The detrital input and removal treatment (DIRT) network: Insights into soil carbon stabilization
Graphical abstract
Introduction
Globally, soils contain more than three times more carbon than the atmosphere, and four and a half times more carbon than the world's biota (Lal, 2004). Despite their importance, however, soil carbon stocks have been reduced through land use change and unsustainable forest management practices (Lal, 2004; Vagen et al., 2005). It has been proposed that management efforts to increase forest productivity can result in increased C storage within living forest biomass and thereby slow the rate of atmospheric CO2 increase (Pan et al., 2011; Post et al., 2012). Forest fertilization studies have shown that forest growth, and hence biomass carbon pools, can be increased as a result of active management (e.g. Chen et al., 2011a; Harrington et al., 2001). Elevated plant inputs to soils associated with higher primary productivity should lead to increased C inputs to soils, which could, in turn, lead to increased C storage in SOM. As such, forest managers are increasingly pressed to manage existing forests in ways that will increase soil carbon storage (Lal, 2005; Post et al., 2012). However, the extent to which forests can be manipulated to enhance C sequestration in soil remains unclear (Jandl et al., 2007; Schöning et al., 2013). Sources of carbon that may potentially be sequestered in soils, and long-term controls of carbon stability in soils are poorly understood (Marín-Spiotta et al., 2014; Schmidt et al., 2011; von Lützow et al., 2006, von Lützow et al., 2008).
Many factors affect SOM carbon accumulation and stabilization, including mineralogy and soil aggregation (Rasmussen et al., 2005; Torn et al., 1997; Spielvogel et al., 2008), land use and forest harvest (Yanai et al., 2003; Nave et al., 2010; Paul et al., 2003; Grandy and Robertson, 2007), and climate (Craine et al., 2010; Fissore et al., 2008; Giardina et al., 2014). Although forest type and vegetation strongly influence biomass carbon balance, the direct role of plant litter inputs on SOM C status is less well known and is neither linearly nor directly linked to rates of input. Due to climate change, net primary productivity (NPP) and thus litterfall are predicted to change in many ecosystems (Melillo et al., 1993; King et al., 1997; Raich et al., 2006), but it is not clear whether parallel changes in SOM stores will accompany changes in NPP. Models of ecosystem C balance generally assume a strong relationship among NPP, litter inputs, and soil C accumulation (Liski et al., 2002; Gottschalk et al., 2012), but there is little direct experimental evidence for these relationships. Net accumulation needs to consider the balance between aboveground (litterfall, throughfall) and belowground (root turnover, exudation of organic compounds from roots) plant detrital inputs and outputs (soil respiration, aqueous loss during leaching, physical loss via erosion).
Numerous factors contribute to non-linear relationships between litter inputs and soil C sequestration. Soils have finite capacities to sequester C and eventually become saturated (Chung et al., 2008; Stewart et al., 2009; Six et al., 2002; Mayzelle et al., 2014), effectively decoupling litter inputs and C accumulation rates; saturation levels might be more dependent on climate and soil mineralogy than on the biochemical composition and quantity of C inputs. Furthermore, additions of simple and complex organic detrital substrates to soil can increase turnover rates of native SOM, a process known as the ‘priming effect’ (Kuzyakov et al., 2000). Enhanced microbial respiration in response to additional plant litter inputs or increased rhizodeposition could lead to destabilization of stored SOM, paradoxically decreasing soil C sequestration.
Litter quality has often been suggested as a driver of potential accumulation rates of SOM (e.g. Berg and Meentemeyer, 2002). Litter constituents are structurally and functionally variable, ranging from soluble low molecular weight organic compounds that decompose rapidly (e.g. sugars), to complex organic compounds (structural and defensive compounds) that are relatively resistant to microbial processing (Berg and McClaugherty, 2007). Hence, litter is often described by its biochemical decomposability, and is thus quantified by a set or sets of properties meant to characterize the ease by which carbon and nitrogen within SOM can be mineralized (Bosatta and Ågren, 1999; Rovira et al., 2008; Aber et al., 1990; Talbot et al., 2012). However, such indices speak more to the decomposability of litter, and less to the dynamics and retention of C within SOM- the end product of litter and root tissue decomposition. Increasingly it is recognized that chemical interactions between SOM and mineral soil particles play perhaps the most significant role in C retention; clay surfaces and aluminum and iron oxides stabilize organic matter, and physical protection within soil aggregates decreases accessibility to microbes (Sollins et al., 1996; von Lützow et al., 2006; Marschner et al., 2008; Schmidt et al., 2011). However, in response to altered environmental conditions, SOM quality can change even if total SOM content does not (Feng et al., 2008; Feng et al., 2010; Simpson and Simpson, 2012).
The Detrital Input and Removal Treatment (DIRT) Project assesses the role of plant detritus input amounts and quality on the accumulation and dynamics of organic matter in forest soils. DIRT uses an experimental approach of chronically adding aboveground litter, excluding litter, and preventing root ingrowth to long-term experimental plots to assess the importance of plant detrital sources and loading rates on SOM formation and accumulation or loss. The prototype for the DIRT network was established in 1956 by Francis Hole in the University of Wisconsin Arboretum in two forest and two prairie sites (here referred to as WISC), where the manipulations included doubling and removal of aboveground litter inputs annually (Nielsen and Hole, 1963; Nadelhoffer and Fry, 1988; Lajtha et al., 2014b) (Fig. 1). The current DIRT network protocol includes doubled aboveground litter inputs (Double Litter), Double Wood, root exclusion by trenching (No Root), No (aboveground) Litter via screening, and complete litter and root exclusion (No Inputs) (Table 1). The Harvard Forest, MA, site (HF) was established in 1990 in a transition/mixed hardwood-forest dominated by Northern red oak (Quercus borealis Michx. F.), red maple (Acer rubrum L.), and paper birch (Betula payrifera Marsh.). The Bousson Experimental Forest, PA, site (BEF) was established in 1991 in a mixed deciduous stand dominated by black cherry (Prunus serotina hrh.) and sugar maple (Acer saccharum Marshall), with American beech (Fagus grandifolia Ehrh.) and red oak (Quercus rubra L.) constituting most of the remainder. The H.J. Andrews, OR, site (HJA) was established in 1997 in a mid-growth conifer forest dominated by western hemlock (Tsuga heterophylla (Rafinesque) Sargent) and Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco). The Síkfőkút forest site in Hungary (SIK) was established in 2000 in a dry oak forest (Fekete et al., 2014; Kotroczó et al., 2014), and a site in Germany (SK) was established in a beech/oak forest in 1999 (Klotzbücher et al., 2013). A DIRT site that was crossed with an N fertilization experiment was established at the University of Michigan Biological Station (UMBS) in 2004 in a dry deciduous forest that is dominated by bigtooth aspen (Populus grandidentata Michx.), and secondarily by red maple (Acer rubrum L.), red oak (Quercus rubra L.), paper birch (Betula paperifera Marsh.), eastern white pine (Pinus strobus L.), sugar maple (Acer saccharum Marsh.), American beech (Fagus grandifolia Ehrh.), and trembling aspen (Populus tremuloides Michx.). More recently, DIRT sites were established in grassland/shrub systems in the Santa Rita Experimental Range and Wildlife Area, AZ (SRER) and in the Reynolds Creek Experimental Watershed, ID (RCEW), both in 2013.
Here we synthesize research in the international DIRT network and show how the DIRT network has contributed to understanding of the role of both above- and belowground plant inputs to soil carbon stabilization and destabilization, as well as the likelihood of increased productivity in mature forests contributing to enhanced soil C sequestration.
Responses of total soil C and density fractions to detrital manipulation: SOM resilience.
Soil carbon content is expected to change in response to detrital manipulation only gradually with time, thus our collections were timed at 5 and 10 year intervals, with major sampling efforts made at decadal anniversaries. Density fractionation (Sollins et al., 2009) to identify free particulate, labile vs. mineral-associated SOM pools has also been measured at decadal intervals.
Because most models of soil organic matter composition assume a direct relationship between litter inputs and soil C accumulation (Gottschalk et al., 2012), we initially predicted that treatments with litter additions (Double Litter and Double Wood) would show relatively rapid increases in surface soil C content and that treatments with litter removals (No Litter, No Roots, No Inputs) would show similar decreases in surface soil C content. Indeed, the trajectory of C concentration from the original DIRT site in Wisconsin clearly exhibited this pattern, although the first analyses of soils were not done until 28 years after the experiment began (Lajtha et al., 2014b; Fig. 2). However, analyses from the other forested DIRT sites that were sampled within the first 20 years showed little response to Doubled Litter inputs, and in fact showed remarkably similar trends of slight, but not significant decreases in both C concentration and total profile C content (Fig. 3). We were surprised that even after 20 years, density fractionation data also showed little to no increase in free light fraction material with litter additions (Lajtha et al., 2014a, Lajtha et al., 2014b; Klotzbücher et al., 2013). However, all sites showed significant decreases in surface soil C concentration with litter removals. In contrast to reports suggesting that root-derived C is preferentially stabilized over aboveground inputs (Rasse et al., 2005; Bird et al., 2008), aboveground litter exclusion had an effect on C levels similar to that of root exclusion, thus we did not see evidence that root-derived C is more critical to soil C sequestration. Across sites, in fact, aboveground litter exclusion had a slightly greater negative effect, although not significantly so at any site, than root exclusion.
Section snippets
Soil respiration
Soil respiration, or CO2 released from soil into the atmosphere, includes CO2 released during microbial decomposition of soil organic matter, and CO2 respired by live roots and soil fauna. Over the last two decades, important insights have been gained in understanding both biotic and abiotic factors that control soil respiration, which is a critical controller of SOM stocks, given that the rate of SOM accumulation depends on a balance between inputs and outputs. Recognizing that soil
Priming: the DIRT perspective
Soil priming, defined as the accelerated decomposition of existing SOM in response to increased litter inputs, is an interaction between the live and dead components of the soil ecosystem, specifically the living soil microbial community and dead soil organic matter (SOM) (Kuzyakov, 2010; Cheng et al., 2014). Generally, priming is a sequence of soil processes initiated by elevated litter inputs that result in increased microbial biomass, higher respiration, and greater extracellular enzyme
Conclusions and the Future of DIRT
Numerous factors influence the quantity and quality of SOM inputs, outputs, and storage (Fig. 7), thus soil carbon pools in forests may not respond linearly or immediately to aboveground or belowground litter inputs. Aboveground and belowground inputs have different biochemical characteristics, and can operate at different time scales. Multiple factors influence both the rates and quality, as well as relative proportion of inputs, as well. On the output side, SOM losses can be gaseous,
Acknowledgements
MJS thanks the Natural Sciences and Engineering Research Council (NSERC) of Canada for funding via a Discovery Grant (#2015-05760) and a Discovery Accelerator Supplement (#478038-15). The Canada Foundation for Innovation, Ontario Research Fund, and University of Toronto are thanked for support of the Environmental NMR Centre. KL was supported by NSF grants 0817064 and 1257032. RDB thanks the Shanbrom and Wells foundations, and Sam Reese and numerous Allegheny College undergraduates for
References (91)
- et al.
13C and 15N stabilization dynamics in soil organic matter fractions during needle and fine root decomposition
Org. Geochem.
(2008) - et al.
Model of apparent and real priming effects: linking microbial activity with soil organic matter decomposition
Soil Biol. Biochem.
(2010) - et al.
Soil organic matter quality interpreted thermodynamically
Soil Biol. Biochem.
(1999) - et al.
Carbon dioxide and methane fluxes by a forest soil under laboratory-controlled moisture and temperature conditions
Soil Biol. Biochem.
(1998) - et al.
Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation
Soil Biol. Biochem.
(2006) - et al.
Effects of temperature and moisture on carbon respired from decomposing woody roots
For. Ecol. Manag.
(2000) - et al.
Increased coniferous needle inputs accelerate decomposition of soil carbon in an old-growth forest
For. Ecol. Manag.
(2009) - et al.
Alterations in forest detritus input influence soil carbon concentration and soil respiration in a Central-European deciduous forest
Soil Biol. Biochem.
(2014) - et al.
Multi-year convergence of biometric and meteorological estimates of forest carbon storage
Agric. For. Meteorol.
(2008) - et al.
Assessing the role of fine roots in carbon and nutrient cycling
TREE
(1993)
How strongly can forest management influence soil carbon sequestration?
Geoderma
Soil enzyme activity in response to long-term organic matter manipulation
Soil Biol. Biochem.
Priming effects: interactions between living and dead organic matter
Soil Biol. Biochem.
Review of mechanisms and quantification of priming effects
Soil Biol. Biochem.
Forest soils and carbon sequestration
For. Ecol. Manag.
Increasing carbon stocks in the forest soils of western Europe
For. Ecol. Manag.
Harvest impacts on soil carbon storage in temperate forests
For. Ecol. Manag.
Predicted change in soil carbon following afforestation or reforestation, and analysis of controlling factors by linking a C accounting model (CAMFor) to models of forest growth (3PG), litter decomposition (GENDEC) and soil C turnover (RothC)
For. Ecol. Manag.
Changes in litter properties during decomposition: a study by differential thermogravimetry and scanning calorimetry
Soil Biol. Biochem.
Drought decreases soil enzyme activity in a Mediterranean Quercus ilex (L.) forest
Soil Biol. Biochem.
Stabilization and destabilization of soil organic matter: mechanisms and controls
Geoderma
Soil carbon saturation: implications for measurable carbon pool dynamics in long-term incubations
Soil Biol. Biochem.
Long-term litter manipulation alters soil organic matter turnover in a temperate deciduous forest
Sci. Total Environ.
Predicting long-term patterns of mass loss, nitrogen dynamics, and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems
Can. J. Bot.
Plant Litter: Decomposition, Humus Formation, Carbon Sequestration
Litter quality in a north European transect versus carbon storage potential
Plant Soil
Temperature-associated increases in the global soil respiration record
Nature
A global relationship between the heterotrophic and autotrophic components of soil respiration?
Glob. Chang. Biol.
Contributions of aboveground litter, belowground litter, and root respiration to total soil respiration in a temperate mixed hardwood forest
Can. J. For. Res.
Litter input controls on soil carbon in a temperate deciduous forest
Soil Sci. Soc. Am. J.
Modeling to discern nitrogen fertilization impacts on carbon sequestration in a Pacific Northwest Douglas-fir forest in the first-postfertilization year
Glob. Chang. Biol.
Relationships between carbon allocation and partitioning of soil respiration across world mature forests
Plant Ecol.
Synthesis and modeling perspectives of rhizosphere priming
New Phytol.
Indications for soil carbon saturation in a temperate agroecosystem
Soil Sci. Soc. Am. J.
Widespread coupling between the rate and temperature sensitivity of organic matter decay
Nat. Geosci.
Sources of plant-derived carbon and stability of organic matter in soil: implications for global change
Glob. Chang. Biol.
Temperature sensitivity of soil carbon decomposition and feedbacks to climate change
Nature
Rhizosphere priming: a nutrient perspective
Front. Microbiol.
Variability of organic matter inputs affects soil moisture and soil biological parameters in a European detritus manipulation experiment
Ecosystems
Increased cuticular carbon sequestration and lignin oxidation in response to soil warming
Nat. Geosci.
Altered microbial community structure and organic matter composition under elevated CO2 and N fertilization in the duke forest
Glob. Chang. Biol.
Temperature and vegetation effects on soil organic carbon quality along a forested mean annual temperature gradient in North America
Glob. Chang. Biol.
Carbon input to soil may decrease soil carbon content
Ecol. Lett.
Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests
Biogeochemistry Letters
Warming-related increases in soil CO2 efflux are explained by increased below-ground carbon flux
Nat. Clim. Chang.
Cited by (108)
Plant roots are more strongly linked to microorganisms in leaf litter rather than in soil across tropical land-use systems
2024, Soil Biology and BiochemistryEffects of litter and root inputs on soil CH<inf>4</inf> uptake rates and associated microbial abundances in natural temperature subalpine forests
2024, Science of the Total EnvironmentImpacts of aboveground litter and belowground roots on soil greenhouse gas emissions: Evidence from a DIRT experiment in a pine plantation
2023, Agricultural and Forest Meteorology