PLOS | ov Gorenaccess Caton: Des Gupta S, Macken MO (2018) Stal Pate of So Respaton inks Above and Blowgroued Presses along a Brea Aspen Fie Chronosequanc. PLoS ONET1(1) 0165602. co 10137 Vural pone o16S612 tor: Lugar Sohwendenmann, The Unesty of Auclan, NEW ZEALAND Received: une 13,2016 ‘Accepted: Ontober15, 2016 Palblished: November 10,2016, Copyright ©2016 0a Gupta, Macerle Tiss an open access arte itbted ude te terms ofthe Crave Commins Atsuton Liens, hich pris unrestricted use, dstributon, and reproduction nany mei, proved the rial author and source are rte. Data Avalabilty Statement Al leant ta ae vit th pape ands supporting inferno es Funding: This works support bythe Envioomental Research and Resamnation Group (ERRG) of th Canaan Oilsands Noor for esearch and Development (CONRAD) and the National Scene and Ergnering Research Cour of Carat (NSERO) No specif permissions were require forthe ste cations howe, research acts on ese tes were epored tack othe ERRG commie. The funders hac no ‘olin sty design, data colecton and nays, RESEARCH ARTICLE Spatial Patterns of Soil Respiration Links Above and Belowground Processes along a Boreal Aspen Fire Chronosequence Sanatan Das Gupta", M. Derek Mackenzie? 1 Natural Resources Canada, Canadian Forest Service, North Forestry Cente, Edmonton, AB, Canada, 2 Departmentof Renewable Resources, Universit of Alberta, Edmonton AB, Canada * sanatan@ualbera.ca Abstract Fire in boreal ecosystems is known to affect CO, offux from forest soll, which is commoniy termed soil respiration (Rs). However, there is imited information on how fire and recovery from this disturbance affects spatial variation in Rs. The main objective ofthis study was to uantiy the spatial variabilty of Rs over the growing season ina boreal aspen (Popul tre- ‘muloides Mich.) fio chronosequence. The chronasequence included three stands in north- em Alberta; postfire stand (1 year old, PF), a stand at canopy closure (8 years old, CO), and a mature stand (72 years old, MA). Sol respiration, temperature and moisture were ‘measured monthly from May to August using an intensive spatial sampling protocol ‘minimum lag = 2m). Key aboveground and belowground propertios were measured one time at each sampling point. No spatial structure was detected in Rs ofthe PF stand during ‘the peak growing season (June and July), whereas Rs was auto-correlated at a scale of <6 min the CC and MA stands. The PF stand had the lowest mean Rs (4.60 umol C ms") fol lowed by the CC (6.41 umol G ms"), and the MA (7.32 umol C m® s") stand. Forest floor depth was the only aboveground factor that influenced the spatial pattern of Rs in all three stands and was strongest in the PF stand. Enzyme activity and fine root biomass, on the other hand, were the significant belowground factors driving the spatial pattern of sin the CC and MA stands. Persistent joint aboveground and belowground control on Risin the CC and MA stands indicates a tight spatial coupling, which was not observed in the PF stand Overall the current study suggests that fire in the boreal aspen ecosystem alters the spatial structure of Rs and that fine scale heterogeneity develops quickly as stands reach the can- opy closure phase (=10 years). 2, Introduction ‘The boreal ecosystem is the largest terrestrial biome on earth, representing about 25% ofthe global forested area and accounting for 289 Pg of carbon (C) most of which isin the sol [1-3 Wildfire is one of the main drivers of C exchange in these ecosystems. Boreal forests are fire adapted and periodic wildfire causes stand renewal, landscape patchiness, large efflux of C to the atmosphere, large influx of stable C (in the form of black C) tothe soil, and modifies the PLOS ONE |DO1:10.1371jouma pone.0165602 November 10,2016 118‘Spata Patterns of Sol Respiration in Aspen Fire Chronosaquence {ison to pubic, opropaatin af he manus. Competing Interests: Te authors have declared atmo competing rest xt. nutrient biogeochemical cycles [4-8]. CO efflux from soil or soil respiration (Rs) is one of the key ecosystem processes affected by wildfire. Rs is mainly composed of COs efflux from two different sources, vz, (i) autotrophic respiration (Ra), and (i) heterotrophic respiration (Rh). Rais from plant roots, rhizosphere mycorrhizae and living mosses, and Rh i from microbial activity [9]. In-situ soil respiration has been shown to be effective for tracking ecosystem, recovery aller stand replacing disturbance such as wildfire [10] Significant efforts have been devoted to understand the potential sources of variation in Rs in different ecosystems [7, 11-13]. The two main state factors of variation thought to be responsible ae soil temperature and moisture [1416]. However, other soil properties such as ‘organic matter quality, concentration of photosynthates in roots, and enzyme activity are also responsible for some ofthe variation in Rs (17, 18}. Despite technological progress in measur- ing Rs, there are few studies that have actually looked at the spatial variation in Rs as a means of quantifying these other potential sources of variation. Current prediction models are mainly based on the empirical relationship between Rs and soil temperature, which does not reflect the importance of other biotic and abiotic factors driving spatial variability in Rs, and therefore limits the mechanistic understanding ofthe variation in carbon efflux from belowground eco- system [7] In boreal ecosystem the spatial variation in Rs is mostly attributed to forest floor depth (FD) [2, 13, 19}, substrate quality [2], root biomass {12, 20], vegetation type [2,21], and soil temperature and moisture [22-26] Spatial variability in Rs, however, depends on hos of other abiotic and biotic factors such as texture and pore distribution in sol [27] stand structure [21, 28], nutrient availability {29}, microbial dynamics [9, 30-32], and enzyme kinetics [33,34] which all have spatial structure, making space an important component of variability in Rs [35, 36]. Therefore, spatial residuals can be used as a surrogate of unmeasured variables which will enable us to focus more directly on causal relationship between Rs and other factors [37] Moreover, there isa general trend in the spatial Rs studies [2, 28, 38~41}to use either cocti- cient of variation as a measure of spatial variation, or non-spatal least square regression approach for modeling the drivers of Rs, both of which are unable to provide information on spatial extent (i. scale and magnitude) at which driving processes are functioning to create patterns in Rs, and prone to give erroneous parameter fit if datais spatially auto-correlated [42-44]. Detailed spatial characterization of aforementioned factors driving Rs is also neces- sary for predicting CO; efflux at larger scale. This is especially important for boreal ecosystem. where accumulation and turnover rate of soil Cis highly variable [45, 46 Variability in CO. efflux from soil is generally high even within pure stands [21]. Therefore, itis not possible to generalize mechanisms of spatial heterogeneity in Rs across ecosystems having different stand characteristics. The boreal Rs literature [12, 19, 36, 47-51] are heavily focused on COs efflux from coniferous stands, specially black spruce (Picea mariana), and spa- tial processes creating Rs heterogeneity in these stands may not be fully applicable to the stands dominated by broadleaf species (eg. aspen) ‘Wildfire is the main natural disturbance inthe boreal ecosystems, and as important as decomposition in cycling soil C to the atmosphere [7]. Given the importance of wildfire in boreal C balance, its effects on the spatial distribution of Rs have not also been studied ade- quately, which s limiting our understanding of CO> efflux in these ecosystems [48]. Wildfire reorganizes the spatial structure in sol processes by removing above ground organisms and consuming the organic layers [48, 52]. Stand-replacing fie can decrease spatial variability by homogenizing abiotic environmental conditions such as temperature and moisture. However, other factors such as organic matter quality, FD, and vegetation regrowth can also exert sigifi- cant control where temperature and moisture are not limiting [7, 36]. We hypothesized that post fire Rs would have low heterogeneity and large scale spatial patterns but overtime as PLOS ONE |D01-10.1571joumal pone 0165602 Noversber 10,2016 2118‘Spata Patterns of Sol Respiration in Aspen Fire Chronosaquence stands mature and structural complexity is recreated, we expect an increase in heterogeneity and fine scale patterns (Hypothesis 1). We expected to see a seasonal effect, with higher sum- ‘mer spatial variability (ie. fine scale patchiness) than in the spring, Summer is the main grow- ing season with the highest temperatures and precipitation, which should stimulate the major autotrophic and heterotrophic drivers of Rs (Hypothesis 2) [10, 53]. Availablity of moisture and C quality are two major drivers that we expected to have significant influence on post-ire Rs (Hypothesis 3) The PF stand should experience a moisture limitation due to higher tem- peratures caused by the charred forest floor and an open canopy structure [54], along with a high number of aspen suckers and therefore high evapotranspiration. Carbon quality in the PF stand should also influence Rs, and as fire generally deereases soluble C, which isthe energy source for microbial activity [55], we assumed that belowground controls would be stronger than aboveground controls in the PF stand (Hypothesis 4) as the old aboveground structure (eg tree canopies and living stems) was totally consumed by fire and the young regeneration might not have developed a strong enough effect on Rs to be detectable at this early stage of disturbance recovery [7, 54,56, 57. ‘Understanding the mechanisms regulating the development of spatial heterogeneity in Rs with recovery from fie inthe boreal aspen ecosystem is important. Besides deepening our eco- logical understanding, this study can also be used as a benchmark for measuring reclamation success of similar areas disturbed by industrial activity in the region. Data from this research will also be applicable for modeling C cycles in similar boreal ecosystems, as wel as for the study design of any future soil respiration studies inthe area. The specific objectives of this study were: i) to quantify the spatial variation in Rs along a chronosequence of stand develop- ‘ment, if to characterize the seasonal pattern of spatial variation in Rs, and ii) to determine the principal factors controlling the spatial variation in R, Methods Study sites ‘The study was conducted in the Athabasca oil sand region (AOSR) around Fort MeMurray, Alberta, Canada (56" 43" N 111° 21° W). The mean annual temperature inthis region is 0.°C and growing season (May-September) temperature is 133°C. Mean annul precipitation is 418.6 mm, of which 283.4 mm is rain during the growing season [53 Soils in the study area are predominantly Otic Gray Luvisol, sandy loam to silty loans, moderately well drained, and developed from tll and glacilacustrine sediments [59] Taree boreal aspen stands were used to create the studied fie chronosequence, a one year postfire (PE) stand, a9 year old stand at canopy closure (CC), and a 72 year old mature stand (MA). The PF stand was created afer the massive stand replacing fire (Richardson Fire; (60) in 2011. Aspen was the dominant toe species and represented! more than 95% of the basal area in all three sites. The maximum distance between sites was 34 km. The number of aspen suckers in the PF stand was counted 8 230, 000-270, 000 stems/ha. The CC stand had a tree density of 1900 stems/ha and was dif- ferent from the other site in that it had a large amount of coarse woody debris (CWD) on the ground due to deadial. The density in the MA stand was approximately 2150 stems/ha. According tothe ecosite classification of northern Alberta, all the three sites fll under the dt ecosite phase (low-bush cranberry Aw) [61]. Geographic location, fire history and dominant shrub, forb, grass and moss species ofthe study sites are given in Table A in SI File Soil Respiration measurements Sampling and in-situ measurements were carried out in a 50 m x 20 m plot at all the three sites, Plots were selected based on topography, slope, and aspect to make them comparable PLOS ONE |D01-10.1571joumal pone 0165602 Noversber 10,2016 ante‘Spata Patterns of Sol Respiration in Aspen Fire Chronosaquence across the sits. A cyclic spatial sampling protocol with variable intervals [62] was used to cap- ture both the scale and directionality in measured properties (Fig 1). In total 42 sampling points were established along,? transects, within a 1000 m” plot, which ensured a minimum detectable spatial lg of 2.0 m (Fig 1). lntervals between sampling points within each transect were 3, 6and 9 m, and inter-transect intervals were 2 m and 4 m. The sampling orientation was reversed in the mide two transects to capture anisotropy. Respiration collars made of high grade PVC pipe (10 cm internal diameter) were installed at each sampling point Collars were inserted 8 em deep into the soil leaving 2 em above the soil surface to house the respira- tion chamber. Side walls ofthe collars were drilled (3 to S holes) to allow lateral water move- ment. Collars were installed 48 hours prior to respiration measurements to avoid the initial flush of CO, due to ground disturbance. CO; concentration was measured using a portable 75 indicates strong spatial dependence, 25-75 indicates moderate dependence, and < 25 indicates poor or no spatial dependence [71]. Coefficient of variation (CV) was used to measureglobal variation and was calculated by dividing the standard deviation of Rs, sol temperature, and soil moisture by their means, and reported as percentage, Cross-vario- ‘grams were calculated for Rs and the aboveground and belowground variables to examine the scale of spatial relationships. A positive cross-variance indicates spatial association, whereas a negative variance means spatial dissociation, Fitted semi-variogram models were used for ere- ating ordinary krieged maps of Rs, Variogram modeling and krieging interpolation was done using GS+ geostatistic software (V9.0, Gammadesign software), Further details on the semi- variogram models are given in SI File. Factors driving Rs and their seasonal influence in different stands were tested using spatial autoregressive (SAR) models. Both the spatial error (SAR) and spatial lag (SARiq) models PLOS ONE |D01-10.1571joumal pone 0165602 Noversber 10,2016 5/18PLOS | ov ‘Spata Patterns of Sol Respiration in Aspen Fire Chronosaquence were tested, and the one with lowest AIC and highest Ry (adjusted for numberof predictors Jn the model) was selected [72, 7]. SAR analysis was done in R (R development Core Team, 2013) and Geoda, an open source geospatial software [74]. Details on SAR calculation and interpretations are given in S1 File Finally, neway-ANOVA was used to differentiate between soil respirations of different sites in different seasons Tukey HSD post hoc tet («= 0.05), Assumptions of normality and homoscedasticity were tested and transformations were made where necessary [18]. Inc. Chicago, IL, USA). Multiple comparisons were made using, Results Soil respiration (Rs) and aboveground and belowground factors Soil respiration varied among stands (p < 0,01) and seasons (p < 0,000), Post fre stand had the lowest average growing season Rs (4.60 £0.17 umol Cm”) followed by the CC (6:41 £0.28 mol Cm?) and MA stand (7.32 + 0.29 umol C ms"), Lowest early summer (ay) Rs as found inthe CC stand whereas lowest late summer (June-August) Rs was in the DE stand (Table 1. With the measured rate, annual daytime C emission from the forest soil of ‘MA stand during growing season (May-August) was 11.2 Mg C ha’. In the PP and CC stands these values were 7.1 and 8.3 Mg C ha’! respectively. Significant differences were also found in soil temperature and moisture indifferent stands (Table 2). trend of increasing sil tempera- ture was observed in all stands from May to July, but then dropped by August. Soil tempera- ture ranged from 11.4 to 16.1°C inthe PF stand, 69 to 16.1" inthe CC stand, and 75 to 138°C inthe MA stand. A trend of decreasing soil moisture was observed in all the stands except July inthe PF stand. ‘The aboveground and belowground properties also varied (p < 0.10) among the stands (able B in S1 File), The MA stand had the highest MBC, MBN, DOC, Phenol oxidase, Total Total N, FRB, FD, and canopy cover. DOC increased with stand age, but not significantly, ‘while DON was significantly higher inthe PF stand than the CC and MA stands. BR was higher inthe PF stand than the CC stand, but not the MA stand (Table Bin SI File) ‘Table 1. Seasonal mean, coefficient of variation (CV) and variogram parameters of soll respiration (jmol C ms) measured in three boreal aspen stands in northern Alberta slong fire chronosequence. Diferen laters forthe same month in each ste indicate signfcant (p= 0.05) ference among sites, site | Month | Mean‘As(2Se) | Cv(%) | Range(m) | Spatialdependence | Dependenceciass | Model e ter 3.16(0.15)° 204 58 0.86 Strong Spherical | 034 June 6.29,0:38)* 304 >a oss Moderate Exponential 0.45, aly 5.98 (0:30)* 365 3ND : August 3.57 020)* 354 52 0.98 Strong Spherical | 0.21 foc | May 1.82(0.14)° 483 44 os7 ‘Stong Spherical | 028 June 427 (031° a7 56 0.96 Strong Spherical 0.81 aly 7.24(055)° 486 43 oe tong Spherical | 026 August 8.30046) 358 ND - 3.24(0.17)° 342 80 0.95 Strong Exponential | 021 9.23 (051)° 356 40 0.94 Strong Gaussian 0.58 9.40 (0.48)° 328 36 0.98 ‘trong, Spherical | 028 7.39 0.46)° 40 50 099 Strong Gaussian 0.78 lature stand; Rs = Sol respiration; ND =not detected 01:10.1371joumal pone o168622:001 PLOS ONE |D01-10.1571joumal pone 0165602 Noversber 10,2016 rte@-PLOS | ove ‘Spata Patterns of Sol Respiration in Aspen Fire Chronosaquence ‘Table 2. Seasonal mean, coefficient of varlation (CV), and variogram parameters of soil temperature ('C) and soll moisture content (nm ‘sured in three boreal aspen stands in northern Alberta along aire chronosequence. Different eters fore same month in each site indeatesigniicant (p= 0.05 difference among sites. site | Month | Factors | Mean(#SE) CV(%) _Range(m) _ Spatialdependence | Dependenceciass | Model A wwe | may | tST | 18011 64 ND. 7 : : tsm | oz2(or? 265 ND. 7 7 7 une | st 1220148 75 19 ose Moderate Gaussian 0.33, su o2ocon* 23 ND. 7 7 7 July) ST 6019) 4a >28 050 Moderate Linear 024 su o22(oo1y 19 48 0.96 ‘Strong Spherical 022 August | ST 152007)" 29 768 0.86 ‘Strong Gaussian 0.88 sm 0.14(0.003)" 18.5 ND. 7 : 7 7 tec | may [st | 69031 | 289 64 0.99 ‘Strong Gaussian 082 sm 02s(o01y"* 24.7 > 23 o7t Moderate Gaussian 0.73, vue | st) 1617" | 95 223 0.85 ‘Strong, Spherical 0.94 su ozt(oo1* 162 20 0.50 Moderate Gaussian 0.47 wuy st 161012) 48 28 0.80 ‘Strong Gaussian 0.96 su o1s(oo1 256. >23 0.63 Moderate Gaussian 056, August | ST | 1510.10 44 > 23 099 ‘trong Spherical 0.869 SM 0:18(0.004)® 205 36 0.99 ‘Strong Gaussian 042 twa | may | ST 7490.1 152 ND 7 : : sm | o2s(oory’ a7. 328 053 Moderate Linear 082 dune | st “98(a08j® 5.4 >23 067 Mocerate Spherical 076 sm o2a(oory ara 434 059 Moderate Spherical 050, July) ST 138006 1 64 oat ‘Strong Gaussian 052 sm o15,0.008)% 217 ND 7 : - 5 August ST 137(006" 28 65 0.89 Strong Exponential 0.19 su 0.00(0.003) 258 42 099 Strong Gaussian 056, ‘PF « Post fire: CC = Canopy closure; MA = Mature stan: ST = Sol temperature; SM = Soll moisture 010.137 joual pone D1 e8602.002 Spatial variation in Rs, soil temperature and moisture Strong to moderate spatial dependency was observed in Rs soil temperature, soil moisture, as well as other above and belowground properties in all three aspen stands (Vable 1), Global var- jation (CV) in Rs did not follow any specific trend, but generally showed higher value during summer measurements (June and July). Overall, the CC stand had the highest global variation in Rs (35.8-48.6%) (Table 1). A gradual decrease in the global variability of soi temperature was observed in all stands ftom May to August. The global variability of soil moisture aso decreased from May to July in the PF and MA stands and then increased, while no specific trend was found in the OC stand. Soil respiration in the PF stand had a spatial range of 6 m in May and August, but very coarse range (> 23 m) in June and July. The spatial range of Rs in the CC stand varied between 44m (May) to 5.6 m (june) o 4.8 m (July), but no spatial autocorrelation was detected in August (Table 1). Soil respiration in the MA stand had a spatial range < 5 m throughout the growing season except in May (8 m). Seasonal changes in Rs in different stands are also shown, {ninterpolated krieged maps which again are indicating an increase in patchiness with time since last disturbance (Fig). Large scale spatial autocorrelation (2 19 m) was detected for sol temperature inthe PF and CC stands during most ofthe growing season, and soil moisture did not show any detectable PLOS ONE |D01-10.1571joumal pone 0165602 Noversber 10,2016 718PLOS | ov ‘Spata Patterns of Sol Respiration in Aspen Fire Chronosaquence &g copy cre ae Sort Fig 2. Krieged map of soil respiration (umol C ms) showing changes in ciferent growing season. ‘months along a ire chronosequence of boreal aspen stands in northern Alberta 10.1371 aumal pon 16862 g002 spatial autocorrelation except in July in the PF stand (48m) and in Augustin the CC stand G.6m) (Table 2). The MA stand had large scale spatial range (> 23 m) in sol temperature and moisture in the ary growing season which gradually became finer by August (1.2 m) Cross-variogram analysis betwoon Rs and aboveground and belowground variables indi cated some spatial association at ranges smaller than the study area fr al stands (Fig 3). For example, sin the PF stand was spatially associated with total Ca 20m and with FD at 13.6 1m, whereas the CC stand was spatially associated with C enzymes at 7 m and canopy cover at 8 & 1 i i : —— : i Fig 3. Cross-variograms between soil respiration (Rs) and the aboveground and belowground properties. Inthe boreal aspen stands in northern Alberta along a fie chronosequence. (TC » Toll organic C; icrobial Biomass C; Cenz = C mineralzing enzymes; FD = Forest oor depth; Tt 010.171 ural poe 165602.9003 PLOS ONE |DO1:10.1371jouma pone.0165602 November 10,2016 atePLOS | ov Spat Pate o So Respeatinn Aspen Fe Cronotequnca _m, Likewise, Rs in the MA stand w: with canopy cover at 7 m, patially associated with MBC at 9 m, FRB at 42 m, and Spatial regressions Spatial regression models indicated significant spatial and non-spatial control on Rs in all three stands along the fire chronosequence (Table 3), These models explained 18 to 52% of the variation in Rs in all stands. FD and soil moisture were the two most significant predictors of Rs in the PE stand, except in late summer (July) when DOC and DON were the main control- ling factors. Results indicated some aboveground dependency in the CC stand, with FD and aspen sapling density consistently exerting positive control on Rs during the summer season (May to July; Table 3). However, the strongest control came from belowground properties such as enzyme activity and DOC, especially during June to August (Table 3). Soil MBC con- sistently had significant positive control and enzyme activity had mostly negative control on ationships between soll respiration (Rs) and aboveground and below- {ound properties In three boreal aspen stands in northern Alberta along aire chronosequence. ‘Spatial regression models tag | Eror | Log Fp | AC | Rag coef. (2) coett.(A)_Likelihood ‘PF May 0.44 + 0.07* FD-t0.003*CWD-0.002°8R- = 6058) 2071 | GAZ 0.001 | 6949 OF Ho2"sit June | Rs =*1.29 - 0.16*FD-'0.01°CWO-'0.07" FRB 7 004 | 1.05 | 878.0 | 0005 | 11.88 | 090 0.003" DOC-*0,06"Perox-'2.53°SM July | Rs="1.46 + M0,001"DOC + 0.004"8R- "0.007" DON- 7 016 | 3411 | 5.8055, | ooo | 56.23 | 034 to0s"st ‘Aug logAs =0.02 + 0.28" loghD-"0.02"log¢wo- : 008 | 7124 | 426sar | 0.01 | -19449 | 018 0.28°IogPhenol eC May | Re = 70.24 + "0.02" + 0.01"Sapling density : 007 | 5844 | 399, | <0.001 | -o486 | 031 40.23*Bglu-'0.23°Phenol-'0.02" MBCN + '0.01°ST ‘June | Fs =0.26 + 50.03" FD + "'0.04"Sapling density >) feao | 1047 | 846,42 | <0001| 695 | 098 111.29" Balu + 0.05" Perox + "0.002" DOC 11.68°SM July | s="1.0.8+ 10.07°FD + 10,04°Sapling density + : one 885 | 57a3 | <0001) 297 | 040 Ho.14"Perox + 1.62°TN +'0.21°ST ‘Aug _ Fs ="1.60+ 10,09" FD + "0.003"DOC- "7.16*SM z 018 | -1652 | 8.1817 | <0.001 | 41.04 | 0.96 YMA May Rs —70.29 + 0.006°MBN + '0,09°Perox +%0.002"D0C- | 015 | 2494 | a9trs | <0.005) 2494 | 029 40,02"DON-"0.05°TC-70.58°S4t June | Rs =0.25 +0.04°FD + 0.09*FRB + '0.003"DOC + : 001 | 1208 | 624,22 | 0.0001 | 38:18 | 048 12:7°Bglu +'0.14°Phenol-*1.60°SM July Bs =0.12 + 70,00°FD-*0.18°Taist « H0.10°FRB = <018 | 1429 | 475) | 0.0008 | 4458 | 0.40 ,001 MBC + $2.28-Bglu +0.10"Phono}-0.01°BR. ‘Aug is =-2.68 + H¥0,025-Canopy +80.03+FD-"o.16-Taist> | 0.29 334 | 5.96.30 | 00001 1131 | 05e 50,08" FRB + "90.001" MBC "0.09" Perox-*0.07°TC. §9<0.10 $p<0.05 1p 0.005 480.0005 §§p< 0.00005 {PF « Post ke; CC = Canopy closure; MA = Mature stand; MBC = Microbial biomass C (ug q* sol): MBN = Microbial biomass N (Lg @* soll) MBGN = Microbial toN ratio: BF = Basal respiration (ug CO.-C 9” s0i day"); DOG = Dissolved ganic C (ug g" sol) DON = Dissolved organic (ua a” sol); Bglu=6-1.4 glucesidease (nmol soilhour'); Phenol = Phenol Oxidase (nmol soil hour): Perox = Peroxidase (nmol sollhour); TC = Total © (9); TN= Total N (%): FD = Forest floor depth (om): FRB = Fine root biomass kg stem: g stem” in CC); Tas = Distance to nearest tee (cm); (CWO = Coarse woody dobris cover). 60110.1371jouma pone 165602003 PLOS ONE |DO1:10.1371jouma pone.0165602 November 10,2016 ote‘Spata Patterns of Sol Respiration in Aspen Fire Chronosaquence Rs in both PF and CC stands, Spatial relationship between Rs and above and belowground controls were more complex in the MA stand. The most significant aboveground contzol was found during July and August through the effect of FD, canopy cover, and tree distance, and for the latter two this got stronger in August. Among the belowground controlling factors, RB appeared to be the most significant driver of Rs throughout the growing season. Discussion Te rate of Rs found here corroborates previous studies done in boreal aspen forests [25,53 J Russell and Voroney [25] reported an eux of2.27 umol Cm” in May and maximum 9.09 mol Cm" sin July in a 70 years old boreal aspen forest. The corresponding valves in our study were 3.24 and 9.40 in May and July, respectively. The lower Rs in July in the PF stand can be attributed to the decrease in autotrophic respiration due tothe premature defolia- tion of aspen seedings in July caused by ink spot disease a common feature in young aspen stands regenerating from suckers [76]. ‘Mean Rsiin the PF stand was 15% and 37% lower than the CC and MA stands, respectively. Studies performed in pyrogenic ecosystems often report similar elfects of fire on soil espira- tion [77]. Fire can have direct negative effects on Rs ina number of ways including removal of the organic layer, reduction in microbial biomass, and thermal conversion of C to more recal- citrant forms [78] The decrease in Rs inthe PF stands can be attributed o a decrease in auto- trophie respiration, however other factors such as soil moisture and microbial activity have also been found to be important in some studies [79,80], Our results confirm the importance of both above and belowground factors for determining mechanistic control on Rs and its spa- tio-temporal variability Spatial patterns ‘The current study showed that spatial heterogeneity in Rs increased with increasing stand structural complexity and age in boreal aspen stands (Table 1 and Fig 2), Soll respiration in the Cand MA stands had stronger spatially predictable heterogeneity than in the PF stand, ‘which appeared tobe more random, These findings support our frst hypothesis that fine scale heterogeneity in Rs would develop overtime. (ur results and the iterature suggest that th lck of spatial structure in Rs po attributed to lower variability in FD, an open canopy structure, and lower living FRB (2,12, 13]. Although mid growing season Rs had large sale spatial structure in the PF stan, it exh ited fine scale structure in the early and late growing season. At these times, aspen growth was probably limited by environmental and physiological conditions such a low soil temperature in May and defoliation in August This indicates that fire might have created patchiness in het- erotrophic respiration, but homogenized the distribution ofiving FRB and therefore auotco- phic respiration [51,81]. Stand replacing fite usually consumes aboveground living biomass, ‘which causes fine root mortality and decomposition, and recovery can take several years (82, 83). The large scale or non-detectable spatial patterns in sol temperature and soil moisture in the PF stand was expected and isan example ofthe typical spatial structure of these variables in fire disturbed ecosystems with open canopies [84]. The detectable spatial patterns in these ‘arablesin the CC stand, and the medium spatial pattern (< 13 m) in the MA stand indicates, recovery of spatial variability due othe development of above and belowground features such as forest loor, fine root development, and enzyme activity. Soil physical conditions in the postfire environment may indirectly control Rs mainly through the fluctuations in soil tem= perature and moisture. However, such physical control remains significant only fora short fire can be PLOS ONE |D01-10.1571joumal pone 0165602 Noversber 10,2016 10118‘Spata Patterns of Sol Respiration in Aspen Fire Chronosaquence period before vegetation control takes over [85,86]. These findings again support our hypothe- sis that stand-replacing fre can decrease spatial variability in Rs by homogenization of abiotic environmental conditions such as temperature and moisture, and fine scale heterogeneity can develop overtime as stands mature and structural compleaity is recreated. The fine scale spa- tial autocorrelation of Rs in the CC and MA stands might have originated from the fine scale spatial association between sland (eanopy cover, FD, and FRB) and soil microbial atteibutes (Table 1 and Fig 3). In a boreal mixedwood (aspen-black spruce) fire chronosequence, Lavoie and Mack [19] showed a gradual decrease in the scale of spatial variability in soil microbial properties and ED with time since as fire. Seasonal variation Only the MA stand followed our hypothesized trend of fine scale structure in Rsand driving factors during the peak growing months (July and August) (Table 1). This indicates that not only the spatial structure of Rs was disturbed by wildfire, bt thatthe seasonal pattern was also disrupted, and the recovery was not fully established even atthe canopy closure phase. Forest stracturein the CC stand was probably not complex enough to create the hypothesize s sonal trend in Rs, In the boreal ecosystem, post fire development of vertical structure including canopy transition and gap dynamics may take more than 25 to 35 years after stand initiation [87]. Moreover, the large amount of CWD in this stand might have masked the effect exerted by aboveground factors (eg, canopy overlap, understory vegetation, and sapling density) Lee [8] found that all the standing snags had fallen down within 15 years of fire ina boreal aspen stand. This pulse of CWD after fire usually disappears 50-100 years [89, 90] as doesits effect of Rsas evidenced by the MA stand. Spatial controls ‘The spatial pattern in residual error of the Rs regression models were considered in our study through the SAR approach, and therefore the resulting relationships between Rs and predictor variables can be treated as mechanistic [91]. Neither of the measured environmental factors (soil temperature and moisture) appeared as the strongest controlling factor of Rs in any of the stands, However, a significant negative elect of soil moisture was found during the early grow- ing season months in al stands, Such a negative control of moisture could be the residual sig- nature of snow melt High moisture (> 20%) content had an overall negative relationship with Rs, but lower moisture contents did not follow any specific trend (data not shown). The expected positive control of DOC and soil moisture on Rs in the PF stand was only supported. partially (in July) and the relationship appeared to be changing seasonally (negative in early and positive in late growing season) indicating a bimodal control on Rs. The CC stand, ho\ ever, showed such evidence of positive control from DOC. ‘The evaporative demand for mois- ture from the growing vegetation in the PF stand might have increased during the late growing season and created a moisture limited condition which in turn generated a positive feedback between soil moisture and Rs, A high evaporative demand in postfire aspen stand is common and likely to negatively affect belowground C balance in fire prone boreal ecosystem [92]. The negative control of DOC and soil moisture on Rs in the PF during the early growing season can be attributed to the high moisture availability from the spring snow melt; not due to the Jower DOC concentration in sil solution per se [93, 94]. Although a similar seasonal trend in the soil moisture and DOC in postfire stands has been reported by other studies [55, 95, 96], their cumulative effect on the spatial variability in Rs seems unclear and require further investigation. PLOS ONE |D01-10.1571joumal pone 0165602 Noversber 10,2016 18‘Spata Patterns of Sol Respiration in Aspen Fire Chronosaquence Some of the strongest controls on Rs were found from enzyme activity although the rela- tionship was mostly negative in the PF and CC stands, and mostly positive in the MA stand, ‘The negative enzymatic control on Rs might be due to the end product inhibition of € miner- alizing enzymes, Presence of readily available C inhibits C mineralizing enzyme activity [97, 98]. Fire effects in broadleaf forest with low combustibility, as in the case of aspen, has been shown to be responsible for higher input of biodegradable C in soil [78] FD had a significant positive effect on Rs which confirms similar findings from several other studies in boreal ecosystems (2,12, 13]. The forest floor layer including the top 3-5.cm ‘mineral sol isthe most biotic active zone in the boreal ecosystems [99]. Most the of the FRB in boreal ecosystems is found in the organic layer and mineral soil interface, which makes the for- est lor very important regulator of the soil respiration (100. Fire consumed a portion of the organic layer in the PF stand, but the residual organic layer became an important microbial hhub and zone of root proliferation. This zone might have captured thermally altered C sub- strates 101] and this could have initiated the positive feedback to Rs. {A joint aboveground and belowground control on Rs was more evident in the CC and MA stands, FD, sapling density, and enzyme activity showed consistent positive control on Rs in the CC stand throughout the growing season which indicates recovery of spatial coupling in this stand. The MA stand, however, showed the strongest spatial coupling between above sground-belowground variables and Rs (maximum R* 0.52, Table 3) Evidence of such above- sground- belowground spatial coupling has been reported previously in pyrogenic ecosystems for other biogeochemical properties such as nutrient cycling [36], but findings from the cur- rent study suggest that ecosystem processes might share a common regulating mechanism as in the case of Rs; an amalgamative process which represents a cumulative effect of microbi rhizosphere, and root respiration [10]. Soil respiration in the CC and MA stands also had significant negative controls from enzyme activity but only during the early growing season (May). This may suggest that Rs in the pyrogenic boreal ecosystem is not substrate limited in the early growing season, and the concentration of labile C is probably higher than the microbial demand. Significant positive relationship, however, inthe later months, particularly in the CC and MA stands, indicates that there isa biotic demand for C during the peak growing season (June-August). The source of respiration in boreal ecosystems has been shown to be changing from stored C pool inthe early growing season to photosynthetic products in peak growing season [7, 102]. Hogherg etal. [103] emphasized that photosynthates drive the peak to late growing season Rs in boreal ecosystem, and belowground C allocation needs to be considered more than the seasonality in determining the respiratory loss of C, Our findings corroborate these studies from a microbial perspective. Peroxidase enzyme is mainly responsible for degrading recalcitrant and aromatic C structure [104]. gradual late emergence of peroxidase enzyme in the spatial Rs models is probably giving an indication thatthe shift in microbial foraging from labile to more reca {rant organic matter depends on the supply of labile C (97], and in the MA stand it happens ‘much later in the growing season than the young fire disturbed stands due to having a greater supply of labile C. Significant space effect in the Rs of PF stand in May was unexpected, but not surprizing given that the some of the variables important for biogeochemical cycling inthe post fire eco- systems such as charcoal and organic matter quality were not measured directly in our study. The distribution of charcoal can have a significant effect on the spatial variability of biotic properties through its high sorption capacity and porous struetuce (35, 105]. In pyrogenic boreal ecosystems, this might be important during snow melt and the subsequent flush of © and nutrients, Therefore, we assume that charcoal directly affected C mineralization through variable water retention inthe forest floor. Despite having a complex spatial prediction model, PLOS ONE |D01-10.1571joumal pone 0165602 Noversber 10,2016 12118‘Spata Patterns of Sol Respiration in Aspen Fire Chronosaquence a significant space factor was also detected in the lag term ofthe spatial model of August Rs in the MA stand, This indicates that a finer spatial lag would probably be more appropriate for quantifying Rs dependency in this stand. Conclusions Studies on post-fire spatial heterogeneity in Rs in boreal ecosystems are few despite its impor- tance in modeling and predicting future net C exchange. To our knowledge, this is the first study which simultaneously looked at the development of spatial heterogeneity in Rs, both sea~ sonally and along a chronosequence of fire disturbance, and modelled the mechanistic rela- tionships among the driving factors (abiotic, plants and microbes) after considering their spatial autocorrelations. Based on our findings, we conclude that stand-replacing fire has ere~ ated large scale spatial pattern (less spatial variability) in the Rs of boreal aspen ecosystem, and a development of fine scale heterogeneity (more spatial variability) was found along the chron- ‘sequence. ‘The similar spatial structure in Rs and its driving mechanisms in the CC and MA. stands implies a quick recovery in the spatial heterogeneity of Rs within 9 years after fire disturbance. A belowground microbial control on Rs in the PF spatial model suggests a dominance of | heterotrophic contribution. However, the emergence of both autotrophic and heterotrophic factors in the spatial models of the CC and MA stands indicates an established aboveground belowground feedback loop. FD could be used as a prime predictor of Rs in all seasons, how- ever, variable combinations of FRB, enzyme activity, and environmental factors (temperature and moisture) would be required for seasonal prediction and process based modeling. The si nificant space term in the MA stand during the early fall indicates spatial mechanisms of Rs ‘operates at much finer scale than the used 2 m scale inthis study. The current study also sup- ports the previously hypothesized trend of C balance in pyrogenic boreal ecosystem that fire reduces respiration and that postfire upland boreal ecosystems are probably a C sink rather than a source. Supporting Information S1 File, This file contains information on study sites, semi-variogram models, and spatial autoregression analysis used inthe current study. Table A: Geographic locations, fie history and dominant understory vegetation in the study sites. Table B: Mean, coefficient of variation (CV), and range of aboveground and sol bio-chemical properties in three boreal aspen stands in northern Alberta along a fire chronosequence. Different leter for the same property indi cates significant difference among sites (p < 0.10) (ocx) Acknowledgments The authors would like to thank the Environmental Research and Reclamation Group (ERRG) ofthe Canadian Oilsands Network for Research and Development, and the National Science and Engineering Research Council of Canada for providing funding, Special thanks goto Dr. Fangliang He fr logistic support and suggestion in spatial data analysis. We would also lke to thank a number of fild technicians for helping to collect data including Megan Lewis, Mark Howell, Sawyer Desaulniers, and Nicole Filipow. Author Contributions Conceptualization: SDG MDM. 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