Hongying Cui
Lili Li
Yingying Song
Wenxiu Guo
Suhong Lv- Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan, China
Increasing crop biodiversity, such as by adjacent managed crops, is recognized as an effective biological control measure. However, few studies have focused on the mechanisms involved in how adjacent managed crops increase natural enemy populations, leading to reduced pest numbers. This study investigated the hypothesis that cotton grown adjacent to sorghum would positively influence the feeding and oviposition preferences of the ladybug Propylaea japonica, which predates cotton aphids, leading to enhanced pest control. The populations of Aphis gossypii were significantly lower and those of P. japonica were significantly higher in cotton grown adjacent to sorghum compared with monoculture cotton fields. Regardless of diet on which the larva of P. japonica were reared (Melanaphis sacchari, A. gossypii, and 50% M. sacchari + 50% A. gossypii), the adults always consumed significantly more M. sacchari compared with A. gossypii. P. japonica also showed significantly higher feeding and oviposition preferences for host plants bearing aphids to only host plants. P. japonica fed M. sacchari preferred to lay eggs on cotton, whereas those fed A. gossypii preferred to lay eggs on sorghum. These results suggest that the habitat of natural enemies can be expanded by influencing their feeding and oviposition preferences to achieve pest control in adjacent cropping systems. This research, which incorporates field and laboratory studies, suggests an approach for the successful conservation and biological control of cotton aphids using adjacent managed cotton and sorghum crops.
Introduction
Large monoculture farming systems reduce farmland biodiversity and have altered the composition and stability of arthropod populations in agriculture, promoting pest outbreaks as well as decreasing the number and effectiveness of natural enemies, particularly indigenous generalist predators (Thies et al., 2005; Mkenda et al., 2019). The adjacent management of crops has been shown to be an efficient tool to enhance the abundance and diversity of natural enemies and reduce the abundance of pests, decreasing crop damage and providing direct benefits by reducing the need for pesticides (Meehan et al., 2011; Paredes et al., 2013). High crop species richness can suppress pest populations, suggesting that crop species richness also enhances biological control services (Sheng et al., 2017). Greenstone et al. (2014) reported that growing soybean adjacent to cotton as part of a conservation biological control strategy significantly decreased the number of the target pest, Megacopta cribraria shield bugs. Natural enemies that moved from adjacent wheat fields to cotton fields were able to maintain the cotton aphid population below the threshold at which significant damage would be caused (Men et al., 2004). Therefore, adjacent crop management has been used to increase natural enemy efficiency to reduce the incidence of crop pests (Scheid et al., 2011; Simpson et al., 2011). There have been many field studies of adjacent crop management on the interactions of pests and their natural enemies. However, little is known about the mechanisms involved.
Host plants on which prey feed affect the nutritional quality of those prey, in turn affecting the feeding preference, development, and mortality of their predators (Banihashemi et al., 2017). The nutritional quality of host plants is an important factor influencing the vigor of predators because not all prey species are equally nutritious (Zhang et al., 2012). Plants respond to herbivore-induced damage by releasing density-related volatiles (Cotes et al., 2015). These volatiles can be used by natural enemies to find their prey on infested plants (Pettersson et al., 2005). For example, the adults of many natural enemies of aphids orient to volatile compounds emitted by host plants in response to aphid feeding (Sasso et al., 2009). Volatiles from aphid-infested cotton have a key role in mediating the orientation behavior of the ladybug Propylaea japonica (Thunberg) (Coleoptera: Coccinellidae) (Wang et al., 2015). Such attraction is likely to increase the fitness of P. japonica because aphids represent a complete food source for both adults and juveniles (Obrycki et al., 2009).
Both the presence and quality of prey have strong effects on not only the retention of adult predators, but also their reproductive output (Hodek and Honek, 2009). For example, the quantity or quality of a prey directly influence whether a female predator will oviposit on the host plant (Yao et al., 2021). In general, natural selection favors predators that lay eggs in a site that is most appropriate for their offspring (Putra et al., 2009). For example, egg clusters of the ladybug Hippodamia convergens are typically found only on aphid-infested sorghum plants in the field but not on uninfested plants (Michaud and Jyoti, 2007). In addition, the abundance and quality of aphids in a habitat affects the survival of larvae (Seagraves, 2009). There is an optimal number of coccinellid eggs that can be laid in an aphid colony to maximize the number of surviving offspring (Rondoni et al., 2014) and aphids constitute a staple food for ladybugs that oviposit in the vicinity of aphid colonies (Oliver et al., 2006). However, how predator feeding and oviposition preferences suppress aphids in adjacent managed host crops is unclear.
Aphids are very serious insect pests in most agroecosystems in the world (Figueroa et al., 2018). The cotton aphid Aphis gossypii and sugarcane aphid Melanaphis sacchari are the two most dominant species in northern China (Ma et al., 2006; Guo et al., 2011). A. gossypii is an important cotton pest, which causes severe damage to crops, leading to economic losses, whereas M. sacchari is one of the most important pests on sorghum (Wu and Guo, 2005; Guo et al., 2011). The ladybird P. japonica preys upon a variety of crop pests in northern China, predominantly aphids and, thus, serves as an excellent biological control agent (Gao et al., 2010). Aphid availability and quality affect the fecundity and survival of P. japonica (Tang et al., 2013). Previous studies showed that sorghum was a source of ladybirds in cotton and, thus, incorporation of sorghum on farms growing cotton has the potential to enhance the biocontrol of cotton aphids on cotton in the field (Tillman and Cottrell, 2012). However, the mechanisms affecting the transfer and dispersal of P. japonica between sorghum and cotton remain to be elucidated.
Thus, the current study investigated: (1) the effects of adjacent managed cotton–sorghum ecosystems on P. japonica and its aphid prey; (2) the effects of aphid species on the consumption by, and behavioral responses of, P. japonica fed M. sacchari, A. gossypii, and 50% M. sacchari + 50% A. gossypii; and (3) the effects of host plant type (sorghum; cotton; sorghum inhabited by M. sacchari; and cotton inhabited by A. gossypii) on the feeding and oviposition preferences of adult P. japonica.
Materials and methods
Field experimental design
The field experiment was performed in 2021 at the Experimental Base of Shandong Agricultural Academy of Science, Jinan, Shandong, China (116.99°E, 36.97°N). Experimental units were 10 m × 100 m sorghum plots (variety Lunuo 8) planted adjacent to 40 × 100 m cotton plots (variety Lumianyan 28). A mono cotton field was used as a control. In the cotton and sorghum fields, each plot was sampled by using a 5-point random sampling method, and the number of A. gossypii, M. sacchari, and P. japonica on three cotton and three sorghum plants per point was recorded on 16 August 2021.
P. japonica breeding
Individuals P. japonica were collected from the Experimental Base of Shandong Agricultural Academy of Science in the field. The offspring of these P. japonica were reared in an artificial chamber (PRX-500D-30, Haishu Safe Apparatus, Ningbo, China), which was maintained at 28°C and 75% relative humidity (RH) under a photoperiod of 14 h:10 h light:dark. Newly hatched P. japonica were fed on three different diets (M. sacchari, A. gossypii, or 50% M. sacchari + 50% A. gossypii).
Host plants
Plants of two crops, cotton (variety LuMianYan 28) and sorghum (variety Lunuo 8), were selected for this study. Plants were grown in a potting mixture of peat moss, vermiculite, organic fertilizer, and perlite (10:10:10:1 by volume) in a greenhouse under natural light at 28 ± 2°C. Plants were randomly placed in the artificial chamber and re-randomized once a week to avoid positioning effects. No fertilizer or pesticides were used throughout the experiment.
Feeding and oviposition preference of P. japonica
The feeding preference of P. japonica was evaluated on sorghum, cotton, sorghum inhabited by M. sacchari, and cotton inhabited by A. gossypii. P. japonica individuals were collected directly from fields located in the Experimental Base, Shandong Agricultural Academy of Science. The experiment was conducted in a covered square cage (2.0 × 2.0 × 2.0 m). Twelve plants (three sorghum plants, three cotton plants, three sorghum plants inhabited by M. sacchari, and three cotton plants inhabited by A. gossypii) were placed in a random order at an equal distance from the center point to form a circle. Twenty adults P. japonica were placed on the center point within a replicate. The positions of the adult beetle were checked and recorded daily at 2-h intervals from 05:00 h to 21:00 h for 3 days.
The oviposition preference of P. japonica was assessed following the same method as described above for the feeding preference. P. japonica fed on M. sacchari, A. gossypii, and 50% M. sacchari + 50% A. gossypii, respectively. Five mated and ovipositing adult females (10 days old) were released in the center of square cover cage. The number of eggs laid on each plant was counted after 3 days to determine the oviposition preference.
Prey biomass consumption
The prey biomass consumed by P. japonica was determined using no-choice and free choice tests. A 24-h-starved adult female P. japonica (10 days old) that had previously been fed one of three different diets (M. sacchari, A. gossypii, or 50% M. sacchari + 50% A. gossypii) was provided with third-instar larvae of M. sacchari and A. gossypii. In the no-choice test, P. japonica was provided with 100 M. sacchari or A. gossypii larvae. In the free choice test, P. japonica was provided with 50 M. sacchari and 50 A. gossypii larvae. After 24 h, the number of unconsumed aphids was counted. The biomass consumption of P. japonica was then calculated based on the weight of 100 aphids and feeding ratio.
Y-tube experiments
A Y-tube olfactometer was used to investigate the behavioral responses of P. japonica adults that had fed on one of five diets (M. sacchari, A. gossypii, or 50% M. sacchari + 50% A. gossypii, fed on M. sacchari then fed on A. gossypii for 1 day and fed on A. gossypii then fed on M. sacchari for 1 day) to: (1) intact sorghum vs. intact cotton; (2) sorghum bearing M. sacchari vs. cotton bearing A. gossypii; and (3) M. sacchari vs. A. gossypii. For the treatments of different plants, plant was placed in a glass enclosure which connected to the ends of arms with five centimeters rubber tube. For the treatment of M. sacchari vs. A. gossypii, aphids were placed on the end of the arms.
The behavioral responses of P. japonica were determined in a 40 mm-diameter × 36 cm-long glass Y-tube olfactometer with a 60° inside angle. The flow rate was 4.8 L/min (equal to 3.8 m/min inside the tube) in each Y-tube arm. A single P. japonica was placed in the olfactometer for 10 min. A “no choice” outcome was recorded when the adults remained inactive during the test period. A “first choice” outcome was recorded when the adults moved >25 cm into either arm (visually assessed by a line marked on each arm). Each experimental pair was repeated with at least adult 80 P. japonica.
Statistical analysis
Two-way factorial ANOVA (SPSS 13.0, SPSS Inc., Chicago, IL, USA) was used to analyze the feeding preference and prey biomass consumption of adult P. japonica. One-way ANOVA was used to analyze the effect of adjacent crop management on the population numbers of M. sacchari, A. gossypii, and P. japonica in the field. Differences among means were determined using Tukey's test at P < 0.05. X2 tests were used to analyze the adult P. japonica feeding and oviposition preferences and to examine the significance of differences in the choosing behaviors of P. japonica in the olfactometer test.
Results
Effect of adjacent crop management on the numbers of M. sacchari, A. gossypii, and P. japonica in the field
The number of M. sacchari on sorghum was significantly higher than the number of A. gossypii on adjacent cotton (89.68%; F = 21.32, P < 0.001; Figure 1A). The same was found for A. gossypii populations on mono cotton compared with the number on adjacent cotton (67.05%; F = 35.90, P < 0.001; Figure 1B). Similarly, the number of P. japonica per 100 sorghum plants was significantly higher than on adjacent cotton (84.73%; F = 209.05, P < 0.001; Figure 1C), as was the number of P. japonica per 100 adjacent cotton plants compared with mono cotton (F = 18.48, P < 0.001; Figure 1D).
Figure 1. Effect of adjacent crop management on the numbers of M. Sacchari, A. Gossypii and P. Japonica in the field. (A) Population of Melanaphis sacchari on sorghum and Aphis gossypii on adjacent cotton. (B) Population of A. gossypii on adjacent cotton and mono cotton. (C) Population of P. japonica per 100 plants of sorghum and adjacent cotton. (D) Population of P. japonica per 100 plants on adjacent cotton and mono cotton. Different lowercase letters indicate significant differences among different crops (Tukey's test: P < 0.05).
Feeding preference
Host plant type significantly influenced the feeding preference of adult P. japonica, whereas time of day and host plant type × time of day did not (Table 1). P. japonica preferred sorghum to cotton, and with a significantly higher feeding preference for both types of host plant bearing aphids compared with host plants without aphids (Figure 2).
Table 1. ANOVA of the effects of host plant type and time of day on the feeding preference of Propylaea japonica.
Figure 2. Effects of host plant type on the feeding preference of adult Propylaea japonica. Different lowercase letters indicate significant differences between host plant type treatments at a set time (X2 test, P < 0.05).
Y-tube experiments
P. japonica fed M. sacchari showed a significant preference for the odor of sorghum compared with cotton (P < 0.01; Figure 3A). However, there was no difference in preference for host plant odor between the other four treatment groups (i.e., P. japonica fed 50% M. sacchari + 50% A. gossypii, A. gossypii + M. sacchari for 1 day, or A. gossypii, M. sacchari + A. gossypii for 1 day) (Figure 3A).
Figure 3. Effect of aphid species on the behavioral responses of Propylaea japonica, originally fed different diets (M. sacchari, A. gossypii, 50% M. sacchari + 50% A. gossypii, fed on M. sacchari then fed on A. gossypii for 1 day, or fed on A. gossypii then fed on M. sacchari for 1 day), to sorghum and cotton (A), sorghum with M. sacchari and cotton with A. gossypii (B), and M. sacchari and A. gossypii (C). The X2 test was used to analyze differences between the numbers of P. japonica in each arm of the Y-tube (*P < 0.05; **P < 0.01; ***P < 0.001; ns, non-significant).
P. japonica fed M. sacchari showed a significant preference for the odor of sorghum bearing M. sacchari compared with cotton bearing A. gossypii (P < 0.05; Figure 3B). However, there was no difference in preference for sorghum bearing M. sacchari vs. cotton bearing A. gossypii between the other four treatment groups (see above) (Figure 3B).
P. japonica fed M. sacchari significantly preferred M. sacchari to A. gossypii (P < 0.001; Figure 3C). However, there was no difference in preference for M. sacchari vs. A. gossypii in any of the other four treatment groups (see above) (Figure 3C).
Prey biomass consumption
Aphid species significantly influenced the biomass consumed by P. japonica in the no-choice and free choice tests (Table 2).
Table 2. ANOVA of the effects of P. japonica treatment (fed on different diets) and aphid species on the aphid biomass consumed by Propylaea japonica.
In the no-choice test, P. japonica adults fed M. sacchari (F = 5.12, P < 0.05), A. gossypii (F = 4.72, P < 0.05), and 50% M. sacchari + 50% A. gossypii (F = 6.50, P < 0.05) consumed significantly more M. sacchari compared with A. gossypii (by 25.74, 21.02, and 24.07%, respectively) (Figure 4A). However, there was no significant difference in the biomass of M. sacchari or A. gossypii consumed by P. japonica adults fed on above three treatments (Figure 4A).
Figure 4. Effects of aphid species on the prey biomass consumed by adult Propylaea japonica fed different aphid-based diets (M. sacchari, A. gossypii, and 50% M. sacchari + 50% A. gossypii) in the no-choice test (A) and free-choice test (B). Different lowercase letters indicate significant differences between aphid species within a P. japonica treatment, and different uppercase letters indicate significant differences between P. japonica treatments involving different aphid species (Tukey's test: P < 0.05).
In the free choice test, P. japonica adults fed A. gossypii (F = 5.61, P < 0.05) and 50% M. sacchari + 50% A. gossypii (F = 26.27, P < 0.001) consumed significantly more M. sacchari compared with A. gossypii (30.83 and 45.68%, respectively) (Figure 4B). However, there was no significant difference in the biomass of M. sacchari or A. gossypii consumed by P. japonica adults fed on above three treatments (Figure 4B).
Oviposition preference
P. japonica fed M. sacchari significantly preferred to lay their eggs on cotton compared with sorghum, and on sorghum bearing M. sacchari rather than sorghum alone (X2 = 7.630, P < 0.05; Figure 5). P. japonica fed A. gossypii significantly preferred to lay their eggs on sorghum bearing M. sacchari compared with cotton bearing A. gossypii, and on sorghum bearing M. sacchari compared with sorghum alone (X2 = 5.678, P < 0.05; Figure 5). P. japonica fed 50% M. sacchari + 50% A. gossypii significantly preferred to lay their eggs on host plants infested with aphids regardless of the aphid species compared with host plants only (cotton and sorghum) (X2 = 10.020, P < 0.05; Figure 5).
Figure 5. Effect of host plant on the oviposition preference of adult Propylaea japonica originally fed different aphid-based diets (M. sacchari, A. gossypii, and 50% M. sacchari + 50% A. gossypii). Different lowercase letters indicate significant differences between the type of host plant treatment within a P. japonica treatment (X2 test: P < 0.05).
Discussion
Researchers have evaluated the role of crop diversity in improving the impact of biological control, which enhances natural enemies and reduces pests (Rusch et al., 2016). High crop species richness suppresses pest populations by increasing the number of natural enemies (Sheng et al., 2017). There is a growing body of evidence suggesting that adjacent habitats positively affect pest regulation by natural enemies compared with monoculture systems (Bianchi et al., 2010). Large numbers of natural enemy taxa that move to adjacent crops provide a biological pest control service (Macfadyen and Muller, 2013). For example, alfalfa grown adjacent to wheat fields significantly increased the abundance of predators, including Hippodamia variegata and Chrysopa sinica, and decreased the densities of Macrosiphum avenae and Schizaphis graminum, which are dominant cereal aphid species in wheat fields (Zhao et al., 2013). In the current study, the number of M. sacchari on sorghum was significantly higher than of A. gossypii on adjacent cotton, whereas P. japonica populations were significantly higher on sorghum than on adjacent cotton, suggesting that the predator population increased with the increasing pest population on the host crop. In addition, A. gossypii populations were significantly smaller and P. japonica populations were significantly larger in adjacent cotton fields than in monoculture cotton fields. These results were consistent with previous studies of cotton grown adjacent to sorghum (Tillman and Cottrell, 2012). This suggests sorghum is an ideal crop for the conservation of predators that subsequently disperse to adjacent cotton fields and help control the aphid population.
The effects of a host plant on the palatability and suitability of the prey for a predator are well-known (Ugine et al., 2021). Prey preference and prey suitability are important for determining predator behavior, such as feeding and habitat selection (Weber et al., 2006). Published data indicate that induced volatiles attract natural enemies to an infested plant (Tan and Liu, 2014). For example, Harmonia axyridis females showed a significant preference for aphid-infested marigolds because of the plant volatiles induced by aphid feeding (Zhang et al., 2022). In the current study, P. japonica showed a significantly higher feeding preference for host plants bearing aphids compared with host plants alone. This might be because aphid-infested host plants, such as sorghum and cotton, release significantly higher amounts of volatiles compared with host plants without aphids, thus attracting higher numbers of natural enemies. Our results also showed that P. japonica preferred sorghum to cotton, which might be because sorghum is a C4 plant, whereas cotton is a C3 plant. Thus, crops grown adjacent to C3 (cotton) or C4 (sorghum) plants provide ideal systems for studying the transfer and dispersal of natural enemies.
Differential biomass consumption is indicative of aphid palatability to ladybugs (Mishra, 2005). Previous studies showed M. sacchari is an optimal food source for P. japonica among five species of aphids (Liu et al., 2013). The current results showed that P. japonica adults consumed significantly more M. sacchari compared with A. gossypii. This suggests that P. japonica prefers to consume M. sacchari, which could explain the increased P. japonica populations found in sorghum crops grown adjacent to cotton in the field. In our study, P. japonica fed M. sacchari also showed a significant preference for the odor of sorghum, sorghum bearing M. sacchari, and M. sacchari alone. After being fed A. gossypii for 1 day, these preferences disappeared. This suggests that, as M. sacchari populations decrease in the field, P. japonica would move to feed on A. gossypii, which could lead to a change in preference of P. japonica for M. sacchari, resulting in the transfer and dispersal of P. japonica in adjacent managed cotton–sorghum ecosystems.
The type of plant can also affect its suitability as a oviposition site for predators, such as ladybugs, and subsequently affect their reproduction (Mirhosseini et al., 2015). Host plants can have a dramatic effect on the survival of coccinellid eggs, with Coleomegilla maculata being shown to preferentially lay eggs on aphid-infested plants (Michaud and Jyoti, 2007). Female Propylea dissecta laid numerous eggs on plants with a high aphid density and fewer eggs on plants with a low aphid density (Omkar, 2004). In addition to coccinellids, oviposition preference of hoverflies varies in response to both the presence of aphids as well as their aphid (Amiri-Jami et al., 2016). In the current study, P. japonica significantly preferred to lay their eggs on aphid-infested cotton and sorghum, a result consistent with previous studies, presumably because the aphids are a food source for the larvae once they've hatched. It was also found that P. japonica fed M. sacchari preferred to lay eggs on cotton, whereas those fed A. gossypii preferred to lay eggs on sorghum. This suggests that oviposition behavior can be exploited to expand the habitat of ladybugs, an ecological adaptation of predatory natural enemies in the farmland ecosystems.
Conclusions
Our results indicate that an adjacent cropping system of cotton and sorghum can result in significantly higher P. japonica populations, leading to decreased aphid abundance compared with monocultures. P. japonica preferred to feed and lay eggs on aphid-infested plants over host plants without aphids, and also prefer to oviposit on other host plants. These results suggest that the habitat of natural enemies can be expanded by influencing their feeding and oviposition preferences to achieve pest control in adjacent cropping systems. Thus, increasing crop diversity, which provides favorable conditions for agriculture based on ecological principles, can contribute to the development of sustainable agroecosystems.
Data availability statement
The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author.
Author contributions
HC and XM conceived, designed, and performed the experiments. LL, YS, WG, SL, and YY contributed reagents, materials, and analysis tools. HC analyzed the data and wrote the paper. All authors contributed to the article and approved the submitted version.
Funding
This study was supported by Technology Innovation Project of Shandong Academy of Agricultural Sciences (CXGC2022E04) and the Key R&D Program of Shandong Province (2020CXGC010802).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
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Keywords: adjacent managed, Propylaea japonica, feeding preference, oviposition preference, Aphis gossypii, Melanaphis sacchari
Citation: Cui H, Li L, Song Y, Guo W, Lv S, Yu Y and Men X (2023) Behavioral mechanism of transfer and dispersal of Propylaea japonica in cotton adjacent to sorghum fields. Front. Sustain. Food Syst. 7:1151404. doi: 10.3389/fsufs.2023.1151404
Received: 26 January 2023; Accepted: 02 March 2023;
Published: 06 April 2023.
Edited by:
Fang Ouyang, Institute of Zoology (CAS), ChinaReviewed by:
Fajun Chen, Nanjing Agricultural University, ChinaXiaobin Shi, Hunan Academy of Agricultural Sciences, China
Copyright © 2023 Cui, Li, Song, Guo, Lv, Yu and Men. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Xingyuan Men, menxy2000n@hotmail.com