Fine root decomposition in two subalpine forests during the freeze–thaw season

Fine root decomposition in two subalpine forestsduring the freeze–thaw season

Fuzhong Wu, Wanqin Yang, Jian Zhang, and Renju Deng

Abstract: Little is known about fine root decomposition during the freeze–thaw season. To characterize fine root decom-position during this time (from October 2006 to April 2007), a field experiment was conducted to examine the decomposi-tion of fine roots (diameters of 0–1 and 1–2 mm) of Minjiang fir (Abies faxoniana Rehd. & E.H. Wilson) and Asian whitebirch (Betula platyphylla Sukaczev) using buried litterbags in their respective habitats in western Sichuan, China. Overone freeze–thaw season, 14%–20% of mass was lost and 12%–31% of C, 6%–36% of N, 15%–25% of P, and 37%–43%of K were released. These losses accounted for about 40%–55% of mass lost and 23%–54% of C, 23%–89% of N, 25%–42% of P, and 48%–58% of K released within the first year of fine root decomposition. The amount of mass loss and bio-elements release during the freeze–thaw season correlated closely with initial substrate quality and bioelement traits. Com-pared with birch fine root, fir fine root decomposition could be influenced more by decomposition processes during thefreeze–thaw season. Results suggest that fine root decomposition during the freeze–thaw season can strongly contribute toecosystem C and nutrient cycling.

Resume : On sait peu de choses au sujet de la decomposition des racines fines durant la saison de gel et degel. Dans lebut de caracteriser la decomposition des racines fines durant cette periode (d’octobre 2006 a avril 2007), une experiencesur le terrain a ete etablie pour etudier la decomposition des racines fines (diametres de 0–1 et de 1–2 mm) du sapin deMinshan (Abies faxoniana Rehd. & E.H.Wilson) et du bouleau de Mandchourie (Betula platyphylla Sukaczev) a l’aide desacs a litiere enfouis dans leur habitat respectif dans l’ouest du Sichuan, en Chine. Au cours d’une saison de gel et degel,14 % – 20 % de la masse a ete perdue et 12 % – 31 % de C, 6 % – 36 % de N, 15 % – 25 % de P et 37 % – 43 % de K ont eteliberes. Ces pertes representaient environ 40 % – 55 % de la perte de masse et 23 % – 54 % du C, 23 % – 89 % de N,25 % – 42 % du P et 48 % – 58 % du K liberes au cours de la premiere annee de la decomposition des racines fines. Laquantite de masse perdue et de bioelements liberes durant la periode de gel et degel etait etroitement correlee avec la qua-lite initiale du substrat et les caracteristiques des bioelements. Comparativement aux racines fines du bouleau, la decompo-sition des racines fines du sapin pourrait etre influencee davantage par les processus de decomposition durant la saison degel et degel. Les resultats indiquent que la decomposition des racines fines durant la saison de gel et degel peut grande-ment contribuer au recyclage de C et des nutriments dans l’ecosysteme.

[Traduit par la Redaction]

Introduction

For many years, plants and microbes were assumed to beeffectively frozen into dormancy during winter. As a conse-quence, ecologists have traditionally focused on ecologicalprocesses during the growing season between snowmelt andsnowfall (Schimel and Mikan 2005). Little attention hasbeen paid to wintertime ecological processes, and there hasbeen little focus on significant freeze–thaw periods that oc-cur during winter and early spring. Research over the lastdecade has convincingly demonstrated that soil freezing inthe late fall, soil thawing in the early spring, and frequentfreeze–thaw cycles between fall and spring play key roles inecosystem functioning in terms of soil processes in cold re-gions (Edwards et al. 2007; Wu et al. 2009). Consequently,there is growing interest in how soil processes respond tothe seasonal freeze–thaw cycle during the cold season.

Fine roots (diameter <2 mm) provide the primary input oforganic C to soils (approximately 30%–80%) with rapid

turnover and decomposition rates (Ruess et al. 2003; Ho-ward et al. 2004; Kalyn and Van Rees 2006). The decompo-sition of fine roots plays an essential role in terrestrialmetabolism, nutrient and water cycling, C sequestration,and C flux in soil (Jobbagy and Jackson 2000; Kalyn andVan Rees 2006), but fine root decomposition is strongly in-fluenced by abiotic and biotic factors (Gill and Jackson2000; McMichael and Quisenberry 1993). Combined withother factors, soil freeze–thaw, with its associated tempera-ture and moisture dynamics, induces fine root mortalitywith the cessation of plant growth in cold regions (Cleavittet al. 2008). These senesced fine roots might be beneficialto plant growth during the following spring and could con-tribute to nutrient cycling via decomposition during thefreeze–thaw season. However, there is little informationavailable on the decomposition of fine roots in the field dur-ing the freeze–thaw season.

Internal and external mechanisms can induce the decom-position of fine roots in winter. Internally, a large amount

Received 4 April 2009. Accepted 1 December 2009. Published on the NRC Research Press Web site at cjfr.nrc.ca on 30 January 2010.

F. Wu, W. Yang,1 J. Zhang, and R. Deng. Faculty of Forestry, Sichuan Agricultural University, Ya’an, Sichuan 625014, PRC.

1Corresponding author (e-mail: [email protected]).

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Can. J. For. Res. 40: 298–307 (2010) doi:10.1139/X09-194 Published by NRC Research Press

of fine roots senesce just prior to the freeze–thaw season(Cleavitt et al. 2008). These fine roots often decompose rap-idly due to high concentrations of labile C in the earlystages of decomposition. However, the rate of decomposi-tion decreases due to an increasing percentage of more re-calcitrant compounds (Yang et al. 2004; Lemma et al.2007). Externally, microbial activity does not completelycease when soil is frozen (Coxson and Parkinson 1987;Clein and Schimel 1995; Schimel and Mikan 2005). Theseasonal freeze–thaw cycle creates considerable changes inthe physical structure of plant litter, which could increasethe available substrate for microorganisms (Schimel andClein 1996; Groffman et al. 2001). Consequently, the initialliable property, physical disruptive process, microbial activ-ity, hydraulic leaching process, and synthetic action mightpromote rapid mass loss and nutrient release during fineroot decomposition in the freeze–thaw season. A betterunderstanding of soil freeze–thaw and winter ecology offine roots is necessary to predict changes in forest nutrientcycling likely to result from climate change.

Additionally, similar to decomposition in the growing sea-son, fine root decomposition in the freeze–thaw season isalso influenced by substrate quality and environmental con-ditions. First, substrates with more liable tissues and highernutrient levels can be easily used by microorganisms, andthey are easily decayed (Lemma et al. 2007). Due to differ-ences in liable tissue and nutrient levels, fine roots of differ-ent diameters and different species might display differentdecomposition processes during the freeze–thaw season.Second, the magnitude of freeze–thaw dynamics and the fre-quency of freeze–thaw cycles during the freeze–thaw seasonmight also promote destructive physical processes and hy-draulic leaching during fine root decomposition (Melick andSeppelt 1992; Sjursen et al. 2005). Finally, since substratewith various amounts of liable and recalcitrant tissues couldrespond differently to freeze–thaw cycles, altered substratequality following the freeze–thaw season might differen-tially affect subsequent fine root decomposition processes.Although these processes are possible, they have not beendocumented in detail.

Fir and birch forests are two representative forests inmany subalpine zones, and both play important roles in reg-ulating regional climate and in conserving water and soil(Yang et al. 2005). Forests such as these in western Sichuan,China, are the dominate components of the second largestforest in China (Wang et al. 2004). The dynamics of freez-ing and subsequent thawing for about 6 months from latefall to early spring could influence belowground processesin these forests (Yang et al. 2006; Wu et al. 2009). As yet,most studies in this region have focused on litter decomposi-tion during the plant growing season (Wu et al. 2005; Yanget al. 2006). Far less information has been available on fineroot decomposition during the freeze–thaw period betweengrowing seasons. Therefore, because fine root decomposi-tion during the freeze–thaw season could contribute greatlyto decomposition over an entire first year, mass loss and nu-trient release were studied in various diameters of fir andbirch fine roots during the freeze–thaw season and over theentire first year. A field experiment was conducted using lit-terbags under Minjiang fir (Abies faxoniana Rehd. & E.H.Wilson) and Asian white birch (Betula platyphylla Sukac-

zev) forests. The objectives were to (i) characterize the de-composition of fir and birch fine roots with differentdiameters during the freeze–thaw season and (ii) explore thecontribution of the seasonal freeze–thaw cycle to annual fineroot decomposition.

Materials and methods

Study siteThis study was conducted in the Wanglang National Na-

ture Reserve (103855’–104810’E, 32849’–33802’N; 2300–4980 m above sea level) located in Pingwu County, westernSichuan, China. Climatic and vegetation features were de-scribed by Wang et al. (2004). According to climate datafor the past 10 years, the mean annual temperature is2.9 8C, the annual cumulative temperature is (‡10 8C)1056.5 8C, and the absolute maximum and minimum tem-peratures are 26.2 and –17.8 8C, respectively. Annual pre-cipitation ranges from 801 to 825 mm depending on theelevation; most of the precipitation falls from May to Au-gust. The freeze–thaw season, with temperatures below0 8C, starts in mid-October after snow fall. Soil remains fro-zen for about 120–150 days, and the maximum freezingdepth is >40 cm during the cold season (Wu et al. 2009).

Two typical forests dominated by Minjiang fir (104805’E,32858’N; 2600 m above sea level) and Asian white birch(104807’E, 32857’N; 2540 m above sea level) were selectedas sample sites in the nature reserve. The fir forest was do-minated by Minjiang fir in the canopy with Lonicera webbi-ana, Ribes glaciale, Impatiens nolitangere, Adiantumcapillus-veneris, and Hylocomium splendens present in theunderstory. The birch forest was dominated by Asian whitebirch in the canopy with Ostryopsis davidiana, Rubus pal-matus, Deyeuxia arundinacea, and Artemisia annua presentin the understory. Aspects of the sample sites were 108northwest and 608 northwest and the forest soils were classi-fied as dark brown soil (Cambosol) and brown soil (Cam-bosol) (Yang et al. 2005) for the fir and birch forests,respectively. Soils for the fir and birch forests had a pH of6.10 and 6.30, organic matter of 193.03 and 73.79 g�kg–1, to-tal N of 7.15 and 9.52 g�kg–1, and total P of 10.82 and6.55 g�kg–1, respectively.

Experimental designDecomposition of fine roots was studied using the litter-

bag procedure, a technique that is widely used even thoughit has been shown to modify decomposition rates (O’Connell1997; Guo et al. 2006).

In September 2006, fine roots (<2 mm) of fir and birchwere randomly collected in the surface (0–10 cm) soil layersfrom the selected fir and birch forests. Based on variationsin decomposition rates and functions of fine roots with dif-ferent diameters, collected fine roots were separated into0–1 and 1–2 mm diameters (Pregitzer et al. 2002; Espeletaet al. 2009). Dark and dead roots were discarded because amajority of these had already decomposed (field observa-tion), and healthy roots were air-dried and then cleaned.Ten-gram samples (corresponding to dry mass) of air-driedfine roots were placed in nylon bags (15 cm � 15 cm,0.50 mm mesh) and the edges were sealed. Ten replicateswere used for each diameter and species for a total of 40

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bags. About 10 g of oven-dried fine roots from each diame-ter and species was retained for determination of initialcharacteristics. The initial characteristics of fine roots aregiven in Table 1.

Because the majority of fine roots occurred in the0–10 cm layer (field observation), litterbags were buried insoils 10 cm under the soil surface of their respective forestson 25 October 2006 just at the beginning of the freeze–thawseason. Data were chosen based on previous observationsand local climate information (unpublished data). A horizon-tal plot with typical forest characteristics was chosen inwhich to bury the mesh bags. At least 2 cm was maintainedbetween the buried bags to avoid disturbance among bags.At the end of the freeze–thaw season (9 April 2007) and atthe end of the following growing season (22 October 2007),five replicate litterbags for each diameter and species wererandomly sampled. Meanwhile, it is considered that thereare numerous soil freeze–thaw cycles that can occur in re-sponse to changing temperatures within a 1 day period dur-ing the freeze–thaw season; one Buttony DS1923-F5recorder (Maxim Co., Torrance California) was used to re-cord soil temperature every hour at the same soil depth inboth forests. Hourly soil temperatures during the freeze–thaw season (from 25 October 2006 to 9 April 2007) are de-scribed in Fig. 1.

Analyses and calculationsThe remaining fine roots were taken from the litterbags.

Foreign materials (living roots, fauna, and soil) were care-fully removed by hand and the roots were oven-dried at70 8C for at least 48 h to constant mass and weighed thenearest 0.001 g. The oven-dried samples and the retained in-itial samples were finely ground to pass through a 1 mmstainless steel sieve to be used in C and nutrient analysis.

Carbon and nutrients in the samples were determined asdescribed by Lu (1999). Carbon concentration was deter-mined using the dichromate oxidation – sulphate ferrous ti-tration method. After acid digestion with 8 mL of H2SO4 (r= 1.84 g�cm–3) and 3 mL of H2O2 solution at 190 8C for10 min, the concentrations of N, P, and K were determinedby indophenol blue colorimetry, phosphor molybdenum bluecolorimetry, and flame photometry, respectively. All analy-ses were carried out in triplicate.

Fine root dry mass loss (L), the net release (R) rate of Cand nutrients, and the percentage (P) of fine root decompo-sition that occurred during the freeze–thaw season of 1 yearwere calculated as follows:

L ð%Þ ¼ 100� ðM0 �MtÞ=M0

R ð%Þ ¼ 100� ðM0C0 �MtCtÞ=M0C0

P ð%Þ ¼ 100� ðM0C0 �M4C4Þ=ðM0C0 �M10C10Þ

where M0 is the initial fine root dry mass. Mt is the dry massof the remaining fine roots in the bag when sampled, M4 andM10 are the dry mass of the remaining fine roots in the bagcollected in April and October, respectively, C0 is the con-centration (g�kg–1) of C or nutrients in the initial fine roots,Ct is the concentration (g�kg–1) of C or nutrients in the re-maining fine roots when sampled, and C4 and C10 are the

concentrations (g�kg–1) of C or nutrients in the remainingfine roots collected in April and October, respectively.

Statistical analysisAll variables were analyzed using ANOVA with substrate

diameter and species (total of four levels) used as factorsafter checking for normal distribution of the data. When sig-nificant differences occurred, an LSD multiple range testwas used to determine where differences existed. Relation-ships between initial fine root characteristics and decompo-sition rates (mass loss and bioelements release) of both firand birch fine roots after the freeze–thaw season were deter-mined using Pearson’s correlation coefficients at the 0.05level. Correlations between two variables that had internaldependent relationships were excluded. All statistical analy-ses were performed using the SPSS software package(standard released version 11.5 for Windows; SPSS Inc.,Chicago, Illinois).

Results

Temperature dynamicsThe incubation time of fine root decomposition was

166 days during the freeze–thaw season. As described inFig. 1, soil freeze began on 6 November 2006 in both firand birch forests and soil temperature remained constantlybelow 0 8C beginning on 23 and 28 December 2006 in thefir and birch forests, respectively. Soil thaw began on 6April 2007 in the fir forest and 3 April 2007 in the birchforest, whereas soil temperature remained constantly above0 8C starting on 8 April 2007 in both forests. Overall, thetotal time above 0 8C was 12 days (before freeze–thaw) +1 day (after freeze–thaw) in both forests. There were47 days (before completely frozen) + 3 days (after com-pletely frozen) and 52 days (before completely frozen) +6 days (after completely frozen) that were both above andbelow 0 8C within a 1 day period in the fir and birch forests,respectively. There were 116 and 108 days below 0 8C in firand birch forests, respectively.

Mass lossOver one freeze–thaw season, about 14%–20% of fine

root mass was lost, which accounted for 40%–55% of totalmass lost (35%–38%) during 1 year of fir and birch fineroot decomposition (Table 2). Mass loss was significantly(p < 0.05, n = 5) greater in the 0–1 mm fir roots than thatin birch roots, but mass loss was not significantly (p > 0.05,n = 5) different in the other three types of fine roots. Thehighest proportion of mass loss in the freeze–thaw seasonwas observed in 0–1 mm fir fine roots, whereas the lowestproportion of mass loss was observed in 0–1 mm birch fineroots. Although the proportion of mass loss in the freeze–thaw season was significantly (p < 0.05, n = 5) higher in0–1 mm fir fine roots than that in the 0–1 mm birch fineroots, the proportion of mass loss was a little lower (p >0.05, n = 5) in 1–2 mm fir fine roots than that in 1–2 mmbirch fine roots.

Bioelement concentrationsConcentrations of C, P, and K in fine roots with different

diameters decreased as decomposition proceeded (Fig. 2),

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with the exception of P concentrations in 0–1 mm fir fineroots, which increased after the freeze–thaw season. In con-trast, N concentrations in fir fine roots (0–1 mm) and birchfine roots (1–2 mm) increased as decomposition proceeded,whereas the seasonal freeze–thaw decreased N concentra-tions in the other two types of fine roots.

Bioelement releasesFir and birch fine roots released 12%–31% of C, 6%–36%

of N, 15%–25% of P, and 37%–43% of K during the freeze–thaw season, whereas the 1-year bioelement release rateswere 52%–59% of C, 21%–50% of N, 56%–62% of P, and75%–80% of K (Fig. 3). Carbon release rates of both 0–1and 1–2 mm fir fine roots were significantly (p < 0.05, n =5) higher than those in corresponding birch fine roots duringthe freeze–thaw season, but over the entire year, there were

no significant (p > 0.05, n = 5) differences among the fourtypes of fine roots. Carbon release rates in the freeze–thawseason were not significantly (p > 0.05, n = 5) different be-tween 0–1 and 1–2 mm fir fine roots, but C release rateswere statistically (p < 0.05, n = 5) higher in 0–1 mm thanin 1–2 mm birch fine roots. In contrast, lower (p < 0.05,n = 5) N release rates occurred in 0–1 mm fir fine roots,but higher N release rates (p < 0.05, n = 5) were found in1–2 mm birch fine roots compared with those in birch fineroots in both the freeze–thaw season and 1-year decomposi-tion. Phosphorus release rates of 0–1 mm fir fine roots in thefreeze–thaw season were lower (p < 0.05, n = 5) than thoseof the other three types of fine roots. However, there wereno significant differences in P release rates among the otherthree types of fine roots. There were no significant (p >0.05, n = 5) variations in K release rates among the four

Table 1. Initial characteristics of Minjiang fir (FF) and Asian white birch (BF) fine roots with different diameters.

Forest Diameter (mm) C (g�kg–1) N (g�kg–1) P (g�kg–1) K (g�kg–1) C/N C/P N/PFF 0–1 448.34 6.29 1.13 0.74 71.48 400.39 5.56

1–2 495.92 6.07 1.14 0.74 82.21 438.79 5.32BF 0–1 420.62 10.28 0.73 0.69 41.75 574.82 14.08

1–2 433.66 6.22 0.60 0.69 64.33 725.13 10.37

Fig. 1. Hourly dynamics of soil temperature in the Minjiang fir (FF) and Asian white birch (BF) samples during the freeze–thaw season(25 October 2006 to 9 April 2007).

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types of fine roots in both the freeze–thaw season and 1-year decomposition.

Percentages of bioelements that were released during thefreeze–thaw season of 1 year were 23%–54% for C, 23%–89% for N, 25%–42% for P, and 48%–58% for K (Fig. 4).Percentages of C release rates were higher (p < 0.05, n = 5)for fir fine roots than those for birch fine roots for both 0–1and 1–2 mm diameters. Percentages were higher (p < 0.05, n= 5) for N and P releases in 1–2 mm than those in 0–1 mmfir fine roots, whereas percentages of N release rates werehigher (p < 0.05, n = 5) in 0–1 mm than those in 1–2 mm

birch fine roots. Percentages of both N and P release rateswere lower (p < 0.05, n = 5) in 0–1 mm fir fine roots thanthose in birch fine roots, although the percentage of N re-lease rates was higher (p < 0.05, n = 5) in 1–2 mm fir fineroots. There were no significant (p > 0.05, n = 5) variationsin the percentages of K release rates among the four types offine roots.

CorrelationsThe mass loss rate during the freeze–thaw season was

positively correlated (p < 0.05) with P and K concentrations

Table 2. Mass loss rates (mean ± SD, n = 5) of Minjiang fir (FF) and Asian white birch (BF) fine roots withdifferent diameters determined after the freeze–thaw season (April) and after 1 year of decomposition (October)and proportions (mean ± SD, n = 5) in the freeze–thaw season of 1 year.

Forest Diameter (mm) Sampling time Residual mass (g) Mass loss (%)Proportions in thefreeze–thaw season (%)

FF 0–1 April 7.89±0.53 20.48±5.60a 54.10±4.32aOctober 6.10±0.21 38.70±2.15x

1–2 April 8.34±0.28 16.50±2.53ab 46.24±5.56bOctober 6.41±0.11 35.72±0.94y

BF 0–1 April 8.55±0.26 14.50±2.26b 39.51±4.66cOctober 6.33±0.20 36.37±2.01y

1–2 April 8.21±0.52 17.47±4.97ab 50.56±7.85abOctober 6.46±0.12 35.00±1.03y

Note: Different letters among variables with the same sampling time but in different species with different diameters denotesignificant difference by LSD within a column (p < 0.05, n = 5).

Fig. 2. Concentrations of elements in Minjiang fir (FF) and Asian white birch (BF) fine roots with different diameters measured at the startof decomposition in October 2006, after a freeze–thaw season (April 2007), and after 1 year (October 2007). Bars indicate SD (n = 5) andasterisks denote the significant differences between the decomposition stages (p < 0.05).

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and C/N, but it was negatively correlated (p < 0.01) with Nconcentration and N/P in the substrate (Table 3). Carbon re-lease rate was positively correlated (p < 0.01) with P and Kconcentrations, but it was negatively correlated (p < 0.01)

with N/P in substrate. Nitrogen release rate was not signifi-cantly correlated (p > 0.05) with any investigated variablesin the substrate. However, P release rate was only correlated(p < 0.05) with C concentrations in substrate. Potassium re-

Fig. 3. Bioelement loss rates (mean ± SD, n = 5) of Minjiang fir (FF) and Asian white birch (BF) fine roots with different diameters (0–1and 1–2 mm) determined after the freeze–thaw season (April) and after 1 year of decomposition (October). Bars indicate SD (n = 5).

Fig. 4. Proportions of bioelments release in the freeze–thaw season of 1 year during decomposition of Minjiang fir (FF) and Asian whitebirch (BF) fine roots with different diameters (0–1 and 1–2 mm). Bars indicate SD (n = 5) and asterisks denote the significant differencesbetween different diameters (p < 0.05); different letters denote significant differences with the same diameter between FF and BF fine roots(p < 0.05).

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lease rate was positively correlated (p < 0.05) with P con-centrations, but it was negatively correlated (p < 0.05) withC/P and N/P in the substrate.

Discussion

Mass loss during the freeze–thaw seasonMass loss is one of the essential processes during fine

root decomposition. In the present study, approximately halfof the fine root mass that was lost in the first year occurredduring the freeze–thaw season. This could be a direct resultof frequent freeze–thaw cycles during the freeze–thaw sea-son (Fig. 1) owing to physical disruptive effects in freezingand hydraulic leaching in thawing. In addition, microbial ac-tivities should not be ignored even in frozen conditions asmany previous studies have declared (Clein and Schimel1995; Schimel and Mikan 2005). Although microbial char-acteristics were not included in the present study, the rapiddecomposition of fine roots during the freeze–thaw seasonimplies that root decomposition processes in winter shouldbe given more attention and might be important in under-standing C and nutrient dynamics in cold ecosystems.

Fine roots smaller than 1 mm often consist of many ab-sorptive roots that have rapid turnover rates, but larger rootsconsist of transport roots with greater presence of recalci-trant tissues (Valenzuela-Estrada et al. 2008). In contrastwith previous findings for the growing season, the results ofthe current study showed that decomposition rates did notdiffer between 0–1 and 1–2 mm diameters for both fir andbirch fine roots during the freeze–thaw season. This mightresult from relatively lower biological activities (microor-ganism and animal) in the freeze–thaw season comparedwith those in the growing season (Mikan et al. 2002) andimplies that the physical processes of freezing–thawingcould be the dominant factors controlling fine root decom-position during the freeze–thaw season. Furthermore, massloss rates of smaller fir fine roots in the freeze–thaw seasonconstituted a higher proportion of mass loss over the entireyear compared with those of larger fir roots; however, birchfine roots showed the opposite pattern. This result might berelated to the proportion of reliable (such as cellulose) andrecalcitrant tissues (such as lignin) in the substrate andchanges in fine root quality after the freeze–thaw season.Nevertheless, changes in fine root quality have not been ex-amined, but it is a topic that warrants further exploration.

Fine root decomposition generally correlates closely withinitial substrate quality, for instance, with initial nutrient

concentrations, C/N, C/P, and N/P (Usman et al. 2000;Chen et al. 2002). Many previous studies have documentedslower decomposition rates in coniferous species due tolower N concentrations, higher C/N, and resin canals inlarger roots (Gallardo and Merino 1999; Chen et al. 2001).However, results of the current study indicate that the massloss rate for 0–1 mm fir fine roots was higher than that forbirch fine roots. There are at least three possible reasons forthis observation. First, P could be the limiting nutrient infine root decomposition processes rather than N during thefreeze–thaw season in this subalpine region. Pearson correla-tions showed that the mass loss rate was positively corre-lated with P concentrations but negatively correlated with Nconcentrations and the N/P ratio (Table 3). Second, smallerfir roots often contain few recalcitrant tissues such as resincanals, but these tissues increase with the increase in rootdiameter (Silver and Miya 2001). The finding that the massloss rate of 1–2 mm fir fine roots was lower than that of0–1 mm fir fine roots and insignificantly varied with that of1–2 mm birch fine roots could be explained by the synthesiseffects of P and recalcitrant tissue concentration in the sub-strate. Finally, variations in soil temperature between fir andbirch forests could also explain differences in mass lossrates and their proportions of the entire year between thetwo species.

Bioelement release during the freeze–thaw seasonBioelement release in fine root decomposition provides

necessary nutrients for plant nutrition and growth. Similarto mass loss, large quantities of bioelements are releasedfrom fine roots during the freeze–thaw season. Microbialprocesses and leaching are the main regulators of bioelementrelease. Freezing in the cold season has strong effects on lit-ter physical properties, leading to increased substrate avail-ability to microorganisms and consequently to bioelementrelease (Schimel and Clein 1996; Groffman et al. 2001).Compared with other elements, K showed the highest valuesof release after one freeze–thaw season and after 1 year,with few differences between species or root thickness. Thisresult might be related to traits of K, including high mobilityand ease of loss by leaching (Yang et al. 2007). Addition-ally, the release rates of K from October to April and fromApril to October were similar, which may signify no sea-sonal effects on K release.

The results here showed that C concentrations in fineroots decreased as decomposition proceeded, which is thedirect result of mass loss during decomposition (Sharma

Table 3. Pearson correlations between the initial bioelement characters in substrate fine roots and therelease rates of mass and bioelements during the freeze–thaw season.

Substrate bioelement characters

Release rate duringthe freeze–thawseason C N P K C/N C/P N/PMass 0.15 –0.66** 0.45* 0.51* 0.54** –0.39 –0.68**C — –0.38 0.97** 0.96** — — –0.81**N 0.15 — 0.02 –0.07 — –0.11 —P 0.44* –0.08 — –0.10 0.22 — —K 0.15 –0.16 0.73** — 0.15 –0.82** –0.54**

Note: **p < 0.01, *p < 0.05, n = 20; a dash indicates not suitable for the correlation test.

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and Ambasht 1987; O’Connell 1988; Lemma et al. 2007).Nitrogen and P are characterized by high mobility (Wu etal. 2005), but they are prone to microbial immobilization(Ribeiro et al. 2002; Tian et al. 2003). In addition, N and Pconcentrations during decomposition are also controlled bynet losses of C (or mass losses) (Ribeiro et al. 2002). There-fore, the increased or decreased N and P concentrations dur-ing decomposition observed here might be a result of thecombined effects of net losses of C and microbial immobili-zation. Potassium concentrations of fine roots deceased asdecomposition proceeded, which is consistent with the factthat K is highly mobile as previously discussed.

Since the bioelement release rate was determined by netmass loss and changes in bioelement concentrations as de-composition proceeded, it was also related to initial sub-strate quality and other factors as discussed above. Fineroots released a high proportion of bioelements during thefreeze–thaw season, but the percentage of bioelements re-leased in the freeze–thaw season compared with that re-leased in 1 year varied with bioelements, root diameters,and species. These variations might be related to the sub-strate quality as indicated by Pearson correlations (Table 3).The results showed that fir fine roots released more C dur-ing the freeze–thaw season than did birch fine roots, but Crelease rates over the entire year were similar between spe-cies. This suggests that the synthesis power including physi-cal destructive, hydraulic leaching, and biological activitiesin the freeze–thaw season had greater effects on fir fineroot decomposition than that on birch fine roots, but theopposite occurred during the growing season. This resultsupports the theory that different factors dominate decompo-sition processes in the freeze–thaw season and growing sea-son: physical destructive forces and hydraulic leaching aredominant in the freeze–thaw season and microbial activitiesare dominant in the growing season. Even so, decompositionprocesses are also related to traits of C and differences inquality of fine roots between species. As a structural ele-ment, C often changes with the change in mass as decompo-sition progresses (Guo et al. 2006). Similarities in C lossrates between the two types of fir fine roots in the freeze–thaw season of this study also support this assertion.Although the details are not clear, variations in C releaserates between 0–1 and 1–2 mm birch fine roots in both thefreeze–thaw season and the growing season were at leastpartly related to substrate characteristics, suggesting that mi-crobial activity also contributed to fine root decompositionin the freeze–thaw season. The fact that smaller fir fineroots exhibited lower N and P release rates in the freeze–thaw season also implies effects of microbial activitiesbecause these two elements can often be immobilized bymicroorganisms (Ribeiro et al. 2002). In addition, smallerfine roots often contain richer liable tissues than do largerfine roots (Valenzuela-Estrada et al. 2008), which could pro-vide a more amenable environment for microorganisms.

Additionally, proportions of element release rates duringfine root decomposition in the freeze–thaw season comparedwith the entire first year differed between root diameters andbetween species, a finding that is also related to variationsin element traits and substrate quality. The proportion of Preleased during the freeze–thaw season compared with P re-leased for the entire first year was lower than that of N and

K. This result not only supports the former speculation thatP could be the limiting factor for microbial activity in thefreeze–thaw season in these subalpine forests but also em-phasizes the important influence of physical processes dur-ing the freeze–thaw season on the release of elements,especially mobile elements such as N and K. Although li-able and recalcitrant tissues in the substrate were not deter-mined, the varied proportions of released C and N in thefreeze–thaw season between root diameters and betweenspecies might largely be a result of concentrations of liableand recalcitrant tissues. The results suggest that fir fine rootsmay consist of larger proportions of recalcitrant tissues com-pared with those of birch fine roots and that the proportionincreases with increasing root diameter. This finding is sup-ported by the widely known observation that coniferous spe-cies, in comparison with broadleaf species, possess higherproportions of recalcitrant components, such as resin canals,especially in larger roots (Chen et al. 2001). The results alsosuggest that a higher amount of recalcitrant tissues in sub-strate could increase the contribution of decomposition dur-ing the freeze–thaw season to the decomposition in theentire first year. However, it is difficult to explain why theproportion of N release rate for 0–1 mm birch fine rootswas higher in the freeze–thaw season than that for the corre-sponding fir fine roots and 1–2 mm birch fine roots. Thismight be related to substrate quality and environmental con-ditions, but detailed explanations require further study.

ConclusionsThe large amount of mass and bioelements released in the

freeze–thaw season supports the hypothesis that seasonalfreeze–thaw cycles significantly affect fine root decomposi-tion and that fine root decomposition in the winter could bean essential part of nutrient cycling and C flux. Althoughdetails of the processes have not been examined, and someexplanations for the observations are not fully clear, decom-position in the freeze–thaw season contributed strongly to firand birch fine root decomposition in these subalpine forests.The percentages of fine root decomposition in the freeze–thaw season within 1 year were tightly related to the sub-strate quality and varied with root diameter and species.The results suggest that different decomposition factorsdominate decomposition processes during the freeze–thawseason as apposed to the growing season. Decompositionprocesses in the freeze–thaw season could have a greater in-fluence on decomposition of substrate with higher amountsof recalcitrant tissues than on decomposition of substratewith more liable tissues. Since wintertime ecological proc-esses in cold regions are sensitive to climate change, theseobservations could be important in understanding ecosystemC and nutrient dynamics in these subalpine forests as influ-enced by global climate change. Nonetheless, internal proc-esses (physical, chemical, and microbial) of fine rootdecomposition in the freeze–thaw season were not clearlycharacterized in detail. More detailed work should be con-ducted to determine the mechanisms controlling fine rootdecomposition during the freeze–thaw season.

AcknowledgementsWe are very grateful to Prof. Shengli Ren, Prof. Bo Zeng,

and two anonymous reviewers for useful suggestions in the

Wu et al. 305


manuscript. This project was financially supported by theNational Natural Science Foundation of China (30771702and 30471378), the Program for New Century Excellent Tal-ents in University (NCET-07-0592), the National Key Tech-nologies R & D Program of China (2006BAC01A11), theSichuan Excellent Youth Science and Technology Founda-tion (07ZQ026-022), and the key cultivation program of theeducation department of Sichuan Province (07ZZ024 and09ZZ023). We gratefully acknowledge the staff of Wan-glang National Nature Reserve for their help with the fieldwork.

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Fine root decomposition in two subalpine forests during the freeze–thaw season