Insect Pathogenic Fungi for Biocontrol of Plague Vector Fleas: A Review
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Journal of Integrated Pest Management, (2021) 12(1): 30; 1–10
https://doi.org/10.1093/jipm/pmab028
Issues
Insect Pathogenic Fungi for Biocontrol of Plague Vector
Fleas: A Review
David A. Eads,1, Stefan T. Jaronski,2 Dean E. Biggins,1 and Jeffrey Wimsatt3,4
1
U.S. Geological Survey, Fort Collins Science Center, Fort Collins, CO 80526, USA 2U.S. Department of Agriculture, Agricultural Re-
search Services (retired), Blacksburg, VA 24060, USA 3Department of Medicine, West Virginia University, Morgantown, WV 26506,
USA, and 4Corresponding author, e-mail: jefwimsatt@gmail.com
Downloaded from https://academic.oup.com/jipm/article/12/1/30/6358184 by guest on 04 December 2021
Subject Editor: Stephen Vantasse
Received 18 April 2021; Editorial decision 30 July 2021
Abstract
Bubonic plague is a lethal bacterial disease of great historical importance. The plague organism, Yersinia pestis,
is primarily transmitted by fleas (Siphonaptera). In natural settings, where its range expands, Y. pestis resides in
association with wild rodents and their fleas (sylvatic plague). While chemical insecticides are used against plague
vector fleas, biological approaches have not been as critically evaluated. Benign and cost-effective control methods
are sorely needed, particularly where imperiled species are at risk. Here we explore the potential of two representative
insect pathogenic fungi, Beauveria bassiana Vuillemin 1912 (Hypocreales: Cordycipitaceae) and Metarhizium
anisopliae Metschnikoff 1879 (Hypocreales: Clavicipitaceae), each already used commercially worldwide in large-
scale agricultural applications, as candidate biopesticides for application against fleas. We review the life cycles, flea
virulence, commercial production, and field application of these fungi, and ecological and safety considerations.
Pathogenic fungi infections among natural flea populations suggest that conditions within at least some rodent
burrows are favorable, and laboratory studies demonstrate lethality of these fungi to at least some representative
flea species. Continued study and advancements with these fungi, under appropriate safety measures, may allow
for effective biocontrol of plague vector fleas to protect imperiled species, decrease plague outbreaks in key rodent
species, and limit plague in humans.
Key words: flea, plague, biopesticide, Beauveria, Metarhizium
Bubonic plague is caused by the bacterium Yersinia pestis Lehmann Antolin et al. 2002, Matchett et al. 2010). In an effort to ensure
and Neumann 1896 (Enterobacteriales: Enterobacteriaceae) and is the reestablishment of these endangered ferrets over their historical
found on all continents except Australia and Antarctica. In many range and to expand the numbers and range of prey species upon
parts of the world, peri-domestic rodents are responsible for moving which they depend, multiple chemical and biological approaches
Y. pestis into close contact with humans, but wild native rodents and have been attempted to control fleas (Seery et al. 2003, Biggins et al.
their fleas (Siphonaptera) seem to provide the conditions for plague 2010, 2021, Matchett et al. 2010, Eads and Biggins 2019, Eads et al.
persistence over extended periods. The primary means of Y. pestis 2020a, b, 2021). Most of these same methods have been employed
dissemination is via infected fleas, which typically complete their life for field application in plague endemic regions around the world as
cycle in host nests. Adult fleas amplify infection rates by infecting ver- public health measures (e.g., Borchert et al. 2010). Here we explore
tebrate hosts while imbibing blood and, once infected, spread plague the potential for flea biocontrol employing insect pathogenic fungi,
bacteria to more hosts and fleas in a cascading manner (Biggins and now widely used on crops (including in organic farming) to control
Eads 2019). Plague expansion in the western United States might be insect ‘pests’. We note, in the context of this paper, native rodents or
facilitated by drier conditions in response to climate change (Eads fleas are not considered ‘pests’; invasive Y. pestis could be considered
et al. 2016, Eads and Biggins 2017, Eads and Hoogland 2016, 2017, a pest in this context.
Biggins and Eads 2019, Carlson et al. 2021). Once established, Effective flea control methods have broad appeal for use in
epizootic die-offs of rodents punctuate less visible periods of con- public health to diminish a range of diseases in which flea species
tinued host losses (Biggins and Eads 2019). The role of plague in serve as the primary vectors. While this review is restricted to flea
challenging survival of the endangered black-footed ferret (Mustela control that could protect wild vertebrate populations where plague
nigripes Audubon and Bachman 1851 [Carnivora: Mustelidae]) is found, approaches discussed may be applicable to other public
and survival of its obligate rodent prey (prairie dogs, Cynomys spp. health interventions. An added impetus to look for new approaches
[Rodentia: Sciuridae]) is well known (Biggins and Kosoy 2001a, b, is based on the observation that chemical insecticide resistance
Published by Oxford University Press on behalf of Entomological Society of America 2021. This work is written by (a) US Govern-
ment employee(s) and is in the public domain in the US.
12 Journal of Integrated Pest Management, 2021, Vol. 12, No. 1
develops during sustained public health uses (Thaung et al. 1975, actuality, based on multi-locus genetic analyses, Beauveria repre-
Renapurkar 1990, Ratovonjato et al. 2000) or when implemented sents a complex of species comprised of one or more fungal lin-
as part of annual operational conservation efforts (Eads et al. 2018). eages (Chandler 2017, Imoulan et al. 2017, Anwar et al. 2018). As
Collateral damage to the local biota also remains a potential down- of 2017, 17 species of Beauveria had been identified based on DNA
side of chemical insecticide applications. In contrast, the use of sequences (Rehner et al. 2011).
biopesticides, such as insect pathogenic fungi, appears to have the Similarly, Metchnikoff first characterized the insect pathogen
potential to be less disruptive (Garrido-Jurado et al. 2011), consider- M. anisopliae (henceforth Metarhizium) in 1879 (Vega et al. 2009,
ably less prone to evolution of resistance by insects (Lacey 2017a, b), Luangsa-ard et al. 2017). Commercial exploitation of Metarhizium
and more cost-effective. We illustrate these points with a literature for insect control started as early as 1888 (Zimmermann 2007b).
review, presenting new ideas to guide research and progress toward The taxonomic relationships of this mostly temperate species have
desired plague mitigation outcomes. been described (Vega et al. 2009). Metarhizium is likewise com-
prised of at least 52 species with local variants (Bischoff et al. 2009,
Scheepmaker and Butt 2010, Chandler 2017).
Both fungi represent the majority of commercially developed
Insect Pathogenic Fungi as Biopesticides
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arthropod control products because of their ease of mass produc-
Insect pathogenic fungi have generated increasing interest for tion, although they are considered by some to have the drawback of
their valuable contributions to integrated (and organic) pest man- acting too slowly and having a relatively short environmental per-
agement during the last several decades. A survey of commercial sistence during foliar applications (i.e., use above ground). In the
mycoinsecticides (i.e., microbial insecticides with a live fungus ac- wild, Beauveria is considered a weak saprophyte limited in number
tive ingredient) in 2007 provided a comprehensive list of products by agents released by soil organisms. Soil inoculated with Beauveria
worldwide, discussing different fungi species and strains (Faria after autoclaving led to longer periods of persistence (Lacey 2017a,
and Wraight 2007). Since then, even more products have become b). Wild Metarhizium remains viable in soil for months, so it appears
available. In the United States, several strains of Beauveria bassiana more persistent than Beauveria (Snow 1893, Zimmermann 2007b).
Vuillemin 1912 (Hypocreales: Cordycipitaceae) and Metarhizium Microbiological effects on Metarhizium and Beauveria in soil have
anisopliae Metschnikoff 1879 (Hypocreales: Clavicipitaceae) are re- been reviewed elsewhere, including negative effects of montmorillite,
gistered for use against insect pests. Our review will focus on these for instance, on fungal respiration, radial growth, and conidial ger-
two commercially available species because they are amenable to mination (Snow 1893; Lacey 2017a, b). The common observation of
large-scale production, and considerable experience has been gained shortened persistence on plant surfaces is attributed to the effects of
from their use against a wide range of agricultural pests (we note, UV-A and UV-B radiation (Fargues et al. 1996, Fernandes et al. 2007)
however, that Cordyceps [Isaria] spp. fungi might be considered in that would not directly apply to in-burrow applications to control
this context in the future, but these seem to be most effective against fleas parasitizing ground-dwelling rodents such as prairie dogs.
Homopterans). Fungus-based biopesticides do not seem to result in naturally
Key pathogenic fungi are found in the Ascomycete order evolved resistance in target insects, one of the advantages of fungi
Hypocreales. Historically, with only asexual stages known, they compared to chemical insecticides (Lacey 2017a, b), though there
were classed within the Deuteromycetes, the Fungi Imperfecti. are exceptions (indeed resistance may develop, but could be costly
However, as molecular tools have allowed their association with to the insects because energies and resources may be concentrated
known sexual stages, they have been reclassified, with Beauveria on front-line defenses such as the integument, thus compromising
species placed within the genus Cordyceps and Metarhizium spe- and reducing the efficacy of other defenses; e.g., Dubovskiy et al.
cies in Metacordyceps (Meyling and Eilenberg 2007), but their ori- 2013). However, natural variation in susceptibility to these fungi
ginal nomenclature was retained. In general, fungi get their nutrition has been demonstrated in Drosophila, and artificial selection for de-
from the products from which they imbibe following the release of creased susceptibility has been demonstrated (Tinsley et al. 2006,
degradative enzymes into their environment (Chandler 2017). The Kraaijeveld and Godfray 2008). In some settings, insects may avoid
insect pathogenic fungi may have evolved from soil saprophytes or areas harboring these biopesticides (Luangsa-ard et al. 2017), al-
possibly plant endophytes, developing the ability to infect and kill lowing the use of these fungi to serve as a pest deterrent or repellant
arthropods for sustenance and reproduction (Araújo et al. 2016). (Villani et al. 1994, Fry et al. 1997, Ekesi et al. 2001). Components
The soil is presumably a reservoir for B. bassiana and M. anisopliae of the outer cuticle of some species of stink bugs (Hemiptera:
(Castrillo et al., 2010), dispersing above-ground by the action of Pentatomidae) are reported to inhibit fungal growth, which seems
wind, rain, and invertebrate activity (e.g., horizontal transmission), to contribute to reduced susceptibility (Sosa-Gomez et al. 1997) and
as well as through infection of and reproduction in soil-dwelling the propensity or lack thereof for insects to molt is likely important
insects, and in some cases endophytism within plants (Snow 1893, (Sherwani and Khan 2015).
Lacey 2017a, b). Wind dissemination does not seem to be of similar Plague fleas found on rodents seem to be a favorable target for
importance for Metarhizium. these agents because their life cycle is almost completely under-
The application of B. bassiana and M. anisopliae has a long ground where there is little to no ultraviolet (UV) exposure, and
history. In 1837, B. bassiana (henceforth Beauveria), a known silk- organic matter, moisture, carbon, and oxygen seem favorable for
worm pathogen, was discovered to infect other insects (Faria and fungal survival, creating a potential for persistence (Sherwani and
Wraight 2007). In 1912, Vuillemin further characterized Beauveria, Khan 2015). Overall, Beauveria and Metarhizium have consider-
and, to date, it has been applied to control an array of agricultural able safety for mammals (Snow 1893, Zimmermann 2007a, b, Lacey
pests (Rehner and Buckley 2005). As early as 1893, Beauveria- 2017a, b). In addition, insect pathogenic fungi might be used where
infected chinch bugs (Blissus leucopterus) were released in Kansas chemical resistance has developed. However, in the laboratory, recent
as an attempted control method (Rehner et al. 2011). The desig- studies have found that the toxicological and biochemical responses
nation of Beauveria as a ‘species’ is convenient but misleading; in of fungi can be affected by either the active or the ‘inert’ ingredientsJournal of Integrated Pest Management, 2021, Vol. 12, No. 1 3
of chemical insecticides, as in the case of residual benzene contam- Other Potential Targets in the Context
inating certain synthetic pyrethroids (Forlani et al. 2014). Chemical of Plague
insecticides can also reduce the efficacy of biocontrol methods by a
A secondary concern is the potential for other biting arthropods
reduction in the number of susceptible insects (Rehner and Buckley
to spread Y. pestis from host to host during terminal host sepsis
2005, but see Meyling et al. 2018). Thus, as discussed below, some
through biting contamination as demonstrated in fleas (Nel’zina
monitoring of flea numbers on and/or off hosts, in nature and under
et al. 1978). Ticks (mainly Ixodida) are found in burrow systems
laboratory conditions, both of which may be time and labor inten-
(Eisen et al. 2006) and could harbor (Treviño-Villarreal et al. 1998)
sive, may be necessary to appropriately stage applications to increase
or transmit Y. pesits (Zykin 1994); albeit, as less mobile ectopara-
the efficacy of biocontrol methods.
sites, they would seem to be ill-suited to initiate a plague epizootic.
Reducing parasite loading on prey species may still have benefi-
cial effects (e.g., increasing host body condition; Eads et al. 2021).
Flea Studies Nevertheless, researchers in Mexico have shown that Metarhizium
Literature on flea susceptibility to insect pathogenic fungi is limited. killed gravid female Rhipicephalus (Boophilus) microplus Canestrini
In one study, spore suspensions containing 0.01% Tween 80 were 1888 (Ixodida: Ixodidae) ticks under tropical conditions on natur-
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tested in a laboratory bioassay. Selected strains of both Metarhizium ally parasitized cattle at a rate of 40–90% (Koul 2016). A standard
and Beauveria were effective against cat fleas (Ctenocephalides felis pasture application had reduced efficacy, although direct tick patho-
Bouché, 1835 [Siphonaptera: Pulicidae]) at a dose of 108 spores ml–1 genicity was demonstrated (Li et al. 2007). UV light exposure and
following 3-min immersions (de Melo et al. 2007). After contact, tropical conditions were suggested causes of the reduced efficacy.
spore-cuticle attachment took 2 h, and full flea cuticle investment by Metarhizium was also lethal to tick larvae (Garcia et al. 2011).
germinating spores took 15 h. Although both fungi were generally Similarly, Metarhizium applied to Bovicola bovis Nitzsch 1818
lethal to all cat flea stages, Metarhizium was more effective on eggs (Trichodectidae: Ischnocera), the common louse of cattle averaged
and larvae (only 13–64% hatchability ≥36 h post-exposure) while 73% effective (Angel-Sahagún et al. 2010). Mite (Sarcoptiformes:
Beauveria was more effective on adults (34–100% mortality ≥36 h Psoroptidae) pathogenicity has also been documented (Briggs et al.
post-exposure) (de Melo et al. 2008). Improved killing was observed 2006). Both lice and mites may contribute to plague transmission
at ≥ 82% humidity and temperatures of 25 ± 2.5°C for these two in some cases (Eads 2019, Eads et al. 2020b). Potential effects on
agents on flea larvae after short (3 h) exposures. Interestingly, under other burrow invertebrates are unknown, but likely less significant
these same laboratory conditions, sporulation on the flea larvae was than chemical insecticide applications, which can also contaminate
not observed (de Melo et al. 2007). ground water (e.g., Mukherjee and Gopal 2002). Specific details of
In another study (Pittarate et al. 2018), adult C. felis were ex- pathogenic fungi life cycles are likely to be highly influential in these
posed to aerial conidia of Metarhizium and Beauveria, from 0.03 × dynamics.
108 to 0.21 × 108 conidia ml−1, suspended in a 0.01% aqueous solu-
tion of Tween 80. Beauveria cultured under red LED and fluorescent
light were the most effective after 36 h. All fleas treated with fungi Insect Pathogenic Fungi Life Cycles
were killed within 48 h. Samish et al. (2020) found that Metarhizium In general, insect pathogenic fungi pass through several life stages
(robertsii) and Beauveria, each in Petri dishes at 0.4 ml 0.01% sur- including attachment of aerial conidia, or spores, to the insect cuticle,
factant, were highly virulent against adult and larval C. felis (e.g., germination, cuticle penetration (Boucias et al. 1988, Ortiz-Urquiza
13–44% mortality for larvae) but the eggs appeared less susceptible and Keyhani 2013), within-host vegetative growth, fungal protrusion
(90–96% hatchability). of fruiting appendages outside the host, and secondary spore produc-
Other studies on different flea species gave comparable results. tion, leading to fungus dissemination (Vega et al. 2009). Pathogenic
For example, in Tanzania, Mnyone et al. (2012) demonstrated a 3- to fungi may use an array of insect-killing strategies, thus making them
4-fold reduction in survival of larval Xenopsylla brasiliensis Baker, less prone to developing host resistance (Sherwani and Khan 2015).
1904 (Siphonaptera: Pulicidae) exposed to strains of Beauveria Both Beauveria and Metarhizium penetrate into an insect by means
and Metarhizium. Russian workers demonstrated the successful of mechanical pressure, aided by enzymes (e.g., proteases, cellulase,
parasitism by both Beauveria and Metarhizium strains against the chitinase, B-glucanase, lipases, and N-acetylglucosaminidase; Vega
northern rat flea (Ceratophyllus fasciatus Authority Bosc 1800 et al. 2009, Sherwani and Khan 2015). Beauveria was thought to
[Siphonaptera: Ceratophyllidae]; Kessler et al. 2003). also infect insect hosts following ingestion by the insect (Sherwani
In 2017, U.S. Department of Agriculture, Agricultural Research and Khan 2015) (e.g., this might occur with larval fleas) but this
Service (S.T.J.) completed a brief fungal survey on flea samples observation with locusts (Orthoptera: Acrididae) more likely reflects
collected between August and October 2017 from prairie dogs at entry through the insect’s mouth parts (Dillon and Charnley 1988,
Buffalo Gap National Grassland, South Dakota. During this survey, Dillon et al. 2005). Death may proceed in response to nutrient de-
at least five morphologically distinct strains of M. anisopliae (wild or- pletion as well as from release of toxic metabolites (Vuillemin et al.
ganism) were isolated from the fleas provided. A culture of each mor- 1912, Zimmermann 2007a, b). Once the fungus is inside its host,
phological type was deposited in the USDA ARS Entomopathogenic evidence suggests that an insect’s behavior (e.g., locomotion) may be
Fungus collection as deposits ARSEF 13760–13764. The prevalence altered well before death (Vega et al. 2009); such effects could con-
of natural Metarhizium infections indicates that conditions within ceivably reduce plague transmission or dissemination by fleas and
prairie dog burrows are favorable for the persistence of these fungi their survival (Shang et al. 2015). Fungal elaboration of chitinase
in association with flea populations at low concentrations; it is sur- inhibitors could likely stop larval fleas from molting and possibly
mised that the Metarhizium organism does not appear to appre- shedding their exocuticle, allowing fungus to completely penetrate
ciably affect flea populations at background levels, at least in the and kill the insect (Sherwani and Khan 2015); generally speaking,
sampling locations, but might serve as a natural flea population adult fleas do not molt during maturation, which may facilitate
regulator when flea densities are high. fungus penetration, perhaps depending on fungal strain virulence.4 Journal of Integrated Pest Management, 2021, Vol. 12, No. 1
Fungal Strain-Based Virulence or washable clothes, and handwashing when applications are com-
pleted. A novel formulation uses a dry finely powdered carnuba wax
We provide a partial list of the best characterized insect toxins pro-
carrier (Nollet and Rathore 2015), whereby the conidia adhere to the
duced by Beauveria and Metarhizium (Molnár et al. 2010, Chen et al.
electrostatically charged wax particles which are themselves strongly
2020, Zhang et al. 2020), how their toxins were evaluated, and any
attracted to insect cuticle, animal fur, etc., that might enhance flea
known effects in vertebrates (Supp Tables S1 and S2 [online only]).
contact. This type of formulation using Beauveria spores has been
The potencies of toxins are commonly tested for their efficacy
successfully commercialized for use against stored product insects
against silkworms (Bombyx mori Linnaeus 1758 [Lepidoptera:
in the United Kingdom (Athanassiou et al. 2016). One delivery ap-
Bombycidae]) or greater wax moth larvae (Galleria mellonella
proach for dust formulations would be to blow dust into the initial
Linnaeus 1758 [Lepidoptera: Pyralidae]) (Koul 2016). This testing
1–2 m of each burrow so that dust-laden spores are tracked more
approach is used when wild isolates of fungus are cultivated to
deeply into burrow systems on rodent feet and fur. Spores could then
ensure their potency before commercialization, and when regu-
transfer from animals to their fleas and perhaps among fleas. In add-
latory agencies require these data (Keller et al. 1989). This bio-
ition, there is a possibility that the dust formulation could be trans-
assay approach is relatively easy and inexpensive to run. A newer
ported by the rodents into nesting areas to affect adult and larval flea
less established European bioassay using brine shrimp (Artemia
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populations residing there; both Beauveria and Metarhizium can in-
salina Linnaeus 1758 [Anostraca: Artemiidae]) has been described
fect all life stages of insects (Vega et al. 2009). Alternatively, rodents
(Strasser et al. 2000, Garrido-Jurado et al. 2016). Similarly, quality
could be dusted during trapping; however, this approach is probably
control in the making of each batch of commercial product would
not practical for large-scale use unless flea transfer rates (e.g., hori-
ideally involve bioassay of production samples against reference in-
zontal transfer of fungi; Membang et al. 2021) are extremely high.
sects at regular intervals. In many cases, passing an individual wild
In addition to the dry conidial preparations, neet oil and emulsifi-
fungal isolate for 10 or more in-vitro generations may degrade its
able oil formulations exist and are the most common form used in
potency (Strasser et al. 2000, Jaronski 2013, Garrido-Jurado et al.
agricultural settings. Oils or other anti-drying binder-containing for-
2016) but not always (Brownbridge et al. 2001); even so, preserving
mulations are used to suspend spores for applications under dry con-
early passage samples for reconstitution is important.
ditions, to increase spore survival (Feng et al. 1994, Exosect 2019).
To assess safety in vertebrates, the U.S. Environmental Protection
The addition of binders may additionally influence safety as well as
Agency requires a first tier of testing based on acute toxicity/infect-
efficacy. Application of aqueous sprays of these formulations to the
ivity assessments in rats or mice, following a range of administration
burrows is probably not practical.
routes. If no adverse effects are seen, fungal metabolites of concern
Optimization of a particular strain for high flea-selectivity or at
to regulators must still be quantitatively determined, in at least the
least a high flea virulence might further increase efficacy and safety.
‘active ingredient’ (spores). For Beauveria, oosporein, beauvericin,
There is a certain degree of host specificity among strains of any
and bassianaolide are currently assayed. For Metarhizium, several of
insect pathogenic fungus for any given insect target species. For ex-
the Destruxin depsipeptides are evaluated.
ample, in one study, the lethal concentration, capable of killing 50%
In the future, Beauveria and Metarhizium may be adaptable via
of insects, of 43 Beauveria strains for European corn borer (Ostrinia
further genetic modifications to improve their selective virulence
nubilalis Mutuura and Munroe 1970 [Lepidoptera: Crambidae])
against insects, including fleas (Lovett and St. Leger 2018). Even so,
spanned a 650-fold range (Wraight et al. 2010). At least one arti-
the addition of genetic modifications is controversial and warrants
ficially generated variant of Metarhizium was demonstrated to
careful study (Lacey 2017a, b). Moreover, even if a fungal strain is
have even greater virulence against selected agricultural pests than
highly virulent against fleas, the method of fungal delivery is likely
the wild-type organism (Nyasani et al. 2015). The advent of gen-
to influence contact rates and, therefore, be a critical determinant of
etic characterizations has ushered in opportunities to refine specific
flea population control.
selected fungi activities during fine-scale or commercial production
in the future (Zimmermann 2007b, Tseng et al. 2014, Lovett and St.
Methods for Fungal Delivery Leger 2018).
In general, high temperatures and UV light readily degrade and kill
Metarhizium and Beauveria, limiting their persistence (Jaronski
2010). The field disposition, environmental degradation, and per-
Commercial Production
sistence of biopesticides have been reviewed (Jaronski 2010). During As previously noted, both Metarhizium and Beauveria have an
field broadcast applications (e.g., 0.5–1 kg ha−1), commercial conidial array of insect host ranges making them ideal targets for commer-
spore preparations typically last ~1.5 d on crops under typical UV cialization, and several different Metarhizium and Beauveria iso-
exposures (Jaronski 2010). In contrast, burrow applications should lates have been developed for commercial sale world-wide (Faria
last longer (e.g., at least 2–3 weeks, assuming lower ambient temper- and Wraight 2007, Mascarin and Jaronski 2016, Jaronski and
atures, some moisture and reduced UV exposures). With heavier flea Mascarin 2017). The optimization and production of commercial
burdens (also where plague risk is high), flea and other insect car- Beauveria was recently reviewed (Jaronski and Mascarin 2017).
casses may become ‘spore generators’, amplifying the killing process All commercial formulations of Beauveria and Metarhizium utilize
and duration of action against plague vector fleas. aerial conidiospores, which retain relatively sturdy cell walls, and
Perhaps the most efficient delivery method for spores into rodent are produced on the solid substrate (Jaronski 2013). The com-
burrows is a dust carrier. Such dust formulations can contain fine mercial production and formulation of Beauveria was recently
talc or clay and are blown into the mouth of an active burrow with reviewed in detail (Mascarin and Jaronski 2016). The shelf-life
a hand- or machine-power duster. Talc has been used as a diluent for of Beauveria is generally longer than for Metarhizium (Jaronski
experimental dry spore applications (Lord 2005). Delivery is gen- 2013). Shelf-life also varies widely with strain and storage con-
erally downwind from the applicator and reasonable precautions ditions (Anwer 2017). Avoiding high storage temperatures and
for applicators including wearing gloves, filtration masks, gowns light exposure are important factors in product durability (AnwerJournal of Integrated Pest Management, 2021, Vol. 12, No. 1 5
2017). With the exception of Beauveria strain GHA, none of the Metarhizium was detected from warmer soils (e.g., 25°C) and
commercial fungi have been evaluated for efficacy against flea spe- Beauveria from colder soils (e.g., 12°C), but soil type, per se, had
cies. Strain GHA was observed to be fairly infective for C. felis minimal impact compared to moisture and agricultural inputs
in laboratory bioassays but was never registered for use against (Jaronski 2007).
fleas (S.T.J., personal observations). Verification of killing effi- Altitude had no effect on fungal diversity up to 1608 m in one
ciency could be accomplished with topical bioassays with adult study (Vega et al. 2009), but impacted diversity above this elevation,
fleas, or soil incorporation assays with larvae. Tanzanian and favoring Beauveria (Sun and Liu 2008). It cannot be ruled out that
Brazilian fungi strains have been tested (de Melo et al. 2007, 2008, Beauveria may prefer specific insect host ranges and favor local con-
Mnyone et al. 2012). Field verification of fungal presence and ditions (Chandler 2017).
killing could be accomplished with short-term culture of fleas and Sampling suggests that Metarhizium is more soil-adapted and
using natural substrate. found commonly in association with plants up to at least 30 cm in
depth. Beauveria, however, has been typically detected closer to the
surface, on foliage, or from a number of plant species as an endo-
Ecological Considerations phyte. In general, roots of some plants tested had a positive effect
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Insect pathogenic fungi are ubiquitous (Rehner and Buckley 2005). on germination of both fungi (Jaronski 2007). Generally, these fungi
However, when soil surveys are performed, sampling bias likely are aerobic and seem to do better in acidic soils assuming reduced
underestimates the occurrence of Metarhizium and Beauveria. biological competition (Jaronski 2007). These soil preferences con-
Insufficient sampling and core samples routinely taken at < 30 cm trast with soil bacteria that may produce fungistatic agents (or like
depth may not capture all fungus residents if present (Zimmermann alkaline soils generally; Jaronski 2007). One possibility is that acidic
2007a, b), especially at many rodent burrow depths (e.g., prairie dog conditions might improve access to Ca and P. Clay soil minerals may
nests are sometimes ≥2 m underground; Verdolin et al. 2008). At pre- facilitate growth of soil bacteria (Vega 2018) and fungi (Stotzky
sent, some ~700–1000 species of insect pathogenic fungi are known and Rem 1966), which in turn become antagonists or competitors
(Lacey 2017a, b, Faria and Wraight 2007). In reviewing natural soil to an introduced insect pathogenic fungus. Conversely, some elem-
levels (colony-forming units [CFU] g−1 of soil) of Metarhizium and ents may provide toxicity (aluminum, manganese, nickel, iron, and
Beauveria, habitat differences likely have influenced isolate counts. silica; Stotzky and Martin 1963, Stotzky and Rem 1966, Jaronski
Further, assay technical issues, host numbers, the occurrence of pred- 2007, Vega 2018), warranting more systematic study (Stotzky
ators feeding on fungi, competition, sampling bias, soil tillage, chem- 1973). Even so, neither soil type nor pH seem to remarkably impact
ical or fertilizer applications, and inter-fungal interactions may have detection rates of these species (Stotzky 1973, Keller et al. 1989,
influenced study counts (Scheepmaker and Butt 2010). In general, Jaronski 2007). Clay in the soils may protect fungal blastospores
insect bioassays appear to detect a fewer number of organisms com- from amoebic and bacterial attack (Jaronski 2007). However, for
pared to soil culture (Jaronski 2007). continued fungal viability, soil clay content appeared less important
Beauveria isolates are reported from many habitats, including than other sometimes ill-defined biotic factors (Bidochka et al. 1998,
above the Arctic Circle, in the tropics, in forested areas, in woodlands, Jaronski 2007). The presence of biotic inhibitors appears to exhibit
and in agricultural areas (Chandler et al. 1997). Beauveria has also a very important fungistatic role that is removed when insect chitin
been isolated from many locales including: South Korea, Denmark, is encountered (Jaronski 2007).
Iraq, United Kingdom (Chandler et al. 1997), Palestine, Mexico Ecologically, carbon sources are very limited in the soil when
(Pérez-González et al. 2014), Morocco, Finland, China, Canada, there is no plant-enriched rhizosphere; in contrast, insects are a rich
and Spain (Vega et al. 2009) and is thought to be found worldwide source and likely serve as a preferred fungal carbon source. Similarly,
(Lacey 2017a, b). Metarhizium is also widely distributed around the essential nutrients (e.g., minerals and nitrogen) may be less access-
world (Snow 1893), but was generally found in warmer locales, was ible in soil than from insects (Reisinger et al. 1977, Bidochka et
potentially more tolerant of agricultural practices (Jaronski 2007). al. 1998, Behie et al. 2012). Evidence from the study of wild-type
Metarhizium has been isolated from Canada, European countries, Beauveria from the Arctic and forested temperate areas, when com-
South America, Australia, and New Zealand. Metarhizium appeared pared to commercial agricultural products, suggests these former
dominant from sites in Denmark, suggesting a possible niche pref- isolates are more cold adapted and retained greater UV light sen-
erence in some settings (Meyling and Eilenberg 2006); reports from sitivity, indicating a degree of regional strain adaptation (Sasan and
other sites tested from the eastern United States and Canada (e.g., Bidochka 2012).
Inglis et al. 2019) yielded similar results, suggesting a more general In general, Beauveria and Metarhizium are dark adapted and ex-
phenomenon of niche-related abundance. Likewise, insect-baiting hibit no phototropism (or growth in response to light); even so, some
studies identified sites in northern Italy where Beauveria dominated suggestions of beneficial light effects are reported (Bidochka et al.
(Jaronski 2007). These differences could also reflect sampling biases 2002, Rangel et al. 2011). Likewise, selected isolates may exhibit
and culture methods as well (Jaronski 2007). more tolerance to UV (Jaronski 2007). Overall, UV exposure has
Overall, Metarhizium and Beauveria are considered ubiquitous a significant negative effect on how long insect pathogenic fungal
(Vega et al. 2009), and under natural conditions and depending spores remain viable (Keller et al. 1989). Humidity and favorable
on local strain fitness, usually range in concentration from 101 temperatures remain major drivers for fungal infection and repro-
to 105 conidial spores g−1 of soil (Zimmermann 2007a, b). Based duction (Keller et al. 1989, Jaronski 2007, Dias et al. 2020, Jaronski
on aggregation of data in 2010 from all published studies to that 2010). Rodent burrow systems may favor longer fungal retention
date, high natural levels of Metarhizium and Beauveria approxi- as a result, because they tend to remain wetter and cooler than the
mate 1000 CFU g−1 soil (Scheepmaker and Butt 2010). After many surface surroundings (Shenbrot et al. 2002); this is even more im-
applications, Beauveria returned to normal background levels in portant in the dry climates prevalent over much of the western US
0.5–1.5 y, whereas the equivalent time for Metarhizium was >10 y, where plague fleas are found. Sustained temperatures over 37°C will
although a number of factors affected the actual longevity of any prevent growth and eventually kill the fungi, while low relative hu-
particular application (Scheepmaker and Butt 2010). Generally, midity (6 Journal of Integrated Pest Management, 2021, Vol. 12, No. 1
2007a, b). For Metarhizium, a relative humidity of 90% or less in- immunosuppressive conditions in captivity, or during importation
hibited germination completely (Snow 1893). These findings suggest (Georg et al. 1963, Müller-Kögler 1967, Fromtling et al. 1979, Lacey
limited fungal proliferation outside the burrow environment, espe- 2017a, b, Schmidt et al. 2018).
cially when coupled with UV exposure on soil or foliar surfaces, Collateral effects are difficult to predict completely. For applica-
suggesting reduced effects on non-target species outside burrows, tors, following the label instructions, wearing proper personal pro-
including humans. tective equipment (PPE), avoiding down-wind exposure, avoiding
spillage, and applying liquid suspensions (where possible) instead of
spore powders could reduce the exposure risks. Typical PPE require-
Human and Animal Exposure Risks ments, as specified on the labels, include wearing a long-sleeved shirt,
Risks posed to vertebrate animals from the commercial production long pants, protective eyewear (Bilgo et al. 2019), waterproof gloves,
and use of Metarhizium (Snow 1893) and Beauveria (Angel-Sahagún and shoes with socks. In addition, mixer/loaders and applicators are
et al. 2010) were recently reviewed and both agents were found to required to wear a dust/mist filtering respirator of at least N-95,
be relatively safe during commercial use, after extensive testing R-95, or P-95 rating. Several of the labels mention that ‘repeated
as required for US EPA registration (Revankar et al. 1999, Amiel exposure to high concentrations of microbial proteins can cause al-
Downloaded from https://academic.oup.com/jipm/article/12/1/30/6358184 by guest on 04 December 2021
et al. 2008, Marsh et al. 2008, Wu et al. 2016). Although not well lergic sensitization’ which is a potential concern beyond the inherent
documented, allergic reactions appear possible and experimental safety of these fungi (De García et al. 1997, Kisla et al. 2000, Tu and
exposure studies have been conducted (Supp Tables S1 and S2 [on- Park 2007, Pariseau et al. 2010, Oya et al. 2016).
line only]). Because their natural temperature maximum is around
30°C, it has been generally assumed to be of low risk in endotherms,
verified by the absence of vertebrate infectivity via oral, pulmonary, Summary
and parenteral routes, and demonstrated by the Beauveria and Biological control of fleas with insect pathogenic fungi might be
Metarhizium strains registered for use in OECD countries. Isolated used for plague mitigation under an IPM strategy. Several strains of
Metarhizium infections, in immunocompromised individuals, have the insect pathogenic fungi Beauveria and Metarhizium are commer-
been reported (Burgner et al. 1998, Revenkar et al. 1999, Amiel cially available in the United States and may represent cost-effective
et al. 2008, Marsh et al. 2008, Wu et al. 2016) and systemic human and environmentally benign approaches to flea and plague control;
cases involved immunocompromised individuals (Muir et al. 1998, these fungi are self-replicating under favorable conditions such as
Marsh et al. 2008, Revenkar et al. 1999). Spontaneous case studies the presence of adequate nutrient sources (fleas), lower temperat-
of Metarhizium infection in ectotherms have been conducted with ures, and the high humidity within many rodent burrows. Likewise,
animals such as exotic lizards (Schmidt et al. 2017a, b, Klasen et al. burrow applications are anticipated to be self-limiting in the envir-
2019) and in two alligators under captive care with unknown im- onment when competition for resources or harsh conditions limit
mune status (Fromtling et al. 1979, Hall et al. 2011). A single report survival. Biological agents appear less prone to resistance develop-
of Metarhizium rhinitis was reported in a cat (Muir et al. 1998). ment than chemical insecticides. Homemade formulations of either
Isolated cases of contact lens wearers developing treatable fungal fungus that may be made for experimental purposes are not allowed
keratitis have been reported (i.e., cornea inflammation; Austwick by law (FIFRA) for commercial use, however. Theoretically, there is
and Keymer 1981, Low et al. 1997, Pariseau et al. 2010, Oya et al. a small risk of unpredictable collateral effects with in-burrow ap-
2016). Reported cases of ocular infections were assumed to be from plications; these fungi have been used worldwide in a wide array
immunocompetent individuals (Kisla et al. 2000, Dorin et al. 2015, of settings without identifiable adverse ecological consequences.
Wu et al. 2016). Eye involvement typically reflects lower temperat- Collateral damage to the local microbiota cannot be discounted,
ures on the eye surface favoring the fungus, a possible predisposition as with the use of chemical agents, but is possibly minimal given
in contact lens wearers, or following ocular steroid use (De García the numbers of introduced fungus propagules relative to the overall
et al. 1997). All cases appeared to involve the wild-type organism microbial population in the surrounding environment. The flea
and had no direct connection to agricultural applications or strains killing persistence of insect pathogenic fungi through time is not
(Revankar et al. 1999, Marsh et al. 2008, Dorin et al. 2015, Eguchi well established for burrow applications and must be considered
et al. 2015, Wu et al. 2016). These risks while real must be com- to understand the true costs involved with their use. Future studies
pared to the risks of applying chemical alternatives. During agri- may consider applications of these entomopathogenic fungi to ro-
cultural production, Beauveria and Metarhizium have been applied dent burrows, their potential impacts on plague vector flea popula-
over large areas during aerial spraying without reported ill-effects tions, and the potential costs and benefits to wildlife conservation
(Exosect 2019). and public health.
Beauveria has systemically infected immunosuppressed patients,
albeit rarely (Jani et al. 2001, Tucker et al. 2004). A very limited
number of case reports regarding Beauveria keratitis in apparently Supplementary Data
healthy people have been published (Henke et al. 2002, Oh et al. Supplementary data are available at Journal of Integrated Pest
2009, Pariseau et al. 2010), but others cases appeared secondary to Management online.
immunosuppressive disease (Tucker et al. 2004, García et al. 2011,
Mitani et al. 2014, Oya et al. 2016), eye procedures (Figueira et al.
2012), or contact lens use (Tu and Park 2007, Ogawa et al. 2016); Acknowledgments
none are known to directly result from agricultural broadcast appli- We thank J. Bowser for his contributions to Jaronski’s sampling of fleas and
cations (Henke et al. 2002, Tucker et al. 2004, Tu and Park 2007, fungi from South Dakota and E. Clifton, S. Wu, and two anonymous reviewers
Oh et al. 2009, Pariseau et al. 2010, Figueira et al. 2012, Oya et al. for constructive comments and suggestions on the manuscript. Any use of
2016, Ogawa et al. 2016). Reports of Beauveria in turtles, giant tor- trade, firm, or product names is for descriptive purposes only and does not
toises, and a single alligator have been reported, and seem to reflect imply endorsement by the U.S. Government.Journal of Integrated Pest Management, 2021, Vol. 12, No. 1 7
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