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Article

Responses of Fine Root Morphological and Chemical Traits among Branch Orders to Forest Thinning in Pinus massoniana Plantations

by
Jiahao Zhao
1,
Xiaodan Sun
2,
Dong Wang
3,
Meiquan Wang
1,
Junjie Li
1,
Jun Wang
4 and
Qingwei Guan
1,*
1
College of Ecology and Environment, Nanjing Forestry University, Nanjing 210037, China
2
Marine Ecology Research Center, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
3
College of Environmental Science and Engineering, China West Normal University, Nanchong 637009, China
4
Hefei College of Finance and Economics, Hefei 230601, China
*
Author to whom correspondence should be addressed.
Forests 2024, 15(3), 495; https://doi.org/10.3390/f15030495
Submission received: 31 January 2024 / Revised: 28 February 2024 / Accepted: 4 March 2024 / Published: 7 March 2024
(This article belongs to the Section Forest Ecology and Management)
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Abstract

:
Fine roots play an essential role in biogeochemical cycling in forest ecosystems; however, little is known about the response of fine root morphology and chemistry in different root orders to forest management activities such as forest thinning. We investigated the fine root morphological and chemical traits in different root orders of Pinus massoniana under different thinning intensities, namely no thinning, low-intensity thinning (LIT), middle-intensity thinning (MIT), and high-intensity thinning (HIT) (0%, 25%, 45%, and 65% of individual trees eliminated, respectively). We found that forest thinning increased the root diameter (RD) of absorptive roots and decreased that of transport roots, while the trend for the specific root length (SRL) was the opposite. LIT and MIT could increase specific surface area (SSA), especially the SSA of absorptive roots in the MIT treatment. The root tissue density (RTD) of all root sequences in the LIT treatment decreased but increased in the HIT treatment. For the fine root chemical traits, thinning increased the root carbon concentration (RCC) of absorptive roots. The root nitrogen concentration (RNC) and root phosphorus concentration (RPC) of first- to fourth-order roots increased in the LIT and MIT treatments after thinning. Meanwhile, thinning increased root lignin, cellulose, and non-structural carbohydrate (NSC) concentrations. Soil temperature, nitrate, and microbial biomass carbon were factors affecting variations in fine root morphology and chemistry. Forest thinning was likely to shift the absorptive roots’ foraging strategy into a resource-conserving one. Thinning increased fine root chemical traits in most root orders. These findings contributed to our ability to predict how belowground ecological processes are mediated by fine roots under forest management activities.

1. Introduction

Fine roots (≤2 mm in diameter) are fundamental organs allowing plants to absorb soil nutrients and water, thereby promoting tree growth and determining forest productivity [1,2]. The morphological and chemical traits of fine roots are essential functional traits that mediate carbon and nutrient cycling in terrestrial ecosystems [3,4]. Forest thinning is an effective management practice used to enhance forest productivity and functionality primarily through optimizing stand structure, understory environment, and soil conditions [5,6,7]. The changes in fine root traits after thinning are key points for forest thinning to regulate forest productivity and carbon sequestration capacity [8,9]. However, few studies focus on the response of fine root morphological and chemical traits to forest thinning, and the intraspecific variations among root branch orders after thinning remains unclear.
Fine root morphology and chemistry have been extensively studied as drivers of ecosystem processes [10], including carbon [11,12] and nutrient cycling [13,14], soil formation, and structural stability [15]. However, to our knowledge, few studies have reported on the various responses of root morphological traits to anthropogenic regulatory measures, including forest thinning. Wang et al. [16] found that thinning increased root length density (RLD) and root tissue density (RTD) and decreased specific root length (SRL) and specific surface area (SSA). In contrast, the root diameter (RD), SRL, and RTD of Chamaecyparis obtuse roots showed no difference 3 years after thinning [17]. For fine root chemical traits, thinning increased C, P, and K concentrations in oak fine roots [18], while high stand density increased organic C and N contents in Populus tomentosa fine roots [19]. The discrepancies in these results are probably due to differences in thinning intensity, time scale, tree species, stand age, and fine root delineation criteria [20,21,22].
Previous studies have mostly examined the responses of root morphological and chemical traits to external disturbance using diameter cut-offs [18,23]. However, variations in fine roots classified by diameter did not describe the actual adaptation to environmental changes [24]. It has been demonstrated that plant fine roots in different branching positions exhibit morphological, chemical, and physiological differences [25,26]. Low-order (i.e., 1st–2nd-order) roots with living cortices are mainly responsible for resource acquisition [27]. As a root system grows radially, high-order (i.e., 3rd–5th-order) roots that have undergone secondary growth develop secondary vascular cambium and cork cambium, which contribute to resource transportation and storage [28,29,30]. Consequently, from first- to fifth-order fine roots, SRL, SSA, and the concentrations of N and phenolic compounds decrease, while RD, RTD, and concentrations of C, cellulose, lignin, and non-structural carbohydrates increase [24,31,32]. Due to differences in the functions and structure of fine roots in different root sequences, the responses of root morphology and chemistry among branch orders to forest management activities showed various trends [16,33,34]. Clarifying the intraspecific variations in fine root traits in different orders after thinning will ultimately deepen the understanding of belowground ecological processes mediated by fine root dynamics.
Plant roots require resources and space in the soil to transfer root growth to new soil profiles, thus altering their morphology [35]. Plants enhance the ability of fine roots to absorb nutrients quickly and efficiently by optimizing root morphology (i.e., increasing root length and surface area) in resource-poor sites [27]. On the contrary, some species are generally characterized by long and thick fine roots that conserve resources when soil nutrients are deficient [36]. Forest thinning directly reduces stand density and thereby increases the light intensity, temperature, and throughfall inside the stand [5,37]. The changes in the remaining trees and microclimate after thinning accelerate plant litter decomposition and nutrient release, which improves the level of soil resources [38,39,40,41]. Therefore, we first hypothesized that forest thinning promotes soil resources such as water and nutrient concentration. In this case, plants do not need to optimize their fine root morphology to absorb the required resources, and the foraging strategy of fine roots tends toward the conservative resource strategy. Consequently, our second hypothesis is that thinning decreases SRL, SSA, and root N concentration whilst increasing RD, RTD, and root C concentration.
Pinus massoniana, characterized by high tolerance and adaptability to barren soil, has become one of the main afforestation tree species in Southern China [42]. The high density and simple structure of P. massoniana plantations lead to several ecological problems such as the reduction in forest productivity and ecosystem services, which could be ameliorated by forest thinning [43,44,45]. Clarifying the changes in fine root functional traits after thinning is beneficial for the sustainable management of P. massoniana plantations. Accordingly, this study aimed to evaluate differences in fine root morphological and chemical traits of P. massoniana among root orders after thinning. As a result, the following two points were investigated: (1) changes in fine root morphological and chemical traits of branch order under different thinning intensities; and (2) the potential soil factors that affect fine root morphology and chemistry after forest thinning.

2. Materials and Methods

2.1. Study Site

The research was conducted in the Wuxiang Mountain National Forest Park, Nanjing, Jiangsu Province, China (31°33′32″–31°36′58″ E, 118°59′33″–119°05′07″ N). The forest is in a subtropical region and covers 1879.73 hm2. The study site has distinct winter and summer temperature differences and adequate light. The average annual precipitation and temperature are 1005.7 mm and 15.5 °C, respectively [46]. The site comprises evergreen and deciduous broadleaved forest vegetation, with P. massoniana, Cunninghamia lanceolate, and Quercus variabilis being the dominant tree species. The main understory vegetation consists of Trachelospermum jasminoides and Serissa japonica [16,41]. The geomorphological features comprise low-mountain and hilly areas, with an average elevation of approximately 100 m above sea level [39]. The soil is slightly acidic with a pH value of about 4.5, and the soil depth in Forest Park is approximately 10–100 cm [8].

2.2. Experimental Design

In April 2006, 20 years after planting, we randomly established four treatments in a P. massoniana plantation: no thinning (CK; 0% of individual trees eliminated), low-intensity thinning (LIT; 25% of individual trees eliminated), middle-intensity thinning (MIT; 45% of individual trees eliminated), and high-intensity thinning (HIT; 65% of individual trees eliminated). Each treatment was set randomly and was replicated thrice to give a total of 12 experimental plots (20 m × 20 m). The sample plots were separated by at least 5 m isolation gaps. All the sample plots were established in the same northwest slope with a slope gradient of about 20°. We conducted a sample survey in 2020 to gain basic stand information on P. massoniana plantation (Table 1).

2.3. Sample Collection

Fine roots from four dominant P. massoniana trees were collected from each plot in September 2020, 14 years after thinning. We ensured that these trees were 5 m away from the edge of each plot to eliminate edge effects on trees and fine roots. Soil profiles were dug about 1 m away from the main trunk of the P. massoniana trees. Soil blocks (20 cm × 20 cm × 20 cm) were obtained from the soil profile, with a total of 4 soil blocks in each plot. The stones and the roots of other understory vegetation in soil blocks were removed completely. And then soil blocks were fully mixed into one piece, so that each treatment had three soil samples. All soil samples were used to evaluate soil physiochemical properties. By harvesting the roots of P. massoniana in soil blocks, an intact fine root system was obtained. At least three intact fine root systems were presented in each treatment to determine morphology and chemistry. Soil and fine roots samples were transferred into self-sealing bags and stored at approximately 4 °C until analysis.

2.4. Fine Root Traits

Fine roots were separated from the soil blocks and gently washed using deionized water. Thereafter, fine roots with complete structures were classified into 1st- to 5th-order roots according to the methods of Pregitzer et al. [47]. Distal roots in root system were the 1st-order roots. The roots attached to the 1st-order roots were the 2nd-order roots, and so on until the 5th-order roots. And roots adhered to higher-order roots without branches were also divided into 1st-order roots. The fine roots in different orders were scanned using an Epson Expression 10,000 XL digital scanner (Seiko Epson Corp., Suwa-shi, Japan), thereafter directly obtaining the root diameter (RD, mm), root length (RL, cm), root surface area (RA, cm2), and root volume (RV, cm3) using WinRHIZO Pro 2016a root analysis software (Regent Instruments Inc., Québec City, QC, Canada). Dry weights of fine roots of different orders were obtained by oven-drying the roots at 65 °C for 72 h and weighing after scanning. The aforementioned measurements were used to calculate the following trait data: specific root length (cm g−1) = RL/dry weight; specific surface area (cm2 g−1) = RA/root dry weight; and fine root tissue density (g cm−3) = dry weight/RV [33]. Root C and N concentrations were determined using an elemental analyzer (Vario Elemental III, Fischer, Waldachtal, Germany). Root P concentration was determined by colorimetric method after microwave digestion. Root lignin and cellulose concentrations were determined using a fiber analyzer (SLQ-6A, NANBEI, Zhengzhou, China) according to the method of Van Soest [48]. Non-structural carbohydrate concentration was the sum of sugar and starch concentrations determined using a UV-VIS spectrophotometer (UV-2450, Shimadzu, Kyoto, Japan) according to the method of Wan et al. [49].

2.5. Soil Properties

Soil temperature was determined directly in the excavated soil profile three times using Thermochron temperature loggers (DS1923Hygrochron, On Solution Pty Ltd., Castle Hill, Australia). Soil water content was determined by oven-drying the soil samples at 105 °C for 48 h. Soil pH was measured using a PHS-3C pH meter (Leici Inc., Shanghai, China) at a soil solution ratio of 1:2.5 (w/v). Bulk density (BD) was determined by drying cylindrical steel cores (100 cm3) at 105 °C for 48 h. After removing carbonate by phosphoric acid, soil organic carbon (SOC) and soil total nitrogen (TN) were determined using an elemental analyzer (Vario Elemental III, Fischer, Waldachtal, Germany). Ammonium and nitrate were determined colorimetrically in 1 M KCl extracts (1:5 w/v) using a continuous flow analyzer (San++; Skalar, Breda, Netherlands). Available phosphorus (AP) (extracted with 0.03 M NH4F-0.02 M HCI) was determined using molybdenum blue colorimetry. Microbial biomass carbon (MBC) (Kc = 0.45) and nitrogen (MBN) (Kc = 0.54) were obtained using chloroform fumigation-K2SO4 extraction methods and calculated using the aforementioned organic carbon analyzer [50]. Soil physical and chemical properties under different thinning intensities are shown in Table 2.

2.6. Statistics Analysis

Linear mixed effects models using a sampling plot as the random effect were used to evaluate the differences in fine root morphological and chemical traits among treatments and root orders, alongside their interaction. We used the least significant difference (LSD) test to determine the fine root traits of different root sequences and soil properties under the four treatments, with all variables being tested for normality. Redundancy analysis (RDA) using the vegan package (version 2.6-4) was applied to determine which soil factors affect fine root morphological and chemical traits. All statistical analyses and diagrams were performed in R v.3.5.3 software [51].

3. Results

3.1. Fine Root Morphological Traits after Thinning

The root diameter (RD), specific root length (SRL), specific surface area (SSA), and root tissue density (RTD) showed significant variations among root branch orders (Table 3). The RD and RTD generally increased, and the SRL and SSA decreased with root order (Figure 1). Thinning increased the RD of first- to second-order roots (Figure 1a). And the RD of third-order roots in the MIT and HIT and fourth- to fifth-order roots in the LIT and MIT treatments were higher than those in the CK treatment (p > 0.05). The SRL, SSA, and RTD differed significantly among thinning intensities (p < 0.05) (Table 3). The SRLs of first- to second-order roots decreased and those of third- to fifth-order roots increased after thinning (Figure 1b). The SRLs of fourth-order roots in the LIT and MIT treatments were higher than that in the CK and LIT ones (p < 0.05), and the highest SRL in fifth-order roots (158.12 cm g−1 on average) was obtained in the MIT treatment (p < 0.05).
The SSA ranking of first- and second-order roots was MIT > CK > LIT > HIT (Figure 1c). The highest values of the SSA of the third- and fourth-order roots were found in the LIT treatment (118.92 cm2 g−1 and 87.92 cm2 g−1 on average, respectively) and the lowest in the HIT treatment (85.43 cm2 g−1, 58.37 cm2 g−1 on average, respectively). The SSA of the fifth-order roots in the HIT treatment was lower than that in the CK, LIT, and HIT treatments (p < 0.05). The RTD of all root sequences in the LIT treatment were lower than those in the CK treatment (p > 0.05). Compared with the CK treatment, MIT decreased the RTD of first- and fourth-order roots and increased the RTD of second-, third-, and fifth-order roots. HIT increased the RTD of first- to fifth-order roots by approximately 29.34%, 30.29%, 30.23%, 6.08%, and 1.78%, respectively.

3.2. Fine Root Chemical Traits after Thinning

The C, N, and P concentrations in roots and the concentration of lignin, cellulose, and NSC were significantly affected by root order (Table 3). The RCC, cellulose, and NSC concentrations increased with root order and the RNC, RNP, and lignin concentrations decreased with root order (Figure 2). From the root order perspective, thinning increased the RCC of the first- and second-order roots (Figure 2a). LIT decreased the RCC of the third- to fifth-order roots, and MIT decreased that of the third- and fifth-order roots. The RNC increased after thinning, with the highest values observed in the MIT treatment and the lowest in the CK treatment (Figure 2b). Meanwhile, the highest RNC values in fifth-order roots were observed in the HIT treatment (8.68 g kg−1 on average), followed by the LIT one (8.08 g kg−1 on average). Other than the fifth-order roots in the LIT treatment, thinning increased the RPC of all root sequences, whilst being significantly higher following MIT compared with the CK treatment (p < 0.05) (Figure 2c).
The root lignin concentration ranking of first- to fourth-order roots was MIT > HIT > LIT > CK (Figure 2d), and the lowest value of lignin concentration in fifth-order roots was observed in HIT (324.86 mg kg−1 on average), followed by the CK treatment (389.01 mg kg−1 on average) (Figure 2d). Overall, compared with the CK treatment, LIT, MIT, and HIT increased root cellulose concentration by approximately 36.94%, 89.86%, and 88.90% on average, as well as root NSC concentration by approximately 4.04%, 58.07%, and 20.41% on average. The root cellulose concentration of second- to fifth-order roots were highest in the LIT treatment, followed by the MIT and HIT treatments (Figure 2e). Meanwhile, the root cellulose concentration in first-order roots in the MIT treatment was the highest (225.09 mg kg−1 on average). In addition to the fourth-order roots, thinning increased the root NSC concentration among the other root orders. And the root NSC concentration of all root orders were highest in the MIT treatment (Figure 2f).

3.3. Soil Factors Affecting Fine Root Traits

The first and second axes of the redundancy analysis (RDA) accounted for 67.58% and 16.34% of the variations in fine root traits, respectively (Figure 3). The significant soil factors explaining the variation in fine root morphological and chemical traits across thinning intensities and root orders were temperature (R2 = 0.38, p < 0.001), nitrate (R2 = 0.57, p < 0.001), and MBC (R2 = 0.11, p < 0.05). The fine root chemical traits, including RCC, RNC, and root lignin and NSC concentrations, increased with soil temperature. Soil nitrate and MBC were essential factors driving changes in fine root morphological traits and nutrient concentrations.

4. Discussion

4.1. Fine Root Morpholofical Traits Variations

Our study suggested that forest thinning increased the RD of absorptive roots (1st–2nd-order roots) and decreased that of transport roots (3rd–5th-order roots), while the SRL showed the opposite variation trend. Fine root morphology is generally affected by soil nutrients and water content [35]. Plants strengthen the ability of fine roots to absorb nutrients quickly and efficiently by increasing the root length and surface area [52], thus supplying adequate nutrients for root growth in infertile soils, which is an adaptation mechanism of trees to environmental changes [25,36,53,54]. In the present study, forest thinning overall promoted soil nutrient level and reduced water content (Table 2). The decrease in stand and canopy density after thinning alters the forest microclimate, accelerates the decomposition of organic matter, and thus increases soil nutrient concentration [39,41]. Although thinning increased throughfall, the reduction in litter quality and the elevated temperature after thinning exacerbated soil moisture loss [55]. However, compared to soil water content, soil nutrients were more likely to affect fine root morphology (Figure 3). In the case where thinning optimized soil nutrient levels, plants had no occasion to append the investment in root length [56], resulting in the changes in absorptive roots morphology (Figure 1). According to the root economics spectrum [57], forest thinning alters the absorptive roots’ foraging strategy, with a tendency to change from resource acquisition to resource conservation.
Interestingly, unlike the SRL, the LIT and MIT treatments could increase SSA, especially the SSA of absorptive roots in the MIT treatment (Figure 1). This may be related to the mycorrhizal fungi of P. massoniana. A larger root surface area supplies a greater intraradical habitat for mycorrhizal fungal partners [58]. These symbioses with mycorrhizal fungi provide a new pattern for plant roots after thinning to obtain resources [59]. Similarly, the relatively higher SRLs and lower RTDs in the MIT treatment (Figure 1) indicated that plant roots acquired resources faster and more efficiently compared with other thinning intensities. Several studies have found that RTD was often negatively related with soil nutrient availability [60]. Roots with high RTDs were beneficial for conserving resources during resource-foraging periods in nutrient-deficient soils [61].

4.2. Fine Root Chemical Trait Variations

In our study, the RCC of absorptive roots increased after thinning, while the RCC of transport roots in the LIT and MIT treatments decreased. Forest thinning increased root lignin, cellulose, and NSC concentrations, with the highest values of those mostly occurring in the LIT or MIT treatments. Trees allocated more C to absorptive roots to absorb more nutrients and water, which further promoted root growth. The accumulation of elements in fine roots caused by thinning can be explained by root growth, element uptake, and translocation under reduced competition [18,62]. We found that thinning increased RNC and RPC in each root order, in addition to the fifth-order roots in the LIT and MIT treatments (Figure 2). This is attributed to a higher soil nitrate content and higher AP in the LIT and MIT treatments (Table 3). The relationship between soil nutrient availability and root nutrient concentration has been widely reported [2]. The soil nitrate content and AP in our plot had a positive influence on the RNC and RPC (Figure 3), which is consistent with previous studies [63]. Higher nitrate availability provided more nitrogen absorption for fine roots and helped with nitrogen storage in fine root tissues [64]. Accordingly, forest thinning could increase the RNC and RPC in first- to fourth-order roots via increasing soil nutrient availability.
To cope with changes in the external environment, plants modify the morphology and biomass of their fine roots to increase their utilization of topsoil resources, which requires a large amount of carbohydrates [60,65]. The degree of soil acidification usually increases with tree growth [66], and thinning in this study also reduced soil pH (Table 3). The increased free Al3+ concentration in the soil promoted plant roots to increase their root diameters and enhance stress resistance, thus increasing the structural carbohydrate concentrations of fine roots [67]. The higher concentration of nutrient elements in absorptive roots depends on greater transportation efficiency of nutrients from roots towards the aboveground mass, which also causes an increase in the lignin and cellulose concentration of fine roots [67]. NSCs, including starch and sugars, provide energy for root regeneration and resource absorption, generally closely related to root respiration [68,69]. In addition, the concentrations of sugar and starch in fine roots expressed different roles in root nutrient-acquisition strategies [70]. There is a need for more research to clarify the role of NSC in root strategies for resource acquisition altered by forest thinning.

4.3. Variations in Fine Root Traits with Root Order

We found that the RD and RTD increased and the SRL and SSA decreased with root order (Figure 1; Table 2). The RCC, cellulose, and NSC concentrations increased with root order and the RNC, RNP, and lignin concentrations decreased with root order (Figure 2; Table 2). Furthermore, the morphology and chemistry of low-order roots and high-order roots showed different changes in response to thinning intensity (Figure 1 and Figure 2). And our data showed that thinning intensity slightly alleviated the significant differences in fine root morphological and chemical traits among root branch orders (Table 3). This may be attributed to the variations in fine root anatomy and function in different root sequences [71]. Low-order roots have more cortex tissue and less secondary tissue and thus are mainly used to absorb resources [72]. The high root turnover and respiration rate of low-order roots requires considerable carbohydrates to be consumed. Correspondingly, roots normally reduce cell division and increase cell wall thickness to prevent water and nutrient loss from fine roots to the soil [73], which enables higher-order roots to better undertake the function of transporting these resources. Therefore, forest thinning was expected to regulate fine root morphology and chemistry among root orders by changing anatomical structures and participating in fine root dynamics.

4.4. Soil Factors Affecting Fine Root Morphology and Chemistry

Our results suggested that soil temperature was an essential soil factor affecting fine root chemical traits and had a positive effect on root chemistry (e.g., lignin and NSC). However, most studies believed that soil temperature decreased the root chemical concentration of fine roots [74,75], and some found that the changes in soil temperature had no significant effect on fine roots’ concentrations of structural carbohydrates and NSCs [76]. The difference in soil temperature between different thinning intensities was small in our study, which could have been responsible for the positive relationship between soil temperature and root chemistry across thinning intensities and root orders. Soil nitrate content not only affected the morphology of fine roots, but also had a significant positive impact on root cellulose concentration (Figure 3). Root lignin and cellulose concentrations are often negatively correlated with fine root decomposition rate [77]. The higher root cellulose concentrations in the LIT and MIT treatments may be a direct factor hindering fine root decomposition and nutrient release. Additionally, a significant effect of MBC on fine root morphological traits was observed in our study (Figure 3), consistent with other studies [33]. Root morphology is a strong determinant of rhizosphere microbial community composition [78]. Plant roots release a large amount of exudations as a source of energy and nutrition for microorganisms, causing them to passively gather around fine roots [56,79]. Thus, the morphology of fine roots determines the colonization probability and quantity of the surrounding microorganisms [80]. However, the complex relationship between fine root morphology and microbial community composition and structure is still poorly understood and requires further research.

5. Conclusions

Our research focused on the intraspecific variations in fine root morphology and chemistry among branch orders under different thinning intensities. The opposite responses of the RD and SRL of absorptive roots to different thinning intensities indicated that forest thinning might promote a shift in resource acquisition strategies for fine roots towards conservative strategies. Soil nitrate and MBC drove the fine root morphological traits and nutrient concentrations after thinning. The elevated soil temperature after thinning increased fine root lignin and NSC concentrations. Forest thinning intensity could mitigate the differences in fine root morphological and chemical traits among root orders.

Author Contributions

Conceptualization, J.Z. and Q.G.; methodology, M.W. and J.L.; software, X.S.; formal analysis, X.S.; investigation, J.Z., M.W. and J.L.; resources, J.W. and Q.G.; data curation, J.Z. and X.S.; writing—original draft preparation, J.Z. writing—review and editing, J.Z. and D.W.; funding acquisition, Q.G. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the National Natural Science Foundation of China (No. 31971453); the Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX22_1045); the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD); and the Scientific Studies of Higher Education Institution of Anhui Province (SK2021A1173).

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Effect of thinning on root diameter (a), specific root length (b), specific surface area (c), root tissue density (d) of different root orders. Values are means ± SE (n = 3). Different lowercase letters in the figure indicate significant differences of morphological traits among root orders under different thinning intensities (p < 0.05).
Figure 1. Effect of thinning on root diameter (a), specific root length (b), specific surface area (c), root tissue density (d) of different root orders. Values are means ± SE (n = 3). Different lowercase letters in the figure indicate significant differences of morphological traits among root orders under different thinning intensities (p < 0.05).
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Figure 2. Effect of thinning on root C concentration (a), N concentration (b), P concentration (c), lignin concentration (d), cellulose concentration (e), NSC (non-structural carbohydrate) concentration (f) of different root orders. Values are means ± SE (n = 3). Different lowercase letters in the figure indicate significant differences in fine root chemical traits among root orders under different thinning intensities (p < 0.05).
Figure 2. Effect of thinning on root C concentration (a), N concentration (b), P concentration (c), lignin concentration (d), cellulose concentration (e), NSC (non-structural carbohydrate) concentration (f) of different root orders. Values are means ± SE (n = 3). Different lowercase letters in the figure indicate significant differences in fine root chemical traits among root orders under different thinning intensities (p < 0.05).
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Figure 3. Redundancy analysis (RDA) for the fine root morphological and chemical traits constrained by soil properties. CK: no thinning; LIT: low-intensity thinning; MIT: middle-intensity thinning; HIT: high-intensity thinning. RD: root diameter; SRL: specific root length; SSA: specific surface area; RTD: root tissue density; RC: root C concentration; RN: root N concentration; RP: root P concentration; LIGNIN: root lignin concentration; CELLU: root cellulose concentration; NSC: root NSC (non-structural carbohydrate) concentration; Temp: soil temperature; WC: soil water content; BD: bulk density; SOC: soil organic C; Nitrate: soil nitrate; MBC: microbial biomass carbon; AP: available phosphorus.
Figure 3. Redundancy analysis (RDA) for the fine root morphological and chemical traits constrained by soil properties. CK: no thinning; LIT: low-intensity thinning; MIT: middle-intensity thinning; HIT: high-intensity thinning. RD: root diameter; SRL: specific root length; SSA: specific surface area; RTD: root tissue density; RC: root C concentration; RN: root N concentration; RP: root P concentration; LIGNIN: root lignin concentration; CELLU: root cellulose concentration; NSC: root NSC (non-structural carbohydrate) concentration; Temp: soil temperature; WC: soil water content; BD: bulk density; SOC: soil organic C; Nitrate: soil nitrate; MBC: microbial biomass carbon; AP: available phosphorus.
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Table 1. Stand characteristics (mean ± SD, n = 3) in Pinus massoniana plantation under different thinning intensities in 2020.
Table 1. Stand characteristics (mean ± SD, n = 3) in Pinus massoniana plantation under different thinning intensities in 2020.
CharacteristicsCKLITMITHIT
Stand density (tree ha−1)2591 ± 661944 ± 481453 ± 25948 ± 20
Tree DBH (cm)13.71 ± 1.5417.63 ± 0.9818.74 ± 3.6019.52 ± 3.96
Tree height (m)11.8 ± 2.1213.7 ± 1.6914.0 ± 2.7714.4 ± 3.62
Canopy density0.88 ± 0.010.80 ± 0.000.65 ± 0.010.50 ± 0.02
Understory coverage (%)51.3 ± 1.2362.1 ± 3.6167.6 ± 2.1780.5 ± 4.11
CK: no thinning; LIT: low-intensity thinning; MIT: middle-intensity thinning; HIT: high-intensity thinning; DBH: diameter at breast height. The abbreviations for thinning intensity (i.e., CK, LIT, MIT, and HIT) are the same as below.
Table 2. Soil properties (mean ± SE, n = 3) in Pinus massoniana plantation under different thinning intensities.
Table 2. Soil properties (mean ± SE, n = 3) in Pinus massoniana plantation under different thinning intensities.
Soil PropertiesCKLITMITHIT
Temperature (°C)25.91 ± 0.43 b26.12 ± 0.19 b26.98 ± 0.52 ab27.61 ± 0.69 a
Water content (%)24.98 ± 0.51 a24.11 ± 1.35 ab24.86 ± 0.82 a22.38 ± 1.01 b
pH4.56 ± 0.06 a4.53 ± 0.03 a4.47 ± 0.04 a4.48 ± 0.08 a
Bulk density1.11 ± 0.19 a1.08 ± 0.14 a1.04 ± 0.11 a1.05 ± 0.17 a
Organic C (g kg−1)28.73 ± 2.40 b34.33 ± 2.46 a30.6 ± 1.21 ab31.57 ± 2.10 ab
Total N (g kg−1)1.93 ± 0.15 b2.67 ± 0.15 a2.54 ± 0.12 a1.98 ± 0.06 b
Ammonium (mg kg−1)3.68 ± 0.39 b5.97 ± 0.36 a7.09 ± 0.70 a4.68 ± 0.89 b
Nitrate (mg kg−1)2.49 ± 0.05 b2.78 ± 0.35 b4.40 ± 0.17 a3.82 ± 0.58 a
Available P (mg kg−1)3.32 ± 1.21 a4.35 ± 1.32 a8.50 ± 3.08 a6.32 ± 2.31 a
Microbial biomass C (mg kg−1)623.59 ± 61.22 a759.79 ± 59.03 a689.81 ± 52.72 a637.38 ± 43.22 a
Microbial biomass N (mg kg−1)62.75 ± 17.60 b97.76 ± 16.76 a105.90 ± 14.03 a76.92 ± 7.36 ab
Different lowercase letters indicate significant differences under four thinning intensities (p < 0.05).
Table 3. Results of mixed models with sampling plot as a random effect for the effect of treatment and root order and their interactions on fine root morphological and chemical traits. F values are reported, with p values indicated as follows: * p < 0.05; ** p < 0.01; *** p < 0.001.
Table 3. Results of mixed models with sampling plot as a random effect for the effect of treatment and root order and their interactions on fine root morphological and chemical traits. F values are reported, with p values indicated as follows: * p < 0.05; ** p < 0.01; *** p < 0.001.
TreatmentRoot OrderTreatment × Root Order
Root diameter1.4246208.9307 ***0.8760
Specific root length4.2454 *259.0730 ***3.4064 **
Specific surface area6.7396 *326.8082 ***7.1374 ***
Root tissue density9.9696 **51.5888 ***0.9066
Root C 2.240018.6409 ***0.7702
Root N 2.51928.3423 *0.3854
Root P 24.1776 ***19.4464 ***1.8726
Root lignin12.6885 **21.3862 ***3.2998 **
Root cellulose27.1723 ***30.6402 ***1.1862
Root non-structural carbohydrate 15.0373 ***8.3388 ***0.9170
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Zhao, J.; Sun, X.; Wang, D.; Wang, M.; Li, J.; Wang, J.; Guan, Q. Responses of Fine Root Morphological and Chemical Traits among Branch Orders to Forest Thinning in Pinus massoniana Plantations. Forests 2024, 15, 495. https://doi.org/10.3390/f15030495

AMA Style

Zhao J, Sun X, Wang D, Wang M, Li J, Wang J, Guan Q. Responses of Fine Root Morphological and Chemical Traits among Branch Orders to Forest Thinning in Pinus massoniana Plantations. Forests. 2024; 15(3):495. https://doi.org/10.3390/f15030495

Chicago/Turabian Style

Zhao, Jiahao, Xiaodan Sun, Dong Wang, Meiquan Wang, Junjie Li, Jun Wang, and Qingwei Guan. 2024. "Responses of Fine Root Morphological and Chemical Traits among Branch Orders to Forest Thinning in Pinus massoniana Plantations" Forests 15, no. 3: 495. https://doi.org/10.3390/f15030495

APA Style

Zhao, J., Sun, X., Wang, D., Wang, M., Li, J., Wang, J., & Guan, Q. (2024). Responses of Fine Root Morphological and Chemical Traits among Branch Orders to Forest Thinning in Pinus massoniana Plantations. Forests, 15(3), 495. https://doi.org/10.3390/f15030495

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