Soil heterotrophic respiration: Measuring and modeling seasonal variation and silvicultural impacts
Graphical abstract
Introduction
Every year, soil respiration (Rs) releases 6–7 times more carbon dioxide (CO2) into the atmosphere than anthropogenic CO2 emissions (Rustad et al., 2000, Le Quéré et al., 2013). Soil respiration includes two components: autotrophic root respiration (Ra) and heterotrophic respiration (Rh). Ra is the CO2 released by the roots during tree growth while Rh is the CO2 released by microorganisms in the soil (Raich and Nadelhoffer, 1989, Kelting et al., 1998). Soil respiration from forests contribute significantly to global Rs since forests cover approximately 30% of the Earth’s surface. Studies report a wide-range in forest Rs (i.e., 10–90%) that is produced via microbial processes (Hanson et al., 2000, Subke et al., 2006, Bonan, 2008). This variability in estimates may result from the differential sensitivity between Ra and Rh to changes in soil temperature and moisture, as well as to vegetation type, or even partitioning method bias (Subke et al., 2006). Unfortunately, the large variance in measures of Rh proportion limits our ability to accurately estimate components of the forest carbon (C) budget [i.e., net primary productivity (NPP) and net ecosystem productivity (NEP)] and determine whether forests and forest management are mitigating or exacerbating climate change (Maier et al., 2004, Kuzyakov, 2006).
Investigations into the factors that affect Ra and Rh have been performed at the regional or ecosystem level, and a few have specifically examined the vast acreage of managed pine plantations of the southeastern United States (Maier and Kress, 2000, Wiseman and Seiler, 2004, Gough et al., 2005, Tyree et al., 2006, Templeton et al., 2015, McElligot et al., 2016). There are an estimated 13 million hectares of planted pine in the South, which offer many ecological services, including atmospheric C sequestration (Wear and Greis, 2002). Southern forests including managed pine have been shown to be strong C sinks, primarily accumulating C in aboveground biomass and the forest floor, and to a lesser extent mineral soil (Richter et al., 1999). However, pine plantations and forests in general also release a substantial amount of CO2, most of which is via Rs (Tyree et al., 2006). In order to determine the effectiveness of southern forests and pine plantations, in particular, in sequestering atmospheric C, we must know the amount of fixed CO2 that is subsequently lost due to heterotrophic microbial activity in the soil. Furthermore, this heterotrophic proportion of total soil respiration must be quantified as it changes between different physiographic regions, seasons, and silvicultural treatments. These proportions are necessary to accurately determine NEP from NPP, thus helping to estimate the amount of C accumulated by the ecosystem. An understanding of what factors have the greatest influence over Rh and NEP in individual ecosystem types is essential to provide “bottom-up” derived data for large-scale extrapolation (Bond-Lamberty et al., 2016).
The most common silvicultural treatments used to enhance growth (i.e., NPP) in southern pine plantations, in addition to enhanced genetics, are fertilizer and herbicide application (Borders and Bailey, 2001, Jokela et al., 2004). Fertilization, besides increasing aboveground NPP, has been shown to decrease soil microbial biomass C (MBC), increase soil C, and either decrease or not affect Rs (Lee and Jose, 2003, Maier et al., 2004, Rifai et al., 2010, Templeton et al., 2015). Understory vegetation control using herbicide also increases stand level NPP but has also been found to suppress Rs, decrease MBC, as well as decrease soil C (Shan et al., 2001, Li et al., 2004, Busse et al., 2006, Rifai et al., 2010). Additionally, decreases in fine root biomass have been associated with both fertilizer and herbicide application in loblolly pine stands (Colbert et al., 1990, Albaugh et al., 1998, Shan et al., 2001). Quantifying how these physical and chemical changes, particularly fine roots and MBC, may affect Rh and the Rh proportion of Rs at the stand level throughout the year is necessary to better calculate NEP.
Quantitative modeling, including statistical and process models, will be necessary to understand and extrapolate Rh and the Rh proportion of Rs regionally and potentially to other forest ecosystems. Further, using field-based empirical data to parameterize or constrain model estimates can greatly decrease model uncertainty for C flows and stocks (Carbone et al., 2016). The DAYCENT biogeochemical model, as well as its predecessor CENTURY, have been used extensively to model trace gas fluxes, nutrient cycling, and land-use effects on agricultural soils, but have limited practice in forested areas (Del Grosso et al., 2005, Fenn et al., 2008, Kim et al., 2009, van Oijen et al., 2011, Gathany and Burke, 2012, Bonan et al., 2013). Few studies have validated DAYCENT Rs estimates using soil efflux measurements taken at the associated research site being simulated (Kelly et al., 2000, Del Grosso et al., 2005, Yeluripati et al., 2009, Chang et al., 2013). Of these studies, two have directly evaluated Rh estimates (Del Grosso et al., 2005, Chang et al., 2013), and one has included a forested site in the evaluation (Del Grosso et al., 2005). A comparison of predicted Rh proportions versus measurements taken seasonally across multiple sites would provide valuable insight into the ability of DAYCENT to estimate this large and complex C flux under varying forest management scenarios and thus its potential for regional extrapolation.
By providing simultaneous estimates of Rs and Rh across multiple sites over an annual cycle, we can refine C budget estimates, and adjust for changes in Rh due to environmental variables and silvicultural treatments. If certain combinations of variables decrease the Rh proportion of Rs, then we can assume an increase in NEP in that area if NPP inputs stay constant. Alternatively, if Rh remains constant under silvicultural treatments that increase NPP (fertilizer and herbicide), we can also assume an increase in NEP. An increase in NEP means more C is being stored in above or belowground components resulting in increased C sequestration and climate change mitigation. The objectives of this research are: (1) to quantify the Rh proportion of Rs in southern loblolly pine plantations in the Piedmont and Upper Coastal Plain regions under fertilizer and herbicide treatments over an annual cycle, and (2) to validate DAYCENT model predictions of Rs, Rh, and Rh proportion to field measurements.
Section snippets
Study sites
This study was a part of PINEMAP (Pine Integrated Network: Education, Mitigation, and Adaptation Project): a large Southeast US region-wide study investigating climate change adaptation and mitigation in loblolly pine plantations (www.pinemap.org). This specific study utilized six planted loblolly pine experimental sites across the Piedmont and Upper Coastal Plain of Georgia and Alabama (Fig. 1 and Table 1). Treatment plots ranged from 400 to 1000 m2 in size. Each site contained one plot per
Soil responses
Soil physical and chemical characteristics were compared between treatments and regions (Tables S1, S2, and S3). Soil C concentration was ∼32% lower in herbicide plots than control and fertilized (p = 0.03 and 0.005, respectively) in the upper 10 cm, but was not significantly different at deeper depths. Piedmont soils had ∼18% higher C concentrations at 20–50 cm than Coastal Plain soils. Soil N concentration was lower by ∼22% in herbicide plots than control and fertilized (p = 0.03 each) in
Silvicultural and seasonal effects on Rh
In this study, Rs and Rh in control and fertilize plots did not differ statistically. Application of N fertilizer in loblolly pine ecosystems has had contradictory effects on Rs and Rh among previous studies. In a region-wide study across the Southeast, Templeton et al. (2015) found Rh to be negatively affected by high application rates of fertilizer, with no significant changes in Rs. Tyree et al. (2008) also found a decrease in Rh following fertilization of 2 year-old clones with an
Conclusions
Accurate estimates of the Rh proportion of Rs are critical for calculating NEP and discrepancies may lead to substantial under or overestimations of C sequestered by ecosystems. DAYCENT proved to be reasonable for predicting forest NPP and produced expected seasonal patterns in Rs and Rh. However, the model was weak when predicting site-specific Rs, Rh, and particularly the Rh proportion and under predicted NPP on sandy sites. Although process models can generally simulate soil Rs with
Funding
This research was supported, in part, by the Pine Integrated Network: Education, Mitigation, and Adaptation Project (PINEMAP), a Coordinated Agricultural Project funded by the USDA NIFA (Award No. 2011-68002-30185).
Declarations of interest
None.
References (71)
- et al.
A comparison of trenched plot techniques for partitioning soil respiration
Soil Biol. Biochem.
(2011) - et al.
Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest
For. Ecol. Manage.
(2004) - et al.
Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil
Soil Biol. Biochem.
(1985) - et al.
Carbon accumulation in loblolly pine plantations is increased by fertilization across a soil moisture availability gradient
For. Ecol. Manage.
(2018) - et al.
Improved methodology to quantify the temperature sensitivity of the soil heterotrophic respiration in croplands
Geoderma
(2017) - et al.
Empirical and simulated critical loads for nitrogen deposition in California mixed conifer forests
Env. Pollution
(2008) - et al.
The influence of environmental, soil carbon, root, and stand characteristics on soil CO2 efflux in loblolly pine (Pinus taeda L.) plantations located on the South Carolina Coastal Plain
For. Ecol. Manage.
(2004) - et al.
Calibration of process-oriented models
Eco. Modell.
(1995) - et al.
Total carbohydrates of the soil microbial biomass in 0.5 M K2SO4 soil extracts
Soil Biol. Biochem.
(1996) - et al.
Production dynamics of intensively managed loblolly pine stands in the southern United States: a synthesis of seven long-term experiments
For. Ecol. Manage.
(2004)
Estimating root respiration microbial respiration in the rhizosphere, and root-free soil respiration in forest soils
Soil Biol. Biochem.
Sources of CO2 efflux from soil and review of partitioning methods
Soil Biol. Biochem.
Soil respiration, fine root production, and microbial biomass in cottonwood and loblolly pine plantations along a nitrogen fertilization gradient
For. Ecol. Manage.
Microbial biomass and bacterial functional diversity in forest soils: effects of organic matter removal, compaction, and vegetation control
Soil Biol. Biochem.
DAYCENT and its land surface submodel: description and testing
Global Plan. Change
Ecosystem sensitivity to land-surface models and leaf area index
Global Plan. Change
Twenty years of intensive fertilization and competing vegetation suppression in loblolly pine plantations: Impacts on soil C, N, and microbial biomass
Soil Biol. Biochem.
Soil and microbial respiration in a loblolly pine plantation in response to seven years of irrigation and fertilization
For. Ecol. Manage.
Environmental and stand management influences on soil CO2 efflux across the range of loblolly pine
For. Ecol. Manage.
Generating surfaces of daily meteorological variables over large regions of complex terrain
J. Hydrol.
Long-term effects of site preparation and fertilization on total soil CO2 efflux and heterotrophic respiration in a 33-year-old Pinus taeda L. plantation on the wet flats of the Virginia Lower Coastal Plain
For. Ecol. Manage.
A Bayesian framework for model calibration, comparison and analysis: Application to four models for the biogeochemistry of a Norway spruce forest
Ag. For. Meteorol.
An extraction method for measuring soil microbial biomass C
Soil Biol. Biochem.
Soil CO2 efflux across four age classes of plantation loblolly pine (Pinus taeda L.) on the Virginia Piedmont
For. Ecol. Manage.
Bayesian calibration as a tool for initialising the carbon pools of dynamic soil models
Soil Biol. Biochem.
Leaf area and above- and belowground growth responses of loblolly pine to nutrient and water additions
For. Sci.
Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest
Glob. Change Biol.
Site index curves for loblolly pine plantations on cutover site-prepared lands
South. J. Appl. Forest.
Fine root biomass and turnover of two fast-growing poplar genotypes in a short-rotation coppice culture
Plant Soil.
Aluminum
Bulk Density
Forests and climate change: forcings, feedbacks, and the climate benefits of forests
Science
Evaluating litter decomposition in earth system models with long-term litterbag experiments: an example using the Community Land Model version 4 (CLM4)
Glob. Change Biol.
Estimating heterotrophic respiration at large scales: challenges, approaches, and next steps
Ecosphere
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