Next Article in Journal
Identifying the Genetic Distance Threshold for Entiminae (Coleoptera: Curculionidae) Species Delimitation via COI Barcodes
Next Article in Special Issue
Identification and Distribution of Human-Biting Ticks in Northwestern Spain
Previous Article in Journal
Identification and Functional Analysis of Glutathione S-Transferases from Sitophilus zeamais in Olfactory Organ
Previous Article in Special Issue
Mapping the Potential Distribution of Ticks in the Western Kanto Region, Japan: Predictions Based on Land-Use, Climate, and Wildlife
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 13
Issue 3
10.3390/insects13030260
insects-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

A Review of Commercial Metarhizium- and Beauveria-Based Biopesticides for the Biological Control of Ticks in the USA

by
Cheryl Frank Sullivan
*,
Bruce L. Parker
and
Margaret Skinner
Entomology Research Laboratory, University of Vermont, Burlington, VT 05405, USA
*
Author to whom correspondence should be addressed.
Insects 2022, 13(3), 260; https://doi.org/10.3390/insects13030260
Submission received: 4 February 2022 / Revised: 18 February 2022 / Accepted: 2 March 2022 / Published: 5 March 2022
(This article belongs to the Special Issue Ecology of Ticks and Their Control)
Versions Notes

Abstract

:

Simple Summary

Microbial biopesticides containing entomopathogenic fungi have potential in tick management. In this review, we compiled a comprehensive list of the use of commercialized Metarhizium and Beauveria-based biopesticides in the USA that have been tested against ixodid ticks under laboratory and field conditions and when used as a part of integrated tick management. Despite considerable progress in the development of fungal biopesticides over the past 20 years, the establishment of commercial products available for use against ticks continues to be slow. There is a need for the development of sustainable, nonchemical tick management strategies. Until efficacious fungus-based products become more available, tick management will rely primarily on synthetic chemical acaricides, with natural-product acaricides as the alternative.

Abstract

There is a need for the development of sustainable, nonchemical tick management strategies. Mycoacaricide and mycoinsecticide product development worldwide has focused primarily on fungi in the genera Beauveria (Hypocreales: Cordycipitaceae) and Metarhizium (Hypocreales: Clavicipitaceae). Microbial biopesticides containing entomopathogenic fungi have potential in tick management. However, despite considerable progress in the development of fungal biopesticides over the past 20 years, the establishment of commercial products available for use against ticks continues to be slow. We reviewed published scientific literature and compiled a comprehensive list of reports of the effectiveness of commercial biopesticides based on the fungal genera Metarhizium and Beauveria and registered for use in the USA against ixodid ticks under laboratory and field conditions. We also report on results when these biopesticides were used as a part of integrated tick management. Until efficacious fungus-based products become more available, tick management will rely primarily on synthetic chemical acaricides, with natural-product acaricides as the alternative.

1. Introduction

Ticks transmit the greatest diversity of pathogenic organisms of medical and veterinary importance among arthropods affecting the health of humans and domestic and wild animals [1]. Worldwide, they cause billions of dollars in annual losses to the livestock industries and in costs for the diagnosis and treatment of tick-borne illnesses [2,3]. Broadcast applications of acaricides (synthetic, natural-product, or biologically based) is the primary strategy used to reduce the abundance of host-seeking ticks [4]. Synthetic chemical acaricides are the most commonly used, and will continue to be until alternatives with comparable efficacy are found that combat acaricide resistance, particularly in Rhipicephalus spp., satisfy consumer interest in ecologically based products, and reduce nontarget effects on other organisms like pollinators [5,6,7,8,9,10].
Entomopathogenic fungi have greater potential to reduce tick densities compared with other biological control agents like parasitic wasps, pathogenic nematodes, and generalist predators such as birds and beetles [2,10,11,12,13]. Mycoinsecticides and mycoacaricides containing entomopathogenic fungi as the active ingredient can be used to suppress arthropods of economic, medical, and veterinary importance when used as an augmentative biocontrol strategy within an integrated pest (tick) management (IPM/ITM) approach [11,14,15,16,17]. Their development and use has been widely studied, with management success against numerous invasive and native arthropod pests and vectors of disease agents in forest, agricultural, and residential settings since the first documented field attempt using mass-produced fungi in 1888 [18,19,20,21,22]. Globally, and in the USA specifically, commercialization has focused primarily on fungi in the genera Beauveria (Hypocreales: Cordycipitaceae) and Metarhizium (Hypocreales: Clavicipitaceae) [14,16,23].
Mycoacaricide use against ticks is a fairly recent technology in the timeline of biopesticide use, with only two dozen reports worldwide prior to the turn of the 21st century [24]. In 2006, only a few field studies had been carried out in the USA [10,12,13], both targeting the blacklegged tick, Ixodes scapularis (Say) [25,26]. A wide breadth of management techniques has focused on this species with the goal of protecting human health from diseases associated with exposure to pathogens the ticks may harbor, particularly Borrelia burgdorferi sensu stricto, the causal agent of Lyme disease [7,14,27,28]. The most recently compiled worldwide list of mycoinsecticides and mycoacaricides identified three fungus-based products labeled for ticks [14]. Two products were registered in the USA. At the time of writing, both are unavailable on the market. Despite product availability limitations, several tick species of concern have been targeted with commercial formulations in laboratory trials, field settings, and within an ITM approach. Herein, we review published scientific literature and present a comprehensive list of reports of the effectiveness of commercial fungal biopesticides based on the genera Metarhizium and Beauveria, registered for use in the USA, and tested against ixodid ticks. The results that are presented are from reports of product applications or applications of fungal strains that were isolated directly from the products.

2. Metarhizium-Based Formulations

Two isolates of Metarhizium brunneum (Petch), formerly M. anisopliae (Metschnikoff) Sorokin, have been used as the active ingredient in products used against ixodid ticks: strains F52 and ESC1, hereafter referred to as Mb-F52 and Mb-ESC1, respectively [7,14,23]. The most recently available strain, Mb-F52, was first isolated from codling moth (Cydia pomonella) in Austria. The strain has several names globally, including ATCC90448, ARSEF1095, ARSEF7711, Ma43, BIPESCO5, and BIO1020 [29]. It has a wide host range and is commonly used to target thrips (Thysanoptera), vine weevils (Coleoptera), and mites (Acari) in field and greenhouse crop production and ticks in turf/residential lawns, and has few negative impacts on nontarget arthropods when used within label guidelines [29,30,31,32]. From 2008 to 2020, two products were available in the USA for use against ticks under the tradename Met52®, formerly Tick-Ex®, (Novozymes Biological, Franklinton, NC, USA). The formulations consisted of rice-based granules (Met52®G) for broadcast application to turf or incorporation into soil, and an oil-based, emulsifiable concentrate (Met52®EC) for foliar spray or soil drench applications. Over the years, market availability has been inconsistent due to reformulation, rebranding, and market consolidations [14,23,33].
Since 2002, most studies using Mb-F52 and Mb-ESC1 have targeted I. scapularis. (Table 1, Table 2 and Table 3). Formulations can cause mortality in all mobile life stages under laboratory, residential yard, and woodland conditions at a variety of application rates. In the laboratory, application rates ranging from 106–109 conidia/unit volume or area generally cause 70–100% adult and nymph mortality within three to four weeks at 23–25 °C and ~90%RH (Table 1). The fungus has also been tested in combination with the synthetic pesticide permethrin, which did not hinder the ability of the fungus to cause mortality [34]. Product tests in the laboratory on other tick species—Dermacentor albipictus (Packard), Dermacentor reticulatus (Fabricius), Ixodes ricinus (L.), Rhipicephalus sanguineus sensu lato, and Rhipicephalus (Boophilus) microplus (Canestrini)—also demonstrated high mortality under high temperature and humidity conditions (>80%RH) (Table 4). Dermacentor albipictus larvae, a one-host tick that parasitizes ungulates like cattle, horses, and moose [35,36,37] has received the most attention. Although 100% mortality is achievable in vitro after three weeks when immersed or sprayed, broadcast applications of a granular formulation achieved a reduced level of mortality (89%). Under seminatural conditions in the laboratory (containers with sand and a nylon rod for ticks to quest on), mortality for this species was influenced by whether larvae were aggregated in a quiescent state or actively questing, and by the fungal formulation with which they were challenged during their off-host period [38].
With the exception of Amblyomma americanum (L.) [42], field applications of Mb-F52 products focused on suppressing I. scapularis nymphs during their questing period (primarily April–May through August) in the northeastern USA (Table 2 and Table 3). When M. brunneum products were applied in the field alone, mixed results were observed (Table 2). A 10 and 41% knockdown control was observed when using Mb-F52 in a woodland setting [41], and up to 36% control with Mb-ESC1 [34]. One study examined the use of nesting material treated with Mb-ESC1 to target larvae that were infesting mice to reduce nymph abundance on the landscape the following year [39]. Although tick mortality of 75% was reported in treated nests versus 35% in control nests in the laboratory, treatments did not have an impact on nymphal densities or the percentage of nymphs infected with B. burgdorferi; however, when data were standardized with the long-term averages, nymphal densities were significantly lower in localized areas surrounding the treated nest boxes. In contrast, one study reported that spray applications of Mb-F52 resulted in 56 and 85% fewer ticks on lawn and woodland plots, respectively, within one season, whereas in the two previous years, the synthetic chemical pesticide bifenthrin, a pyrethroid, provided 86 and 87% control. The Mb-F52 sprays resulted in an 8.6% risk of an infected tick bite compared to 30% in the controls [44]. Repeat applications of fungal products are needed for sustained tick suppression. One report showed only short-term suppression of I. scapularis nymphs below a suppression threshold set at 90% [42]. Reapplications of Mb-F52 were made every two to three weeks to provide suppression, whereas one early-season application of the chemical pesticide bifenthrin provided 100% suppression. Low residual effectiveness using one application of Mb-F52 (<2 weeks) was also observed in a different study [41].
Integrated tick management uses a combination of strategies such as host reduction/treatments, habitat manipulation, and least-toxic pesticides (i.e., fungal biopesticides) targeting different tick life stages as well as their hosts [17,55,56]. Single interventions to manage ticks are often limited in their time to effectiveness, duration, and efficacy [47]. Because of the complex ecology of ticks and tick-borne diseases, single interventions are likely not enough to provide sustained tick suppression that will reduce the risks of pathogen exposure, while ITM has greater potential to overcome these issues [17]. Fungal biopesticides are commonly used as part of the IPM of agricultural and forest pests [19,22] and there is interest in their inclusion in ITM for residential landscapes. When Mb-F52 was used in combination with other interventions for the management of I. scapularis, reductions in host-seeking ticks generally ranged from 50 to 95% (Table 3). Questing nymphs were reduced by 78–95% at a woodland–lawn edge when Mb-F52 was used along with deer reduction and fipronil-based rodent bait boxes [46]. It was also determined that larvae infesting the white-footed mouse, Peromyscus leucopus, a primary host, were reduced by as much as 94% in residential neighborhoods that received the treatments [47]. A reduction of up to 53% in the possibility of encountering a questing nymph infected with a pathogen was observed when Mb-F52 and fipronil bait boxes were used in combination [45]. These studies demonstrate the effectiveness of an integrated approach to managing I. scapularis using Mb-F52 as a component to help reduce the risk of encountering pathogen-infected nymphs.
Several reports of Mb-F52 use under both laboratory and field conditions have focused on spray applications of oil-based formulations. Spray applications of oil-based formulations generally have superior efficacy against ticks while protecting conidia from adverse environmental effects such as ultraviolet radiation exposure and desiccation, maintaining viability [2,57]. Spray applications targeting foliage/turf where ticks quest have been extensively studied because of the increased potential for tick contact with infective conidia, a critical factor for successful fungal infection [11]. Granule/pellet formulations applied in their solid form also show effectiveness against ticks and there has been recent interest in the development of Metarhizium-based types, particularly for one-host species like D. albipictus and R. microplus, which infest large ungulates [58,59,60,61]. Granules are formulated as an aerial conidia-based material grown on a nutritive substance (i.e., grains) or from microsclerotia (hyphal aggregates) or blastospores produced in liquid culture [59,61,62]. Because granules target the soil/duff layer, the fungi’s natural environment, and have persistence potential [63], they can provide sustained suppression over time, reducing the need for repeat applications. Examinations of the use of Mb-F52 granules for ticks are limited to laboratory trials. Two studies examined the use of conidia-based commercial products [38,40]. One of the studies exposed I. scapularis to granular Mb-F52 and mortality among nymphs ranged from 30.2 to 81.5% after four weeks in the laboratory [40]. Mortality was variable likely due to the nonuniform distribution of the coarse-textured rice, where ticks either contacted a large dose of conidia or missed contact. The other study observed similar results against D. albipictus larvae, with mortality ranging from 79 to 82% after three weeks [38]. In a follow-up study, a Mb-F52 granular material was formulated using millet, a finer material, and mortality of ~80% was observed with no difference in mortality among application rates [61]. To overcome environmental effects and prolong longevity, prototype granular microsclerotia formulations using Mb-F52 have also been tested, with results providing up to 56 and 74% mortality for unfed and fed I. scapularis nymphs, respectively, within seven weeks [64]. The ticks were treated with granules that provided 6.3–4.3 × 108 conidia/cm2 which persisted over time and remained viable for eight weeks. These are concentrations that would presumably cause mortality to ticks that come into contact with infective conidia. Field efficacy studies using prototype formulations are lacking and should be encouraged.

3. Beauveria-Based Formulations

The use of commercial strains of Beauveria bassiana (Balsamo-Crivelli) Vuillemin against ticks has been investigated to a lesser extent than the use of Metarhizium. Reports of the use of these strains are increasing, presumably due to their wide market availability [16]. There are currently five strains formulated as active ingredients (GHA, ATCC 74040, ANT-03, HF-23, and PPRI 5539). They fall under several product lines and are formulated mostly as concentrated suspensions, wettable powders, emulsifiable concentrates, and oil dispersions, primarily with conidia as the infective propagule [16,23]. Evaluations against I. scapularis have focused on strain GHA (ARSEF 6444, ATCC74250), referred to as Bb-GHA hereafter, the active ingredient in the BotaniGard® and Mycotrol® (LAM International, USA) product lines (Table 3). Strain GHA has also been tested against A. americanum, D. albipictus, D. reticulatus, I. ricinus, R. sanguineus, and H. lusitanicum, primarily under laboratory conditions (Table 5). The strain was first isolated from a chrysomelid beetle in the USA. It is a popular biopesticide that is used in a variety of agricultural, landscape, and turf settings to manage a diversity of pests, with few published nontarget effects [16,65]. Currently, no B. bassiana products specifically labeled for ticks are available in the USA.
Like M. brunneum products, the efficacy of products using Bb-GHA has been variable under both laboratory and field conditions. In the laboratory, A. americanum adults treated with Bb-GHA survived 7.2 days compared to 17.9 days in the control and the strain caused noticeable desiccation, an effect of fungal infection [66]. When immersed in up to 108 conidia/mL, 100% mortality occurred after three weeks in the European species I. ricinus and D. reticulatus [53]. Over 90% mortality within four weeks has been observed in aggregated R. sanguineus sensu lato [54]. This species is commonly found indoors in dog kennels and homes and is known to be permethrin resistant and tolerant to fipronil, which are commonly used for its control [69]. In contrast, only 30–41% mortality after three weeks occurred in D. albipictus larvae that were sprayed with 1 × 106–108 conidia/mL, respectively [52].
Beauveria bassiana strain GHA has been shown to cause significant mortality and reduce tick abundance under arena and field conditions. In an arena experiment with cages placed within a forested area in which Bb-GHA was tested against A. americanum, there was significantly greater mortality among adult ticks recovered from treated arenas compared to untreated control arenas [67]. In Spain, when rabbit (Oryctolagus cuniculus) burrows were sprayed with Bb-GHA to manage Hyalomma lusitanicum Koch and other associated ticks, on-host tick numbers were reduced in spring by 79% and 63% by day 30 and 60, respectively, and in summer by 36% on day 30 [68]. Applications of Bb-GHA and Bb-ATCC (Naturalis™) to lawn–woodland perimeters and residential woodlands for I. scapularis nymphs in combination with a wood chip ground barrier was shown to reduce tick abundance on the landscape [44]. In the first year, a reduction of nymph populations was 89% when used with the barrier and 74% without. In the second year, nymph reductions were 55% for both treatments. The probability of encountering a B.-burgdorferi-infected tick was 28.5 and 25.3%, which was lower or comparable to sites treated with the synthetic chemical pesticide bifenthrin (37.7 and 24.3%) for each of the two years. Further research using B. bassiana products against ticks is warranted given their potential to cause mortality. Given the accessibility of B. bassiana products on the market, reports of efficacy testing against ticks will presumably increase in the future until a Metarhizium-based product becomes consistently available.

4. Factors to Consider

Fungal biopesticides reduce tick abundance via direct mortality or through sublethal effects that reduce fecundity [12,17,70]. Ticks vary greatly in susceptibility to fungal infection based on several factors including their species, life stage, engorgement status, and the fungal species, strain, formulation, and rate challenged against [11]. The results described herein demonstrate these variations in fungal effectiveness when tested under laboratory and field conditions. For example, fungi are not universal in their ability to cause mortality, and some reports have shown that increased application rates of Bb-GHA may be needed against some tick species to provide suppression comparable to the same rate of Mb-F52 under controlled laboratory conditions. For example, mortality of D. albipictus larvae was significantly less when treated with Bb-GHA (30–41%) in comparison to Mb-F52 (82–99%) when the two strains were applied at the same rates [52]. In contrast, Bb-GHA killed R. sanguineus sensu lato nymphs faster and caused greater sporulation than Mb-F52 [54]. This difference might be attributed to B. bassiana’s propensity for profuse sporulation under more diverse conditions, where 91.5% of ticks that were infected with Bb-GHA sporulated compared with 77.3% of those infected with Mb-F52.
The performance of entomopathogenic fungi in field settings relies on the environmental conditions in which they are applied. Factors affecting the persistence and virulence of fungi within the environment include temperatures outside the general range of 23–28 °C, low humidity, ultraviolet radiation, precipitation, soil type and pH, and duff layer composition and nutrition [62,71,72]. Site (i.e., soil type, pH, leaf litter depth), weather, and microclimate conditions (i.e., soil moisture, temperature, humidity) were generally unreported in most studies mentioned herein, except for vegetation structure and composition. These factors play an integral role in explaining the efficacy of fungal treatments. For example, sandy, well-drained soils with acidic pH (5.1 to 4.5) and leaf litter and duff layers may have led to limited conidia contact with questing ticks that might have contributed the low performance of Mb-F52 in one report [73]. In another study, differences in interannual climatic conditions likely influenced differences in tick suppression using fungal biopesticides, where one year was hot and dry (drought-like) and the other was mild and wet [44]. The authors also indicated that factors related to the timing and delivery of fungal biopesticides to tick habitats are also a critical factor influencing efficacy and warrant further investigation (i.e., application rates and optimal sprayer volume and pressure). Applications of fungi early and later in the day may allow more optimal humidity conditions and protect from meteorological events such as wind [67]. Given some species like I. scapularis have been reported to be more active in the early morning and evening [74], the effects of application timing in relation to the diurnal activity of ticks should also be considered. Further evaluations against ticks should also focus on the performance of existing products and the development of novel delivery systems. Examples include the efficacy of fungal products that contain mixtures with reduced-risk pesticides such as neem oil and pyrethrins, or the development of auto-dissemination devices for use with trapping technologies like semiochemical and pheromone traps that take advantage of the tick’s host-seeking biology [75,76].
The requirements for appropriate environmental conditions (i.e., temperature, humidity) needed by fungal biopesticides create a challenge in reaching a level of suppression consistently comparable to that of synthetic acaricides and in reducing tick numbers to an acceptable level across a diverse range of conditions [11,43]. Synthetic chemical acaricides, with a few exceptions, consistently achieve a percent reduction in host-seeking nymphs in the field of 80–100% [7]. Chemical pesticides are the top choice made by pest management firms to suppress ticks, followed by natural or organic products, and bifenthrin continues to be the industry standard for management [4,9,41,42]. Natural-product-based acaricides containing cedar extracts are frequently used by commercial pest control firms [9]. Nootkatone has been extensively field tested and, with two exceptions, was shown to reduce questing nymphs by 41–100% [7]. However, like fungus-based biopesticides, natural products are more variable in their ability to reduce ticks and have less robust residual activity than synthetic pyrethroids (i.e., bifenthrin), often requiring multiple applications [9,41,73].
Ultimately, the intent of tick management is to reduce tick bites and the effects of parasitism (e.g., human disease) or to reduce the population of pathogen-infected vectors while considering effectiveness, environmental impact, and cost [77]. Ticks are long-lived arthropods and individuals of some species may spend 98% of their time off-host, free-living in the environment [78]. Research has demonstrated that it takes several weeks for significant tick mortality to occur. Arguably, mortality occurring after a few weeks using fungi is not too long considering the tick life span [64]. For mortality to occur, targeting host-seeking ticks with fungal applications when environmental conditions are conducive is critical (i.e., for fungal infection to suppress ticks in environments where there is a high-risk of tick–human contact to prevent tick-borne disease such as residential settings). For management of pathogen-vectoring ticks, applications should be applied prior to or at onset of activity (i.e., mid-April–May) in the northeastern to mid-Atlantic USA). For example, applications of synthetic pesticides close to the onset of nymphal activity can reduce the risk of exposure to host-seeking ticks and reduce the frequency of applications needed to maintain a high level of suppression (90%), thus saving on management costs from repeat applications, which were needed for Mb-F52 [42]. However, the cost and effects of multiple applications of minimal-risk products in the field on tick populations remain unclear [41], as do acceptable and realistic tick suppression thresholds [4,17], especially for microbial pesticides used in the context of ITM.
Use of fungal biopesticides has not gained traction with pest management companies. Pest management firms were surveyed in Pennsylvania, New Jersey, and New York USA and it was found they routinely charge $100–150 USD (34.9% of respondents) or $151–200 (56.1%) per visit to treat a 1 acre (0.4 ha) area for control of ticks with conventional synthetic pesticides [9]. Pathogenic fungi were not used by applicators and 88% indicated their lack of familiarity with the method as the reason why they lacked experience with its use, whereas only 3% indicated that the products were too expensive. Information on direct cost comparisons between chemical versus microbial controls of ticks is lacking. When residents in Lyme-disease-endemic communities (Connecticut, USA) were surveyed, most were not willing to spend over $100 USD on tick control [79]. In a more recent survey [80], 85% of respondents from Connecticut and Maryland, USA, were willing to pay for a yard treatment, yet still would not spend over $99 USD. Of those willing to pay, 95% would invest in natural pesticides and 63% would pay for chemical pesticides. This suggests there is a consumer demand for alternative control options for ticks if effective; however, public perception of control methods and willingness to pay for prevention would likely differ across states and should be assessed more closely.
A primary goal of the development of effective fungal biopesticides is to identify an entomopathogen as an active ingredient that economically produces stable propagules that can consistently manage the target pest under a variety of field conditions [81]. Quality control issues, the need for repeat applications, and relatively short shelf lives compared to synthetic acaricides drive up the associated costs in both production and application, both common drawbacks to fungal biopesticide use [73,82]. Improvements to the mass production of fungal biopesticides focus on propagule stability, infectivity and shelf life, and formulations and their delivery methods to optimize efficacy for targeted pests under a diversity of conditions [62,81,82,83].

5. Conclusions

It is likely that ticks will shift their ranges as the climate changes, continuing to impact the health of humans, domestic animals, and wildlife [5,84,85,86,87]. Under certain conditions, which generally remain unclear across tick habitats, the use of fungal biopesticides when used in combination with other reduction strategies might achieve results comparable to those achieved synthetic and natural-product-based acaricides if products were consistently available. The quest to identify efficacious, storage-stable, and environmentally persistent fungal biopesticide formulations for use against ticks should continue, given market attraction and adequate funding being allocated towards their development. Although product expansion has been slow for biopesticides for some of the reasons described herein, and in part because of registration complexities and the length of time from proof of concept to the marketing stage, there continues to be interest in production with growth potential as ITM/IPM approaches become more established across a diversity of pest management sectors [4,23,82,88,89,90]. Until alternative tick management strategies become widely available and more research on integrated approaches for other ticks of concern (i.e., A. americanum and D. variabilis) is conducted, management will rely primarily on synthetic, and to a lesser extent, natural-product acaricides [4,9]. The public is concerned about the negative impacts of synthetic pesticides on the environment and their health. As alternatives to synthetic pesticides become more readily available, it is likely that homeowners and commercial pest control firms will consider them if they are efficacious and economical [9,42,80].

Author Contributions

Conceptualization, C.F.S.; writing—original draft preparation, C.F.S.; writing—review and editing, C.F.S., M.S. and B.L.P.; supervision, M.S. and B.L.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We appreciate the University of Vermont, College of Agriculture and Life Sciences for their ongoing support and the anonymous reviewers for their insightful suggestions and comments on an earlier version of this manuscript. The use of trade or corporation names is for informative purposes and does not constitute an official recommendation or endorsement by the University of Vermont.

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.

References

  1. Sonenshine, D.E.; Roe, R.M. Overview: Ticks, people, and animals. In Biology of Ticks; Sonenshine, D.E., Roe, R.M., Eds.; Oxford University Press: New York, NY, USA, 2014; Volume 1, pp. 3–16. [Google Scholar]
  2. Beys-da-Silva, W.O.; Rosa, R.L.; Berger, M.; Coutinho-Rodrigues, C.J.B.; Vainstein, M.H.; Schrank, A.; Bittencourt, V.R.E.P.; Santi, L. Updating the application of Metarhizium anisopliae to control cattle tick Rhipicephalus microplus (Acari: Ixodidae). Exp. Parasitol. 2002, 208, 107812. [Google Scholar] [CrossRef] [PubMed]
  3. Mac, S.; da Silva, S.R.; Sander, B. The economic burden of Lyme disease and the cost-effectiveness of Lyme disease interventions: A scoping review. PLoS ONE 2019, 14, e0210280. [Google Scholar] [CrossRef] [PubMed]
  4. Eisen, L.; Stafford, K.C. Barriers to effective tick management and tick-bite prevention in the United States (Acari: Ixodidae). J. Med. Entomol. 2021, 58, 588–1600. [Google Scholar] [CrossRef] [PubMed]
  5. Alonso-Díaz, M.A.; Fernández-Salas, A. Entomopathogenic fungi for tick control in cattle livestock from Mexico. Front. Fungal Biol. 2021, 2, 657694. [Google Scholar] [CrossRef]
  6. Burtis, J.C.; Poggi, J.D.; Payne, B.; Campbell, S.R.; Harrington, L.C. Susceptibility of Ixodes scapularis (Acari: Ixodidae) to permethrin under a long-term 4-poster deer treatment area on Shelter Island, NY. J. Med. Entomol. 2021, 58, 1966–1969. [Google Scholar] [CrossRef]
  7. Eisen, L.; Dolan, M.C. Evidence for personal protective measures to reduce human contact with blacklegged ticks and for environmentally based control methods to suppress host-seeking blacklegged ticks and reduce infection with Lyme disease spirochetes in tick vectors and rodent reservoirs. J. Med. Entomol. 2016, 53, 1063–1092. [Google Scholar] [CrossRef] [Green Version]
  8. Ginsberg, H.S.; Bargar, T.A.; Hladik, M.L.; Lubelczyk, C. Management of arthropod pathogen vectors in North America: Minimizing adverse effects on pollinators. J. Med. Entomol. 2017, 54, 1463–1475. [Google Scholar] [CrossRef] [Green Version]
  9. Jordan, R.; Schulze, T. Availability and nature of commercial tick control services in three lyme disease endemic states. J. Med. Entomol. 2020, 57, 807–814. [Google Scholar] [CrossRef]
  10. Samish, M.; Ginsberg, H.; Glazer, I. Anti-tick biological control agents: Assessment and future perspectives. In Ticks: Biology, Disease and Control; Bowman, A., Nuttall, P., Eds.; Cambridge University Press: Cambridge, UK, 2008; pp. 447–469. [Google Scholar] [CrossRef]
  11. Fernandes, É.K.K.; Bittencourt, V.R.E.P.; Roberts, D.W. Perspectives on the potential of entomopathogenic fungi in biological control of ticks. Exp. Parasitol. 2012, 130, 300–305. [Google Scholar] [CrossRef]
  12. Ostfeld, R.S.; Price, A.; Hornbostel, V.L.; Benjamin, M.A.; Keesing, F. Controlling ticks and tick-borne zoonoses with biological and chemical agents. BioScience 2006, 56, 383–394. [Google Scholar] [CrossRef] [Green Version]
  13. Samish, M.; Ginsberg, H.; Glazer, I. Biological control of ticks. Parasitology 2004, 129, 389–403. [Google Scholar] [CrossRef] [PubMed]
  14. Faria, M.R.; Wraight, S.P. Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biol. Control. 2007, 43, 237–256. [Google Scholar] [CrossRef]
  15. Fischhoff, I.R.; Keesing, F.; Pendleton, J.; DePietro, D.; Teator, M.; Duerr, S.T.K.; Mowry, S.; Pfister, A.; LaDeau, S.L.; Ostfeld, R.S. Assessing effectiveness of recommended residential yard management measures against ticks. J. Med. Entomol. 2019, 56, 1420–1427. [Google Scholar] [CrossRef] [PubMed]
  16. Mascarin, G.M.; Jaronski, S.T. The production and uses of Beauveria bassiana as a microbial insecticide. World J. Microbiol. Biotechnol. 2016, 32, 177. [Google Scholar] [CrossRef] [PubMed]
  17. Stafford, K.C., III; Williams, S.C.; Molaei, G. Integrated pest management in controlling ticks and tick-associated diseases. J. Integr. Pest Manag. 2017, 8, 28. [Google Scholar] [CrossRef] [Green Version]
  18. Butt, T.M.; Jackson, C.W.; Magan, N. Fungi as Biocontrol Agents: Progress, Problems and Potential; CAB International: Wallingford, UK, 2001. [Google Scholar]
  19. Dara, S.K.; Montalva, C.; Barta, M. Microbial control of invasive forest pests with entomopathogenic fungi: A review of the current situation. Insects 2019, 10, 341. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Lord, J.C. From Metchnikoff to Monsanto and beyond: The path of microbial control. J. Invertebr. Pathol. 2005, 89, 19–29. [Google Scholar] [CrossRef] [Green Version]
  21. Maina, U.M.; Galadima, I.B.; Gambo, F.M.; Zakaria, D. A review on the use of entomopathogenic fungi in the management of insect pests of field crops. J. Entomol. Zool. Stud. 2018, 6, 27–32. [Google Scholar]
  22. Skinner, M.; Parker, B.; Kim, J.S. The role of entomopathogenic fungi in integrated pest management. In Integrated Pest Management: Current Concepts and Ecological Perspective; Abrol, D.P., Ed.; Academic Press: San Diego, CA, USA, 2014; pp. 169–197. [Google Scholar]
  23. Arthurs, S.; Dara, S.K. Microbial biopesticides for invertebrate pests and their markets in the United States. J. Invertebr. Pathol. 2019, 165, 13–21. [Google Scholar] [CrossRef]
  24. Samish, M.; Rehacek, J. Pathogens and predators of ticks and their potential in biological control. Annu. Rev. Entomol. 1999, 44, 159–182. [Google Scholar] [CrossRef]
  25. Benjamin, M.A.; Zhioua, E.; Ostfeld, R.S. Laboratory and field evaluation of the entomopathogenic fungus Metarhizium anisopliae (Deuteromycetes) for controlling questing adult Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 2022, 39, 723–728. [Google Scholar] [CrossRef] [PubMed]
  26. Hornbostel, V.L.; Ostfeld, R.S.; Zhioua, E.; Benjamin, M.A. Sublethal effects of Metarhizium anisopliae (Deuteromycetes) on engorged larval, nymphal, and adult Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 2004, 41, 922–929. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Eisen, R.J.; Eisen, L. The blacklegged tick, Ixodes scapularis: An increasing public health concern. Trends Parasitol. 2018, 34, 295–309. [Google Scholar] [CrossRef] [PubMed]
  28. White, A.; Gaff, H. Review: Application of tick control technologies for blacklegged, lone star and American dog ticks. J. Integr. Pest Manag. 2018, 12, 12. [Google Scholar] [CrossRef]
  29. EFSA (European Food Safety Authority). Peer review of the pesticide risk assessment of the active substance Metarhizium brunneum BIPESCO 5/F52. EFSA J. 2010, 18, 6274. [Google Scholar] [CrossRef]
  30. Fischhoff, I.R.; Keesing, F.; Ostfeld, R.S. The tick biocontrol agent Metarhizium brunneum (= M. anisopliae) (strain F52) does not reduce non-target arthropods. PLoS ONE 2017, 12, e0187675. [Google Scholar] [CrossRef] [Green Version]
  31. USEPA (United State Environmental Protection Agency). Biopesticides Registration Action Document Metarhizium anisopliae Strain F52. Washington, DC, USA. 2003. Available online: https://www3.epa.gov/pesticides/chem_search/reg_actions/registration/decision_PC-029056_18-Jun-03.pdf (accessed on 5 January 2022).
  32. Zimmerman, G. Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Sci. Technol. 2007, 17, 879–920. [Google Scholar] [CrossRef]
  33. Stafford, K.C., III. Tick Management Handbook: An Integrated Guide for Homeowners, Pest Control Operators, and Public Health Officials for the Prevention of Tick-Associated Disease, Revised ed.; The Connecticut Agricultural Experiment Station: New Haven, CT, USA, 2007. Available online: https://portal.ct.gov/-/media/CAES/DOCUMENTS/Publications/Bulletins/b1010pdf.pdf (accessed on 10 January 2022).
  34. Hornbostel, V.L.; Zhioua, E.; Benjamin, M.A.; Ginsberg, H.; Ostfeld, R.S. Pathogenicity of Metarhizium anisopliae (Deuteromycetes) and permethrin to Ixodes scapularis (Acari: Ixodidae) nymphs. Exp. Appl. Acarol. 2005, 35, 301–316. [Google Scholar] [CrossRef]
  35. Debow, J.; Blouin, J.; Rosenblatt, E.; Alexander, C.; Gieder, K.; Cottrell, W.; Murdoch, J.; Donovan, T. Effects of winter ticks and internal parasites on moose survival in Vermont, USA. J. Wildl. Manag. 2021, 85, 1423–1439. [Google Scholar] [CrossRef]
  36. Hays, S.R.; Teel, P.D.; Heath, D.; Starns, N.G.; Moen, R.; Tolleson, D.R. Tick burden observed on cattle and sheep during winter season on the Edwards Plateau of Texas. J. Anim. Sci. 2019, 97, 53–54. [Google Scholar] [CrossRef]
  37. Sundstrom, K.D.; Lineberry, M.W.; Grant, A.N.; Duncan, K.T.; Ientile, M.M.; Little, S.E. Equine attachment site preferences and seasonality of common North American ticks: Amblyomma americanum, Dermacentor albipictus, and Ixodes scapularis. Parasit. Vectors. 2021, 14, 404. [Google Scholar] [CrossRef] [PubMed]
  38. Sullivan, C.F.; Parker, B.L.; Davari, A.; Lee, M.R.; Kim, J.S.; Skinner, M. Pathogenicity of Metarhizium anisopliae and Metarhizium brunneum isolates and efficacy of Met52G against winter tick larvae, 2019. Arthropod Manag. Tests 2020, 45, tsaa100. [Google Scholar] [CrossRef]
  39. Hornbostel, V.L.; Ostfeld, R.S.; Benjamin, M.A. Effectiveness of Metarhizium anisopliae (Deuteromycetes) against Ixodes scapularis (Acari: Ixodidae) engorging on Peromnyscus leucopus. J. Vector Ecol. 2005, 30, 91–101. [Google Scholar]
  40. Bharadwaj, A.; Stafford, K.C., III. Susceptibility of Ixodes scapularis (Acari: Ixodidae) to Metarhizium brunneum F52 (Hypocreales: Clavicipitaceae) using three exposure assays in the laboratory. J. Med. Entomol. 2012, 105, 222–231. [Google Scholar] [CrossRef] [PubMed]
  41. Dyer, M.C.; Requintina, M.D.; Berger, K.A.; Puggioni, G.; Mather, T.N. Evaluating the effects of minimal risk natural products for control of the tick, Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 2021, 58, 390–397. [Google Scholar] [CrossRef]
  42. Schulze, T.L.; Jordan, R.A. Synthetic pyrethroid, natural product and entomopathogenic fungal acaricide product formulations for sustained early season suppression of host-seeking Ixodes scapularis (Acari: Ixodidae) and Amblyomma americanum nymphs. J. Med. Entomol. 2021, 58, 814–820. [Google Scholar] [CrossRef] [PubMed]
  43. Bharadwaj, A.; Stafford, K.C., III. Evaluation of Metarhizium anisopliae strain F52 (Hypocreales: Clavicipitaceae) for control of Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 2010, 47, 862–867. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Stafford, K.C., III; Allan, S.A. Field applications of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae F52 (Hypocreales: Clavicipitaceae) for the control of Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 2010, 47, 1107–1115. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Little, E.A.H.; Williams, S.C.; Stafford, K.C., III; Linske, M.A.; Molaei, G. Evaluating the effectiveness of an integrated tick management approach on multiple pathogen infection in Ixodes scapularis questing nymphs and larvae parasitizing white-footed mice. Exp. Appl. Acarol. 2020, 80, 127–136. [Google Scholar] [CrossRef]
  46. Williams, S.C.; Stafford, K.C., III; Molaei, G.; Linske, M.A. Integrated control of nymphal Ixodes scapularis: Effectiveness of white-tailed deer reduction, the entomopathogenic fungus Metarhizium anisopliae, and fipronil-based rodent bait boxes. Vector Borne Zoonotic Dis. 2018, 18, 55–64. [Google Scholar] [CrossRef]
  47. Williams, S.C.; Little, E.A.H.; Stafford, K.C., III; Molaei, G.; Linske, M.A. Integrated control of juvenile Ixodes scapularis parasitizing Peromyscus leucopus in residential settings in Connecticut, United States. Ticks Tick-Borne Dis. 2018, 9, 1310–1316. [Google Scholar] [CrossRef] [PubMed]
  48. Bharadwaj, A.; Stafford, K.C., III; Behle, R.W. Efficacy and environmental persistence of nootkatone for the control of the blacklegged tick (Acari: Ixodidae) in residential landscapes. J. Med. Entomol. 2012, 49, 1035–1044. [Google Scholar] [CrossRef] [PubMed]
  49. Thomas, D.B.; Tidwell, J.P.; Pérez de León, A.A. In vitro efficacy testing of a commercial formulation of the acaropathogenic fungus Metarhizium brunneum Petch (Hypocreales: Clavicipitaceae) strain F52 against the southern cattle fever tick Boophilus microplus Canestrini (Acari: Ixodidae). Subtrop. Agric. Environ. 2017, 68, 1–6. [Google Scholar]
  50. Yoder, J.A.; Krieger, M.; Oakley, M.; Trotter, J.; Schmelzer, P.; Niksic, A.; Rodell, B.M.; Klever, L.A. Growth characteristics and pathogenic consequences of predominant entomopathogenic Yukon soil fungi Mortierella alpina and Penicillium expansum, and effectiveness of Met52®, against larvae of the winter tick, Dermacentor albipictus. Stud. Fungi 2019, 4, 94–103. [Google Scholar] [CrossRef]
  51. Yoder, J.A.; Rodell, B.M.; Klever, L.A.; Dobrotka, C.J.; Pekins, P.J. Vertical transmission of the entomopathogenic soil fungus Scopulariopsis brevicaulis as a contaminant of eggs in the winter tick, Dermacentor albipictus, collected from calf moose (New Hampshire, USA). Mycology 2019, 10, 174–181. [Google Scholar] [CrossRef] [Green Version]
  52. Sullivan, C.F.; Parker, B.L.; Davari, A.; Lee, M.R.; Kim, J.S.; Skinner, M. Evaluation of spray applications of Metarhizium anisopliae, Metarhizium brunneum and Beauveria bassiana against larval winter ticks, Dermacentor albipictus. Exp. Appl. Acarol. 2020, 82, 559–570. [Google Scholar] [CrossRef]
  53. Szczepańska, A.; Dorota, K.; Plewa-Tutaj, K.; Dagmara, D.; Guz-Regner, K. Sensitivity of Ixodes ricinus (L., 1758) and Dermacentor reticulatus (Fabr., 1794) ticks to entomopathogenic fungi isolates: Preliminary study. Parasitol. Res. 2020, 119, 3857–3861. [Google Scholar] [CrossRef]
  54. Weeks, E.N.I.; Allan, S.A.; Gezan, S.A.; Kaufman, P.E. Auto-dissemination of commercially available fungal pathogens in a laboratory assay for management of the brown dog tick Rhipicephalus sanguineus. Med. Vet. Entomol. 2020, 34, 184–191. [Google Scholar] [CrossRef]
  55. Keesing, F.; Ostfeld, O. The tick project: Testing environmental methods of preventing tick-borne diseases. Trends Parasitol. 2018, 34, 447–450. [Google Scholar] [CrossRef]
  56. Linske, M.A.; Williams, S.C.; Stafford, K.C., III; Li, A.Y. Integrated tick management in Guilford, CT: Fipronil-based rodent-targeted bait box deployment configuration and Peromyscus leucopus (Rodentia: Cricetidae) abundance drive reduction in tick burdens. J. Med. Entomol. 2021, tjab200. [Google Scholar] [CrossRef]
  57. Samish, M.; Rot, A.; Ment, D.; Barel, S.; Glazer, I.; Gindin, G. Efficacy of the entomopathogenic fungus Metarhizium brunneum in controlling the tick Rhipicephalus annulatus under field conditions. Vet. Parasitol. 2014, 206, 258–266. [Google Scholar] [CrossRef] [PubMed]
  58. Marciano, A.F.; Mascarin, G.M.; Franco, R.F.F.; Golo, P.S.; Jaronski, S.T.; Fernandes, É.K.K.; Bittencourt, V.R.E.P. Innovative granular formulation of Metarhizium robertsii microsclerotia and blastospores for cattle tick control. Sci. Rep. 2021, 11, 4972. [Google Scholar] [CrossRef] [PubMed]
  59. Lorenz, S.C.; Humbert, P.; Patel, A.V. Chitin increases drying survival of encapsulated Metarhizium pemphigi blastospores for Ixodes ricinus control. Ticks Tick-Borne Dis. 2021, 11, 101537. [Google Scholar] [CrossRef] [PubMed]
  60. Santos, T.R.; da Paixão, F.R.S.; Catão, A.M.L.; Muniz, E.R.; Ribeiro-Silva, C.S.; Taveira, S.F.; Luz, C.; Mascarin, G.M.; Fernandes, É.K.K.; Marreto, R.N. Inorganic pellets containing microsclerotia of Metarhizium anisopliae: A new technological platform for the biological control of the cattle tick Rhipicephalus microplus. Appl. Microbiol. Biotechnol. 2021, 105, 5001–5012. [Google Scholar] [CrossRef] [PubMed]
  61. Sullivan, C.F.; Parker, B.L.; Kim, J.S.; Skinner, M. Effectiveness of granular formulations of Metarhizium anisopliae and Metarhizium brunneum (Hypocreales: Clavicipitaceae) on off-host larvae of Dermacentor albipictus (Acari: Ixodidae). Biocontrol Sci. Technol. 2021, 31, 113–1127. [Google Scholar] [CrossRef]
  62. Jackson, M.A.; Jaronski, S.T. Production of microsclerotia of the fungal entomopathogen Metarhizium anisopliae and their potential for use as a biocontrol agent for soil-inhabiting insects. Mycol. Res. 2009, 113, 842–850. [Google Scholar] [CrossRef] [PubMed]
  63. Jackson, M.A.; Dunlap, C.A.; Jaronski, S.T. Ecological considerations in producing and formulating fungal entomopathogens for use in insect biocontrol. BioControl 2010, 55, 129–145. [Google Scholar] [CrossRef]
  64. Behle, R.W.; Jackson, M.A.; Flor-weiler, L.B. Efficacy of a granular formulation containing Metarhizium brunneum F52 (Hypocreales: Clavicipitaceae) microsclerotia against nymphs of Ixodes scapularis (Acari: Ixoididae). J. Econ. Entomol. 2013, 106, 57–63. [Google Scholar] [CrossRef]
  65. Zimmerman, G. Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Sci. Technol. 2007, 17, 553–596. [Google Scholar] [CrossRef]
  66. Cradock, K.R.; Needham, G.R. Physiological effects upon Amblyomma americanum (Acari: Ixodidae) infected with Beauveria bassiana (Ascomycota: Hypocreales). Exp. Appl. Acarol. 2011, 53, 361–369. [Google Scholar] [CrossRef]
  67. Cradock, K.R.; Needham, G.R. Beauveria bassiana (Ascomycota: Hypocreales) as a management agent for free-living Amblyomma americanum (Acari: Ixodidae) in Ohio. Exp. Appl. Acarol. 2011, 53, 57–62. [Google Scholar] [CrossRef] [PubMed]
  68. González, J.; Valcárce, F.; Pérez-Sánchez, J.L.; Tercero-Jaime, J.M.; Cutuli, M.T.; Olmeda, A.S. Control of Hyalomma lusitanicum (Acari: Ixodidade) ticks infesting Oryctolagus cuniculus (Lagomorpha: Leporidae) using the entomopathogenic fungus Beauveria bassiana (Hyocreales: Clavicipitaceae) in field conditions. J. Med. Entomol. 2016, 53, 1396–1402. [Google Scholar] [CrossRef] [PubMed]
  69. Eiden, A.L.; Kaufman, P.E.; Ol, F.M.; Allan, S.A.; Miller, R.J. Detection of permethrin resistance and fipronil tolerance in Rhipicephalus sanguineus (Acari: Ixodidae) in the United States. J. Med. Entomol. 2015, 52, 429–436. [Google Scholar] [CrossRef] [PubMed]
  70. Ginsberg, H.S. Tick control. In Biology of Ticks; Sonenshine, D.E., Roe, R.M., Eds.; Oxford University Press: New York, NY, USA, 2014; Volume 2, pp. 409–444. [Google Scholar]
  71. Jaronski, S.T. Ecological factors in the inundative use of fungal entomopathogens. BioControl 2010, 55, 159–185. [Google Scholar] [CrossRef]
  72. Wu, S.; Toews, M.D.; Oliveira-Hofman, C.; Behle, R.W.; Simmons, A.M.; Shapiro-Ilan, D.I. Environmental tolerance of entomopathogenic fungi: A new strain of Cordyceps javanica isolated from a whitefly epizootic versus commercial fungal strains. Insects 2020, 11, 711. [Google Scholar] [CrossRef]
  73. Schulze, T.L.; Jordan, R.A. Early season applications of bifenthrin suppress host-seeking Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae) nymphs. J. Med. Entomol. 2020, 57, 797–800. [Google Scholar] [CrossRef]
  74. Dubie, T.R.; Turner, J.; Noden, B.H. Questing behavior and analysis of tick-borne bacteria in Ixodes scapularis (Acari: Ixodidae) in Oklahoma. J. Med. Entomol. 2018, 55, 1569–1574. [Google Scholar] [CrossRef] [Green Version]
  75. Gaff, H.D.; White, A.; Leas, K.; Kelman, P.; Squire, J.C.; Livingston, D.L.; Sullivan, G.A.; Baker, E.W.; Sonenshine, D.E. TickBot: A novel robotic device for controlling tick populations in the natural environment. Ticks Tick Borne Dis. 2015, 6, 146–151. [Google Scholar] [CrossRef]
  76. Maranga, R.O.; Hassanali, A.; Kaaya, G.P.; Mueke, J.M. Performance of a prototype baited-trap in attracting and infecting the tick Amblyomma variegatum (Acari: Ixodidae) in field experiments. Exp. Appl. Acarol. 2006, 38, 211–218. [Google Scholar] [CrossRef]
  77. Ginsberg, H.S. Integrated pest management and allocation of control efforts for vector-borne diseases. J. Vector Ecol. 2001, 26, 32–38. [Google Scholar]
  78. Anderson, J.F.; Magnarelli, L.A. The biology of ticks. Infect. Dis. Clin. Am. 2008, 22, 195–215. [Google Scholar] [CrossRef] [PubMed]
  79. Gould, L.H.; Nelson, R.S.; Griffith, K.S.; Hayes, E.B.; Piesman, J.; Mead, P.S.; Cartter, M.L. Knowledge, attitudes, and behaviors regarding Lyme disease prevention among Connecticut residents, 1999–2004. Vector Borne Zoonotic Dis. 2008, 8, 769–776. [Google Scholar] [CrossRef] [PubMed]
  80. Niesobecki, S.; Rutz, H.; Niccolai, L.; Hook, S.; Feldman, K.; Hinckley, A. Willingness to pay for select tick-borne disease prevention measures in endemic areas. J. Public Health Manag. Pract. 2022, 28, E37–E42. [Google Scholar] [CrossRef] [PubMed]
  81. Jaronski, S.T.; Mascarin, G.M. Mass production of fungal entomopathogens. In Microbial Control of Insect and Mite Pests: From Theory to Practice; Lacey, L.A., Ed.; Elsevier: Amsterdam, The Netherlands, 2017; pp. 141–154. [Google Scholar]
  82. de la Cruz Quiroz, R.; Cruz Maldonado, J.J.; Alanis, M.R.; Torres, J.A.; Saldivar, R.P. Fungi-based biopesticides: Shelf-life preservation technologies used in commercial products. J. Pest Sci. 2019, 92, 1003–1015. [Google Scholar] [CrossRef]
  83. Lacey, L.A.; Grzywacz, D.; Shapiro-Ilan, D.I.; Frutos, R.; Brownbridge, M.; Goettel, M.S. Insect pathogens as biological control agents: Back to the future. J. Invertebr. Pathol. 2015, 132, 1–41. [Google Scholar] [CrossRef] [Green Version]
  84. Dantas-Torres, F. Climate change, biodiversity, ticks and tick-borne diseases: The butterfly effect. Int. J. Parasitol. Parasites. Wildl. 2015, 28, 452–461. [Google Scholar] [CrossRef] [Green Version]
  85. Eisen, L. Stemming the rising tide of human-biting ticks and tickborne diseases, United States. Emerg. Infect. Dis. 2020, 26, 641–647. [Google Scholar] [CrossRef]
  86. Hofmeister, E.; Hemert, C.V. The effects of climate change on disease spread in wildlife. In Miller-Fowler’s Zoo and Wild Animal Medicine Current Therapy, 1st ed.; Miller, E., Lamberski, N., Calle, P., Eds.; Elsevier: Amsterdam, The Netherlands, 2019; Volume 9, pp. 247–254. [Google Scholar] [CrossRef]
  87. Ogden, N.H.; Beard, C.B.; Ginsberg, H.S.; Tsao, J.I. Possible effects of climate change on ixodid ticks and the pathogens they transmit: Predictions and observations. J. Med. Entomol. 2021, 58, 1536–1545. [Google Scholar] [CrossRef]
  88. Frederiks, C.; Wesseler, J.H. A comparison of the EU and US regulatory frameworks for the active substance registration of microbial biological control agents. Pest Manag. Sci. 2019, 75, 87–103. [Google Scholar] [CrossRef] [Green Version]
  89. Ravensberg, W.J. A Roadmap to the Successful Development and Commercialization of Microbial Pest Control Products for Control of Arthropods; Springer: Heidelberg, Germany; Zoetermeer, The Netherlands, 2011. [Google Scholar]
  90. Zaki, O.; Weekers, F.; Thonart, P.; Tesch, E.; Kuenemann, P.; Jacques, P. Limiting factors of mycopesticide development. Biol. Control 2020, 144, 104220. [Google Scholar] [CrossRef]
Table
Table 1. Effects of commercial products containing Metarhizium brunneum (formerly M. anisopliae) on Ixodes scapularis evaluated under laboratory conditions.
Table 1. Effects of commercial products containing Metarhizium brunneum (formerly M. anisopliae) on Ixodes scapularis evaluated under laboratory conditions.
Product/StrainLife a StageMethodExposure Rate
and Time b		Experiment DurationTreatment Effect cReference
Bio-Blast Biological Termiticide™ (strain ESC1)A (u)Spray4 × 106–9 c/mL4 weeks96% mortality at
109 conidia/mL,
LC50 = 4 × 107 conidia/mL		[25]
N (u)Spray106–9 c/mL; 2.8 mL4 weeks70% mortality at
109 conidia/mL,
LC50 = 107 conidia/mL		[34]
N (u)Topical with chemical pesticidePermethrin (Bonide®) (0.1–1 ppm) at 2 µL then 107–9 c/mL at 10 µL 1 min later23 daysMortality up to ~80% when ticks treated with 0.05 ppm permethrin and fungi at 108 c/mL[34]
L, NTreated cotton batting (nesting material)108 c/mL72 hMortality of ticks dropped from P. leucopus was 75% in treated nest treatment[39]
Tick-Ex® EC (strain F52)A (u)Spray2.6 × 102–6 c/cm2
(3, 30, or 300 min)		4 weeks8.3–100% mortality (3 and 30 min exposures); 0–100% (300 min exposure)[40]
N (u)Spray2.6 × 103–5 c/cm2
(3 or 30 min)		4 weeks10–14.2% mortality (3 min exposure); 6.1–70.8% mortality (30 min exposure)[40]
A (u)Immersion7.4 × 105–9 c/mL
(30 s)		4 weeks8.3–100% mortality[40]
A (u)Treated surface2.6 × 105–8 c/cm2
(3, 30, or 300 min)		4 weeks8.3–100% mortality (3 min exposure); 0–100% (30 min exposure); 16.7–100% (300 min exposure)[40]
N (u)Treated surface2.6 × 103–6 c/cm2
(3 or 30 min)		4 weeks9.2–100% mortality (3 min exposure); 0–100% (30 min exposure)[40]
Tick-Ex®G (strain F52)A (u)Broadcast2.6 × 105–7 c/cm2
(3, 30, or 300 min)		4 weeks27.8–81.9% mortality[40]
N (u)Broadcast2.6 × 105–7 c/cm2
(3, 30, or 300 min)		4 weeks30.2–81.5% mortality[40]
a Life stage: A (adult); L (larvae); N (nymphs); (u) unfed. b c (in numerator) = conidia; cfu (in numerator) = colony-forming units; Time is the length of exposure to the treatment (if specified). c Treatment effect is cumulative to the specified evaluation time.
Table
Table 2. Effects of commercial products containing Metarhizium brunneum (formerly M. anisopliae) on Ixodes scapularis evaluated in the field in residential lawn or woodland settings.
Table 2. Effects of commercial products containing Metarhizium brunneum (formerly M. anisopliae) on Ixodes scapularis evaluated in the field in residential lawn or woodland settings.
Product/StrainLife a StageMethodExposure
Rate b		Experiment DurationTreatment Effect cReference
Bio-Blast Biological Termiticide™ (strain ESC1)A (u)Spray4 × 109 c/mL;
1–1.5 L/100 m2		6 weeks53% mortality among ticks collected from treated plots[25]
A (u)Spray108 c/mL;
1–1.5 L/100 m2 (2×)		3 weeks52% mortality among adults collected from field, 36% control in the field[26]
NSpray109 c/mL;
1–1.5 L/100 m2		4 weeks6–36% control in the field; 20–36% mortality in lab from field collected ticks post treatment[34]
LTreated cotton batting (nesting material)10 mL of 108 c/mL (×10) at density of 9 boxes/ha5 months-1 yearNo significance difference in nymphal densities between areas with treated nest boxes and control; no effect on proportion of nymphs infected with B. burgdorferi[39]
Met52®EC (strain F52)N (u)Spray0.96 mL/m2 (year 1) 1.02 mL/ m2 (year 2) per arena1 month; 2 years10% knockdown control; 0% residual control (year 1), 41.3% and 29.8%, control respectively (year 2)[41]
NSpray10.6 mL/100 m2 (×3)2.5 monthsTarget 90% suppression threshold inconsistently met[42]
Tick-Ex® EC (strain F52)NSpray3.2 × 105 and 1.3 × 106 c/cm2 (×2)3 and 5 weeks87.1 and 96.1% fewer ticks collected from low- and high-rate sites, respectively, after 3 weeks, 53.2 and 73.8% reduction after 5 weeks, 36.4% nymphs collected infected with fungus[43]
a Life stage: A (adult); L (larvae); N (nymphs); (u) unfed. b c (in numerator) = conidia; cfu (in numerator) = colony-forming units; Time is the length of exposure to the treatment (if specified). c Treatment effect is cumulative to the specified evaluation time.
Table
Table 3. Effects of commercial products containing Beauveria bassiana or Metarhizium brunneum (formerly M. anisopliae) on Ixodes scapularis evaluated in combination with other reduction strategies or as part of an integrated tick management program in residential lawn or woodland settings.
Table 3. Effects of commercial products containing Beauveria bassiana or Metarhizium brunneum (formerly M. anisopliae) on Ixodes scapularis evaluated in combination with other reduction strategies or as part of an integrated tick management program in residential lawn or woodland settings.
Product/StrainLife a StageMethodExposure Rate bExperiment Duration c Treatment Effect dReference
Beauveria bassiana
BotaniGard® ES (strain GHA)NSpray + wood chip barrier + lawn perimeter debris removal9.9 × 1011 c/100 m2 (×2)3 months;
2 years 		Without wood chip barrier: 74.5% (year 1) and 55.2% (year 2) tick reduction; with barrier: 88.9% (year 1) 55.1% (year 2) tick reduction[44]
Naturalis® T&O (strain ATCC 74040)NSpray + wood chip barrier + lawn perimeter debris removal2.2 × 109 c/100 m2 (×2)3 months;
2 years		Without wood chip barrier: 83% (year 1) and 38% (year 2) tick reduction; with barrier: 90% (year 1) 56% (year 2) tick reduction[44]
Metarhizium brunneum
Met52®EC
(strain F52)		L, NSpray + deer reduction + fipronil bait box5.5 × 109 cfu/g 0.63–0.96 mL/m2 (×2) 3 months;
2 years		53% reduction in the potential to encounter a questing nymph infected with a pathogen in fungus/bait box treatment; 90% reduction in immature ticks parasitizing P. leucopus in the three combined treatments, 93% reduction in fungus/bait box treatment[45]
NSpray + deer reduction + fipronil bait box5.5 × 109 cfu/g 0.63–0.96 mL/m2 (×2) 3 months;
4 years		78–95% reduction in questing nymphs in fungus/bait box treatment each year; 66% reduction in the potential to encounter a pathogen-infected questing nymph observed in one year[46]
LSpray + deer reduction + fipronil bait box5.5 × 109 cfu/g 0.63–0.96 mL/m2 (×2) 3 months;
3 years		94% reduction in pathogen-infected larvae parasitizing P. leucopus in fungus/bait box treatment; 85% reduction in the three combined treatments[47]
Tick-Ex® EC (strain F52)NSpray with botanical pesticide2.8 × 109 c/m2 with 0.05% nootkatone3 months;
3 years		50% control for one week and no control for the remainder of the season[48]
NSpray + lawn perimeter debris removal2.5 × 1011 c/100 m2 (×2)3 months;
1 year		55.6% tick reduction from lawn perimeter treatment; 84.6% reduction from woodland treatment[44]
a Life stage: A (adult); L (larvae); N (nymphs). b c (in numerator) = conidia; cfu (in numerator) = colony-forming units. c Duration of sampling effort within a season; year after fungal application. d Treatment effect is cumulative to the specified evaluation time.
Table
Table 4. Effects of commercial Met52® products containing Metarhizium brunneum strain F52 (formerly M. anisopliae), or the isolate, on ixodid ticks evaluated under laboratory conditions (unless indicated otherwise).
Table 4. Effects of commercial Met52® products containing Metarhizium brunneum strain F52 (formerly M. anisopliae), or the isolate, on ixodid ticks evaluated under laboratory conditions (unless indicated otherwise).
Tick SpeciesMaterial aLife b StageMethodExposure Rate
and Time c		Experiment DurationTreatment Effect dReference
Amblyomma Americanum
(Lone star tick)		P-ECA, NSpray (woodlands)10.6 mL/100 m2 (3×)2.5 monthsTarget 90% suppression threshold inconsistently met for nymphs, low suppression for adults[42]
Boophilus microplus (Cattle tick)P-ECA (f)Immersion1 × 106–8 cfu/mL (30 s)12 days100% mortality; egg mass weight reduced by ~80%[49]
P-ECL (f)Immersion1 × 106–8 cfu/mL (30 s)1 weekNearly 100% at 108[49]
Dermacentor albipictus
(Winter tick)		IS-ECL (u)Immersion1.6 × 107 c/mL (1 min)15 daysLT50 = 3.7; 100% mortality[50]
IS-ECL (u)Immersion1.3 × 107 c/mL
(1 min)		10 days83.1% mortality for hatching-age; 86.8% for 14-day-old and 81.1% for 5-months-old[51]
IS-ECEImmersion1.3 × 107 c/mL
(1 min)		10 days71.5% failed to hatch treated at oviposition; 67.4% failed to hatch 14 days after oviposition[51]
P-ECL (u)Spray1 × 105 and 2 × 105 c/cm29 days94% and 98% mortality[52]
P-ECL (u)Spray2.4 × 107 c/0.007 m218 weeks and 3 weeks~39% mortality when treated during summer quiescence and ~71%, during fall questing[38]
Dermacentor albipictus
(Winter tick)		IS-GL (u)Spray1 × 106–8 c/mL3 weeks82–99% mortality[52]
IS-GL (u)Immersion1 × 106–8 c/mL
(1 min)		3 weeks46.7%, 100% and 100% mortality [38]
P-GL (u)Broadcast1–4 × 107 c/0.002 m2 dish3 weeks72–89.3% mortality[38]
P-GL (u)Broadcast1 × 108 c/0.007 m218 weeks and 3 weeks~95% mortality when treated during summer quiescence and ~1%, during fall questing[38]
Dermacentor reticulatus
(Ornate cow tick)		IS-GA (u)Immersion102–8 cfu/mL
(3 min) 		3 weeksUp to 100% mortality; LC50 = 2.0 × 106 cfu/mL (females)[53]
Ixodes ricinus
(Castor bean tick)		IS-GA (u)Immersion102–8 cfu/mL
(3 min)		3 weeksUp to 100% mortality; LC50 = 1.6 × 106 cfu/mL (females). [53]
Rhipicephalus sanguineus
(Brown dog tick)		P-ECNTreated surface1 × 109 c/mL (1.48 × 107 c/cm2)/pack
(60 min)		4 weeks>80% mortality; 77.3% of infected ticks sporulated[54]
a EC, emulsifiable concentrate; G, granular; IS, strain was isolated from product then tested; P, product was tested. b Life stage: A (adult); E (egg); L (larvae); N (nymphs); (f) fed; (u) unfed. c c (in numerator) = conidia; cfu (in numerator) = colony-forming units; Time is the length of exposure to the treatment (if specified). d Treatment effect is cumulative to the specified evaluation time.
Table
Table 5. Effects of the commercial Beauveria bassiana product BotaniGard® (strain GHA), or the isolated strain, on ixodid ticks evaluated under laboratory and field conditions.
Table 5. Effects of the commercial Beauveria bassiana product BotaniGard® (strain GHA), or the isolated strain, on ixodid ticks evaluated under laboratory and field conditions.
Tick SpeciesMaterial aLife b
Stage		MethodExposure Rate
and Time c		Experiment
Duration		Treatment Effect dReference
Laboratory
Amblyomma americanum (Lone star tick)P-ESA (u)Immersion108 c/mL
(10 s)		26 daysTreated ticks survived a mean of 7.2 days[66]
Dermacentor albipictus
(Winter tick)		ISL (u)Spray1 × 106–8 c/mL21 days30–41% mortality[52]
Dermacentor reticulatus
(Ornate cow tick)		IS-WPA (u)Immersion102–108 cfu/mL
(3 min)		3 weeksUp to100% mortality;
LC50 = 6.8 × 103 cfu/mL		[53]
Ixodes ricinus
(Castor bean tick)		IS-WPA (u)Immersion102–108 cfu/mL
(3 min)		3 weeksUp to 100% mortality;
LC50 3.3 × 106 cfu/mL for adult females		[53]
Rhipicephalus sanguineus
(Brown dog tick)		P-ESNTreated surface1 × 109 c/mL (1.48 × 107 c/cm2)/pack (60 min)4 weeks>90% mortality[54]
Field
Amblyomma americanum (Lone star tick)PA (u)Immersion then placed in arenas108 c/mL
(1 s)		2 weeksUp to 96% mortality [67]
Hyalomma lusitanicumePAll stagesSprayed host burrows2.43 × 108 c/mL (spring)30 and 60 days78.63% and 63.28% parasitism reduction on rabbits in spring, 35.72% and 29.01% in summer[68]
a ES, a emulsifiable concentrate; IS, strain was isolated from product then tested; P, product was tested; WP, wettable powder. b Life stage: A (adult); E (egg); L (larvae); N (nymphs); (f) fed; (u) unfed. c c (in numerator) = conidia; cfu (in numerator) = colony-forming units; Time is the length of exposure to the treatment (if specified). d Treatment effect is cumulative to the specified evaluation time. e During summer, Hyalomma lusitanicum was dominant species (79.95%), others included Rhipicephalus pusillus (11.08%), Haemaphysalis hispanica (8.94%), Ixodes ventalloi (0.02%), and Dermacentor marginatus (0.01%).
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Sullivan, C.F.; Parker, B.L.; Skinner, M. A Review of Commercial Metarhizium- and Beauveria-Based Biopesticides for the Biological Control of Ticks in the USA. Insects 2022, 13, 260. https://doi.org/10.3390/insects13030260

AMA Style

Sullivan CF, Parker BL, Skinner M. A Review of Commercial Metarhizium- and Beauveria-Based Biopesticides for the Biological Control of Ticks in the USA. Insects. 2022; 13(3):260. https://doi.org/10.3390/insects13030260

Chicago/Turabian Style

Sullivan, Cheryl Frank, Bruce L. Parker, and Margaret Skinner. 2022. "A Review of Commercial Metarhizium- and Beauveria-Based Biopesticides for the Biological Control of Ticks in the USA" Insects 13, no. 3: 260. https://doi.org/10.3390/insects13030260

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop