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Article

Expansion of Field Margin Size Mitigate the Hazard of Rotary Tillage to Earthworm in Rice-Rape Rotation System

by
Chao Li
1,2,
Yang Zhao
3,
Kaikai Cheng
2,
Junyu Zhou
2,
Xiaoping Xiao
2,
Anas Iqbal
4,
Haiming Tang
2 and
Min Huang
1,*
1
Rice and Product Ecophysiology, Key Laboratory of Ministry of Eduction for Crop Physiology and Molecular Biology, Hunan Agricultural University, Changsha 410128, China
2
Soil and Fertilizer Institute, Hunan Academy of Agricultural Sciences, Changsha 410125, China
3
Rice Research Institute, Hunan Academy of Agricultural Sciences, Changsha 410125, China
4
State Key Laboratory for Conservation and Utilization of Agro-Bioresoueces, College of Agriculture, South China Agriculture University, Guangzhou 510642, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(9), 2209; https://doi.org/10.3390/agronomy12092209
Submission received: 18 August 2022 / Revised: 12 September 2022 / Accepted: 14 September 2022 / Published: 16 September 2022
(This article belongs to the Special Issue In Memory of Professor Longping Yuan, the Father of Hybrid Rice)
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Abstract

:
Field margin (FM) provides refuges for earthworm survival in rape-rice system after flooding, while the effects of FM with different size on earthworm in arable field (AF) is unclear. In this study, we investigated the effects of different FM sizes, a conventional size (FM I) and three expanding sizes (FM II, FM III, FM IV), on earthworm population characteristics in FM and AF. The results showed that the mean abundance of earthworm under the expanding sizes at 1 day and 60 day of flooding after rape harvest was 16.5 and 20.2 times higher than that of FM I, respectively. After stopping flooding, juveniles first migrated from FM to AF, whereas more than half of them were killed by subsequent rotary tillage, and the mortality decreased with expanding FM size. Subsequently, expanding FM sizes promoted earthworm to distribute evenly through the AF at faster speeds. At rape maturity, the mean abundance and total biomass of earthworm of AF under expanding FM sizes were significantly greater than that of FM I, and this positive effect increased with expanding FM size. The results indicated that expanding FM size can mitigate the hazard of rotary tillage to earthworm and promote rapid recovery of earthworm population in AF.

1. Introduction

Earthworms are essential to soil biota, accounting for 80% of soil biomass [1]. They are considered as indicators of soil health and fertility [2,3]. Their bioturbation improve soil physical, chemical, and biological properties associated with crop yield, and provides important ecosystem service for promoting agricultural sustainability [4]. However, the abundance and activity of earthworms are susceptible to agricultural management such as soil tillage and irrigation [5,6].
Soil tillage and irrigation management are the essential measures to achieve high yield in the cropping systems [7,8]. The rice-rape rotation is a major cropping system in the Yangtze River basin of China, many earthworms have been found in this system [9], and their casts can significantly increase rice yield [10]. However, flooding forces earthworms to escape their burrows [11,12], and the abundance of earthworms was significantly decreased by soil tillage [5], such as rotary tillage [13], which has been widely applied in the rice-rape rotation system. Therefore, mitigating the hazard of rotary tillage to earthworms and subsequently maintaining a higher earthworm population in arable field is important basis for increasing crop yield.
In general, field margins (FM) suffer less disturbance than the arable field (AF), and it can promote earthworm growth and reproduction [14,15], which is a key source for earthworm population recovery in AF after applying soil tillage [16]. To date, little attention has been paid to the relationship between FM and the recolonization of earthworm in AF. Theoretically, larger FM has a greater capacity for earthworm refuge and reproduction, which can provide more sources for earthworm population recovery in AF. Therefore, this study proposed the following hypotheses: (1) Expanding FM size is more favorable for earthworm refuge during the rice-growing stages when flooded; (2) Expanding FM size can reduce the mortality caused by rotary tillage, and favor the recovery of earthworms population in AF, thus mitigating the hazard of rotary tillage to earthworms. Hence, an on-farm experiment was conducted to study the effects of expanding FM size on earthworm survival after AF flooded and population recovery in AF after applying rotary tillage.

2. Materials and Methods

2.1. Study Area

This study was carried out in Nanxian city, Hunan Province (112°24′ E, 29°09′ N). The region has a moist subtropical monsoon climate with an annual average temperature of 16.6 °C, rainfall of 1238 mm, and sunshine duration of 1776 h. The soil texture is purple calcareous clay (Fluvisol, FAO taxonomy). The characteristics of soil (0–20 cm) were as following: sand 4.4%, silt 44.1%, clay 51.5%, pH 7.8, organic matter 44.1 g/kg, available N 234.7 mg/kg, available P 12.1 mg/kg, available K 82.6 mg/kg. The mechanical composition was determined by modified Kachinsky’s method, pH by digital pH meter, organic matter by potassium dichromate method, available N by Kjeldahl method, available P by Olsen method, available K by atomic absorption spectro-photometry. Rice-rape rotation with rotary tillage was the major cropping system in this region, the rotary tillage was performed by loosening the surface soil to a depth of 10–15 cm with a rotary cultivator (1GKN-200, Lianyungang Huayun Machinery Manufacturing Co., Ltd., Lianyungang, China). The dominant earthworm species was divided into anecic Pheretima. guillelmi (P.guillelmi) according to their habitats of digging deep burrows and seeking food on the soil surface [17,18].

2.2. Earthworms Migration between FM and AF

A large number of earthworms were forced to migrate from AF to FM to take refuge in response to flooding (Figure 1A) before planting rice (Figure 1A), then the FM planted with soybean provided earthworm with favorable survival conditions (Figure 1B,C), after stopping flooding in the late growing stage of rice, earthworms began to migrate from FM to AF when (Figure 1D) and then kept living in the rape-growing stage. The schematic diagram of earthworm migration between FM and AF during the growth stage of rice and rape was showed in Figure 2.

2.3. Experimental Design

An on-farm experiment was conducted from 2016 to 2018, the conventional size (width/height) of FM I (30 ± 2 cm/15 ± 1 cm) was set as the control, and expanding size to FM II (45 ± 2 cm/20 ± 1 cm), FM III (60 ± 3 cm /25 ± 2 cm), FM IV (75 ± 3 cm/30 ± 2 cm) on the basis of conventional size after harvesting rape in 2016, each treatment selected three fields about 1500 m2, the plane figure and profile map of plot was indicated in Figure 3.
Rice-rape rotation cultivation was performed in AF. The AF was alternately flooded in the rice-growing stage while dried during the rape-growing stage. Field management was consistent with local routine measures. Rice was direct-seeded at a seed rate of 90 kg/ha at 2–3 days after applying rotary tillage. The fertilizer management was as follows: 90 kg/ha urea (46% N) used at the 3–4 leaf stage, 600 kg/ha compound fertilizer (17% N, 5% P2O5, and 26% K2O) applied at the 6–7 leaf stage and 120 kg/ha compound fertilizer applied at the panicle initiation stage. After rice harvesting, rice straw was left on the field, and then rotary tillage was performed at a depth of about 13 cm before planting the rape. The rape seed (3 kg/ha) was mixed with urea (45 kg/ha) and then evenly broadcast- seeded onto the soil surface. Urea was top-dressed at a rate of 150 kg/ha in the 3–4 leaf period and compound fertilizer (26% N, 10% P2O5, and 15% K2O) was top-dressed at a rate of 300 kg/ha at the 5–6 leaf period of rape. Straw was left on the field after rape harvesting.

2.4. Earthworm Sampling

After rape harvest in 2017 and 2018, we investigated the earthworm population at five soil sites (30 cm length × 30 cm width × 50 cm depth) in FM before flooding (T1), 1 day after field flooding (T2) and 60 days after field flooding (T3), respectively. The earthworms in AF was monthly sampled at three distances with 0–1 m, 2–3 m and 7–8 m from field edge at the five soil sites (30 cm length × 30 cm width × 30 cm depth) in FM, respectively, which started in September 2016 when the flood stopped. The distance between two adjacent sample sites was horizontally spaced 4 m, earthworm investigation was carried out using digging and hand-sorting, and then marked with a bamboo, separated from the next sampling point by more than 40 cm, the detailed survey time was indicated in Table 1.
Sampling earthworms were weighed fresh, identified as adults using [19] and then returned to the original sampling location. Based on the above data that the spatial uniformity of the earthworm population was defined as follows:
S p a t i a l   u n i f o r m i t y = 100 % − | ( P ¯ − P 0 ) × 100 P 0 |
P ¯ was the average value of earthworm abundance at 0–1 m, 2–3 m, 7–8 m from the field edge, and P0 was the earthworm abundance at 0–1 m from the field edge.
Rotary tillage was applied to plant rape after rice harvest in 2016 and 2017. The adult, dead, injured, and uninjured earthworms were hand-sorted in 36 (4 FM × 3 distances × 3 samples) soil points (30 cm length × 30 cm width × 30 cm depth), injured earthworms were placed in moistened soil for one week, observed for survival, and calculated for mortality.

2.5. Statistical Analysis

All statistical analyses were conducted with SPSS 21.0 software (SPSS Inc., Chicago, IL, USA). Data were tested for normality with Shapiro-Wilk, and one-way ANOVA was performed by the Student-Newman- Keuls (S-N-K). The data were expressed as means and SE in 95% confidence intervals, and analysis of variance and correlation analysis were used for statistical evaluation. The statistical model for the analysis of variance included replication (n = 3) and FM size classes (n = 4).

3. Results

3.1. Earthworms Refuge in Response to FM Size

After rape harvest, FM provided a refuge for earthworms when flooding was applied for planting rice. The average abundance of earthworms in FM at 1 day after field flooding (T2) and 60 day after field flooding (T3) was 26.5 and 14.9 times higher (p < 0.05) than before flooding (T1). The average abundance of earthworms of expanding FM size at T2, T3 were 16.5 and 20.2 times higher (p < 0.05) than that of FMⅠ, respectively. The earthworms abundance increased with the expansion of FM size, the average earthworms abundance of expanding FM in T2 and T3 ranged from 127 to 456 individual/m2 and 89 to 241 individual/m2 in 2017, and ranged from 84 to 267 individual/m2 and 61 to 150 individual/m2 in 2018, respectively (Figure 4). These results indicated that expanding FM size can provide more favorable conditions for earthworm refuge.

3.2. Earthworms Mortality in Response to FM Size Induced by Rotary Tillage

Rotary tillage was applied for planting rape in October 2016. More than half (53% on average across all treatments) of earthworms were killed by rotary tillage, and the earthworm mortality decreased with the expansion of FM size, ranging from 43% to 51% for FM II, FM III and FM IV in 2016, and from 52% to 56% in 2017 (Figure 5). These results indicated that expanding FM size can reduce earthworm mortality due to rotary tillage operation in the field.

3.3. Earthworm Population Recovery of AF in Response to FM Size

After stopping flooding in September 2016, juvenile earthworms first migrated from the FM towards the area of 0–1 m from the FM edge (Figure 6A,D), and the earthworm abundance of FM II, FM III, FM IV was 6.3, 13.3, 18.7 times greater than that of FM I. Subsequent rotary tillage caused a substantial decline of earthworms abundance of AF in October 2016, and then the earthworms abundance of AF recovered gradually and increased with the expansion of FM size at the rape-growing stage (Figure 6B,C), there was a gradual increase in the adult earthworms rate and no significant differences among treatments at the maturity stage of rape (Figure 6D–F). The spatial uniformity increased with the expansion of FM size and more quickly than that of FM I (Figure 7). These results indicated that the earthworms in AF harmed by rotary tillage was mainly juveniles, and expanding FM can promote the recovery of earthworm population in AF.
The abundance and total biomass of earthworms were significantly (p < 0.05) increased with the expansion of FM size. For the expanding size, the abundance of earthworms was 5.4–11.7 and 4.8–11.0 times greater than that of FM I in 2017 and 2018, respectively. The total biomass of expanding size was 4.3–8.4 and 4.1–8.0 times greater than that of FM I in 2017 and 2018, respectively. However, the individual earthworm biomass decreased with the expansion of FM size. The expanding size were 20–28% and 14–27% less than FM I in 2017 and 2018, respectively (Table 2). These results demonstrated that expanding FM size could significantly increase the earthworm population under rotary tillage conditions.

4. Discussion

4.1. Importance of FM and Effect of Its Sizes on Earthworms Refuge

Earthworm abundance in AF was reduced by flooding as the anaerobic conditions [20]. In present study, Pheretima Guillelmi was droved out of their burrows by flooding to escape the adverse survival environment in the rice-rape rotation system, and then FM served as the critical refugia for earthworms that migrated seasonally between FM and AF in response to flooding, previous study also found that earthworm abundance in FM was significantly greater than that of AF with frequently flooding [21]. The reason why FM provided refuge function to earthworms can be explained as follows: (1) the space of FM provided a non-flooded habitat for earthworms; (2) covering plants such as soybean and weeds may have lowered soil temperature, and provided suitable conditions for earthworms aestivation [22,23]; (3) the frequent irrigation applied during the rice growth period was beneficial for ensuring sufficient moisture of FM, which was beneficial for earthworm survival, as rising soil moisture generally mitigated the harmful effects of increased soil temperature on earthworms [24,25]. Usually, a larger FM enhanced the diversity and abundance of above-ground fauna [26,27]. In present study, earthworms in FM increased significantly with increasing FM size at 1 and 60 days after flooding, the reason may be that expanding FM size can provide sufficient refuge space above the flooded layer and more favorable living environments such as lower soil temperature or better food supply for earthworms [28,29].

4.2. Influence of FM Size on Mitigating the Harmful Effects of Rotary Tillage on Earthworms

Rotary tillage easily causes stronger mechanical damage to earthworms, caused 61–68% of earthworms biomass to be killed [13]. In present study, the mean earthworm mortality of all treatments was 53% after rotary tillage, the dead earthworms mainly composed of juveniles, as the juveniles first migrated from FM to the area of 0–1 m from the FM edge. The earthworms mortality decreased with the increase in FM size, and more earthworms migrated from FM forward AF after applying rotary tillage under the condition of expanding FM size, and then quickly distributed throughout the field, which was contrary to the previous studies that found earthworms abundance increased towards the middle of the AF [30].
The permanent and new arable FM supported large earthworm communities but did not increase AF abundance in upland crop system [31]. However, in rice-rape rotation system, the abundance of earthworms in AF under the condition of expanding FM size increased faster than that of conventional size after applying rotary tillage, the possible causes of these findings: (1) adult earthworms were not damaged by rotary tillage, expanding FM size provided more source for subsequent population recovery of earthworms in AF; (2) soil characteristics with a high clay content and a high soil organic matter content were more conducive to earthworm growth [5,30], which was confirmed in this study, e.g., clay 51.5% and soil organic matter 44.1 g/kg; (3) abundant and good quality food promotes recolonization of earthworms [32,33], and plant litterfall is more essential than root in sustaining earthworm communities [34]. In present study, plenty of rape litterfall throughout the growing season ensured the food supply for P. guillelmiin. Additionally, crop residue quality is an important factor affecting earthworm abundance, and high-quality crop residue generally have a low C:N ratio [29,35], the rape litterfall with low C:N ratio were easily eaten and digested by earthworms [36], which was beneficial to promote the recovery of earthworms population in AF. Consequently, the average abundance and total biomass of earthworms in AF under expanding FM size at the maturity stage of rape were significantly greater than that of under conventional FM size, which mitigated the harmful effects of rotary tillage on the earthworm population.
In this study, we only focused on the effects of expanding FM size on the recovery of earthworm abundance in AF after applying rotary tillage in rice-rape rotation system, and did not study its effect on crop growth and soil fertility after recovering earthworm population, which will be our next research direction.

5. Conclusions

In the rice-rape rotation system, FM served as a critical refuge for earthworms in response to flooding. Expanding FM size can reduce the earthworm mortality caused by rotary tillage, promote rapid recovery of earthworm populations in AF, and mitigate the hazard of rotary tillage to earthworms.

Author Contributions

Conceptualization, M.H. and H.T.; Data curation, C.L., Y.Z., K.C. and J.Z.; Formal analysis, C.L.; Funding acquisition, C.L.; Investigation, C.L. and K.C.; Methodology, C.L. and X.X.; Project administration, M.H.; Writing—original draft, C.L.; Writing—review & editing, A.I., H.T. and M.H. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Hunan Province Science and technology talents bootstrap project (2022TJ-N07), the Science and Technology Innovation Project of Hunan Academy of Agricultural Sciences in China (2022CX75, 2021CX37, 2017QN26) and the National Natural Science Foundation of China (41807008, 31872851).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data is contained within the article.

Acknowledgments

Thanks to San’an Nie for revising this paper.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 02209 g001 550
Figure 1. Earthworms migrated between field margins (FM) and arable field (AF). (A): Earthworms migrated forward FM after applying flooding. (B): Planting soybean in FM. (C): Earthworm casts and burrows in FM after applying flooding. (D): Earthworms migrated from FM to adjacent AF in September.
Figure 1. Earthworms migrated between field margins (FM) and arable field (AF). (A): Earthworms migrated forward FM after applying flooding. (B): Planting soybean in FM. (C): Earthworm casts and burrows in FM after applying flooding. (D): Earthworms migrated from FM to adjacent AF in September.
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Figure 2. The schematic diagram of earthworm migration between field margins (FM) and arable field (AF) during the growth stage of rice and rape. Dotted arrow represented the movement of earthworms between FM and AF.
Figure 2. The schematic diagram of earthworm migration between field margins (FM) and arable field (AF) during the growth stage of rice and rape. Dotted arrow represented the movement of earthworms between FM and AF.
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Figure 3. The plane figure and profile map of plot. (A): Rice growth period; (B): Rape growth period.
Figure 3. The plane figure and profile map of plot. (A): Rice growth period; (B): Rape growth period.
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Figure 4. Effect of field margins (FM) size on earthworm abundance in FM in response to flooding. T1, T2, T3 represented the sampling time of earthworms before flooding, 1 day after field flooding, 60 days after field flooding, respectively. Data were medians with 95% confidence intervals (n = 3). Treatments having no letters in common represented significantly differences (S-N-K, p < 0.05).
Figure 4. Effect of field margins (FM) size on earthworm abundance in FM in response to flooding. T1, T2, T3 represented the sampling time of earthworms before flooding, 1 day after field flooding, 60 days after field flooding, respectively. Data were medians with 95% confidence intervals (n = 3). Treatments having no letters in common represented significantly differences (S-N-K, p < 0.05).
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Figure 5. Effect of field margin (FM) size on earthworm mortality of arable field (AF) after applying rotary tillage. Data were medians and their 95% confidence intervals (n = 3). Treatments having no letters in common represented significantly differences (S-N-K, p < 0.05).
Figure 5. Effect of field margin (FM) size on earthworm mortality of arable field (AF) after applying rotary tillage. Data were medians and their 95% confidence intervals (n = 3). Treatments having no letters in common represented significantly differences (S-N-K, p < 0.05).
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Figure 6. Effects of field margins (FM) size classes on the dynamic of earthworm abundance and adult rate in the rice-rapeseed system under rotary tillage. Data were medians and their 95% confidence intervals (n = 3). Treatments having no letters in common represented significantly differences (S-N-K, p < 0.05). (A–C) represented the earthworm abundance in the area of 0–1 m, 2–3 m and 7–8 m from field edge respectively, and (D–F) represented the adult rate in the area of 0–1 m, 2–3 m and 7–8 m from field edge respectively.
Figure 6. Effects of field margins (FM) size classes on the dynamic of earthworm abundance and adult rate in the rice-rapeseed system under rotary tillage. Data were medians and their 95% confidence intervals (n = 3). Treatments having no letters in common represented significantly differences (S-N-K, p < 0.05). (A–C) represented the earthworm abundance in the area of 0–1 m, 2–3 m and 7–8 m from field edge respectively, and (D–F) represented the adult rate in the area of 0–1 m, 2–3 m and 7–8 m from field edge respectively.
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Figure 7. Effects of field margins (FM) size classes on the earthworm population spatial uniformity of arable field (AF) of the rice-rapeseed system under rotary tillage from September 2016 to May 2017. The logistic regression model Y = 1 − k/[1 + EXP(a − bx)] was applied to simulate the spatial uniformity in time series.
Figure 7. Effects of field margins (FM) size classes on the earthworm population spatial uniformity of arable field (AF) of the rice-rapeseed system under rotary tillage from September 2016 to May 2017. The logistic regression model Y = 1 − k/[1 + EXP(a − bx)] was applied to simulate the spatial uniformity in time series.
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Table
Table 1. Cropping managements and sampling dates.
Table 1. Cropping managements and sampling dates.
Item201620172018
Jun.–Aug.Sep.Oct.Nov.–Dem.Jan.–Apr.MayJun.–Aug.Sep.Oct.Nov.–Dem.Jan.–Apr.May
Cropping management RT1, H1, DS1 H2, RT2, DS2 RT3, H3, DS3 H4, RT4, DS4,
Sampling date 12, M13–45–89 M2 10
H = Harvest (H1, H2, H3, H4 = harvest rapeseed and rice on 4 October, 12 May, 25 October, 17 May), RT = Rotary tillage (RT1, RT2, RT3, RT4 = rotary tillage for planting rapeseed and rice on 8 October, 23 May, 27 October, 22 May), DS = direct seeding(DS1, DS2, DS3, DS4 = rapeseed and rice were established by direct seeding on 9 October, 25 May, 29 October, 24 May). Earthworms population dynamic sample composed of 1th–9th. 1st (22 September), 2nd (26 October), 3rd (23 November), 4th (20 December), 5th (22 January), 6th (20 February), 7th (19 March), 8th (21 April), 9th (18 May), 10th (19 May). M = mortality (M1, M2 = the earthworms mortality caused by rotary tillage was tested on 8 October and 27 October).
Table
Table 2. Effects of field margins (FM) size on earthworm biomass at the maturity stage of a rice-rapeseed cropping system.
Table 2. Effects of field margins (FM) size on earthworm biomass at the maturity stage of a rice-rapeseed cropping system.
YearsFM SizeEarthworm AbundanceTotal BiomassIndividual Biomass
(Earthworms/m2)(g/m2)(g/Individual)
2017FM I8.4 ± 1.1 d4.32 ± 0.28 d36.3 ± 3.9 d
FM II45.3 ± 3.6 c3.46 ± 0.09 c156.9 ± 8.6 c
FM III79.0 ± 5.9 b3.21 ± 0.06 b253.2 ± 13.8 b
FM IV98.5 ± 7.4 a3.11 ± 0.07 a306.3 ± 16.5 a
2018FM I4.7 ± 0.6 d4.64 ± 0.23 d21.8 ± 1.7 d
FM II22.4 ± 2.0 c3.99 ± 0.14 c89.3 ± 5.4 c
FM III38.3 ± 2.6 b3.60 ± 0.04 b137.9 ± 8.1 b
FM IV51.8 ± 3.5 a3.38 ± 0.06 a175.1 ± 9.8 a
Earthworms were sampled in the rapeseed maturity stage. Numbers in brackets are the standard deviation of the mean. Treatments having no letters in common represented significantly differences (S-N-K, p < 0.05).
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Li, C.; Zhao, Y.; Cheng, K.; Zhou, J.; Xiao, X.; Iqbal, A.; Tang, H.; Huang, M. Expansion of Field Margin Size Mitigate the Hazard of Rotary Tillage to Earthworm in Rice-Rape Rotation System. Agronomy 2022, 12, 2209. https://doi.org/10.3390/agronomy12092209

AMA Style

Li C, Zhao Y, Cheng K, Zhou J, Xiao X, Iqbal A, Tang H, Huang M. Expansion of Field Margin Size Mitigate the Hazard of Rotary Tillage to Earthworm in Rice-Rape Rotation System. Agronomy. 2022; 12(9):2209. https://doi.org/10.3390/agronomy12092209

Chicago/Turabian Style

Li, Chao, Yang Zhao, Kaikai Cheng, Junyu Zhou, Xiaoping Xiao, Anas Iqbal, Haiming Tang, and Min Huang. 2022. "Expansion of Field Margin Size Mitigate the Hazard of Rotary Tillage to Earthworm in Rice-Rape Rotation System" Agronomy 12, no. 9: 2209. https://doi.org/10.3390/agronomy12092209

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