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Perspective

Natural-Enemy-Based Biocontrol of Tobacco Arthropod Pests in China

by
Wenxin Xue
†,
Pengjun Xu
†,
Xiufang Wang
,
Guangwei Ren
and
Xinwei Wang
*
Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2023, 13(8), 1972; https://doi.org/10.3390/agronomy13081972
Submission received: 21 June 2023 / Revised: 19 July 2023 / Accepted: 25 July 2023 / Published: 26 July 2023
(This article belongs to the Special Issue Biological Pest Control in Agroecosystems)
Versions Notes

Abstract

:
The devastating impact of chemical pesticides has prompted a shift towards sustainable agricultural pest management, such as biological control with natural enemies. In recent years, commercialization advancements have enabled the suppression of pest populations through augmentative releases of biological control agents, with natural enemies being a major tactic. China has successfully implemented natural-enemy-based biocontrol strategies, particularly for controlling aphids and lepidopterans. This article provides a comprehensive overview of the state-of-the-art natural-enemy-based biocontrol against arthropod pests in tobacco in China, including practical achievements in mass-rearing methods, augmentative release strategies, and the wide-scale use of natural enemies. Current and potential future challenges for natural-enemy-based biocontrol in China are also discussed.

1. Introduction

Arthropod pests, including insects and mites, pose a major challenge to agriculture worldwide, causing substantial loss to global crop production [1]. Herbivorous arthropods, in particular, can cause yield losses of up to 20%, which can have a significant impact on sustainable crop growth [2,3]. In China, tobacco (Nicotiana tabacum L.) is a non-food crop of great economic importance, with a cultivation area of 9.4 billion hm2 in 2020 [4]. However, arthropod pests have a significant impact on the yield and quality of tobacco leaves, resulting in substantial economic losses (as shown in Table 1).
In the past few decades, chemical pesticides have been the primary method of controlling arthropod pests. However, this approach has led to the development of widespread pesticide resistance, as well as the contamination of agroecosystems and negative health effects [6]. Therefore, Integrated Pest Management (IPM) should focus on more sustainable approaches, such as physical, cultural, or biological controls. While physical and cultural controls that rely on engineering techniques demand more labor and time, their implementation is often limited to specific treated areas, which restricts their effectiveness in the field-crop market [7]. As such, biological control is a main contributor to sustainable agriculture, which involves using one species or biological agent to control the population size of another species [8,9]. Predators and parasitoids are among the core components of biological control agents used in agroecosystems [10,11,12]. China has a rich diversity of natural enemies for arthropods, with 283 natural enemy species from 71 families known to control sugarcane pests [13,14]. For example, species from the genus Trichogramma have been successfully used to control Lepidopteran pests [15].
Three primary methods for manipulating predator and parasitoid densities are classical, conservation, and augmentative biological control, as outlined by Van Lenteren et al. (2006) [16]. Classical biological control involves releasing natural enemies collected from the pest’s area of origin into invasive areas, resulting in permanent pest population reduction. Conservation biological control seeks to protect and enhance the performance of naturally occurring natural enemies [17]. Augmentative biological control involves mass-rearing and releasing natural enemies, either in large numbers for immediate control in crops with short production cycles (inundative biological control) or over several generations in crops with long production cycles (seasonal inoculative biological control) [18]. This strategy is becoming an increasingly popular and important option for mitigating economic losses caused by pest damage worldwide [18]. The small populations of natural enemies in China have limited their ability to significantly control tobacco pests [19]. Moreover, the potential breakdown of current biological control agents and the predicted increase in pest outbreaks due to global climate change have further reduced the effectiveness of natural enemies in pest control [20,21,22,23,24]. In more detail, the occurrence of warmer winters or a decrease in the frequency of deep frosts is resulting in a rise in pest outbreaks [22,23,24,25]. Moreover, pests are spreading into regions that are lacking their natural enemies, while climate change, host plants, herbivores, and farmers’ adaptive management strategies are altering the abundance and activity of natural enemies. These spatial and temporal mismatches between pests and their enemies may reduce the effectiveness of these biocontrol measures [21]. However, the augmentative releases of biological control agents partially compensate for these drawbacks and have proven to be a successful strategy in maintaining high densities of natural enemies, even in suboptimal conditions [18]. Currently, over 150 species of natural enemies are available for augmentative releases, allowing for the control of approximately 100 pest species [26]. Since the 1970s, China has made significant progress in exploring augmentative releases of biological control agents, including the use of the Trichogramma species [15].
In this article, we present a comprehensive review of the practical knowledge and achievements gained through the development of natural-enemy-based augmentative biological control programs in tobacco-growing regions of China. Furthermore, we highlight the successful implementation of natural enemies on a wide scale and identify the key traits that contribute to effective biological control. We believe that our findings will renew interest in natural-enemy-based methods both in China and in other countries.

2. Major Pests and Potential Natural Enemy Species on Tobacco

To date, over 700 species of arthropod pests have been identified in Chinese tobacco fields and storage facilities [27]. The common species are listed in Table 1, among which the major pests are Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae), Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae), Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae), Myzus persicae (Sulzer) (Hemiptera: Aphididae), and Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae).
A survey conducted in a tobacco-growing region of China revealed the presence of 743 natural enemy species belonging to 273 genera and 27 families [28]. Table 2 presents a list of arthropod species that have undergone successful mass-rearing for large-scale application in China. This list includes one parasite (Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae)) and three predators (Arma chinensis (Fallou) (Hemiptera: Pentatomidae), Amblyseius cucumeris (Oudemans) (Acari: Phytoseiidae), and Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae)), as well as predators with the potential for future development in pest management, such as: Eocanthecona furcellata (Heteroptera: Pentatomidae) and Habrobracon hebetor (Say) (Hymenoptera: Braconidae). In the following section, we will delve into several biocontrol cases that utilize natural enemies to showcase China’s efforts and achievements in managing tobacco arthropod pests.

3. Study of Biocontrol Cases

Over the last decade, China has witnessed a steadfast commitment to natural enemies in the control of economically significant pests on tobacco. This dedication has yielded several noteworthy successes in natural-enemy-based biocontrol against tobacco’s key arthropod pests. These triumphs primarily stem from two factors: mass-rearing production and release strategies. Establishing mass production systems is a crucial prerequisite for achieving effective and cost-efficient large-scale releases in the field. Additionally, the success of release strategies is closely tied to the control effect.

3.1. Case 1: Aphidius-Gifuensis-Based Biocontrol

A. gifuensis is a versatile endoparasitoid that can parasitize various species of aphids. It is the most commonly used biological control agent for managing M. persicae on tobacco crops in China due to its high parasitism rate, reaching over 85% in the field [29,30]. The study and application of A. gifuensis for aphid control in China began in the early 1970s. Since 2010, A. gifuensis has been widely promoted and utilized in the tobacco system of Yunnan Province [31]. Since 2019, this biological control agent has been adopted as the main technology for aphid management, leading to a decrease in pesticide usage. Through systematic research on the biological and ecological characteristics of A. gifuensis, China has accumulated extensive experience in breeding and applying this species. Furthermore, a national standard, “Code of Practice for Myzus persicae (Sulzer) Biological Control with Aphidius gifuensis,” was released in 2019. This standard specifies the technical requirements for breeding A. gifuensis for the management of M. persicae, including A. gifuensis breeding, M. persicae release, investigation of control effects, seed conservation, and more.

3.1.1. Mass-Rearing Production

Most of the mass-rearing techniques for A. gifuensis have been mechanized and/or automated.
In certain tobacco planting areas in China, the mass-rearing of A. fumigatus is carried out in greenhouses located near the fields. This involves cultivating aphid host plants, propagating M. persicae, inoculating parasitoids, and selecting and collecting mummified aphids, M. persicae, and A. gifuensis for preservation [31,32]. This method offers the advantages of convenient transportation, detachable structures, intelligent controls of environmental conditions, and immediate release of parasitoids after production. However, the cost of mass-rearing on potted tobacco in greenhouses is high. To address this issue, a study on floating tobacco seedlings and the simultaneous inoculation method was conducted. This method is characterized by a short cycle, low cost, and high efficiency in feeding M. persicae [33,34,35]. In regions with specific climate characteristics such as seasonal rainfall and low temperature, the growth of tobacco and propagation of A. gifuensis may be greatly restricted. In such cases, the floating radish seedlings and simultaneous inoculation method can be a targeted solution [29]. Radish is a semi-cold-tolerant vegetable that supports the short growth and development period and the fast propagation of M. persicae. Moreover, the technique of simultaneous inoculation of M. persicae with A. gifuensis simplifies the breeding process to some extent [36].
A. gifuensis can be stored and transported in two forms: adult A. gifuensis or mummified parasitized aphids. Due to the strong activity and short life span of adults, storage and transportation conditions are more demanding and costly. Therefore, it is suggested to carry on packing transport in the form of mummified aphids. A high degree of mechanization and automation has been achieved in the separation, drying, impurity removal, collection, counting, and packaging of mummified aphids. Through multiple generations of iterative updates, a range of devices and machines have been introduced for application [37], namely the digital image recognition and counting system, an assembly line separating and washing device to collect the mummified aphids, an electrical device to dry the mummified aphids, an automatic selection machine to remove impurities, and an automatic quantitative divider to put the mummified aphids into the box with the specific packaging specifications [38,39,40,41,42,43,44,45]. To sum up, this equipment would greatly increase the mummified aphid efficiency; save money, time, and labor with a fully automatic operation; and keep the damage rate of mummified aphids at a low level.
Other key factors that restrict the industrial application of A. gifuensis are long-term storage and long-distance transportation. In the south and the north, the generation number of A. gifuensis is completely different, so the parameter setting up should be studied in different ways according to local conditions. A large number of targeted research also enables the natural enemy produce companies to master the rich experience of temperature and humidity preservation transportation [46,47,48,49,50,51].

3.1.2. Field Application

The release of the natural enemy is affected by the host crop, environment, and other factors. The amount and way of releasing are also different with different control objects. Additionally, to achieve a better aphid control effect, the augmentative release strategies of A. gifuensis are continuously explored. Several strategies have been developed: the release of an adult wasp A. gifuensis, hanging the card of mummy aphids, naturally scattering them field sheds, releasing them by the cage of A. gifuensis, etc. For example, the population of aphids can be controlled in a short time by the release of adult A. gifuensis. But it also has some limitations, such as the high mortality rate of A. gifuensis during the release process and that the control effect can be achieved only after multiple releases [52]. The auto-sustained continuous release through naturally scattering them by filed A. gifuensis breeding sheds and releasing them by the cage of A. gifuensis could perform better on the persistence control of aphids. Hence, the combination of different release methods should be considered in the application to achieve a better prevention effect [53]. Moreover, suitable release strategies (the release number and times of A. gifuensis) for different regions or situations have been further studied (Table 3) [53,54,55,56].
Regarding field application scales, in 2018, the national promotion area reached 890,000 hm2, covering more than 99 percent of the total tobacco planting area [57] and obtaining an excellent control effect (82.2%). Since then, the coverage of the promoted area has been kept in full tobacco field coverage, and the effect of aphid control has been continuously improved.

3.2. Case 2: Arma-Chinensis-Based Biocontrol

A. chinensis is an polyphagous predator with a broad prey range [58]. Originating from China, it is commonly utilized for controlling Lepidopteran pests such as H. armigera, S. litura, and S. exigua on tobacco crops [13]. Over the past three decades, extensive research has been conducted on its geographical distribution, morphology, and biological characteristics, leading to advancements in artificial breeding and field release methods.

3.2.1. Mass-Rearing Production

One of the key issues in the efficient mass-rearing production of polyphagous predators is finding the proper food. The palatability and nutrient composition of food directly affects the feeding behavior, growth and development, and reproductive characteristics of the predators. The first part is artificial breeding based on natural preys. In China, A. chinensis is mainly reared on the pupae of Antheraea pernyi (Guérin-Méneville) (Lepidoptera: Saturniidae). During the production, it was found that the inability to completely feed on pupae and the production time and cost of A. pernyi pupae would restrict the mass-rearing of A. chinensis [59]. Therefore, a study from Xie et al. (2020) compared the fitness of three preys, the larvae and pupae of Mythimna separate (Walker) (Lepidoptera: Noctuidae) and larvae of Tenebrio molitor (Coleoptera: Tenebrionidae), by monitoring the developmental duration, egg hatchability, adult body weight, egg production, and mortality of A. chinensis. The results showed that M. separate pupae performed best on each monitoring index, followed by T. molitor larvae and M. separate larvae. A similar study comparing the performance of T. molitor, M. separate, and Prodenia litura larvae as preys confirmed the advantages of T. molitor and M. separate as preys for the mass-rearing of A. chinensis [60]. In addition, Wang et al. (2020) showed that the mixed diet of M. separate larvae with a small amount of H. axyridis pupae was beneficial to the early development and reproduction of stinkbugs [61]. Compared with M. separate pupae, T. molitor pupae could improve fecundity as food during the adult mating period [62].
In mass-rearing with prey, besides the high economic and time cost, the risk of prey shortage also exists but could be effectively solved by an artificial diet. An artificial semi-synthetic feed of a micro-encapsulated A. pernyi pupa reduces the feeding cost by 50% while ensuring the normal production quality by feeding A. pernyi pupae directly [63].
Meridic diets have been developed for rearing several hemipteran predators and are a staple of the future. The main recipes studied so far include the following three: major ingredient of Recipe 1—eggs, liver, and tuna [64]; Recipe 2—beef, beef liver, and egg yolk [65]; Recipe 3—milk and egg [66]. All formulations meet the basic nutritional requirements of A. chinensis growth but need to be modified to achieve the same or even better performance than preys. The nutritional analysis of preferred preys is helpful to clarify the requirement and ratio of certain nutrients for predators and to provide nutritional guidance for the development of artificial diets [67]. The growth, development, and reproduction of A. chinensis at different stages could be significantly and positively affected by adjusting the content of saturated fatty acids and unsaturated fatty acids in the artificial diet to increase the adult acquisition rate and population growth rate of A. chinensis [68].
In addition to the development of food for rearing A. chinensis, other constraints to its mass production were explored. For example, the process of how to adjust the parameters of density and sex ratio to obtain the optimal survival rate and fecundity and to avoid intraspecific mutilation behavior was detailed [69,70,71].

3.2.2. Field Application

At present, research mostly stays in the laboratory stage, and there are limited cases of large-scale field release. The year of 2018 was the first year of the national pilot promotion of 2000 hm2 for H. assulta and S. litura management. The average control efficiency was 51.48% [57]. By 2021, the promotion area reached 35,000 hm2 with a 57.68% control efficiency.
It is worth noting that the density of A. chinensis decreased quickly as individuals dispersed from the release sites, and the efficiency of pest control was largely discounted. In this scenario, early population establishment on the crop was needed to use A. chinensis as a biological control agent [72].

3.3. Other Cases

3.3.1. Ladybeetle-Based Biocontrol (Coccinella septempunctata and Harmonia axyridis)

Predacious ladybeetles, Coccinella septempunctata (ladybird) (Coleoptera: Coccinellidae) and H. axyridis, are widely distributed in China and have a strong predation ability on aphids. They possess the characteristics of a big appetite, long life, and strong ability to adapt to the environment. Several studies have indicated that they have broad application prospects in the control of M. persicae in tobacco fields. At present, many studies report on bioecological characteristics, artificial diet, artificial feeding, and field application, among which there are also related studies on M. persicae.
The artificial rearing of C. septempunctata and H. axyridis mainly adopts aphids as a natural prey. Attempts have also been made on male honeybee pupae, the eggs of Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae), the eggs of Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae), artificial Trichogramma pupae, a mix of sucrose and pig liver, and meridic diets, etc. Among them, the nutritive value of male honeybee pupae was the highest, which had no adverse effect on larval growth and development and on adult C. septempunctata. Artificial Trichogramma pupae can meet the growth and development of larvae but have effects on the fertility of an adult. But, it could be served as an alternative supplement when natural prey is insufficient. Niijima et al. (1977) originally developed a synthetic diet containing 18 amino acids (60%), 6 inorganic salts (6.9%), sucrose (32.5%), cholesterol (0.5%), and 10 vitamins (0.1%) to feed adult ladybeetles, and following chemically defined diets were generally proven to influence the production of ladybeetles [73]. Moreover, factory production of H. axyridis can also be realized based on the industrial production of S. exigua larvae [74].
Ladybeetles are selected for release as eggs, larvae, and adults. The egg card release is convenient but highly affected by weather factors. The dispersal ability of larvae is small, which is conducive to the rapid establishment of population in the field. However, the resistance of the larvae is poor, and the larvae are not tolerant to long-distance transport. When the density of M. persicae was the same, both adults of C. septempunctata and H. axyridis had the largest predation [75]. Therefore, in view of the spread of adult beetles, one third of the hind wings of ladybeetles are subtracted and released after sunset on calm and sunny days in China. Next, whichever ratio of ladybugs is released, the control effect of M. persicae comes slower than pesticide, usually reaching an 80% control effect after 5 to 10 days. But, the ladybeetles have stronger persistence than pesticide [76,77].
Ladybeetles can also work with A. gifuensis to control aphids. Studies have shown that parasitoid and predatory natural enemies can complement each other to enhance predation efficiency and persistence. The joint release of H. axyridis and A. gifuensis demonstrated a significant synergistic effect on the control of M. persicae through intra-group predation [78]. A similar improved suppression of B. tabaci was found with the combination of Eretmocerus eremicus (Mercet) (Hymenoptera: Aphelinidae) and Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae) [79]. This suggests that a higher level of biodiversity among enemies could potentially result in a more effective pest suppression, especially when the natural enemies occupy diverse and complementary feeding niches [80]. However, the optimal proportion and technique for joint release require further investigation. Additionally, we should pay more attention to the observation that an overall increase in prey community richness could lead to trophic complexity, potentially influencing the overall suppression effectiveness [80].

3.3.2. Reduviid-Based Biocontrol (Sphedanolestes impressicollis and Harpactor fuscipes)

Reduviids (Sphedanolestes impressicollis (Stål) (Hemiptera: Reduviidae) and Harpactor fuscipes (Fabricius) (Hemiptera: Reduviidae)) are versatile predators that can feed on over 44 insect pests of economic significance [81,82]. Unlike other predacious hemipterans, they have a wider prey range and consume more prey to sustain their larger body size [81]. An overbroad diet may deprive it of the advantages used to hunt specific pests. However, in the presence of multiple pests, they can be very valuable predators. The biocontrol potential of predatory insects such as reduviids must be assessed under controlled conditions, which will form the baseline for their utilization in natural field conditions. The biocontrol potential of reduviids must be evaluated under controlled conditions, which will set the stage for their use in the natural field conditions [83].
Hence, multiple experiments were conducted on the predation function, search effect, self-density interference response, and dispersal ability of S. impressicollis and H. fuscipes. Field experiments revealed that both reduviids prey on H. armigera, S. litura, or M. persicae. The Y-tube was used to study the selectivity and selection preference of H. fuscipes for the aforementioned prey species. The result showed that H. fuscipes preferred to select the third-instar larvae of S. litura [84]. In addition, prey densities increased the predation capacity of H. fuscipes and S. impressicollis, while negatively interfering with their search efficiency [85]. Another study showed that the fifth-instar nymphs and adults of H. fuscipes, which have a strong dispersal ability, are not ideal for releasing time [86]. These findings provide important guidance for the widespread application in tobacco production in China.

4. Conclusions

The current artificial mass-rearing procedures of A. gifuensis are relatively cumbersome, especially in the host plant cultivation and M. persicae propagation steps, which significantly slow down the breeding speed. The same applies to natural predators. Therefore, the development of applicable artificial media is of particular importance. This artificial diet could extend beyond aphids and predators and could be used to provide the nutritional needs of A. gifuensis directly with artificial aphids while maintaining or even increasing survival, eclosion, and parasitic rates. If artificial materials were available, the entire large-scale reproduction process could be significantly optimized, and the disadvantages of traditional reproduction methods—such as complicated processes, large space occupation, and high costs—could be resolved.
Through studying biocontrol cases, it becomes apparent that there is a need to increase the abundance of available commercial natural enemies. While commercial explorations are primarily focused on controlling aphids, other pests such as lepidopterans also cause significant damage. However, the development and application of corresponding natural enemies for these pests, as well as other potential candidates, like E. formosa against B. tabaci and predatory mites against thrips, is relatively lacking. Additionally, further work is needed to quantify the advantages inherent in mechanizing mass-rearing systems.
Moreover, it remains uncertain whether the over-reliance on a few particular natural enemy species could have negative environmental impacts. Despite the lack of addressed potential risks associated with the widespread mass release of natural enemies in China, the continuous manual intervention over the years calls for increased awareness of the risks, such as the superseding of native natural enemy species [16,87]. Therefore, to enhance the quality control of commercial natural enemy releases, environmental monitoring should be incorporated into the routine supervision of mass-rearing production and field application policies.
Finally, the decision regarding the production, importation, and release of biological control agents is a national matter and involves multiple authorities. The National Plant Protection Organization, responsible for implementing the guidelines outlined in the International Plant Protection Convention, oversees this process. Through advancements in homogeneous density, enemy breeding technology, automation, storage, packaging, and release techniques, a technical system was established to stabilize the production of natural enemies. Moving forward, industry standards must be established to clarify product quality indexes, inspection methods, and classification standards in order to create a healthy and sustainable application system for the natural-enemy-based biocontrol of tobacco arthropod pests. The industry is also actively promoting the implementation of biological control, especially the natural-enemy-based biocontrol and providing extensive services to farmers.
Natural-enemy-based biocontrol offers numerous advantages, including safety for humans, animals, and plants, as well as no pollution to the environment and easy development with abundant natural resources. Although, from this study, we can also see some of the drawbacks of natural enemy control, such as its slow effect, reliance on complex artificial breeding technology, limitations imposed by natural conditions, and issues with practical application. However, these limitations can be mitigated by integrating other control measures. It is worth noting that the advancement of plant genetic engineering technology has greatly facilitated the development of efficient insect-resistant crop varieties. Insecticidal Bt endotoxins have been successfully incorporated into transgenic varieties of eggplant, maize, potato, soybean, tomato, and rice, demonstrating remarkable effectiveness in insect control [88]. Nevertheless, it is essential to emphasize the necessity for long-term and systematic scientific research, along with continuous follow-up evaluations to assess the impact of insect-resistant crops on predator insects. Such evaluations are crucial for ensuring the sustainability and effectiveness of biocontrol strategies in the context of integrated pest management.
In general, the widespread use of natural enemies as a means of augmentative application has proven to be an effective way of reducing the reliance on pesticides and meeting the growing demand for sustainable agriculture and safer food. However, in comparison to pesticides, which offer a more immediate solution, the practical application of natural enemies among farmers needs to be improved. To remain competitive with other protection methods such as pesticides, the natural-enemy-based biocontrol methods used in China’s agricultural industry must continue to evolve, particularly by expanding the range of targeted pests, increasing the diversity and efficiency of native natural enemies, and combining natural enemy biocontrol agents with other pest management methods to achieve additive control effects. In the future, the key to controlling arthropod pests in China’s agricultural fields will be to integrate and optimize multiple management measures based on the local ecological environment, the types of pests present, and their occurrence patterns, while also reducing the cost of natural-enemy-based biocontrol.

Funding

This work was supported by Major Special Projects for Green Pest Control (110202001035 (LS-04), 110202201017 (LS-01)), Major Special Projects for Big Data (110202201051 (SJ-01)), and the Central Public-interest Scientific Institution Basal Research Fund (No. 1610232023027).

Data Availability Statement

Data openly available in the public repository.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. Common arthropod pest species in tobacco field in China.
Table 1. Common arthropod pest species in tobacco field in China.
SpeciesDamage PartsHazardous Degree *
Lepidoptera
Helicoverpa assultaleaf, bud, flower, fruitH
Heliothis armigeraleaf, bud, flower, fruitH
Spodoptera lituraleaf, budH
Mamestra brassicaeleafL
Spodoptera exigualeafL
Mythimna separataleafL
Agrotis ipsilonstem, leafH
Agrotis tokionisstem, leafL
Agrotis segetumstem, leafL
Phthorimaea operculellaleafM
Scrobipalpa heliopastem, leafL
Peridroma saucialeafL
Hemiptera
† Bemisia tabacileafH
† Myzus persicaestem, leaf, bud, flowerH
Trialeurodes vaporariorumleafL
Cyrtopeltis teniusleafL
Nezara viridulaleaf, stemL
Dolycoris baccarumleaf, stem, fruit L
Coleoptera
Pleonomus canaliculatusroot, stemL
Agriotes fuscicollisroot, stemL
Opatrum subaratumroot, stem, leafL
Maladera formosaeleaf, rootL
Maladera orientalisleaf, rootL
Holotrichia oblitaroot, stem, leafL
Holotrichia parallelaroot, stem, leafL
Anomala corpulentaroot, stem, leafL
Popillia quadriguttataroot, stem, leafL
Henosepilachua vigintioctopunctataleafL
Orthoptera
Gryllotalpa orientalisseed, root, stemL
Gryllotalpa unispinaseed, root, stemL
Thysanoptera
Thrips flavidulusleaf, flowerL
† Frankliniella occidentalisstem, leaf, flower, fruitM
Thrips tabacileaf, flowerM
Mollusca
Agriolimax agrestisleafL
† vectors of virus transmission; * hazardous degree: classification of hazardous degree according to annual yield loss caused by pests. H: high, M: medium, and L: low; information was adopted from Wang et al. (2018) [5].
Table
Table 2. Natural enemy species against tobacco arthropod pests.
Table 2. Natural enemy species against tobacco arthropod pests.
OrderSpeciesTarget Pests
Predators
ArachnidaAmblyseius cucumerismites and thrips
Amblyseius mckenziei
Neoseiulus barkeri
ColeopteraCoccinella septempunctataaphids and whiteflies
Harmonia axyridis
Propylea japonica
Adonia variegata
Pheropsophus javanuslepidopterans
Microcosmodes flavospilosus
Cylindera kaleea
Cicindela aurulenta
DipteraEupeodes corollaeaphids
Episyrphus balteatus
Sphaerophoria scripta
Melanostoma scalare
Aphidoletes aphidimyza
Atylotus bivittateinuslepidopterans
HemipteraArma chinensislepidopterans, hemipterans, homopterans, etc.
Rhynocoris fuscipes
Eocanthecona furcellata
Orius sauteri
Harpactor fuscipes
Sphedanolestes impressicollis
MantodeaTenodera sinensislepidopterans
Hierodula patellifera
NeuroperaChrysopa pallensaphids, stinkbugs, lepidopterans
Chrysoperla nipponensis
Chrysopa formosa
Parasites
HymenopteraAphidius gifuensisaphids
Diaeretiella rapae
Habrobracon hebetorlepidopterans (Store-product pest)
Encarsia formosawhiteflies
Campoletis chlorideaelepidopterans
Table
Table 3. The reference standard of the quantity of released Aphidius gifuensis based on the occurrence degree of Myzus persicae.
Table 3. The reference standard of the quantity of released Aphidius gifuensis based on the occurrence degree of Myzus persicae.
Number of M. persicae per PlantThe Quantity of Released A. gifuensis per HectareThe Release Mode
1–53000–7500dot scope a
6–207500–15,000planar scope b
21–3015,000–18,000regional scale c
a A. gifuensis was released from the M. persicae-infected plants. b A. gifuensis was released to the parcel of field found with M. persicae. c A. gifuensis was released to the region found with M. persicae.
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Xue, W.; Xu, P.; Wang, X.; Ren, G.; Wang, X. Natural-Enemy-Based Biocontrol of Tobacco Arthropod Pests in China. Agronomy 2023, 13, 1972. https://doi.org/10.3390/agronomy13081972

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Xue W, Xu P, Wang X, Ren G, Wang X. Natural-Enemy-Based Biocontrol of Tobacco Arthropod Pests in China. Agronomy. 2023; 13(8):1972. https://doi.org/10.3390/agronomy13081972

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Xue, Wenxin, Pengjun Xu, Xiufang Wang, Guangwei Ren, and Xinwei Wang. 2023. "Natural-Enemy-Based Biocontrol of Tobacco Arthropod Pests in China" Agronomy 13, no. 8: 1972. https://doi.org/10.3390/agronomy13081972

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