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Article

Understanding the Feeding Behavior and Identifying the Plant Parts Preferences of Fall Armyworm on Peanut Seedlings

by
Yuanyuan Cheng
1,2,
Lulu Liu
2,
Hongmei Li
2,3,*,
Xianming Yang
2 and
Suqin Shang
1,*
1
College of Plant Protection, Gansu Agriculture University, Lanzhou 730070, China
2
MARA-CABI Joint Laboratory for Bio-Safety, Institute of Plant Protection, Chinese Academy of Agricultural Science, Beijing 100193, China
3
CABI East and Southeast Asia, Beijing 100081, China
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(10), 2432; https://doi.org/10.3390/agronomy14102432
Submission received: 5 September 2024 / Revised: 12 October 2024 / Accepted: 17 October 2024 / Published: 20 October 2024
(This article belongs to the Section Pest and Disease Management)
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Abstract

:
Fall armyworm (FAW), Spodoptera frugiperda, has posed a serious threat to global food security since its discovery in Africa in 2016. Intercropping peanuts with maize is a very common cultivation practice, which can result in a high possibility of peanut damage by FAW. Our study investigated the feeding behavior, plant part preferences, and damage symptoms of FAW larvae on peanuts throughout the larval period, considering changes in population densities and the passage of time over the number of investigations. The results indicated that FAW larvae frequently inhabited peanut leaves, particularly the undersides of the leaves. Larvae moved from the leaves to the soil in the seedling pot to complete development. Furthermore, FAW larvae tended to feed on peanut leaves rather than stems regardless of population densities. Based on the damage symptoms, the feeding preferences of FAW larvae tended to be heart leaves, followed by mature leaves and stems. The most frequent damage symptoms caused by FAW to peanuts were “window panes”, followed by “leafless”. This study provides a reference for the integrated management of FAW in peanut fields.

1. Introduction

Fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), is a major polyphagous agricultural pest worldwide. This pest can infest over 300 different plants, including maize, rice, sorghum, wheat, peanuts, soybeans, and cotton [1,2]. Abdulqader in 2024 reported on the impacts of FAW on agriculture, where the impacts of FAW in western Australia were AUD 14.2–39.3 million/10 years, permanently impacting 0.8 million hectares and periodically impacting 150,000 hectares. Production losses in Africa ranged from 17.7% to 55.6% of grain yield. Globally, this could result in billions of dollars in crop losses each year, threatening food security in the invaded areas [3]. The key hosts vary between the different continents. In North America, maize, sorghum, and peanuts are the top hosts, while in South America, maize, soybeans, and cotton are predominant. Thus, the major hosts of FAW are not limited to maize; both Poaceae and Fabaceae plants are also favorable hosts [4]. Regardless of its host preference, FAW may explore other food resources and migrate to other crop-growing areas, causing damage to other crops [5,6].
Assessing pest preferences for different plants not only helps predict the occurrence of pests in different agro-ecosystems [7], but also helps develop effective monitoring and control programs for pests. For instance, Prasanna et al. reported that the preferred feeding site for FAW larvae is the still-rolled leaves of the maize plant, suggesting that this should be the first location to observe when looking for larvae. During the vegetative tassel stage, as the FAW larvae grow larger, they may be squeezed out of the whorl by the newly emerging tassel. Following this, the larvae move to the growing ear and bore into one side of it. When the plant is in its reproductive phase, the larvae will feed and take shelter within the ear. In addition, moths often lay their eggs on the newest 2–3 leaves emerging from the whorl [8]. FAW larvae initially feed on cotton leaves, but as larvae mature, there is a notable shift in their feeding preferences towards fruiting structures like squares, blooms, and bolls of cotton. FAW larvae at instar stages 1–3 were discovered on the main stem or branches of cotton plants, while later instars were observed on the middle to terminal portions of the plant, including branch tips. When scouting for FAW larvae in cotton fields, it is advisable to search near the main stems and low in the plant canopy [9]. In addition, understanding the behavioral preferences and habitat positions of FAW larvae can also aid in the development of new control strategies and techniques. Li et al. found that the developmental stage, habitat, and diet affect the gut bacteria of FAW, emphasizing the importance of a comprehensive understanding of the gut microbiome for effective pest management [10].
There have been a number of studies on legumes being damaged by FAW. In 1977, FAW attacked peanuts, soybeans, cotton, grains, sorghum, maize, Sudangrass or “Sudex”, and others, causing very serious damage to agriculture in Alabama [11] and peanut losses in Georgia exceeding USD 17 million [12]. FAW is regarded as the key Lepidopteran pest of peanut cultivation in Suriname [13]. FAW could complete its full life cycle on six different crops including leaves (peanut, cotton, soybean, sorghum, millet, and maize) and maize kernels, but prefers maize kernels, and the leaves of maize, peanut, and millet under laboratory conditions [14].
Peanuts are regarded as a cash crop and one of the most important oil and protein crops globally. China is the largest peanut producer with 18 million tons of production per year, followed by India, Nigeria, and the United States [15]. Cereal and legume intercropping is practiced worldwide [16,17]. Intercropping peanut and maize has shown many advantages in agricultural cultivation and intercropping peanut and common bean can greatly reduce FAW infestation in maize [18]. An indoor study of a maize-based intercropping system revealed the effects of four host plants, namely maize, sweet potato, soybean, and peanut, on the growth, development, and selective behavior of FAW [7]. However, these experiments did not explore the biology of FAW in relation to its behavioral preferences and habitat position on peanuts.
Understanding the behavior of FAW on different host plants is essential for the development of appropriate control strategies in peanut fields as well as intercropped fields. Under laboratory conditions, the probability of being located on different plant parts in peanut seedling pots, damage probability, and the number of times that peanut seedlings bore damage symptoms due to FAW larvae were studied for three different population densities. Studying the feeding behavior and plant part preferences of FAW larvae can help predict where FAW larvae may be located and thus how best to protect the peanut plants.

2. Results

2.1. Effects of Population Densities and Number of Investigations on Selection of Different Plant Parts and Other Positions by FAW Larvae

The plant part preferences of FAW larvae were significantly affected by the number of investigations (df = 7, F = 43.04, p < 0.001). As the number of investigations increased, the observed number of FAW larvae choosing the undersides of the leaves as their habitat decreased, while the observed number of insects choosing stems and soil gradually increased (Figure 1). There were significant interactions among the three factors: number of investigations, positions, and population densities (df = 91, F = 1.958, p < 0.001), and two of three factors (the number of investigations and positions, df = 49, F = 8.324, p < 0.001; the number of investigations and population densities, df = 14, F = 7.714, p < 0.001).
FAW larvae were found to primarily inhabit the undersides of the leaves during investigations 1–5, and although the probability decreased with larvae development, it was significantly higher than the rates for other positions during investigations 1–3, exceeding 40%. Stems were also an important habitat position throughout the entire larval stage, and at the fifth investigation, the probability of FAW larvae on stems (28.14 ± 6.51%) was almost equivalent to that on the undersides of the leaves (28.38 ± 6.95%). Hanging larvae were only observed during investigations 2–3 when the larvae were 2–3 instar and not so large and heavy with the highest probability at the third investigation (18.93 ± 7.68%). The probability of FAW larvae in the soil was significantly higher than all other positions during the seventh and eighth investigations. Since the larvae were about to pupate, the mature larvae preferred the soil.

2.2. Effect of Different Population Densities and Number of Investigations on Damage Probability Within Different Peanut Plant Parts

Different plant parts significantly affected the damage probability of seedlings (df = 3, F = 269.821, p < 0.001), and the interaction between different plant parts and the number of investigations also had significant effects (df = 21, F = 27.144, p < 0.001).
Throughout the whole study, the most damaged plant parts were the heart and mature leaves. The damage probability of the heart leaves peaked at the fourth investigation (46.94 ± 1.67%) and then gradually decreased. The damage probability of mature leaves was significantly higher (p < 0.05) than that of other parts of peanut plants, except for the first, second, and fourth investigations, because the number of mature leaves was the largest in the whole peanut plants. For the first investigation, the damage probability of young leaves was significantly higher (p < 0.05) than that of the heart leaves at all population densities (Table 1).

2.3. Effect of Different Population Densities and Number of Investigations on the Number of Occurrences of Damage Symptoms in Peanut Plants

The number of occurrences of damage symptoms was significantly associated with the number of investigations (df = 7, F = 5.792, p < 0.001), the population density (df = 2, F = 7.203, p = 0.001), and the types of damage symptom (df = 5, F = 51.166, p < 0.001). The interaction between the types of damage symptom and the number of investigations was also significant (df = 35, F = 2.915, p < 0.001) (Table 2).
The number of occurrences of “window panes” was significantly higher (p < 0.05) than other damage symptoms, as observed during investigations 1–4, indicating that this is the most common symptom [19]. The number of occurrences of “leafless” was significantly higher (p < 0.05) than the other damage symptoms in investigations 5–7 but was not significantly different from the number of occurrences of “window panes”. This indicates that FAW larvae can quickly cause serious damage. Moreover, “window panes” had the highest number of occurrences of all damage symptoms, regardless of population density, and occurred most significantly at a population density of 10 (Figure 2).

3. Materials and Methods

3.1. Plants

The seeds of the peanut variety “HUAYU 9511”, which belongs to Arachis hypogaea L. (Fabales: Fabaceae), were obtained from the Shandong Peanut Research Institute, China. Initially, the seeds were fully immersed in water to soak, followed by planting in plastic pots (D: 28 cm, H: 30 cm). A planting arrangement of 2 seeds per hole and 2 holes per pot was adopted. A transparent plastic cylinder (D: 25 cm, H: 42 cm) was positioned with its base inserted into the soil of each pot. The top of the cylinder was securely covered with mesh gauze and fastened with elastic bands to prevent insect infestation while facilitating easy observation. Once the seedlings reached the stage of having 4 to 6 leaves, they were deemed ready for the subsequent tests.

3.2. Insects

The initial population of FAW was collected from an untreated maize field in Mang Town, Mangshi county (24°28′40″ N, 98°36′2″ E), Yunnan Province, China. The larvae fed on leaves from the peanut variety “HUAYU 9511” [20] and were reared individually in plastic boxes (D: 2.5 cm, H: 3 cm), starting from the third instar stage to prevent any instances of cannibalism. Adults were reared in cages (D: 40 cm, H: 40 cm) and fed on a 10% honey–water solution as a nutritional supplement. These insects were continuously reared in an incubator (MGC-350HP, Shanghai Yiheng Scientific Instruments Co., Ltd., Shanghai, China) at 28 ± 1 °C, 60 ± 10% RH, and 14:10 (L:D). F5 generation newly hatched larvae were used in this study.

3.3. FAW Larvae on the Different Plant Parts of Peanuts Seedling and Damage Symptoms

Healthy FAW larvae that hatched within 24 h were transferred onto peanut leaves at three different population densities; 5 larvae, 10 larvae, or 20 larvae per pot. There were 4 replicates per population density, and each replicate included 6 peanut seedling pots. Therefore, there were 24 peanut seedling pots at each density, with a total of 72 pots in the whole experiment.
The plant part preferences and other positions of FAW larvae in the peanut seedling pot were divided into seven main categories: the undersides of leaves, the adaxial surfaces of leaves, heart leaves, stems, soil, hanging (on leaves/from the top cylinder, and on the gauze. Once the FAW larvae had been transferred to the leaves, the number of larvae in each position was counted and recorded. Following the removal of the transparent cylinder, a thorough inspection of the seedlings was conducted to determine the positions and number of FAW in each pot, along with their developmental stage, to complement and consolidate the recorded data.
The peanut plant parts were divided into four categories: heart leaves, young leaves, mature leaves, and stems [21]. If any damage was found on any plant part, it was recorded as 1, otherwise 0 was recorded.
The types of damage on peanut seedlings were also recorded and categorized as “window panes”, “leafless”, “withered”, “notching”, “pinhole”, and “filmy window panes” [22,23]. Filmy window panes: Translucent, filmy symptoms on the leaves caused by larvae scraping away the green tissue. Window panes: Large, window-like whorls caused by severe larval feeding [24]. Notching and pinhole: Small holes and irregular incisions form on the leaves after they are nibbled by larvae [25]. Leafless: State with virtually no leaves that the plant ends up in after the plant enters the vegetative stage and is defoliated severely by larvae. Withered: The central branches of the plant are cut off by larvae, ultimately leading to wilting. The number and type of damage symptoms on each plant part within the pot was recorded [26]. Finally, the height of the peanut seedling from the soil surface to the seedling tip was measured using a ruler and growth stage was recorded.
The first investigations began 24 h after the FAW larvae were transferred onto the seedlings. Any dead first instar larvae were replaced to maintain population densities. Subsequently, we conducted follow-up surveys, with a rough frequency of once every four days, but with extended intervals for the mature larval stage. The specific survey days were the 4th, 8th, 12th, 16th, 20th, 28th, and 42nd days. The total number of investigations conducted was eight. This allowed the capture of behavioral and population changes in FAW larvae at different development stages.
It is noteworthy that all experiments were conducted under environmental conditions at 26 ± 2 °C temperature and with 50 ± 10% relative humidity, which helped ensure that the results we observed were not disturbed by external factors.

3.4. Data Analysis

The original data were first sorted according to population densities and the times of investigation before performing significance analysis. All percentage data were transformed using Arcsine, and then subjected to the Shapiro–Wilk normality test [27]. The plant part preferences of FAW larvae, damage probability of peanut seedlings, and number of occurrences of damage symptoms were analyzed by GLM (multi-factor analysis of variance) in SPSS version 19.0 (IBM, New York, NY, USA). Similarly, one-way ANOVA was used to determine the effect of different population densities on the number of occurrences of the same damage symptom. The significance (p < 0.05) was identified for all means, which were compared using Tukey’s HSD test.

3.4.1. Plant Part Preferences of FAW Larvae Within Peanut Seedling Pots

The observed number of FAW larvae within each position was summed for each replication, and then all the subtotals from the seven positions were added together to obtain the total number of FAW larvae per replication. The probability of FAW larvae at each position per replication was calculated as follows: probability of FAW larvae at each position (%) = (observed number in each position/ total number) × 100.
Experiments were conducted comparing population densities, number of investigations, and position as independent variables. Then, the effect of the interaction between either of these factors as well as the interaction of all three factors was tested using GLM.

3.4.2. Damage Probability of the Peanut Seedling Plants by FAW Larvae

The damage frequencies per pot were summed across the replications. The damage probability of each plant part was calculated as follows: damage probability of each plant part for each replication (%) = (sum of damage frequencies to each plant part/all damage frequencies on all plant parts) × 100.
Damage probability was analyzed among population densities, number of investigations, and different plant parts as independent variables, and the effect of the interaction between any two of these factors as well as the interaction between all three factors was also tested by GLM.

3.4.3. Number of Occurrences of Damage Symptoms of Peanut by FAW

The number of occurrences of each symptom observed in each pot was summed to obtain the total number of occurrences of each symptom in each replicate, and then the number of occurrences of each damage symptom for each replicate at different population densities were summed. The number of occurrences of damage symptoms was analyzed with population densities, the number of investigations, and damage symptoms as independent variables, and the effect of the interaction between any two of these factors as well as the interaction of all three factors was also tested by GLM.

4. Discussion

FAW, renowned for its exceptional migratory capabilities and devastating polyphagous feeding patterns, is a prominent invasive pest [28]. The availability of alternative host crops and the adoption of crop rotation practices play pivotal roles in shaping the population dynamics and potential outbreaks of such polyphagous pests. Therefore, gaining a comprehensive understanding of the biological characteristics and feeding behaviors of these pests across diverse food sources is imperative for devising effective, long-term, and environmentally sustainable management strategies [29].
At different population densities, FAW larvae were generally consistent in their selection of positions, preferring the undersides of the leaves. As the number of investigations increased, the probability of FAW larvae within other positions increased, which indicated that FAW larvae disperse as they develop. It is a common phenomenon for insects that an initial cluster of eggs is followed by larvae finding different sources of both shelter and food for their survival. Similarly, Luehdorfia chinensis leei started to separate and disperse into different habitats from the third instar stage onwards, to molt and find new food resources [30]. We found that 5th–6th instar FAW larvae began to hide in the soil in preparation for pupation, which may provide a safe environment that maintains moisture and temperature during pupation. FAW mature larvae have been shown to hide on the soil surface of peanut fields during the day [23].
The feeding behavior of FAW larvae on peanut plants can be inferred from the damage probability of FAW larvae on each plant part. In this study, FAW preferred to feed on peanut leaves rather than stems, but as the population density increased and time went on, their feeding range gradually extended from leaves to the whole plant. Overall, peanut leaves had the highest damage probability. Similarly, FAW larvae primarily feed on leaves in maize, but under high density conditions, they may turn to feeding on cobs [31]. Furthermore, on crops such as soybeans and sugarcane, FAW larvae also prefer tender parts like young leaves, buds, and flower clusters, while mature larvae tend to hide on the soil in the field [32,33]. The feeding sites of FAW larvae on cotton plants vary with the age of the larvae [9]. These observations indicate that FAW larvae exhibit a preference for young and tender tissues across multiple crop species, but their feeding behavior also adjusts according to the crop and the stage of their growth and development.
FAW larvae can cause varying degrees of damage to plants, manifesting as various damage symptoms. In this study, damage symptoms on leaves were the most obvious. The occurrence of “window panes” was significantly higher than other damage symptoms, followed by “leafless”. The relationship between leaf damage and peanut yield was not analyzed, however, as leaf damage may affect photosynthesis and normal plant growth, and this would then impact peanut yield and quality. Leuck et al. found a correlation between reductions in yield and an increase in the severity of leaf ragging damage among different plant varieties [34]. Chisonga et al. [35] found that leaf damage scores obtained from scouting could be used to predict yield loss and that the sensitivity of plants to leaf damage was related to the maturity rate of the variety.
In addition, Costa et al. [36], in their study of the effect of peanut varieties and neem oil on the feeding preferences, developmental period, and mortality of FAW, indicated that the selection of peanut varieties is also important and that the varieties to be planted should be selected based on the history of the pest in the area. Therefore, we should pay close attention to the occurrence of FAW and strengthen its monitoring, reducing the yield loss in peanut fields.

5. Conclusions

This study has shown that FAW larvae preferred to stay on the undersides of leaves but that they also spread to other positions such as soil over time. In addition, FAW larvae preferred to feed on peanut heart and mature leaves, with “window panes” and “leafless” being the most predominant of all damage symptoms.
By understanding the preferred feeding parts and preference of plant parts for FAW larvae on peanuts, precise control measures can be taken to mitigate damage, for example, hanging parasitoid cards on the undersides of the leaves, or directing liquid, powder, or granular control products to precise locations. FAW larvae can also be manually removed from the undersides of the leaves and the stems in cases of high population densities. Reasonable management practices and scientific control methods will help to minimize the damage of FAW to peanuts and ensure safe growth and a good harvest of the crop.

Author Contributions

Conceptualization, H.L. and S.S.; methodology, Y.C., L.L. and H.L.; validation, H.L., Y.C. and X.Y.; formal analysis, Y.C.; investigation, L.L.; data curation, L.L. and H.L.; writing—original draft preparation, Y.C. and L.L.; writing—review and editing, H.L., X.Y. and S.S.; funding acquisition, H.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the CABI Development Fund (IVM10051), the European Union’s Horizon Europe framework programme (101060430) and International Science & Technology Innovation Program of the Chinese Academy of Agricultural Sciences (CAASTIP).

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Probability of FAW larvae at each position: Varying with population densities and number of investigations. All data are presented as the mean ± SE. Different lowercase letters indicate significant differences between probability at each position for the same number of investigations and population densities (Tukey’s HSD test, p < 0.05).
Figure 1. Probability of FAW larvae at each position: Varying with population densities and number of investigations. All data are presented as the mean ± SE. Different lowercase letters indicate significant differences between probability at each position for the same number of investigations and population densities (Tukey’s HSD test, p < 0.05).
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Figure 2. Number of occurrences of each damage symptom in peanut plants at different population densities. All data are presented as the mean ± SE. Different lowercase letters indicate significant differences between the number of damage symptom occurrences at different population densities for the same damage symptom (Tukey’s HSD test, p < 0.05).
Figure 2. Number of occurrences of each damage symptom in peanut plants at different population densities. All data are presented as the mean ± SE. Different lowercase letters indicate significant differences between the number of damage symptom occurrences at different population densities for the same damage symptom (Tukey’s HSD test, p < 0.05).
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Table 1. Damage probability of the different seedling parts of peanut at different population densities and number of investigations.
Table 1. Damage probability of the different seedling parts of peanut at different population densities and number of investigations.
Number of InvestigationsPopulation DensityDamage Probability (%)
Young LeavesHeart LeavesStemsMature Leaves
1587.05 ± 8.85 a12.95 ± 8.85 b--
1074.70 ± 4.05 a25.30 ± 4.05 b--
2083.93 ± 5.92 a16.07 ± 5.92 b--
25 33.33 ± 23.57 a-66.67 ± 23.57 a
10 6.25 ± 6.25 b-93.75 ± 6.25 a
2014.29 ± 14.29 b15.48 ± 8.99 b-70.24 ± 20.24 a
354.17 ± 4.17 b20.83 ± 12.5 b-75.00 ± 14.43 a
10-17.61 ± 10.99 b-82.39 ± 10.99 a
20-7.74 ± 4.49 b-92.26 ± 4.49 a
45-50.00 ± 0.00-50.00 ± 0.00
1010.00 ± 5.77 b45.00 ± 2.89 a-45.00 ± 2.89 a
20-45.83 ± 4.17 a8.33 ± 8.33 b45.83 ± 4.17 a
55-21.07 ± 10.52 b-78.93 ± 10.52 a
10-15.53 ± 10.72 b-84.47 ± 10.72 a
20-6.67 ± 6.67 b-93.33 ± 6.67 a
65-5.56 ± 5.56 b-94.44 ± 5.56 a
10-4.17 ± 4.17 b-95.83 ± 4.17 a
20---100.00 ± 0.00
75--5.56 ± 5.56 b94.44 ± 5.56 a
10--27.98 ± 7.86 b72.02 ± 7.86 a
20--28.89 ± 10.6 b71.11 ± 10.60 a
85---100 ± 0.00
10--23.33 ± 14.53 a76.67 ± 14.53 a
20--30.00 ± 10.00 b70.00 ± 10.00 a
All data are presented as the mean ± SE. Different lowercase letters indicate significant differences between different damage probabilities with the same number of investigations and population densities (Tukey’s HSD test, p < 0.05); - means data not available.
Table 2. Multi-factor analysis of variance of factors influencing the number of occurrences of damage symptoms in peanut plants.
Table 2. Multi-factor analysis of variance of factors influencing the number of occurrences of damage symptoms in peanut plants.
Dependent VariableFactordfF Valuep Value
Occurrence timesNumber of investigations75.7920.001
Population density27.2030.001
Types of damage symptoms551.1660.001
Number of investigations * Population density141.1210.336
Number of investigations * Types of damage symptoms352.9150.001
Population density * Types of damage symptoms101.7700.064
Number of investigations * Population density * Types of damage symptoms700.5420.999
* represents the interaction between the two factors.
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Cheng, Y.; Liu, L.; Li, H.; Yang, X.; Shang, S. Understanding the Feeding Behavior and Identifying the Plant Parts Preferences of Fall Armyworm on Peanut Seedlings. Agronomy 2024, 14, 2432. https://doi.org/10.3390/agronomy14102432

AMA Style

Cheng Y, Liu L, Li H, Yang X, Shang S. Understanding the Feeding Behavior and Identifying the Plant Parts Preferences of Fall Armyworm on Peanut Seedlings. Agronomy. 2024; 14(10):2432. https://doi.org/10.3390/agronomy14102432

Chicago/Turabian Style

Cheng, Yuanyuan, Lulu Liu, Hongmei Li, Xianming Yang, and Suqin Shang. 2024. "Understanding the Feeding Behavior and Identifying the Plant Parts Preferences of Fall Armyworm on Peanut Seedlings" Agronomy 14, no. 10: 2432. https://doi.org/10.3390/agronomy14102432

APA Style

Cheng, Y., Liu, L., Li, H., Yang, X., & Shang, S. (2024). Understanding the Feeding Behavior and Identifying the Plant Parts Preferences of Fall Armyworm on Peanut Seedlings. Agronomy, 14(10), 2432. https://doi.org/10.3390/agronomy14102432

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