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Review

A Review of Prospective Biocontrol Agents and Sustainable Soil Practices for Bulb Mite (Acari: Acaridae) Management

by
Eric Palevsky
1,
Jana Konopická
2,
Diana Rueda-Ramírez
3 and
Rostislav Zemek
2,*
1
Newe-Ya’ar Research Center, Agricultural Research Organization, Department of Entomology, P.O. Box 1021, Ramat Yishay 3009500, Israel
2
Biology Centre, Czech Academy of Sciences, Institute of Entomology, Branišovská 31, 370 05 České Budějovice, Czech Republic
3
Institute of Biology, Ecology, Humboldt-Universität zu Berlin, 10115 Berlin, Germany
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(7), 1491; https://doi.org/10.3390/agronomy12071491
Submission received: 30 April 2022 / Revised: 30 May 2022 / Accepted: 20 June 2022 / Published: 22 June 2022
(This article belongs to the Special Issue Soil Management: Implications for Pest and Disease Control)
Browse Figure
Review Reports Versions Notes

Abstract

:
Mites of the genus Rhizoglyphus (Acari: Acaridae) are serious pests of plants belonging to the orders Liliales and Asparagales such as onions, garlic, lilies, and tulips. Their control by synthetic pesticides is becoming problematic as a result of resistance development in these mites and environmental and health issues. New pest control methods thus need to be developed. This review provides an overview of studies related to bulb mite management. Entomopathogenic fungi and generalist predatory mites are prospective agents for biological control of these pests while entomopathogenic nematodes and the metabolites of their symbiotic bacteria seems to be less effective. There are, however, many more organisms in the soil that might play important roles in biological control of bulb mites as well as other soil pests of these bulbous plants. Therefore, a holistic approach based on the understanding of food webs in the soil environment and their ecological services is essential for developing effective control of bulb mites. For the rehabilitation and conservation of soil biodiversity supporting these ecosystem services, emphasis must be placed on sustainable soil management (e.g., ensuring green coverage, minimal soil disturbance and high content of organic matter).

1. Introduction

Many bulbous plants belonging to the orders Liliales and Asparagales are cultivated throughout the world for food, their therapeutic and medicinal properties, or for ornamental purposes [1,2,3,4]. Some plants are also used in plant protection, mostly as botanical insecticides [5,6,7,8,9]. The most important bulb crops are onion (Allium cepa L.) and garlic (Allium sativum L.) with the total world production estimated in 2020 to be 109,007,186 and 28,054,318 tonnes, respectively [10]. Both onion and garlic are attacked by many pathogens and pests causing considerable losses in yield [1,11]. Fusarium basal rot, Botrytis leaf blight, onion smut, downy mildew, pink root and neck rot are some of the most serious diseases, while bulb mites, onion maggot, and thrips are the most serious arthropod pests [12,13,14].
Bulb mites of the genus Rhizoglyphus (Acari: Acaridae) are economically important soil-dwelling pests of bulbous plants that often attack other important crops such as potatoes and carrots [15]. Among many Rhizoglyphus species around the world [16,17], Rhizoglyphus robini (Claparède) is considered one of the most serious pests of onion, garlic and ornamental plants such as tulips, lilies and hyacinths cultivated in greenhouses and open fields, and is also a pest of stored bulbs [15,16]. The mites cause both direct damage by feeding and indirect damage by facilitating entry of plant pathogen into attacked host plants, and by vectoring phytopathogenic bacteria and fungi such as Fusarium oxysporum Schltdl. (Hypocreales: Nectriaceae) to other plants [14,15,18,19,20,21].
The objective of this paper is to review current knowledge of bulb mite control strategies, including an overview of various biocontrol agents, a holistic approach to onion and garlic pests, as well as the role that soil management can play in conservation biological control.

2. Bulb Mite Management Using Synthetic Pesticides

The control of bulb mites has been based almost entirely on pesticides [15]. Among 35 compounds tested against Rhizoglyphus echinopus (Fumouze and Robin), the highest toxicity was exhibited by cyclodiene GABA antagonists (dieldrin, endrin and aldrin), some organophosphate (chlorpyrifos, diazinon and azinphosethyl) and carbamate (carbofuran) anticholinesterases and a thiazolidine flubenzimine [22]. Oxythioquinox, fenazaflor, fenazaquin and amitraz were less toxic than the cyclodienes, organophosphates and carbamates [22]. However, bulb mites can quickly develop resistance to synthetic pesticides [15,23,24,25] and many of these pesticides are toxic to the environment, having negative impacts on non-target soil-dwelling organisms (e.g., earthworms and microorganisms) and leaving residues in food crops and contaminating groundwater. For these reasons, usage of broad-spectrum pesticides has been limited or completely banned by the European community [26]. Thus, alternative, environmentally safe control strategies need to be developed and implemented for crop protection against bulb mites [12,15,27].

3. Biological Control of Bulb Mites

Efforts to develop biological control programs for bulb mites have taken place in a number of countries. Several biocontrol agents have been tested against Rhizoglyphus spp. under laboratory and some also under field conditions (Table 1). The most promising results have been obtained with acaropathogenic/entomopathogenic fungi and predatory mites as described below. Other possible prospective control agents attacking mites are viruses, bacteria, and protista [28], but except for some bacteria (Table 1) their efficacy against bulb mites has not been investigated yet.
Besides the above mentioned natural enemies, other beneficial microorganisms such as mycoparasitic fungi and antagonistic soil bacteria are suitable companions for reducing secondary damage caused by dissemination of phytopathogenic bacteria and fungi [48,49,50,51,52] but this is beyond the scope of this review.

3.1. Bacteria

The soil bacterium Bacillus thuringiensis Berliner has been proven to be effective against some mite pests [53,54]. To our knowledge, there are only two reports on the efficacy of this biocontrol agent or its toxins against bulb mites. The study by Carter et al. [29], did not find any significant effect of B. thuringiensis Cry3Aa and Cry3Bb1 coleopteran-active delta-endotoxins on R. robini. On the other hand, a recent (2020) Chinese patent [30] claims genetically modified B. thuringiensis to be highly efficient for Rhizoglyphus spp. control with the example of R. echinopus where its population was reduced by 93.2%.
Nermuť et al. [31] investigated whether metabolites of nematode symbiotic bacteria of the genus Xenorhabdus sp. or Photorhabdus sp. (Table 1) could be suitable for R. robini control. Mortality of mites treated by culture supernatants of these bacteria varied considerably among Xenorhabdus species and strains. The most effective were strains of X. doucetiae, X. bovienii, X. griffiniae and an unidentified Xenorhabdus sp., causing mortality between 10% to almost 30%. Despite the low mortality, some bacterial strains had a repellent effect on mites [31].

3.2. Acaropathogenic and Entomopathogenic Fungi

Acaropathogenic (APFs) and entomopathogenic fungi (EPFs) are common in nature, have a cosmopolitan distribution and cause natural epizootics in populations of insects, mites or other arthropods [55,56]. Fungal pathogens are a permanent component of mite natural habitats [57]. The advantage of EPFs, in contrast to other biocontrol agents, is that most of them are able to persist in soils for months or even years, in the absence of arthropod hosts [58,59,60]. A recent (2022) study by Konopická et al. [61] evaluated species richness and density of these fungi in soil samples collected in onion and garlic fields. EPFs Beauveria spp., Cordyceps spp., Lecanicillium spp., Metarhizium spp. and Purpureocillium spp. were isolated. The highest density was observed in the genus Metarhizium in which the average density of colony forming units (CFU) per 1 mL of soil sample reached 1.47 × 104 while the lowest density was observed in the genus Beauveria. Interestingly, soils in the Czech Republic contained about ten times higher number of EPFs compared to Israel [61].
Besides Acari-specific pathogens such as Hirsutella thompsonii (Fisher) and Neozygites spp. (Entomophthorales), ‘nonspecialist’ mitosporic fungi (Hyphomycetes) such as Beauveria bassiana (Bals.-Criv.) Vuill., Metarhizium anisopliae (Metsch.) Sorokin, Cordyceps fumosorosea (Wize) Kepler, B. Shrestha and Spatafora (formerly Isaria fumosorosea), Cordyceps farinosa (Holmsk.) Kepler, B. Shrestha and Spatafora (formerly Isaria farinosa), and Lecanicillium lecanii (Zimm.) Zare and W. Gams have potential to control some mite species [28,32,34,62].
Soil is considered to be a very favorable environment for EPFs application due to the high humidity conditions necessary for spore germination and host infection. On the other hand, soil-inhabiting bulb mites might have evolved at least to some extent resistance to EPFs. Indeed, a compound named hexyl rhizoglyphinate found in R. robini cuticle was shown to possess antifungal activity [63]. The role of other compounds, such as the monoterpenoids robinal [64] and isorobinal [65] in adaptation of bulb mites to live next to some acaro/entomopathogenic fungi in soil environments remains to be explored.
To our knowledge, only four studies have tested whether APFs or EPFs are effective in controlling bulb mites under laboratory or greenhouse conditions [32,33,34,35]. Sztejnberg et al. [35] reported no pathogenicity of an isolate of Hirsutella kirchneri (Rostrup) Minter, Brady and Hall, obtained from the cereal rust mite, Abacarus hystrix Nalepa (original accession number CMI 257456) against R. robini, despite several procedures attempted for mite infection (spraying, dipping, tipping fungal cultures over hosts).
Konopická et al. [32] evaluated the effecacy of 17 isolated and 3 reference strains of EPFs against R. robini females. Results revealed high variability in R. robini mortality among EPF species and strains. The highest efficacy against R. robini mites was found in the strain of M. anisopliae isolated from soil samples collected in the Czech Republic which caused mortality up to 99.3%, and strain of Metarhizium indigoticum (Kobayasi and Shimizu) Kepler, S.A. Rehner and Humber from Israel causing 98.3% mortality, four days from spray application. The concentration-response models indicated that the latter strain was more virulent than M. anisopliae strains. The median lethal concentration (LC50) in M. indigoticum strain was estimated as 1.01 × 104. Cordyceps fumosorosea strains did not cause mortality higher than 40%. The lowest virulence was then found in Beauveria spp. strains causing mortality of mites between 5 and 25%.
Another recent (2020) study by Ment et al. [34] demonstrated high efficacy of Metarhizium brunneum Petch (isolate Mb7) against R. robini, which was susceptible to directly applied Mb7 conidia. Conidia of this fungus applied in vitro at concetration 1 × 107 caused 43% and 100% mortality of mites at three- and seven-days post inoculation, respectively and the estimated LT50 value was 4.3 days. Drench application in potted onion experiments also significantly reduced bulb mite populations compared to the untreated control.
The fungus Metarhizium spp. was also effective against R. robini in the study by Ko et al. [33]. In total, 11 isolates were selected for further study through a re-evaluation of the pathogenicity of the isolates. Conidial suspension with a concentration 1 × 107 conidia/mL of fungi Metarhizium pinghaense Q.T. Chen and H.L. Guo (isolate 3–1–2) and M. anisopliae (isolates 3–2–2 and 4–18–3) caused more than 80% mortality after 7 days. An isolate of Metarhizium pemphigi (Driver and R.J. Milner) Kepler, S.A. Rehner and Humber (isolate 1–1–1) and two isolates of M. anisopliae (isolates 4–3–2 and 4–31–2) showed mortality of 90% or more on the fifth day and 100% mortality after seven days.

3.3. Entomopathogenic Nematodes

Nematodes are not common parasites of mites but some mite-parasitic species are known. For example several allantonematid nematodes use mites as definitive hosts [28]. Usually the host is not killed but is slowly sterilised. Since these obligate parasites have not been raised on artificial media, their usefulness as biological control agents is limited. Mites can also serve as intermediate hosts of nematode parasites of vertebrates [28].
On the other hand, entomopathogenic nematodes (EPNs) belonging to families Steinernematidae and Heterorhabditidae can be produced in large scale with some species commercially available and successfully applied against many pests [66,67,68,69]. The only study that has explored the potential of entomopathogenic nematodes to infect bulb mites, specifically R. robini, was published in 2019 [31]. In this study, the bulb mites were exposed to the infective juveniles of 20 strains of Steinernema and Heterorhabditis species applied at a dose of 300 infective juveniles per mite, and the invasion rate and mite mortality were assessed. The results showed that some EPNs, especially those with small body diameter, are able to invade and kill adult females of R. robini. The most promising species were Steinernema huense Phan, Mráček, Půža, Nermuť and Jarošová, Heterorhabditis bacteriophora Poinar and Heterorhabditis amazonensis Andaló, Nguyen and Moino, which caused mortality in R. robini up to 30%. The authors concluded that although some EPN species are able to invade and kill bulb mites, their efficacy is in general quite low and they do not seem to represent a viable option for bulb mite biocontrol as a standalone approach [31]. EPNs have, however, other important functions in soil as they can disseminate fungal spores [70], serve as prey for invertebrate predators including mites and springtails or as a host for nematode-trapping fungi, such as Orbilia oligospora (Fresen.) Baral and E. Weber, Monacrosporium eudermatum (Drechsler) Subram. and Geniculifera paucispora (R.C. Cooke) Rifai [71].

3.4. Predatory Mites

Biological control programs for bulb mites have focused on using predatory mitesmainly in the family Laelapidae (Table 1), which feed on soil-dwelling pests [40]. Studies prior to 1990 were limited to examination of predator behavior and their ability to feed and reproduce on a diet of bulb mites. Zedan [42] reported that protonymphs, deutonymphs, and adults of Gaeolaelaps aculeifer (Canestrini) feed and developed on all stages of R. echinopus. Reproductive potential of the predator was highest when it fed on adult prey, but fewer prey was consumed. Ragusa and Zedan [43] examined interactions between these two species collected from local populations in Italy, and found that both immature and adult G. aculeifer preferred to feed on immature rather than adult R. echinopus. In contrast to Zedan [42], reproductive potential was highest when predators fed on a diet of eggs and immatures of R. echinopus.
In a preliminary study to find potential predators of R. robini, Lesna et al. [39] demonstrated that contrary to Stratiolaelaps miles (Berlese), G. aculeifer was able to feed and reproduce on a diet of R. robini. The authors also showed that local populations of G. aculeifer often differ in their feeding preference and reproductive potential and suggested that it may be advantageous to exploit these ‘local’ strains as biological control agents. In the follow-up study [41] the authors showed significant suppression of R. robini abundance by G. aculeifer on lilies under constant laboratory conditions and in a large-scale experiment carried out from February to June in storage rooms. Control of the pest was affected by both the spatial scale and the structural complexity of the habitat, with bulb mite populations declining faster in less complex and smaller habitats. In a greenhouse experiment using intact bulbs grown in peat soil, Lesna et al. [45] reported the elimination of bulb mites when the predator:prey ratio was 3:1.
Other Mesostigmata have also been reported feeding on R. echinopus [37,40,47] and R. robini [36,38,39]. Wu et al. [37] reported that an unidentified species of Lasioseius (Blattisociidae) developed and reproduced by feeding on R. echinopus. Castilho et al. [47] demonstrated that Protogamasellopsis zaheri Abo-Shnaf, Castilho and Moraes (mentioned as Protogamasellopsis posnaniensis Wisniewski and Hirschmann) (Rhodacaridae) fed on R. echinopus and reproduced. Moreira and Moraes [40] observed that Cosmolaelaps barbatus Moreira, Klompen and Moraes and Cosmolaelaps jaboticabalensis Moreira, Klompen and Moraes (Laelapidae) oviposited when fed R. echinopus. Azevedo et al. [46] observed that Macrocheles embersoni Azevedo, Berto and Castilho, Macrocheles muscaedomesticae (Scopoli) and Macrocheles robustulus (Berlese) (Macrochelidae) were able to consume R. echinopus, but with a very low consumption compared to other prey. In the case of R. echinopus, Afifi et al. [36] observed the development and reproduction of Protogamasellus minutus Nasr (Ascidae) when fed with this prey. Also, Lesna et al. [39] reported that Lasioseius allii Chant (mentioned as Lasioseius bispinosus Evans) (Blattisociidae) and Parasitus fimetorum (Berlese) (Parasitidae) were successfully reared on R. robini, and the latter was able to suppress the prey when peat was used as substrate. Mowafi [38] observed the development and reproduction of Lasioseius africanus Nasr (Blattisociidae) feeding on R. robini. However, all of these studies were conducted in the laboratory and only in the case of P. fimetorum were small-scale population experiments conducted in closed flasks. Further studies are needed to explore the potential of these species as biocontrol agents in potted plant and field trials.

4. The Importance of a Holistic Approach for Better Pest Management

Many pest management programs for bulb mite control fail to consider the complex web of interactions in the soil that can be disrupted by applying these strategies. For example, soil solarization can be effective against R. robini [72], but it can also be detrimental to important bio-control agents such as soil-dwelling Mesostigmata [73], which play an important role in controlling populations of organisms, including several pests. Although Mesostigmata are recognized as important soil bio-control agents, they are only part of a food web that functions efficiently in natural ecosystems. It is important to consider that in agroecosystems where Rhizoglyphus spp. populations cause damage, there are also other organisms in this food web (Figure 1) that may be positively or negatively affected by the strategies used. The establishment of agro-ecosystems and their management can reduce the diversity of organisms in the soil, affecting interactions and, in this way, favoring the increase of certain populations that can cause significant damage to plants, as some Rhizoglyphus species, and the reduction of others with regulatory effects.
Although the effect of re-establishing soil biodiversity has not been explored on Rhizoglyphus spp. populations, it has been observed that the use of conservation strategies such as organic mulching can increase soil diversity and ultimately decrease populations of other pest organisms or their negative effect on crop plants. In several cases, the use of organic amendments has been shown to reduce populations of organisms considered to be pests such as phytoparasitic nematodes (e.g., [74,75,76,77,78]), and phytophagous mites (e.g., [79]), as well as damage by some phytophagous insects (e.g., [80]), and the increase of organisms considered beneficial such as free-living nematodes (e.g., [74,76,78,80]) and predatory mites (e.g., [74,75,79]). At laboratory level and on a small scale, it has been shown that, for some organisms such as some predatory mite species, the addition of alternative such as free-living nematodes can enhance their survival and reproduction and, in turn, their densities [81,82,83], which would be reflected in an increase in the control of phytophagous organisms [82,83]. Thus, increasing diversity in the soil, which also includes alternative prey, can favor the increase and permanence of biological control agents. While the use of organic amendments is only one of the techniques explored, the central strategy is to take advantage of local diversity and restore soil food webs so that population control and soil processes occur as in natural ecosystems.

5. Potential Role of Soil Management on Rhizoglyphus Control in Conventional and Organic Systems in Garlic and Onion

Although bulb mites are recognized as key pests, no agro-chemicals are registered for its control in the USA during the growing season [84,85,86], nor are there any known biocontrol agents reported from intensively managed agro-system [87]. The latter may be attributed to several factors including conventional tillage prior to each crop, lack of organic matter, and negative impacts of pesticides [88]. Cover crops or soil solarization are generally not applied in conventional management as there is too little time between crop rotations. In fields with previous bulb mite problems, soil fumigants containing metam sodium are still recommended as a pre-plant treatment [89], but are used limitedly due to high cost [87] and potential negative environmental impact [90]. California produces approximately 90% of all commercially grown garlic in the U.S., mostly (over 92%) grown conventionally on bare soil as a monoculture in large plots. While a four-year rotation out of garlic/onions is generally practiced, conventional management is still highly dependent on pesticides for disease, insect, nematode and weed control, with resistance being a major problem, as few chemicals are registered [87].
In contrast to conventional management described above, in organically produced onion and garlic in the USA, cover cropping combined with crop rotation are used as a strategy for soil fertility and pest management, with only marginal use of certified organic pesticides [91,92,93]. While soil sterilization techniques, both solar and chemical, are known to reduce pest pressure as cited above for R. robini, they also can negatively impact beneficial microbiota in the soil food web such as those responsible for suppression of soil pathogens [94]. Similarly, weed control by sterilization has its drawbacks as it exposes the soil to erosion and extreme temperatures, reduces water retention and contributes to the continuous depletion of soil organic matter. Minimal tillage coupled with permanent organic cover are the most effective agriculture management practices for reducing soil erosion [95,96]. Mix cover crops, recently named ‘service crops’, as they are meant to provide ecosystems services, are incorporated into the crop rotation for weed suppression and species diversification. Service crops regulate soil moisture and temperature, enhance organic matter and soil structure, paving the way for the rehabilitation of beneficial microbiota and mesofauna (including mites and nematodes) in agricultural soils [95,97,98,99]. Free living nematodes (FLN) are known to move to bacterial and fungi hotspots [100], attracted by volatiles released from the microbiota community developing on organic matter. FLN use the microbiota as a food source, but apart from this, FLN may disperse bacteria and fungi [101]. They bring a complex of associated microbes to the decomposing substrate, and thereby may influence community dynamics of soil microbiota [102], including plant growth promoting bacteria. Predatory mites and FLN cannot dig through the soil, but need to move freely in the soil to search for food and feed [103]. This movement can be impaired in agricultural soils that are often compact, lacking suitable levels of aeration and moisture to support these beneficial species. It is interesting to note that bulb mites, despite their relatively large size, are very able to reach their host plants, possibly due to their unsclerotized body, allowing them to squeeze through tight spaces and their ability to sense plants infested with the plant pathogen Fusarium oxysporum [14]. Implementing the three FAO conservation agriculture (CA) principles [104]; minimum mechanical soil disturbance, permanent soil organic cover and species diversification are steps that conventional agriculture needs to take to rebuild soil organic matter, structure and a healthy soil food web. Future research will determine how this holistic soil management approach will support the conservation biological control of bulb mites.

6. Conclusions

Bulb mites are serious pests of many crops and have proven to be difficult to control. This review summarizes knowledge on various approaches of alternative, non-chemical, control of bulb mites. Many studies, mostly laboratory or small scale experiments were conducted to evaluate efficacy of natural enemies. Among them, predatory mites and some strains of EPFs, especially from the genus Metarhizium, could be prospective biocontrol agents. EPNs and the metabolites of their symbiotic bacteria seems to be less promising. Soil health, however, is based on many other organisms such as FLN, mycoparasitic fungi, bacteria etc. and understanding their interactions and factors affecting their biodiversity are very important. Further studies are needed, especially potted plant and field studies, to assess the effects of soil management practices on the conservation and efficacy of soil biocontrol agents for the development of better and sustainable methods of bulb mites control in the future.

Author Contributions

Conceptualization, E.P.; writing—original draft preparation, J.K., E.P., D.R.-R. and R.Z.; writing—review and editing, J.K., E.P., D.R.-R. and R.Z; illustration, D.R.-R.; funding acquisition, R.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Czech Academy of Sciences (RVO: 60077344). The APC was funded by the Technology Agency of the Czech Republic (project GAMA 2 No. TP01010022).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

To DFG Deutsche Forschungsgemeinschaft and Humboldt Universität zu Berlin (HU), Ecology group, for the support to D.R-R. E.P.’s contribution to this manuscript was inspired by DFG grant number RU 780/20-1 ‘Harnessing the soil food web for the biological control of root-knot nematodes’.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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Agronomy 12 01491 g001 550
Figure 1. Schematic representation of some organisms (in part or in their entire life cycle) composing the soil food web associated with bulb crops. In such soils, complex interactions occur between bacteriophages, decomposers, fungivores, microbial grazers, parasites, phytophages, predators, saprophytes, among others. Key to food web diagram: (1) bulbous plant, (2) onion fly (e.g., Delia antiqua (Meigen)), (3) Thysanoptera (e.g., Thrips tabaci Lindeman), (4) fly pupa, (5) pupa and prepupa of Thysanoptera, (6) bulb mite (e.g., Rhizoglyphus robini Claparède), (7) plant parasitic nematodes, (8) fungi, (9) and (10) bacteria, (11) bacteriophagous nematodes, (12) fungivorous nematodes, (13) predatory nematodes, (14) predatory Prostigmata mites, (15) predatory Mesostigmata mites, (16) entomopathogenic nematode. Illustration: Diana Rueda-Ramírez.
Figure 1. Schematic representation of some organisms (in part or in their entire life cycle) composing the soil food web associated with bulb crops. In such soils, complex interactions occur between bacteriophages, decomposers, fungivores, microbial grazers, parasites, phytophages, predators, saprophytes, among others. Key to food web diagram: (1) bulbous plant, (2) onion fly (e.g., Delia antiqua (Meigen)), (3) Thysanoptera (e.g., Thrips tabaci Lindeman), (4) fly pupa, (5) pupa and prepupa of Thysanoptera, (6) bulb mite (e.g., Rhizoglyphus robini Claparède), (7) plant parasitic nematodes, (8) fungi, (9) and (10) bacteria, (11) bacteriophagous nematodes, (12) fungivorous nematodes, (13) predatory nematodes, (14) predatory Prostigmata mites, (15) predatory Mesostigmata mites, (16) entomopathogenic nematode. Illustration: Diana Rueda-Ramírez.
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Table
Table 1. List of biocontrol agents tested for control of bulb mites.
Table 1. List of biocontrol agents tested for control of bulb mites.
GroupFamilySpeciesReferences
BacteriaBacillaceaeBacillus thuringiensis Berliner[29,30]
Morganellaceae *Xenorhabdus bovienii Akhurst and Boemare[31]
Xenorhabdus budapestensis Lengyel et al.
Xenorhabdus cabanillasii Tailliez et al.
Xenorhabdus doucetiae Tailliez et al.
Xenorhabdus griffiniae Tailliez et al.
Xenorhabdus kozodoii Tailliez et al.
Xenorhabdus magdalenensis Tailliez et al.
Xenorhabdus nematophila (Poinar and Thomas) Thomas and Poinar
Xenorhabdus poinarii (Akhurst) Akhurst and Boemare
Xenorhabdus stockiae Tailliez et al.
Xenorhabdus sp.
Photorhabdus sp.
Entomo- pathogenic fungiClavicipitaceaeMetarhizium anisopliae (Metsch.) Sorokin[32,33]
Metarhizium brunneum Petch[34]
Metarhizium indigoticum (Kobayasi and Shimizu) Kepler, S.A. Rehner and Humber[32]
Metarhizium pemphigi (Driver and R.J. Milner) Kepler, S.A. Rehner and Humber[33]
Metarhizium pinghaense Q.T. Chen and H.L. Guo[33]
CordycipitaceaeBeauveria bassiana (Bals.-Criv.) Vuill.[32]
Beauveria brongniartii (Sacc.) Petch[32]
Cordyceps fumosorosea (Wize) Kepler, B. Shrestha and Spatafora[32]
OphiocordycipitaceaeHirsutella kirchneri (Rostrup) Minter, Brady and Hall[35]
Entomo-
pathogenic nematodes		SteinernematidaeSteinernema carpocapsae (Weiser)[31]
Steinernema huense Phan, Mráček, Půža, Nermuť and Jarošová
Steinernema surkhetense Khatri-Chhetri, Waeyenberge, Spiridonov, Manandhar and Moens
Steinernema sp.
HeterorhabditidaeHeterorhabditis amazonensis Andaló, Nguyen and Moino[31]
Heterorhabditis bacteriophora Poinar
Heterorhabditis beicherriana Li, Liu, Nermuť, Půža and Mráček
Heterorhabditis floridensis Nguyen, Gozel, Koppenhöfer and Adams
Heterorhabditis indica Poinar et al.
Heterorhabditis taysearae Shamseldean
Heterorhabditis sp.
Predatory mitesAscidaeProtogamasellus minutus Nasr[36]
BlattisociidaeLasioseius sp.[37]
Lasioseius africanus Nasr[38]
Lasioseius allii Chant (mentioned as Lasioseius bispinosus Evans)[39]
LaelapidaeCosmolaelaps barbatus Moreira, Klompen and Moraes[40]
Cosmolaelaps jaboticabalensis Moreira, Klompen and Moraes[40]
Gaeolaelaps aculeifer (Canestrini)[39,41,42,43,44,45]
Stratiolaelaps miles (Berlese)[39]
MacrochelidaeMacrocheles embersoni Azevedo, Berto and Castilho[46]
Macrocheles muscaedomesticae (Scopoli)[46]
Macrocheles robustulus (Berlese)[46]
ParasitidaeParasitus fimetorum (Berlese)[39]
RhodacaridaeProtogamasellopsis zaheri Abo-Shnaf, Castilho and Moraes (mentioned as Protogamasellopsis posnaniensis Wisniewski and Hirschmann)[47]
* Entomopathogenic nematode-associated bacteria.
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Palevsky, E.; Konopická, J.; Rueda-Ramírez, D.; Zemek, R. A Review of Prospective Biocontrol Agents and Sustainable Soil Practices for Bulb Mite (Acari: Acaridae) Management. Agronomy 2022, 12, 1491. https://doi.org/10.3390/agronomy12071491

AMA Style

Palevsky E, Konopická J, Rueda-Ramírez D, Zemek R. A Review of Prospective Biocontrol Agents and Sustainable Soil Practices for Bulb Mite (Acari: Acaridae) Management. Agronomy. 2022; 12(7):1491. https://doi.org/10.3390/agronomy12071491

Chicago/Turabian Style

Palevsky, Eric, Jana Konopická, Diana Rueda-Ramírez, and Rostislav Zemek. 2022. "A Review of Prospective Biocontrol Agents and Sustainable Soil Practices for Bulb Mite (Acari: Acaridae) Management" Agronomy 12, no. 7: 1491. https://doi.org/10.3390/agronomy12071491

APA Style

Palevsky, E., Konopická, J., Rueda-Ramírez, D., & Zemek, R. (2022). A Review of Prospective Biocontrol Agents and Sustainable Soil Practices for Bulb Mite (Acari: Acaridae) Management. Agronomy, 12(7), 1491. https://doi.org/10.3390/agronomy12071491

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