Revisao Controle Biológico de Acaros

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Fungal Biocontrol of Acari

a a b
D. Chandler , G. Davidson , J. K. Pell , B. V.
b b a
Ball , K. Shaw & K. D. Sunderland
a
Department of Entomological Sciences ,
Horticulture Research International ,
Wellesbourne, Warwick, CV35 9EF, UK
b
Department of Entomology and Nematology ,
IACR Rothamsted , Harpenden, Herts, AL5 2JQ, UK
Published online: 28 Jun 2010.
To cite this article: D. Chandler , G. Davidson , J. K. Pell , B. V. Ball , K. Shaw & K.

D. Sunderland (2000) Fungal Biocontrol of Acari, Biocontrol Science and Technology,
10:4, 357-384, DOI: 10.1080/09583150050114972
To link to this article: http://dx.doi.org/10.1080/09583150050114972
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Biocontrol Science and Technology (2000) 10, 357 ± 384
REVIEW ARTICLE
Fungal Biocontrol of Acari
D. CHANDLER, 1 G. DAVIDSON, 1 J. K. PELL, 2 B. V. BALL, 2 K. SHAW 2

and K. D. SUNDERLAND 1
1
Department of Entomological Sciences, Horticulture Research International,
Wellesbourne, Warwick CV35 9EF, UK; 2 Department of Entomology and
Nematology, IACR Rothamsted, Harpenden, Herts AL5 2JQ, UK
(Received for publication 30 September 1999; revised manuscript accepted 29 February 2000)
Mites and ticks are susceptible to pathogeni c fungi, and there are opportunitie s to exploit these
micro-organism s for biologica l control. We have collated records of 58 species of fungi infecting
at least 73 species of Acari, either naturally or in experiments. Fungal pathogens have been
reported to kill representatives of all three orders of the Actinotrichida (the Astigmata, Oribatida
and Prostigmata) and the Ixodida and Mesostigmata in the Anactinotrichida . Most reports
concern infections in the Prostigmata, particularly in the families Tetranychida e and Eriophyi-
dae. Two species of Acari-speciWc pathogensÐ Hirsutella thompsonii and Neozygites
¯ oridanaÐ are important natural regulators of pestiferous eriophyoi d and tetranychid mites
respectively. Research has been done to understand the factors leading to epizootics of these
fungi and to conserve and enhance natural pest control. Hirsutella thompsonii was also developed
as the commercial product Mycar for the control of eriophyoi d mites on citrus, but was withdrawn
from sale in the 1980s, despite some promising eVects in the Weld. Beauveria bassiana, Metarhiz-
ium anisopliae, Paecilomyce s farinosus, Paecilomyce s fumosoroseus and Verticillium lecanii
infect ixodid ticks in nature, and B. bassiana and M. anisoplia e are being studied as biological
control agents of cattle ticks in Africa and South America. Beauveria bassiana also has potential
as a mycopesticide of the two-spotted spider mite, Tetranychus urticae. There is scope to develop
fungal biocontrol agents against a range of acarine pests, both as stand-alon e treatments and for
use in integrated pest management. Further research is required to clarify the taxonomic status
of fungal pathogens of Acari, to study their ecosystem function, and to develop eYcient mass
production systems for species of Hirsutella and Neozygites.
Keywords: Acari, entomopathogenic, fungi, mites, ticks, Tetranychidae, Eriophyidae, Ixodida,

Beauveria, Hirsutella, Metarhizium, Neozygites, Paecilomyces, Verticillium, biologica l control
INTRODUCTION
The Acari (mites and ticks) exploit a wide range of trophic niches, and some species are
pests of agricultural , veterinary and medical importance. Acarine pests have been controlled
Correspondence to D. Chandler. E-mail david.chandler@hri.ac.uk
ISSN 0958-3157 (print)/ISSN 1360-047 8 (online)/00/040357-28 2000 Taylor & Francis Ltd
358 D. CHANDLER ET AL.
widely with chemicals (Gratwick, 1992). However, the onset of pesticide resistance in some
key pest species (Cranham & Helle, 1985; Messing & Croft, 1996; Hoy, 1998), and public
concerns about the environmenta l impact and safety of chemical applications, are driving
research into alternative, sustainabl e methods for their control, including biologica l control.
Fungi are important natural enemies of arthropods and can be used for biologica l control.
Most attention has been given to fungal pathogens of insects, which are widespread in nature
and are being exploited to control pests through introduction and augmentation . Less atten-
tion has been given to the exploitation of fungal pathogens for the control of acarine pests.
There are, however, a range of fungal species which attack Acari and which can be used for
biologica l control. In this article, we review the biology of fungal pathogens of Acari, docu-
ment research into their development for biological control, and highlight opportunitie s for
further research and exploitation . A brief account of acarine classi® cation and biology is
included for the bene® t of mycologists, who may be unfamiliar with acarology. Similarly, we
have also included a section on fungal classi® cation for the bene® t of acarologists.
CLASSIFICATION OF THE ACARI

The host range of a pathogen can be determined, in part, by the phylogeny of its hosts.
Hence, understandin g acarine taxonomy could be crucial to the rapid identi® cation of a
mycopathoge n of acarine pests. Unfortunately, the taxonomic relationship s within the Acari
have yet to be resolved with certainty. We have based our review on Evans’ (1992)
classi® cation, in which the Acari (a monophyletic subclass of the Arachnida) comprises two
superorders, subdivided into three and four orders respectively:
Subclass Acari
Superorder Actinotrichida Superorder Anactinotrichida
Order Astigmata Order Holothyrid a
Order Oribatida Order Ixodida ( 5 Metastigmata)
Order Prostigmata ( 5 Trombidiformes) Order Mesostigmata
Order Notostigmata ( 5 Opilioacariformes)
The diversity and function of the assemblages are summarised brie¯ y in Table 1. Comparative
spermatologica l studies indicate a wide separation of the two superorders (Alberti, 1984).
Conventionall y, the Astigmata and Oribatida are thought to constitute sister orders within
the Actinotrichida and are described collectively as the Sarcoptiformes, although recent
evidence suggests that the Astigmata may form a subgroup within the Oribatida (Norton,
1998). The Holothyrida, Ixodida and Mesostigmata form sister orders within the Anactino-
trichida and are described collectively as the Parasitiforme s. There is a developing consensus
on the ordinal and subordinal phylogeny of the Actinotrichida, but that of the Anactinotrich-
ida remains unresolved (Evans, 1992). Other descriptions of the taxonomy of the Acari can
be found in Lindquist (1984) and Walter et al. (1996).
ACARI AS PESTS OF AGRICULTURAL, MEDICAL AND VETERINARY IMPORTANCE

Most species of Acari have no detrimental impact on humans. Indeed many perform vital
functions within natural and managed ecosystems as decomposers and predators. However,
there are still a large number of acarine species which have a negative impact on people,
either directly or through damage to crops or livestock. A brief summary of the pest status
of the diVerent acarine orders is given in Table 2, and detailed reviews can be found in Helle
and Sabelis (1985a,b) , Sonenshine (1993), Hill (1994) and Lindquist et al. (1996).
Most acarine pests of crops are contained within the Prostigmata (Actinotrichida), espe-
cially the Eriophyidae and the Tetranychidae, which are obligate plant feeders. Members of
these groups attack a wide range of cultivated plants including pome fruits, citrus, currants
FUNGAL BIOCONTROL OF ACARI 359
TABLE 1. Acari ± biodiversity and ecosystem function
Superorder Order Description
Actinotrichida Astigmata Two ecomorphological divisions: (i) the Acaridia, comprising free
(ca. 300 families, living scavengers (many in bird nests or mammal dens), pests of
ca. 30 000 known stored products, and species associated with arthropods; (ii) the
species) Psoroptidia, mainly commensals or ectoparasites (feeding on skin
and feathers/fur) of birds and mammals.
Oribatida Six suborders, mainly detritivores inhabiting soil and leaf litter.
Highly abundant and probably play a key role in decomposition and
nutrient cycling.
Prostigmata Seven suborders, most are free living predators and some are
parasites of arthropods, molluscs and vertebrates. Members of the
families Tetranychidae and Eriophyidae (suborder Rhaphignathina)
are obligate plant feeders, and include some important crop pests.
Anactinotrichida Holothyrida Three families (14 species), inhabit soil and leaf litter, most are
(ca. 75 families, thought to be predacious.
ca. 11 000 known
species) Ixodida Parasites of a wide range of vertebrates. Two main familial groupings
within the Order: (i) the Argasidae, comprising soft bodied ticks,
often located on hair or in the den of the host; (ii) the Ixodidae,
comprising hard bodied ticks that feed on blood. Vectors of a wide
range of diseases and important pests of man and livestock.
Mesostigmata Ecologically diverse group comprised of 12 suborders. Includes free
living and phoretic species in litter, decaying material, nests etc.
Many species are predacious ± members of the Phytoseiidae are
predators of phytophagous mites, especially the Tetranychidae. Other
species show a range of associations with arthropods and vertebrates,
including obligate parasitism. Some species are pests of livestock and
honeybees.
Notostigmata Single family (eight genera) ± mainly scavengers (detritivores)
inhabiting soil and leaf litter.
and berries, vegetables, cereals, coconut, cassava, sugarcane, and ornamentals (Hill, 1994).
The Tetranychidae feed by piercing the epidermal tissue of the host plant and feeding from
cells of the palisade layer and the spongy mesophyll (Bondada et al., 1995; Warabieda et al.,
1997). Once considered to be of secondary importance, they have become serious pests because
of their capacity to develop resistance to pesticides. Pesticide resistance has been observed in
at least 17 species of tetranychids, with multiple resistance in six species (Cranham & Helle,
1985). In the case of the two-spotted spider mite, Tetranychus urticae, attacking glasshouse
crops and many outdoor crops, this has forced a change from chemical to biologically-base d
control using predatory phytoseiid mites (Hussey & Scopes, 1985; Coop & Croft, 1995).
Elsewhere, e.g. on apples and citrus, control of tetranychids has moved increasingly to integ-
rated pest management strategies that conserve natural enemies (McMurtry, 1985; Hardman
et al., 1995; Croft & Slone, 1998; Lester et al., 1998). In Africa, the exotic cassava green mite,
Mononychellu s tanajoa, introduced accidentally from South America, is a major threat to
cassava production (Yaninek & Herren, 1988). Programmes to control the pest are based on
the introductio n of predatory mites as classical biocontrol agents (Yaninek et al., 1993), but
mite pathogeni c fungi are also being evaluated (Yaninek et al., 1996).
The Eriophyidae are second in importance to the Tetranychidae as phytophagous pests,
but still contain some economically important species. Of the ca. 3000 known species of
eriophyoid mites, some 40 species are considered major pests (Lindquist et al., 1996).
Eriophyoid mites cause the formation of galls on leaves and buds and browning or russeting
on leaves and fruit. Some species transmit viruses. The wheat curl mite, Aceria tulipae, for
TABLE 2. Acarine pests of agricultural, veterinary and medical importance
Superorder Order Pest status
Actinotrichida Astigmata Generally minor pests. The group includes pests of stored products
such as the ¯ our mite, Acarus siro, and cheese mites, Rhizoglyphus
spp. The bulb mite, Rhyzoglyphu s echinopus, is a pest of bulbs,
including onion, and mushrooms. The skin parasite Sarcoptes scabiei
causes scabies on humans and mange on animals. The dust mite
Dermatophagoide s pteronyssinus is widespread in houses and causes
asthma and allergies in humans.
Oribatida No major pests. Some species act as intermediate hosts for cestode
parasites.
Prostigmata The Eriophyidae contains ca. 40 species that signi® cantly aVect crop
production. Some of the more important species include: the apple
rust mite, Aculus schlechtendali; the citrus bud mite, Aceria sheldoni;
the citrus rust mite, Phyllocoptrut a oleivora; the tomato russet mite,
Aculops lycopersici; the coconut mite, Aceria guerreronis; the wheat

curl mite, Aceria tulipae.
The Tetranychidae contains ca. 20 species of important crop pests
which, together, cause more economic damage than the Eriophyidae.
Important species include: the two-spotted mite, Tetranychus urticae;
the six spotted mite, Eotetranychus sexmaculatus; the Banks grass
mite, Oligonychus pratensis; and the green cassava mite,
Mononychellus tanajoa.
The Tarsonemidae contains a few species that are crop pests. Key
species are: the broad mite, Polyphagotarsonemu s latus; the
strawberry mite, Tarsonemus pallidus; and the sugarcane stalk mite,
Stenotarsonemus bancrofti.
Anactinotrichida Holothyrida No major pests, although Holothyrus coccinella can cause a toxic
reaction in poultry.
Ixodida The Order contains over 100 species that are important pests of man
and livestock. Members of the Ixodida transmit more blood-borne
diseases than all other arthropods. A number of ticks cause zoonoses.
Key genera include Ixodes, Ripicephalus, Amblyomma, Dermacentor
and Boophilus.
Mesostigmata The Mesostigmata contains a small number of important pests. The
red poultry mite, Dermanyssus gallinae (Dermanyssidae), is a vector
of viruses to domestic fowl. The tropical rat mite, Ornithonyssus
bacotic (Dermanyssidae), is an ectoparasite of rats and humans. The
varroa mite, Varroa jacobsoni (Varroidae) is a major pest of honey
bees.
Notostigmata No pest species.
example, is the vector of the highly destructive wheat streak mosaic rymovirus, which is
widespread in the grain belts of the USA and Canada (Styer & Nault, 1996). Elsewhere,
eriophyoid mites are important pests of crops such as grapes (Duso, 1993), pome fruit
(Easterbrook, 1984), citrus (McCoy, 1996) and coconut (Moore & Howard, 1996). Messing
and Croft (1996) have reported pesticide resistance in six species of eriophyoi d mite, with
multiple resistance in four species.
The Ixodida (Anactinotrichida ) are blood feeding ectoparasites of vertebrates, and are
important pests of humans and domesticated animals. There are two major grouping s within
the order; the Argasidae and the Ixodidae. The Argasidae are soft bodied, cosmopolitan
parasites of terrestrial vertebrates and feed on a wide range of hosts, often being found on
the hair or nest of the host animal. They include the fowl tick, Argas persicus, a disease
vector of domesticated birds in the tropics, and the genus Ornithodorus, some members of
which attack domesticated birds and mammals (Hill, 1994). The Ixodidae are biologicall y
more diverse than the Argasidae (650 spp. compared to 170) and the more important group
in economic terms. They are hard bodied but possess an integument which distends
considerably during feeding. They are highly fecund, eggs being laid on or near the ground,
and neonate larvae climb onto vegetation to attach to passing hosts. The most common life
cycle involve s detachment from the host between moults. Tick-borne diseases include a
paralysis caused by toxins secreted during feeding (Stone et al., 1989), but they are principally
vectors of pathogeni c micro-organism s and transmit a wider variety of infectious diseases
than any other group of blood feeding arthropods (Sonenshine, 1993). Ticks transmit
diseases to humans, many as a result of zoonotic associations, and constrain livestock
production throughou t the world. The genera which have most impact on humans and
livestock are Amblyomma, Boophilus, Dermacentor, Ixodes, and Rhipicephalus. Tick-borne
diseases of humans include Lyme disease, transmitted by Ixodes ricinus in Europe and
Ixodes dammini in North America (Lane et al., 1991), Colorado tick fever (Dermacentor
andersoni) and tick-borne encephalitis (I. ricinus) (Sonenshine, 1993). Diseases of livestock,
particularly cattle, include babesioses such as Texas cattle fever (Boophilu s annulatu s) and
louping ill (I. ricinus), a viral disease of sheep in the UK (Sonenshine, 1993). Pesticide
resistance is developin g in some tick species, for example strains of Boophilu s microplus have
been reported with resistance to organophosphat e and pyrethroid acaricides (Brun, 1992;
Wright & Ahrens, 1989; Rosario-Cruz et al., 1997).
Acarine pests of domestic animals are also to be found in the Mesostigmata (Anactinotrich-
ida). Of the 12 suborders, the Dermanyssina is the most species rich and biologicall y diverse
group, and it contains free living members as well as parasitic and paraphagic species on
arthropods and vertebrates. Members of the family Dermanyssidae are blood-feedin g ectopar-
asites, and include pests such as the red poultry mite Dermanyssus gallinae, a vector of disease
in domestic fowl, and the tropical rat mite Ornithonyssus bacotic, which feeds on humans and
rodents (Hill, 1994). Varroa jacobsoni (Dermanyssina: Varroidae) is a pest of honey bees
which has severely depleted population s of managed and feral population s of Apis mellifera
around the world (De Jong et al., 1982; Allen-Wardell et al., 1998). However, the Dermanys-
sina also includes the Phytoseiidae, which are predators of phytophagou s mites, especially the
Tetranychidae, and species of the genera Typhlodromus, Amblyseius and Phytoseiulus are used
widely as biocontrol agents of phytophagous mites on protected and unprotected crops.
CLASSIFICATION OF THE FUNGI

Fungi exhibit high levels of parallel and convergent evolution in their structure and physiolog y
(Cooke & Whipps, 1993) and their evolutionar y relationships are therefore best understood
using DNA-based methodologies. Indeed, the phylogenetic s of the fungi have undergone
considerable revision in recent years with the introduction of molecular techniques to tax-
onomy, and while the overall picture appears to be falling into place, considerabl e work
remains to be done (Berbee & Taylor, 1999). This review concerns members of the true fungi
which kill insects and mites. A range of eukaryotic micro-organisms are also studied by
mycologists, but are no longer classi® ed with the Fungi. Of these, Lagenidium spp. (Strameno-
pila, Oomycota) are noteworthy as pathogens of mosquito larvae (Tanada & Kaya, 1993).
The kingdom Fungi is a monophyletic assemblage which at present comprises four phyla:
Chytridiomycota , Zygomycota , Basidiomycota, and Ascomycota (Berbee & Taylor, 1999).
Approximately 70 000 species have been described, although the true number may be closer
to 1.5 million (Hawksworth, 1991; Hawksworth et al., 1995). Fungi play major roles in
ecosystems as decomposers, pathogens, and symbionts. The Chytridiomycot a and Zygomy-
cota (collectively termed the coenomycetes) are usually placed at the base of the clade and
comprise ca. 3% of extant fungal species (Berbee & Taylor, 1999). These two groups share
common features, most notably the absence of cross walls in hyphae, but the Chytridiomycot a
are distinguishe d by the production of motile, ¯ agellated zoospores. However, nucleotide

sequence analysis of entomophthoralean and trichomycete species indicates that this separa-
tion does not re¯ ect phylogeny (Nagahama et al., 1995) and revision may be required. The
coenomycetes include saprotrophs, plant and animal pathogens, and symbionts, most
notably the Glomales (Zygomycota ) which contain arbuscular mycorrhizal fungi. The
Chytridiomycot a contain few entomopathogeni c species, but include two genera
(Coelomomyces and Coelomycidium) that kill the larvae of haematophagou s Diptera and
have been studied for the biocontrol of mosquitoes and black ¯ ies (Tanada & Kaya, 1993).
The Entomophthorale s (Zygomycota ) include some important obligate entomopathogen s
that cause natural epizootics in a range of agricultural pests, and contain some key species
that cannot be grown readily in vitro (McCoy et al., 1988). The most widely studied
genera of entomophthoralean fungi, associated with pest control, include Conidiobolus,
Entomophthora, Erynia and Neozygites.
The Ascomycota and Basidiomycot a (collectively termed the dikaryomycetes ) grow as hap-
loid yeasts, hyphae, or both, and are characterised by hyphal cross walls (septa) and the
abundan t production of propagule s. Meiotic spores are often produced within fruiting bodies.
Hyphal fusion of compatible mating types can lead to nuclei of diVerent karyotype s existing
in the same, haploid organism (heterokaryosis) . The Basidiomycota comprise ca. 35% of
described fungi (Berbee & Taylor, 1999) and include saproptrophs, ectomycorrhiza, and plant
pathogens, most notably rusts and smuts. They also include a limited number of entomopatho-
gens (McCoy et al., 1988). The Ascomycota comprise some 45% of known species and are
distinguishe d structurally from the Basidiomycota by the anatomy of their fruiting bodies.
The Ascomycota contain many of the major plant pathogens and, together with the Mitosp-
oric fungi (see below), they also constitute the majority of the entomopathogens. The Laboulb-
eniales (Ascomycota) comprise a large number of commensal species that are con® ned to the
exoskeleton of insects. Entomopathogeni c Ascomycota are most common in tropical latitudes
and are well represented in tropical forest habitats, especially on scale insects, white¯ ies, and
ants (Evans, 1989). Some 20% of species of septate fungi have no known sexual phase and
thus have been diYcult to classify on morphologica l characteristics alone. They are generally
referred to as Deuteromycota or Mitosporic fungi (the preferred term in this review) (Hawk-
sworth et al., 1995), although nucleotide sequence analysis suggests that the majority belong
to the Ascomycota (Berbee & Taylor, 1999). The Mitosporic fungi include many species of
saproptrophs, plant pathogens, and also many of the most important entomopathogens. The
true aYnities of most of these entomopathogen s have yet to be resolved and hence, for
this review, we continue to refer to them as Mitosporic fungi. Members of the Mitosporic
entomopathogen s are the most widely used for biologica l pest control, and important genera
include Beauveria, Metarhizium, Paecilomyces, and Verticillium. These fungi have global dis-
tributions and can be mass produced readily. Over 15 mycopesticides, formulated from these
genera, are available commercially for the management of a range of pests in the Homoptera,
Coleoptera, Lepidoptera, Diptera, and Orthoptera (Shah & Goettel, 1999).
ACAROPATHOGENIC FUNGI AND THEIR USE IN BIOCONTROL

Pathogens of arthropods are represented in all the major groups of fungi. Approximately
750 species of fungi in 56 genera are known to be pathogens or parasites of arthropods
(Hawksworth et al., 1995). Most species are in the Entomophthorale s (Zygomycota) ,
Ascomycota, and the Mitosporic fungi. These groups also contain the most virulent fungal
pathogens of insects and Acari, all of which are transmitted horizontally. The fungal
pathogens of Acari (`acaropathogenic ’ fungi) probably form a functional subgroup within
the entomopathogeni c fungi, occurring in the same phylogenetic assemblages as the latter,
but being less diverse (Poinar & Poinar, 1998). A number of species, e.g. Hirsutella thompsonii
(Mitosporic fungi) and Neozygites Xoridana (Entomophthorales ) are speci® c to Acari
whereas other species of entomopathogeni c Mitosporic fungi kill both Acari and insects.
Entomopathogeni c fungi usually infect their hosts through specialised spores which attach
to, germinate on, and penetrate the integument. The penetrating fungus multiplies within the
haemocoel and soft tissues of the host, and death occurs usually within three to ten days after
infection by water loss, nutrient deprivation , gross mechanical damage and the action of
toxins. Under favourabl e conditions, the fungus sporulates extensively on the cadaver to
facilitate further infections in the host populatio n and thus continue the disease cycle. Com-
prehensive accounts of the infection processes, patholog y and epizootiolog y of entomopa-
thogenic fungi are given by Tanada and Kaya (1993), St Leger (1993) and Hajek and St
Leger (1994). The infection cycles of the two main groups of interest to this reviewÐ the
Entomophthorale s and the Mitosporic fungiÐ have basic similarities. However, the entom-
ophthoralea n fungi exhibit a wide array of ecomorphologica l adaptation s to the life cycles of
their hosts, whereas the entomopathogeni c Mitosporic fungi (with the probabl e exceptions of
Hirsutella spp. and Verticillium lecanii) tend to operate more opportunistically (Samson et al.,
1988). Some species of Mitosporic entomopathogen s are thought to consist of a range of
clonal groups, maintained by heterkaryon incompatibilit y mechanisms, which can diVer sub-
stantially in host range and other pathogenicity-relate d characteristics (McCoy et al., 1988;
Hajek & St Leger, 1994). The intraspeci® c phylogenies of these fungi are complex. For
example, Metarhizium anisoplia e exhibits a very high level of inter-isolate variabilit y (St Leger
et al., 1992) but the majority of isolates of this fungus can be grouped into a few geographically
widespread genotypic classes, with the remainder located in many, geographically-localised ,
genotypic classes (Hajek & St Leger, 1994). Geographic proximity is also often accompanied
by close genetic relationship s in M. anisopliae (Leal et al., 1994).
Members of the Entomophthorale s and the Mitosporic fungi have been exploited to
control insect and mite pests by using inoculative releases (often as classical introductions )
(Weseloh & Andreadis, 1992), by habitat manipulatio n to enhance the activity of naturally
occurring fungi (Wilding et al., 1986), and by the applicatio n of inundativ e mycopesticide s.
Mitosporic fungi tend to be favoured as mycopesticides as they can be produced more
readily in bulk than entomophthoralea n fungi. Mycopesticides have proved successful
against a range of pests, particularly where the use of chemical pesticides is inappropriat e
because of the development of resistance or through environmenta l concerns. Examples
include the use of V. lecanii against glasshouse aphids and white¯ ies (Quinlan, 1988),
Metarhizium spp. agains t cockroaches, locusts and termites (Zimmerman, 1993; Harmon,
1994; Bateman, 1997; Milner et al., 1998), and Beauveria brongniarti i to control the
cockchafer, Melolontha melolontha (Keller, 1992).
In theory, Acari make good hosts for fungal pathogens because they are generally soft
bodied and many inhabit environments with humid microclimates (Ferro & Southwick,
1984; Evans, 1992) which favour infection and disease transmission (Hajek & St Leger,
1994). Their small size, however, makes them diYcult to study so it is likely that many
interactions between fungal pathogens and Acari remain undocumented. We have collated
records of 58 species of fungi reported to infect at least 73 species of Acari, both naturally
and in experiments (Table 3). Where possible we have tried to include only causal agents in
the list. However, because these reports include a number of observation s where Koch’s
postulates have not been completed, they may include saprotrophs or weak pathogen s that
have infected weakened or moribund hosts. There are reports of fungal pathogens of all
three orders of the Actinotrichida (i.e. the Astigmata, Oribatida and Prostigmata) and in
the Ixodida and Mesostigmata of the Anactinotrichida . Most reports concern infections in
prostigmatid mites (24 spp. of fungi from 45 hosts), particularly the Tetranychida e (15
spp. of fungi from 21 hosts) and Eriophyidae (9 spp. from 15 hosts). This may in part re¯ ect
the research interests of invertebrate pathologists, who historically have concentrated on the
biology of diseases of crop pests, for biologica l control purposes.
For this review, we have divide d the fungal pathogens of Acari into three functional
groups as follows:
364
TABLE 3. Fungi reported to infect Acari
Acarine host
Origin of fungal
Species of fungus order family species isolate(s) Reference
Ascomycota
Torrubiella sp. Mesostigmata Unidenti® ed Unidenti® ed tick Korea Steinhaus & Marsh, 1962
Zygomycota
Basidiobolus sp. Prostigmata Tetranychidae Tetranychus urticae Former USSR Jegina, 1976* (in van der Geest, 1985)
Conidiobolus brefeldionis Astigmata Acaridae Tyrophagus perniciosus Ð Batko, 1965 (in Lipa, 1971)
Conidiololus chlapowski Mesostigmata Parasitidae Pergamasus sp. Poland Balazy et al., 1987
Conidiololus coronatus Ixodida Ixodidae Ixodes ricinus Czech Republic Samsinakova et al., 1974
Conidiololus obscurus Mesostigmata Phytoseiidae Phytoseiulus sp. Uganda Nyiira, 19821 *
Phytoseiulus persimilis Former USSR Petrova & Petrov, 1976 (in van der Geest, 1985)
Prostigmata Tetranychidae Mononychellus tanajoa Uganda Nyiira, 19821 *
Tetranychus bimaculatus Uganda Nyiira, 19821 *
T. urticae (i) Former USSR (i) Jegina & Cinowskis, 1970 (in van der Geest, 1985)
(ii) Russia (ii) Andreeva & Shternshis, 1995
Conidiololus thromboides Prostigmata Tetranychidae Tetranychus urticae Former USSR Jegina, 1976 (in van der Geest, 1985)
Neozygites sp. Prostigmata Tetranychidae Eotetranychus Ð Selhime & Muma, 1966 (in Lipa, 1971)
( 5 Triplosporium sexmaculatus
5 Entomophthora) Mononychellus sp. Kenya Bartowski et al., 1988
D. CHANDLER ET AL.
Mononychellus tanajoa Brazil Delalibera et al., 1992

Panonychus citri Florida USA Fisher, 1951 (in Lipa 1971)
Tetranychus evansi Brazil Humber et al., 1981
Tetranychus paciWcus California USA Steinhaus & Marsh, 1962
Tetranychus tumidis Florida USA Saba, 1974 (in Bartowski et al., 1988)
Tetranychus turkestani Alabama Carner & Canerday, 1968 2
Tetranychus urticae (i) Alabama USA (i) Carner & Canerday, 1968 2
(ii) S. Carolina USA (ii) Carner, 1976
(iii) N. Carolina USA (iii) Brandenburg & Kennedy, 1981
(iv) Iowa USA (iv) Klubertanz et al., 1991
Trombiculidae Vatacarus sp. Ð Thomas & Poinar, 1973 (in Poinar & Poinar, 1998)
Neozygites acaricida Prostigmata Eupodidae Halotydeus destructor Australia James, 1992
Penthaleidae Penthaleus major Australia James, 1992
Neozygites acaridis Prostigmata Eupodidae Halotydeus destructor Australia Ridsdill-Smith & Annells, 1997
Mesostigmata Macrochelidae Macrocheles peregrinus Australia Milner, 1985 3
Neozygites acarina Prostigmata Penthaleidae Penthaleus major Ð Hastings, 1994
TABLE 3. Continued
Acarine host
Origin of fungal
Neozygites Xoridana Prostigmata Tetranychidae Bryobia sp. Poland Mietkiewski et al., 1993
Eotetranychus sexmaculatus Florida USA Selhime & Muma, 1966*
Eutetranychus banksi Florida USA Weiser & Muma, 1966
Mononychellus tanajoa (i) Benin (i) Yaninek et al., 1996
(ii) Brazil (ii) Oduor et al., 1997
Oligonychus gossypii Benin Yaninek et al., 1996
Oligonychus hondoensis Japan Nemoto & Aoki, 1975
Oligonychus pratensis Kansas USA Dick & Buschman, 1995 4
Panonychus citri Ð Selhime & Muma, 1966 (in Poinar & Poinar,
1998)
Tetranychus cinnabarinus Ð Kenneth, 1983
Tetranychus ludeni India Ramaseshiah, 1971 (in van der Geest, 1985)
Tetranychus urticae (i) N Carolina USA (i) Smitley et al., 1986a*,b
(ii) Switzerland (ii) Keller 1991
(iii) Poland (iii) Mietkiewski et al., 1993
(iv) Taiwan (iv) Shih & Shiue, 1994 4
(v) Kansas USA (v) Dick & Buschman 1995 4
(vi) Israel (vi) Kenneth et al., 1972
Neozygites tetranychi Prostigmata Tetranychidae Tetranychid mites Ð Remaudiere & Keller 1980
Tetranychus urticae Czech Republic Weiser 1968 5
FUNGAL BIOCONTROL OF ACARI
Tarichium azygosporicum Mesostigmata Parasitidae Pergamasus brevicornis Poland Balazy et al., 1987
Tarichium distinctum Mesostigmata Parasitidae Pergamasus sp. Poland Balazy et al., 1987
Tarichium hyalinum Tectocepheus velatus Poland Balazy et al., 1987
Tarichium Mesostigmata Uropododidae Trichouropoda szczecinensis Poland Balazy et al., 1987
monokaryoticum
Tarichium svalbardense Mesostigmata Prodinychidae Dinychus carinatus Poland Balazy et al., 1987
Mesostigmata Parasitidae Pergamasus sp. Poland Balazy et al., 1987
Veigaiidae Veigaia sp. Poland Balazy et al., 1987
Tarichium Mesostigmata Parasitidae Pergamasus sp. Poland Balazy et al., 1987
tenusculpturatum Veigaiidae Veigaia sp. Poland Balazy et al., 1987
Tarichium uropodinis Mesostigmata Trachyuropodidae Trachyuropoda coccinea Poland Balazy & Wisniewski, 1982
Tarichium verruculosum Mesostigmata Celaenopsidae Celaenopsis badius Poland Balazy et al., 1987
Oribatidae Galumnidae Unidenti® ed Poland Balazy et al., 1987
365
366
TABLE 3. Continued
Acarine host
Origin of fungal
Zoophthora radicans Prostigmata Tetranychidae Tetranychus urticae Former USSR Jegina & Cinowskis, 1972 (in van der Geest, 1985)
Mitosporic fungi
Acremonium larvarum Oribatida Unidenti® ed Unidenti® ed Poland Balazy et al., 1987
Acremonium strictum Cymbaeremaeidae Micreremus brevipes Poland Balazy et al., 1987
Prostigmata Tetranychidae Tetranychus sp. Ð Li et al., 1993 6
Aspergillus sp. Ixodida Ixodidae Rhipicephalus appendiculatus Kenya Mwangi et al., 1995
Mesostigmata Varroidae Varroa jacobsoni Brazil Lui & Ritter, 1988
Prostigmata Tetranychidae Mononychellus sp. Kenya Bartowski et al., 1988
Mononychellus tanajoa Benin Yaninek et al., 1996
Aspergillus depauperatus Prostigmata Tetranychidae Tetranychus urticae Ð Charles, 1941 (in Lipa, 1971)
Aspergillus Xavus Ixodida Ixodidae Ixodes ricinus Former USSR Cherepanova, 1964 (in Kalsbeek et al., 1995)
Aspergillus fumigatus Ixodida Ixodidae Dermacentor marginatus Ð Kolomiec, 1950* (in Lipa, 1971)
Hyalomma scupense Ð Kolomiec, 1950* (in Lipa, 1971)
Ixodes ricinus Former USSR Cherepanova, 1964 (in Kalsbeek et al., 1995)
Aspergillus niger Ixodida Ixodidae Ixodes ricinus Czech Republic Samsinakova et al., 1974
D. CHANDLER ET AL.
Aspergillus ochraceus Ixodida Ixodidae Rhipicephalus sanguineus Spain Estrada-Pena et al., 1990
Ixodes dammini Ð ARSEF culture collection 7 ,8
Aspergillus parasiticus Ixodida Ixodidae Ixodes ricinus Czech Republic Samsinakova et al., 1974
Beauveria bassiana Ixodida Ixodidae Amblyomma variegatum Kenya Kaaya et al., 1996*
Boophilus microplus Brazil Verissimo, 1995
Dermancentor sp. Czech Republic Samsinakova et al., 1974
Ixodes ricinus (i) Ð (i) Boicev & Rizanov, 1960 9 (in Jenkins, 1964)
(ii) Czech Republic (ii) Samsinakova et al., 1974 1 0
(iii) Denmark (iii) Kalsbeek et al., 1995
Rhipicephalus appendiculatus (i) Kenya (i) Mwangi et al., 1995*
(ii) Kenya (ii) Kaaya et al., 1996*
Mesostigmata Ascidae Proctolaelaps sp. Poland Balazy et al., 1987
Varroidae Varroa jacobsoni Russia Chernov, 1981*
Prostigmata Eupodidae Halotydeus destructor Ð Ireson & Rath, 1991
TABLE 3. Continued
Acarine host
Origin of fungal
Tarsonemidae Tarsonemus spirifex Ð Oudemans, 1915 (in Lipa, 1971)

Polyphagotarsonemus latus Ð Pena et al., 1996*
Tetranychidae Bryobia rubrioculus Ð Dyadecho, 1958, 1959a,b (in Lipa, 1971)
Mononychellus sp. Kenya Bartowski et al., 1988
Tetranychus urticae (i) Ð (i) Dresner, 19491 1 (in Lipa, 1971)
(ii) Ð (ii) Wright & Kennedy, 1996*
Tetranychus viennensis Ð Dyadecho, 1959 (in Lipa, 1971)
Beauveria brongniartii Ixodida Ixodidae Ixodes ricinus Denmark Kalsbeek et al., 1995
Fusarium sp. Ixodida Ixodidae Boophilus sp. Mexico ARSEF culture collection7
Rhipicephalus appendiculatus Kenya Mwangi et al., 1995
Rhipicephalus sanguineus Ð Lombardini, 1950
Prostigmata Tetranychidae Mononychellus sp. Kenya Bartowski et al., 1988
Mononychellus tanajoa Benin Yaninek et al., 1996
Hirsutella sp. Prostigmata Tetranychidae Mononychellus sp. (i) Kenya (i) Bartowski et al., 1988
(ii) California USA (ii) ARSEF culture collection7
Tydeidae Pronematus sp. Cuba Cabrera & McCoy, 1984
Hirsutella brownorum Unidenti® ed Unidenti® ed Unidenti® ed New York USA ARSEF culture collection7
Hirsutella gregis Prostigmata Eriophyidae Abacarus hystrix UK Minter et al., 1983
Unidenti® ed Unidenti® ed Unidenti® ed Poland Balazy et al., 1987
Hirsutella haptospora Unidenti® ed Unidenti® ed Unidenti® ed Poland ARSEF culture collection7

Hirsutella heteroderae Unidenti® ed Unidenti® ed Soil mite California USA CBS culture collection1 2
Hirsutella kirchneri Prostigmata Eriophyidae Abacarus hystrix UK Minter et al., 1983
Phyllocoptruta oleivora Cuba Cabrera & Dominguez, 1987 (in McCoy, 1996)
Hirsutella necatrix Prostigmata Eriophyidae Abacarus hystrix UK Minter et al., 1983
Tetranychidae Tetranychus cinnabarinus UK Chernin et al., 1997*
Hirsutella nodulosa Mesostigmata Parasitidae Hydrogamasus sp. Bermuda CCFC culture collection1 3
Prostigmata Eriophyidae Aceria guerreronis Cuba Cabrera & Dominguez, 1987b (in McCoy, 1996)
Phyllocoptruta oleivora Cuba Cabrera & Dominguez, 1987a (in McCoy, 1996)
Tarsonemidae Polyphagotarsonemus latus Cuba Cabrera et al., 1987b (in Pena et al., 1996)
Hirsutella rostrata Mesostigmata Ascidae Proctolaelaps sp. Germany Balazy et al., 1987
Digamasellidae Dendrolaelaps tetraspinosus Germany Balazy et al., 1987
367
368
TABLE 3. Continued
Acarine host
Species of Origin of fungal
fungus order family species isolate(s) Reference
Hirsutella Mesostigmata Phytoseiidae Amblyseius peregrinus Ð McCoy & Selhime, 1974 1 4 (in McCoy, 1981)
thompsonii Trachyuropodidae Trachyuropoda coccinea Poland Balazy & Wisniewski, 1982
Prostigmata Eriophyidae Abacarus hystrix UK Lewis et al., 1981
Acalitus vaccinii Carolina USA Baker & Neunzig, 1968
Aceria cynodoniensis USA McCoy, 1981
Aceria guerreronis (i) Ivory Coast (i) Hall et al., 1980 1 5
(ii) Jamaica (ii) Hall et al., 1980 1 5
(iii) Mexico (iii) Lampedro & Luis-Rosas, 19891 5
Aceria sheldoni Zimbabwe McCoy & Selhime, 1974 (in McCoy, 1981)
Aculops lycopersici Cuba Cabrera & McCoy, 1984
Colomerus novahebridensis (i) Philippines Hall et al., 1980
(ii) New Guinea Hall et al., 1980
(iii) New Hebrides Hall et al., 1980
Phyllocoptruta oleivora (i) Florida USA (i) Fisher, 1950
(ii) Surinam (ii) van Brussel 1975 (in McCoy, 1981)
Retracrus elaeis Colombia Urueta 1980 (in McCoy 1996)
Rhynacus sp. Cuba Cabrera et al., 1987
Vasates destructor Cuba Cabrera 1984 (in McCoy 1996)
D. CHANDLER ET AL.
Tarsonemidae Polyphagotarsonemus latus Florida USA Pena et al., 1996

Unidenti® ed tarsonemid mite (i) Cuba (i) Cabrera et al., 1987
(ii) Ð (ii) Rombach et al., 1986
Tetranychidae Dolichotetranychus sp. Sri Lanka Hall et al., 1980
Dolichotetranychus Xoridanus Costa Rica Zoebisch et al., 1992
Eutetranychus sexmaculatus USA McCoy & Selhime, 1974 (in McCoy, 1981)
Eutetranychus banksi USA McCoy & Selhime, 1974 (in McCoy, 1981)
Eutetranychus orientalis Florida USA Gerson et al., 1979*
Mononychellus tanajoa (i) Kenya (i) Odongo et al., 1998*
(ii) Benin (ii) Yaninek et al., 1996
Oligonychus ulicus Florida Gardner et al., 1982
Panonychus citri Florida USA McCoy & Selhime, 1974 (in McCoy, 1981)
Tetranychus cinnabarinus Florida USA Gerson et al., 1979*
Tetranychus turkestani Ð McCoy, 1978* (in Samson et al., 1980)
TABLE 3. Continued
Acarine host
Origin of fungal
Tetranychus urticae Florida USA Gardner et al., 1982*

Hirsutella tydeicola Prostigmata Tydeidae Lorryia formosa Florida USA Samson & McCoy, 1982; Samson & McCoy, 1984
Metarhizium anisopliae Astigmata Acaridae Histiogaster anops N. Carolina USA Schabel, 1982*
Ixodida Ixodidae Amblyomma variegatum Madagascar Kaaya et al., 1996*
Boophilus sp. Mexico & Florida USA ARSEF culture collection 7
Boophilus microplus (i) Ð (i) Bittencourt et al., 1994a,b
(ii) Ð (ii) Verissimo, 1995
(iii) Brazil (iii) Correia et al., 1998*
Ixodes dammini Ð Zhioua et al., 1997 8 *
Rhipicephalus (i) Kenya (i) Mwangi et al., 1995*
appendiculatus (ii) Madagascar (ii) Kaaya et al., 1996*
Mesostigmata Macrochelidae Macrocheles sp. N. Carolina USA Schabel, 1982*
Prostigmata Eupodidae Halotydeus destructor Ð Ireson & Rath, 1991
Paecilomyces eriophyes Prostigmata Eriophyidae Aceria hippocastani UK Leatherdale, 1965*
Cecidophyopsis ribis Ð Lipa, 1971
Eriophyes padi UK Leatherdale, 1965
Tetranychidae Panonychus ulmi UK Leatherdale, 1965*
Parasitidae Pergamasus mediocris Poland Balazy et al., 1987
Oribatida Unidenti® ed Unidenti® ed Poland Balazy et al., 1987
Mycobatidae Mycobates sp. Canada CCFC culture collection 1 3

Paecilomyces farinosus Ixodida Ixodidae Ixodes ricinus Denmark Kalsbeek et al., 1995
Paecilomyces Ixodida Ixodidae Ixodes ricinus (i) Czech Republic (i) Samsinakova et al., 1974
fumosoroseus (ii) Denmark (ii) Kalsbeek et al., 1995
Prostigmata Tarsonemidae Polyphagotarsonemus Ð Pena et al., 1996*
latus
Paecilomyces terricola Prostigmata Tetranychidae Tetranychus cinnabarinus Israel Ben-Ze-ev, 1993
Tetranychus urticae Israel Kenneth et al., 1971
Penicillium insectivorum Ixodida Ixodidae Ixodes ricinus Former USSR Cherepanova, 1964 (in Kalsbeek et al., 1995)
Ramularia ludoviciana Prostigmata Eriophyidae Abacarus hystrix UK Minter et al., 1983
Sporothrix schenckii Prostigmata Eriophyidae Aculus fockeui Germany Schliesske, 1992
Tolypocladium inXatum Oribatidae Mycobatidae Mycobates sp. Canada ARSEF culture collection 7
Tolypocladium niveum Oribatidae Mycobatidae Mycobates sp. Canada CCFC culture collection 1 3
369
370
TABLE 3. Continued
Acarine host
Origin of fungal
Trichothecium roseum Ixodida Argasidae Argas persicus Ð Koval, 1974 (in Balazy et al., 1987)
Ixodidae Dermacentor marginatus Ð Koval, 1974 (in Balazy et al., 1987)
Ixodes ricinus Ð Koval, 1974 (in Balazy et al., 1987)
Ascidae Proctolaelaps sp. Poland Balazy et al., 1987
Verticillium sp. Prostigmata Eupodidae Halotydeus destructor Australia Ridsdill-Smith & Gaull, 1995
Verticillium aranearum Ixodida Ixodidae Ixodes ricinus Denmark Kalsbeek et al., 1995
Verticillium bulbillosum Oribatida Unidenti® ed Unidenti® ed Poland Balazy et al., 1987
Verticillium lecanii Ixodida Ixodidae Ixodes ricinus (i) Czech Republic (i) Samsinakova et al., 1974 1 6
(ii) Denmark (ii) Kalsbeek et al., 1995
Oribatida Unidenti® ed Unidenti® ed Poland ARSEF culture collection 7
Prostigmata Bdellidae Bdellid mite Poland Balazy et al., 1987
Eriophyidae Abacarus hystrix UK Lewis et al., 1981
Cecidophyopsis ribis Ð IMI culture collection1 7
Tetranychidae Tetranychus urticae (i) Netherlands (i) Gams, 1971 (in van der Geest, 1985)
(ii) Ð (ii) Gillespie et al., 1982
D. CHANDLER ET AL.
(iii) Ð (iii) Andreeva & Shternshis, 1995

Eutetranychus orientalis Ð Sewify & Mabrouk, 1990
Verticillium psaliotae Oribatida Schleroribatidae Scheloribates latipes Poland Balazy et al., 1987
Fungi are classi® ed according to Brady (1979a,b), Keller (1991) and Hawksworth et al. (1995). Acari are classi® ed according to Baker & Wharton (1952), Wood (1989),
Sonenshine (1993) and Evans (1992). Preferred names of Acari are taken from Wood (1989) and Sonenshine (1993). Reports are of natural infections, except where indicated
by * which denotes an experimental inoculation of the host in the laboratory or ® eld.
(1) fungus described as Entomophthora thaxteriana ( 5 Conidiobolus obscurus). (2) host described as Tetranychus telarius ( 5 T. urticae). (3) fungus described as Empusa
acaridis ( 5 Neozygites acaridis). (4) fungus described as Neozygites adjarica ( 5 Neozygites Xoridana). (5) host described as Tetranychus althaeae ( 5 T. urticae). (6) fungus
described as Cephalosporium acremonium ( 5 Acremonium strictum). (7) ARSEF (USDA-ARS Collection of Entomopathogenic Fungal Cultures, USA). (8) host described
as Ixodes scapularis ( 5 Ixodes dammini). (9) fungus described as Beauveria cinerea ( 5 Beauveria bassiana). (10) contains one description of B. bassiana and one of Beauveria
tenella ( 5 B. bassiana). (11) includes reference to B. bassiana from T. urticae and T. telarius ( 5 T. urticae). (12) CBS (Centraal Bureau voor Schimmelcultures, Netherlands).
(13) CCFC (Canadian collection of fungal cultures, Canada). (14) host described as Typhlodromalus peregrinus ( 5 Amblyseius peregrinus). (15) host described as Eriophyes
guerreronis ( 5 Aceria guerreronis). (16) fungus described as Cephalosporium coccorum ( 5 Verticillium lecanii). (17) IMI (International Mycological Institute, UK).
(a) Acari-speci® c pathogens (some of which are important natural regulator s of phyto-
phagous mites);
(b) `Nonspecialist’ species of fungi which infect a range of insects and Acari;
(c) `Minor’ species which are rarely reported as pathogens of Acari and have not been
studied for biologica l control.
ACARI SPECIFIC PATHOGENSÐ IMPORTANT NATURAL REGULATORS OF

PHYTOPHAGOUS MITES
Hirsutella thompsonii (Mitosporic Fungi)Ð A Pathogen of Prostigmatid Mites
The taxonomy of Hirsutella is complex and not fully understood (Samson et al., 1988).
Most species are pathogen s of tropical invertebrates (McCoy, 1981) and 10 species kill Acari
(Table 3). Teleomorphs of Hirsutella have been reported as Cordyceps or Torrubiella
spp. (Kendrick & Carmichael, 1973; Samson et al., 1988). The most widely studied member
of the genus is Hirsutella thompsonii (Fisher, 1950), a speci® c pathoge n of Acari (McCoy,
1981). The fungus was ® rst reported as the causative agent of epizootics in the citrus rust
mite, Phyllocoptrut a oleivora (Prostigmata: Eriophyidae ) in Florida (Speare & Yothers, 1924;
Yothers & Mason, 1930; both cited in Samson et al., 1980), and it was ® rst cultured and its
pathogenicit y con® rmed by McCoy and Kanavel (1969). The fungus grows slowly in axenic
culture, vegetative growth being favoured by media rich in carbon while conidiatio n is
promoted by nutrient-de® cient media (McCoy & Kanavel, 1969).
Although it has been observed infecting mesostigmatid mites on two occasions in nature
(McCoy & Selhime, 1974, cited in McCoy, 1981; Balazy & Wisniewski, 1982), H. thompsonii
is normally associated with eriophyoid and tetranychid mites, 22 species of which have been
recorded as hosts (Table 3). In laborator y experiments, an isolate of H. thompsonii originating
from P. oleivora was lethal also to tetranychid mites but would not kill tarsonemid mites
(Prostigmata) or representatives of the Astigmata, Oribatida, Mesostigmata or Ixodida
(Gerson et al., 1979). However, laborator y infection in a tarsonemid, Polyphagotarsonemus
latus, has been documented using a tarsonemid-derive d isolate (Pena et al., 1996).
Samson et al. (1980) proposed three varieties of H. thompsonii based on the morphologie s
of 11 isolates from eriophyoid mites: H. thompsonii var. thompsonii, var. vinacea, and var.
synnematosa. All three varieties are pleomorphic. Hirsutella thompsonii var. synnematosa
appears to be restricted to the tropics, on Eriophyes spp. or their kin, while H. thompsonii var.
thompsonii and var. vinacea occur mainly in temperate or subtropical areas (Samson et al.,
1980). These varieties may need to be revised and expanded as more information becomes
availabl e on H. thompsonii isolates from tarsonemid and tetranychid mites.
Under favourabl e conditions (see below), H. thompsonii kills its hosts quickly. Conidia of
the fungus can penetrate the integument of P. oleivora within 4 h of application , and death
and sporulation on the cadaver can occur within 72 h (McCoy, 1981). The LC 5 0 of
H. thompsonii to P. latus was estimated at 2.4 3 10 3 conidia ml - 1 six days post treatment
(Pena et al., 1996), while Gardner et al. (1982) achieved 97% mortality of T. urticae mites
inoculate d with a single conidium each of H. thompsonii using a micromanipulatio n
technique. These are very low lethal doses for an entomopathogeni c Mitosporic fungus.
Optimum growth, infection and conidiatio n of H. thompsonii occurs at 25± 30ë C (Kenneth
et al., 1979; McCoy, 1981) and is signi® cantly impaired below 13ë C and above 35ë C (Gerson
et al., 1979). As for all entomopathogeni c fungi, infection by H. thompsonii is dependent
upon a high humidity in the microclimate surroundin g the point of entry. In laborator y
experiments, Gerson et al. (1979) observed 94% mycosis of Tetranychus cinnabarinu s within
four days of inoculatio n at a constant 100% relative humidity (RH), 68% mycosis at 100%
RH for 18 h per day, and 23% mycosis at 100% RH for 6 h per day. In nature, hyphae of
H. thompsonii within cadavers of P. oleivora may break up and form multinucleat e
chlamydospore s as the host decomposes (McCoy, 1981).
Hirsutella thompsonii is the most important natural enemy of P. oleivora in Florida, where
it regularly causes epizootics leading to a rapid decline in mite population s. Populatio n

declines in the blueberry bud mite, Aceria vaccinii, in Carolina are also correlated with the
abundanc e of H. thompsonii (Baker & Neunzig, 1968). Epizootics in population s of
P. oleivora are associated with warm, wet weather and high mite populatio n densities,
which tend to peak around mid-June (McCoy, 1981). The abundanc e of H. thompsonii in
population s of cassava mites in Benin is also associated with periods of rainfall, although
here the fungus does not reach epizootic levels (Yaninek et al., 1996). In Florida citrus
groves, H. thompsonii epizootics last for three to four weeks and suYcient inoculum remains
within the environment to suppress mite population s for several months (McCoy, 1981).
Epizootics in P. oleivora are inhibited by the applicatio n of some fungicides, leading to
secondary mite outbreaks, and IPM strategies for oranges have been devised to promote the
natural activity of H. thompsonii by using selective fungicides and withholdin g the applicatio n
of acaricides (McCoy et al., 1976). Such an approac h can be highly successful, particularly
where fruit is grown for processing and surface quality is not so important to the grower
(McCoy et al., 1976).

Hirsutella thompsonii was developed by McCoy and co-workers, in collaboratio n with
Abbott Laboratories, as a mycopesticide for control of P. oleivora and other eriophyoids in
the 1970s, and was registered under the trade name MycarTM in the USA in 1981 (McCoy,
1996). Mycar has also been evaluated as a control for P. oleivora and the citrus mite
Panonychus citri in Australia (Rath, 1991). In Florida citrus groves, the fungus was applied
early in the growing season to suppress mite populatio n development at low densities. In
® eld experiments under favourabl e weather conditions, control of P. oleivora with Mycar
was comparable to that achieved with chemical acaricides (McCoy, 1996). Epizootics were
often initiated within two weeks of applicatio n and mite population s remained low for six
months to a year after applicatio n (McCoy, 1981). However, in commercial practice, the
product gave variabl e results, attributed to factors such as poor product stability in storage
and transport, variabl e ® eld persistence, and dependence upon high humidity, and sales
were terminated in 1985 (McCoy, 1996). Detailed accounts of the development and use of
Mycar, and the role of H. thompsonii as a natural regulator of P. oleivora are given in
McCoy (1981), Allen et al. (1994), and Bergh and McCoy (1997).
In Cuba, H. thompsonii isolated from the eriophyoi d Vasates destructor, gave 60± 90%
control of mites within 6 days at 27ë C and > 88% RH, when sprayed onto mite infested
tomato plants (Cabrera & McCoy, 1984). Hirsutella thompsonii was also investigate d as the
cause of natural epizootics in Dolichotetranychus Xoridanus (Prostigmata; Tetranychidae ) a
pest of pineapple, in Costa Rica, by Zoebisch et al. (1992). The fungus was identi® ed as a
candidate mycopesticide but we were unable to determine if it was studied further. Hirsutella
thompsonii has also been studied in Kenya as a mycopesticide of the cassava green mite,
M. tanajoa, and was reported to give signi® cant reductions of mite population s in ® eld cage
experiments conducted during the dry season, attributed to a favourable microclimate sur-
rounding mites on the plant surface (Odongo et al., 1998). It has also been recorded as
widespread in population s of the eriophyoid, Abacarus hystrix, on ryegrass in the UK (Lewis
et al., 1981).
Hyphal anastomosis and heterokaryosis in H. thompsonii have been documented (Mozes-
Koch et al., 1995), indicating the possibility for strain improvement through parasexual
breeding. A protein, hirsutellin A, produced in vitro by H. thompsonii, has also been shown
to be toxic per os to neonate mosquito larvae, Aedes aegypti, and by injection to larvae of
the wax moth Galleria mellonella (Mazet & Vey, 1995).
Neozygites spp. (Entomophthorales) Ð Natural Regulators of Tetranychid Mites

There are few entomophthoralea n pathogens of Acari (Humber et al., 1981). The most
commonly observed species belong to the genus Neozygites ( 5 Triplosporium
5 Entomophthora). The taxonomic status of Neozygites is not fully understood and has
been revised several times since the 1960s. It was originally classi® ed as a member of the
genus Entomophthora, but was separated in a series of revisions of the Entomophthorale s

(see reviews by McCoy et al., 1988 and Tanada & Kaya, 1993). In the ® rst (controversial )
revision (Batko, 1964), the fungus was assigned to the genus Triplosporium. However, the
type species on which Triplosporium was based had already been described and termed
Neozygites (Witlaczil, 1885, cited in Remaudiere & Keller, 1980) and, in a second revision
(Remaudiere & Keller, 1980), the name Neozygites was reinstated, according to the rules of
precedence for botanical nomenclature. Although subsequent subordinal revisions by
Humber (1981) and Ben Ze’ ev and Kenneth (1982a,b) reverted to Triplosporium, Neozygites
is now the accepted title (Humber, 1989).
Neozygites has a world-wide distribution and includes species that kill Homoptera,
Thysanoptera , and Acari (Dick et al., 1992). At least six species have been described which
are speci® c to Acari, from 19 species of host (see Table 3). However, it is diYcult to
distinguish them, because morphologica l characteristics overlap and can be altered by the
host and by the method used to prepare specimens for examination (Keller & Wuest, 1983;
Dick et al., 1992). Most Neozygites infections of Acari have been ascribed to Neozygites
Xoridana and Neozygites cf adjarica, although a comparison of fresh and paratype material
suggests that these two species are identical, the former binomial being recommended as the
valid name (Keller, 1991). Until molecular methods can determine with certainty the
discontinuitie s within the group, it is likely that the taxonomy of Neozygites will remain in
a state of ¯ ux.
Neozygites Xoridana is a speci® c pathogen of tetranychid mites (Prostigmata). It was ® rst
described as the cause of population declines in the Texas citrus mite, Eutetranychus banksi,
in Florida (Weiser & Muma, 1966). It is a key natural enemy of T. urticae, and the Banks
grass mite, Oligonychu s pratensis, in the mid-western and southeastern USA and causes
periodic but devastating epizootics in population s of these pests on maize, soybean, peanut
and sorghum (Smitley et al., 1986b; Dick et al., 1992). Isolates from South America are
being considered for classical biological control of the cassava green mite M. tanajoa in
Africa (Odongo et al., 1998). However, it cannot yet be cultured in bulk, which restricts its
use as a mycopesticide. There are also published observation s of: Neozygites acaricida from
the Eupodidae and Penthaleidae (Prostigmata) (James, 1992); Neozygites acaridis from the
Eupodidae (Ridsdill-Smit h & Annells, 1997) and Macrochelida e (Mesostigmata) (Milner,
1985); Neozygites acarina from the Penthaleidae (Hastings, 1994); and Neozygites tetranychi
from tetranychid mites (Remaudiere & Keller, 1980).
Neozygites Xoridana is highly adapted to its hosts, and an understandin g of its life cycle
is proving central to its exploitatio n as a biocontrol agent. The fungus develops within the
haemocoel of diseased mites as hyphal bodies which multiply by budding (Carner and
Canerday, 1968). The ® rst symptoms of disease occur three to four days post infection,
depending upon the host, when mites become sluggish, pale, and swollen with hyphal bodies,
and death follows shortly thereafter (Carner, 1976). Under dry conditions, the cadaver
becomes mummi® ed, but in a humid environment, fungal conidiophore s grow through the
cuticle and a single pyriform conidium is formed on each (Remaudiere & Keller, 1980). The
cadaver quickly adopts a `glass beaded’ appearance at this point with conidiophore s tightly
packed upon the integument (Dick et al., 1992). These primary conidia are forcibly
discharged over the ® rst 24 h after death, forming an aureole 1± 3 mm from the cadaver
(Brown & Hasibuan, 1995). The primary conidia are not infective to mites, and the majority
germinate to form a slender capillary, ca. 60 l m high, terminating in an almond-shaped,
infective capilliconidiu m (Carner, 1976). The capilliconidi a are passively disseminated,
attaching to passing mites by means of an adhesive haptor on the distal terminus (Dick
et al., 1992). Some of the primary conidia may germinate to form identical, but smaller,
secondary conidia on conidiophore s which are, again, actively discharged. Tertiary conidia
can also be produced in the same way. The ratio of capilliconidi a to secondary conidia may
be determined by the availabilit y of water (Oduor et al., 1995a).
Under some circumstances, which appear to be related to geography and may also be
linked to the weather, the hyphal bodies of N. Xoridana remain within the haemocoel of the
host where they form resting spores. Little is known about the physiology and function of
N. Xoridana resting spores, although in other entomophthoralean s they enable the fungus
to persist in the absence of hosts or during unfavourabl e weather conditions (Milner, 1997).
Mite cadavers that contain N. Xoridana resting spores may be anchored to the plant surface
by fungal rhizoids (Keller, 1991). Resting spores are formed late season (October to
November) in population s of T. urticae in Alabama USA (Carner, 1976), but in North
Carolina the fungus is thought to pass the winter in mummies or by infection cycling
(Brandenburg & Kennedy, 1981). Resting spores were not found in T. urticae in Israel
(Kenneth et al., 1972), but they were found in diseased M. tanajoa in Brazil (Delalibera
et al., 1992). They may remain associated with mite cadavers (Dick et al., 1992), but the
cadavers that contain them are fragile and easily ruptured (Carner, 1976), in which case they
could become redistributed over plant material or onto the soil.
Dissemination and infection of N. Xoridana happens mainly at night when RH exceeds
97% (Brown & Hasibuan, 1995) and is then probably regulated by subtle shifts in temper-
ature. Although the requirement for such high humidity seems restrictive, conditions condu-
cive to infection may be more common than ® rst expected, because tetranychid mites are
situated well within the boundary layer of the plant surface, where the microclimate
humidity is signi® cantly higher than ambient (Ferro & Southwick, 1984). When humidity
is not limiting, transmission is rapid and could occur within a single night, although
transmission over successive nights appears more likely. Under non-limiting conditions,
the growth of conidiophore s through the host cuticle and the formation of primary conidia
can occur within 6 h of death, while the median time for the germination of primary
conidia and the subsequent formation of capilliconidi a takes approximately 9 h (Carner,
1976; Dick et al., 1992; Oduor et al., 1996b). Capilliconidi a start to germinate rapidly,
for example within 2 h of attachment to the integument of M. tanajoa (Oduor et al.,
1996a) suggesting that, host density aside, it is the formation of primary and capilliconidi a
that is the rate limiting step to disease transmission. Although the formation of primary
conidia occurs at night, light is not physiologicall y damaging to the process (Oduor et al.,
1996b), and it is possible that the fungus detects nightfall as a cue for an impending rise
in humidity or a change in temperature.
The interactions between light, humidity and temperature, and their eVects on the
transmission of N. Xoridana are complex. DiVerent isolates of N. Xoridana may be adapted
to local temperature conditions. For example, the optimal temperature range for the
formation of primary conidia is 18± 23ë C for isolates from Brazil (Oduor et al., 1996b),
16± 21ë C for isolates from the southern USA (Smitley et al., 1986a), while an isolate from
Israel was able to produce primary conidia at 37ë C (Kenneth et al., 1972). Oduor et al.
(1995b; 1996a) observed that the production of primary conidia of a Brazilian strain of
N. Xoridana on M. tanajoa was inhibited above 23ë C, and the germination of primary
conidia and capilliconidi a was curtailed above 28ë C, but mites died rapidly at 33ë C once
infection had taken place. Thus the infection cycle is capable of responding to quite small
changes in temperature, and while dissemination may require moderate temperatures that
occur at night, infection and the subsequent colonisatio n of host tissues can take place
at higher temperatures that occur during daytime. Although only one to four capilliconidi a
are needed to kill a mite (Oduor et al., 1997), it is possible that the daytime acquisition
of capilliconidi a is important to transmission, because mites become more active and
acquire more capilliconidi a with rising temperatures (Oduor et al., 1996a). Certainly, the
capilliconidi a are signi® cantly more tolerant of adverse climatic factors than the primary
conidia, and are able to survive for at least 4 d under conditions likely to be encountered
in the ® eld, so that a capilliconidiu m formed on one night is still able to infect a mite
on the next night (Oduor et al., 1995a; 1996a).
In the southern states of the USA, the factors leading to outbreaks of N. Xoridana in
spider mites on ® eld crops are being determined. Disease outbreaks are periodic and are
triggered by a drop in the maximum daily temperature to below 29ë C and an elevation in
humidity, usually caused by rain (Brandenburg & Kennedy, 1982). Epizootics usually start
in mid summer and cause declines in mite population s in mid-August to September. In
Kansas, epizootics of N. Xoridana in population s of O. pratensis and T. urticae were initiated
when ambient RH exceeded 80% for 8± 10 h per day (Dick & Buschman, 1995). In North
Carolina, RH in excess of 90% for ca. 40 h (minimum 5 h per day) was required for fungal-
induced populatio n decline of T. urticae on maize (Brandenburg & Kennedy, 1982; Smitley
et al., 1986b), but leaf wetness was not required for fungal activity (Smitley et al., 1986a).
Although high humidity is necessary to trigger epizootics, some infection can also occur
during dry periods if capilliconidi a have already been formed (Dick & Buschman, 1995).
When initiated, epizootics of N. Xoridana can cause precipitous falls in spider mite
populations. Klubertanz et al. (1991), for example, observed reductions in spider mite
population s by up to 84% in two days on soybean, although the levels of infection varied
from year to year. Critically, the fungus does not infect predatory phytoseiid mites in the
® eld (Smitley et al., 1986b). Epizootics of N. Xoridana are delayed and/or suppressed by
regular sprays of fungicide s (Brandenburg & Kennedy, 1983; Boykin et al., 1984; Smitley
et al., 1986b) , and farmers have been encouraged to modify their spray programmes
appropriatel y to take full advantage of the fungus (Klubertanz et al., 1991). Although
N. Xoridana undoubtedly plays an important role in T. urticae populatio n dynamics,
epizootics may occur too late to prevent crop damage on some crops such as maize (Dick
& Buschman, 1995). However, epizootics in maize may well restrict the migration of spider
mites to other crops such as peanut (Smitley et al., 1986b). Moist conditions can also
sometimes stimulate early season epizootics in peanut which keep mite population s at basal
levels all season (Smitley et al., 1986b).
In Africa, N. Xoridana is being considered as a classical biologica l control agent of M. tanajoa
(Yaninek et al., 1996). Pathotypes of Neozygites from South America, which suppress popula-
tions of M. tanajoa in areas of high rainfall, are being assessed for release in Africa, where
native strains of N. Xoridana are thought to be weakly pathogenic and cause low levels of
mortality in M. tanajoa population s (Delalibera et al., 1992; Yaninek et al., 1996).
`NONSPECIALIST’ MITOSPORIC FUNGI

The most widely studied fungal pathogens of arthropods belong to just eight species of
entomopathogeni c Mitosporic fungi (Hyphomycetes) in four genera; Beauveria, Metarhiz-
ium, Paecilomyces and Verticillium. For convenience, we have described these genera
collectively as `nonspecialist ’ Mitosporic fungi, because they lack the overt ecomorphologica l
adaptation s to the life cycles of speci® c insect /acarine hosts observed in other fungi (Samson
et al., 1988), although this description has its limitations (see above). Metarhizium (three
species) and Beauveria (two species) are monophyletic genera, all species of which are
pathogens of insects. Metarhizium anisoplia e, Beauveria bassiana and Beauveria brongniartii
are also pathogens of Acari (Table 3). Verticillium is probably polyphyleti c with one truly
entomopathogeni c species, V. lecanii (which also kills Acari) although other members of the
genus have been reported very occasionally to kill insects and mites (Table 3). Paecilomyces
contains six species that can kill insects, but only Paecilomyces farinosus and Paecilomyces
fumosoroseus have been considered in any depth for biological control. Four species of
PaecilomycesÐ Paecilomyces eriophyes, P. farinosus, P. fumosoroseus and Paecilomyces
terricolaÐ infect Acari (Table 3).
Beauveria, Metarhizium and Paecilomyces show adaptations to the soil environment,
exhibit wide host ranges within the Insecta, occupy broadly similar trophic niches and
possibly form a guild. Verticillium lecanii is more commonly associated with epigeal and
aerial habitats. All these fungi have world-wide distribution s and they can be cultured readily
in bulk. To date they have been the most popular choices for development as myco-
insecticides. This group of fungi also kill Acari. Unfortunately, it is not known whether the
pathotype s involve d are opportunist s or have evolved a degree of specialisation for Acari.
Most reports concern mycoses in the Parasitiforme s (Mwangi et al., 1991), especially species
that spend all or part of their lives near to the soil or in detritus, where entomopathogeni c
Mitosporic fungi are common (Chandler et al., 1997). Metarhizium anisoplia e and
B. bassiana, for example, have been observed infecting soil-dwellin g stages of the cattle tick,
Boophilu s microplus, in Brazil (Verissimo, 1995). Balazy et al. (1987) isolated B. bassiana,
P. eriophyes, and V. lecanii from mesostigmatid mites associated with birds’ nests in Poland.
In Czechoslovakia , Samsinakov a et al. (1974) observed natural mycoses in the ticks I. ricinus,
Dermacentor marginatus and Dermacentor reticulatis by 17 species of fungi, of which four
were obligat e pathogens Ð Aspergillus parasiticus, B. bassiana ( 5 B. tenella), V. lecanii and
P. fumosoroseus. In this case, fungal infections caused up to 57% mortality in engorged
females of I. ricinus held in ® eld cages during the summer.
A comprehensive study of mycoses in natural population s of I. ricinus in Denmark was
undertaken by Kalsbeek et al. (1995). Ticks collected from vegetation, small rodents and
deer were found infected by six species of Mitosporic fungi: B. bassiana, B. brongniartii,
P. farinosus, P. fumosoroseus, V. lecanii and Verticillium aranearum. Paecilomyces farinosus
was the most frequently encountered species. Fungi appeared to be important regulators of
the tick population . Fungal infections were most common on engorged females (22.2%
incidence) and ¯ at females (10.3%), while infections in males, nymphs and larvae did not
exceed 1.1%.
Metarhizium anisopliae and B. bassiana have been studied as potential microbial control
agents of cattle ticks, which are a major constraint to livestock production in many areas of
the world. In Brazil, two isolates of M. anisopliae, originatin g from the pasture froghopper
Deois schach (Hemiptera: Cercopidae) and the leafcutter ant Atta sexdens rubropilos a,
(Hymenoptera: Formicidae) killed laborator y population s of engorged adult females, eggs
and larvae of B. microplus and aVected ovipositio n behaviour (Bittencourt et al., 1992;
Bittencourt et al., 1994a,b) . However, an isolate of M. anisopliae did not reduce numbers of
B. microplus when applie d to ticks feeding on stalled cattle, although ticks became infected
when collected from treated cattle and incubate d in the laborator y (Correia et al., 1998). In
Kenya, the cattle tick Rhipicephalu s appendiculatu s was susceptible in laborator y bioassays
to an isolate of B. bassiana originating from the banana weevil, Cosmopolite s sordidus, and
an isolate of M. anisopliae originatin g from the migratory locust Locusta migratoria (Mwangi
et al., 1995). These fungi subsequently caused up to 100% mortality of free living ticks in
the ® eld (Kaaya et al., 1996). An isolate of M. anisopliae of unnamed origin was also
pathogenic to the black-legged tick, Ixodes scapularis, a vector of human diseases (Zhioua
et al., 1997). Treatment of engorged larvae and adult females with 10 8 and 10 7 conidia ml - 1
respectively caused 100% mortality two weeks after treatment. Varroa jacobsoni was also
reported to be susceptible to infection by B. bassiana and Aspergillus spp. when mites were
kept on cultures of the fungus (Chernov, 1981).
There are few reports of natural mycoses by these fungi in population s of phytophagou s
prostigmatid mites (Actinotrichida). Whether this re¯ ects biology, or a lack of biologist s
studying the phenomenon, is open to question. Lewis et al. (1981) observed frequent
infections by V. lecanii (and H. thompsonii) in population s of A. hystrix on ryegrass in
the UK in some years. Little research has been done on the development of nonspecialis t
Mitosporic fungi as mycopesticides of phytophagou s mites, despite their increasing use
elsewhere. NaturalisTM (Thermo Trilogy Corp.), a commercial mycopesticide based on
B. bassiana, reportedly gave excellent control of T. urticae on glasshouse roses (Wright &
Kennedy, 1996). The phytophagou s broad mite, Polyphagotarsonemu s latus (Prostigmata;
Tarsonemidae) was susceptible to B. bassiana (derived from a hymenopteran host) and
P. fumosoroseus (derived from a homopteran), although both were less virulent than an
isolate of H. thompsonii originatin g from an unidenti® ed tarsonemid mite (Pena et al., 1996).
Despite this, B. bassiana and P. fumosoroseus were selected for study in glasshouse
experiments against P. latus, because of their good spore production in culture.
`MINOR’ SPECIES
There are a range of fungi which have occasionally been observed to infect Acari, but which
have not been studied as natural regulators or as mycoacaricides (Table 3). Some of these
observation s undoubtedly include weak pathogens or saprotrophs, but others may deserve
further attention. Lipa (1971) describes three instances of infection of Acari by Aspergillus
fumigatus and Penicillium insectivorum. Balazy et al. (1987) identi® ed 24 species of fungi
from dead mesostigmatid mites collected from soil, birds’ nests and ant hills, of which only
three (B. bassiana, P. farinosus, and V. lecanii) have been studied elsewhere as biocontrol
agents, although the list included some saprotrophi c species (e.g. Trichothecium roseum and
Gliocladiu m roseum). Conidia of an Aspergillus-like fungus were observed on the cuticle of
V. jacobsoni from Brazil, and hyphae were often observed penetrating the cuticle (Lui &
Ritter, 1988). Mwangi et al. (1995) reported low levels of infection (1.7%) by species of
Aspergillus and Fusarium in engorged females of the cattle tick R. appendiculatus placed in
soil for eight days. Similarly, Samsinakova et al. (1974) observed ® eld infections by
A. parasiticus and Conidiobolu s coronatus in population s of I. ricinus maintained in ® eld

cages. A range of saprotrophi c species were also isolated from tick cadavers. Aspergillus sp.
and Fusarium sp. have also been observed on cadavers of cassava green spider mites,
Mononychellus spp., together with Hirsutella sp. and Neozygites sp. (Bartowski et al., 1988).
CONCLUSIONS
The requirement for non-chemical methods to control acarine pests is likely to increase in
the future, given concerns about the safety and sustainabilit y of chemical pesticides. Although
the study of fungal pathogen s of Acari has tended to be a minor branch of invertebrate
patholog y, they have been shown to be important natural enemies of Acari, and there are
some good opportunitie s to use them for biocontrol . The role of fungal pathogens in the
regulation of some major pest species of prostigmatid, phytophagou s mites has been
established, and strategies have been developed to conserve and enhance natural fungal
activity. There is emerging evidence also that naturally occurring Mitosporic fungi are
involve d in the regulation of population s of ticks in some habitats. We recommend that
these studies are continue d and expanded. With the exception of Mycar, the development
of mycopesticides of Acari has been limited, but this could change relatively quickly. The
fact that representatives of the main acarine pests, viz. the phytophagou s prostigmatids and
the Ixodida, are susceptible to entomopathogeni c fungi, including `nonspecialist’ Mitosporic
pathogens, in nature and in the laborator y, bodes well for the future development of
mycoacaricides. It should be noted too that some insect pests, for example cockroaches and
termites, are highly susceptible to mycopesticides but are rarely infected by entomopathogeni c
fungi in nature (Miller, 1990; Milner & Staples, 1996). Recent advances in formulation
technology should also make it possible to use mycoacaricides in environments where
humidity has been previously limiting (Milner, 1997). In some cases, for example where the
pest occurs at high populatio n densities, e.g. livestock ticks in animal units, or varroa mites
in beehives (Dietz & Hermann, 1988), mycoacaricide s could be suitable as stand alone
treatments. In others, they are more likely to be used as components of IPM or biologically -
based systems, for example on protected crops to supplement the control of phytophagou s
mites with introduce d predators. In integrated systems, the compatibilit y of the mycoacaric-
ide with other living components of the system must be paramount , while in all cases
consideration must be given to maintaining the sustainabilit y of the mycoacaricide. Particular
attention would have to be paid to the compatibilit y of fungi used against phytophagou s
mites with predatory mites.
Concomitant with the development of mycoacaricides, there is a requirement to obtain
and characterise, from nature, more specimens of fungal pathogen s of Acari. The fact that
these fungi appear to be less diverse than fungal pathogens of insects may be due to the
lower diversity of the Acari compared to the Insecta, but it may also be because they have
been studied less (Poinar & Poinar, 1998). The Acari are numerically abundant and occupy
a broad variety of habitats and trophic niches, and it is reasonable to assume that a
comprehensive range of pathogens will have evolved to exploit them. Certainly many Acari
inhabit environments favourabl e to fungal infection, such as the soil and within leaf
boundar y layers, and mycoses have been observed from these environments. However,
because Acari in general, and mycosed Acari in particular, are diYcult to observe in the
® eld, it is likely that the frequency of occurrence of acaropathogeni c fungi has been
underestimated (Poinar & Poinar, 1998).
The taxonomic status of many species of entomopathogeni c fungi is poorly understood,
but the phylogenie s (including subgeneric relationships ) of Hirsutella and Neozygites need
particular attention for their further development as biocontrol agents. It is somewhat ironic
that, in nature, these fungi kill mites rapidly and can respond quickly to changes in host
density, but grow slowly in culture or not at all. The likely cause for this fastidiousness lies
in their high degree of host speci® city; understandin g the biochemical basis of their
adaptation s to their hosts may facilitate improvements in their mass production , which is
essential if they are to be developed as mycoacaricides.
ACKNOWLEDGEMENTS
This work was funded by the UK Ministry of Agriculture, Fisheries and Food. IACR-
Rothamsted receives grant-aided support from the Biotechnology and Biological Sciences
Research Council of the UK. The authors wish to thank Dr Mark Tatchell, Rob Jacobson,
Mike Easterbrook, John Carder and Dr Mike Solomon for critically evaluating the
manuscript.
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This article was downloaded by: [Laurentian University]

On: 06 December 2014, At: 08:14

Biocontrol Science and

Fungal Biocontrol of Acari

To cite this article: D. Chandler , G. Davidson , J. K. Pell , B. V. Ball , K. Shaw & K.

To link to this article: http://dx.doi.org/10.1080/09583150050114972

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Fungal Biocontrol of Acari

D. CHANDLER, 1 G. DAVIDSON, 1 J. K. PELL, 2 B. V. BALL, 2 K. SHAW 2

Nematology, IACR Rothamsted, Harpenden, Herts AL5 2JQ, UK

Keywords: Acari, entomopathogenic, fungi, mites, ticks, Tetranychidae, Eriophyidae, Ixodida,

Correspondence to D. Chandler. E-mail david.chandler@hri.ac.uk

CLASSIFICATION OF THE ACARI

ACARI AS PESTS OF AGRICULTURAL, MEDICAL AND VETERINARY IMPORTANCE

TABLE 1. Acari ± biodiversity and ecosystem function

Superorder Order Description

TABLE 2. Acarine pests of agricultural, veterinary and medical importance

Superorder Order Pest status

Aculops lycopersici; the coconut mite, Aceria guerreronis; the wheat

CLASSIFICATION OF THE FUNGI

are distinguishe d by the production of motile, ¯ agellated zoospores. However, nucleotide

ACAROPATHOGENIC FUNGI AND THEIR USE IN BIOCONTROL

TABLE 3. Fungi reported to infect Acari

Mononychellus tanajoa Brazil Delalibera et al., 1992

Tarsonemidae Tarsonemus spirifex Ð Oudemans, 1915 (in Lipa, 1971)

Hirsutella haptospora Unidenti® ed Unidenti® ed Unidenti® ed Poland ARSEF culture collection7

Tarsonemidae Polyphagotarsonemus latus Florida USA Pena et al., 1996

Tetranychus urticae Florida USA Gardner et al., 1982*

Mycobatidae Mycobates sp. Canada CCFC culture collection 1 3

(iii) Ð (iii) Andreeva & Shternshis, 1995

ACARI SPECIFIC PATHOGENSÐ IMPORTANT NATURAL REGULATORS OF

it regularly causes epizootics leading to a rapid decline in mite population s. Populatio n

(McCoy et al., 1976).

Neozygites spp. (Entomophthorales) Ð Natural Regulators of Tetranychid Mites

genus Entomophthora, but was separated in a series of revisions of the Entomophthorale s

`NONSPECIALIST’ MITOSPORIC FUNGI

A. parasiticus and Conidiobolu s coronatus in population s of I. ricinus maintained in ® eld

dosage on the pathogenicity of Neozygites Xoridana (Zygomycetes: Entomophthorales) to Mononychellus

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