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Списък на естествено срещащи се гъбни
патогени, заразяващи корояди и пеперуди –
вредители в горите от България
Даниела Пиларска1,2, Данаил Таков2, Данаил Дойчев3
1Нов български университет, Департамент „Природни науки“,
бул. „Монтевидео“№ 21, 1618 София, България
2Институт по биоразнообразие и екосистемни изследвания, Българска
академия на науките, бул. „Цар Освободител“ № 1, 1000 София, България
3Лесотехнически университет, бул. „Климент Охридски“,
№ 10, 1797 София, България,
dpilarska@nbu.bg
List of natural fungal pathogens infecting bark
beetles and lepidopteran forest pests from Bulgaria
Daniela Pilarska1,2, Danail Takov2, Danail Doychev3
1New Bulgarian University, Department of Natural Sciences,
21 Montevideo St., 1618 Soa, Bulgaria
2Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of
Sciences, 1 Tsar Osvoboditel Blvd., 1000 Soa, Bulgaria
3University of Forestry, 10 Kliment Ohridski Blvd., 1797 Soa, Bulgaria
dpilarska@nbu.bg
Резюме: Представена е информация за установените гъбни инфек-
ции в различни видове вредни насекоми – корояди и пеперуди от
България. В 12 вида корояди и 10 вида пеперуди са идентифицирани
общо 18 вида ентомопатогенни гъби и многобройни изолати, принад-
лежащи към разредите Hypocreales, Eurotiales и Entomophthorales за
шейсетгодишен период. Обобщени са резултатите от лабораторни и
полеви опити, проведени с част от намерените гъбни изолати срещу
корояди и гъботворката (Lymantria dispar).
Ключови думи: ентомопатогенни гъби, корояди, пеперуди
Abstract: Information about fungal infections detected in dierent bark bee-
tles and lepidopteran forest pests in Bulgaria is presented. Eighteen species
of entomopathogenic fungal species and numerous isolates of orders Hypo-
creales, Eurotiales и Entomophthorales have been reported from 12 bark
beetles and 10 moths within a sixty years period. The results from conduct-
https://doi.org/10.33919/ansd.19.1.10
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ed laboratory and eld bioassays with several isolates of entomopathogenic
fungi against bark beetles and the gypsy moth were summarized.
Keywords: entomopathogenic fungi, bark beetles, lepidopteran pests
Introduction
Insect pests are a major cause of economic and aesthetic loss in forestry
systems and are of particular concern as habitats become more fragmented, land
use pressures increase, and climate change impacts forest ecosystems. Chemical
pest controls cause additional concerns about eects on non-target organisms in
treated areas and in the larger watersheds.
The most signicant pests of European forests are species in the orders
Coleoptera and Lepidoptera [Day & Leather, 1997]. In the coniferous forests
of Bulgaria, bark beetles (Coleoptera: Curculionidae) and the pine procession-
ary moth Thaumetopoea pityocampa (Denis & Schiermüller), are of greatest
concern. Important pests of broadleaf forests include moths from the families
Erebidae (Lymantria dispar L., Euproctis chrysorrhoea L.), Notodontidae (Tha-
umetopoea processionea L.), Tortricidae and Geometridae [Zaemdzhikova et al.,
2019]. Forestry administrations are committed to reducing the use of pesticides in
the environment and to emphasizing the use of biological control agents. There-
fore the research on the natural enemies of these insect pests including fungal
pathogens is of great importance.
The aim of this study is to present information about fungal infections
found in dierent bark beetles and lepidopteran forest pest species in Bulgaria.
1. Entomopathogenic fungi of bark beetles
Entomopathogenic fungi which attack bark beetles belong to the division
Ascomycota, order Hypocreales and Eurotiales. They infect their hosts through the
integument. The fungus proliferates throughout the insect and causes mortality of
its host. Host specicity of entomopathogenic fungi varies. While some species are
very host specic, others have a broad host range [Wegensteiner et al., 2015].
There are many reports for the occurrence of entomopathogenic fungi in
bark beetles [Wegensteiner, 2004; Wegensteiner et al., 2015]. The rst publica-
tions about fungal pathogens in bark beetles were from Great Britain, Poland,
France and the Netherlands [Wegensteiner et al., 2015]. Petch [1932] reported
Beauveria bassiana (Balsamo) Vuillemin from Hylastes ater (Paykull) in Great
Britain and Karpinski [1935], Siemaszko [1939] discovered it in Poland. Since
then the number of publications dealing with entomopathogenic fungi in bark
beetles increased and at least 13 fungal species from 15 bark beetle species were
reported by dierent authors [Wegensteiner et al., 2015]. Moreover entomopath-
ogenic fungi were evaluated as bark beetles control agents. The most studied
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species was B. bassiana. Various bioassays have been conducted against dier-
ent bark beetle species. First Doane [1959] reported high mortality of Scolytus
multistriatus (Marsham) caused by B. bassiana in larvae, pupae and adults of the
host. Later Novak and Samsinakova [1962] showed that B. bassiana was highly
pathogenic to Ips typographus L. Other fungi such as Metharizium anisopliae
(Metschn.) Sorokin, M. brunneum Petch and Isaria fumosorosea Wize were also
tested against dierent bark beetles [Wegensteiner et al., 2015]. Commercial iso-
lates of B. bassiana were also developed and evaluated [Castrillo et al., 2011].
In Bulgaria the investigations on bark beetles pathogens started in 2005 when
Takov et al. [2006] detected B. bassiana in I. typographus. It was established in
2005 in 3 localities in Vitosha Mt. and its prevalence was very low (0.7%) [Takov
et al., 2006, 2019]. In the same host were observed also B. caledonica [Draganova
et al., 2017] and Fusarium sp. [Draganova, personal communication]. B. bassiana
was found in Ips sexdentatus (Börner) [Takov et al., 2007; Draganova et al., 2010],
Dryocoetes autographus (Ratzeburg) [Draganova et al., 2010] and Hyllurgops pal-
liatus (Gyllenhal) [Takov et al., 2011, 2012] [Table 1]. Additionally Draganova et
al. [2010] isolated B. brongniartii from I. typographus and Isaria farinosa from I.
sexdentatus. The authors revealed totally 3 fungal species in 6 bark beetle species
collected in 4 mountains – Vitosha, Rila, Maleshevska and Rhodopes. The most
frequently found fungus of bark beetles in Bulgaria was B. bassiana followed by B.
caledonica and B. brongiartii [Table 1 and Table 2].
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Table 1. Data of insect hosts and their natural
entomopathogenic fungi reported from Bulgaria
Insects Host plant *Localities Fungal pathogens Reference
Coleoptera, Curculionidae, Scolytinae
Dendroctonus micans
(Kugelann) Picea abies 1Beauveria bassiana Draganova et al.,
2017
Dryocoetes autogra-
phus (Ratzeburg) P. abies
3Beauveria bassiana Draganova et al.,
2010
1Beauveria bassiana Draganova et al.,
2017
Hylastes cunicularius
(Erichson) P. abies 1
Beauveria bassiana
Beauveria caledonica
Isaria farinosa
Draganova et al.,
2017
Hylurgops palliatus
(Gyllenhal)
Pinus sylvestris 45 Beauveria bassiana Takov et al., 2011
Picea abies 38 Beauveria bassiana
Beauveria brongniartii Takov et al., 2012
Pinus sylvestris 45 Beauveria caledonica Draganova et al.,
2017
Ips acuminatus
(Gyllenhal)
P. sylvestris 16 Isaria farinosa
Aspergillus sp. Takov et al., 2012
Pinus nigra 52
Beauveria bassiana
Isaria farinosa
Fusarium sp.
unpublished data
Ips sexdentatus
(Börner)
Pinus sylvestris
51 Beauveria bassiana Takov et al., 2007
49 Beauveria bassiana
Isaria farinosa Takov et al., 2012
50 Beauveria bassiana
Isaria farinosa
Draganova et al.,
2010
P. sylvestris 49 Beauveria brongniartii unpublished data
Ips typographus (L.) Picea abies
3Beauveria bassiana Takov et al., 2006
4
Beauveria bassiana
Beauveria brongniartii
Draganova et al.,
2010
Fusarium sp. unpublished data
Beauveria caledonica Draganova et al.,
2017
2Beauveria bassiana Takov et al., 2007
4Aspergillus sp. Takov et al., 2012
Orthotomicus erosus
(Wollaston) Pinus sylvestris 48 Beauveria bassiana Takov et al., 2012
Orthotomicus longicol-
lis (Gyllenhal) P. sylvestris 49 Beauveria bassiana Takov et al., 2012
Taphrorychus villifrons
(Dufour) Fagus sylvatica 5Beauveria bassiana Takov et al., 2012
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Insects Host plant *Localities Fungal pathogens Reference
Tomicus minor (Hartig) P. nigra 8Beauveria bassiana unpublished data
Tomicus piniperda (L.) P. sylvestris 47 Beauveria bassiana
Aspergillus sp. Takov et al., 2012
Lepidoptera
Catocala nymphagoga
(Esper, 1787) Quercus spp.
13
Entomophaga aulicae
Beauveria bassiana
Isaria farinosa Lecan-
icillium sp.
Georgieva et al.,
2014
14, 53 Tarichium dissolvens
Conidiobolus sp.
25 Beauveria bassiana
Beauveria sp.
15 Beauveria sp.
Fusarium sp.
Erannis defoliaria
(Clerck) Quercus spp. 28 Aspergillus niger
Beauveria bassiana
Draganova et al.,
2013
Eriogaster lanestris
(L.) Crataegus sp. 33 Beauveria bassiana
Fusarium sp. unpublished data
Euproctis chrysor-
rhoea (L.)
Quercus spp.
7, 9, 10, 12,
17, 18, 26,
27, 36, 37,
39, 40, 41,
43, 44, 46
Entomophaga aulicae Pilaska et al., 2001
Q. frainetto 35 Entomophaga aulicae Pilaska et al., 2018
Leucoma salicis (L.) Populus x eur-
americana 42 Beauveria bassiana Markova and Geor-
giev, 1992
Lymantria dispar (L.)
Quercus spp. 23, 24
Beauveria bassiana
Beauveria globulifera
Isaria farinosa
Panajotov et al.,
1960
Quercus
frainetto,
Q. cerris
19, 20, 21
Aspergillus avus
Aspergillus sp.
Fusarium sp.
Mucor globosus
Mucor mucedo
Penicillium frequentans
Scopulariopsis
brevicaulis
Mirchev, 2004
Quercus spp. 28 Beauveria bassiana Draganova et al.,
2011
Quercus spp.
28, 29, 32 Beauveria bassiana
Aspergillus sp.
Draganova et al.,
2013
31, 33, 34 Beauveria bassiana
Aspergillus sp. unpublished data
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Insects Host plant *Localities Fungal pathogens Reference
Malacosoma neustria
(L.) Quercus spp.
32 Beauveria bassiana
Fusarium sp.
Draganova et al.,
2013
30 Beauveria bassiana
Fusarium sp. unpublished data
Thaumetopoea pityo-
campa (Denis & Schif-
fermüller)
Pinus nigra 6
Beauveria bassiana
Aspergillus sp.
Fusarium sp.
Draganova et al.,
2013
Thaumetopoea soli-
taria (Freyer)
Pistacia tere-
binthus 31 Beauveria bassiana Mirchev et al.,
2012
Tortrix viridana (L.) Quercus spp. 11, 22, 28
Beauveria bassiana
Aspergillus sp.
Fusarium sp.
Draganova et al.,
2013
*Localities. Vitosha Mt.: 1 – Aleko Hut, 2 – Artista Hut, 3 – Bistrishko
branishte Biosphere Reserve, 4 – Zlatni mostove Place; Lyulin Mt.: 5 – St. St.
Cyril and Methodius Monastery; Sredna gora Mt.: 6 – Banya Vill., 7 – Babek
Vill., 8 – Hisarya, 9 – Kavakliyka Vill., 10 – Koprinka Vill., 11 – Pobit kamak
Vill., 12 – Turiya Vill.; Balkan range: 13 – Elovitsa Vill., 14 – Skravena Vill.,
15 – Ravna gora Vill., 16 – Gabrovo, 17 – Kalofer, 18 – Kazanlak, 19 – Kosta
Perchevo Vill., 20 – Makresh Vill., 21 – Mramoren Vill., 22 – Plakovo Vill.;
Strandzha Mt.: 23 – Bosna Vill., 24 – Zvezdets Vill., 25 – Indzhe Voyvoda Vill.;
Sakar Mt.: 26 – Glavan Vill., 27 – Kostur Vill.; Eastern Rhodopes Mts.: 28
– Gnyazdovo Vill., 29 – Gugutka Vill., 30 – Huhla Vill., 31 – Ivaylovgrad, 32 –
Kamenets Vill., 33 – Karaml Vill., 34 – Silen Vill, 35 – Zhenda Vill.; Western
Rhodopes Mts.: 36 – Asenovgrad, 37 – Bachkovo Vill., 38 – Beglika Place, 39
– Byala cherkva Vill., 40 – Iskra Vill., 41 – Parvomay, 42 – Pazardzhik, 43 – Pe-
rushtitsa, 44 – Ruen Vill., 45 – Yundola Vill., 46 – Zhalt kamak Vill.; Rila Mt.:
47 – Yakoruda; Maleshevska planina Mt.: 48 – Mikrevo Vill., 49 – Nikudin
Vill., 50 – Razdol Vill., 51 – Tsaparevo Vill.; Pirin Mt.: 52 – Dobrinishte Vill.;
Danubian Plain: 53 – Slavyanovo Vill.
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Table 2. List of established fungal species and their insect hosts
Entomopathogenic fungi Insect hosts
Bark beetles Moths
Aspergillus avus Link Lymantria dispar
Aspergillus niger Tiegh. Erannis defoliaria
Aspergillus sp.
Ips acuminatus
Ips typographus
Tomicus piniperda
Erannis defoliaria
Lymantria dispar
Thaumetopoea pityo-
campa
Tortrix viridana
Beauveria bassiana (Bals.-Criv.)
Vuill.
Dendroctonus micans
Dryocoetes autographus
Hylastes cunicularius
Hylurgops palliates
Ips acuminatus
Ips sexdentatus
Ips typographus
Orthotomicus erosus
Taphrorychus villifrons
Tomicus minor
Tomicus piniperda
Catocala nymphagoga
Erannis defoliaria
Eriogaster lanestris
Euproctis chrysorrhoea
Leucoma salicis
Lymantria dispar
Malacosoma neustria
Thaumetopoea pityo-
campa
Thaumetopoea solitaria
Tortrix viridana
Beauveria brongniartii (Sacc.) Petch Hylurgops palliates
Ips sexdentatus
Ips typographus
Beauveria globulifera (Speg.) F.
Picard Lymantria dispar
Beauveria caledonica Bissett &
Widden
Hylastes cunicularius
Hylurgops palliatus
Ips typographus
Beauveria sp. Catocala nymphagoga
Conidiobolus sp. Catocala nymphagoga
Entomophaga aulicae (E. Reichardt)
Humber
Catocala nymphagoga
Euproctis chrysorrhoea
Fusarium sp. Ips acuminatus
Ips typographus
Eriogaster lanestris
Lymantria dispar
Malacosoma neustria
Thaumetopoea pityo-
campa
Tortrix viridana
Isaria farinosa (Holmsk.) Fr. Hylastes cunicularius
Ips acuminatus
Ips sexdentatus
Catocala nymphagoga
Lymantria dispar
Lecanicillium sp. Catocala nymphagoga
Mucor globosus A. Fisch. Lymantria dispar
Mucor mucedo (Tode) Spreng. Lymantria dispar
Penicillium frequentans Westling Lymantria dispar
Scopulariopsis brevicaulis (Sacc.)
Bainier Lymantria dispar
Tarichium dissolvens Vosseler Catocala nymphagoga
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Laboratory experiments with fungal species against bark beetles
In 2000 Markova [2000] performed laboratory experiments with Beauver-
ia bassiana, Verticillium lecanii (Zimm.) Viégas, Isaria farinosa and Metarhi-
zium anisopliae against Ips typographus and showed that the bark beetle was
susceptible to these fungi.
Later Draganova et al. [2007] also conducted laboratory bioassays with
conidial suspensions of B. bassiana and Isaria farinosa isolates against I. sexden-
tatus and I. acuminatus. They established that 3 dierent isolates of B. bassiana
caused the highest lethal eect to adults of Ips sexdentatus – between 89.33 and
96.67%. The adults of I. sexdetnatus were more susceptible to the isolates of B.
bassiana than to these of I. farinosa.The results from bioassays with adults of I.
acuminatus revealed that the host was not susceptible to I. farinosa.
In other research Draganova et al. [2017] performed laboratory bioassays
using as test and control insects adults of Ips typographus. Conducted labora-
tory bioassays showed that mortality caused by the examined fungal isolates
to adults of I. typographus was signicantly higher when compared to control
treatments. Initial eect established on the second day in the variants with 3
isolates was 26.67% ± 8.12, 23.33% ± 13.03 and 31.67% ± 13.92, respectively.
Four days after the treatment with conidial suspensions of one isolate of M.
anisopliae, and two from B. bassiana the mortality rates increased to 100%
and to 75.00% ± 13.92, respectively. Mortality rates in the variants treated with
isolates of B. bassiana were lower.
Field experiments with fungal species against bark beetles
Draganova et al. [2017] conducted the rst eld experiment under natural
conditions in Bulgaria with bark beetles fungal pathogens. Totally, larvae and
adults of insects belonging to 11 species were examined. The results showed that
adults and larvae of Hylastes cunicularius were the most aected by mycoses
after contact with Norway spruce logs treated with one isolate of B. bassiana
(55 specimens) and one of M. anisopliae (77 specimens). Only single numbers
of bark beetles belonging to other species were infected by entomopathogenic
fungi including Ips typographus. In this study for the rst time for Bulgaria Den-
droctonus micans was registered as a host of B. bassiana and natural infections
caused by B. bassiana, B. caledonica, Isaria farinosa in Hylastes cunicularius,
Dendroctonus micans and Dryocoetes autographus [Table 1, Table 2].
2. Entomopathogenic fungi of lepidopteran forest pests
The study of fungal pathogens of leidopteran pest species was provoked
in order to improve the existent strategies for their control. Entomopathogenic
fungi infecting insects of order Lepidopetra belong to the division Ascomycota,
order Hypocreales, Eurotiales and to the division Entomophthoromycota, order
Entomophthorales.
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In Bulgaria, the rst report of entomopathogenic fungi in lepidopterans
was published by Panajotov et al. [1960]. The authors recorded B. bassiana, B.
globulifera and I. farinosa in larvae of the gypsy moth (Lymantria dispar). Mark-
ova and Georgiev [1992] reported B. bassiana in dead larvae of Leucoma salicis.
Later Mirchev [2004] found Scopulariopsis brevicaulis, Aspergillus avus, Pen-
icillium frequentans, Mucor mucedo, M. globosus, Aspergillus sp. and Fusarium
sp. which were the cause of 24.5% of mortality of L. dispar pupae. Draganova
et al. [2011] conrmed the presence of B. bassiana in L. dispar larvae and and
Mirchev et al. [2012] found it for the rst time in two new hosts – Thaumetopoea
pityocampa and T. solitaria. Later Draganova et al. [2013] established B. bassi-
ana in 6 lepidopteran species – T. pityocampa, Lymantria dispar, Malacosoma
neustria, Tortrix viridana, Erannis defoliaria and Melitaea didyma (Esper). The
most aected by this pathogen were the larvae of T. pityocampa. The fungus was
detected in 66.7% of all dead pine processionary moth larvae. Тhis fungus caused
mortality also in 7.2% of all L. dispar, 6.9% of Malacosoma neustria, 5.1% of T.
viridana and 37.5% of Erannis defoliaria collected individuals. The mycosis was
observed mainly in larvae, rarely in pupae. Besides B. bassiana these authors re-
corded more fungal pathogens – Aspergillus niger in E. defoliaria, Aspergilus sp.
in T. pityocampa, L. dispar and T. viridana, and Fusarium sp. in T. pityocampa,
M. neustria and T. viridana [Table 2]. B. bassiana and Fusarium sp were detect-
ed also in Eriogaster lanestris [Draganova, personal communications] [Table 1
and Table 2]. Georgieva et al. [2014] revealed 7 fungals species in another host,
Catocala nymphagoga (Esper, 1787)[Table 1 and Table2].
Using seven dierent isolates of B. bassiana and one of Metharisium an-
isopliae Draganova et al. [2010] studied the susceptibility of L. dispar larvae to
these fungi. The results of the conducted bioassays showed that these caterpillars
were tolerant to all tested isolates.
The rst fungus of order Entomophthorales recorded in lepidopterans from
Bulgaria was Entomophaga aulicae [Pilarska et al., 2001]. It was observed in
2000 in high density of populations of the brown tail moth, Euproctis chrysor-
rhoea collected in Balkan range, Sakar, Sredna gora and Rhodopes Mountains.
The authors established the pathogen in 16 out of 72 sites with brown tail moth
infestation. E. aulicae was the main factor reducing E. chrysorrhoea population
density. E. aulicae was recorded again in 2016 in a brown tail moth population in
the region of Asenovgrad [Pilarska et al., 2018] [Table 1 and Table 2].
In order to improve the existing biological control of Lymantria dispar in
1999 in the region of Karlovo, a successful introduction of the entomopathogenic
fungus Entomophaga maimaiga Humber, Shimazu & R.S. Soper was conducted in a
gypsy moth population. In 2005 strong epizootics caused by this fungus were detect-
ed in dierent areas of Bulgaria. In the next years several new epizootics occurred
and suppressed some strong outbreaks of the pest. As a result over the past 20 years,
almost no insecticides have been used to control L. dispar [Pilarska et al., 2016].
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In 2016 a successful release of another entomophthorous fungus, E. auli-
cae for control of Euproctis chrysorrhoea was performed. It was conducted in a
healthy brown tail moth population near Kardzhali and larval mortality of 19%
has been established subsequently [Pilarska et al., 2018].
Conclusion
During a sixty years period numerous isolates of 18 entomopathogenic
fungal species and representatives of 11 genera from orders Hypocreales,
Entomophthorales and Eurotiales were reported from 12 bark beetle and 10
lepidopteran species collected in 53 localities in Bulgaria. Several laboratory and
eld bioassays with entomopathogenic fungi were conducted and introductions of
two entomophthoralean fungi were performed. In order to improve the biological
control of forest pest insects the research on the entomopathogenic fungi should
continue and should be intensied.
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