ArticlePDF Available

List of natural fungal pathogens infecting bark beetles and lepidopteran forest pests from Bulgaria, Annual of Natural Sciences Department, New Bulgarian University. Volume 5, 88-99.

Authors:

Abstract and Figures

Abstract: Information about fungal infections detected in different bark beetles and lepidopteran forest pests in Bulgaria is presented. Eighteen species of entomopathogenic fungal species and numerous isolates of orders Hypocreales, Eurotiales и Entomophthorales have been reported from 12 bark beetles and 10 moths within a sixty years period. The results from conducted laboratory and field bioassays with several isolates of entomopathogenic fungi against bark beetles and the gypsy moth were summarized.
Content may be subject to copyright.
88
Годишник на департамент „Природни науки“, 20182019
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 Soa, Bulgaria
2Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of
Sciences, 1 Tsar Osvoboditel Blvd., 1000 Soa, Bulgaria
3University of Forestry, 10 Kliment Ohridski Blvd., 1797 Soa, 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 dierent 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
89
Annual of Natural Sciences Department, 2018–2019
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 eects on non-target organisms in
treated areas and in the larger watersheds.
The most signicant 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 & Schiermüller), 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 dierent 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 specicity of entomopathogenic fungi varies. While some species are
very host specic, 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 dierent authors [Wegensteiner et al., 2015]. Moreover entomopath-
ogenic fungi were evaluated as bark beetles control agents. The most studied
90
Годишник на департамент „Природни науки“, 20182019
species was B. bassiana. Various bioassays have been conducted against dier-
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 dierent 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].
91
Annual of Natural Sciences Department, 2018–2019
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
92
Годишник на департамент „Природни науки“, 20182019
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
93
Annual of Natural Sciences Department, 2018–2019
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 – Karaml 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.
94
Годишник на департамент „Природни науки“, 20182019
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
95
Annual of Natural Sciences Department, 2018–2019
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 dierent isolates of B. bassiana
caused the highest lethal eect 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 signicantly higher when compared to control
treatments. Initial eect 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 aected 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.
96
Годишник на департамент „Природни науки“, 20182019
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] conrmed 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 aected 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 dierent 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 dierent 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].
97
Annual of Natural Sciences Department, 2018–2019
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 intensied.
REFERENCES
Castrillo L.A., M.H. Griggs, C.M. Ranger, M.E. Reding, J.D. Vandenberg, Virulence
of commercial strains of Beauveria bassiana and Metarhizium brunneum
(Ascomycota: Hypocreales) against adult Xylosandrus germanus (Coleoptera
Curculionidae) and impact on brood, Biological Control 58, 2011, 121-126.
Day K., S. Leather, Threats to forestry by insect pests in Europe. In: Watt A., N.
Storck, D. Hunter (Eds.), Forests and Insects, 1997, 177-207.
Doane C. Beauveria bassiana as a pathogen of Scolytus multistriatus, Annals of
the Entomological Society of America 52, 1959, 109-111.
Draganova S., D. Takov, D. Doychev, Bioassays with isolates of Beauveria bas-
siana (Bals.,) Vuill. and Paecilomyces farinosus (Holm.) Brown and Smith
against Ips sexdentatus Boerner and Ips acuminatus Gyll. (Coleoptera: Sc-
olytidae), Plant Sciences 44 (1), 2007, 24-28.
Draganova S., D. Takov, D. Doychev, Naturally occurring entomopathogenic
fungi on three bark beetle species (Coleoptera: Curculionidae) in Bulgaria,
Pesticides and Phytomedicine 25, 2010, 59-63.
Draganova S., D. Pilarska, D. Takov, D. Doychev, Utilization of carbohydrates
by Beauveria bassiana isolates obtained from forest pests, Journal of Plant
Protection Research 51 (4), 2011, 349-354.
Draganova S., D. Takov, D. Pilarska, D. Doychev, P. Mirchev, G. Georgiev, Fun-
gal pathogens on some lepidopteran forest pests in Bulgaria, Acta zoolog-
ica bulgarica 65, 2013, 179-186.
Draganova S., D. Doychev, D. Pilarska, D. Takov, Bioassays of entomopatho-
genic fungi against xylophagous insects in Bulgaria: Laboratory and eld
Experiments, Acta zoologica bulgarica 69, 2017, 411-419.
Georgieva M., D. Takov, G. Georgiev, D. Pilarska, P. Pilarski, P. Mirchev, R.
98
Годишник на департамент „Природни науки“, 20182019
Humber, Studies on non-target phyllophagous insects in oak forests as po-
tential hosts of Entomophaga maimaiga (Entomophthorales: Entomoph-
thoraceae) in Bulgaria, Acta zoologica bulgarica 66, 2014, 115-120.
Karpinksi J.J. Przyczyny organiczajce rozmnazanie sie kormikow drukarzy
(Ips typographus L. i Ips duplicatus Sahlb.) w lesie pierwotnym, Instytut
Badawczy Lasow Panstwowych, Seria A – Rozprawy I sprawozdania, 15,
gypsy moth, 1935, 1-86.
Markova G. Pathogenicity of several entomogenous fungi to some of the most seri-
ous forest insect pests in Europe, IOBC/wprs Bulletin 23 (2), 2000, 231-239.
Markova G., G. Georgiev, Beauveria bassiana – a pathogen on Satin Moth (Stilp-
notia salicis), Gorsko stopanstvo 5, 1992, 22. (In Bulgarian)
Mirchev P. Longevity of Lymantria dispar L. at the pupa stage in low species
population number, Forest Science 3, 2004, 77-85. (In Bulgarian, Eng-
lish summary)
Mirchev P., G. Georgiev, S. Draganova, Disease caused by Beauveria bassiana
(Bals.Criv.) Vuill. on new hatched larvae of Thaumetopoea solitaria Frey-
er, 1838, Silva Balcanica 13 (1), 2012, 61-65.
Novak V., A. Samsinakova, Les essais d`aplication du champignon parasite
Beauveria bassiana (Bals.) Vuill. dans la lutte contre les parasites en agri-
culture et sylviculture en CSSR, Colloques Internationaux de Pathologique
des Insectes, Paris, 1962, 133-135.
Panajotov P., B. Zashev, R. Grigorova, G. Tsankov, Entomopathogenic fungi on
caterpillars of Lymantria dispar L. in Bulgaria, Bulletin de l‘Institut central
des forests 6, 1960, 205-208.
Petch T. A list of the entomogenous fungi of Great Britain, Transaction of the
British mycological Society 17, 1932, 170-178.
Pilarska D., R. Zimmermann, A. Linde, M. McManus, D. Takov, On the occur-
rence of Entomophaga aulicae in high density browntail moth (Euproctis
chrysorrhoea L.) populations in Bulgaria, Proceedings of Third Balkan
Scientic Conference, Study, Conservation and Utilisation of Forest Re-
sources, III, Soa, 2-6.10.2001, 139-143.
Pilarska D., G. Georgiev, V. Golemansky, P. Pilarski, P. Mirchev, M. Georgieva,
M. Tabakovic-Tosic, M. Todorov, D. Takov, M. Pernek, B. Hrasovec, M.
Milotoc, M. Dautabasic, O. Mujezinovic, S. Naceski, I. Anakieva-Papazo-
va, M. Matova, P. Vafeidis, Entomophaga maimaiga (Entomophthorales,
Entomophthoraceae) in Balkan peninsula – an overview, Silva Balcanica
17, 2016, 31-40.
Pilarska D., G. Georgiev, M. Dobreva, D. Takov, P. Mirchev, D. Doychev, M.
Georgieva, R. Nachev, P. Dermendzhiev, S. Draganova, A. Linde, A.E. Ha-
jek, Pathogens and parasitoids of forest pest insects in the region of Forest
Protection Station Plovdiv during the period 1990 – 2017, Silva Balcanica
19 (3), 2018, 41-49.
99
Annual of Natural Sciences Department, 2018–2019
Siemaszko W. Fungi associated with bark beetle in Poland, Planta Polonica 7,
1939, 1-54.
Takov D., D. Pilarska, R. Wegensteiner, Occurrence of pathogens in Ips typogra-
phus (Coleoptera, Scolytidae) from several Picea abies (L.) (Karst.) stands
in Bulgaria, Acta zoologica bulgarica 58, 2006, 409-420.
Takov D., D. Doychev, R. Wegensteiner, D. Pilarska, Study on the pathogens of
bark beetles (Coleoptera, Scolytidae) from dierent coniferous stands in
Bulgaria, Acta zoologica bulgarica 59, 2007, 87-96.
Takov D., D. Doychev, A. Linde, S. Draganova, D. Pilarska, Pathogens of bark
beetles (Coleoptera: Curculionidae) in Bulgarian forests, Phytoparasitica
39, 2011, 343-352.
Takov D., D. Doychev, A. Linde, S. Draganova, D. Pilarska, Pathogens of bark
beetles (Curculionidae: Scolytinae) and other beetles in Bulgaria, Biologia
67 (5), 2012, 966-972.
Takov D., D. Pilarska, D. Doychev, S. Nedelchev, S. Draganova, Investigations on
the complex of pathogens and parasites in spruce bark beetle Ips typogra-
phus in Bulgaria – A review, Annual of Department of Natural Sciences,
New Bulgarian University, 2019, 53-61.
Wegensteiner R. Pathogens in bark beetles, In: Lieutier F., K. Day, A. Battisti,
J.-C. Gregoire, H. Evans (Eds.), Bark and wood boring insects in living
trees in Europe, a synthesis, Dordrecht, the Netherlands: Kluwer Academic
Publishers, 2004, 291-313.
Wegensteiner R., B. Wermelinger, M. Herrmann, Natural enemies of bark bee-
tles: Predators, parasitoids, pathogens and nematodes. In: Vega F.E., R.W.
Hoftstetter (Eds.), Bark Beetles: Biology and Ecology of Native and Inva-
sive Species, Academic Press, London, 2015, 247-304.
Zaemdzhikova G., P. Mirchev, G. Georgiev, Economically important insect pests
in Bulgarian forests during the period 2003-2018, Forest science 55 (2),
2019, 105-113.
... Due to the specific features of bark beetle life cycle, namely its hidden lifestyle under the bark, effective control measures are quite limited and often reduced to the sanitary felling of infested trees [ 2 ]. During the past decades, a number of researchers have studied natural enemies of bark beetles, with emphasis on pathogens causing infectious diseases in natural populations [3][4][5][6]. In particular, hypocrealean entomopathogenic fungi (Ascomycota: Hypocreales) are considered promising control agents [ 4 ] with no adverse effects on trees, forest vertebrates or humans [ 7 ]. ...
Article
Full-text available
Efficacy of entomopathogenic fungus Metarhizium pemphigi was evaluated against Ips typographus adults in a laboratory bioassay for the first time. A series of four conidial concentrations (2×104–2×107 conidia/ml) were used. The cumulative mortality caused by M. pemphigi varied between 75% and 100% ten days post-treatment, with LC50 value of 2.9×103 conidia/ml and LC90 value of 6.4×104 conidia/ml. The median lethal time (LT50) of treated beetles depended on conidial concentrations and ranged from 1.78 to 5.98 days. Pathogenicity of M. pemphigi was reported for the first time and the tested strain was found to be promising for further evaluation in terms of management options against the spruce bark beetle.
Article
Full-text available
The pathogen complex of the spruce bark beetle, Ips typographus of the Vitosha and the Rhodope mountains area in Bulgaria was surveyed and evaluated. Beetles were collected from four different localities including one reserve and three managed spruce stands from March 2003 to August 2005. The following pathogens were recovered: I. typographus Entomopoxvirus (ItEPV), Gregarina typographi, Chytridiopsis typographi, Beauveria bassiana, and the nematodes Contortylenchus diplogaster and Cryptaphelenchus macrogaster. ItEPV, G. typographi, Ch. typographi, C. diplogaster and C. macrogaster are new species to the Bulgarian fauna. The dominant pathogen species was G. typographi, which was found in beetles from all sites. In several cases male beetles showed significantly higher G. typographi infection rates than female beetles. No gender dependant differences in the infection rates were observed for C. typographi and ItEPV. The pathogen distribution in single and mixed infections was higher in the beetles from the Bistrishko Branishte Reserve.
Article
Full-text available
Ips typographus is one of the major insect pest species on Norway spruce (Picea abies) in Bulgaria. The species infests wind-thrown trees or wind-broken logs, but also attacks physiologically stressed living trees. The global climate changes influence negatively the spruce forest health and create conditions for its massive infestation. After 2003, research in this area started more intensively. To study I. typographus pathogens and parasites, nine localities in Vitosha, Lуulin and Rhodope Mountains were chosen as collection sites. In the period 2003 - 2018, 2916 individuals of Ips typographus were examined for the presence of pathogens and parasites. As a result of conducted studies - a virus, a protozoan, a microsporidium, a fungus and nematodes were detected. The protozoan Gregarina typographi was relatively high in the beetles from all studied sites and was the dominant pathogen species. The percentage of infected beetles varied from 1.4% to 50.4%. The prevalence of the microsporidium Chytridiopsis typographi ranged from 0.8% to 8% in the host beetles. Five nematode species (four parasite and one associated with the host beetles) were also found. The infection rates of nematodes ranged from 38.8% to 96.2% for different localities. Important data about pathogen localization, distribution and infection levels were established. Annual of Natural Sciences Department
Article
Full-text available
During the period 1990-2017, a survey of the entomopathogens and parasitoids of several pest insects was conducted, including the lepidopterans Lymantria dispar, Euproctis chrysorrhoea, Leucoma salicis, Malacosoma neustria, Orthosia cerasi, Aporia crataegi, Operophtera brumata, Eilema complana, Tortix viridana, Archips xylosteana, Paranthrene tabaniformis, Gypsonoma aceriana, Thaumetopoea pityocampa, T. solitaria, Phyllocnistis unipunctella, the coleopterans Saperda populnea, Ips typographus, I. acuminatus, I. sexdentatus, Pityogenes chalcographus, Dryocoetes autographus, Hylurgops palliatus, Phyllobius sp. and the hymenopterans Diprion pini, Neodiprion sertifer, Gilpinia sp. and Tremex fuscicornis. As a result of these studies 5 viruses, 1 protozoan species, 7 microsporidian species, 5 species of entomopathogenic fungi and 46 parasitoid species have been documented in 27 host insects collected in the region of the Forest Protection Station Plovdiv. The first successful introduction in Bulgaria of the entomopathogenic fungus Entomophaga maimaiga in populations of L. dispar was conducted in 1999 in the region of the Forest Protection Station at Plovdiv (in the village of Gorni Domlyan, Karlovо Forestry) and 7 subsequent introductions were later performed in the region of the station. As a result, L. dispar density has been maintained at low levels in that area and only 60 hectares were sprayed with insecticides for L. dispar control in the last 18 years. Another success was the first field release in Europe and Bulgaria of the entomopathogenic fungus Entomophaga aulicae in a healthy population of the brown tail moth, Euproctis chrysorrhoea, in 2016 in the village of Zhenda (Kardzhali Forestry). Investigations in 2017 showed that 19% of E. chrysorrhoea larvae sampled from release sites had died due to infection by E. aulicae.
Article
Full-text available
Six isolates of Beauveria bassiana (Bb) and one Metarhizium anisopliae (Ma) isolate were tested against adults of the European spruce bark beetle, Ips typographus, in laboratory assays. At a dosage of 1.5 x 106 conidia/cm2, mortality was significantly higher for treated I. typographus than for control individuals. Mortality rates of I. typographus reached 100% at four days post treatment with the isolates 619Ma, 638Bb and 639Bb. Field bioassays were then conducted using these three isolates in the Vitosha Mt., Bulgaria. Spruce logs were treated with conidial suspensions (106 conidia/cm2). Three months later, bark was peeled from the logs and 1126 beetles belonging to ten coleopteran species (Curculionidae and Cerambycidae) were collected, identified and analysed for fungal pathogens. Analysis revealed natural occurrence of B. bassiana, B. caledonica and Isaria farinosa. Mortality rates of beetles collected from logs treated with 562Bb, 638Bb and 619Ma were 3.88%, 23.08% and 30.56%, respectively, and isolates 638Bb and 619Ma were significantly different from controls (P = 0.001). Isolate 562Bb was marginally significantly different from the control (P = 0.05). Results showed the potential to inoculate bark beetles with entomopathogenic fungi by treating spruce tree logs.
Article
Full-text available
Through a fifteen-year period, by the continuous monitoring to establish the distribution of Entomophaga maimaiga in Bulgaria, it is clear that the fungus already occurs in many localities among 22 State Forest and/or Hunting Enterprises where it was introduced or has spread by natural means. Consequently, as a result of the introduction of E. maimaiga in Bulgaria, almost no insecticides were used over the past 15 years and more than 10 million BGN (5 million Euros) were saved. E. maimaiga epizootics occurred in the neighbouring countries in 2005, 2010 and 2011, intensifying the spread further, so by the end of 2013 it expanded its range throughout the Balkan Peninsula. The fungus is now present, and to our best knowledge, it was established in Serbia, FYRMacedonia, Greece, European part of Turkey, Croatia and Bosnia and Herzegovina. It has clearly shown a dramatic impact on gypsy moth populations, possessing a capability to cease gypsy moth outbreaks and maintain pest population density at low levels under favourable climatic conditions.
Article
Full-text available
Carbohydrate utilization profiles of ten isolates of the entomopathogenic fungus Beauveria bassiana (Bals.-Criv.) Vuillemin were studied and compared to assist in determining their phenotypic characterization. Isolates were obtained in pure cultures from dead individuals of several forest pests collected from different regions in Bulgaria. Studies on utilization profiles were based on the acidification of twenty carbohydrates. The results indicate that sucrose, maltose and trehalose were assimilated at a high degree compared to esculin, arabinose and dul-citol. According to the results of a cluster analysis of the carbohydrate utilization profiles, the B. bassiana isolates were divided into two larger groupings. All isolates in the first larger cluster were obtained from the coleopteran insects – Stenomax aeneus, Ips typographus, I. sexdentatus and Dryocoetes autographus. Isolates from the other cluster were obtained from the lepidopteran larvae of Thaumetopoea pityocampa and Lymantria dispar, and from an adult of the coleopteran species Hylurgops palliatus. We determined that each B. bassiana isolate exhibited a different and specific carbohydrate utilization profile but differences at the p-level < 0.05 were significant among some of them. The most distinguishable was the isolate 560Bb obtained from T. pityocampa. Differences between the isolate 560Bb and the other nine B. bassiana isolates were highly significant at the p-level < 0.005. Isolate 433Bb obtained from a dead adult of I. typogra-phus was significantly different from five of the studied isolates at the p-level < 0.05.
Article
Full-text available
The impact of entomopathogenic fungus Entomophaga maimaiga HUMBER, SHIMAZU & SOPER (Entomophthorales: Entomophthoraceae) on the complex of phyllophagous insects in oak forests in Bulgaria was studied during the period 2009-2011. From 15 populations of gypsy moth, Lymantria dispar (L.), i.e. six sites where E. maimaiga was introduced and nine sites where the pathogen occurred naturally, a total of 1499 larvae of non-target phyllophagous insects were collected. These insects belonged to 38 species of 10 families of Lepidoptera: Lycaenidae (1 species), Tortricidae (5), Pyralidae (1), Ypsolophidae (1), Geometridae (11), Noctuidae (8), Nolidae (1), Erebidae (5), Notodontidae (1), Lasiocampidae (2) as well as to two species of Tenthredinidae (Hymenoptera). Microscopic analyses indicated no presence of E. maimaiga life stages in any of dead larvae. In one species, Catocala nymphagoga (Esper) (Lepidoptera: Erebidae), the entomopathogenic fungi Entomophaga aulicae (Reich.) Humber, Tarichium dissolvens (Vosseler) Lakon, Isaria farinosa (Holmsk.) Fr, Beauveria bassiana (Bals.-Criv.) Vuill., Beauveria sp., Conidiobolus sp. and Lecanicillium sp. did cause high mortality of larvae and pupae (between 39.1 and 100%, average 61.8%). The present study represents the first record of Tarichium dissolvens in Bulgaria. The results of this study confirm that E. maimaiga is a host-specific pathogen of gypsy moth and its introduction is not dangerous for the non-target insect species in these oak forests.
Chapter
The occurrence and action of natural enemies of bark beetles (Coleoptera: Curculionidae, Scolytinae) are reviewed. Bark beetles have a diverse and important community of natural enemies. The community includes predators such as birds, beetles, flies, true bugs, and mites; parasitoids such as wasps and flies; pathogens such as viruses, bacteria, fungi, microsporidia, and protozoa; as well as nematodes. The general ecology of the various taxonomic groups is discussed and some of the species most relevant to biological control are treated in detail. Morphological descriptions and the biology of pathogens, field data on natural enemies’ prevalence and geographical distribution are presented. The role of these antagonistic agents in bark beetle population dynamics and their potential for use as biological control agents are evaluated based on literature, data from experiments, observations in the field, and from controlled laboratory experiments.