of a response difficult (Miller et al., 1986). Further the stand had not been recently thinned and this reduces the likelihood of a response (Ballard, 1984). Finally, the response to a single fertilization generally declines within 5–7 years (Brix, 1983; Carter et al., 1998), and may even become negative in the longer term, due to the influence of other limiting nutrients or water (Pettersson and Ho¨gbom, 2004). 4.3. Labelled-urea recovery over time A total of 59.1% (averaged across the spring vs. fall applications; Tables 7 and 9) of the applied-N was recovered some 10 years after the N was applied. This is the same as that recovered after 8 years in a lodgepole pine stand in interior British Columbia (Preston and Mead, 1994). In the lodgepole experiment the total recovery was 61.6% for the urea treatment and 60.7% for the 15NH4NO3 treatment. While the tree recovery was higher in this Douglasfir stand than in the lodgepole pine stand (14.5 compared to 8.4%, respectively) the tree recovery is typical of many studies (Preston et al., 1990). Most of the fertilizer N after 10 years was in the LFH and mineral soil which accounted for almost 40% of that applied. Again this is very similar to the lodgepole pine experiment where 33% was recovered in soil within the plot, plus another 8% outside the treated area (Preston and Mead, 1994). The lodgepole pine experiment used single-tree plots that were much smaller than what was used in this experiment, necessitating an estimate of N outside the plot boundary. The uptake into fine roots and understory was also roughly the same in the two experiments. About a year after the treatments were applied (averaged for the two treatments made at eight sampling dates between 28 and 105 weeks after application), Nason (1989) found that there was
25.4% of the labelled-N in the LFH and 31.6% in the mineral soil layers, or a total of 57.0% in the soil. This had decreased over the 9 years to 16.9 and 22.9% in the LFH and mineral soil, respectively, giving a total soil recovery of 39.8% (Table 9). The loss of labelled-N from the mineral soils was equivalent to 3.0% per year. In the lodgepole pine experiment in interior British Columbia, soil organic 15N decreased by 48% over 7 years (a decrease of 7% per year, Preston and Mead, 1994), indicating higher mineralization rates than in the current study. The decrease of labelled-N in the LFH layer was initially very high immediately following the urea applications but after the first year averaged 3.7% per year. This rate of loss from the LFH layer is similar to that found after 3 years when 15N-labelled, dry Douglasfir needles were added to the forest floor (Preston and Mead, 1995). The loss rate in that experiment was 48% in the first year, 15% per year over the next 2 years and 1.9% per year between years 3 and 7.5. The differences could be the result of a number of factors: for example, climatic differences, restriction on rooting in the litter decomposition study, and 15N-recycling in litterfall occurring in the current study. In our study, there would have been some recycling of 15N through litterfall but, while it was not measured directly, it would have been relatively small. Using information given by Mitchell et al. (1996) on litterfall in the fertilized-thinned treatment in Douglas-fir at Shawnigan Lake, together with measurements of 15N enrichments soon after the fertilizer was applied (Fig. 2), the labelled-N in litterfall over the 10 years would be about 3.5% of that applied. This was equivalent to 24 and 20% of the N recovered in the trees and LFH layer after 10 years, respectively. However, the results of both experiments indicated that stabilization of 15N in increasingly recalcitrant forms occurred over time; the incorporation of fertilizer 15N into stable soil organic matter fractions such as the humin fraction was found to be very fast in a forest soil in the Pacific Northwest (Chang and Preston, 1998). The great ability of the soil to immobilize and retain the added N has been demonstrated in 15N studies of conventional N fertilization (Mead and Pritchett, 1975; Heilman et al., 1982; Preston and Mead, 1994; Chang and Preston, 1998), and N fixation (Kaye et al., 2002), as well as in studies that simulated elevated atmospheric N deposition (Buchmann et al., 1996; Nadelhoffer et al., 2004; Holub and Lajtha, 2004); in most situations soil organic matter is the dominant sink of applied-N up to the decade-long timescales that have been studied. Work in an old-growth temperate evergreen mixed-angiosperm forest in southern Chile indicates that the transformation of applied inorganic N was dominated by rapid assimilation and turnover through microbial biomass in the short term (weeks), and transfer from microbial biomass into nitrogen-conserving plant (and to a lesser extent soil organic matter) pools in the long term (years) (Perakis and Hedin, 2001). Such processes (whether the soil or plant biomass is the main sink for the applied-N) result in efficient long-term retention of nitrogen in forest ecosystems, with the bulk of residual fertilizer N generally found in the organic and upper mineral horizons, in both short- and longer-term studies (e.g., Mead and Pritchett, 1975; Noˆmmik and Larsson, 1989; Preston and Mead, 1994). The uptake into coarse roots should be considered indicative as they were not excavated or sampled during the study. However, the estimated recovery was similar to those found in large roots in slash (Pinus elliottii var. elliottii) and lodgepole pine (Mead and Pritchett, 1975; Preston and Mead, 1994). Heilman et al. (1982) found higher recoveries in young Douglas-fir stands but these included fine as well as coarse roots. In our study Douglas-fir fine roots (<4 mm) were not differentiated from understory roots. Fertilizer-N uptake and storage in the root system and in aboveground biomass accounted for the decrease in soil 15N,
D.J. Mead et al. / Forest Ecology and Management 256 (2008) 694–701
resulting in little changes in total fertilizer-N recovery in the ecosystem over time. 5. Conclusions There have been few long-term studies using 15N to track fertilizer-N recovery. Our 10-year recovery of 15N-labelled urea demonstrated that 15N enrichment in plants and soil was still quite adequate for analysis. While the original reports by Nason (1989) and Nason et al. (1988, 1990) described some short-term effects of fall vs. spring urea application, we found no long-term effects on either stand productivity or fertilizer use efficiency, suggesting that if fertilization is properly done, timing of fertilization is not a critical issue in decision making in terms of maximizing fertilizer use efficiency for the coastal Douglas-fir forest we studied. While complete short-term recovery data were not available, our results are consistent with many previous studies indicating that fertilizer N is largely taken up in the first growing season, and that tissue 15N remains mobile and can be transferred to new growth. Our results and Nason (1989) show that after both 1 and 10 years, the highest proportion of 15N was recovered in the soil, mainly in the humus and 0–10 cm mineral soil. Between 1 and 10 years after fertilization, mineral soil 15N was lost at an average rate of 3.0% per year, but it appears that there was little further uptake by trees. This study again highlights the high capacity of temperate forest ecosystems such as this coastal Douglas-fir forest to retain externally applied inorganic N over the long term, the importance of maximizing nitrogen uptake in the first year, and also the continuing need to develop new approaches to overcome the generally low efficiency of forest N fertilization. Acknowledgements We would like to thank Ted Nason for helpful discussions and MacMillan Bloedel for allowing and encouraging us to sample their experiment and making available their growth data on the plots. We greatly appreciate the outstanding field and laboratory efforts of Kevin McCullough. Dr. Woo-Jung Choi (Chonnam National University, Republic of Korea) assisted with some of the calculations of 15N recoveries in the soil and understory vegetation. References Ballard, R., 1984. Fertilization of plantations. In: Bowen, G.D., Nambiar, E.K.S. (Eds.), Nutrition of Plantation Forests. Academic Press, London, pp. 327–360, 516 pp. Bevege, D.I., 1984. Wood yield and quality in relation to tree nutrition. In: Bowen, G.D., Nambiar, E.K.S. (Eds.), Nutrition of Plantation Forests. Academic Press, London, pp. 293–326, 516 pp, pp. 293–326. Brix, H., 1983. Effects of thinning and nitrogen fertilization on growth of Douglasfir: relative contribution of foliage quantity and efficiency. Can. J. Forest Res. 13, 167–175. Buchmann, N., Gebauer, G., Schulze, E.-D., 1996. Partitioning of 15N-labeled ammonium and nitrate among soil, litter, below- and above-ground biomass of trees and understory in a 15-year-old Picea abies plantation. Biogeochemistry 33, 1– 23. Carter, R.E., McWilliams, E.R.G., Klinka, K., 1998. Predicting response of coastal Douglas-fir to fertilizer treatments. Forest Ecol. Manage. 107, 275–289. Chang, S.X., Preston, C.M., 1998. Incorporation and extractability of residual 15N in a coniferous forest soil. Soil Biol. Biochem. 30, 1023–1031. Chang, S.X., Preston, C.M., 2000. Understorey competition affects tree growth and fate of fertilizer-applied 15N in a Coastal British Columbia plantation forest: 6year results. Can. J. Forest Res. 30, 1379–1388. Chang, S.X., Preston, C.M., McCullough, K., Weetman, G.F., Barker, J., 1996. Effect of understory competition on distribution and recovery of 15N applied to a
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western red cedar-western hemlock clear-cut site. Can. J. Forest Res. 26, 313–321. Chappell, N.H., Cole, D.W., Gessel, S.P., Walker, R.B., 1991. Forest fertilization research and practice in the Pacific Northwest. Fert. Res. 27, 129–140. Elhani, S., Lema, B.F., Zeller, B., Bre´chet, C., Guehl, J.M., Dupouey, J.L., 2003. Interannual mobility of nitrogen between beech rings: a labeling experiment. Ann. Forest Sci. 60, 503–508. Fife, D.N., Nambiar, E.K.S., 1984. Movement of nutrients in radiata pine needles in relation to the growth of shoots. Ann. Bot. 54, 303–314. Hart, S.C., Classen, A.T., 2003. Potential for assessing long-term dynamics in soil nitrogen availability from variations in d15N of tree rings. Isot. Environ. Health Stud. 39, 15–28. Heilman, P.E., Dao, T.H., Cheng, H.H., Webster, S.R., Christensen, L., 1982. Comparison of fall and spring applications of 15N-labeled urea to Douglas-fir. II. Fertilizer nitrogen recovery in trees and soil after 2 years. Soil Sci. Soc. Am. J. 46, 1300–1304. Holub, S.M., Lajtha, K., 2004. The fate and retention of organic and inorganic N-15nitrogen in an old-growth forest soil in western Oregon. Ecosystems 7, 368– 380. Hopmans, P., Chappell, H.N., 1994. Growth response of young, thinned Douglas-fir stands to nitrogen fertilizer in relation to soil properties and tree nutrition. Can. J. Forest Res. 24, 1684–1688. Kaye, J.P., Binkley, D., Zou, X., Parrotta, J.A., 2002. Non-labile soil 15nitrogen retention beneath three tree species in a tropical plantation. Soil Sci. Soc. Am. J. 66, 612–619. Klinka, K., Pojar, J., Meidinger, D.V., 1991. Revision of biogeoclimatic units of coastal British Columbia. Northwest Sci. 65, 32–47. Kurz, W.A., Beukema, S.J., Apps, M.J., 1996. Estimation of root biomass and dynamics for the carbon budget model of the Canadian forest sector. Can. J. Forest Res. 26, 1973–1979. Madgwick, H.A.I., 1994. Pinus radiata—Biomass, Form and Growth. H.A.I. Madgwick, Publisher, Rotorua, New Zealand, 428 pp. Mead, D.J., Preston, C.M., 1994. Distribution and retranslocation of 15N in lodgepole pine over eight growing seasons. Tree Physiol. 14, 389–402. Mead, D.J., Pritchett, W.L., 1975. Fertilizer movement in a slash pine ecosystem. II. N distribution after two growing seasons. Plant Soil 43, 467–478. Miller, R.E., Atherton, M.V., Wilcox, J.E., 1986. Comparative effects of three nitrogen fertilizers applied in fall and spring to a 29-year-old Douglas-fir plantation. Can. J. Forest Res. 16, 910–917. Mitchell, A.K., Barclay, H.J., Brix, H., Pollard, D.F.W., Benton, R., deJong, R., 1996. Biomass and nutrient element dynamics in Douglas-fir: effects of thinning and nitrogen fertilization over 18 years. Can. J. Forest Res. 26, 376–388. Nadelhoffer, K.J., Colman, B.P., Currie, W.S., Magill, A., Aber, J.D., 2004. Decadal-scale fates of 15N tracers added to oak and pine stands under ambient and elevated N inputs at the Harvard Forest (USA). Forest Ecol. Manage. 196, 89–107. Nason, G.E., 1989. Dynamics of fertilizer and native nitrogen in a Douglas-fir ecosystem. Thesis. University of Alberta, 197 pp. Nason, G.E., Pluth, D.J., Hardin, R.T., McGill, W.B., 1990. Dynamics of foliar N in Douglas-fir after spring and fall application of ammonium nitrate and urea. Can. J. Forest Res. 20, 1515–1523. Nason, G.E., Pluth, D.J., McGill, W.B., 1988. Volatilization and foliar recapture of ammonia following spring and fall application of nitrogen-15 urea to a Douglasfir ecosystem. Soil Sci. Soc. Am. J. 52, 821–828. Noˆmmik, H., Larsson, K., 1989. Assessment of fertilizer nitrogen accumulation in Pinus sylvestris trees and retention in soil by 15N recovery technique. Scand. J. Forest Res. 4, 427–442. Perakis, S.S., Hedin, L.O., 2001. Fluxes and fates of nitrogen in soil of an unpolluted old-growth temperate forest, southern Chile. Ecology 82, 2245–2260. Pettersson, F., Ho¨gbom, L., 2004. Long-term growth effects following forest nitrogen fertilization in Pinus sylvestris and Picea abies stands in Sweden. Scand. J. Forest Res. 19, 339–347. Preston, C.M., Marshall, V.G., McCullough, K., Mead, D.J., 1990. Fate of 15N-labelled fertilizer applied on snow at two forest sites in British Columbia. Can. J. Forest Res. 20, 1583–1592. Preston, C.M., Mead, D.J., 1994. Growth response and recovery of 15N-fertilizer one and eight growing seasons after application to lodgepole pine in British Columbia. Forest Ecol. Manage. 65, 219–229. Preston, C.M., Mead, D.J., 1995. Long-term recovery in the soil profile of 15N from Douglas-fir needles decomposing in the forest floor. Can. J. Forest Res. 25, 833– 837. SAS Institute Inc., 1989. SAS/STAT User’s Guide, Version 6, 4th ed., vol. 1–2. SAS Institute Inc., Cary, NC, 1686 pp. Soil Survey Staff, 1975. Soil Taxonomy. United States Department of Agriculture Handbook, vol. 436. U.S. Govt. Print. Office, Washington, DC, 754 pp. Systat Inc., 1986. Systat: The System for Statistics. Systat Inc., Evanston, IL, 822 pp. Thomas, R.C., Mead, D.J., 1992. Uptake of nitrogen by Pinus radiata and retention within the soil after applying 15N labelled urea at different frequencies. 1. Growth response and nitrogen budgets. Forest Ecol. Manage. 53, 131–151.
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Recovery of 15N-urea 10 years after application to a Douglas-fir pole stand in coastal British Columbia Donald J. Mead a, Scott X. Chang b, Caroline M. Preston c,* a
P.O. Box 6, Collingwood, New Zealand Department of Renewable Resources, 442 Earth Sciences Building, University of Alberta, Edmonton, Alberta, Canada T6G 2E3 c Pacific Forestry Centre, Natural Resources Canada, 506 West Burnside Road, Victoria, BC, Canada V8Z 1M5 b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 14 December 2007 Received in revised form 13 May 2008 Accepted 17 May 2008
The long-term fate of fertilizer N in forest ecosystems is poorly understood even though such information is critical for designing better forest fertilization practices. We studied the distribution and recovery of 15 N (4.934 atom% excess)-labelled fertilizer (applied as urea at 200 kg N ha 1) 10 years after application to a 38–39-year-old Douglas-fir (Pseudotsuga menzeisii (Mirb.) Franco) stand in coastal British Columbia. The urea was applied in the spring (May 1982) or fall (November 1982). Sampling was conducted in October 1992, and we found that after 10 years, there were few differences between the fall and spring fertilizer applications in total N and 15N distribution within the tree and forest ecosystem. On average total fertilizer-N recovery was 59.4%; about 14.5% of the applied-N was recovered in the trees including coarse roots, with foliage containing 41% of the labelled-N recovered in the aboveground tree biomass. Tissue 15N remained mobile and could be transferred to new growth. Soil recovery was 39.8%, which had decreased from 57.0% at a previous 1-year sampling, with an average loss of 3.0% per year from the mineral soil and 3.7% from the litter layers. However, it appears that there was little continuing tree uptake. While short-term effects of fall vs. spring urea application were previously reported, there were no long-term effects on either stand productivity or fertilizer use efficiency, suggesting that if fertilization is properly done, timing of fertilization is not a critical issue in terms of maximizing fertilizer use efficiency for the coastal Douglas-fir forest we studied. Our results also highlight the high capacity of this ecosystem to retain externally applied inorganic N over the long-term, the importance of maximizing nitrogen uptake in the first year, and also of the continuing need to develop new approaches to overcome the generally low efficiency of forest N fertilization. Crown Copyright ß 2008 Published by Elsevier B.V. All rights reserved.
Keywords: Pseudotsuga menzeisii Fertilization 15 N Long-term change N budget N distribution
1. Introduction Nitrogen fertilizer, usually as urea, is frequently applied to midrotation stands of Douglas-fir (Pseudotsuga menzeisii (Mirb.) Franco) in western North America and typical responses for Ndeficient stands are 2–4 m3 ha 1 year 1 for 8–15 years (Chappell et al., 1991). This practice is based on substantial research into estimating growth responses and intensive studies on nutrient cycling and other ecosystem processes over a wide range of sites (Chappell et al., 1991; Mitchell et al., 1996). The application of N fertilizers to late-rotation Douglas-fir stands is less common but is considered more attractive financially if a positive growth
* Corresponding author. Tel.: +1 250 363 0720. E-mail address: [email protected] (C.M. Preston).
response can be established because of the fewer number of years the investment has to be made to realize a return (Bevege, 1984). However, there has been relatively little effort in estimating fertilizer-N uptake and its long-term fate in Douglas-fir ecosystems using labelled-N. Such information is often critical in establishing the effectiveness of the fertilization program and the efficiency of N fertilization (Chang et al., 1996). There have been three short-term studies, two with young Douglas-fir trees and the other in an older Douglas-fir stand (see below), where 15N was used to quantify fertilizer-N uptake or its fate in the ecosystems. Two years after applying urea at 224 kg N ha 1 to 7- and 9-year-old stands on two fertile sites in coastal Washington, Heilman et al. (1982) recovered 30 and 38% of the fertilizer-N in the trees and soils, respectively. They did not find consistent differences between spring and fall applications. The application of 200 kg N ha 1 as urea on snow, under a 13-year-old Douglas-fir stand in the interior of British Columbia resulted in 6, 11, and 33% being recovered in the trees,
0378-1127/$ – see front matter . Crown Copyright ß 2008 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2008.05.022
D.J. Mead et al. / Forest Ecology and Management 256 (2008) 694–701
understory and soil, respectively, after 1 year (Preston et al., 1990). The third experiment was established to understand the processes that occur when urea is applied to forest floor of a 38–39-year-old Douglas-fir stand and how these might differ between fall and spring applications (Nason et al., 1988; Nason, 1989). The results showed greater urea volatilization in the spring than the fall (see later), and after 1 year 57.0% of the applied-N was found, on average, in the soil. A major long-term 15N study with trees was undertaken with lodgepole pine (Pinus contorta Dougl. var. latifolia Engelm.) in interior British Columbia (Preston and Mead, 1994). In this study the distribution from the application of 100 kg N ha 1 as 15N-urea, 15 NH4NO3 and NH415NO3 in the ecosystem was compared 1 and 8 years after application to 11-year-old trees. The results showed that uptake was largely complete after 1 year, and that urea and NH4+ uptakes were similar and considerably higher than from NO3 . There was also evidence of plants outside the plots utilizing the labelled-N and there was a continuing loss of fertilizer-N from the ecosystem. Similar results were obtained in another 15N study that compared fertilizer 15N recovery 2 and 6 years after application to newly planted western redcedar (Thuja plicata Donn.), western hemlock (Tsuga heterophylla (Raf.) Sarg.), and Sitka spruce (Picea sitchensis (Bong.) Carr.) stands in coastal British Columbia (Chang and Preston, 2000). The latter study did not find significant differences in fertilizer-N uptake between the 2- and 6year measurements. Whether labelled fertilizer N is retained or continuously lost from the forest ecosystem thus appears to be site-specific, and long-term studies will help clarify the mechanisms involved in controlling the dynamics of applied-N. The objective of this study was to compare the long-term recovery and ecosystem distribution of 15N-urea applied at 200 kg N ha 1 in the spring or fall to a 38–39-year-old Douglasfir stand. The study was made 10 years after the fertilizer had been applied by Nason et al. (1988) as summarized above. In the initial study, Nason et al. (1988) reported that volatilization losses were higher in the spring than in the fall (14% vs. <1% of applied-N, respectively), although part of the volatilized ammonia was able to be utilized by plants. Furthermore, N moved down the soil profile faster when applied in the fall. Both of these results were related to throughfall patterns shortly after the urea was applied. Nason et al. (1990) also reported that foliar N concentration in current foliage was increased by 19% after 6 months when urea was applied in the spring; with the fall application the same response was measured the following fall. 2. Methods 2.1. Site and experimental design The site and experimental design have been described in detail by Nason (1989) and Nason et al. (1988, 1990). The experiment is located 14 km northwest of Nanaimo on the east side of Vancouver
695
Island at 300-m elevation. The area falls into the Very Dry Maritime Coastal Western Hemlock biogeoclimatic Subzone (CWHxm), previously designated at the time of establishment as the Wetter Coastal Douglas-fir Biogeoclimatic Subzone (Klinka et al., 1991). The climate has cool wet winters and warm summers that are often droughty between mid-July and October. Annual precipitation is 900–1400 mm with the main rainfall being between November and April. Nason et al. (1988) provided details of the temperature and throughfall under the stands immediately after the application of the urea treatments, during the time ammonia volatilization was being measured. The slope of the study site is <5% and the soil, a Typic Haplorthod (Soil Survey Staff, 1975), is well-drained, 75–125-cm thick gravelly loamy sand till overlying basaltic bedrock. The basic soil properties for the LFH and 0–10 cm mineral soil were not significantly different between the spring- and fall-applied urea treatments (Table 1). The forest floor had 354 and 389 g kg 1 of organic C (see below for a description of the methods of analyses), and C:N ratio of 46 and 50, respectively, in the spring and fall treatments. Those organic C concentrations are typical for representative organic horizons in coastal forest ecosystems in the Pacific Northwest (Chang et al., 1996). Organic C concentrations in the 0–10 cm mineral soil layer were much lower. The 15N abundance in the forest floor was also much greater than in the 0– 10 cm mineral soil but in both cases the abundance was greater than the natural abundance (Table 1), indicating that the organic and mineral soil layers were still highly 15N-enriched 10 years after the 15N-labelled fertilizer application. Associated with the high organic C concentration was the high nutrient (total N, NH4+-N, P, K, Ca and Mg) concentrations and cation exchange capacity in the forest floor as compared with the mineral soil. At the time the trial was established the LFH layer was 1–3-cm thick and the A horizon had a pH of 4.6 (Nason et al., 1988). At the time of the trial establishment the 38–39-year-old Douglas-fir stand had a stocking of about 1050 stems ha 1 and a site index of 27 m at 50 years (Table 2). The patchy understory, with cover ranging from 20 to 55%, was dominated by salal (Gaultheria shallon Pursh.) with minor components of Oregon grape (Mahonia nervosa (Pursh.) Nutt.) and bracken fern (Pteridium aqualinum (L.) Kuhn). The original fertilization experiment consisted of five treatments, of which three are the subject of this paper: 1. Control—no fertilizer application, 2. 200 kg N ha 1 as urea applied in the spring, 3. 200 kg N ha 1 as urea applied in the autumn. There were three replications in a completely randomized design. Individual plots were 11 m 11 m (0.0121 ha) and were separated by at least 10 m to prevent cross-contamination. The urea granules of about 5-mm diameter were enriched with 4.934 atom% excess 15N and were uniformly applied to the spring
Table 1 Basic soil properties of the spring- and fall-applied urea treatments at Nanaimo (means with S.E.s in brackets) Treatment
LFH Spring Fall
C (g kg
1
)
N (g kg
1
)
N abundance (%)
NH4+-N (mg kg 1)
P (avail) (mg kg 1)
K (ex) (mg kg
15
1
)
Ca (ex) (mg kg 1)
Mg (ex) (mg kg 1)
CEC (cmol+ kg
102 (4.1) 122 (13.6)
354 (16.3) 389 (22.5)
7.77 (0.61) 7.80 (0.63)
0.8670 (0.0472) 0.8770 (0.0314)
6.4 (1.40) 9.4 (2.43)
53 (6.3) 55 (11.8)
1086 (159.7) 1363 (56.6)
6376 (189.0) 6866 (847.3)
507 (50.7) 641 (126.7)
0–10 cm mineral soil Spring 31 (10.5) Fall 67 (19.7)
0.82 (0.29) 1.25 (0.36)
0.5868 (0.0471) 0.6370 (0.0405)
1.6 (0.20) 1.2 (0.28)
30 (10.9) 26 (10.8)
83 (22.0) 216 (65.5)
973 (390.8) 588 (46.9)
72 (22.0) 73 (11.1)
Fertilization was in May and November 1982, and sampling in October 1992.
17.9 (4.4) 27.2 (5.6)
1
)
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696
Table 2 Douglas-fir stand characteristics at the start of the Nanaimo experiment compared to the T2F2 thinning/fertilizer treatment at Shawnigan Lake experiment from where the biomass regression equations were obtained (Mitchell et al., 1996)
Site index age 50 years (m) Stocking (stems ha 1) Mean D.B.H. (cm) Basal area (m2 ha 1) Mean height (m) Mean foliage N (mg g 1)a
Nanaimo experiment
Shawnigan T2F2
27 1054 20.9 35.2 18.7 10.9
25 915 22.0 34.8 19.4 9.1
Both stands are the same age. a At least 9 years after fertilizer was applied.
treatment on 21 May 1982 and to the fall treatment on 26 November 1982. 2.2. Tree uptake methodology In October 1992, about 10 years after the fertilizer was applied, all urea-treated plots and two control plots were sampled to determine tree uptake of fertilizer N based on 15N enrichment. In each treated plot two trees were climbed and a branch sampled at whorl 6 (first formed at age 43 years), whorl 9 (age 40 years) and whorl 15 (age 34 years). In the laboratory these branches were divided into foliage and branches by issue age, with five annual foliage ages being available. Foliage and branch material formed before age 43 years were bulked. This sampling pattern resulted in five foliage samples from whorl 6 and six elsewhere. Their dry weights were recorded. Wood cores and bark plugs were collected at six points along the stem, at whorls 6, 9 and 15, immediately below the live crown, at mid-bole, and at breast height. In each control plot only one tree was sampled to obtain background 15N enrichment data. To estimate the aboveground biomass, we used biomass equations (Table 3) for 42-year-old trees of the T2F2 (heavy thinning with two-thirds of basal area removal and heavy fertilization with application of 448 kg N ha 1 as urea) treatment at the Shawnigan Lake Douglas-fir fertilization-thinning experiment (Mitchell et al., 1996). The equations from this experiment and treatment were used because the stand characteristics were similar to the experimental area in terms of stocking, site index, growth rates and foliar N levels (Table 2). Both experiments had been fertilized with urea and were on shallow glacial till underlain by basalt and at 300-m altitude, although Shawnigan Lake is in a dryer climatic zone (Mitchell et al., 1996). The equations were used to estimate the biomass of trees with mean diameter and the basal area ratio method was employed to obtain individual plot biomass estimates (Madgwick, 1994). As the Nanaimo experimental plots were not measured annually it was sometimes necessary to estimate mean plot diameters for given ages by interpolating between measurement years. Table 3 Equations used to estimate the biomass of various components (obtained from Mitchell et al., 1996) Component Foliage Live branches Stem wood Stem bark
a
b 4.092 4.439 1.689 3.438
2.092 2.491 2.132 2.088
The equations take the form: ln (B) = a + b(ln D), where B is the biomass (kg dry weight) and D is the diameter at breast height (cm); all equations were reported to be highly significant, with the probabilities of F-tests exceeding 0.01 for all biomass components.
Foliar biomass tends to be stable after crown closure as the study at Shawnigan Lake clearly illustrated (Mitchell et al., 1996). As the Shawnigan equations were for trees of age 42 years, the foliage biomass in individual plots at Nanaimo was estimated for this age and these were used for the age 49-year calculations of total N and 15N recovery. Applying the equation to mean diameters at age 49 years would result in excessively high amounts of foliage. Live branch biomass increases with age, unlike foliage biomass (Mitchell et al., 1996). Thus the equation in Table 3 was applied to the diameters at age 49 years to obtain branch biomass and subsequently total N and 15N recovery. Dead branches were ignored as the trees had largely self-pruned. As a statistical analysis revealed that there was a gradient in total N and 15N concentrations (expressed as percent N derived from the fertilizer (%NDFF, Mead and Preston, 1994)) in wood and bark down the tree trunks (see Section 3) it was necessary to weight the chemical analysis means according to the proportion of the trunk they represented. Three stem sections were recognised: 1. The upper 12 years of growth which contained 2% of the biomass, represented by the wood samples collected at whorls 6 and 9. 2. The mid-section of the stem containing the same number of annual sections (between mean tree heights at stand ages 22 and 34 years) and representing 10% of the wood biomass. This proportion was represented by the cores collected at whorl 15 and below the live crown. 3. The lower bole of the tree (to height at age 22 years) that contains 88% of the biomass. The cores taken at mid-bole and at breast height represented this section. The proportions were obtained using mean plot heights in the relevant years and from average taper. Fine roots of the Douglas-fir and understory were sampled directly (see below). Coarse root biomass of Douglas-fir was estimated using published equations for softwoods that relate root biomass to aboveground biomass (Kurz et al., 1996). As these coarse roots were not sampled for analysis, the N and 15N recoveries were estimated using the mean, for that treatment, of all stem and branch total and labelled-N concentrations. The resulting 15 N root recovery was similar to Mead and Pritchett (1975) where roots were excavated and analyzed. 2.3. Soil and fine root sampling Forest floor (LFH) as well as mineral soil samples were collected from 20 cm 20 cm quadrats. The forest floor samples were excavated down to the mineral soil surface and the mineral soil was then excavated by 10 cm intervals to 40 cm. For each treated plot, four LFH quadrats were sampled, of which two were further excavated for mineral soil sampling. For control plots, one quadrat and pit were sampled. In the laboratory, the total fresh weights of the forest floor and mineral soil samples were determined. Then the fine roots (4 mm) were manually separated from the samples, washed and weighed. Tree and understory roots were not separated. Soil moisture content was determined gravimetrically. This allowed the bulk density of the forest floor and mineral soil to be calculated for converting the N concentration data to content. 2.4. Understory vegetation and woody debris sampling Aboveground understory vegetation and woody debris were sampled from two 1 m 1 m quadrats within each treated plot, and similarly from one quadrat for each control plot. Understory vegetation was separated into salal and other understory species.
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2.5. Sample preparation and chemical analyses All plant and woody debris samples were dried at 70 8C, weighed and then coarse-ground, subsampled and fine-ground (to 20-mesh in a Wiley mill) for chemical analysis. Total C was determined by combustion using a LECO CR12 carbon analyzer. Available P was determined by the Bray 1 method utilizing an acid fluoride extractant and subsequent colorimetric analysis for phosphate-P. Exchangeable Ca, Mg and K were determined on unbuffered ammonium chloride leachates of the soil by inductively coupled plasma emission spectrometry using an ARL 3410 Sequential Plasma system. Cation exchange capacity (CEC) was determined on the extracted soil using the alcohol wash, NaCl replacement procedure with subsequent distillation and titration to quantify retained ammonium ions. As previously described in more detail (Chang and Preston, 2000; Preston et al., 1990), soil and plant samples were analyzed for total N and 15N concentrations using Kjeldahl digestion and steam distillation. The NH4+-N collected into boric acid was titrated, then converted into N2 gas and analyzed using a Vacuum Generators Sira 9 isotope-ratio mass spectrometer. 2.6. Statistical analyses The analysis of variances of biomass, N contents and N uptake estimates for the treatments sampled in 1992 were made using either SYSTAT (Systat Inc., 1986) or by SAS (SAS Institute Inc., 1989), while soil and understory data were analyzed using the SPSS software (SPSS Inc., Chicago, IL, USA, v.14). Where appropriate, as with sampling within the trees or down the soil profile, a split-plot model was used. Tukey’s HSD test was used for testing differences among foliage and branch ages. Statistical significance at a = 0.05 was used as the decision criterion, unless otherwise noted. 3. Results 3.1. Labelled-N distribution in the trees The ANOVA of crown samples, taken 10 years after the fertilizer was applied, for N concentration and nitrogen derived from the fertilizer (%NDFF) did not reveal differences between the spring and fall applications (Table 4). Foliar N concentration was generally higher in younger foliage and in the upper part of the crown (Table 4), although the difference between whorls was smaller for the fall treatment (0.05%) compared to the spring treatment (0.20%). The age whorl interaction resulted from younger and older foliage age classes following different trends with whorl number. The N concentration of branch woody material had significant treatment age whorl and treatment whorl interactions (Table 4) due to the treatments showing different patterns between whorls, for different aged branch material. On average, N concentrations were higher in the lower than in the upper whorls, and in the younger branches than in the older ones; the N concentration in the oldest and thickest branch material was 35% of that in the youngest twig material (Table 4). The distribution pattern of %NDFF was simpler than for N concentrations, there being no significant interactions. For foliage, the age differences dominated (Table 4), with older foliage having higher enrichments than younger foliage. This trend contrasts with total N concentration. A similar pattern is apparent in branches, but there branch whorl is also important with the branches lower in the crown having higher levels of N and lower levels of %NDFF. The youngest age of branch material had higher %NDFF levels than older branchwood (Table 4).
697
Table 4 ANOVA degrees of freedom (d.f.) and probabilities for foliage and branch N concentrations and 15N derived from the fertilizer (%NDFF), together with the whorl and age means Source
d.f.
Foliage (probability)
N (mg g Treat. (T) Whorl (W) TW Age (A) AT AW ATW Whorl 6 vs. whorl 9, 15 Whorl 9 vs. whorl 15
1 2 2 5 5 9 9 1 1
1
)
0.833 0.001 0.007 0.001 0.953 0.001 0.076 nt nt
Foliage N (mg g Means Whorl 6 9 15 Age 1 2 3 4 5 6
d.f.
%NDFF 0.180 0.080 0.453 0.001 0.227 0.261 0.655 nt nt
Branches (probability) N (mg g
1 2 2 5 5 10 10 1 1
0.570 0.001 0.141 0.001 0.001 0.001 0.004 0.001 0.001
1
)
%NDFF 0.252 0.016 0.545 0.001 0.645 0.685 0.658 0.010 0.090
Branches 1
)
1
%NDFF
N (mg g
)
%NDFF
11.5 11.0 10.2
8.98 9.08 8.64
4.5 4.9 5.1
7.98 7.68 7.38
11.1a 11.8b 11.7ab 11.1a 9.9c 9.1d
8.48c 8.50c 8.91bc 9.11ab 9.14ab 9.44a
7.0a 5.8b 5.0c 4.7c 4.1d 2.5e
8.30a 7.65b 7.69b 7.54b 7.35b 7.54b
Probabilities highlighted in bold are significant at P 0.05. nt, not testable due to imbalance in number of age classes. Means followed by the same letters (a,b,c) are not significantly different at P = 0.05 by Tukey’s test.
The N concentrations for stem wood and bark samples were highest at the top of the tree and lowest below the crown, and lower in the wood than in the bark (Table 5). The %NDFF in stem wood and bark followed a similar trend except that whorl 6 and 9 samples, that grew after the urea were applied, had similar levels. Bark had higher %NDFF levels than wood at whorl 15 and in samples taken from below this height. 3.2. Nitrogen recovery in the trees Ten years after the urea was applied 14.5% of the applied-N was recovered in the trees. There were no significant treatment differences in aboveground biomass, N content or fertilizer recovery (Tables 6 and 7). Foliage contained 41% of the labelledN recovered in the trees (excluding fine roots), whereas it contained 30% of the N content and made up only 4% of tree biomass. This emphasises the importance of N retranslocation within the tree as well as the biological functions of foliage. Branches, which made up 12% of dry weight, had 28 and 32% of the N and labelled-N, respectively. The stem dominated the weight but contained less labelled-N than either of these crown components. Only 10% of the fertilizer-N in the trees was estimated to be in coarse roots. 3.3. Understory and soil Fine root biomass in both the forest floor and mineral soil sampled 10 years after the treatments were applied was not affected by the timing of fertilizer application (Table 8). The variations for most parameters we measured were high, and in particular the amount of fine roots in the mineral soil appears excessive for the fall application.
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698
Table 5 ANOVA degrees of freedom (d.f.) and probabilities for wood and bark samples for N concentrations and 15N derived from the fertilizer (%NDFF), together with location means Source
d.f.
N (mg g 1 5 5 1 1 1 1 1
0.881 0.001 0.333 0.001 0.001 0.001 0.833 0.674
N (mg g
Biomass (t ha Spring Fall P value
Bark 1
)
%NDFF
N (mg g
0.323 0.001 0.092 0.001 0.541 0.001 0.001 0.753
0.742 0.001 0.474 0.001 0.001 0.001 0.030 0.164
Wood
Means Location Whorl 6 Whorl 9 Whorl 15 Below live crown Mid-bole Breast height
Treatment
Probability Wood
Treat. (T) Location (L) TL Whorl 6 vs. others Whorl 6 vs. whorl 9 Mid vs. lower Whorl 15 vs. blc* mb* vs. bh*
Table 8 Root and understory aboveground biomass in a urea fertilization experiment near Nanaimo, British Columbia, about 10 years after treatment (stand age 49)
1
)
%NDFF 0.506 0.001 0.832 0.001 0.586 0.001 0.254 0.026
)
1.25 1.08 0.46 0.45 0.35 0.33
%NDFF
N (mg g
8.16 8.35 5.46 3.94 2.03 1.93
5.05 4.22 3.45 3.06 1.85 1.61
1
)
Fine root in mineral soil
Salal
Other understory
1.9 (1.16) 1.1 (0.45) 0.562
12.2 (3.01) 39.9 (21.17) 0.264
1.3 (0.55) 2.6 (0.29) 0.110
0.2 (0.12) 0.4 (0.27) 0.500
1
)
Means, with S.E.s in brackets, together with ANOVA treatment probabilities (P).
labelled-N was recovered in understory biomass, fine roots and coarse woody debris, compared to 17% in the LFH and 23% in mineral soil to 40 cm depth. Recoveries of 15N fertilizer in mineral soil and fine roots decreased with depth (Fig. 1), with most of the 15 N remaining found in the LFH and 0–10 cm layers.
Bark 1
Fine root in LFH
%NDFF
3.4. Total recovery of labelled urea At the end of 10 years we were able to account for 60.2 5.25% (mean S.E.) and 58.6 12.0% of the 15N-urea that was applied (Tables 7 and 9) in the spring and fall applications, respectively. Total recovery in the forest ecosystem was not affected by the timing of urea application (P = 0.911).
8.28 8.01 8.32 7.76 5.86 4.71
4. Discussion
Probabilities highlighted in bold are significant at P 0.05. *blc, mb and bh are below live crown, mid-bole and at breast height, respectively.
4.1. Fertilizer-N distribution within the trees Total N contents in kg N ha 1 in any of the components (woody debris, the forest floor, mineral soil, roots in both the forest floor and mineral soil, and understory vegetation) were not affected by the timing of fertilizer application (Table 9). In terms of total fertilizer-N recovery, the only possible difference was with understory vegetation (P = 0.080), which was higher in the fall than in the spring application treatment. Overall, only 5% of the
Branches and foliage had different patterns of %NDFF and total N concentration (Table 4). Branchwood N concentration tended to be higher in lower than in upper crown branches, but on average was highest in current branchwood, although the significant interactions suggest that this oversimplifies the picture. Of greater importance is that %NDFF was highest with upper branchwood and that current branchwood had a higher level than 2–6-year-old
Table 6 Douglas-fir biomass and N content, by components and treatment, at stand age 49 years, together with standard errors (in parentheses) and ANOVA treatment probabilities (P) Foliage Biomass (t ha 1) Control Urea spring Urea fall Mean P value N content (kg ha Control Urea spring Urea fall Mean P value
1
Branches
Stem bark
Stem wood
Aboveground
Coarse roots
9 (1.3) 13 (1.1) 11 (1.1) 11.1 0.135
29 (4.4) 41 (3.6) 36 (3.6) 35.3 0.181
21 (3.2) 31 (2.6) 27 (2.6) 26.3 0.163
142 (21.0) 205 (17.2) 177 (17.2) 174.5 0.163
201 (29.7) 290 (24.3) 250 (24.3) 247.3 0.162
42 60 53 51.7 na
95 (18.0) 145 (14.7) 121 (14.7) 120.5 0.189
89 (16.9) 130 (13.8) 117 (13.8) 111.9 0.264
40 (7.6) 59 (6.2) 53 (6.2) 50.7 0.268
51 (11.2) 77 (9.1) 65 (9.1) 64.0 0.282
275 (50.8) 410 (41.5) 356 (41.5) 347.2 0.215
40 58 52 49.7 na
)
na, not appropriate. Table 7 Recovery of applied nitrogen in the trees 10 years after treatment (stand age 49 years) by component and treatment, together with standard errors (in brackets) and ANOVA treatment probabilities (P)
% recovery Spring Fall Mean P value
Foliage
Branch
Stem bark
Stem wood
Aboveground
Coarse roots
Total tree
6.1 (0.57) 5.8 (0.57) 5.9 0.740
4.6 (0.37) 4.6 (0.37) 4.6 0.978
1.5 (0.27) 1.6 (0.27) 1.6 0.796
0.9 (0.09) 0.8 (0.09) 0.8 0.322
13.1 (1.20) 12.8 (1.20) 13.0 0.864
1.5 1.5 1.5 na
14.6 14.3 14.5 na
na, not appropriate.
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699
Table 9 Total N content and recovery of applied-N in woody debris, mineral soil (0–40 cm), fine roots and understory in a urea fertilization experiment near Nanaimo, British Columbia, about 10 years after treatment (stand age 49) Treatment Total N (kg ha Spring Fall P value % recovery Spring Fall P value
Woody debris
LFH
Mineral soil
Roots in LFH
Roots in mineral soil
Understory
Total
15 (4.7) 11 (1.7) 0.396
361 (93.6) 320 (73.4) 0.745
1480 (281.3) 1104 (134.4) 0.294
6 (3.9) 4 (1.6) 0.575
47 (8.6) 112 (48.4) 0.258
10 (4.8) 19 (2.2) 0.189
1920 (206.8) 1568 (242.0) 0.331
1
)
0.43 (0.21) 0.36 (0.09) 0.770
17.8 (4.05) 16.0 (4.55) 0.778
25.0 (9.50) 20.8 (6.50) 0.736
0.27 (0.13) 0.23 (0.09) 0.845
1.8 (0.48) 4.8 (1.67) 0.166
0.5 (0.25) 1.2 (0.15) 0.080
45.8 (5.85) 43.4 (12.40) 0.866
Means, with S.E.s in brackets, together with ANOVA treatment probabilities (P).
branchwood. Crown stem wood and bark also had higher %NDFF compared to the lower bole (Table 5). In contrast, foliage N levels were higher on upper crown branches, and in younger than older foliage (Table 4), while %NDFF was not influenced by branch position in the crown, but was higher in older than young foliage. Mead and Preston (1994) found a similar pattern with foliage N and %NDFF for lodgepole pine sampled 8 years after the fertilizer was applied. These patterns suggest that the higher %NDFF in older foliage largely, but not completely, reflects the levels of 15N enrichment in available N to the tissue when these were formed, whereas the lower total N in old foliage illustrates the retranslocation out of the foliage as it ages. One-year-old needles can take up additional N from the soil or from retranslocation from current needles (Mead and Preston, 1994; Fife and Nambiar, 1984) but these effects are very much smaller for older needles. The %NDFF levels in branches, wood and bark within the crown, particularly that formed since the fertilizer was applied, appear stable, but these data hide the retranslocation that occurs as these tissues die. Woody tissues
largely formed before the fertilizer was applied, such as lower branches and lower bole samples, have lower 15N enrichments. The 15 N enrichments indicate that movement of fertilizer N to those pre-fertilization woody tissues occurred, a finding also supported by Mead and Preston (1994), Hart and Classen (2003) and Elhani et al. (2003). Looking at recently formed foliage, branches, stem wood and bark, the %NDFF values are remarkably similar, being 8.5, 8.3, 8.3 and 8.2%, respectively. This is an indication of the high mobility of N to tissues formed within the same year. Salal had a slightly higher labelling (11.9%) than the minor understory (6.2%) while fine roots from 0 to 10 cm averaged 9.8%. The current %NDFF values in the LFH and in the 0–10 cm of mineral soil are 10.1 and 4.0%, respectively, which ties closely with the current %NDFF levels in the trees and understory. The change of %NDFF with time illustrates the initial pulse of fertilizer N that went into trees, followed by a gradual decline since that time (Fig. 2). The long-term study in lodgepole pine also found a decrease with time in age sequences of foliage taken from either stem or branch needles (Mead and Preston, 1994). In the lodgepole pine study, foliage was retained for 12 years and the highest 15N enrichment was found in needles that were current or 1-year-old at time of fertilization, but older foliage also contained some fertilizer-N. Nason et al. (1990) also found that nitrogen increased in both current and 1-year-old foliage at Nanaimo following the application of urea, and other studies have reported a similar response in foliage existing at the time the N was applied (Heilman et al., 1982; Mead and Pritchett, 1975; Thomas and Mead, 1992). 4.2. Spring vs. fall urea application We found no differences in Douglas-fir stand biomass, N content or fertilizer-N recovery between urea applied in the spring and fall (Tables 6 and 7). The result agrees with Heilman et al.
Fig. 1. Percent of fertilizer-N recoveries in: (a) mineral soil and (b) fine roots by depth. Error bars are standard errors.
Fig. 2. Change in percent nitrogen derived from the fertilizer (%NDFF) with time for current foliage. The fall 1982 and 1983 data are from Nason (1989).
700
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(1982) who found inconsistent differences at 2 years between spring- and fall-applied urea in young stands of Douglas-fir. Nason et al. (1988), in this study, found that the volatilization from the urea applied in the spring was 14% of that applied, compared to 0.7% for fall-applied urea. However, they also found that some of this volatilized ammonia was able to be recaptured by Douglas-fir seedlings, so the percentage lost to the ecosystem might have been smaller. Nevertheless, samples of 1-year-old foliage taken 11 and 15 weeks after the fertilizers were applied had significantly higher %NDFF for fall-applied (16%) than for springapplied urea (12%) (Nason, 1989). Heilman et al. (1982) also found higher %NDFF levels in 1-year-old foliage when N was applied in the fall. In the first 2 years the fertilizer-N in the soil was also higher in the fall than in the spring treatment (Nason et al., 1988; Nason, 1989). In the first 3 weeks, the application in the fall was followed by 195 mm of throughfall compared to 6 mm for the spring application. This resulted in less volatilization in the fall application and greater movement of fertilizer-N from the organic horizons down into the mineral soil (Nason et al., 1988). Taken together, this information suggests that the fall application may have resulted in slightly more fertilizer-N being available to plants, but this was not detectable 10 years later. Based on the initial needle N concentrations (around 11 mg g 1 in the fall) and the site index (27 m at 50 years) (Table 2; Nason et al., 1990) a growth response would have been expected on this site (Brix, 1983; Hopmans and Chappell, 1994; Carter et al., 1998). Furthermore, Nason et al. (1990) found that N concentration in current foliage was increased by about 19%. However, like tree biomass measurements (Table 6), tree volume measurements did not detect a significant response to urea fertilizers (Van den Driessche, pers. comm.). There are several explanations for this apparent non-response. First, the volume response could have been missed as tree form was not measured (Bevege, 1984). Second, the experiment had low replication which may have made detection of a response difficult (Miller et al., 1986). Further the stand had not been recently thinned and this reduces the likelihood of a response (Ballard, 1984). Finally, the response to a single fertilization generally declines within 5–7 years (Brix, 1983; Carter et al., 1998), and may even become negative in the longer term, due to the influence of other limiting nutrients or water (Pettersson and Ho¨gbom, 2004). 4.3. Labelled-urea recovery over time A total of 59.1% (averaged across the spring vs. fall applications; Tables 7 and 9) of the applied-N was recovered some 10 years after the N was applied. This is the same as that recovered after 8 years in a lodgepole pine stand in interior British Columbia (Preston and Mead, 1994). In the lodgepole experiment the total recovery was 61.6% for the urea treatment and 60.7% for the 15NH4NO3 treatment. While the tree recovery was higher in this Douglasfir stand than in the lodgepole pine stand (14.5 compared to 8.4%, respectively) the tree recovery is typical of many studies (Preston et al., 1990). Most of the fertilizer N after 10 years was in the LFH and mineral soil which accounted for almost 40% of that applied. Again this is very similar to the lodgepole pine experiment where 33% was recovered in soil within the plot, plus another 8% outside the treated area (Preston and Mead, 1994). The lodgepole pine experiment used single-tree plots that were much smaller than what was used in this experiment, necessitating an estimate of N outside the plot boundary. The uptake into fine roots and understory was also roughly the same in the two experiments. About a year after the treatments were applied (averaged for the two treatments made at eight sampling dates between 28 and 105 weeks after application), Nason (1989) found that there was
25.4% of the labelled-N in the LFH and 31.6% in the mineral soil layers, or a total of 57.0% in the soil. This had decreased over the 9 years to 16.9 and 22.9% in the LFH and mineral soil, respectively, giving a total soil recovery of 39.8% (Table 9). The loss of labelled-N from the mineral soils was equivalent to 3.0% per year. In the lodgepole pine experiment in interior British Columbia, soil organic 15N decreased by 48% over 7 years (a decrease of 7% per year, Preston and Mead, 1994), indicating higher mineralization rates than in the current study. The decrease of labelled-N in the LFH layer was initially very high immediately following the urea applications but after the first year averaged 3.7% per year. This rate of loss from the LFH layer is similar to that found after 3 years when 15N-labelled, dry Douglasfir needles were added to the forest floor (Preston and Mead, 1995). The loss rate in that experiment was 48% in the first year, 15% per year over the next 2 years and 1.9% per year between years 3 and 7.5. The differences could be the result of a number of factors: for example, climatic differences, restriction on rooting in the litter decomposition study, and 15N-recycling in litterfall occurring in the current study. In our study, there would have been some recycling of 15N through litterfall but, while it was not measured directly, it would have been relatively small. Using information given by Mitchell et al. (1996) on litterfall in the fertilized-thinned treatment in Douglas-fir at Shawnigan Lake, together with measurements of 15N enrichments soon after the fertilizer was applied (Fig. 2), the labelled-N in litterfall over the 10 years would be about 3.5% of that applied. This was equivalent to 24 and 20% of the N recovered in the trees and LFH layer after 10 years, respectively. However, the results of both experiments indicated that stabilization of 15N in increasingly recalcitrant forms occurred over time; the incorporation of fertilizer 15N into stable soil organic matter fractions such as the humin fraction was found to be very fast in a forest soil in the Pacific Northwest (Chang and Preston, 1998). The great ability of the soil to immobilize and retain the added N has been demonstrated in 15N studies of conventional N fertilization (Mead and Pritchett, 1975; Heilman et al., 1982; Preston and Mead, 1994; Chang and Preston, 1998), and N fixation (Kaye et al., 2002), as well as in studies that simulated elevated atmospheric N deposition (Buchmann et al., 1996; Nadelhoffer et al., 2004; Holub and Lajtha, 2004); in most situations soil organic matter is the dominant sink of applied-N up to the decade-long timescales that have been studied. Work in an old-growth temperate evergreen mixed-angiosperm forest in southern Chile indicates that the transformation of applied inorganic N was dominated by rapid assimilation and turnover through microbial biomass in the short term (weeks), and transfer from microbial biomass into nitrogen-conserving plant (and to a lesser extent soil organic matter) pools in the long term (years) (Perakis and Hedin, 2001). Such processes (whether the soil or plant biomass is the main sink for the applied-N) result in efficient long-term retention of nitrogen in forest ecosystems, with the bulk of residual fertilizer N generally found in the organic and upper mineral horizons, in both short- and longer-term studies (e.g., Mead and Pritchett, 1975; Noˆmmik and Larsson, 1989; Preston and Mead, 1994). The uptake into coarse roots should be considered indicative as they were not excavated or sampled during the study. However, the estimated recovery was similar to those found in large roots in slash (Pinus elliottii var. elliottii) and lodgepole pine (Mead and Pritchett, 1975; Preston and Mead, 1994). Heilman et al. (1982) found higher recoveries in young Douglas-fir stands but these included fine as well as coarse roots. In our study Douglas-fir fine roots (<4 mm) were not differentiated from understory roots. Fertilizer-N uptake and storage in the root system and in aboveground biomass accounted for the decrease in soil 15N,
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resulting in little changes in total fertilizer-N recovery in the ecosystem over time. 5. Conclusions There have been few long-term studies using 15N to track fertilizer-N recovery. Our 10-year recovery of 15N-labelled urea demonstrated that 15N enrichment in plants and soil was still quite adequate for analysis. While the original reports by Nason (1989) and Nason et al. (1988, 1990) described some short-term effects of fall vs. spring urea application, we found no long-term effects on either stand productivity or fertilizer use efficiency, suggesting that if fertilization is properly done, timing of fertilization is not a critical issue in decision making in terms of maximizing fertilizer use efficiency for the coastal Douglas-fir forest we studied. While complete short-term recovery data were not available, our results are consistent with many previous studies indicating that fertilizer N is largely taken up in the first growing season, and that tissue 15N remains mobile and can be transferred to new growth. Our results and Nason (1989) show that after both 1 and 10 years, the highest proportion of 15N was recovered in the soil, mainly in the humus and 0–10 cm mineral soil. Between 1 and 10 years after fertilization, mineral soil 15N was lost at an average rate of 3.0% per year, but it appears that there was little further uptake by trees. This study again highlights the high capacity of temperate forest ecosystems such as this coastal Douglas-fir forest to retain externally applied inorganic N over the long term, the importance of maximizing nitrogen uptake in the first year, and also the continuing need to develop new approaches to overcome the generally low efficiency of forest N fertilization. Acknowledgements We would like to thank Ted Nason for helpful discussions and MacMillan Bloedel for allowing and encouraging us to sample their experiment and making available their growth data on the plots. We greatly appreciate the outstanding field and laboratory efforts of Kevin McCullough. Dr. Woo-Jung Choi (Chonnam National University, Republic of Korea) assisted with some of the calculations of 15N recoveries in the soil and understory vegetation. References Ballard, R., 1984. Fertilization of plantations. In: Bowen, G.D., Nambiar, E.K.S. (Eds.), Nutrition of Plantation Forests. Academic Press, London, pp. 327–360, 516 pp. Bevege, D.I., 1984. Wood yield and quality in relation to tree nutrition. In: Bowen, G.D., Nambiar, E.K.S. (Eds.), Nutrition of Plantation Forests. Academic Press, London, pp. 293–326, 516 pp, pp. 293–326. Brix, H., 1983. Effects of thinning and nitrogen fertilization on growth of Douglasfir: relative contribution of foliage quantity and efficiency. Can. J. Forest Res. 13, 167–175. Buchmann, N., Gebauer, G., Schulze, E.-D., 1996. Partitioning of 15N-labeled ammonium and nitrate among soil, litter, below- and above-ground biomass of trees and understory in a 15-year-old Picea abies plantation. Biogeochemistry 33, 1– 23. Carter, R.E., McWilliams, E.R.G., Klinka, K., 1998. Predicting response of coastal Douglas-fir to fertilizer treatments. Forest Ecol. Manage. 107, 275–289. Chang, S.X., Preston, C.M., 1998. Incorporation and extractability of residual 15N in a coniferous forest soil. Soil Biol. Biochem. 30, 1023–1031. Chang, S.X., Preston, C.M., 2000. Understorey competition affects tree growth and fate of fertilizer-applied 15N in a Coastal British Columbia plantation forest: 6year results. Can. J. Forest Res. 30, 1379–1388. Chang, S.X., Preston, C.M., McCullough, K., Weetman, G.F., Barker, J., 1996. Effect of understory competition on distribution and recovery of 15N applied to a
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