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Article

Appropriate Removal of Forest Litter is Beneficial to Pinus tabuliformis Carr. Regeneration in a Pine and Oak Mixed Forest in the Qinling Mountains, China

by
Xueying Huo
,
Dexiang Wang
*,
Deye Bing
,
Yuanze Li
,
Haibin Kang
,
Hang Yang
,
Guoren Wei
and
Zhi Chao
College of Forestry, Northwest A&F University, Yangling 712100, China
*
Author to whom correspondence should be addressed.
Forests 2019, 10(9), 735; https://doi.org/10.3390/f10090735
Submission received: 21 July 2019 / Revised: 21 August 2019 / Accepted: 23 August 2019 / Published: 27 August 2019
(This article belongs to the Section Forest Ecology and Management)
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Abstract

:
Research Highlights: Natural regeneration is important in pine–oak mixed forests (Pinus armandii Franch., Pinus tabuliformis Carr., and Quercus aliena Bl. var. acuteserrata Maxim.ex Wenz.), but allelopathy as a limiting factor has not been studied. Our research provides insights into allelopathy in pine–oak mixed forest litter. Background and Objectives: Allelopathy among tree species occupying the same ecological niche in mixed forests may adversely affect regeneration. We studied allelopathy in pine and oak forest litter to determine the effect on regeneration, whether it is offset by adding activated carbon or plant ash, and what allelopathic substances are present. Materials and Methods: We used laboratory seed culture and field seeding to determine pine and oak litter regeneration effects on P. tabuliformis and P. armandii in the Qinling Mountains, China. In the laboratory, we irrigated seeds with three different litter concentrations. A fourth treatment incorporated activated carbon. The field study established small quadrats in mixed forest to study how removing or retaining litter and spreading plant ash affected sown seeds. High performance liquid chromatography–mass spectrometry was used to compare differences in chemical substances in extracts with and without activated carbon. Results: Litter extracts significantly affected germination rates in both species. Seedling morphological and physiological indexes showed that litter extracts negatively affected growth in both species, but activated carbon alleviated this inhibitory effect on P. armandii. Forest stand and litter did not affect P. armandii seed germination. Pinus tabuliformis germination rates were significantly higher in plots with removed litter than when litter was retained or plant ash spread, and lower in oak than pine forest. Allelopathic substances detected in pine forest were trioctyl trimellitate, amyloid β-Peptide 10–20, and triisobutyl phosphate, potentially affecting P. armandii seed germination and growth. Conclusions: Appropriate removal of litter in mixed forests can improve the natural regeneration ability of P. tabuliformis.

1. Introduction

Natural regeneration of tree species in forests is an important and complex ecological process [1]. It is not only the process by which forest ecosystems self-restore, but also forms the basis for maintaining their stability and sustainable utilization [2,3]. The continuum, development, or succession in time and space of woody plant populations have a profound influence on future community composition, succession pattern, promotion of forest resources, and biodiversity conservation in forests [4]. Natural regeneration in pine–oak mixed forests has therefore been the focus of global research into community succession and forest ecosystems research [5,6,7,8].
In China, the Qinling Mountain forest ecosystem is a natural secondary forest formed since the end of a period of intensive logging in the 1960s and 1970s [9]. About 40% of this area is occupied by pine–oak mixed forests (Pinus armandii Franch., Pinus tabuliformis Carr., and Quercus aliena Bl. var. acuteserrata Maxim.ex Wenz) [9], which form one of the most widely distributed, typical, and important community types in the forest ecosystem, and play an irreplaceable role in maintaining biodiversity and ecosystem services [10,11]. Natural regeneration of the dominant species of the pine–oak mixed forests community has an important influence on the formation, development, and stability of community structure [12], but is often unsuccessful due to certain limiting factors. Previous studies have mainly focused on resource limitation [9], animal diffusion [13], and environmental factors [12,14], but no research has been undertaken on allelopathy within the pine–oak mixed forests community.
Allelopathy, which exists widely in plants, refers to the direct or indirect effects that one plant has on others (including microorganisms) by secreting metabolites into the environment [15]. Allelopathy and competition among plants for light, water, nutrients, and space constitute the interactions affecting the distribution, formation, and succession of plant communities [16]. In North America, secondary compounds in the extract of beech leaves in late-succession forests inhibited the development of sugar maple seeding, suggesting that the influence of beech allelopathy on maple seedlings is a key factor hindering maple regeneration [17]. In south China, eucalyptus root systems had no effect on seed germination in four native tree species (Schima superba Gardn. Et Champ., Michelia macclurei Dandy, Cinnamomum burmanni (Nees et T. Nees) Blume, and C. camphora (L.) Presl), but inhibited seedling growth [18]. Similarly, Acacia dealbata Link controlled the growth of new conspecific seedlings beneath its own canopy to improve interspecific competitive performance in its adult plants within its non-native range [19]. Thus, community composition and coexistence in forest communities are regulated by certain allelopathy.
During tree growth, a large amount of litter is returned to the forest surface [20]. Many studies have shown that this litter produces a series of intermediate products during decomposition, some of which may have an impact on forest regeneration and seedling germination and growth [21,22]. The litter of three main tree species (pitch pine, huckleberry and white oak) in New Jersey had no effect on seed germination in pitch pine, but significantly inhibited seedling growth [23]. Methanol–water extract derived from Japanese red pine litter had an inhibitory effect on cress and Digitaria sanguinalis (L.) Scop., indicating that the pine litter contained substances with allelopathic activity [24]. Coincidentally, the observation that Acacia tortilis seedlings do not naturally grow under Prosopis Linn. canopies suggests the influence of Prosopis litter allelopathy on A. tortilis seed germination as a partial explanation [25]. Thus, we suspect that the natural regeneration of pine species in pine–oak mixed forests communities may be affected by allelopathy via the litter.
Activated carbon with an adsorption function can be used to reduce allelopathy between different species [26]. Allelopathy in garlic mustard (Alliaria petiolata (M.Bieb.) Cavara & Grande) poses a serious threat to the native vegetation of North American woodlands, where it is an invasive species; however, the addition of activated carbon may counteract the inhibitory effect on seed germination [27]. Similarly, applying activated carbon in the presence of A. petiolata was beneficial to the growth of the native plant Impatiens capensis Meerb. [28]. The experimental use of activated carbon on farmland dominated by invasive species for 47 consecutive years showed that activated carbon effectively reduced the frequency of invasive species and increased native species richness [29]. Therefore, activated carbon is a key tool in verifying the existence of allelopathy.
In this study, we used a novel method that combined the adsorption properties of activated carbon in a bioassay to test the allelopathy of water extract from pine and oak forest litter, with and without activated carbon, on seed germination and seedling growth in P. tabuliformis and P. armandii. To further verify the experimental results, we designed a field experiment in pine–oak mixed forest on the south slope of the Qinling Mountains. Three sample types were established under each stand (litter removing, litter retained, and plant ash added). In addition, high performance liquid chromatography–mass spectrometry (HPLC-MS) was used to compare differences between chemical substances found in extracts with and without activated carbon. We tested the following three hypotheses: (1) allelopathy in the litter of mixed pine and oak forests influences regeneration in P. tabuliformis and P. armandii within the community; (2) activated carbon or plant ash can either slow down or offset the inhibitory effect of extracts on seedlings through adsorption of allelopathic substances; and (3) several specific allelopathic substances are present in the litter of pine–oak mixed forests.

2. Materials and Methods

2.1. Collection of Leaf Litter, Soil, and Seeds

With reference to Whitmore’s description of forest mosaics, we divided the pine–oak mixed forest of the Qinling Mountains (108°21′–108°39′ E, 3°18′–33°28′ N) into pine and oak forest [30]. Leaf litter and soil (depth, 0–10 cm) were collected under the pine and oak forest canopies in the autumn of 2018. Leaf litter samples were oven-dried and stored in paper bags. Soil samples were refrigerated at −4 °C immediately on return to the laboratory, until required for the experiment. Seeds were taken from cones newly harvested in autumn 2018.

2.2. Preparation of Water Extracts

The collected dead leaves were screened and divided into two parts: the first part was soaked in deionized water for 24 h with water (1:10), and activated carbon (1% of the litter mass) was added to the second before soaking. Using a qualitative filter paper for the first filtration, and filter paper comprising 0.45 µm microporous membrane after the suction filter, the soaked solutions were poured into a brown glass bottle and sterilized at a low temperature of 2 °C in the refrigerator. At the beginning of the experiment, the mother liquor without added activated carbon was diluted with distilled water to different concentration gradients (0.02 g mL−1, 0.05 g mL−1, and 0.1 g mL−1). The extraction solution with activated carbon was not diluted, and was irrigated directly. We then repeated this same method for the soil collected from the forest.

2.3. Cultivation and Germination of Seeds

The sand culture method was used for seed germination. A germination bed was constructed of filter paper and Petri dishes sterilized at 170 °C: two layers of filter paper were placed in a prepared Petri dish, an amount of water appropriate to wet the filter paper was added, and then fine sand was sieved and placed in each dish to a depth of 1–2 cm, after which 30 treated seeds were added.
The two seed types (P. armandii and P. tabuliformis) were irrigated with four types of extracts: soil extract from oak forest, litter extract from oak forest, soil extract from pine forest, and litter extract from pine forest. Seeds watered with the same extract type were further subdivided into four groups to which different extract concentrations were applied: 0.02 g·mL−1 (T1), 0.05 g·mL−1 (T2), 0.1 g·mL−1 (T3), and 0.1 g·mL−1 + activated carbon (T4). Each treatment was repeated three times.
The experiments were placed in an artificial climate chamber with a humidity of 70% (25 °C, 12 h light/18 °C, 12 h dark). The number of germinated seeds was counted each day until a stable level was reached. After completion of the germination experiment, root length, seedling height, and malondialdehyde (MDA) content of seedlings were determined.

2.4. Field Seeding

Twelve sample plots (1 m × 1 m) were selected from each of the pine and oak forest areas for the seeding experiment, ensuring that groups of three samples were located in the same 20 m × 20 m large sample, and with similar conditions of light and other environmental factors. In each of these groups, one sample plot was treated by removing litter, litter was retained on a second plot, and plant litter ash (produced by burning) was added to the third (Figure 1). Each treatment was repeated four times and there are eight large squares (20 m × 20 m). Pinus armandii and P. tabuliformis seeds were sown on the left and right side of each sample square, respectively. All seeds were covered with barbed wire to protect them from rodents.

2.5. Identification of Water Extracts

Dry extract was obtained by low-temperature distillation of the litter and soil water extract samples filtered through a 0.45 µm microporous membrane; 0.1 g of concentrated water extract was then dissolved in 100 mL methanol, an ultrasound was conducted for 30 min, and the supernatant was taken as a reserve. A Kromasil C18 chromatographic column was used, and the detection wavelength was 254 nm. The mobile phase was methanol–water containing 0.02 mol L−1 tetraethyl iodide (20:80 V/V). The mass spectrometry condition was electrospray ionization, and the positive ion was detected by the full-scanning method, with a mass range of 60–1000 amu. In the bioassay experiments, if the addition of activated carbon significantly alleviated the inhibitory effect of the extract, we believed that the allelochemicals were adsorbed by activated carbon. By comparing the specific types of chemical substances in the water extracts with and without activated carbon, the allelopathic substances that exert allelopathy in pine forest litter can be determined.

2.6. Statistical Analysis

All data analyses were performed using SPSS 23.0 (SPSS Inc., Chicago, IL, USA), the difference between treatment groups was compared using a least significant difference (LSD) test, and the significance level was α = 0.05. The effect of different concentrations on seed germination and seedling growth of recipient plants was determined using a one-way analysis of variance (ANOVA). All the charts were completed using Origin 9.1 (OriginLab Corporation, Northampton, MA, USA).

3. Results

3.1. Effects of Different Treatments on P. tabuliformis and P. armandii Seeds

3.1.1. Germination Rates

Our findings revealed no significant differences among the soil extracts of pine and oak forests for the seed germination rate of the two seed types, which may be related to the lower concentration of allelochemicals in the soil. In contrast, when P. tabuliformis and P. armandii seeds were irrigated with pine and oak forest litter extracts, seed germination was inhibited at the highest concentration (Table 1). The addition of activated carbon only played a role in slowing the inhibition rate when P. armandii seeds were irrigated with pine soil and litter extracts; this showed that the activated carbon adsorbed allelopathic substances from the water extract. However, we also observed that the inhibitory effect was significantly enhanced after the addition of activated carbon (when the soil extract of oak was used to water P. tabuliformis seeds), which may be related to the decrease in organic nutrients in the soil water extract.

3.1.2. Root Length

When the soil extract from the oak forest was used to water the seeds of P. tabuliformis, the root length did not change significantly, but the addition of activated carbon significantly inhibited root elongation (Figure 2a), which was consistent with the effects on seed germination. The root length was significantly inhibited when P. tabuliformis seeds were watered with different concentrations of litter water extract from the oak forest (Figure 2a), which may be related to the higher concentration of allelochemicals in the litter. Similar to P. tabuliformis, P. armandii had no significant change in the root length when treated with soil extracts of three concentrations from oak and pine forests. When the litter extracts of pine and oak forests were applied at a high concentration, it inhibited root elongation (T3) (Figure 2b). We observed that the allelopathic effect has certain concentration dependence. Activated carbon significantly reduced the inhibitory effect only when P. armandii seeds were irrigated with the soil and litter water extracts of pine forest (Figure 2b), which showed that the activated carbon adsorbed allelopathic substances from the water extract.

3.1.3. Seedling Height

When treated with oak forest litter extract, the seedling height of P. tabuliformis was consistent with the germination rate and root length, and was significantly inhibited. However, the addition of activated carbon alleviated the inhibition of seedling growth to some extent (Figure 3a), indicating that the sensitivity of seedling height was not as high as that of the germination rate and root length. There were no significant differences among the soil extract of pine and oak forests for the seedling height of P. tabuliformis, and the same effect was observed when P. armandii seeds were irrigated with these two extracts (Figure 3a,b).When the oak forest litter extract was used to treat P. armandii seeds, the seedling height did not show a significant inhibitory effect under high concentration of water extract, similar to the germination rate and root length (Figure 3b). Furthermore, the addition of activated carbon not only alleviated the inhibition of seedling height in P. armandii treated with the pine forest litter extract, but also significantly improved the seedling height of P. armandii seeds treated with pine forest soil extract (Figure 3b). This again proves that the effect of seedling height on allelopathic effects is not as sensitive as the germination rate and root length, and its own inhibition can be easily relieved.

3.1.4. Malondialdehyde Content

The MDA content reflects the degree of peroxidation of plant cell membranes; a high MDA content indicates high peroxidation and that injury is serious. The MDA content in P. tabuliformis seeds was not significantly different when treated with the three concentrations of oak forest soil extract. However, activated carbon significantly increased the MDA content in P. tabuliformis seedlings (Figure 4a). This physiological index confirmed the germination rate and morphological index results. The addition of activated carbon reduced the content of MDA in P. tabuliformis seedlings watered by two kinds of extracts of pine forest to a certain extent (Figure 4a), showing that it adsorbed some organic components, which inhibited growth. When pine forest litter extract was used to treat the seeds of P. armandii, the content of MDA increased significantly at a high concentration, but there was no significant change in the content of MDA when the seeds were treated with the other three types of extracts (Figure 4b). The addition of activated carbon significantly reduced the MDA content in the seed of P. armandii treated with litter extract of pine forest (Figure 4b), indicating that activated carbon adsorbed allelopathic substances affecting P. armandii.

3.2. Seed Germination in the Field Experiment

The germination rate of P. armandii seeds was not affected by litter, while the germination rate of P. tabuliformis seeds in the two stands after litter removal was significantly higher than that under the other two treatments, indicating that P. tabuliformis seeds with thin seed coats are more susceptible to the litter. However, the two stands had negligible effect on the germination rate of P. armandii seeds, but exerted a significant effect on P. tabuliformis seeds. Furthermore, the germination rate of P. tabuliformis seeds was considerably lower in the oak forest than in the pine forest, which may be related to the small size of P. tabuliformis seeds as they are more susceptible to physical obstruction of broadleaf litter (Table 2).

3.3. Allelochemicals in Pine Forest Litter

In our bioassay experiment, the addition of pine forest litter extract with activated carbon reduced the negative effect on the seed germination rate and seedling growth in P. armandii and P. tabuliformis, indicating that activated carbon adsorbs allelochemicals in the litter. Therefore, by comparing the specific types of chemical substances in the water extracts with and without activated carbon, the allelopathic substances that exert allelopathic effects in pine forest litter can be determined. According to the results of HPLC-MS, the allelopathic substances in the pine litter of the mixed Pinus forests in the Qinling Mountains are trioctyl trimellitate, amyloid β-peptide 10–20, and triisobutyl phosphate (Figure 5).

4. Discussion

4.1. Effect of Leaf Litter Water Extract on Seed Germination and Initial Growth

As a result of intraspecific or interspecific competition, plants secrete secondary capital products, which are distributed among the branches, leaves, stems, and litter, which enhances their competitiveness [31,32]. Litter decomposition and transformation cause allelochemicals to be released either directly or by changing inactive into active substances, therefore affecting the growth of surrounding plants; this is a very common way to release allelopathic substances [33]. In the bioassays used in the experiment to determine allelopathy, the litter water extract from both pine and oak forests significantly inhibited germination and initial growth in both seed types at high concentrations, which may be related to secondary metabolites in the litter. Our results are in agreement with the reports from other studies, i.e. allelopathy frequently depends on allelochemical concentrations [34]. Studies have shown that allelochemicals inhibit the synthesis of indoleacetic acid and gibberellin, thus hindering germination in target plants [35]. Similarly, allelochemicals may affect plant photosynthesis, and further alter cell respiration and metabolism, thereby affecting plant growth [36]. These studies on allelopathic mechanisms support our experimental results.
Activated carbon can inactivate organic molecules due to its strong adsorption capacity [37]. In the allelopathy experiment, the addition of activated carbon in the bioassays alleviated the inhibitory effect of pine forest litter extract on P. armandii and P. tabuliformis, but not that of oak forest litter extract, which may be related to the amount of added activated carbon being too small to completely absorb organic substances in oak forest. Previous studies have found that the addition of activated carbon can alleviate root interactions and self-toxicity in larch [38]. When activated carbon was added to the growth medium in an experiment with canola, the density and affinity reaction disappeared, indicating that activated carbon played a neutralizing role and inactivated organic allelopathic substances released by the root system [38]. In our study, all the evidence indicated that the germination and growth patterns of P. tabuliformis and P. armandii seeds were in response to water litter extracts that contained allelochemicals.

4.2. Allelopathy of Pine and Oak Forest Litter in the Field Experiment

As the allelopathy studies mentioned in the literature have mostly been carried out under controlled conditions [17,23], little consideration has been given to whether allelopathic substances in their natural state exhibit allelopathic activity and exert allelopathic effects. We therefore conducted the field seeding experiment with different litter treatments, in order to verify the results of the laboratory-based biological determination. Our field experiments on litter removal showed that it increased the germination rate of P. tabuliformis significantly in two stands, but had no effect on P. armandii, indicating that P. tabuliformis may be more susceptible to the influence of litter because of its thin seed coat and other characteristics. These findings could possibly be related to allelopathic substances entering the soil and becoming subject to adsorption, desorption, degradation, and other effects, and the migration and residence time of allelopathic substances in the soil being extended, even affecting the expression of allelopathic activities [39,40]. The results of other studies confirm that the concentration of allelopathic substances under natural conditions is much lower than in laboratory experiments [41]. Of course, the results may also be related to the fact that the litter provides a suitable micro-habitat of water and temperature to offset the allelopathic effect.
Plant ash is the residue of burned plants (herbs and woody plants) that can act as a source of adsorbents and nutrients. In the field experiment, we collected litter from under the forest canopy, burned it under certain conditions to obtain plant ash, and dispersed it in the retained litter plot square, in an attempt to alleviate the allelopathic effect of litter on seeds. The results were not, however, significant. This indicated that the inhibition effect of litter on P. tabuliformis seed might be related to allelopathy and biofiltration. The physical and chemical effects of litter on seedling emergence have been studied using natural and plastic litter, concluding that the short-term effects of Chinese fir litter on seedlings are mainly physical [42]. Similarly, many previous studies have shown that the influence of litter on seed and seedling growth exerts physical hindrance as well as allelopathic effects [43,44,45]. Therefore, the physical and chemical characteristics of litter have an ecological filtering effect on the regeneration of understory seedlings.

4.3. Allelopathic Substances that Exert Allelopathic Effects in Pine Forests

In another study, allelochemicals were divided into water-soluble organic acids, aliphatic aldehydes, ketones, aliphatic alcohols, simple unsaturated lactone, long chain fatty acids, acetylene, quinones, phenol, benzoic acid and its derivatives, cinnamic acid and its derivatives, purine nucleoside and coumarin, flavonoids, tannins, alkaloids and cyanohydrin, amino acids and peptides, sulfide, and glucosinolate [15]. The allelochemicals studied are diverse in the context of different research purposes and objectives, but all belong to the above categories.
The bioassay of litter and soil water extract with and without activated carbon showed that activated carbon could slow the inhibitory effect of pine forest litter water extract on the two seed species, indicating that it adsorbed allelochemicals in pine forest litter. Then, the water extracts with and without activated carbon were investigated using HPLC-MS; the allelopathic substances in pine forest litter were determined to be trioctyl trimellitate, amyloid β-Peptide 10–20 and triisobutyl phosphate. A prior study had found that esters and amino acids have strong allelopathic potential [46]. In an earlier study, the allelochemicals in flue-cured tobacco root zone soil were determined by HPLC, and the results showed that tobacco regeneration failure was related to ester allelopathic substances secreted by tobacco [47]. Similarly, in another study, Codonopilate A, a triterpenyl ester, was isolated from monocultivated soil of annual Codonopsis pilosula (Franch.) Nannf. and identified as the main autotoxin [48]. An analysis using protoplast co-culture method with digital imaging indicated that canavanine was the allelochemical in Vicia villosa Roth epicotyl protoplasts in etiolated seedlings, but its effect differed according to the developmental stage of the recipient plant [49]. Therefore, it can be observed that esters and amino acids exert allelopathic effects, further confirming our experimental results.

5. Conclusions

Esters and amino acids were detected in pine forest (P. tabuliformis and P. armandii) litter, but the litter naturally accumulated only inhibited seed germination of P. tabuliformis at a small seed volume, and had no significant effect on seed germination of P. armandii. The litter in the pine–oak mixed forest has not only the potential to exert allelopathic effects, but it also serves as an ecological filtration barrier for the regeneration of P. tabuliformis seeds with very small individual sizes. Therefore, appropriate removal of litter under the forest canopy can improve the natural regeneration ability of P. tabuliformis.

Author Contributions

Conceptualization, X.H.; methodology, X.H.; software, Y.L.; validation, X.H., D.B. and Y.L.; investigation, D.B., G.W., and Z.C.; data curation, X.H.; writing—original draft preparation, X.H.; writing—review and editing, H.K. and H.Y.; supervision, D.W.; and project administration, D.W.

Funding

The authors are grateful for the financial support from the National Natural Science Foundation of China and responses of regeneration pattern of constructive species in pine and oak forest to seeds dispersal process and influencing factors in Qinling Mountains (grant number 31470644).

Acknowledgments

The authors thank three anonymous reviewers for valuable comments on the manuscript and Editage (www.editage.cn) for English language editing.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Schematic diagram of the quadrat design used in the field sowing experiment.
Figure 1. Schematic diagram of the quadrat design used in the field sowing experiment.
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Figure 2. Effect of soil and litter water extracted from pine and oak forests on the root length of: Pinus tabuliformis (a); and P. armandii (b). T1 (concentration of 0.02 g·mL−1), T2 (0.05 g·mL−1), T3 (0.1 g·mL−1), and T4 (0.1 g·mL−1 + activated carbon). The data indicate mean ± SE (n = 3). Different letters in inset plots indicate significant differences at p < 0.05.
Figure 2. Effect of soil and litter water extracted from pine and oak forests on the root length of: Pinus tabuliformis (a); and P. armandii (b). T1 (concentration of 0.02 g·mL−1), T2 (0.05 g·mL−1), T3 (0.1 g·mL−1), and T4 (0.1 g·mL−1 + activated carbon). The data indicate mean ± SE (n = 3). Different letters in inset plots indicate significant differences at p < 0.05.
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Figure 3. Effect of soil and litter water extracted from pine and oak forests on seedling height of: Pinus tabuliformis (a); and P. armandii (b). T1 (concentration of 0.02 g·mL−1), T2 (0.05 g·mL−1), T3 (0.1 g·mL−1), and T4 (0.1 g·mL−1 + activated carbon). The data indicate mean ± SE (n = 3). Different letters in inset plots indicate significant differences at p < 0.05.
Figure 3. Effect of soil and litter water extracted from pine and oak forests on seedling height of: Pinus tabuliformis (a); and P. armandii (b). T1 (concentration of 0.02 g·mL−1), T2 (0.05 g·mL−1), T3 (0.1 g·mL−1), and T4 (0.1 g·mL−1 + activated carbon). The data indicate mean ± SE (n = 3). Different letters in inset plots indicate significant differences at p < 0.05.
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Figure 4. Effect of soil and litter water extracts from pine and oak forests on the MDA content in seedlings: of Pinus tabuliformis (a); and Pinus armandii (b). T1 (concentration of 0.02 g·mL−1), T2 (0.05 g·mL−1), T3 (0.1 g·mL−1), and T4 (0.1 g·mL−1 + activated carbon). The data indicate mean ± SE (n = 3). Different letters in inset plots indicate significant differences at p < 0.05.
Figure 4. Effect of soil and litter water extracts from pine and oak forests on the MDA content in seedlings: of Pinus tabuliformis (a); and Pinus armandii (b). T1 (concentration of 0.02 g·mL−1), T2 (0.05 g·mL−1), T3 (0.1 g·mL−1), and T4 (0.1 g·mL−1 + activated carbon). The data indicate mean ± SE (n = 3). Different letters in inset plots indicate significant differences at p < 0.05.
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Figure 5. Structural formula of three allelochemicals in pine forest litter of the mixed forests in the Qinling Mountains.
Figure 5. Structural formula of three allelochemicals in pine forest litter of the mixed forests in the Qinling Mountains.
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Table
Table 1. Germination rate of seeds under different treatments. CK (control), T1 (concentration of 0.02 g·mL−1), T2 (0.05 g·mL−1), T3 (0.1 g·mL−1), and T4 (0.1 g·mL−1 + activated carbon). The data indicate mean ± SE (n = 3). Different letters in inset plots indicate significant differences at p < 0.05.
Table 1. Germination rate of seeds under different treatments. CK (control), T1 (concentration of 0.02 g·mL−1), T2 (0.05 g·mL−1), T3 (0.1 g·mL−1), and T4 (0.1 g·mL−1 + activated carbon). The data indicate mean ± SE (n = 3). Different letters in inset plots indicate significant differences at p < 0.05.
Tree SpeciesComponentSampleGermination Rate (%)
CKT1T2T3T4
Pinus tabuliformisOak forestSoil61.11 ± 2.94a63.33 ± 3.85a68.89 ± 1.11a61.11 ± 2.22a48.89 ± 5.88b
Litter61.11 ± 2.94a53.33 ± 5.09ab54.44 ± 4.84ab43.33 ± 5.77bc36.67 ± 1.93c
Pine forestSoil52.22 ± 4.01a52.22 ± 4.84a44.45 ± 2.22a50.00 ± 3.85a51.11 ± 2.94a
Litter52.22 ± 4.01ab54.45 ± 2.22a36.67 ± 1.93c41.67 ± 2.89bc44.44 ± 2.94bc
Pinus armandiiOak forestSoil61.11 ± 2.94a56.67 ± 1.93a51.67 ± 5.85a53.34 ± 3.33a60.00 ± 1.92a
Litter61.11 ± 2.94a61.67 ± 5.36a38.33 ± 4.40b38.89 ± 4.01b38.33 ± 1.67b
Pine forestSoil37.78 ± 2.22a32.22 ± 6.19a32.22 ± 4.45a30.00 ± 1.92a37.78 ± 7.29a
Litter37.78 ± 2.22a28.89 ± 4.01a36.67 ± 3.33a12.22 ± 2.94b36.67 ± 5.77a
Table
Table 2. Germination rate in the field seeding experiment. The data indicate mean ± SE (n = 4). Different letters in inset plots indicate significant differences at p < 0.05.
Table 2. Germination rate in the field seeding experiment. The data indicate mean ± SE (n = 4). Different letters in inset plots indicate significant differences at p < 0.05.
Seed CategoriesPine ForestOak Forest
Remove LitterKeep LitterPlant AshRemove LitterKeep LitterPlant Ash
Pinus armandii85.00 ± 6.31a85.83 ± 3.70a89.17 ± 3.70a84.17 ± 6.85a75.00 ± 3.47a78.33 ± 7.52a
Pinus tabuliformis77.78 ± 1.11a50.00 ± 8.92b47.50 ± 7.50b57.50 ± 3.70a20.00 ± 3.60b23.33 ± 3.85b

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MDPI and ACS Style

Huo, X.; Wang, D.; Bing, D.; Li, Y.; Kang, H.; Yang, H.; Wei, G.; Chao, Z. Appropriate Removal of Forest Litter is Beneficial to Pinus tabuliformis Carr. Regeneration in a Pine and Oak Mixed Forest in the Qinling Mountains, China. Forests 2019, 10, 735. https://doi.org/10.3390/f10090735

AMA Style

Huo X, Wang D, Bing D, Li Y, Kang H, Yang H, Wei G, Chao Z. Appropriate Removal of Forest Litter is Beneficial to Pinus tabuliformis Carr. Regeneration in a Pine and Oak Mixed Forest in the Qinling Mountains, China. Forests. 2019; 10(9):735. https://doi.org/10.3390/f10090735

Chicago/Turabian Style

Huo, Xueying, Dexiang Wang, Deye Bing, Yuanze Li, Haibin Kang, Hang Yang, Guoren Wei, and Zhi Chao. 2019. "Appropriate Removal of Forest Litter is Beneficial to Pinus tabuliformis Carr. Regeneration in a Pine and Oak Mixed Forest in the Qinling Mountains, China" Forests 10, no. 9: 735. https://doi.org/10.3390/f10090735

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