- Open Access
Trajectories in nitrogen availability during forest secondary succession: illustrated by foliar δ15N
Ecological Processes volume 11, Article number: 31 (2022)
Forest succession is an important ecological process and has been studied for more than a century. However, changes in nitrogen (N) availability during succession remain unclear as they may lead to either N saturation or N limitation. Here, we propose a conceptual model to illustrate changes in N availability during four stages of secondary succession using the natural abundance of 15N in plant leaves (foliar δ15N). We predicted that N availability would decline in the early stages of succession and then increase in late stages, coinciding with the changes in foliar δ15N, with the inflection point varying in different climate zones. Data on foliar δ15N from 16 succession sequences were synthesized to explore changes in N availability during forest succession.
The compiled data were consistent with the proposed conceptual model. Foliar δ15N in boreal and temperate forests decreased significantly in the first two stages of succession (estimated to last at least 66 years in temperate forests), at a rate of 0.18‰ and 0.38‰ per decade, respectively, and decreased slightly in tropical forests in the first 23 years. Foliar δ15N is projected to increase in later stages in all forests, which is supported by observations in both temperate and tropical forests. The inflection points of N availability when N limitation peaked during succession were different in different climate zones, implying different ecosystem N turnovers.
Our study reconciles the controversies regarding changes in N availability during forest secondary succession. Our findings are also useful for predicting the recovery of N and carbon accumulation during succession. Nonetheless, studies on forest secondary succession using foliar δ15N have thus far been limited, and more research should be conducted to further verify the conceptual model proposed here.
Forests are important terrestrial ecosystems that cover 20% of land area and acts as a pivotal C sink in alleviating global warming (Pan et al. 2011). From 2011 to 2020, the global anthropogenic carbon dioxide (CO2) emissions were 10.6 Pg C yr−1, of which 24% of the emitted CO2 has been sequestered by forests (Friedlingstein et al. 2021). To date, disturbance and land-use change have increased the proportion of secondary forests worldwide. Although secondary forest contributes higher rates of net primary production (NPP) and, therefore, a larger C sink (He et al. 2017; Yang et al. 2011; Zhao et al. 2021), the process of forest recovery after disturbance, i.e., secondary succession, is likely to be limited by nutrient availability.
Nitrogen is a major limiting nutrient that affects primary production (LeBauer and Treseder 2008) and C accumulation (Luo et al. 2004) during secondary succession. Nitrogen availability, defined here as the supply of N relative to the demands of plants and microbes, changes during forest succession and is likely to regulate the progress of other ecosystem processes (McLauchlan et al. 2007; Odum 1969; Vitousek and Reiners 1975). During the early and middle stages of secondary succession, forests recover biomass quickly and C accumulates rapidly, resulting in low soil N supply relative to the plant N demand. In the later stages, forest ecosystems reach a steady state, with net primary production approaching respiration losses. In these stages, net C accumulation rate would be close to zero (Odum 1969; Vitousek and Reiners 1975). Forest ecosystems reach N saturation with higher N leaching and gaseous losses. Vitousek and Reiners (1975) suggested that forest ecosystems would eventually reach an equilibrium stage with N inputs balancing N outputs (Fig. 1). However, changes in N availability during forest development have not been well examined and these conclusions are still tentative. For example, McLauchlan et al. (2007) suggested that N availability gradually decreased in temperate secondary forests of the United States using tree δ15N data. In contrast, Sullivan et al. (2019) noted that N availability in tropical forests showed an upward trend by synthesizing soil and foliar N metrics from 10 tropical forest studies. Furthermore, the inflection point of time in N changes during secondary succession remains unknown.
The lack of consensus on the changes in N during forest succession can be attributed to the following reasons. First, the process of forest succession is slow, especially in colder climate. Forest successions lasting several hundred years are difficult to study (Buma et al. 2017, 2019). Second, parameters for quantifying the changes in N varied in different studies, so direct comparisons are difficult. General parameters include ecosystem N input and output (Oulehle et al. 2021), soil available N (Xiao et al. 2018; Yan et al. 2009), soil mineralization and nitrification rates (Dai et al. 2020; Figueiredo et al. 2019; Fisk et al. 2002), and plant and soil N contents or C/N ratios (Johnson et al. 2001; Yanai et al. 2013). However, ecosystem N budgets require long-term monitoring and repeated sampling, resulting in few data sets thus far. Soil available N and soil mineralization and nitrification rates also have large spatial and temporal heterogeneities. In addition, although plant and soil N contents and C/N ratios can reflect changes in ecosystem N status, they cannot be considered reliable sensitive indicators due to the internal stability strategies of plant nutrients (i.e., stoichiometric homoeostasis) (Wang et al. 2021).
Stable nitrogen isotope ratios (15N:14N, expressed as δ15N values) in foliage or tree rings can provide an integrated index to reveal changes in N status during forest succession (Compton et al. 2007; McLauchlan et al. 2007; McLauchlan and Craine 2012; Poulson et al. 1995; Sullivan et al. 2019). Foliar or tree ring δ15N has been demonstrated to decrease with the decline in N availability (Craine et al. 2009; McLauchlan et al. 2017). McLauchlan et al. (2007) proposed four stages of changes in N availability during forest secondary succession: stage (I) recovery of uptake potential, stage (II) recovery of immobilization, stage (III) equilibration of litter pools, and stage (IV) progressive increase in base cation limitation. Their conceptual model was confirmed by tree ring δ15N data from Mirror Lake in the northeastern United States (McLauchlan et al. 2007). However, this concept has not been well verified by other studies. On the basis of this model and the general patterns of forest development (Odum 1969; Oliver 1980; Vitousek and Reiners 1975), we further propose that foliar δ15N can be used to indicate the change in N availability during forest secondary succession (Fig. 1). In the first stage of forest succession, the soil N supply exceeds plant N demand, i.e., high N availability, with reduced soil N immobilization after forest disturbance and a large fraction of 15N-depleted N lost through nitrification and denitrification. Therefore, foliar δ15N and soil δ15N are relatively high in this stage. Forest recovers biomass quickly and plant N demand increases. Nitrogen availability, N loss and foliar δ15N begin to decrease with forest succession. In the second stage, tree biomass accumulation continues to increase. Meanwhile, soil organic matter accumulates gradually and a portion of soil N is immobilized in organic matter. The soil N supply may be insufficient to meet plant N demands, resulting in a progressive decline in N availability, N loss and foliar δ15N. The third stage is the mature stage with the recovery of soil N immobilization and equilibrium of the soil N pool. The soil N supply exceeds N demand for plant growth, indicating that N availability would increase gradually. During the last successional stage, i.e., the fourth stage, N is no longer the limiting nutrient for plant growth, while base cation limitation increases.
In the present study, we synthesized data on foliar δ15N from succession sequences in different climate zones using “space-for-time” substitutions and examined whether the changes in N availability during forest secondary succession were consistent with the conceptual model proposed above. If the changes in N availability were consistent with the conceptual model, we hypothesized that the inflection point of changes in N availability from the second stage to the third stage would vary in different climate zones. The inflection point of changes in N availability during secondary succession in boreal and temperate forests would take a longer time than that in tropical forests, depending on the ecosystem N turnover.
We collected foliar N content and δ15N data from peer-reviewed literature. From the Web of Science, we used the key words “leaf”, “leaves”, “foliar”, “forest”, “nitrogen stable isotope”, “delta N-15”, “15N natural abundance”, “succession”, “secondary succession”, “development”, and “chronosequence” in different combinations to search targeted publications. Studies related to forest retrogression and primary succession were not considered, and studies that did not collect samples based on forest development time were also excluded from this study. Finally, 14 forest succession sequences from the literature were selected, including 6 tropical forest successions from Sullivan et al. (2019) (detailed information can be found in Additional file 1: Table S1). All studies were of secondary succession, which regenerated after previous disturbances. The “space-for-time” substitutions combined with stable isotope techniques of 15N natural abundance in leaves were used to investigate the changes in N status during secondary succession. We extracted the data from the figures in references using the software “GetData”.
Data were obtained from 2 boreal forests, 4 temperate forests, and 8 tropical forests. The study sites were located from 65.6°N to 56.6°N, 44.6°N to 39.3°N, and 23.2°N to 22.6°S in boreal, temperate, and tropical forests, respectively. The mean annual temperature was − 2 °C to − 1.7 °C, 4.7 °C to 15 °C, and 21.0 °C to 25.8 °C in boreal, temperate, and tropical forests, respectively. Successional durations differed in the studied biomes, with the longest succession history of 350–400 years in boreal and tropical forests versus approximately 150 years in temperate forests. Among all studies, only the tropical Dinghushan (Fang et al. 2008, 2010) in China had slopes of 15° to 35°, and the others were gently sloping. The dominant species varied in different regions and succession stages. The foliar N contents in seven succession sequences were also compiled.
Furthermore, foliar δ15N data from two long-term N addition experiments in Swedish boreal forests were collected. This result could indicate the changes in N availability with forest succession. The Norrliden site was in a Pinus sylvestris forest in northern Sweden (Hasselquist and Hogberg 2014; Högberg et al. 2011). Data from Norrliden are available between 1970 and 2009. The first sampling was when this plantation was 18 years. The Stråsan site (Blaško et al. 2013; Högberg et al. 1992) was located on a steep slope in central Sweden with the dominant species Picea abies. The experiment at Stråsan started in 1967 and lasted for 43 years after sampling in 2009. The locations of the study sites are shown in Fig. 2.
To find the changes in N availability during forest succession, we used an “lm” fitting regression model (package “lme4” in R) to evaluate the variation in foliar δ15N with stand age at each site. For all forest sites, linear regression analysis was first used to analyze the overall trends of foliar δ15N overtime. Then, quadratic regressions were used to explore the temporal pattern with multiple sampling times and two continuous sampling observations of Swedish boreal forests. However, the succession sequences with only two or three available time points were not used for quadratic equations due to insufficient sampling.
For all “space-for-time” substitution sequences, linear regression analysis was performed in N content with succession. For two continuous sampling observation of Swedish boreal forests, quadratic regression fitting was used to assess the temporal pattern in N content with succession.
The changes in N availability with forest successions in different climate regions were also analyzed. To minimize differences in isotope ratios induced by variations in regions, sites, climate and species, foliar δ15N data were standardized relative to the average value of the first 50 years since succession. Then quadratic regression was used to assess the temporal pattern of normalized foliar δ15N with forest succession.
The piecewise linear regression function in the “segmented” package was also used for each individual succession sequence and the three climate regions to find the time inflection point of changes in foliar δ15N. Data were analyzed statistically in R (4.0.3).
Foliar δ15N and N contents with forest succession by continuous observation at the same site
To date, foliar δ15N has been monitored in only two Swedish forests for a long time period. At Norrliden site (Hasselquist and Hogberg 2014; Högberg et al. 2011), the N content in leaves ranged from 0.9 to 1.5% (with an average of 1.2%), and showed a pattern of first decreasing, and then increasing (Additional file 1: Figure S1). The foliar N content varied significantly with succession time (P < 0.05). Foliar δ15N decreased significantly with forest succession. The values decreased from 0.4‰ to −3.1‰, with an average rate of decline of 0.93‰ per decade (Fig. 3).
At Stråsan site (Blaško et al. 2013; Högberg et al. 1992), the foliar δ15N was generally lower than that at Norrliden, ranging from −0.9‰ to −4.7‰. As at Norrliden, the foliar δ15N at Stråsan declined over the measurement period. The foliar δ15N in Stråsan forest decreased rapidly in the first 35 years, by an average of 1.5‰ per decade. However, the foliar δ15N increased significantly in the following 20 years from −4.7‰ to −3.6 ‰ (Fig. 3). The leaf N content at this site did not change significantly (Additional file 1: Figure S1).
Foliar δ15N and N contents with forest succession by “space-for-time” substitutions
The data sets of foliar δ15N using the “space-for-time” substitutions were synthesized from two boreal, four temperate, and eight tropical forest sequences. The foliar δ15N in three climate regions differed significantly from each other (P < 0.001), with tropical forests having the highest value (2.1 ± 2.3‰), temperate forests having an intermediate value (1.5 ± 2.1‰), and boreal forests having the lowest value (− 4.0 ± 1.4‰) (Fig. 4b). In the same climate region, the foliar δ15N differed significantly among different succession sequences within temperate and tropical forest biomes (Fig. 4a, P < 0.001). However, the foliar δ15N in boreal forest biome was not significantly different (Fig. 4a).
The foliar δ15N in two boreal forest sequences (Hu et al. 2014; Hyodo et al. 2013) decreased at a rate of 0.11‰ and 0.44‰ per decade, respectively, which was a lower rate than that in the two Swedish forests using continuous observations. Further quadratic regression indicated that the foliar δ15N had a slightly shifting trend with succession in boreal forests (Additional file 1: Table S2). The time inflection points of the Alberta and northern Sweden sites were 52 and 123 years after the beginning of succession, respectively, using piecewise linear regressions (Fig. 5).
The foliar δ15N in the four temperate forest sequences (Compton et al. 2007; LeDuc et al. 2013; Li et al. 2013; Wang et al. 2007) also showed a decreasing trend with succession. However, compared with boreal forests, the rate of decline was faster, with an average rate of 0.2‰ to 1.31‰ per decade (on average 0.73‰). Further quadratic regression for the Michigan forest with multiple sampling times and data indicated that the foliar δ15N first decreased and then increased with succession (Additional file 1: Table S2). Through piecewise linear regression analysis, we found that the inflection point appeared in the 36th year (Fig. 5).
Only five succession sequences (Broadbent et al. 2014; Buzzard et al. 2015; Davidson et al. 2007; Gehring et al. 2005; Piccolo et al. 1994) were sampled more than three times in tropical forests, and their temporal patterns were inconsistent. Among these five sites, a similar trend with boreal and temperate forests was found in Molienda, showing a marked decrease with succession. The average rate of decline was 0.32‰ per decade, which was faster than the observed rates in temperate and boreal forests. Piecewise linear regression analysis indicated that the inflection point was in the 22nd year. The foliar δ15N in Santa Rosa showed an increasing trend and subsequently decreased with succession, with the inflection point at the 40th year. The foliar δ15N in other three forests increased significantly with succession (Fig. 5).
The pooled data from each of three climatic regions showed that the foliar δ15N decreased with succession in boreal and temperate forests. The inflection point of foliar δ15N in boreal forest was not found by analyzing data from all of “space-for-time” substitutions and continuous observations. We further assessed the asymptotic point of inflection using a single-exponential model and found that the inflection point from the second to third stage occurred over 350 years (Additional file 1: Figure S2). The inflection point in temperate forests was found in the 66th year, and the foliar δ15N increased with succession. The overall trend in tropical forest succession was indistinct, although it exhibited a slight increase (Fig. 6). The inflection point was found in the 23rd year based on analyses of data less than 100 years in the tropical forest.
Only seven forest successions by the “space-for-time” substitutions in this study reported foliar N content. The foliar N content of the tropical Para and Dinghushan sites increased significantly with succession (P < 0.001). For the other forests, the foliar N content did not change significantly with succession (Additional file 1: Figure S3).
Across all data from forest secondary succession studies, we found no distinct pattern in the foliar N content (Additional file 1: Figure S2). Furthermore, the N content among the different climatic zones did not differ significantly. These results indicated that foliar N content could not be used as a sensitive indicator to reflect N availability. In contrast, temporal patterns of foliar δ15N were clear in 12 of 14 forest succession sequences with relatively complete data. The foliar δ15N in three climate biomes was significantly different, with the maximum value in tropical forest, followed by that in temperate and boreal forests (Fig. 4b), suggesting the differences in N availability. Our results are consistent with those of studies of N availability in boreal (Blaško et al. 2013; Högberg et al. 1992, 2011), temperate (McLauchlan et al. 2007, 2017), and tropical forests (Hietz et al. 2011), and suggest that foliar δ15N can be used as a sensitive indicator to evaluate N availability.
Either by continuous observation at the same site (Fig. 3) or by “space-for-time” substitutions (Figs. 4 and 5), the foliar δ15N in boreal and temperate forests supports our proposed conceptual model, which was consistent with the patterns of tree ring δ15N. For instance, McLauchlan et al. (2007) analyzed the tree ring δ15N of temperate forests at Mirror Lake in the northeastern United States and indicated that δ15N decreased significantly with succession. They then measured δ15N for more tree rings from 49 undisturbed forest sites in the United States and found that tree ring δ15N declined since 1850 (McLauchlan et al. 2017). In addition, the trajectory of tree ring δ15N in the United States since 1970 suggested that N availability gradually decreased, i.e., forests became more N limited. The authors, however, suggested that the potential reason for the decline in N availability was the “fertilization effect” of increasing atmospheric CO2 concentration, enhancing plant growth and thus progressive N limitation (McLauchlan et al. 2017).
Previous studies demonstrated that nitrate (NO3−) concentrations in stream water changed with forest succession by the long-term (continuous decades) monitoring of N loss within the same forest catchments (Bosch and Hewlett 1982; Vitousek et al. 1979), which can be used to reflect the changes in N availability. For example, Bernal et al. (2012) analyzed the related factors affecting the N cycle of the Hubbard Brook Forest in North America, and found that the NO3− concentration of stream water could be influenced by forest logging. They suggested that the NO3− concentration changed with the succession process using the 18-year NO3− record combined model. When tree biomass continues to increase, more N will be needed for tree growth, resulting in a reduction in the NO3− concentration in streams. Tokuchi and Fukushima (2009) carried out a more comprehensive study on the NO3− concentration from 0- to 87-year catchments after afforestation in Japan. They demonstrated that the NO3− concentration of stream water was related to the stand age, namely, the stages of forest succession. In their study, the NO3− concentration increased sharply after cutting, but the NO3− concentration gradually decreased with forest age. When forest was in the mature stage (approximately 25 years), the NO3− concentration was lowest and remained stable for the long term. These results indicated the inflection point of N availability in the Japanese temperate forest, and the value was similar to our results. Furthermore, Lucas et al. (2016) found that the inorganic N concentration in nine different forest watersheds in northern Sweden decreased from 1985 to 2011, as forest biomass accumulation increased over time. Their results suggested that these forests were still under fast growth and needed more N, which was consistent with our results here. In summary, these studies on the NO3− concentration of stream water in forest watersheds agreed with our proposed model, indicating that the N supply is insufficient to meet the N demand for tree growth in the early and middle stages of forest succession, therefore, leading to a declining trend of ecosystem N availability.
Unlike boreal and temperate forests, the foliar δ15N in tropical forest succession exhibited diverse patterns. Among these forests, the foliar δ15N increased with succession in three of five sequences. The reasons for the different patterns remain unclear. One potential reason might be that trees in colder climate zones need a longer time to reach peak growth and maturity than those in the tropics. Conversely, tropical climates are suitable for tree growth, so trees grow fast and reach their prime quickly. Sierra et al. (2021) indicated that it took approximately 30–50 years to mature according to their study on C turnover time in tropical forests. Poorter et al. (2016, 2021) pointed out that the biomass recovery rate reached 85% after 20 years of succession. They suggested that tropical secondary forests probably reached maturity in approximately just over 20 years, which was consistent with our results that the transition of forest status occurred in the 23rd year. However, the rate of soil N turnover in tropical forests differed from that in boreal and temperate forests (Berg et al. 1993). The process of soil N cycling is influenced by climate conditions, vegetation, soil microbial community, soil properties and their interactions. Previous studies have demonstrated that soil organic layers are thicker in boreal and temperate forests than in tropical forests, and there are slower decomposition rates in boreal and temperate forests than in tropical forests (Melillo et al. 1982; Prescott 2010; Vivanco and Austin 2006). This may lead to a large amount of N being immobilized in the organic layer, resulting in the lack of N available for tree growth in boreal and temperate forests (Attiwill and Adams 1993). For example, the results of 15N-tracer experiments in temperate forests have suggested that most added inorganic N was immobilized in the organic layer (Li et al. 2019). In contrast, the fast turnover within the organic layer in tropical forests might release the N retained and facilitate plant N uptake (Giweta 2020). A 15N-tracer study in tropical forest indicated that the organic layer was a short-term sink for N, with most of the N lost after 1 year (Wang et al. 2018).
Our study proposed a conceptual model of N availability during forest succession and explored trajectories of N availability based on foliar δ15N from different forest successions. Our results suggest that although the general patterns of N availability were consistent among different climate regions, the trajectories of N availability were nonlinear. The inflection points of N availability in succession sequences varied among different climate regions. The shifting time from the second stage to the third stage during secondary succession in boreal forests was much longer than that in temperate forests, while the inflection point in tropical forests appeared the earliest. Our findings are useful for predicting the recovery of N and C accumulation during forest succession in the context of future climate change. However, it is worth noting that studies on foliar δ15N during succession are still limited. More studies should be conducted to further confirm the conceptual model we proposed. Nonetheless, our results have reconciled some controversial issues about N availability in different studies.
Availability of data and materials
The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
- CO2 :
Natural abundance of 15N
- NO3 − :
Attiwill PM, Adams MA (1993) Nutrient cycling in forests. New Phytol 124:561–582. https://doi.org/10.1111/j.1469-8137.1993.tb03847.x
Berg B, Berg MP, Bottner P, Box E, Breymeyer A, de Anta RC, Couteaux M, Escudero A, Gallardo A, Kratz W, Madeira M, Mälkönen E, McClaugherty C, Meentemeyer V, Muñoz F, Piussi P, Remacle J, de Santo AV (1993) Litter mass loss rates in pine forests of Europe and Eastern United States: some relationships with climate and litter quality. Biogeochemistry 20:127–159. https://doi.org/10.1007/bf00000785
Bernal S, Hedin LO, Likens GE, Gerber S, Buso DC (2012) Complex response of the forest nitrogen cycle to climate change. Proc Natl Acad Sci USA 109:3406–3411. https://doi.org/10.1073/pnas.1121448109
Blaško R, Högberg P, Bach LH, Högberg MN (2013) Relations among soil microbial community composition, nitrogen turnover, and tree growth in N-loaded and previously N-loaded boreal spruce forest. For Ecol Manag 302:319–328. https://doi.org/10.1016/j.foreco.2013.02.035
Bosch JM, Hewlett JD (1982) A review of catchment experiments to determine the effect of vegetation changes on water yield and evapo-transpiration. J Hydrol 55:3–23. https://doi.org/10.1016/0022-1694(82)90117-2
Broadbent EN, Almeyda Zambrano AM, Asner GP, Soriano M, Field CB, de Souza HR, Pena-Claros M, Adams RI, Dirzo R, Giles L (2014) Integrating stand and soil properties to understand foliar nutrient dynamics during forest succession following slash-and-burn agriculture in the Bolivian Amazon. PLoS One 9:e86042. https://doi.org/10.1371/journal.pone.0086042
Buma B, Bisbing S, Krapek J, Wright G (2017) A foundation of ecology rediscovered: 100 years of succession on the William S. Cooper plots in Glacier Bay, Alaska. Ecology 98:1513–1523. https://doi.org/10.1002/ecy.1848
Buma B, Bisbing SM, Wiles G, Bidlack AL (2019) 100 yr of primary succession highlights stochasticity and competition driving community establishment and stability. Ecology 100:e02885. https://doi.org/10.1002/ecy.2885
Buzzard V, Hulshof CM, Birt T, Violle C, Enquist BJ, Larjavaara M (2015) Re-growing a tropical dry forest: functional plant trait composition and community assembly during succession. Funct Ecol 30:1006–1013. https://doi.org/10.1111/1365-2435.12579
Compton JE, Hooker TD, Perakis SS (2007) Ecosystem N distribution and δ15N during a century of forest regrowth after agricultural abandonment. Ecosystems 10:1197–1208. https://doi.org/10.1007/s10021-007-9087-y
Craine JM, Elmore AJ, Aidar MP, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Penuelas J, Reich PB, Schuur EA, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–992. https://doi.org/10.1111/j.1469-8137.2009.02917.x
Dai W, Bai E, Li W, Jiang P, Dai G, Zheng X (2020) Predicting plant-soil N cycling and soil N2O emissions in a Chinese old-growth temperate forest under global changes: uncertainty and implications. Soil Ecol Lett 2:73–82. https://doi.org/10.1007/s42832-020-0021-y
Davidson EA, de Carvalho CJ, Figueira AM, Ishida FY, Ometto JP, Nardoto GB, Saba RT, Hayashi SN, Leal EC, Vieira IC, Martinelli LA (2007) Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447:995–998. https://doi.org/10.1038/nature05900
Fang YT, Gundersen P, Mo JM, Zhu WX (2008) Input and output of dissolved organic and inorganic nitrogen in subtropical forests of South China under high air pollution. Biogeosciences 5:339–352. https://doi.org/10.5194/bg-5-339-2008
Fang H, Yu G, Cheng S, Zhu T, Zheng J, Mo J, Yan J, Luo Y (2010) Nitrogen-15 signals of leaf-litter-soil continuum as a possible indicator of ecosystem nitrogen saturation by forest succession and N loads. Biogeochemistry 102:251–263. https://doi.org/10.1007/s10533-010-9438-1
Figueiredo V, Enrich-Prast A, Rutting T (2019) Evolution of nitrogen cycling in regrowing Amazonian rainforest. Sci Rep 9:8538. https://doi.org/10.1038/s41598-019-43963-4
Fisk MC, Zak DR, Crow TR (2002) Nitrogen storage and cycling in old- and second-growth northern hardwood forests. Ecology 83:73–87. https://doi.org/10.1890/0012-9658(2002)083[0073:Nsacio]2.0.Co;2
Friedlingstein P, Jones MW, O’Sullivan M, Andrew RM, Bakker DCE, Hauck J, Le Quéré C, Peters GP, Peters W, Pongratz J, Sitch S, Canadell JG, Ciais P, Jackson RB, Alin SR, Anthoni P, Bates NR, Becker M, Bellouin N, Bopp L, Chau TTT, Chevallier F, Chini LP, Cronin M, Currie KI, Decharme B, Djeutchouang L, Dou X, Evans W, Feely RA, Feng L, Gasser T, Gilfillan D, Gkritzalis T, Grassi G, Gregor L, Gruber N, Gürses Ö, Harris I, Houghton RA, Hurtt GC, Iida Y, Ilyina T, Luijkx IT, Jain AK, Jones SD, Kato E, Kennedy D, Klein Goldewijk K, Knauer J, Korsbakken JI, Körtzinger A, Landschützer P, Lauvset SK, Lefèvre N, Lienert S, Liu J, Marland G, McGuire PC, Melton JR, Munro DR, Nabel JEMS, Nakaoka SI, Niwa Y, Ono T, Pierrot D, Poulter B, Rehder G, Resplandy L, Robertson E, Rödenbeck C, Rosan TM, Schwinger J, Schwingshackl C, Séférian R, Sutton AJ, Sweeney C, Tanhua T, Tans PP, Tian H, Tilbrook B, Tubiello F, van der Werf G, Vuichard N, Wada C, Wanninkhof R, Watson A, Willis D, Wiltshire AJ, Yuan W, Yue C, Yue X, Zaehle S, Zeng J (2021) Global carbon budget 2021. Earth Syst Sci Data Discuss 2021:1–191. https://doi.org/10.5194/essd-2021-386
Gehring C, Vlek PLG, de Souza LAG, Denich M (2005) Biological nitrogen fixation in secondary regrowth and mature rainforest of central Amazonia. Agr Ecosyst Environ 111:237–252. https://doi.org/10.1016/j.agee.2005.06.009
Giweta M (2020) Role of litter production and its decomposition, and factors affecting the processes in a tropical forest ecosystem: a review. J Ecol Environ 44:81–89. https://doi.org/10.1186/s41610-020-0151-2
Hasselquist NJ, Högberg P (2014) Dosage and duration effects of nitrogen additions on ectomycorrhizal sporocarp production and functioning: an example from two N-limited boreal forests. Ecol Evol 4:3015–3026. https://doi.org/10.1002/ece3.1145
He NP, Wen D, Zhu JX, Tang XL, Xu L, Zhang L, Hu HF, Huang M, Yu GR (2017) Vegetation carbon sequestration in Chinese forests from 2010 to 2050. Glob Chang Biol 23:1575–1584. https://doi.org/10.1111/gcb.13479
Hietz P, Turner BL, Wanek W, Richter A, Nock CA, Wright SJ (2011) Long-term change in the nitrogen cycle of tropical forests. Science 334:664–666. https://doi.org/10.1126/science.1211979
Högberg P, Tamm CO, Högberg M (1992) Variations in 15N abundance in a forest fertilization trial-critical loads of N, N-saturation, contamination and effects of revitalization fertilization. Plant Soil 142:211–219. https://doi.org/10.1007/Bf00010967
Högberg P, Johannisson C, Yarwood S, Callesen I, Nasholm T, Myrold DD, Högberg MN (2011) Recovery of ectomycorrhiza after ‘nitrogen saturation’ of a conifer forest. New Phytol 189:515–525. https://doi.org/10.1111/j.1469-8137.2010.03485.x
Hu YL, Yan ER, Choi WJ, Salifu F, Tan X, Chen ZC, Zeng DH, Chang SX (2014) Soil nitrification and foliar δ15N declined with stand age in trembling aspen and jack pine forests in northern Alberta, Canada. Plant Soil 376:399–409. https://doi.org/10.1007/s11104-013-1994-4
Hyodo F, Kusaka S, Wardle DA, Nilsson MC (2013) Changes in stable nitrogen and carbon isotope ratios of plants and soil across a boreal forest fire chronosequence. Plant Soil 367:111–119. https://doi.org/10.1007/s11104-013-1667-3
Johnson CM, Vieira ICG, Zarin DJ, Frizano J, Johnson AH (2001) Carbon and nutrient storage in primary and secondary forests in eastern Amazonia. For Ecol Manag 147:245–252. https://doi.org/10.1016/S0378-1127(00)00466-7
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379. https://doi.org/10.1890/06-2057.1
LeDuc SD, Rothstein DE, Yermakov Z, Spaulding SE (2013) Jack pine foliar δ15N indicates shifts in plant nitrogen acquisition after severe wildfire and through forest stand development. Plant Soil 373:955–965. https://doi.org/10.1007/s11104-013-1856-0
Li MC, Zhu JJ, Zhang M, Song LN (2013) Foliar δ15N variations with stand ages in temperate secondary forest ecosystems, Northeast China. Scand J Forest Res 28:428–435. https://doi.org/10.1080/02827581.2012.755563
Li SL, Gurmesa GA, Zhu WX, Gundersen E, Zhang SS, Xi D, Huang SN, Wang A, Zhu FF, Jiang Y, Zhu JJ, Fang YT (2019) Fate of atmospherically deposited NH4+ and NO3- in two temperate forests in China: temporal pattern and redistribution. Ecol Appl 29:.e01920 https://doi.org/10.1002/eap.1920
Lucas RW, Sponseller RA, Gundale MJ, Stendahl J, Fridman J, Hogberg P, Laudon H (2016) Long-term declines in stream and river inorganic nitrogen (N) export correspond to forest change. Ecol Appl 26:545–556. https://doi.org/10.1890/14-2413
Luo Y, Su B, Currie WS, Dukes JS, Finzi AC, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739. https://doi.org/10.1641/0006-3568(2004)054[0731:Pnloer]2.0.Co;2
McLauchlan KK, Craine JM (2012) Species-specific trajectories of nitrogen isotopes in Indiana hardwood forests, USA. Biogeosciences 9:867–874. https://doi.org/10.5194/bg-9-867-2012
McLauchlan KK, Craine JM, Oswald WW, Leavitt PR, Likens GE (2007) Changes in nitrogen cycling during the past century in a northern hardwood forest. Proc Natl Acad Sci USA 104:7466–7470. https://doi.org/10.1073/pnas.0701779104
McLauchlan KK, Gerhart LM, Battles JJ, Craine JM, Elmore AJ, Higuera PE, Mack MC, McNeil BE, Nelson DM, Pederson N, Perakis SS (2017) Centennial-scale reductions in nitrogen availability in temperate forests of the United States. Sci Rep 7:7856. https://doi.org/10.1038/s41598-017-08170-z
Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626. https://doi.org/10.2307/1936780
Odum EP (1969) The strategy of ecosystem development. Science 164:262–270. https://doi.org/10.1126/science.164.3877.262
Oliver CD (1980) Forest development in North America following major disturbances. For Ecol Manag 3:153–168. https://doi.org/10.1016/0378-1127(80)90013-4
Oulehle F, Goodale CL, Evans CD, Chuman T, Hruška J, Krám P, Navrátil T, Tesař M, Ač A, Urban O, Tahovská K (2021) Dissolved and gaseous nitrogen losses in forests controlled by soil nutrient stoichiometry. Environ Res Lett 16:064025. https://doi.org/10.1088/1748-9326/ac007b
Pan YD, Birdsey RA, Fang JY, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG, Ciais P, Jackson RB, Pacala SW, McGuire AD, Piao SL, Rautiainen A, Sitch S, Hayes D (2011) A large and persistent carbon sink in the world’s forests. Science 333:988–993. https://doi.org/10.1126/science.1201609
Piccolo MC, Neill C, Cerri CC (1994) Natural abundance of 15N in soils along forest-to-pasture chronosequences in the Western Brazilian Amazon Basin. Oecologia 99:112–117. https://doi.org/10.1007/Bf00317090
Poorter L, Bongers F, Aide TM, Almeyda Zambrano AM, Balvanera P, Becknell JM, Boukili V, Brancalion PHS, Broadbent EN, Chazdon RL, Craven D, de Almeida-Cortez JS, Cabral GAL, de Jong BHJ, Denslow JS, Dent DH, DeWalt SJ, Dupuy JM, Duran SM, Espirito-Santo MM, Fandino MC, Cesar RG, Hall JS, Hernandez-Stefanoni JL, Jakovac CC, Junqueira AB, Kennard D, Letcher SG, Licona JC, Lohbeck M, Marin-Spiotta E, Martinez-Ramos M, Massoca P, Meave JA, Mesquita R, Mora F, Munoz R, Muscarella R, Nunes YRF, Ochoa-Gaona S, de Oliveira AA, Orihuela-Belmonte E, Pena-Claros M, Perez-Garcia EA, Piotto D, Powers JS, Rodriguez-Velazquez J, Romero-Perez IE, Ruiz J, Saldarriaga JG, Sanchez-Azofeifa A, Schwartz NB, Steininger MK, Swenson NG, Toledo M, Uriarte M, van Breugel M, van der Wal H, Veloso MDM, Vester HFM, Vicentini A, Vieira ICG, Bentos TV, Williamson GB, Rozendaal DMA (2016) Biomass resilience of Neotropical secondary forests. Nature 530:211–214. https://doi.org/10.1038/nature16512
Poorter L, Craven D, Jakovac CC, van der Sande MT, Amissah L, Bongers F, Chazdon RL, Farrior CE, Kambach S, Meave JA, Munoz R, Norden N, Ruger N, van Breugel M, Almeyda Zambrano AM, Amani B, Andrade JL, Brancalion PHS, Broadbent EN, de Foresta H, Dent DH, Derroire G, DeWalt SJ, Dupuy JM, Duran SM, Fantini AC, Finegan B, Hernandez-Jaramillo A, Hernandez-Stefanoni JL, Hietz P, Junqueira AB, N’Dja JK, Letcher SG, Lohbeck M, Lopez-Camacho R, Martinez-Ramos M, Melo FPL, Mora F, Muller SC, N’Guessan AE, Oberleitner F, Ortiz-Malavassi E, Perez-Garcia EA, Pinho BX, Piotto D, Powers JS, Rodriguez-Buritica S, Rozendaal DMA, Ruiz J, Tabarelli M, Teixeira HM, de Sa V, Barretto Sampaio E, van der Wal H, Villa PM, Fernandes GW, Santos BA, Aguilar-Cano J, de Almeida-Cortez JS, Alvarez-Davila E, Arreola-Villa F, Balvanera P, Becknell JM, Cabral GAL, Castellanos-Castro C, de Jong BHJ, Nieto JE, Espirito-Santo MM, Fandino MC, Garcia H, Garcia-Villalobos D, Hall JS, Idarraga A, Jimenez-Montoya J, Kennard D, Marin-Spiotta E, Mesquita R, Nunes YRF, Ochoa-Gaona S, Pena-Claros M, Perez-Cardenas N, Rodriguez-Velazquez J, Villanueva LS, Schwartz NB, Steininger MK, Veloso MDM, Vester HFM, Vieira ICG, Williamson GB, Zanini K, Herault B (2021) Multidimensional tropical forest recovery. Science 374:1370–1376. https://doi.org/10.1126/science.abh3629
Poulson SR, Chamberlain CP, Friedland AJ (1995) Nitrogen isotope variation of tree rings as a potential indicator of environmental change. Chem Geol 125:307–315. https://doi.org/10.1016/0009-2541(95)00097-6
Prescott CE (2010) Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochemistry 101:133–149. https://doi.org/10.1007/s10533-010-9439-0
Sierra CA, Estupinan-Suarez LM, Chanca I (2021) The fate and transit time of carbon in a tropical forest. J Ecol 109:2845–2855. https://doi.org/10.1111/1365-2745.13723
Sullivan BW, Nifong RL, Nasto MK, Alvarez-Clare S, Dencker CM, Soper FM, Shoemaker KT, Ishida FY, Zaragoza-Castells J, Davidson EA, Cleveland CC (2019) Biogeochemical recuperation of lowland tropical forest during succession. Ecology 100:e02641. https://doi.org/10.1002/ecy.2641
Tokuchi N, Fukushima K (2009) Long-term influence of stream water chemistry in Japanese cedar plantation after clear-cutting using the forest rotation in central Japan. For Ecol Manag 257:1768–1775. https://doi.org/10.1016/j.foreco.2009.01.035
Vitousek PM, Reiners WA (1975) Ecosystem succession and nutrient retention: a hypothesis. Bioscience 25(6):376–381. https://doi.org/10.2307/1297148
Vitousek PM, Gosz JR, Grier CC, Melillo JM, Reiners WA, Todd RL (1979) Nitrate losses from disturbed ecosystems. Science 204:469–474. https://doi.org/10.1126/science.204.4392.469
Vivanco L, Austin AT (2006) Intrinsic effects of species on leaf litter and root decomposition: a comparison of temperate grasses from North and South America. Oecologia 150:97–107. https://doi.org/10.1007/s00442-006-0495-z
Wang L, Shaner P-JL, Macko S (2007) Foliar δ15N patterns along successional gradients at plant community and species levels. Geophys Res Lett 34:L16403. https://doi.org/10.1029/2007gl030722
Wang A, Zhu W, Gundersen P, Phillips OL, Chen D, Fang Y (2018) Fates of atmospheric deposited nitrogen in an Asian tropical primary forest. For Ecol Manag 411:213–222. https://doi.org/10.1016/j.foreco.2018.01.029
Wang K, Wang GG, Song LN, Zhang RS, Yan T, Li YH (2021) Linkages between nutrient resorption and ecological stoichiometry and homeostasis along a chronosequence of Mongolian pine plantations. Front Plant Sci 12:692683. https://doi.org/10.3389/fpls.2021.692683
Xiao KC, Li DJ, Wen L, Yang LQ, Luo P, Chen H, Wang KL (2018) Dynamics of soil nitrogen availability during post-agricultural succession in a karst region, southwest China. Geoderma 314:184–189. https://doi.org/10.1016/j.geoderma.2017.11.018
Yan ER, Wang XH, Guo M, Zhong Q, Zhou W, Li YF (2009) Temporal patterns of net soil N mineralization and nitrification through secondary succession in the subtropical forests of eastern China. Plant Soil 320:181–194. https://doi.org/10.1007/s11104-008-9883-y
Yanai RD, Vadeboncoeur MA, Hamburg SP, Arthur MA, Fuss CB, Groffinan PM, Siccama TG, Driscoll CT (2013) From missing source to missing sink: long-term changes in the nitrogen budget of a northern hardwood forest. Environ Sci Technol 47:11440–11448. https://doi.org/10.1021/es4025723
Yang Y, Luo Y, Finzi AC (2011) Carbon and nitrogen dynamics during forest stand development: a global synthesis. New Phytol 190:977–989. https://doi.org/10.1111/j.1469-8137.2011.03645.x
Zhao M, Yang J, Zhao N, Xiao X, Yue T, Wilson JP (2021) Estimation of the relative contributions of forest areal expansion and growth to China’s forest stand biomass carbon sequestration from 1977 to 2018. J Environ Manage 300:113757. https://doi.org/10.1016/j.jenvman.2021.113757
We thank Kai Huang, Haoming Yu, and Tao Sun for their help in data analysis.
The work was jointly supported by National Key Research and Development Program of China (No. 2016YFA0600802), K.C. Wong Education Foundation (GJTD-2018–07), Liaoning Vitalization Talents Program (XLYC1902016) and the National Natural Science Foundation of China (41773094 and 31901134).
Ethics approval and consent to participate
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Tu, Y., Wang, A., Zhu, F. et al. Trajectories in nitrogen availability during forest secondary succession: illustrated by foliar δ15N. Ecol Process 11, 31 (2022). https://doi.org/10.1186/s13717-022-00374-0
- Foliar δ15N
- Forest secondary succession
- Nitrogen availability
- Space-for-time substitution