ArticlePDF Available

Pathogens and Parasitoids of Forest Pest Insects in the Region of the Forest Protection Station on Plovdiv (Bulgaria), during the period 1990-2017

Authors:

Abstract

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.
41
Silva Balcanica, 19(3)/2018 DOI: 10.6084/m9.gshare.8198294
PATHOGENS AND PARASITOIDS OF FOREST PEST INSECTS
IN THE REGION OF FOREST PROTECTION STATION PLOVDIV
DURING THE PERIOD 1990 – 2017
Daniela Pilarska1,2, Georgi Georgiev3, Maria Dobreva4, Danail Takov2, Plamen Mirchev3,
Danail Doychev5, Margarita Georgieva5, Rumen Nachev4, Pencho Dermendzhiev4,
Slavimira Draganova6, Andreas Linde7, Ann E. Hajek8
1New Bulgarian University – Soa, Department of Natural Sciences
2Institute of Biodiversity and Ecosystem Research – Soa, Bulgarian Academy of
Sciences 3Forest Research Institute – Soa, Bulgarian Academy of Sciences,
4Forest Protection Station Plovdiv
5Forestry University – Soa
6Institute of Soil Science, Agrotechnology and Plant Protection
‘Nikola Poushkarov’ – Soa
7 Eberswalde University for Sustainable Development – Eberswalde
8 Department of Entomology, Cornell University, Ithaca – New York
Abstract
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, aumetopoea 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.
e rst 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 rst eld 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.
Key words: insect pests, pathogens, parasitoids, Entomophaga maimaiga, biological control
Forest pest insects are a major cause of economic and aesthetic loss in forestry
systems and are of particular concern as forest habitats become more fragmented, land
use pressures increase, and climate change impacts forest ecosystems.
Many insects in Bulgaria attained pest status when plantation forestry increased in
importance and created monocultures that favour pest outbreaks. e most signicant
42
pests of Bulgarian forests are species in the orders Coleoptera and Lepidoptera. In the
coniferous forests bark beetles (Coleoptera: Curculionidae) and the processionary moth,
aumetopoea pityocampa (Denis & Schiermüller) (Lepidoptera: Notodontidae) are
of greatest concern. Important pests of broadleaf forests include moths in the families
Erebidae [Lymantria dispar (Linnaeus), Euproctis chrysorrhoea (Linnaeus), Leucoma salicis
(Linnaeus)], Tortricidae [Archips xylosteana (Linnaeus), Tortrix viridana Linnaeus] and
Geometridae [(Operophtera brumata (Linnaeus), Erannis defoliaria (Clerck), Alsophila
aescularia (Denis et Schiermüller), Alsophila aceraria (Denis et Schiermüller)]. ese
pests can cause signicant damage and each year huge areas of forests are aected. Forestry
administrations are committed to reducing the use of pesticides in the environment and
to emphasizing the use of biological control agents.
Pathogens and parasitoids as natural enemies are such control agents that play
important roles in regulating population densities of forest pest insects.
In the region of Plovdiv Forest Protection Station the main pests during the last
twenty years are the lepidopterans T. pityocampa, L. dispar, E. chrysorrhoea, A. xylosteana,
T. viridana, E. defoliaria, O. brumata and the bark beetles Ips typographus (Linnaeus), Ips
acuminatus (Gyllenhal), Ips sexdentatus (Börner) and Pityogenes chalcographus (Linnaeus).
In order to set the stage for practical application of conservation practices and
control measures for the biological protection of our forest ecosystems, a survey of
entomopathogens and parasitoids of several pest insects was conducted in the region of
the Forest Protection Station Plovdiv.
In this paper we present results of investigations on pathogens and parasitoids of
pest lepidopterans, coleopterans and hymenopterans.
As a result of our studies 5 viruses, 1 protozoan species, 7 microsporidian species,
5 species of entomopathogenic fungi, and 46 parasitoid species have been documented
in 27 insect species collected in the region of the Forest Protection Station Plovdiv during
the years 1990 – 2017.
Viruses
Five viruses were detected in the lepidopterans L. dispar, T. pityocampa, L. salicis,
the bark beetle I. typographus and the hymenopteran Neodiprion sertifer (Georoy).
e rst virus was the L. dispar nuclear polyhedrosis virus (LdNPV; Baculoviridae).
LdNPV infects all tissues and develops in the nuclei of infected cells. It was detected
in 1999 in 2.3% of the gypsy moth larvae collected in Gorni Domlyan village,
Karlovo State Forestry, where in the same year the rst successful introduction of the
fungus Entomophaga maimaiga Humber, Shimazu & Soper (Entomophthoromycota,
Entomophthorales) was conducted (Pilarska et al., 2000). e same virus was detected
in 2003 in 85.2% in larvae collected in the region of Chekeritsa State Game Enterprise
(Annual Report of Forest Protection Station Plovdiv, 2003) .
In 2004, after an outbreak of the satin moth, L. salicis, in the region of Plovdiv
State Forestry, an epizootic caused by an undetermined nuclear polyhedrosis virus was
observed. As a result, 69% of the collected larvae died with symptoms of NPV (Annual
Report of Forest Protection Station Plovdiv, 2004).
43
In 2008, a granulosis virus, TpGV (Baculoviridae), was detected in dead larvae of
the pine processionary moth, T.pityocampa, collected from the village of Banya, Karlovo
State Forestry. Viral infections caused 100% mortality of pine processionary moth larvae
(Annual Report of Forest Protection Station Plovdiv, 2008).
During the period 2003 and 2011, an entomopox virus, ItEPV Wegensteiner &
Weiser (Entomopoxviridae) was observed in spruce bark beetles, I. typographus, collected
in Beglika, Batak State Forestry and Borino, Borino State Forestry. ItEPV spheroids were
detected in midgut epithelial cells. Prevalence of this virus in the beetles collected in Beglika
in 2005 was 16.6 and the virus caused 4.7% infection in 2011. In Borino the virus was
detected in 2003 in 3.8% of the investigated individuals (Takov et al., 2006, 2007).
e fth virus documented in the region of Forest Protection Station Plovdiv
was the nuclear polyhedrosis virus of the satin moth Neodiprion sertifer (Georoy). It
was detected in the region of Karlovo State Forestry in 2016, where 1.8 ha of pine trees
were infested with the satin moth. is virus caused 50% mortality of the sawy larvae
(Annual Report of Forest Protection Station Plovdiv, 2016).
Protozoa
Protozoa of the genus Gregarina (Apicomplexa, Eugregarinoida) were detected
in three bark beetle species: I. typographus, I. acuminatus and I. sexdentatus. Gregarina
typographi Fuchs was detected in I. typographus collected in three sites: Beglika, Borino
and Yundola from 2003 to 2011 (Takov et al., 2006, 2007, 2012). is gregarine was
observed in the midgut lumen of beetles collected in Beglika in 2005 and 2011, with a
prevalence of 16.6% and 31.7%, respectively. In Borino, 7.3% of all investigated beetles
were infected with G. typographi in 2003 and 5.9% in 2005. e pathogen was also
found in 5.1% of individuals collected in Yundola in 2009. Gregarina spp. were also
found in I. acuminatus (prevalence of 7.2% in Borino in 2005) (Takov et al., 2007)
and in I. sexdentatus (prevalence of 11.1% in Slaveyno State Forestry in 2017) (Annual
Report of Forest Protection Station Plovdiv, 2017).
Microsporidia
In total, seven microsporidian species (Microsporidia) were detected in the gypsy
moth L.dispar, E. chrysorrhoea, tortricids and I. typographus.
e rst microsporidian documented in the study period was Endoreticulatus
schubergi (Zwolfer) Cali et Garhy in L. dispar in 1996 and 1997, near Asenovgrad
(Asenovgrad State Forestry). It infects the gut epithelium and is transmitted horizontally
by oral uptake of spores. e prevalence of E. schubergi in the host population increased
with the growth of the host larvae as the season progressed. e prevalence of E. schubergi
in 1996 varied from 2.0 to 11.5% (average 6.1%) and in 1997 varied from 27.0 to
56.0% (average 3.2%) (Pilarska et al., 1998).
In the same host, a second microsporidian species, Nosema lymantriae Weiser was
detected in two sites (Chekeritsa State Game Enterprise and Gorni Domlyan, Karlovo
State Forestry) in 2009 and 2010. is microsporidium infects the fat body, silk glands,
Malpighian tubules and gonads. It is transmitted horizontally and transovarially. e
44
prevalence in Chekeritsa was 13.9% (2009) and 1.9% in Gorni Domlyan (2010) (D.P.,
unpublished).
In 2000, 72 brown tail moth, E. chrysorrhoea, populations in Balkan, Sredna
Gora, Sakar and Rodope Mountains were screened for microsporidian infections. In 13
populations collected in Sakar and Rodope Mountains, a Nosema sp. was detected, and
in 8 populations in Balkan, Sredna Gora and Sakar Mountains an Endoreticulatus sp.
was observed (Pilarska et al., 2001a). e prevalence of Nosema sp. was 37.9% (Rodope
Mt.) and 21.4% (Sakar Mt.), and the prevalence of Endoreticulatus sp. in Balkan and
Sredna Gora Mountains was 11.1% and 10.0%, respectively (Annual Report of Forest
Protection Station Plovdiv, 2000).
An undetermined Nosema isolate was discovered in the fat body tissues and silk
glands of larvae of Orthosia cerasi (Fabricius) from Gorni Domlyan in 2010, with a
prevalence of 20.0% (Pilarska et al., 2017).
In 2011, during an investigation of newly hatched tortricid larvae from the
region of Rakitovo and Alabak Forestry Stations, another Nosema sp. was detected. Its
prevalence was 12.5% in the larvae from Rakitovo and 5.0% in the larvae from Alabak
(Annual Report of Forest Protection Station Plovdiv, 2011).
Chytridiopsis typographi Weiser was found in the bark beetle I. typographus,
collected in 2003 in Borino and in 2011 in Beglika. Spores were observed in the cells of
the midgut epithelium, enclosed in sporophorous vesicles or without such enclosures.
Prevalence was 1-6% in beetles from Beglika and 3.8% in beetles from Borino (Takov et
al., 2006, 2012).
Fungi
In total, ve species of entomopathogenic fungi were detected in the lepidopterans
L. salicis, E. chrysorrhoea, L. dispar, E. defoliaria, aumetopoea solitaria (Freyer),
T.pityocampa, Malacosoma neustria (Linnaeus), Aporia crataegi (Linnaeus), T. viridana,
in the bark beetles Dryocoetes autographus (Ratzeburg), Hylurgops palliatus (Gyllenhal),
and in the weevil Phyllobius sp.
e rst fungal entomopathogen discovered was Entomophaga aulicae (E. Reichardt)
Humber (Entomophthoromycotina, Entomophthorales) in 16 outbreak populations of
brown tail moth, E. chrysorrhoea, in Balkan, Sakar, Sredna Gora and Rodope Mountains
in 2000. e fungus was identied as the cause of high larval mortality with the result of
a reduced population density of this moth (Pilarska et al., 2001b).
In 2016, mortality of brown tail moth larvae was also observed in the region of
Asenovgrad State Forestry. Microscopic analyses showed that mortality was also caused
by E. aulicae. In order to preserve inoculum of the fungus, dead brown tail moth larvae
were collected and stored in the soil humus layer (Pilarska et al., 2016a).
e third fungal pathogen identied was the hypocrealean fungus Beauveria
bassiana (Balsamo) Vuillemin (Ascomycota, Hypocreales), found in dead larvae of
L. salicis (Markova, Georgiev, 1992), T. solitaria (Mirchev et al., 2012), L. dispar, A.
crataegi, E. defoliaria, T.pityocampa, M. neustria, T. viridana, D. autographus, H. palliatus
and Phyllobius sp., collected from 20 sites (Draganova et al., 2013).
45
Aspergillus niger van Tieghem (Ascomycota, Eurotiales) was found in E. defoliaria,
another Aspergillus sp. was detected in T. pityocampa, L. dispar and T. viridana, and in
T. pityocampa, M. neustria and T. viridana an entomopathogenic fungus belonging to
the genus Fusarium Link was discovered (Ascomycota, Hypocreales) (Draganova et al.,
2013).
Introduction and release of entomopathogenic fungi
e rst successful introduction of the entomopathogenic fungus Entomophaga
maimaiga into populations of L. dispar in Bulgaria was conducted in 1999 in the region
of the Forest Protection Station at Plovdiv, in the village of Gorni Domlyan (Karlovо
Forestry) (Pilarska et al., 2000). In the period 2000-2004 the prevalence of E. maimaiga
in local populations of L. dispar ranged from 6.1% (2000) to 15.9% (2004). However,
the fungus persisted in the introduction site and in 2005, massive epizootics caused by
this fungus were recorded in State Forestry Haskovo and State Forestry Kirkovo (Pilarska
et al., 2007). In 2012 fungal epizootics were reported from the regions of State Forestry
Haskovo and Harmanli with larval mortality of 100%. In the period 2005-2013, seven
subsequent introductions were performed in the region of the Forest Protection Station
Plovdiv (Georgiev et al., 2013; Pilarska et al., 2016b). As a result, the L. dispar density
has remained at low levels in that area and only 60 hectares had to be sprayed with
insecticides for L. dispar control during the last 18 years.
e release of the entomopathogenic fungus Entomophaga aulicae using the
methodology for introduction of E. maimaiga was an attempt to conduct biological
control against one of the most important insect pests – the brown tail moth. erefore, in
2016, we conducted the rst controlled eld release of E. aulicae in Bulgaria, in a healthy
population of E.chrysorrhoea in the village of Zhenda (Kardzhali State Forestry) (Pilarska
et al., 2017b). e release of E. aulicae was performed in the beginning of November
2016 using the inoculum from an outbreak site of E. chrysorrhoea in Asenovgrad. Our
investigations in 2017 showed that the introduction was successful, with 19% of E.
chrysorrhoea larvae sampled from the release sites dying due to infections caused by E.
aulicae (Annual Report of Forest Protection Station Plovdiv, 2017).
Parasitoids
In total, 46 parasitoid species were detected in 11 insect hosts: the small poplar
longhorn beetle Saperda populnea (Linnaeus), the lepidopterans Phyllocnistis unipunctella
(Stephens) (syn. Phyllocnistis suusella Z.), Gypsonoma aceriana (Duponchel), Paranthrene
tabaniformis (Rottemburg), L. salicis, T. pityocampa, T. solitaria, the sawies Diprion pini
(Linnaeus), N. sertifer, Gilpinia sp., and the tremex wasp Tremex fuscicornis (Fabricius).
In S. populnea larvae, 5 hymenopteran and dipteran parasitoids were found in
Plovdiv, Ognyanovo, Simeonovgrad, Manole, and Klisura regions: Iphiaulax impostor
(Scopoli) (Hymenoptera: Braconidae), Dolichomitus populneus (Ratzeburg), Xylophrurus
lancifer (Gravenhorst), Gelis ornatulus (omson) (Hymenoptera: Ichneumonidae) and
Billaea irrorata (Meigen) (Diptera: Tachinidae) (Georgiev, 2001a; Georgiev et al., 2004).
G. ornatulus was found as a hyperparasitoid.
46
In P. unipunctella larvae, 10 primary and secondary hymenopteran parasitoids
were found in the Pazardzhik region: Chrysocharis nephereus (Walker), Chrysocharis sp.
1, Chrysocharis sp. 2, Cirrospilus elegantissimus Westwood, Cirrospilus lyncus Walker,
Cirrospilus pictus (Nees), Kratoisma usticrus (Erdös), Sympiesis sericeicornis (Nees),
Sympiesis sp. and Tetrastichus sp. (Hymenoptera: Eulophidae) (Georgiev, Pelov, 1996;
Georgiev, 2005). e hyperparasitoid Tetrastichus sp. was detected in K. usticrus, C.
nephereus, S. gyori, S. sericeicornis and Sympiesis sp. e host mortality caused by all
parasitoid species reached up 77.6%, and K.usticrus had the strongest impact on the host
population (Georgiev, 2005).
In G. aceriana larvae, 6 hymenopteran parasitoids were found in the Pazardzhik
region: Bracon variator Nees, Macrocentrus marginator (Nees), Orgilus obscurator (Nees),
Apanteles erevanicus Tobias (Hymenoptera: Braconidae), Pristomerus ruabdominalis
Ucida and Pristomerus vulnerator (Panzer) (Hymenoptera: Ichneumonidae) (Georgiev,
1995). e total mortality of G. aceriana larvae caused by parasitoids ranged between
5.9 and 28.6% in the rst host generation and between 35.8-44.4% in the second host
generation (Georgiev, Samuelian, 1999). A. erevanicus was the most common parasitoid,
causing host mortality of up to 27.5%.
In larvae of P. tabaniformis, 5 parasitoids were found in the Pazardzhik region:
Apanteles evonymellae (Bouché), Bracon intercessor Nees (Hymenoptera: Braconidae),
Eriborus terebrans (Gravenhorst), Pristomerus vulnerator (Panzer) and Dolichomitus
populneus (Ratzeburg) (Hymenoptera: Ichneumonidae) (Georgiev, Tsankov, 1995;
Georgiev et al., 2001). Host mortality caused by all parasitoid species was 27.6%, and A.
evonymellae was the most common parasitoid, causing host mortality of 18.6%.
In L. salicis larvae and pupae, 9 parasitoid species were found in the Pazardhik region:
eronia atalantae (Poda) (Hymenoptera: Ichneumonidae), Brachymeria intermedia
(Nees), Brachymeria minuta (Linnaeus) (Hymenoptera: Chalcididae), Monodontomerus
aereus Walker (Hymenoptera: Torymidae), Compsilura concinnata (Meigen), Exorista
larvarum (Linnaeus), Pales pavida (Meigen) (Diptera: Tachinidae), Agria mamillata
(Pandelle) (Diptera: Sarcophagidae) and Megaselia sp. (Diptera: Phoridae) (Georgiev,
1996a). Six species (B. intermedia, M. aereus, C. concinnata, E. larvarum, P. pavida and
A. mamillata) were conrmed as primary parasitoids. One species (T. atalantae) was both
a primary and secondary parasitoid, and two species (B. minuta and Megaselia sp.) as
hyperparasitoids on P.mamillata. e parasitoids reduced the pest population by 36.7%,
and A. mamillata and B. intermedia had the strongest impacts.
In T. pityocampa, 7 egg parasitoids were found in Kurtovo, Banya, Yanino, Kardzhali,
Ivaylovgrad, Rozino, and Klisura regions: Baryscapus servadeii (Domenichini), Baryscapus
transversalis Graham, Pediobius bruchicida Rondani (Hymenoptera: Eulophidae),
Anastatus bifasciatus (Georoy), Eupelmus vesicularis (Retzius) (Hymenoptera:
Eupelmidae), Ooencyrtus pitiocampae Mercet (Hymenoptera: Encyrtidae) and
Trichogramma embryophagum Hartig (Hymenoptera: Trichogrammatidae) (Tsankov et
al., 1996a, 1996b; Mirchev et al, 1998; Mirchev, Tsankov, 2001; Mirchev, 2005; Mirchev
et al., 2011). Six of these species are primary parasitoids, and one (B. transversalis) is a
hyperparasitoid of B. servadeii and O.pitiocampae.
47
Four species were found as egg parasitoids of T. solitaria in the regions of
Ivaylovgrad and Madzharovo for the rst time: Anastatus bifasciatus (Hymenoptea:
Eupelmidae), Ooencyrtus pityocampae Mercet, Ooencyrtus masii (Mercet) and Ooencyrtus
sp. (close to O. indenitus Myartseva) (Hymenoptea: Encyrtidae) (Mirchev et al., 2014;
Boyadzhiev et al., 2017).
In D. pini pupae in Topolovgrad region, 4 hymenopteran and dipteran parasitoid
species were found: Agrothereutes adustus (Gravenhorst), Exenterus amictorius (Panzer),
Olesicampe sp. (Hymenoptera: Ichneumonidae) and Drino inconspicua (Meigen)
(Diptera: Tachinidae) (Georgiev, Bochev, 1996). Parasitoids caused mortality rates of
31.6% in D. pini and A. adustus had the strongest impact on the host population
In Ognyanovo region, 3 parasitoids of N. sertifer were detected. Two species,
Dipriocampe diprioni (Ferriére) (Hymenoptera: Tetracampidae) and Baryscapus oophagus
(Otten) (Hymenoptera: Eulophidae), were reared from host eggs (Georgiev, 2001b), and
Agrothereutes adustus from host pupae (Georgiev, Kolarov, 1999). D. diprioni was found
as a primary parasitoid, and B. oophagus as a hyperparasitoid.
Two parasitoids were detected and reported for rst time in Bulgaria: Diplostichus
janithrix (Hartig) (Diptera: Tachinidae) in Gilpinia sp. in the Ognyanovo region
(Georgiev, 1996b), and Ibalia leucospoides (Holchenwarth) (Hymenoptera: Ibaliidae) in
Tremex fuscicornis in the Manole region (Ljubomirov et al., 2006).
We conclude that the pathogens and parasitoids found in the region of the Forest
Protection Station Plovdiv form an extensive natural enemy complex, maintaining the
population densities of insect pest species at lower levels. is is particularly important for
species that potentially increase to outbreak densities and whose populations then cause
economic losses in forest ecosystems or severe allergies to humans and animals (L. dispar,
E. chrysorrhoea, E. defoliaria, T. pityocampa, L. salicis, T. solitaria, etc.). Some fungal
pathogens (E. maimaiga, E. aulicae, B. bassiana) are already used in forest protection as
classical or augmentation biological agents.
REFERENCES
Boyadzhiev, P., P. Mirchev, G. Georgiev. 2017. Species of the genus Ooencyrtus Ashmead, 1900 (Hymenoptera:
Encyrtidae), egg parasitoids of aumetopoea solitaria (Lepidoptera: Notodontidae) in Bulgaria. Acta
zoologica bulgarica, Supplement 8, 107-112.
Draganova, S., D. Takov, D. Pilarska, D., Doychev, P. Mirchev, G. Georgiev, 2013. Fungal entomopathogens
on some lepidopteran forest pests in Bulgaria. Acta zoologica bulgarica, 65, 179-186.
Georgiev, G. 1995. Study of the parasitoids of poplar twig borer (Gypsonoma aceriana Dup., Lepidoptera,
Tortricidae) in Bulgaria. – In: ird National Conference of Entomology, Soa, September 18-20,
190-197 (In Bulgarian, English summary).
Georgiev, G. 1996b. Diplostichus janithrix Hart. (Diptera, Tachinidae) – parasitoid on Gilpinia sp.
(Hymenoptera: Diprionidae) and a new species for the Bulgarian fauna. Forestry Ideas, 2, 103-105 (In
Bulgarian, English summary).
Georgiev, G. 2000. Studies on larval parasitoids of Paranthrene tabaniformis (Rott.) (Lepidoptera: Sesiidae)
on urban poplars (Populus spp.) in Soa, Bulgaria. Annals of Forest Science, 57 (2), 181-186.
Georgiev, G. 2001a. Parasitoids of Saperda populnea (L.) (Coleoptera: Cerambycidae) on aspen (Populus
tremula L.) in Bulgaria. Journal of Pest Science, 74 (6), 155-158.
48
Georgiev, G. 2001b. New egg parasitoids of the pine sawy, Neodiprion sertifer (Geor.) (Hymenoptera:
Diprionidae), in Bulgaria. Forest Science Soa, 3/4, 87-90.
Georgiev, G., M. Raikova, N. Bochev. 2001. Parasitoids of the poplar clearwing moth, Paranthrene
tabaniformis (Rott.) (Lepidoptera: Sesiidae) in Pazardzhik region. – In: (Naydenova, Ts. Ed.).
Proceedings of ird Balkan Scientic Conference ‘Study, Conservation and Utilisation of Forest
Resources’, 2-6 October 2001, Soa, III, 111-118.
Georgiev, G. 2005. Phytophagous insects on poplars (Populus spp.) and parasitoids on them in Bulgaria.
DSc esis, Soa, 276 (In Bulgarian, English summary).
Georgiev, G., N. Bochev. 1996. Biological features of parasitoids on the pine sawy (Diprion pini L.,
Hymenoptera: Diprionidae). Forestry Ideas, 2, 86-92 (In Bulgarian, English summary).
Georgiev, G., J. Kolarov. 1999. New Ichneumonidae (Hymenoptera) parasitoids on forest insect pests in
Bulgaria. Journal of Pest Science, 72 (3), 57-61.
Georgiev, G., V. Pelov. 1996. Parasitizing peculiarities and parasitoids role in the regulating of the
Phyllocnistis suusella Z. (Lepidoptera, Phyllocnistidae) number in Bulgaria. Forest Science Soa, 1,
78-83 (In Bulgarian, English summary).
Georgiev, G., M. Raikova, T. Ljubomirov, K. Ivanov. 2004. New parasitoids of Saperda populnea (L.)
(Coleoptera: Cerambycidae) in Bulgaria. Journal of Pest Science, 77 (3), 179-182.
Georgiev, G., S. Samuelian. 1999. Species composition, structure and impact of larval parasitoids of poplar
twig borer, Gypsonoma aceriana (Dup.) (Lepidoptera, Tortricidae), on poplar ornamental trees in Soa.
Journal of Pest Science, 72 (1), 1-4.
Georgiev, G., G. Tsankov. 1995. Some parasitoid insect species on the larvae of the poplar clearwing moth
(Paranthrene tabaniformis Rott., Lepidoptera: Sesiidae) in Bulgaria. Forest Science Soa, 2, 51-58 (In
Bulgarian, English summary).
Georgiev G., P. Mirchev, B. Rossnev, P. Petkov, M. Georgieva, D. Pilarska, V. Golemansky, P. Pilarski,
Z. Hubenov. 2013. Potential of Entomophaga maimaiga for supressing Lymantria dispar outbreaks in
Bulgaria. Comptes rendus de l’Academie Bulgare des Sciences, 66, 1025-1032.
Ljubomirov, T., M. Raikova, G. Georgiev. 2006. Ibaliidae and Embolemidae (Hymenoptera), new families
for the Fauna of Bulgaria. Acta zoologica bulgarica, 58 (3), 425-430.
Markova, G., G. Georgiev. 1992. Beauveria bassiana – a pathogen on Satin Moth (Stilpnotia salicis). Gorsko
stopanstvo, 5, 22 (In Bulgarian).
Mirchev, P. 2005. Egg parasitoids on pine processionary moth aumetopoea pityocampa (Den. et Schi.)
(Lepidoptera: aumetopoeidae) in countries of Balkan Peninsula. DSc esis, Soa, 1-64 (In
Bulgarian, English summary).
Mirchev, P., G. Georgiev, P. Boyadzhiev. 2014. First record of egg parasitoids of pistachio processionary moth,
aumetopoea solitaria (Freyer) (Lepidoptera: aumetopoeidae). Acta zoologica bulgarica, 66 (1), 109-113.
Mirchev, P., G. Tsankov. 2001. Structure of eggs parasitoids complex of aumetopoea pityocampa bulgarica
(Lepidoptera: Notodontidae) found in Sub-Balkan of Central Bulgaria. Acta entomologica bulgarica, 7
(1/2), 60-64 (In Bulgarian, English summary).
Mirchev, P., G.H. Schmidt, G. Tsankov. 1998. e egg parasitoids of the pine processionary moth
aumetopoea pityiocampa (Den. et Schi.) in the Eastern Rhodopes, Bulgaria. Bollettino di Zoologia
agraria e di Bachicoltura, Ser. II, 30 (2), 131-140.
Mirchev, P., G. Georgiev, S. Draganova. 2012. Disease caused by Beauveria bassiana (Bals.-Criv.) Vuill. on
new hatched larvae of aumetopoea solitaria Freyer, 1838. Silva Balcanica, 13 (1), 61-65.
Pilarska, D., L. Solter, J. Maddox, M. McManus. 1998. Microsporidia from gypsy moth (Lymantria dispar
L.) populations in Central and Western Bulgaria. Acta zoologica bulgarica, 50(2/3), 109-113.
Pilarska, D., M. McManus, A. Hajek, F. Herard, F. Vega, P. Pilarski, G. Markova. 2000. Introduction
of the entomopathogenic fungus Entomophaga maimaiga Hum., Shim. & Sop. (Zygomycetes:
Entomophthorales) to a Lymantria dispar (L.) (Lepidoptera: Lymantriidae) population in Bulgaria.
Journal of Pest Science, 73(5), 125-126.
Pilarska, D., A. Linde, D. Goertz, D., M. McManus, L. Solter, N. Bochev, M. Rajkova. 2001a. First
report on the distribution of microsporidian infections of browntail moth (Euproctis chrysorrhoea L.)
populations in Bulgaria. Journal of Pest Science, 74(2), 37-39.
49
Pilarska, D., R. Zimmermann, A. Linde, M. McManus, D. Takov. 2001b. On the occurrence of Entomophaga
aulicae in high density browntail moth (Euproctis chrysorrhoea L.) populations in Bulgaria. Proceedings
of ird Balkan Scientic Conference, Study, Conservation and Utilisation of Forest Resources, Soa,
2-6.10. 2001, III, 139-143.
Pilarska, D., G. Georgiev, G., McManus, M., Mirchev, P., Pilarski, P., Linde, A. 2007. Entomophaga
maimaiga – an eective introduced pathogen of the gypsy moth (Lymantria dispar L.) in Bulgaria.
Proceedings of the International Conference ‘Alien Arthropods in South East Europe – Crossroad of
three continents’, 19-21.09, Soa, Bulgaria, 37-43.
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_Papazova, M. Matova, P. Vafeidis. 2016. Entomophaga maimaiga (Entomophthorales,
Entomophthoraceae) in Balkan peninsula – an overview. Silva Balcanica, 17 (1) 31-40.
Pilarska D., D. Takov, M. Hylis, R. Radek, I, Fiala, L. Solter, A. Linde. 2017a. Natural occurrence of
microsporidia infecting Lepidoptera in Bulgaria. Acta Parasitologica, 62(4), 853-858.
Pilarska, D., P. Dermendzhiev, R. Nachev, M. Dobreva. 2017b. Field release of Entomophaga aulicae
(Entomophthoromycota, Entomophthorales) for control of brown tail moth Euproctis chrysorrhoea
(Lepidoptera, Erebidae). Seminar of Ecology, 2017 with International participation, 27-28.04.2017,
Soa.
Mirchev, P., G. Tsankov, G. Georgiev, P. Boyadzhiev. 2011. Pediobius bruchicida (Rondani) (Hymenoptera:
Eulophidae) – an egg parasitoid of pine processionary moth, aumetopoea pityocampa (Denis &
Schiermuller) (Lepidoptera: Notodontidae) and a new species for Bulgarian fauna. Acta zoologica
bulgarica, 63 (3), 319-322.
Takov, D., D. Pilarska, R. Wegensteiner R. 2006. Entomopathogens in Ips typographus (Coleoptera,
Scolytidae) from several spruce stands in Bulgaria. Acta zoologica bulgarica, 58(3), 409-420.
Takov, D. Doychev, R. Wegensteiner, D. Pilarska. 2007. Study of bark beetle (Coleoptera, Scolytidae)
pathogens from coniferous stands in Bulgaria. Acta zoologica bulgarica, 59(1), 87-96.
Takov, D., D. Doychev, A. Linde, S. Draganova, D. Pilarska. 2012. Pathogens of bark beetles (Curculionidae:
Scolytinae) and other beetles in Bulgaria. Biologia, 67(5), 966-972.
Tsankov, G., G.H. Schmidt, P. Mirchev. 1996a. Parasitism of egg-batches of the pine processionary moth
aumetopoea pityocampa (Den. et Schi.) (Lep., aumetopoeidae) in various regions of Bulgaria.
Journal of Applied Entomology, 120, 93-105.
Tsankov, G., G.H. Schmidt, P. Mirchev. 1996b. Structure and parasitism of egg-batches of a processionary
moth population dierent from aumetopoea pityocampa (Den. et Schi.) (Lep. aumetopoeidae)
found in Bulgaria. Bollettino di Zoologia agraria e di Bachicoltura, Ser. II, 28 (2), 195-207.
E-mail: dpilarska@yahoo.com
... 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 2016 a successful release of another entomophthorous fungus, E. aulicae 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]. ...
Article
Full-text available
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.
... There is a long tradition for utilizing insect DNA viruses as biocontrol agents, and many have been already commercialized [see 153]. Concerning forest insects, large dsDNA viruses of family Baculoviridae have been successfully used to control populations of the European pine sawfly (Neodiprion sertifer), and baculoviruses are also found in lepidopteran species including, e.g., Lymantria monarcha, Lymantria dispar, and Leucoma salicis [154]. These DNA viruses are specific to insects, and no spillover to plants or fungi has been reported. ...
Article
Full-text available
Purpose of Review The collective virome of forest trees can be considered to include not only plant viruses, but also viral communities harbored by all tree-associated organisms. In this review, we will concentrate on reviewing recent developments in the two fields of forest tree virology that have received the most research input during the last 5 years: (1) current knowledge of virus diseases affecting forest trees and their causal agents and (2) fungal viruses (mycoviruses) and properties that are required for utilizing them for biocontrol purposes. Recent Findings The discovery of plant and mycoviruses has been revolutionized during the last few years due to high-throughput sequencing (HTS). This has altered our view of virus diversity and prevalence, but also their host ranges, transmission routes, and host effects. Utilization of HTS has greatly expanded our knowledge of plant virus diversity and disease etiology in forest trees and revealed the commonness of cross-kingdom transmission events between fungi, oomycetes, plants, and arthropods. Research on mycoviruses has also identified several new mycoviruses that restrict the growth or virulence of forest pathogenic fungi. Summary Gaining knowledge of the collective virome of forest ecosystems is essential not only for understanding virus evolution and diversity but also for improving our understanding on virus impacts, and our ability for biocontrol-based and environmentally friendly management of viral and fungal diseases that affect economically important plants and beneficial insects, and for preventing possible disease outbreaks in the future. Virus infections play a central role in plant health, but viral symptoms on forest trees remain often unrecognized and may be confused with other biotic or abiotic damages. However, recent studies have revealed previously unknown viruses as causes of forest tree symptoms and suggest that viruses are responsible for far greater economic losses than recognized earlier. However, many knowledge gaps still need to be filled, particularly on the diversity of viruses that infect different species of forest trees, their irregular distribution within the plant, their mode of transmission, epidemiology and choice of hosts also regarding crop plants, their effect on the metabolism of their host tree, and their interaction with other microorganisms. Mycovirus research has already deciphered detailed information on many critical properties that affect utilizing them for biocontrol purposes. Still, more knowledge is needed concerning mycoviral transmission mode and stability in field conditions, the level of host tolerance against mycoviral infection, and the occurrence of interspecies mycovirus transmission in nature, and safety issues related to these topics.
... Beauveria species attack many insect species worldwide (Sevim et al. 2010), including larvae and pupae of many Thaumetopoea species (Halperin 1990;Battisti et al. 2000;Zamoum et al. 2007;Mirchev et al. 2012). Beauveria species, such as B. bassiana, are already used in forest protection as classical or augmentation biological agents (Pilarska et al. 2018). ...
... and Endoreticulatus spp. had a wide prevalence throughout the region (Pilarska et al 2018). Cory et al (2000) investigated the host range of EcNPV to discern the risk to non-targets as NPV has been considered for commercial use. ...
Article
The browntail moth (Euproctis chrysorrhea) is an invasive forest pest that has been present in the Northeast since it was first introduced from Europe in 1897. Originally, its range expanded very rapidly until it reached its peak invasion of 150,000 km2, which included most of New England and parts of Southern Canada and Long Island, NY, in 1915. After this point, its range collapsed until only relic populations remained on islands in the Casco Bay Region of Maine and outer Cape Cod in Massachusetts. In 2016, a large population outbreak occurred that expanded its range into inland Central Maine and appears to be continuing to expand north and east today. Our research aims to assess the relative abundance and diversity of parasitoid natural enemies present within the browntail moth population and the factors that influence browntail moth population dynamics over this outbreak period. We sampled browntail moth in infested areas across mid-coast and central areas of Maine to assess overwintering survival, larval and pupal density, healthy moth emergence, and parasitoid diversity and abundance. We estimated densities using timed 10-minute density counts, while survival and emergence was estimated by rearing out samples. Models to test important factors for both hosts and parasitoids were conducted, where year, distance to coast, age of infestation, habitat, and annual climate variables were tested. Nine parasitoid species were recovered from browntail moth pupation nests, three of which were hyperparasitoids. The highest parasitism occurred from Townsendiellomyia nidicola, a primary parasitoid accounting for 24 percent and Monodontomerus aerus, a hyperparasitoid accounting for 36 percent parasitism across all years. Between 2016 and 2018, hyperparasitoids increased in their proportion and mean percent parasitism while primary parasitoid decreased in these regards. Negative binomial results indicated habitat, year, and total annual precipitation were the most significant factors for the abundance of parasitoids, where distance to coast and age of the infestation were not significant. The mean number of pupation nests per 10-minute density count increased slightly in 2017 (28 ± 6) but decreased in 2018 (20 ± 4). In comparison, the mean rank of MFS winter hibernacula per tree decreased across all years. Browntail moth post-diapausing larvae, late-stage larvae, and pupation nests significant decreased at coastal sites in 2017 while inland sites significantly increased in 2018. Moth survival, however, significantly increased between 2017 and 2018. Negative binomial results indicated that habitat was an important factor across post-diapausing larvae, late-stage larvae, and pupation nests while post-diapausing larvae was the only significant factor for moth abundance. Abundance significantly decreased in 2017 across all browntail moth life stages, likely due to an epizootic outbreak of an entomopathic fungi. This study presents data that indicates a higher incidence of hyperparasitoids that may negatively impact primary parasitism, which could positively impact browntail moth survival. Both parasitoids and hosts were negatively impacted in 2017, likely due to an epizootic outbreak, another factor that may drastically impact population dynamics. The data presented gives new insight to the current population dynamics of browntail moth and their parasitoids.
Preprint
Full-text available
Global change alters forestry habitats and facilitates the entry of new pathogens that do not share a co-evolution history with the forest, leading them into a spiral of decline. As a result, relationships between forests organisms get disbalanced. Under this scenario, RNA viruses are of particular interest, as they participate in many of such relationships thanks to their ability to infect a wide range of hosts, even from different kingdoms of life. For this reason, the study of RNA viruses is essential to understand how viral flow across different hosts might occur, and to prevent possible outbreaks of diseases in the future. In this work the RNA virus diversity found in trees, arthropods and fungi from declining Mediterranean forests is described. To this extent, three habitats (Quercus ilex, Castanea sativa and Pinus radiata) were sampled and RNAseq was performed on tree tissues, arthropods and fungi. 146 viral sequences were detected by searching for matches to conserved motifs of the RNA-dependent RNA polymerase (RdRP) using Palmscan. Up to 15 viral families were identified, with Botourmiaviridae (28.7%) and Partitiviridae (9.6%) being the most abundant. In terms of genome type, ssRNA(+) viruses were the most represented (83.5%), followed by dsRNA (15%) and two ssRNA(-) representatives. Viruses belonging to families with cross-kingdom capabilities such as Hypoviridae (1), Mitoviridae (6) and Narnaviridae (5) were also found. Distribution of viruses across ecosystems was: Q.ilex (57.5%), P.radiata (26.7%) and C.sativa (15.8%). Interestingly, two RdRP sequences had no matches in available viral databases. This work constitutes a starting point to gain insight into virus evolution and diversity occurring in forests affected by decline, as well as searching for novel viruses that might be participating in unknown infectious pathways.
Article
Full-text available
The study examines the results of complex geophysical research of threearchaeological sites located near the southern part of the Black Sea coastline in Bulgaria:Propadnalata Voda, Atiya, and Alepu. The authors discuss the use of complex geophysical methodsin archaeology depending on the objectives of archaeological research, on the one hand, and thelikely properties of the archaeological sites, on the other. As known, the methods of appliedgeophysics involve reverse geophysical problems, which do not have definitive solutions. Toovercome potential ambiguities in this regard, the study demonstrates how the complementary useof different methods makes the interpretation of the final results easier.
Article
Full-text available
The paper presents the results of a successfully completed international project of the Department of Natural Sciences titled “Monitoring and identification of the entomopathogenic fungus Entomophaga maimaiga in Lymantria dispar populations” and funded by the National Research Fund in 2017-2019. Investigating the distribution of E. maimaiga in Austria and Bulgaria in 2018-2019 shows that the pathogen has expanded its range to the west and reached Lower Austria. E. maimaiga has been identified in Bulgaria as well and has become part of the natural enemy complex of L. dispar.
Article
Full-text available
Fourteen hundred and sixty three larvae of 10 lepidopteran species collected from trees and bushes in the spring and summer of 2017, 2018 and 2019 from 5 localities in Northwest and South Bulgaria were investigated for presence of microsporidian and fungal pathogens. Also, 77 grasshopper individuals of Poecilimon thoracicus (Orthoptera, Tettiigoniidae) collected from various shrubs and perennial plants in the spring and summer of 2017 were examined. Conducted microscopic analyses showed the presence of microsporidian infection caused by Endoreticulatis poecilimonae in P. thoracicus and fungal infection in the larvae of mottled umber, Erannis defoliaria caused by Entomophaga auliciae. The studies showed that the average infection rate with the microsporidium E. poecilimonae was 57.1%. The prevalence of the fungus Entomophaga auliciae was 100% during the observed epizootic. E. auliciae is an efficient fungal pathogen which causes strong epizootics and can be used as classical or augmentation biological agent.
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
We examined 34 lepidopteran species belonging to 12 families to determine presence and prevalence of microsporidian pathogens. The insects were collected from May 2009 to July 2012 from 44 sites in Bulgaria. Nosema species were isolated from Archips xylosteana, Tortrix viridana, Operophtera brumata, Orthosia cerasi, and Orthosia cruda. Endoreticulatus sp. was isolated from Eilema complana. The prevalence of all isolates in their hosts was low and ranged from 1.0% to 5.3%. Phylogenetic analyses of the new isolates based on SSU rDNA are presented.
Article
Full-text available
The study was carried out in 2010-2015 at 6 sites in the Eastern Rhodopes: Madzharovo, Dam Ivailovgrad, Dupkata, Quarry, Liikanen and Meden Buk. A total of 424 Thaumetopoea solitaria egg clusters were collected from these sites and kept at room temperature. Out of a total of 52,628 eggs in the samples, 3 species of parasitoids of the genus Ooencyrtus, i.e. O. masii, O. pityocampae and Ooencyrtus sp. nr. indefinitus, were found. The dominant species was O. masii. The least abundant species, represented only by two emerged female individuals, was O. pityocapae. In the other two species, individuals of both sexes were recorded. In O. sp. nr. indefinitus, the ratio ♀♀:♂♂ was almost 1:1, whereas in O. masii the female individuals predominated. In laboratory conditions, the period of emergence of parasitoids was 41 days. For both species, O. masii and O. sp. nr. indefinitus, a similarity in the emergence dynamics was observed. In 2014, it was more extended, and shorter in the next year. The peak of emergence of O. masii was 20-25 days, earlier than that of the other parasitoids.
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
The Asian fungal entomopathogen Entomophaga maimaiga was first introduced in Bulgaria for biological control of gypsy moth, Lymantria dispar, in 1999 and the first epizootics in gypsy moth populations were observed in 2005. Six introductions of E. maimaiga in oak forests with heavy L. dispar infestations were conducted from 2008 to 2011 in different regions of the country, including Nova Zagora, Gorna Oryahovitsa, Popovo, Targovishte and Staro Oryahovo. As a result of these introductions, host density was decreased by 55.1-100% and the outbreaks were suppressed. After the introduction of the pathogen in Bulgaria, no microbiological or chemical control of L. dispar has been necessary and the last two gradations have been estimated to be 15-30% of the values in previous gradations.
Article
Full-text available
The pathogen species composition and distribution in a variety of bark beetle species from different coniferous stands was investigated. Seven pathogen species were recovered: I. typographus Entomopoxvirus (ItEPV), Malamoeba scolyti, Gregarina typographi, Menzbieria chalcographi, Chytridiopsis typographi, Nosema-like microsporidium and Beauveria bassiana. Nosema–like microsporidium, M. chalcographi and M. scolyti are new reports for the Bulgarian fauna. I. sexdentatus, Pityophthorus pityographus, Cryphalus saltuarius, Orthotomicus proximus and Polygraphus subopacus are newly reported hosts for B. bassiana, M. scolyti, Chytridiopsis cf. typographi and Gregarina cf. typographi respectively. G. typographi appears to have the broadest host range the beetles we examined, followed by C. typographi, M. chalcographi. M. scolyti and Nosema-like microsporidium appear to have narrower host ranges.
Article
Full-text available
During the period 2010-2012, egg parasitoids of pistachio processionary moth {Thaumetopoea solitaria) were studied in Bulgaria. A total of 215 egg clusters containing 26 453 eggs were collected on Pistacia terebinthus in 4 sample plots at 3 sites in the Eastern Rhodopes. Directly after collection, egg clusters with part of branches, about 5 cm long, were individually separated in test tubes, closed with cotton stoppers and stored under laboratory conditions at 20-22 °C. As a result, three egg parasitoids were recorded for the first time in T. solitaria: Anastatus bifasciatus (Hymenoptea: Eupelmidae), Ooencyrtus pityocampae and Ooencyrtus sp., closely related to O. masii and O. ascalaphi (Hymenoptea: Encyrtidae). The new records enlarge the host ranges of polyphagous species O. pityocampae and A. bifasciatus. The main part of the parasitoids emerged after hibernation. Their survival was about 80%. The impact of egg parasitoids on the host was calculated to be 2.9-21.5%.
Article
The entomopathogenic fungus Entomophaga maimaiga was introduced into a L. dispar population situated in South Bulgaria for the first time in Europe. It was found that of all larvae collected in the five experimental plots, 6.3% contained conidia and resting spores of E. maimaiga, 14.2 % contained parasitoids and 2.3 % were infected with nucleopolyhedrovirus (NPV). The presence of the fungus in cadavers collected from each experimental plots and on five of the six collection dates was observed.