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Article

The Characteristics and Influential Factors of Earthworm and Vermicompost under Different Land Use in a Temperate Area, China

by
Li Ma
1,
Ming’an Shao
2,3,
Yunqiang Wang
4,
Tongchuan Li
2,*,
Xuanxuan Jing
1,
Kunyu Jia
1 and
Yangyang Zhang
1
1
Key Laboratory of Disaster Monitoring and Mechanism Simulating of Shaanxi Province, Baoji University of Arts and Sciences, Baoji 721013, China
2
State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water Conservation, Chinese Academy of Sciences and Ministry of Water Resources, Xianyang 712100, China
3
Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographical Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
4
State Key Laboratory of Loess and Quaternary Geology, Institute of Earth Environment, Chinese Academy of Sciences, Xi’an 710061, China
*
Author to whom correspondence should be addressed.
Forests 2024, 15(8), 1389; https://doi.org/10.3390/f15081389 (registering DOI)
Submission received: 14 May 2024 / Revised: 18 July 2024 / Accepted: 5 August 2024 / Published: 8 August 2024
(This article belongs to the Special Issue Agroforestry Soil Fertility Monitoring and Management)
Browse Figures
Review Reports Versions Notes

Abstract

:
Earthworm communities influence soil carbon and nitrogen circulation by altering the diversity and composition of microbial communities, which improves soil fertility. Studying the soil nutrient composition and bacterial communities change in response to earthworm community natural invasion may be key to exploring earthworm ecological functions and accurately assessing C and N mineralization in artificial forests and croplands. In this study, we examined the communities of five earthworm species in ecosystems characterized by six different land-use types, such as buttonwood forest, walnut forest, apple orchard, kiwi orchard, ryegrass land, and corn field. The Metaphire baojiensis (d) and Amynthas carnosus planus were dominant earthworm species. Among different land-use types, earthworm densities ranged from 2 to 27 ind·m−2 in summer and 15 to 40 ind·m−2 in spring. However, surface vermicompost weight in summer (296.7 to 766.0 g·m−2) was greater than in spring. There was a positive correlation between the weight of the vermicompost and earthworm numbers in the same season. Soil carbon (C) and total nitrogen (N) of vermicompost ranged from 5.12 to 20.93 g·kg−1 and from 0.52 to 1.35 g·kg−1, respectively. Compared with soil, the contents of vermicompost C and N increased 2.0 to 4.3 times and 1.6 to 7.7 times, respectively. The average C/N of vermicompost (9.5~23.5) was higher than in the soil (7.3~19.8). Due to the higher abundances of C and N in the soil of corn fields and kiwi orchards, which cultivate higher abundances of earthworms and more vermicompost, the C and N and C/N of vermicompost is higher than in the soil. C and N were accumulated by earthworms’ excreting and feeding activity instead of vegetation in vermicompost. Earthworm community structure plays key roles in decreasing bacterial diversity and adding Proteobacteria, Actinobacteria, Acidobacteria, Bacteroidetes, and Chloroflex in vermicompost, resulting in enriching soil C and N content and increasing C/N in vermicompost. Therefore, the evaluation of different vegetation ecosystems in soil C and N pool accumulation and mineralization should be given more attention regarding the function of earthworm communities in the future.

1. Introduction

The community composition (diversity, biomass, abundance, ecological categories) and activities (excretion and feeding behaviors) of earthworms are typically influenced by their living natural environment [1]. Philips [2] reported that climate variables are more important in shaping earthworm communities than soil properties. The optimal temperature ranged from 12 to 20 °C for earthworms. In a sufficient soil water content condition, there was a positive relationship between abundance, biomass, and activity of earthworms and temperature [3]. In addition, the type of land use can indirectly affect earthworm communities’ biology and populations by species diversity, food supply, and habitat cover [4]. Specifically, in the forest soil carbon research field, leaf litter and roots derived carbon can provide a food source for earthworms [5].
At the same times, earthworms change soil structure, soil water, nutrient cycles, and improve plant growth [6,7,8,9]. Earthworms can significantly increase the organic carbon (C) and total nitrogen (N) contents of soil and maintain the stability of C/N by feeding, decomposing, and transforming themselves [10]. Earthworm activity contributes to the conversion of relatively recalcitrant N to more available forms that more readily utilize plants [11] and increase the exchangeable P content of soil [12,13]. Specifically, the walls of their burrows are richer in organic matter and nutrient substances than is the surrounding soil [14,15]. They have also been found to alter the composition of the microbial community (bacteria, fungi, and archaea) [16], thereby contributing to an enhancement of nutrient cycling [17,18,19,20]. Earthworms can also interact with other soil animals and microbial communities via belowground soil food webs [7], thereby contributing to an increase in C or N.
In natural soil ecosystems, earthworm communities produce an important metabolite, referred to as “vermicompost”, the output of which has been estimated to range from 36 to 108 g·ha−1·yr−1 in temperate areas [21]. Given its rich nutrient content, including soil C, N, P, and potassium (K) content; humic acid; different amino acids; and trace elements, vermicompost is an excellent organic fertilizer [22]. It is estimated that the total N produced by the earthworm community can reach between 30 and 50 kg·ha−1·year−1 [23]. It has been reported that vermicomposting technology is wildly used for agricultural and industrial wastes due to its efficient nutrient recovery potential and pollutant remedial role [24]. Some researchers have suggested that vermicompost also serves as a water-stable soil aggregate that protects soil organic matter and reduces the rate of mineralization in the soil biogeochemical cycle [23,25]. Furthermore, other researchers have reported that the soil digested by earthworms contains larger microbial populations, not only in terms of a larger number of species but also regarding their abundances and activities [26]. However, these findings have generally been based on studies that have focused on the earthworms in European and American area or in a single category test. However, there were few reports on the study of common native earthworms in a temperate area of China. Usually, earthworms live in mixed-category communities in natural systems.
Formerly, the effects of earthworms and vermicompost on soil have often been most studied separately; thus, the proportionate contribution of vermicompost to background soil nutrients has yet to be sufficiently clarified for natural eco-environments. Given the aforementioned considerations, the objectives of this study were to (1) investigate earthworm communities (species and populations) in temperate artificial ecosystems in China, which will provide basic data for earthworm research; (2) examine the main factors influencing earthworm communities and vermicompost distribution; and (3) explore C and N accumulation in the soil from the perspective of the roles that bacteria have in order to reveal the part played by earthworms in soil nutrition accumulation and mineralization in different land-use types.

2. Materials and Methods

2.1. Study Site

This study was conducted within the framework of a project investigating the ecosystem responses to an exotic earthworm invasion in the Guanzhong Plain, Northwest China in June 2022 and April 2023. The climate is temperate continental monsoon. The average annual temperature of the region is 12 °C, and annual precipitation is approximately 680–750 mm. It is supplied an optimal survival environment for earthworms in this region, owing to the flat terrain, diverse land-use types, good weather conditions, and fertile soil.

2.2. Experimental Design and Sample Preparation

Six representative land-use types, named buttonwood forest (BS), walnut forest (WS), apple orchard (AS), kiwi orchard (KS), ryegrass land (RS), and corn field (CS), in the Baoji region were selected for field surveys. In each land-use type, we established five randomly distributed 1.0 × 1.0 m plots for determining earthworm community and vermicompost characteristics. Earthworms were collected by excavating and manual sorting in soil depth from 0 cm to 50 cm, and soil adhering to body surfaces of earthworm was washed away. Sexually mature earthworms of different colors were selected and preserved in ethanol for gene detection with tagging to determine the species. In each plot, soil surface vermicompost was collected manually, and soil samples were collected at 10 cm depth intervals from 0 to 100 cm using a soil auger. Surface impurities were removed from soil samples by passing them through a 0.25 mm sieve, and the sieved samples were thereafter used to determine the pH and the contents of soil organic carbon (SOC) and total N. SOC was determined using the potassium dichromate oxidation-external heating method; total N was determined using the Kjeldahl method. Meanwhile, soil water content, soil particle-size distribution, pH, and bulk density were measured in different land-use soil types. The average values of physical and chemical properties of the soil samples collected from these sites are listed in Table 1.
The soil microbial abundance was determined commercially by Shanghai Pineno Biotechnology Co., Ltd. (Shanghai, China). Briefly, total DNA was extracted from soil samples using an Omega Soil DNA Kit (Omega Biotek, Norcross, GA, USA) and quantified using a Nanodrop 2000 spectrophotometer (SeymerFisher Technology, Waltham, MA, USA) according to the manufacturer’s instructions. The integrity of the extracted DNA was determined by electrophoresis using a 1.2% agarose gel. A sample-specific barcode sequence (338 F: 5′-ACTCCTACGGGAG-GCAGCA-3′, 806R: 5′-CGGACTACH-VGGGTWTCTAAT-3′) was used to carry out PCR amplification on the 16S rRNA specific gene segment V3–V4 using Pfu high-fidelity DNA polymerase. The amplified products were purified, and fluorescence was assessed using a Quant-iT PicoGreen dsDNA Assay Kit (Thermo Fisher Technology) and an FLx 800 microplate reader (Omega BioTek, Norcross, GA, USA). The samples were mixed based on the fluorescence results, and a sequencing library for high-throughput sequencing was prepared using an Illumina TruSeq Nano DNA LT Library Prep Kit (Illumina Inc., San Diego, CA, USA). The target segment was purified by electrophoresis using a 2% agarose gel.

2.3. Data and Statistical Analysis

Sequential denoising and amplicon sequence clustering based on amplicon sequence variants (ASVs) were performed according to the QIIME 2 data analysis process. The Chao1 index and the Shannon and Simpson indices were used to evaluate the diversity of soil microbial communities. Statistical analyses were performed using SPSS Statistics for Windows (version 26.0; IBM Corp., Armonk, NY, USA). One-way analysis of variance (one-way ANOVA) was used to compare the density of the earthworm community, nutrients, and diversity of the microbial community (significance level: p < 0.05). Alpha diversity—the diversity within a particular region or ecosystem—is a comprehensive indicator of richness and uniformity. To comprehensively evaluate the alpha diversity of farmland soil microbial communities, we evaluated the Chao1 index as a representative measure of richness and the Shannon and Simpson indices as representative measures of diversity. Microbiological data processing was conducted using the Parsenor Gene Cloud data analysis platform (http://www.genescloud.cn, accessed on 14 July 2023), and alpha diversity (Chao1 and Shannon) was calculated. The independent sample Levene’s t-test was conducted to determine the effects of different land-use types on earthworm population density and vermicompost weight. The impacts of environmental factors and earthworm density on bacterial communities were analyzed using redundancy analysis (RDA, Canoco 5). Origin software (version 2022b) was used to create the figures.

3. Results

3.1. Earthworm Community Composition and Vermicompost Characteristics

Among the six land-use patterns on the Guanzhong Plain, the most frequently detected earthworm species were Esienia foetida, Amynthas carnosus planus (new subspecies, unpublished), Amynthas carnosus carnosus, Metaphire vulgaris, and Metaphire baojiensis (new subspecies, unpublished). Across the Guanzhong Plain as a whole, the predominant earthworm species were Amynthas carnosus planus (new subspecies, unpublished) and Metaphire baojiensis (new subspecies, unpublished). The composition of the earthworm communities varied greatly with land use and seasons. The earthworm density ranged from 2 to 27 ind·m−2 in summer and from 15 to 40 ind·m−2 in spring (Table 2). The surface coverage of vermicompost ranged from 296.7 to 766.0 g·m−2 in summer and from 189.2 to 286.0 g·m−2 in spring. This signifies a significant positive correlation between the weight of the vermicompost and earthworm density in the same season under different land-use types. There are more earthworm populations in artificial forests, such as AS, WS, and CS, in spring.

3.2. C, N, and C/N of Vermicompost and Soil in Different Land-Use Types

Among the different land-use types, the soil organic content (C) ranged from 5.12 to 29.31 g·kg−1 in summer and 5.71 to 26.54 in spring (Figure 1a1,a2), whereas the C content of vermicompost varied from 20.93 to 47.48 mg·kg−1 in summer and 23.96 to 53.18, with the C content of soil being 2.0 to 4.3 times higher. The average soil organic content of all the land-use types was in the following order: RV > KS > WS > AS > BS > RS. The average vermicompost organic content decreased in the following order: RV > BV > CV > KV > AF > WV. There was a lower consistency in soil organic content between soil and vermicompost in different land-use types. For example, soil organic content was the lowest in soil (RS) but the highest in vermicompost (RV).
Figure 1b1 shows that the total N content in the soil and vermicompost of different land-use types ranged from 0.014 to1.31 g·kg−1 and from 0.54 to 1.35 mg·kg−1 in summer, respectively, with the latter values being 1.6 to 7.7 times higher than the former. Figure 1b2 shows that the total nitrogen content in soil ranged from 0.26 g·kg−1 to 1.64 g·kg−1 under different land-use types. The total nitrogen content of vermicompost ranged from 1.44 g·kg−1 to 2.3 g·kg−1 in different land-use types, with the values being 1.6 to 3.7 times higher than the former. The soil total N content of all the land-use types was in the following order: AS > CS > KS > RS > BS > WS. The average soil total N content of vermicompost was in the following order: BV > AV > CV > KV > RV > WV. There is good consistency in total N content between soil and vermicompost.
The density of earthworms was found to be positively correlated with the contents of soil organic carbon and total N in different land-use types. In summer, the average C/N was 15.8 to 19.8 in soil, and the average C/N in vermicompost was 15.0 to 23.5. In spring, the average C/N was 7.3 to 10.3 in soil, and the average C/N was 9.5 to 12.7 in vermicompost (Figure 1c1,c2). In different land-use types, the highest C/N of vermicompost was 23.5 in ryegrass land. The C/N of apple orchard soil was the lowest (12.6).

3.3. Comparison of the Microbial Community Diversity between Soil and Vermicompost

Table 3 shows the differences in the bacterial diversity of vermicompost and soil under different land-use types. For the same land-use type, the diversity of bacteria and fungi in vermicompost was lower than that in soil, with KV < KS and RV < RS. It is beneficial for soil bacteria to be abundantly diverse as it increases earthworm populations (Table 2 and Table 3).
At the phylum level, bacterial communities in soils from the six land-use types were dominated by Proteobacteria, Actinobacteria, Acidobacteria, Chloroflexi, Bacteroidetes, Gemmatimonadetes, Planctomycetes, Nitrospirae, Firmicutes, Rokubacteria, Verrucomicrobia, and Cyanobacteria, with most core taxa belonging to the phyla Proteobacteria (36.7%–56.8%), Actinobacteria (11.9%–32.6%), Acidobacteria (2.1%–13.7%), Chloroflexi (2.0%–6.7%), and Bacteroidetes (3.7%–22.6%) (Figure 2a).
Compared with soil, we observed differences in the proportional composition of dominant bacteria in vermicompost, with communities primarily comprising Proteobacteria (30.2%–52.3%), Actinobacteria (8.5%–43.0%), Bacteroidetes (3.7%–24.7%), Acidobacteria (1.9%–14.5%), and Chloroflexi (1.2%–4.6%) (Figure 2b). Comparatively, Proteobacteria and Chloroflexi were identified as being significantly more abundant in soil than in vermicompost. Verrucomicrobia (2.0%), Cyanobacteria (1.0%), and Patescibacteria (1.0%) were detected exclusively in vermicompost, whereas, in contrast, Planctomycetes, Rokubacteria, and Nitrospirae were absent (Figure 2).

3.4. The Environmental Factors of Bacterial Communities in Vermicompost

The associations among earthworm density, environmental factors, and the bacterial community in vermicompost under different land-use types were examined with redundancy analysis (RDA) (Figure 3). The results indicated that the interpretation rates of environmental factors at the phylum level were 55.85% and 48.7% on the x-axis (Figure 3a,b), respectively.
With respect to vermicompost, the earthworm density (ED), soil water content (SWC), soil organic carbon (SOC), total nitrogen (total N), and total porosity (PS) were identified as the main environmental factors influencing the abundance of Bacteroidetes, Proteobacteria, Verrucomicrobia, and Firmicutes. There were positive correlations between Actinobacteria and SOC, pH, and silt content, and positive correlations between Acidobacteria, Cyanobacteria, Chloroflexi, and Gemmatimonadetes and total N, pH, and sand. However, we also detected positive correlations between the environmental factors (bulk density (BD), pH, clay, and total N) and Acidobacteria and Gemmatimonadetes. Moreover, with the exception of sand, there were negative correlations between environmental factors and Actinobacteria in soil. In addition to environmental factors, earthworm community structure was identified as a key factor influencing the main bacterial communities in vermicompost.

4. Discussion

4.1. Effects of Different Land-Use Types on Earthworm Communities

Earthworms can be classified into three ecological categories, namely epigeic, endogeic, and anecic earthworms [27,28], which differ with respect to living habits and ecological service functions [29]. On the Guanzhong Plain, most of the earthworm communities were anecic and epi-endogeic earthworms, such as the species of Metaphire and Amynthas, whereas the epigeic earthworm Esienia foetida was found only in the land planted with ryegrass and in kiwi orchards. Usually, earthworms live in humid and warm ecosystems [2,30]. The optimal temperature of earthworms ranges from 10 °C to 40 °C [31]. In this study, the population density of earthworms in spring was more higher the one in summer because of the optimal average temperature in spring being at 21 °C, which is lower than the temperatures in summer at 33 °C. The total abundance of the local earthworm community is less than the one found in Philip’s study, which was between 5 and 150 individuals per m2 [2]. Notably, in summer, we recorded reductions in the numbers of earthworms in soil, whereas there was a corresponding increase in earthworm abundance in surface soil vermicompost. Conversely, in spring, the opposite trends were observed (Table 1). Perhaps this was because more vermicompost accumulates on the soil surface in the summer after the earthworms’ active phase in the spring. In spring, there was less vermicompost accumulation on the surface because earthworms’ excretion activities being limited due to the lower temperature of the previous winter. The number of vermicompost can directly impact soil structure and nutrient distribution [22,31].
Land use influences the species and populations of earthworms and their behaviors in soil [32,33]. There was a significant difference in earthworm community composition among the six assessed land-use types (p < 0.05) (Table 2). Amynthas were the most abundance and had the widest distribution of species in this area. Epi-endogecic (Amynthas) and epigeic (Esienia foetida) species who heavily feed on organic matter can accelerate the decomposition and mineralization of organic matter and improve the comprehensive fertility of soil, such as in RS and KS. Anecic (Metaphire baojiensis (d) and Metaphire vulgaris) species live in the following land-use types: BS, KS, WS, and CS. Compared with epigeic earthworms, they have larger biomasses and high levels of feeding, burrowing, and excretory activities; moreover, they are more effective regarding soil macroaggregates [33], such as with the vermicomposting of TS (766 g/m2) and MS (732.7 276 g/m2) in summer and with the vermicomposting of WS (240.8 g/m2) and MS (235.4 g/m2) in spring (Table 1).

4.2. Functional Role of Earthworm Communities on Bacterial Communities and C, N, and C/N

Earthworms decompose vegetative litter through a series of digestion and excretory processes, leading to the cycling of nutrients and an enrichment in vermicompost [22,25,34,35]. There was a good consistency between earthworm numbers and the C and N contents of soil and vermicompost (Figure 1, Table 2), which is consistent with the findings of Eriksen-Hamel et al. [36]. Vermicompost is the “gathered hot point” of soil fertilities in natural ecosystems. However, it is not a good match between earthworm populations and organic C and total N contents in different land-use types. Our result is the same as in Philip’s studies [2]. Earthworms are a rich source of organic C and total N in vermicompost on the surface (Figure 1). In this study, the organic C content of vermicompost is 2.0 to 4.3 times higher than that in the surrounding soil, which is somewhat higher than the contents (40%–48%) reported by Van Groenigen et al. [35]. Comparing the surrounding soil, total N content in vermicompost was 1.6 to 7.7 times greater than in the different land-use types, and the average C/N of vermicompost (9.5~23.5) was higher than them in soil (7.3~19.8).
Compared with other land-use types, we recorded the higher abundances of C and N in the soil of corn fields and kiwi orchards, which we suspect could be attributed to the higher abundances of anecic earthworms and more vermicompost in this soil (Table 2). However, the organic carbon content is relatively poor in grassland, and earthworms can only obtain all the energy they need by frequently feeding on a mixture of soil particles, which eventually leads to the accumulation of carbon content in vermicompost in ryegrass land, in which it was the highest among all land-use types (Figure 1a). However, their action could not remarkable accumulate N in ryegrass land (Figure 1b,c). In apple orchard (AS), the total N of vermicompost was richer than in the soil and vermicompost of other land-use types solely due to epi-endogecic (Amynthas) activities. Moreover, organic C contents are not high in the vermicompost of AS. Therefore, the diversity of earthworm populations and soil nutrients are affecting each other mutually, and their relationship could be a great future research area to explore.
Furthermore, a high vermicompost fertility was associated with an enrichment of a core microbial community in different land-use types [37]. For the same land-use type, the diversity of bacteria in the soil was notably richer than that in vermicompost. The diversity of the soil microbial community plays a vital role in soil nutrient cycling and organic C and N mineralization [38]. It was good for vermicompost to have a lower bacteria diversity as this enhances the physical protection of soil organic matter and reduces the decomposition and mineralization of organic C and N [39,40], thereby contributing to an enrichment of soil nutrients. Lavelle et al. [23] have suggested that aged vermicompost has better stability than new vermicompost, which contributes to the protection of soil organic C for several years. We speculated that the field-collected vermicompost assessed in the present study may have been of different ages; consequently, this is a reason for the significant differences in the microbial communities within the same land-use types (Figure 2b). In soil and vermicompost, the average C/N was higher in summer than it was in spring. C and N mineralization was stronger in spring than in summer. Compared to soil, the average C/N was higher in vermicompost in different land-use types that had their C and N contents protected by vermicompost. However, this protective function of vermicompost varies between seasons.
There are good correlations between earthworm populations and bacterial diversity in the soils of different land-use types (Chao1, R2 = 0.73); however, no similar correlation was observed in the case of vermicompost. Affinity to C/N is important for the earthworm populations, bacterial diversity, and bacterial composition in various soil and vermicompost types (Table 4). The main factors that affect C and N contents are earthworm populations, soil water content (SWC), and bacterial communities. There was no correlation between earthworm populations and soil water content (SWC). So, the main factor affecting earthworm populations is temperature, which is different based on what season it is.
Moreover, earthworm intestinal digestion and excretion contribute to the alteration of microbial community structures [16,41]. In the present study, we identified numerous unique bacteria—including those in the phyla Verrucomicrobia, Cyanobacteria, and Patescibacteria—in vermicompost. Among these, Patescibacteria have been established to play an important role in the oxidation and degradation of soil material and in the decomposition of harmful substances, such as pesticides and fertilizers, thereby contributing to improvements in soil health [42]. Cyanobacteria can fix the N and C balance in soil and enhance the supply of soil P [43,44]. Verrucomicrobia, which are present in the gut mucosa of healthy individuals, can be excreted into soil, wherein they can enhance biodiversity, the environment, and soil fertility [45]. Proteobacteria and Chloroflexi are the main heterotrophic bacterial resolvers of soil organic C [46], which contribute to enhancing C/N, as observed in the present study (Table 4). These are the bacteria that play prominent roles in nutrient cycles, controlling pollution and improving soil health. Therefore, in future studies, it would be valuable to evaluate soil C and N pool accumulation and mineralization in natural ecosystems as earthworm communities keep changing.

5. Conclusions

In this study, we established that different patterns of land use can influence the structure of earthworm communities and the distribution of soil nutrients, which are dependent on earthworm behavior (vermicompost). Earthworm community structure was in turn found to influence the composition of soil nutrients, with positive correlations being observed between earthworm density and the contents of C, N, and soil water. In addition, the distribution and accumulation of C and N were found to be influenced by earthworm community activities. Soil organic C and total N were enriched in vermicompost through earthworm community activity, and, in turn, vermicompost contributed to altering the bacterial community diversity. The carbon content of vermicompost is 2.0 to 4.3 times higher than that of soil. Compared to the total nitrogen content of soil, total nitrogen content increases 1.6 to 3.7 times more in vermicompost. Furthermore, we established that the diversity of bacteria in vermicompost was lower than that in soil, which can have the effect of retarding the conversion rates of C and N, thereby resulting in long-term nutrient accumulation in the soil. In addition, vermicompost was found to be populated by a number of beneficial bacterial species, including those of the phylum Cyanobacteria, Verrucomicrobia, and Patescibacteria, which play important roles in nutrient fixation, thus contributing to the accumulation of these nutrients in the soil. Collectively, our findings confirm that in addition to the influence of environmental factors, earthworm community structure plays key roles in determining bacterial community composition and activity in vermicompost. The affinity of earthworm communities to soil C and N pool accumulation and mineralization is important in different natural ecosystems.

Author Contributions

Contributions: L.M. (manuscript writing and data analysis), T.L. (writing assistance, sequencing strategy), M.S. (analytical strategy), Y.W. (proofreading, providing linguistic assistance), X.J. (laboratory experiments), K.J. (field experiments), and Y.Z. (field experiments). 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 (42007006), the China Postdoctoral Science Foundation funded project (2022M722612), and the Opening Foundation of the State Key Laboratory of Loess and Quaternary Geology, Institute of Earth Environment, CAS (SKLLQG2032).

Data Availability Statement

Data are contained within the article.

Acknowledgments

We would like to thank Shanghai Pineno Biotechnology Co., Ltd. for their technical help. We thank the editors and reviewers for their constructive comments and help with refining this manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

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Forests 15 01389 g001aForests 15 01389 g001b
Figure 1. (a) The soil organic (a1,a2), (b) total nitrogen (b1,b2) content, and (c) C/N (c1,c2) in vermicompost and soil under different land-use types. (The soil in different land-use types: buttonwood forest (BS), apple orchard (AS), walnut forest (WS), ryegrass land (RS), kiwi orchard (KS), and corn field (CS); the vermicompost in different land-use types: buttonwood forest (BV), apple orchard (AV), walnut forest (WV), ryegrass land (RV), kiwi orchard (KV), and corn field (CV)). (Different lowercase letters indicate significant differences in treatment at the 0.05 level). Blue: soil organic of vermicompost; green: total nitrogen of vermicompost; orange: C/N of vermicompost.
Figure 1. (a) The soil organic (a1,a2), (b) total nitrogen (b1,b2) content, and (c) C/N (c1,c2) in vermicompost and soil under different land-use types. (The soil in different land-use types: buttonwood forest (BS), apple orchard (AS), walnut forest (WS), ryegrass land (RS), kiwi orchard (KS), and corn field (CS); the vermicompost in different land-use types: buttonwood forest (BV), apple orchard (AV), walnut forest (WV), ryegrass land (RV), kiwi orchard (KV), and corn field (CV)). (Different lowercase letters indicate significant differences in treatment at the 0.05 level). Blue: soil organic of vermicompost; green: total nitrogen of vermicompost; orange: C/N of vermicompost.
Forests 15 01389 g001aForests 15 01389 g001b
Forests 15 01389 g002
Figure 2. The characteristics of bacterial classification in soil (a) and vermicompost (b) under different land-use types. (Soil: buttonwood forest (BS1, BS2, BS3), walnut forest (WS1, WS2, WS3), apple orchard (AS1, AS2, AS3), kiwi orchard (KS1, KS2, KS3), ryegrass land (RS1, RS2, RS3), and corn field (CS1, CS2, CS3). Vermicompost: buttonwood forest (BV1, BV2, BV3), walnut forest (WV1, WV2, WV3), apple orchard (AV1, AV2, AV3), kiwi orchard (KV1, KV2, KV3), ryegrass land (RV1, RV2, RV3), and corn field (CV1, CV2, CV3)).
Figure 2. The characteristics of bacterial classification in soil (a) and vermicompost (b) under different land-use types. (Soil: buttonwood forest (BS1, BS2, BS3), walnut forest (WS1, WS2, WS3), apple orchard (AS1, AS2, AS3), kiwi orchard (KS1, KS2, KS3), ryegrass land (RS1, RS2, RS3), and corn field (CS1, CS2, CS3). Vermicompost: buttonwood forest (BV1, BV2, BV3), walnut forest (WV1, WV2, WV3), apple orchard (AV1, AV2, AV3), kiwi orchard (KV1, KV2, KV3), ryegrass land (RV1, RV2, RV3), and corn field (CV1, CV2, CV3)).
Forests 15 01389 g002
Forests 15 01389 g003
Figure 3. RDA (redundancy analysis) map of relationship between earthworm population density, environmental factors, and bacterial community in earthworm compost. ((a): in soil; (b): in vermicompost). (Soil: buttonwood forest (BS), walnut forest (WS), apple orchard (AS), kiwi orchard (KS), ryegrass land (RS), and corn field (CS). Vermicompost: buttonwood forest (BV), walnut forest (WV), apple orchard (AV), kiwi orchard (KV), ryegrass land (RV), and corn field (CV)). The red line were bacterial communities. The blue lines were the environmental factors.
Figure 3. RDA (redundancy analysis) map of relationship between earthworm population density, environmental factors, and bacterial community in earthworm compost. ((a): in soil; (b): in vermicompost). (Soil: buttonwood forest (BS), walnut forest (WS), apple orchard (AS), kiwi orchard (KS), ryegrass land (RS), and corn field (CS). Vermicompost: buttonwood forest (BV), walnut forest (WV), apple orchard (AV), kiwi orchard (KV), ryegrass land (RV), and corn field (CV)). The red line were bacterial communities. The blue lines were the environmental factors.
Forests 15 01389 g003
Table 1. Soil physical and chemical properties at the experimental site.
Table 1. Soil physical and chemical properties at the experimental site.
Land-Use Soil TypeLocationSoil Water Content/%Particle-Size Distribution/%pHBulk Density/g·cm−3
SandSiltClay
Buttonwood forest (BS)33.45 N,
107.63 E		13.3 ± 0.0128.95 ± 1.8964.11 ± 1.146.94 ± 3.038.15 ± 0.011.39 ± 0.04
Walnut forest (WS)34.48 N,
107.44 E		18.7 ± 0.0132.21 ± 1.1363.19 ± 1.134.60 ± 2.028.14 ± 0.041.42 ± 0.06
Apple orchard (AS)34.43 N,
107.88 E		15.0 ± 0.0133.27 ± 0.4962.16 ± 0.494.57 ± 1.768.07 ± 0.191.30 ± 0.04
Kiwi orchard (KS)34.26 N,
107.72 E		21.3 ± 0.0128.92 ± 1.9365.12 ± 1.925.96 ± 2.768.00 ± 0.021.40 ± 0.08
Ryegrass land (RS)34.35 N,
107.20 E		11.0 ± 0.0229.03 ± 2.5359.04 ± 2.5311.93 ± 4.568.19 ± 0.031.45 ± 0.05
Corn field (CS)34.28 N,
107.64 E		21.0 ± 0.0129.30 ± 1.9057.81 ± 1.9013.88 ± 1.587.81 ± 0.041.36 ± 0.08
Table 2. Earthworm communities and vermicompost weights in different land-use types.
Table 2. Earthworm communities and vermicompost weights in different land-use types.
Earthworm SpeciesEarthworm Populations/
ind·m−2		Vermicompost Weight/
g·m−2
Summer 2022 Spring 2023 Summer
2022 		Spring
2023
Buttonwood forest (BS)Amynthas carnosus planus,
Metaphire baojiensis		4 ± 0.6 c20 ± 3.6 b308.3 ± 25.1 b240.8 ± 25.4 a
Walnut forest (WS)Amynthas carnosus carnosus, Metaphire baojiensis26 ± 2.3 a15 ± 5.3 b 766.0 ± 35.4 a198.8 ± 8.5 b
Apple orchard (AS)Amynthas carnosus planus2 ± 0 c40 ± 0.7 a296.7 ± 4.2 b286.0 ± 25.5 a
Kiwi orchard (KS)Esienia foetida, Amynthas carnosus planus, Metaphire vulgaris13 ± 3.2 b32 ± 4.7 a732.7 ± 40.9 a235.4 ± 23.1 a
Ryegrass land (RS)Esienia foetida, Amynthas carnosus carnosus18 ± 1.7 a19 ± 6.7 b434.0 ± 14.9 b189.2 ± 7.6 b
Corn field (CS)Amynthas carnosus planus,
Amynthas carnosus carnosu,
Metaphire baojiensis		17 ± 3.1 a38 ± 9.5 a482.0 ± 2.8 b232.2 ± 5.9 b
Different lowercase letters indicate a significant difference in land use at the 0.05 level; values are represented as mean + standard error.
Table 3. Statistical analysis of soil bacterial diversity index under different land-use patterns.
Table 3. Statistical analysis of soil bacterial diversity index under different land-use patterns.
Land-Use Type
Soil Species		Bacteria
Chao1ShannonSimpson
BS3819.87 ± 1929.24 ± 0.350.9557 ± 0.0162
AS3774.57 ± 2099.70 ± 0.680.9737 ± 0.0240
WS4227.74 ± 3429.44 ± 0.620.9570 ± 0.0239
RS3747.06 ± 37510.44 ± 0.070.9954 ± 0.0019
KS3880.09 ± 3249.72 ± 0.320.9843 ± 0.0089
CS4053.62 ± 52010.35 ± 0.120.9927 ± 0.0047
BV2660.24 ± 2809.83 ± 0.420.9966 ± 0.0015
AV3648.09 ± 27710.58 ± 0.130.9979 ± 0.0002
WV3350.85 ± 58210.54 ± 0.330.9985 ± 0.004
RV2796.03 ± 56610.01 ± 0.580.9974 ± 0.0017
KV3695.76 ± 69310.14 ± 0.470.9973 ± 0.0007
CV2831.19 ± 30510.00 ± 0.580.9957 ± 0.0037
Soil: buttonwood forest (BS), walnut forest (WS), apple orchard (AS), kiwi orchard (KS), ryegrass land (RS), and corn field (CS); Vermicompost: buttonwood forest (BV), walnut forest (WV), apple orchard (AV), kiwi orchard (KV), ryegrass land (RV), and corn field (CV). Values are represented as mean + standard error.
Table 4. Pearson’s correlation analysis of C, N, C/N, earthworm populations, and bacterial communities in soil and vermicompost under different land-use types.
Table 4. Pearson’s correlation analysis of C, N, C/N, earthworm populations, and bacterial communities in soil and vermicompost under different land-use types.
C/
g·kg−1		N/
g·kg−1		C/N
/%		EDSWC
/%		Chao1ProteobacteriaActinobacteriaAcidobacteriaChloroflexiBacteroidetesGemmatimonadetes
SoilC/
g·kg−1		1
N/
g·kg−1		0.62 *1
C/N/%0.15−0.81 *1
ED0.60 *−0.330.451
SWC/%0.82 *0.260.260.331
chao1−0.34−0.20.67 *0.73 *0.63 *1
Proteobacteria0.48−0.180.57 *0.050.79 *0.441
Actinobacteria−0.190.19−0.57 *0.03−0.61 *−0.48−0.85 *1
Acidobacteria−0.77 *−0.400.200.03−0.70 *0.04−0.56 *0.151
Chloroflexi−0.070.48−0.69 *−0.53 *−0.61 *−0.57 *−0.75 *0.71 *0.281
Bacteroidetes0.64 *0.24−0.050.120.75 *0.070.66 *−0.32−0.95 **−0.53 *1
Gemmatimonadetes−0.26−0.170.30−0.53 *−0.170.040.19−0.55 *0.51 *0.075−0.50 *1
VermicompostC/g·kg−11
N/g·kg−10.181
C/N/%0.61 *−0.65 *1
ED0.01−0.62 *0.55 *1
SWC/%0.61 *0.04−0.52-1
chao1−0.71 *0.22−0.64 *−0.070.461
Proteobacteria−0.44−0.24−0.230.350.88 *0.161
Actinobacteria0.38−0.120.42−0.31−0.94 **−0.41−0.89 *1
Acidobacteria0.090.05−0.070.100.53 *−0.0010.76 *−0.76 *1
Chloroflexi0.440.310.20.37−0.11−0.2−0.380.13−0.371
Bacteroidetes0.30.30.130.074−0.460.043−0.79 *0.52−0.750.80 *1
Gemmatimonadetes−0.380.42−0.56 *−0.060.320.22−0.087−0.059−0.50.510.451
* Significant difference at p < 0.05. ** Significant difference at p < 0.01. (ED: earthworm density; SWC: soil water content; C: soil organic carbon; N: total nitrogen; Chao1: bacterial diversity).
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Ma, L.; Shao, M.; Wang, Y.; Li, T.; Jing, X.; Jia, K.; Zhang, Y. The Characteristics and Influential Factors of Earthworm and Vermicompost under Different Land Use in a Temperate Area, China. Forests 2024, 15, 1389. https://doi.org/10.3390/f15081389

AMA Style

Ma L, Shao M, Wang Y, Li T, Jing X, Jia K, Zhang Y. The Characteristics and Influential Factors of Earthworm and Vermicompost under Different Land Use in a Temperate Area, China. Forests. 2024; 15(8):1389. https://doi.org/10.3390/f15081389

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Ma, Li, Ming’an Shao, Yunqiang Wang, Tongchuan Li, Xuanxuan Jing, Kunyu Jia, and Yangyang Zhang. 2024. "The Characteristics and Influential Factors of Earthworm and Vermicompost under Different Land Use in a Temperate Area, China" Forests 15, no. 8: 1389. https://doi.org/10.3390/f15081389

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