Global Change Biology (2015) 21, 3169–3180, doi: 10.1111/gcb.12904
Anthropogenic nitrogen deposition enhances carbon sequestration in boreal soils NADIA I. MAAROUFI1, ANNIKA NORDIN2, NILES J. HASSELQUIST1, LISBET H. BACH3, K R I S T I N P A L M Q V I S T 3 and M I C H A E L J . G U N D A L E 1 1 Department of Forest Ecology and Management, Swedish University of Agricultural Sciences (SLU), Ume a SE-901, Sweden, 2 Ume a Plant Science Center (UPSC), Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Ume a SE-901 83, Sweden, 3Department of Ecology and Environmental Science (EMG), Ume a University, Ume a SE-901 87, Sweden
Abstract It is proposed that carbon (C) sequestration in response to reactive nitrogen (Nr) deposition in boreal forests accounts for a large portion of the terrestrial sink for anthropogenic CO2 emissions. While studies have helped clarify the magnitude by which Nr deposition enhances C sequestration by forest vegetation, there remains a paucity of long-term experimental studies evaluating how soil C pools respond. We conducted a long-term experiment, maintained since 1996, consisting of three N addition levels (0, 12.5, and 50 kg N ha1 yr1) in the boreal zone of northern Sweden to understand how atmospheric Nr deposition affects soil C accumulation, soil microbial communities, and soil respiration. We hypothesized that soil C sequestration will increase, and soil microbial biomass and soil respiration will decrease, with disproportionately large changes expected compared to low levels of N addition. Our data showed that the low N addition treatment caused a non-significant increase in the organic horizon C pool of ~15% and a significant increase of ~30% in response to the high N treatment relative to the control. The relationship between C sequestration and N addition in the organic horizon was linear, with a slope of 10 kg C kg1 N. We also found a concomitant decrease in total microbial and fungal biomasses and a ~11% reduction in soil respiration in response to the high N treatment. Our data complement previous data from the same study system describing aboveground C sequestration, indicating a total ecosystem sequestration rate of 26 kg C kg1 N. These estimates are far lower than suggested by some previous modeling studies, and thus will help improve and validate current modeling efforts aimed at separating the effect of multiple global change factors on the C balance of the boreal region. Keywords: boreal forest, boreal soil, carbon sequestration, carbon sink, nitrogen deposition, soil C pool, soil respiration Received 15 December 2014 and accepted 4 February 2015
Introduction During the past century, anthropogenic activities such as the production and use of nitrogen (N) fertilizers and the combustion of fossil fuels have greatly increased the quantity of reactive nitrogen (Nr) released into the atmosphere, which subsequently enters the biosphere via deposition (IPCC, 2013). Many ecosystems in cold climate regions, such as boreal forests, are strongly N limited due to low rates of biological N2 fixation and slow soil mineralization rates (Tamm, 1991; Vitousek & Howarth, 1991; Lindo et al., 2013). Thus, increased inputs of anthropogenically derived Nr (NHx and NOy) have the potential to enhance productivity and carbon (C) sequestration in these systems (De Vries et al., 2006; Gruber & Galloway, 2008; Schlesinger, 2009; De Vries, 2014; Fern andez-Martınez et al., 2014). In the last decade, several studies have focused on quantifyCorrespondence: Nadia I. Maaroufi, tel. +46 90 786 86 25, fax +46 90 786 81 63, e-mail:
[email protected]
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ing the ratio of C sequestered per unit N deposition in the northern latitudes to understand the impacts of Nr deposition on the global C cycle. Some modeling and experimental studies have suggested that as much as 500 parts of C are sequestered in plant biomass per unit of N deposition, which would account for a large portion of annual anthropogenic CO2 emissions (Holland et al., 1997; Magnani et al., 2007). In contrast, long-term forest N fertilization experiments have shown that N deposition causes a much lower quantity of C to be sequestered in boreal, temperate, and tropical vegetation, ranging from 5 to 30 parts C per unit of N deposition (H€ ogberg et al., 2006; Hyv€ onen et al., 2008; Pregitzer et al., 2008; Sutton et al., 2008; De Vries et al., 2009, 2014; Gundale et al., 2014a). While these studies help to clarify the magnitude by which Nr deposition enhances C sequestration by forest vegetation, there remains a paucity of studies evaluating whether corresponding changes in soil C pools occur in these ecosystems (H€ ogberg et al., 2006; Pregitzer et al., 2008; De Vries et al., 2014), which is important when predicting 3169
3170 N . I . M A A R O U F I et al. how net ecosystem C balances will respond to Nr deposition. Boreal forest ecosystems cover approximately 15% of terrestrial land surface area and store a substantial quantity of C in its aboveground biomass (88 Pg of C); however, to an even greater extent, they store C belowground (471 Pg of C) (Malhi et al., 1999; Lal, 2005). Therefore, gains or losses of soil C in response to Nr deposition could substantially influence the magnitude to which forest ecosystems in the northern latitudes sequester C (Mack et al., 2004; De Vries et al., 2006; Janssens et al., 2010). The limited number of studies evaluating the long-term impacts of chronic N enrichment on soil C sequestration have shown that Nr enrichment can enhance C storage in both temperate and boreal soils (H€ ogberg et al., 2006; Hyv€ onen et al., 2008; Pregitzer et al., 2008). Pregitzer et al., 2008 showed more C sequestrated in soil than vegetation in northern temperate forest in response to long-term chronic N enrichment, while H€ ogberg et al. (2006) and Hyv€ onen et al. (2008) found the opposite trend with more C sequestrated in vegetation than soil in boreal forests. However, uncertainty remains regarding the magnitude to which Nr deposition enhances C sequestration in soils because previous studies estimating this relationship have applied N at rates several times greater than maximum N deposition rates in each region of study. Furthermore, N addition experiments are often located in areas with high background Nr deposition rates, making it experimentally difficult to isolate the impact of actual Nr deposition (De Vries et al., 2009). While there remains uncertainty regarding the magnitude to which soil C pools change in response to Nr deposition, there also remains uncertainty regarding key mechanisms underlying these changes (Janssens et al., 2010). One of several mechanisms by which Nr deposition is thought to enhance soil C accumulation is by negatively impacting soil microbial biomass, composition, and activity (Treseder, 2008; Janssens et al., 2010). Several studies have shown reductions in microbial biomass and activity to high doses of N fertilizers (50–100 kg N ha1 yr1), with greater decreases in fungal than bacterial biomass (H€ ogberg et al., 2007; Demoling et al., 2008) or a concomitant decrease in both bacterial and fungal biomass (Treseder, 2008; Blasko et al., 2013). Likewise, several studies in temperate and boreal ecosystems have shown that the applications of high doses of N fertilizers (>50 kg N ha1 yr1) can have negative effects on total soil respiration (i.e., autotrophic and heterotrophic combined) (Olsson et al., 2005; Janssens et al., 2010), or a decline in microbial abundance and biomass (Treseder, 2008). Interestingly, recent studies
have shown that relatively low rates of N addition can have contrasting effects relative to higher N doses. For example, several studies have shown that the addition of relatively low quantities of N (20 kg N ha1 yr1) over short timescales can have positive effect on autotrophic soil respiration (including tree root and mycorrhizal fungi components) (Hasselquist et al., 2012), as well as decomposition rates (Allison et al., 2009). These studies highlight that low chronic N addition rates (i.e., 30% on average above 25 kg N ha1 yr1 (MacDonald et al., 2002; De Vries
© 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3169–3180
et al., 2007, 2014; Van der Salm et al., 2007; Dise et al., 2009). The increase in C in the organic horizon was due to the combined effect of a non-significant increase in the O-horizon thickness, bulk density, and C concentration (Fig. S1). They are also consistent with a study by Pregitzer et al. (2008) who showed that 10 years of N fertilization (30 kg N ha1 yr1) increased O-horizon C by 6.9 Mg ha1 in temperate hardwood forests. They are also consistent with a study by Franklin et al. (2003) who used the 14C bomb signature within a 20-year-simulated N addition experiment (30 kg N ha1 yr1) to estimate an increase of approximately 13 Mg soil C ha1 in a boreal forest. Despite the significant increase in O-horizon C in response to N enrichment, we did not detect any response in living root biomass at any depth, or soil C in either of the mineral soil layers. The absence of change in mineral soil C could be the result of several factors, including inherently lower rates of biological activity with potential to be responsive to N compared to the O-horizon (H€ ogberg et al., 2001; Lindahl et al., 2007), greater spatial heterogeneity that may disguise subtle changes in C pool sizes, the predominance of older C that accumulates more slowly and is inherently less responsive (Gleixner, 2013), or the absence of soil fauna capable of redistributing newly produced surface C into the mineral horizons (e.g., anecic earthworms) (Jegou et al., 1998). Contrary to our first hypothesis, we did not find any evidence that the amount of C added per unit N changed with increasing N addition rates. Instead, our data show that the relationship between N enrichment and C sequestration in the O-horizon followed a linear
3176 N . I . M A A R O U F I et al. Table 3 Mean (SE) response of phospholipid fatty acid analysis (PLFA) expressed in lmol PLFA g1 organic matter of the soil organic horizon in 0.1 ha plots treated with 0, 12.5, 50 kg N ha1 yr1 annually for 15 years Nitrogen deposition (kg N ha1 yr1) 0 Total PLFA Bacteria Fungi Fungi: bacteria Gram positive Gram negative Actinomycetes PCA 1 (83.06%) PCA 2 (11.98%)
2.24b 0.66 0.48b 0.74 0.24 0.35 0.13 0.11a 0.01
12.5 0.15 0.05 0.05 0.05 0.02 0.26 0.01 0.06 0.02
1.97ab 0.56 0.42b 0.80 0.21 0.29 0.11 0.03a 0.01
50 0.10 0.06 0.01 0.11 0.02 0.04 0.01 0.02 0.03
1.61a 0.50 0.28a 0.57 0.19 0.25 0.13 0.14b 0.01
0.09 0.04 0.02 0.03 0.01 0.02 0.01 0.03 0.01
F-value
P-value
7.33 2.66 9.84 2.55 1.79 2.88 0.98 10.72 0.26
0.008 0.111 0.003 0.120 0.209 0.095 0.402 0.002 0.778
The F- and P-values were derived from one-factor ANOVA (df = 2, 12) for each variable, and different letters (a or b) next to means which each row indicate differences determined using Student–Newman–Keuls post hoc analyses. The percentage in brackets next to the variables PCA 1 and PCA 2 indicate the percentage of total variation explained by axis 1 and axis 2, respectively. Bold values indicate statistical significance at P < 0.05.
Fig. 3 Total phospholipid fatty acid analysis (PLFA) samples scores from principal component analysis for each N addition levels. Treatments consisted of 0 kg N ha1 yr1;(white circle), 12.5 kg N ha1 yr1; (grey circle), and 50 kg N ha1 yr1; (black square). Small symbols correspond to mean PLFA for each plot, large symbols correspond to mean PLFA per treatment. Bars indicate 95% confidence intervals.
relationship with a slope of 10 kg C sequestered in the soil per kg of N added (Fig. 2). This relationship suggests that even low levels of Nr deposition should promote soil C sequestration, albeit in quantities too small to appear significantly different using ANOVA analysis in our experiment. The estimate of C sequestration derived from our regression is consistent with Hyv€ onen et al. (2008), who estimated on average 11 kg C kg N1 in boreal forest in response to a much higher range of N addition rates (30–200 kg N ha1 yr1) than applied in our study; however, they showed that N addition rates ≤50 kg N ha1 yr1 were more effective
in C accumulation than N addition rates between 50 and 200 kg N ha1 yr1. Our finding is also in the same order of magnitude as evaluated by De Vries et al. (2009), who estimated on average 23 kg C kg N1 after a decade of N fertilization in a northern deciduous forest (Pregitzer et al., 2008). Consistent with our second hypothesis, we found a significant decrease in the total microbial and fungal PLFAs in response to chronic N addition, but only in response to the high N treatment (i.e., 50 kg N ha1 yr1) (Table 3). Although, inconsistent with our second hypothesis, we did not observe a significant reduction in the fungal: bacterial ratio due to a simultaneous non-significant reduction also in bacterial biomass. The decrease in total and fungal PLFA markers we observed corresponded with a significant increase in soil C that accumulated in the high N plots, suggesting that reductions in soil microbial activity likely contributed to this accumulation of C. Several studies have suggested that reduction in fungi in response to N addition may result in a competitive release of r-strategist microbes that are relatively more N-demanding (e.g., bacteria) at the expense of N-conservative microbes less efficient in C assimilation (Andrews & Harris, 1986; Fog, 1988; Agren et al., 2001). However, our data do not support these suggestions, as bacteria showed a non-significant concomitant decline with fungi. This pattern is instead more consistent with suggestions that fungi, and ectomycorrhizal fungi specifically, can have priming affects that can enhance soil saprotrophs, including bacteria, through the production of hyphal exudates and the breakdown of complex carbon substrates (H€ ogberg & H€ ogberg, 2002; Janssens et al., 2010). © 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3169–3180
N I T R O G E N D E P O S I T I O N A N D C A R B O N S E Q U E S T R A T I O N 3177 (a)
(b)
Fig. 4 Soil respiration measured during summer 2013. (a) Data points represent mean ( SE) of all plots (n = 5) at each sampling time. Treatments consisted of 0 kg N ha1 yr1; (white circle), 12.5 kg N ha1 yr1; (grey circle), and 50 kg N ha1 yr1; (black square). (b) Mean (SE) soil respiration averaged across all sampling times. Data were analyzed using a repeated-measures ANOVA, and a post-hoc Bonferoni test was used to compare mean effect of treatments averaged across all times. Different letters (a or b) in sub-panel b indicate significant differences between treatments. Significance at *P < 0.05, and ***P < 0.001, respectively. n.s indicates not significant.
A variety of mechanisms have been proposed to explain the fungal declines in response to N addition. For instance, several studies have suggested that alleviation of N limitation by trees results in reduced belowground C allocation to support mycorrhizae (Haynes & Gower, 1995; H€ ogberg et al., 2010; Kaiser et al., 2010). Soil fungal biomass in boreal forests is often dominated by ectomycorrhizal species (Wallander et al., 2001, 2003), thus reduced belowground tree C allocation in response to N additions may help explain the greater sensitivity of fungi relative to bacteria that we observed in this study. An additional mechanism that may explain the greater sensitivity of fungi relative to bacteria is that nitrate (NO3) has been shown to slow down several fungal lignolytic enzymes, including fungal phenol oxidases and peroxidases of white-rot basidiomycetes (Waldrop & Zak, 2006; Ekberg et al., 2007; Kaiser et al., 2010). This impairment of enzyme activity can reduce the ability of fungi to decompose compounds rich in lignin (e.g., spruce needles), resulting in a reduction in fungal biomass and an increase in soil C (Waldrop et al., 2004), as we observed. Additionally, abiotic stabilization mechanism caused by N addition may also be responsible for the decline of fungal biomass. It has been proposed that added N and high soil organic matter density can interact and produce recalcitrant compounds that are protected from microbial decay (Neff et al., 2002; Swanston et al., 2004), thereby potentially © 2015 John Wiley & Sons Ltd, Global Change Biology, 21, 3169–3180
impacting fungal metabolism. The disproportionately large reduction in fungal biomass relative to microbial biomass we observed emphasizes the need of future research to understand the mechanisms controlling their decline (Litton et al., 2007; Fernandez-Martınez et al., 2014). In support of our third hypothesis, the high N addition treatment caused an approximately 11% decrease in total soil respiration (i.e., autotrophic and heterotrophic combined), which corresponded with the decline in total microbial and fungal biomass we observed. Consistent with our third hypothesis, the impact of the high N treatment was greater than the low N treatment, whereas no significant change occurred for the low N treatment relative to the control (Fig. 3b). The decrease in respiration caused by our high N treatment is substantially lower (~30% lower) than what has previously been reported in other long-term N fertilization studies in boreal forest (Franklin et al., 2003; Olsson et al., 2005), yet these previous studies had much higher N addition rates (60–180 kg N ha1 yr1). This result also contrasts Hasselquist et al. (2012), where relatively low N addition rates (20 kg N ha1 yr1) caused an increase of soil respiration. These discrepancies may be explained by differences in forest age, forest productivity, tree species, and soil characteristics (Pregitzer & Euskirchen, 2004; Hyv€ onen et al., 2008; Thomas et al., 2010).The study by Hasselquist et al. (2012) was carried
3178 N . I . M A A R O U F I et al. out in a relatively young Pinus sylvestris forest where the application of N fertilizer was much shorter (5 years) compared to the current study. Similarly, Bowden et al. (2004) measured soil respiration in temperate forests in response to chronic N additions and found an initial increase of soil respiration, followed by an eventual decrease after more than a decade of chronic N addition. They proposed that the initial increase could be due to an increase in tree productivity that resulted in increased C allocation to roots and mycorrhizae, whereas belowground allocation would eventually decline as tree N limitation gradually decreases. These studies emphasize the value of longterm response data derived from realistic experiments for clarifying the effects of chronic environmental change factors, such as Nr deposition. As such, our long-term data clearly show that N input levels approximating upper level atmospheric N deposition rates in the boreal region are likely to have relatively subtle effects on soil respiration. Our estimates of soil C accumulation in response to simulated chronic Nr deposition have substantial implications for understanding the impacts of Nr deposition on the global C cycle. Boreal forests cover approximately 15% of the terrestrial land surface area, and they serve as a major global C pool and sink, and approximately 2/3 of the C in these systems exists in the soil (Malhi et al., 1999; Lal, 2005; DeLuca & Boisvenue, 2012). Some studies have proposed that C sequestration in response to Nr deposition in boreal and temperate forests accounts for a large portion of the yet unidentified terrestrial sink for anthropogenic CO2 emissions, but in doing so assume C sequestration rates in the range of 200–500 parts C per unit of N deposition (Holland et al., 1997; Magnani et al., 2007; Reay et al., 2008). Modeling the quantitative impacts of Nr deposition on C sequestration in the boreal region has been controversial and remains unresolved due to uncertainty in the magnitude and linearity of the relationship between Nr deposition and C sequestration at the stand level. Our data complements a recent study from the same experimental system describing aboveground C sequestration (Gundale et al., 2014a) and thus provides a complete accounting of C at our experimental system, which is the longest running experiment in the boreal region simulating realistic levels of Nr deposition. The accumulation of 10 kg C kg1 N sequestered in soils reported in this study, and 16 kg C kg1 N sequestered in aboveground biomass (reported in Gundale et al., 2014a,b), result in a total C sequestration rate of 26 kg C kg1 N at our study site. While this rate is likely to vary somewhat among tree species, stand ages, or soil type (Pregitzer & Euskirchen, 2004; Thomas et al., 2010), they are consistent with more recent model
estimates (De Vries et al., 2006, 2014; Mol Dijkstra et al., 2009), as well as previous experimental data using much higher N addition rates (Hyv€ onen et al., 2008; De Vries et al., 2009). As such, our data provide a substantial contribution to the growing consensus that Nr deposition in the boreal region has a relatively minor impact on the global C cycle (Hyv€ onen et al., 2008; Sutton et al., 2008; De Vries et al., 2009; Gundale et al., 2014a,b) than what has previously been proposed (Holland et al., 1997; Magnani et al., 2007).
Acknowledgements We thank Ann Sehlstedt, Agnes V€ appling and Maja Sandstr€ om for assistance with field and laboratory work. We thank Jonatan Klaminder and Cedric L. Meunier for helpful comments on a previous draft of this manuscript. The project was supported by the Center for Environmental Research in Ume a (CMF), the Swedish Research Council (FORMAS) for the project Sustainable Management of Carbon and Nitrogen in Future Forests (NiCaf), the Mistra Future Forests program, and the SLU strong research environment Trees and Crops for the Future (TC4F).
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Supporting Information Additional Supporting Information may be found in the online version of this article: Figure S1 Soil temperature at 5 cm depth measured during summer 2013 (means SE). Table S1 Mean (SE) response of soil parameters to three levels (0, 12.5, and 50 kg N ha1 yr1) of simulated chronic N deposition.
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