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Article

Behavioral and Physiological Adaptation to Soil Moisture in the Overwintering Larvae of the Rice Stem Borer in the Subtropics

by
Changgeng Dai
1,2,
Yuqi Zhong
1,
Jing Yu
1,
Yiyu Cheng
1 and
Maolin Hou
1,*
1
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
2
Institute of Plant Protection, Guizhou Academy of Agricultural Sciences, Guiyang 550006, China
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(12), 2177; https://doi.org/10.3390/agriculture13122177
Submission received: 27 September 2023 / Revised: 23 October 2023 / Accepted: 17 November 2023 / Published: 21 November 2023
(This article belongs to the Special Issue Sustainable Crop Production and Pest Control)
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Abstract

:
Diapausing larvae of the rice stem borer, Chilo suppressalis Walker, overwinter in rice stubble. During overwintering, the larvae may move to sites with suitable moisture and undergo physiological changes to prepare for the declining temperature. This study measured the behavioral and physiological adaptation to soil moisture (25%, 50%, and 75% of saturated soil water content) in the diapausing larvae at 30, 60, and 90 days of treatment. The results showed that the diapausing C. suppressalis larvae behaviorally exhibited hygrotaxis and distributed mainly (65%) in the lower part (0–10 cm above the soil level) of the rice stem where the moisture was higher. Physiologically, the insects showed significantly decreased glycogen content and weight whereas increased trehalose content with decreasing soil moisture. In the subtropics where this study was conducted, the supercooling points of the insects were lower than the lowest ambient temperature, and the soil moisture had no significant effects on the cold hardiness (supercooling point) and survival of the diapausing C. suppressalis larvae. The decreased larval weight at low soil moisture may reduce the post-diapause reproductive potential of the larvae, which may open the potential of developing agronomic measures-based management of the overwintering C. suppressalis population.

1. Introduction

Insects have evolved the ability to withstand harsh environments by entering diapause, a state characterized by reduced metabolic activity and suspension of development and reproduction. This allows them to survive periodic extreme conditions and maintain continuity in their populations [1,2]. Diapause is not simply a halt in morphological development, but a process of dynamic physiological changes in the insect’s body [3]. Once diapause begins, it cannot be terminated immediately even if the adverse environment changes or is relieved; it requires a period of activation before development can continue [4]. This process includes a pre-diapause phase (induction and preparation), a diapause phase (initiation, maintenance, and termination), and a post-diapause developmental phase, each of which is regulated and influenced by one or more environmental factors [5].
The rice stem borer, Chilo suppressalis Walker (Lepidoptera: Crambidae), is the most widely distributed stem borer in Asia countries. It occurs throughout the rice growing areas in China from the tropical to the northern temperate (18°9′ N–53°29′ N) for five to one generation. With global warming, changes in the rice cultivation system, and extensive use of chemicals, C. suppressalis has emerged as the most devastating pest in rice [3]. It overwinters as a mature larva in facultative diapause, primarily in response to reduced daylight hours [6]. During winter, diapause larvae of C. suppressalis cope with low temperatures through behavioral and physiological adaptations. Specifically, behavioral adaptation is evidenced by larvae shifting their location to avoid unfavorable low temperatures [7]. In addition, physiological adaptation is manifested by an increase in the content of cryoprotectants such as glycerol, which improves their survival at low temperatures [8].
Factors such as photoperiod, temperature, humidity, or moisture have been observed to influence insect diapause [1,2]. Photoperiod and temperature are usually considered the most important drivers of insect diapause. For example, photoperiod induces diapause [6], low temperature plays a critical role in diapause maintenance [9], and high temperature accelerates post-diapause development [10]. In contrast, humidity or moisture is often considered a secondary factor [1], but it may directly affect the development, survival, and overwintering behavior of diapause insects [11,12,13,14,15,16] through influence on internal water balance in the insects or effects on microhabitat temperature, and it may exert indirect effects through influence on host plants [17,18,19].
Previous studies have shown that the supercooling point (SCP) of overwintering larvae of C. suppressalis in the temperate region is closely associated with soil water content [12]. However, given that C. suppressalis distributes widely from the tropical to the subtropical and temperate regions and that the overwintering period of larvae lasts about three months, there may exist regional differences in the response of the overwintering larvae of C. suppressalis to soil moisture. Further studies are needed to elucidate the dynamic effects of soil moisture in the subtropical regions, where the pest does the greatest damage to rice production. In this study, the dynamic effects of soil moisture on diapausing larvae of C. suppressalis were measured under natural winter conditions at the Guilin Experimental Station of Crop Pests, Ministry of Agriculture and Rural Affairs, China. For this purpose, we assessed the distribution and survival of diapausing larvae in rice stems, cold hardiness (SCP) and associated physiological indicators (larval weight, body water content, and contents of glycogen, trehalose, and glycerol), and moisture content of rice stems. The results of the study are of significance for the development of agronomic measures-based management of the overwintering population and prediction of the post-overwintering population of C. suppressalis.

2. Materials and Methods

2.1. Insects

Diapausing larvae of C. suppressalis were obtained from a laboratory stock culture reared under a short photoperiod. Briefly, newly hatched C. suppressalis larvae were reared on an artificial diet we developed [20] at 25 ± 1 °C, 60–70% relative humidity, and photoperiod L:D = 11:13. After 51 days, the fifth instar or older larvae that had not yet pupated were regarded as diapausing larvae [6]. Diapausing larvae of similar size and age were used in the tests.

2.2. Experimental Design

The experiments were conducted at the Guilin Experimental Station of Crop Pests (25°36′15″ N, 110°41′28″ E), Ministry of Agriculture and Rural Affairs, China that is located in the subtropics. Referring to Hou et al. [12], the effects of soil moisture were tested by setting up three levels of soil moisture contents, i.e., 25%, 50%, and 75% of saturated soil water content (SSWC). Specifically, sandy loam soil from the paddy fields at the experimental station was dried to constant weight in an oven at 105 °C, then ground to a fine powder and passed through a 2 mm sieve. The SSWC was determined to be 56.34% using the cutting ring method [21]. The dried fine soil powder was placed in plastic basins (length 49 cm, width 32 cm, height 14.5 cm) to a height of 10 cm, and tap water was added to obtain soil moisture of 25%, 50%, and 75% of SSWC (referred as M25, M50, and M75, respectively). The plastic basins were placed outdoors in a semi-natural environment sheltered from rain. Air temperature data were recorded from a nearby meteorological station (Table S1). During the experimental period (from 27 October 2021 to 25 January 2022), the highest daily air temperature averaged 14.9 °C (ranging from 2 to 25 °C) and the lowest daily temperature averaged 8.5 °C (ranging from −1 to 18 °C).
The effects of soil moisture on diapausing larvae of C. suppressalis were measured by transferring the larvae into rice stems that were transplanted in the basin soil. To this end, rice stubbles with roots washed of soil were cut at the upper end to leave a 30 cm rice stem and then completely submerged in water for 4 h to eliminate any insects inside the stems. After being air-dried in the shade for 16 h, the rice stubbles were transplanted evenly into the plastic basins at 15 per basin, with the base of the rice stems leveling with the soil surface in the basin. On 27 October 2021, diapausing larvae were individually transferred to the top end of a rice stubble to allow them to bore into the rice stems. Eighteen plastic basins were set up for each soil moisture treatment, among which three basins were not provided with the diapausing larvae and were used to measure the moisture content of the rice stem. The plastic basins (including soil, moisture, rice stubbles, and C. suppressalis larvae) were each weighed for initial weight on the day when the experiment started and then weighed every other day, and deficient water was added to maintain the initial weight and to keep the soil moisture consistent during the experimental period.

2.3. Distribution and Cold Hardiness of Diapausing C. suppressalis Larvae

At 30, 60, and 90 days of treatment (DOT) of soil moisture, 30 rice stems were randomly selected from each treatment (5 stems per basin) to record the larval survival status and height in the rice stems. The proportion of larvae distributing at the height of 0–10, 10–20, and 20–30 cm was calculated. And then the larvae were collected and divided into two groups. One group of the larvae was used to measure SCP, body water content, and glycogen content. Briefly, the diapausing larvae were measured individually for SCP using a SUN-V instrument (Beijing Pengcheng Electronic Technology Center, China) after fresh weight (FW) was measured [12]. Then, the larvae were dried at 60 °C until a constant dry weight (DW). Body water content (%) was calculated as (FW-DW) × 100/FW. The dried larvae were used in measuring glycogen content using the anthrone method as described by Yu et al. [22]. Another group of the larvae was used in obtaining hemolymph by the piercing method [23] for the measurement of glycerol and trehalose content using copper glycerinate colorimetry and anthrone trichloroacetic acid colorimetry, respectively, as described by Yu et al. [22].
To measure the moisture content of the rice stems, five rice stubbles were harvested from each treatment group and were each cut from the base of the rice stems into three segments (0–10, 10–20, and 20–30 cm). The segments were then weighed for fresh weight (FW) and then dried at 105 °C for 1 h and further dried at 65 °C until constant dry weight (DW). The moisture content of the rice stem (%) was calculated as (FW − DW) × 100/FW.

2.4. Statistical Analysis

Fisher’s exact test was used to examine significant differences in larval distribution height between soil moisture treatments. Influence of soil moisture, treatment time, and rice stem height on rice stem moisture content was analyzed using a multi-factor analysis of variance. A two-way analysis of variance was used to evaluate the effects of soil moisture and treatment time on larval SCP, weight, body water content, glycerol, glycogen, and trehalose content, and where there was a significant effect, means were compared using the least significant difference (LSD) test at the significance level of P = 0.05. The relationship between the distribution height of larvae and the moisture content of rice stems was fitted using linear regression. These statistical analyses were performed using DPS version 19.05 for Windows [24]. The mortality rates of the diapausing C. suppressalis larvae were compared between soil moisture treatments at certain treatment times using the Marascuilo procedure which is suitable for comparing multiple proportions [25].

3. Results

3.1. Distribution Height of Larvae within Rice Stems

It was found that the larvae distributed largely at the height of 0–10 cm of rice stems above the soil, with an average percentage of 64.6%. However, the distribution height of diapausing C. suppressalis larvae within rice stems was not statistically affected by soil moisture (Fisher’s exact test, P30 d = 0.153, P60 d = 0.696, P90 d = 0.669) and treatment time (Fisher’s exact test, PM25 = 0.218, PM50 = 0.382, PM75 = 0.132) (Figure 1).

3.2. Moisture Content of Rice Stems

Diapausing C. suppressalis larvae overwinter in rice stubble and rice stem moisture content can affect their distribution in the stubbles and their cold hardiness physiology. As our data showed, rice stems moisture content was significantly influenced by soil moisture (F = 8.75, df = 2,108, P < 0.001) and rice stem height (F = 14.36, df = 2,108, P < 0.001), but not by treatment time (F = 0.62, df = 2,108, P = 0.538) (Table 1). The moisture content of rice stems treated with 75% SSWC was approximately 4% higher than those treated with 25% and 50% (Figure 2A). The moisture content at 0–10 cm rice stem was significantly higher than that at the upper segments (Figure 2B). Rice stem moisture content was also significantly influenced by the interaction between soil moisture and rice stem height (F = 4.88, df = 4,108, P = 0.001), the highest at a combination of 75% SSWC and 0–10 cm rice stem height and the lowest at a combination of 25% SSWC and 20–30 cm rice stem height (Figure 2C).

3.3. Correlation between Larval Distribution Height and Rice Stem Moisture Content

Considering that soil moisture and treatment time had no significant effects on the distribution height of C. suppressalis diapausing larvae in rice stems, the data of rice stem moisture content under different soil moisture and treatment time conditions were combined in the analysis of the correlation between rice stem moisture content and larval distribution height. The results showed that larval distribution height was significantly and positively correlated with rice stem moisture content (F = 17.12, P < 0.001) (Figure 3).

3.4. Larval Cold Hardiness and Related Physiological Indicators

Soil moisture significantly affected larval weight (F = 5.60, df = 2,211, P = 0.004), glycogen content (F = 3.61, df = 2,32, P = 0.039), and trehalose content (F = 6.92, df = 2,18, P = 0.006), whereas it had no significant effects on SCP (F = 1.47, df = 2,99, P = 0.235), body water content (F = 0.20, df = 2,96, P = 0.819), and glycerol content (F = 1.39, df = 2,18, P = 0.274) (Table 2). Both larval weight and glycogen content decreased significantly with decreasing soil moisture (Figure 4A,B), while trehalose content increased with decreasing soil moisture (Figure 4C).
Treatment time significantly affected SCP (F = 6.18, df = 2,99, P = 0.003), larval weight (F = 18.03, df = 2,211, P < 0.001), trehalose content (F = 35.41, df = 2,18, P < 0.001), and glycerol content (F = 25.97, df = 2,18, P < 0.001), whereas it had no significant effect on body water content (F = 2.68, df = 2,96, P = 0.073) and glycogen content (F = 3.15, df = 2,32, P = 0.056) (Table 2). Larval supercooling capacity and glycerol content reached a maximum at 90 DOT (Figure 5A,D), while trehalose content was highest at 60 DOT (Figure 5C) and larval weight decreased significantly during treatment (Figure 5B).

3.5. Larval Mortality Rate

Analysis by the Marascuilo procedure shows that soil moisture and treatment time had no significant effects on the mortality rate of diapausing larvae of C. suppressalis (P > 0.05). All diapausing larvae survived at 30 DOT, and the mortality rates were less than 12% at 60 and 90 DOT in different soil moisture treatments (Figure 6).

4. Discussion

Insects exposed to unfavorable conditions may show behavioral adaptations to avoid damage. In this study, the diapausing C. suppressalis larvae were found to gather more at the lower part of the rice stem during the winter, where the moisture is higher than that at the upper part of the rice stem. This result is consistent with previous investigations [26,27]. Hygrotaxis is common in many insects, because high environmental humidity may help reduce body water loss and energy consumption [28,29]. In this study, soil moisture affected the moisture content of rice stems and the diapausing larvae distributed largely at the height of 0–10 cm of rice stems above the soil; however, the distribution height of diapausing C. suppressalis larvae in the rice stems was not under significant influence of soil moisture. Considering that moisture content in rice stems with 75% SSWC was only 4% higher than those in stems with 25% and 50% SSWC, the above result is not unexpected.
Substrate moisture affects the cold hardiness of many insects. In this study, soil moisture had no significant effect on the supercooling capacity and glycerol content of the diapausing larvae of C. suppressalis. However, Hou et al. [12] found that treatment with 25% SSWC significantly improved the supercooling capacity and glycerol content of overwintering larvae of C. suppressalis. The difference between this study and the previous report could be related to the temperature to which the C. suppressalis larvae were exposed. The lowest temperature in the northern temperate region during the experiment of Hou et al. [12] can reach −10 °C, while the lowest temperature in this study in the subtropics was only −1 °C (Table S1). Lower temperatures may amplify the influence of soil moisture on insect cold hardiness. Similar phenomena have been observed in other insects. For example, Zheng et al. [30] found that the SCP of Spodoptera exigua (Hübner) pupae treated with 30% SSWC was significantly lower than that of pupae treated with 60% SSWC when the lowest ambient temperature was −1 °C, but the difference between the soil moisture treatments disappeared at a minimum ambient temperature of 5 °C [31]. In addition, in this study, it was found that the supercooling capacity and glycerol content of C. suppressalis larvae were significantly increased at 90 DOT compared with 30 and 60 DOT, which might be related to the changes in ambient temperature from 30 and 60 DOT to 90 DOT. During this study in the subtropical Xing’an County, the average temperature from 27 December 2021 to 25 January 2022 (the 61–90 DOT) was lower than that from 27 October 2021 to 26 November 2021 (the 1–30 DOT) and from 27 November 2021 to 26 December 2021 (the 31–60 DOT) (Table S1). This result is consistent with previous findings that the seasonal variation in cold hardiness of overwintering C. suppressalis larvae is coupled with the seasonal variation of ambient temperature [8,32,33].
Soil moisture affects the survival of many insects, especially those that overwinter in the soil. At 80 DOT in soils with varying moisture, both high (≥80%) and low (15%) SSWC were found to be unfavorable for the survival of overwintering larvae of Carposina sasakii Matsumura [34]. In contrast, in this study, soil moisture was found to have no significant effects on the survival of C. suppressalis diapausing larvae in the subtropics. This difference could result from the difference in the specific overwintering sites of the insects. The C. suppressalis larvae overwinter in rice stubbles so that the influence of soil moisture on them is not as direct as that on insects overwintering in soil. Moisture content in rice stems with 75% SSWC was only 4% higher than those in stems with 25% and 50% SSWC, which may have attenuated the impact of soil moisture on the survival of C. suppressalis larvae. Moreover, the lowest ambient temperature during this experiment in the subtropics was only −1 °C (Table S1), while the SCPs of C. suppressalis overwintering larvae in soil moisture treatments were lower than the lowest ambient temperature, which may preclude the probability of overwintering larvae frozen to death [23].
Overwintering larvae that conserve much energy can improve their reproductive potential after diapause. In this study, dry soils significantly reduced the weight of diapausing C. suppressalis larvae. It is interesting that this result obtained in the subtropical ambient conditions corresponds to our previous investigation [12] in the northern temperate ambient conditions for the insect. The result can be due to that insects in humid soil may lose less water and expend less energy to maintain their body’s water balance than those in dry environments [28,29]. Xu et al. [35] found that the body weight of overwintering C. suppressalis larvae positively correlated with post-diapause reproductive potential. In this study, the body weight of C. suppressalis larvae decreased with decreasing soil moisture and gradually decreased with increasing treatment time. This phenomenon has also been observed in other insects, such as Diatraea grandiosella Dyar [36,37]. Studies have shown that trehalose is an important anti-desiccant substance that can improve cell membrane stability and alleviate damage caused by desiccation [38], while glycogen serves as an important energy reserve substance [39,40]. In this study, it was found that at low SSWC (25% and 50%), trehalose content of diapausing larvae of C. suppressalis increased significantly, while glycogen content decreased significantly. One possible explanation for this phenomenon is that the larvae consume more energy substances (e.g., glycogen) at low SSWC to accumulate anti-desiccants such as trehalose, which needs to be confirmed by further studies. What is certain is that dry soils significantly reduce the weight of diapausing C. suppressalis larvae, which decreases their post-diapause reproductive potential.

5. Conclusions

The results of this study indicate that overwintering larvae of C. suppressalis were behaviorally hygrotaxic and primarily concentrated at the lower part of rice stems where humidity is high. Physiologically, the insects showed significantly decreased glycogen content and weight whereas increased trehalose content with decreasing soil moisture. In the subtropics where this study was conducted, soil moisture did not significantly affect the supercooling capacity of C. suppressalis larvae, and the SCP was lower than ambient temperatures. Although soil moisture had no significant effects on larval mortality, the decreased weight of C. suppressalis larvae may result in a decrease in post-diapause reproductive potential. This opens the potential of developing agronomic measures-based management of the overwintering C. suppressalis population. However, to make that happen, it is necessary to further determine the role of draining paddy fields during winter in the subtropics in suppressing the population buildup of C. suppressalis in the spring.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/agriculture13122177/s1, Table S1: daily maximum, minimum, average ambient air temperatures (°C) from 27 October 2021 to 25 January 2022 at Xing’an, Guangxi.

Author Contributions

Conceptualization, C.D. and M.H.; data curation, J.Y. and Y.C.; investigation, C.D., Y.Z., J.Y. and Y.C.; software, C.D. and M.H.; writing—original draft, C.D. and Y.Z.; writing—review and editing, C.D. and M.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Science Foundation of China (32172413).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

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

Acknowledgments

The authors would like to thank Yue Cong, Jia Ding, Aocheng He, Xiaoyu Wang, and Huan Ke for their technical assistance with all the experiments. Thanks also to Ronggui Qin for his coordination of the experiments at the Guilin Experimental Station of Crop Pests, Ministry of Agriculture and Rural Affairs, China.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

SCP: supercooling point; SSWC, saturated soil water content; DOT, day of treatment; M25, soil moisture of 25% SSWC; M50, soil moisture of 50% SSWC; M75, soil moisture of 75% SSWC; FW, fresh weight; DW, dry weight; LSD, least significant difference.

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Agriculture 13 02177 g001
Figure 1. The effect of soil moisture on the distribution height of diapausing C. suppressalis larvae in the rice stems under natural environmental conditions in subtropical Xing’an. Each of the proportion data is based on observation of 30 insects.
Figure 1. The effect of soil moisture on the distribution height of diapausing C. suppressalis larvae in the rice stems under natural environmental conditions in subtropical Xing’an. Each of the proportion data is based on observation of 30 insects.
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Figure 2. Effects of soil moisture (A), rice stem height (B), and their combination (C) on rice stem moisture content. Mean values (±SD) are shown. Different letters over the bars indicate significant differences between soil moisture or rice stem heights (LSD test, P < 0.05).
Figure 2. Effects of soil moisture (A), rice stem height (B), and their combination (C) on rice stem moisture content. Mean values (±SD) are shown. Different letters over the bars indicate significant differences between soil moisture or rice stem heights (LSD test, P < 0.05).
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Figure 3. The correlation between the distribution height (y) of diapausing larvae of C. suppressalis and rice stem moisture content (x).
Figure 3. The correlation between the distribution height (y) of diapausing larvae of C. suppressalis and rice stem moisture content (x).
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Figure 4. Effects of soil moisture on larval weight (A) (n = 16–30), glycogen content (B) (n = 3–5), and trehalose content (C) (n = 3) of C. suppressalis larvae. Different letters over the bars indicate significant differences between soil moisture treatments (LSD test, P < 0.05).
Figure 4. Effects of soil moisture on larval weight (A) (n = 16–30), glycogen content (B) (n = 3–5), and trehalose content (C) (n = 3) of C. suppressalis larvae. Different letters over the bars indicate significant differences between soil moisture treatments (LSD test, P < 0.05).
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Figure 5. Effects of treatment time on larval SCP (A) (n = 9–14), weight (B) (n = 16–30), trehalose content (C) (n = 3), and glycerol content (D) (n = 3) of C. suppressalis larvae. Different letters over the bars indicate significant differences between treatment times (LSD test, P < 0.05).
Figure 5. Effects of treatment time on larval SCP (A) (n = 9–14), weight (B) (n = 16–30), trehalose content (C) (n = 3), and glycerol content (D) (n = 3) of C. suppressalis larvae. Different letters over the bars indicate significant differences between treatment times (LSD test, P < 0.05).
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Figure 6. Soil moisture effect on the mortality rate of diapausing larvae of C. suppressalis at 30 (n = 30), 60 (n = 25–30), and 90 (n = 20–30) days of treatment. Different letters over the bars indicate significant differences between treatment times (Marascuilo procedure, P < 0.05).
Figure 6. Soil moisture effect on the mortality rate of diapausing larvae of C. suppressalis at 30 (n = 30), 60 (n = 25–30), and 90 (n = 20–30) days of treatment. Different letters over the bars indicate significant differences between treatment times (Marascuilo procedure, P < 0.05).
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Table 1. Multi-factor ANOVA on the effects of soil moisture, rice stem height, and treatment time on rice stem moisture content.
Table 1. Multi-factor ANOVA on the effects of soil moisture, rice stem height, and treatment time on rice stem moisture content.
SourceSum of SquareDegrees of FreedomMean SquareFP
Soil moisture (M)450.222225.118.75<0.001
Rice stem height (H)739.192369.6014.36<0.001
Treatment time (T)32.09216.050.620.538
M × H502.404125.64.880.001
M × T100.00425.000.970.426
H × T23.1345.780.220.924
M × H × T32.9384.120.160.995
Table 2. Two-factor ANOVA for influence of soil moisture and treatment time on physiological parameters of diapausing C. suppressalis larvae.
Table 2. Two-factor ANOVA for influence of soil moisture and treatment time on physiological parameters of diapausing C. suppressalis larvae.
Physiological ParametersSource
Soil Moisture (M)Treatment Time (T)M × T
SCPF1.476.180.26
P0.2350.0030.905
Larval weightF5.6018.030.41
P0.004<0.0010.804
Body water contentF0.202.680.31
P0.8190.0730.873
Glycogen contentF3.613.150.14
P0.0390.0560.965
Trehalose contentF6.9235.413.81
P0.006<0.0010.021
Glycerol contentF1.3925.970.37
P0.274<0.0010.829
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Dai, C.; Zhong, Y.; Yu, J.; Cheng, Y.; Hou, M. Behavioral and Physiological Adaptation to Soil Moisture in the Overwintering Larvae of the Rice Stem Borer in the Subtropics. Agriculture 2023, 13, 2177. https://doi.org/10.3390/agriculture13122177

AMA Style

Dai C, Zhong Y, Yu J, Cheng Y, Hou M. Behavioral and Physiological Adaptation to Soil Moisture in the Overwintering Larvae of the Rice Stem Borer in the Subtropics. Agriculture. 2023; 13(12):2177. https://doi.org/10.3390/agriculture13122177

Chicago/Turabian Style

Dai, Changgeng, Yuqi Zhong, Jing Yu, Yiyu Cheng, and Maolin Hou. 2023. "Behavioral and Physiological Adaptation to Soil Moisture in the Overwintering Larvae of the Rice Stem Borer in the Subtropics" Agriculture 13, no. 12: 2177. https://doi.org/10.3390/agriculture13122177

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