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IZVORNI I ZNANSTVENI ČLANCI – ORIGINAL SCIENTIFIC PAPERS Šumarski list br. 7–8, CXXXIV (2010), 403-410
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PARASITOIDS AND HYPERPARASITOIDS OF ERANNIS DEFOLIARIA CL.
(LEPIDOPTERA, GEOMETRIDAE) IN OAK FORESTS


PARAZITOIDI I HIPERPARAZITOIDI ERANNIS ERANNIS DEFOLIARIA CL.
(LEPIDOPTERA, GEOMETRIDAE) U HRASTOVIM ŠUMAMA


1


Milka GLAVENDEKIĆ


ABSTRACT: The research on biology and ecology of Mottled Umber Moth


–Erannis defoliariaCl. (Lepidoptera, Geometridae) was carried out in the period
1985–2009 in oak forests in Serbia. Mottled Umber Moth was mainly in
the latency during the investigation. Only at the locality Miroč in East Serbia
and in Forest unit Zlatica (National Park Djerdap), it was dominant in the
complex of early defoliators. Natural enemies ofE. defoliariaand especially
parasitoids and hyperparasitoids are important mortality factors.


Egg parasitoidTrichogrammasp. (Hym., Trichogrammatidae) was recorded
at few localities in the vicinity of Belgrade and in the wide area of National
Park Djerdap. They are nonspecific parasitoids. Somewhat more specific Telenomus
minutus(Hym., Scelionidae) was recorded from East Serbia – locality
Miroč. Larval parasitoids are Protapanteles immunis,Cotesia limbata,C. jucunda(
Hym., Braconidae);Casinaria ischnogaster,Casinaria moesta,Phobocampe
crassiuscula, Phobocampe pulchella, Phobocampe sp. (Hym.,
Ichneumonidae), Euplectrus bicolor, Eulophus larvarum (Hym., Eulophidae),
Blondelia nigripes,Phryxe magnicornis,P. nemea,Peribaea fissiconis(Diptera,
Tachinidae). There are 16 parasitoids recorded. Five species of hyperparasitoids
recorded on E. defoliariaare following: Gelis areator,Bathythrix lamina
(Hym., Ichneumonidae), Perilampus ruficornis (Hym., Perilampidae), Habrocytus
chrysos. (Hym., Pteromalidae), Tetrastichussp. (Hym., Eulophidae).


Key words: Quercus spp., oak, Erannis defoliaria, Mottled Umber
Moth, parasitoid, hyperparasitoid


INTRODUCTION– Uvod


Agood condition and stability of forest ecosystems rests. In Serbia following winter moth species are out-
is of the main importance of all forest functions. A breaking and among the most significant oak defoliagreater
part of forest regions in Serbia is covered with tors: Colotois pennaria L., Agriopis aurantiaria Hbn.,
oak climate-zonal communities.The most represented Erannis defoliariaCl.,Alsophila aesculariaD.& Sch.,
species are sessile oak Quercus petraea (Matt.) Lie-A. acerariaD.& Sch.,Operophtera brumata L.,Apocblein,
Turkey oakQ. cerrisL., Hungarian oakQ. frai-heima pilosaria D.& Sch., Agriopis leucophaearia D.
nettoTenore, Vergilius’s oakQ. virgilianaTenore and & Sch. andA. marginaria F. (Glavendekić,1999).
pedunculate oakQ. roburL. Winter moths are defined as a group of species homo


logy as the winter moth fly during autumn and winter,


Mottled umber moth –Erannis defoliariaCl. (Lepifemales
are apterous or they have reduced wings, they


doptera, Geometridae) is one of nine outbreaking winter
overwinter in egg or pupal stages, the first instar larvae


moths, which are responsible to defoliations in oak fodisperse
by ballooning with the aid of wind.


Insects feeding on the foliage of live plants are cal-


Associate. Prof. Milka Glavendekić, PhD.


led defoliators. Oak defoliators are mostly moths,


(milka.glavendekic@nadlanu.com), University of Belgrade,
Faculty of Forestry, Kneza Višeslava 1, Belgrade, Serbia
sawflies, leaf beetles and weevils. Based on the time of




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occurrence, they are divided in early-season (spring)
defoliators, the long-season defoliators and late-season
defoliators.To early-season defoliators belong species
which overwinter in the stages of egg or pupa and
whose activity is related to early spring.Their caterpillars
feed on the buds or young leaves and their development
ends very quickly. This group is faunistically
most versatile (leaf rollers, winter moths, noctuid
moths, sawflies, oak leaf beetles, weevils).Their defoliations
occur chronically and the consequence of defoliation
is the reduction of increment (Klepac &
Spaić,1965;Rubcov,1996). For this reason, defoliators
are paid special attention to and the control measures
are most often directed against them.


The first data aboutE. defoliaraoutbreaks in oak forests
from 1887 to 1898 are given by Langhoffer,
1899. Long-term study of winter moths in Croatia - Slavonia
oak forests were undertaken in 1960 (Spaić,
1974).The significance of winter moths in Serbia, as forest
pests was emphasised by Tomić,1980; Vasić &
Tomić,1980. Predators and parasitoids of herbivores
can reduce the pests or prevent their outbreak. After
multiannual application of DDTpreparations in the suppression
of gypsy moths in forests, ecological study was
undertaken in the fifties of last century, in order to find
alternate methods of forest insect pests suppression
(Pschorn - Walcher,1977).These researches were
aimed at the development of the concept of biological
control applied in Canada, where the outbreak of the
winter moth was suppressed by biological control (Embree,
1966).The application of biological methods in
the control of forest insect pests was studied byMihajlović,
Lj., (1986),Harapin (1992),Glavendekić
(1992) and many other authors. Based on the literature,
53 parasitoids and 11 hyperparasitoids have so far been
identified forE. defoliariain Europe (Herting,1965,
1976; Čapek, and Čepelak, 1981; Čapek, 1985;
Djorović,1980). The most of parasitoids belong to
Hymenoptera (41 species) and the rest belong to Diptera
(Tachinidae 11 species and Phoridae one species). The
majority of hyperparasitoids are from family Ichneumonidae
(10 species) and only one species from the family
Perilampidae (Hymenoptera, Chalcidoidea).The following
parasitoids in Serbia were recorded on mottled
umber moth:Cotesia jucundaMarsh., Meteorus versicolorWesm.
(Hymenoptera: Braconidae), Eulophus larvarum
L. (Hymenoptera: Eulophidae) and Phorocera
obscuraFall. (Diptera:Tachinidae).


MATERIALAND METHODS – Materijali i metode rada


The research done on all development stages of E.
defoliariaClerck, 1759.The research was carried out by
field and laboratory methods. Field work included standard
methods of entomological research of moths in all
development stages.The method of exposure in nature
was applied to eggs and larvae by using sticky bands at
the time of female activity. Females laid eggs in bark
crevices below sticky bands.The parts of the bark with
eggs were cut and the samples were taken to the laboratory
for rearing and processing. Sticky bands were also
used for larval exposure, but inApril and May.


To monitor population dynamics and the change of
quality composition of winter moths, absolute and relative
abundance of E. defoliaria was assessed every
year. Caterpillar density was assessed when they were
predominantly the second and partly the third instars.
Absolute abundance was assessed by counting the leaves
or opened buds and caterpillars in the sample. Relative
abundance was assessed based on the number of
caterpillars on 1000 leaves.


Biology and ecology ofE. defoliariawere studied on
the following localities and types of forests: 1. Fruška
gora Mt., Brankovac, Compartment 41 – forest ofTurkey
oak and sessile oak (Quercetum petraeae-cerris) on
brown and lessive brown soil on serpentinite. 2. Forest
Unit Košutnjak - one sample plot was set aside in the forest
of sessile oak,Turkey oak and hornbeam (Carpino-
Quercetum petraeae-cerris) on brown forest soil and
lessive brown forest soil.The second in the plantation of
red oak (Quercus rubra L.) on humus brown forest soil.
The third one was set aside in the association Orno-
Quercetum pubescentis-virgilianae.3. Forest Unit Mala
Moštanica compartment 52 – artificially regenerated
stand of black locust and a mixture of oaks are established
on a typical site of Hungarian oak andTurkey oak.


4.Forest UnitAvala, Compartment 15, in a climatogenic
communityQuercetum frainetto-cerris aculatetosumon
lessive brown forest soil. 5. Forest Unit Jamena – Radjenovci,
Visoka šuma, compartment 4c – forest type pedunculate
oak and hornbeam (Carpino Quercetum
roboris) on brown forest soil to lessive brown forest soil
in the non-flooded area. 6. Forest Unit Visoka šuma
Lošinci, compartments 1a, 2d, 15a. – forest type pedunculate
oak, hornbeam andTurkey oak (Carpino-Quercetum
robori-cerris typicum) on brown forest soil to
lessive brown forest soil. 7. Forest Unit Visoka šuma
Lošinci, compartment 23g. – forest type pedunculate
oak, hornbeam andTurkey oak (Carpino-Quercetum robori-
cerris typicum)on lessive to semigley soils. 8. Forest
Unit Miroč, compartment 73a – forest of sessile oak
Quercetum montanum typicum) on brown soils. 9. Forest
Unit Porečke šume, compartment: 54b – forest type
beech and sessile oak (Querco-Fagetum typicum) on
acid brown and lessive acid brown soil. 10. Forest Unit
Porečke šume, compartment 54 f – forest type sessile
oak (Quercetum montanum typicum) on acid brown soil.


11.Forest Unit Zlatica, compartment 93a – forest type
sessile oak (Quercetum montanum typicum) on acid




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brown soil. 12. Forest Unit Zlatica, compartment 96a forest
type beech and sessile oak (Querco-Fagetum typicum)
on acid brown and lessive acid brown soil. 13. Forest
Unit Kožica, compartment 30b – forest of sessile
oak andTurkey oak (Quercetum petraeae cerris pauperum)
on acid brown and lessive acid brown soils. 14. Forest
Unit Kožica, compartment 31a – forest of
submontane beech (Fagetum submontanum) on deep
eutric brown soils (brown forest soil and brown soil on
loamy sediments). 15. Forest Unit Bukovik, compartment
4a – coppice forest of Hungarian oak andTurkey
oak with Eastern hornbeam (Quercetum frainetto - cerris
carpinetosum orinetalis) on dystric and eutric brown
soils. 16. Forest administration Raška, Forest unit Kosovac
– coppice forest of Hungarian oak andTurkey oak
with Eastern hornbeam (Quercetum frainetto - cerris
carpinetosum orinetalis) on dystric and eutric brown
soils.


RESULTS – Rezultati


Biology and population dynamic of mottled umber moth


Biologija i populaciona populacijska dinamika velikog mrazovca


Erannis defoliaria Clerck, 1759 – Mottled umber
moth, Grosser Frostspanner, ....................,
veliki mrazovac. During our study the first adults were
found in the third decade of November, and the last ones
in the first decade of January. Females oviposit individually
or in small groups around the buds, in bark crevi-


Figure 1 Caterpillars of E. defoliaria


Slika 1. Gusjenice E. defoliaria


ces or in other hidden places. Caterpillars can vary in the
colour (figure 1).


It was recorded in all localities, most often in a
lower population density. In Forest unitMiroč, however,
it was dominant (65% of early season defoliator
population). It exceeded threshold on the locality National
Park Djeradp in Forest unit Zlatica, comp. 54f in
2002 (213 larvae/1000 leaves). In compartments 101,
95 and 55 relative abundance was from 98–123 larvae/
1000 leaves in 2009.


Winter moth population dynamics has been studied
in different forest types. It was found out that frequent
outbreaks are characteristic for the following forest
types: forest ofTurkey oak and sessile oak (Quercetum
petraeae-cerris) on brown and lessive brown soil on
serpentinite; forests of sessile oak (Quercetum montanum
typicum) on acid brown soil; in the forest of Hungarian
oak and Turkey oak with Eastern hornbeam
(Quercetum frainetto-cerris carpinetosum orientalis)
on dystric and eutric brown soils; in the association
Orno-Quercetum pubescentis-virgilianaeand in the artificially
established stand of mixed oaks at Mala Moš ta
nica. In plantations of pedunculate oak with
hornbeam in forest unitVisoka šuma Lošinci outbreaks
of winter moths are frequently observed.Winter moths
occur regularly, but as a rule there are no outbreaks in
the forest of sessile oak, Turkey oak and hornbeam
(Carpino-Quercetum petraeae-cerris) onbrown forest
soil and lessive brown forest soil.


Distribution and bioecology of mottled umber moth parasitoids


Rasprostranjenje i bioekologija parazitoida velikog mrazovca
During our study on parasitoids ofE. defoliariain
oak forests following species were recorded:
Protapanteles immunis Haliday, 1834 (Hymenoptera:
Braconidae) is a parasitoid ofE. defoliariaandA.


marginaria caterpillars. It is recorded in Forest units:
Mala Moštanica, Rađenovci,Visoka šuma, and Bukovik.
Cotesia limbata Marshall, 1885 (Hymenoptera:
Braconidae) was recorded in several localities as the
parasitoid of A. leucophaearia,E. defoliaria and O.
brumatacaterpillars. It was found in Forest unit Mala


Moštanica andVisoka šuma Lošinci.


Figure 2 Larvae of E. defoliaria with Braconidae


Slika 2. Larva E. defoliaria sa brakonidom




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Cotesiajucunda Marshall, 1885 (Hymenoptera: Braconidae)
was recorded in Forest units: Košutnjak, Mala
Moštanica, and Bukovik. It was reared from the caterpillars
of mottled umber moth (figure 2).


Casinaria ischnogaster Thoms., 1887 (Hymenoptera:
Ichneumonidae) was observed in Forest unit Košutnjak,
as the parasitoid of A. marginaria and E.
defoliariacaterpillars.


Casinaria moestaGrav., 1829 (Hymenoptera: Ichneumonidae)
was observed in Forest units Mala Moštanica,
Košutnjak and Avala. All specimens of this
species were reared from the caterpillars of the mottled
umber moth.


Phobocampe crassiusculaGrav., 1829 (Hymenoptera:
Ichneumonidae) was observed in the Forest units
Košutnjak and Mala Moštanica as the parasitoid ofE.
defoliariaandA. pilosariacaterpillars.


Phobocampe pulchella Thoms., 1887 (Hymenoptera:
Ichneumonidae) was observed in Forest units: Košutnjak,
Mala Moštanica, Bukovik and inVisoka šuma
Lošinci. It was reared from the caterpillars of A. leucophaearia,
E. defoliaria and O. brumata. Larvae of
parasitoid leave the host before pupation (figure 3).


Figure 3 Larvae of Ichneumonidae


Slika 3. Larva Ichneumonidae


Phobocampe sp. (Hymenoptera: Ichneumonidae)
was reared from the mottled umber moth caterpillars
originating from Forest unit Bukovik.


Euplectrus bicolor (Swed., 1795) (Hymenoptera:
Eulophidae) was found in Forest unitVisoka šuma Lošinci,
reared from the mottled umber moth caterpillar.


Eulophus larvarum (Linnaeus, 1758) (Hymenoptera:
Eulophidae) was the most abundant parasitoid of
young caterpillars ofE. defoliariaduring the investigation
at several localities: Forest unit RađenovciVisoka
šuma, Visoka šuma Lošinci, compartment 1, 2, compartment
22, compartment 23. In Forest unit Mala Moštanica
it was reared from caterpillars of the mottled
umber moth,A. leucophaeariaandO. brumata.


Trichogramma sp.(Hymenoptera: Trichogrammatidae)
is egg parasitoid recorded in the region of the Forest
Administration Belgrade, Mala Moštanica. From
the winter moth and mottled umber moth eggs collected
in March, adults emerge in late April. In the National
Park Djerdap, Forest unit Zlatica, compartment 59 and
Boljetinska Reka, compartment 44, the eggs ofO. bru


th


mata,E. defoliariawere collected at March, 27 and the


th


first wasps hatched in the laboratory onApril, 27 .
Telenomus minutus Ratzeburg (Hymenoptera: Scelionidae)
was reared from eggs ofO. brumata, A. aurantiaria
and E. defoliaria in the Forest unit Miroč,
compartments 73/74.
Blondelia nigripesFall., 1810 (Diptera:Tachinidae)
was recorded in Forest units:Avala, as parasitoids caterpillars
of the mottled umber moth andA. marginaria.
In Forest unitVisoka šuma Lošinci, compartments
1 and 2 it was reared from the winter moth,A. pilosaria,
A. leucophaeariacaterpillars. In Forest unit Bukovik,
B. nigripes was reared from the C. pennaria
caterpillars. Population dynamic of this species is connected
with outbreaks of various winter moths and it
was the most abundant in the phase of retrogradation.
Phryxe magnicornis Zetterstedt, 1838 (Diptera:
Tachinidae) in Forest unit Mala Moštanica was recorded
as the parasitoid of the mottled umber moth caterpillars.
It is also recorded also in the Forest unitVisoka
šuma Lošinci, compartment 1 and Forest unit Bukovik
as the parasitoid of the winter moth caterpillars.
Phryxe nemeaMeigen, 1824 (Diptera:Tachinidae)
was reared from several Forest units:Visoka šuma Lošinci,
compartment 22 and Avala from the mottled
umber moth caterpillar. From Forest unit Mala Moštanica
and Košutnjakit was reared from grown up caterpillars
ofC. pennariaandE. defoliaria.In Forest unit
Boljetinska Reka, it was obtained fromO. brumatacaterpillar.
In Forest unit Bukovik P. nemea was reared
from caterpillars of the winter moth the mottled umber
moth andC. pennaria.
Peribaea fissicornisStrobl, 1909 (Diptera:Tachinidae)
was recorded in the Forest unit Mala Moštanica as


Figure 4 Larvae of E. defoliaria withTachinidae


Slika 4. Larva E. defoliaria sa tahinidom




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the parasitoid of A. marginaria caterpillar. In Forest
unitVisoka šuma Lošinci, compartment 22 it was reared
from the mottled umber moth caterpillar.


There are all together 16 parasitoid species recorded
onE. defoliariain oak forests in Serbia.The most frequent
species wasPhryxe nemea, which was recorded
at 6 localities. On four localities were recordedPhobocampe
pulchellaandPhryxe nemea.The highest diversity
of parasitoids was in Forest unit Mala Moštanica,
where 11 of 16 species were recorded. High diversity
of parasitoids was also found in pedunculate oak plantation
mixed with hornbeam in Forest unitVisoka šuma
Lošinci, where 50% of parasitoid species were recorded.
It is easy to distinguish parasitized caterpillars by
tachinide due to chorion on the front part of its body
and dark marking around it (figure 4).


Distribution and bioecology of mottled umber moth hyperparasitoids


Rasprostranjenje i bioekologija hiperparazitoida velikog mrazovca


During our study on hyperparasitoids ofE. defoliariain
oak forests following species were recorded:


Gelis areator Panzer, 1804 (Hymenoptera: Ichneu moni
dae) was found in two Forest units: Avala, Compartment
15, and Forest unit Kosovac as a hyperparasitoid of
mottled umber moth and winter moth caterpillars.


Bathythrix lamina Thomson, 1884 (Hymenoptera:
Ichneumonidae) was recorded in the Forest unitAvala.
It was reared from the cocoon Casinaria sp.(Hymenoptera,
Ichneumonidae) as a secondary parasitoid of


E.defoliaria.
Perilampus ruficornis(Fabricius, 1793) (Hymenop


tera: Perilampidae) was recorded in several Forest
units: Rađenovci, Compartment 4, from theTachinidae
cocoon; Forest unit, Mala Moštanica, Forest unit
Miroč, Compartment 73/74, from Tachinidae cocoon
reared from theE. defoliariacaterpillar.


Habrocytus chrysos Walker, 1836 (Hymenoptera:
Pteromalidae) was reared fromE.defoliariacaterpillar
originating from Forest unit Mala Moštanica.The host
died in the second instar.


Tetrastichussp.(Hymenoptera:Eulophidae) wasreared
from the several localities: Forest unit Mala Moštanica
– fromO. brumataandA. leucophaeariacaterpillars;
Forest unitVisoka šuma Lošinci, compartment 23 – from


O.brumatacaterpillars; Forest unitVisoka šuma Lošinci,
compartments 1 and 2 – from caterpillars ofA. aescularia,
A. leucophaearia,E. defoliariaandO. brumata.


Influence of parasitoids and hyperparasitoids on population dynamic of E. defoliaria


Uticaj parazitoida i hiperparazitoida na populacionu populacijsku dinamiku E. defoliaria


Population dynamics of parasitoids and hyperparasitoids
were studied in the culmination and in the first
years of the postculmination phase. Hyperparasitoids
fly before primary parasitoids.Their larvae were found
in the caterpillars before the primary parasitoid infected
the caterpillar. It is significant, however, that hyper-
parasitoids coincidence with primary parasitoid larva
was low compared to their frequency. In the phases of
retrogradation and latency, the coincidence was even
lower at some localities. Parasitoids and hiperparasitoids
are well adapted to their hosts. Locally they can
contribute to break down of the gradation.At the locality
Kožica we recorded the calamity of winter moths in
1992. Parsitism of mature caterpillars was 68.97%.The
presence of hyperparasitoids in them was only 6.9%,
the coincidence of parasitoids and hyperparasitoids
was 3.45%. In the following year, relative abundance
of winter moths decreased by half, but the percentage
of parasitized caterpillars remained very high – 37.5%.
The presence of hyperparasitoids was recorded in
15.63% of caterpillars and all of them coincided with
primary parasitoids.


Absolute parasitism of exposed caterpillars and
pupae was recorded on the locality Brankovac. In the
first postculmination year 64.51% of caterpillars were
parasitized.The hyperparasitoid larvae were present in
12.90% of caterpillars and the coincidence of parasitoids
and hyperparasitoids occurred only in 9.68% of
caterpillars.


In Forest unit Košutnjak in exposed conditions, the
abundance of parasitoids varied from 27.27% to
43.75%. Infestation of hyperparasitoids was very high
and it varied from 38.46% to 93.75%.The degree of
their coincidence, however, was not harmonised. The
highest percentage of caterpillars infected by parasitoid
and hyperparasitoid larvae was 31.25%, i.e. averagely
only 17.29% caterpillars.


The results of t-test (LSD), for the differences regarding
the time of sampling proves that there is no statistically
significant difference in parasitism depending
on the time of sampling of younger caterpillars.This
can be an important warning to the experts who plan
forest protection, especially if repressive measures of
control are applied. Suppression should be applied


th


against early instars of larvae (e.g. about 20 of April),
because in this way the natural potential of parasitoids
is going to be preserved.This depends of local climate,
elevation and specific ecological conditions.


To determine the level of egg parasitoids, the method
of exposing eggs was applied at many localities.
Thus egg parasitoidT. minutuswas identified at the lo


cality Miroč, compartments 73/74.Total parasitism of
winter moth eggs was 43.24%.Almost 30% ofO. brumataeggs
were parasitized.AlthoughE. defoliariawas




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dominant at the locality Miroč, eggs of this species
were less parasitized (8.11%). Egg parasitism of A. aurantiariawas
lower - only 5.4%. Parasitized eggs are
brown, so they can be readily differentiated from the
eggs parasitized by waspsTrichogramma sp. Thedissection
of dead eggs revealed the presence ofT. minutuslarva
in them.


In the Forest units Zlatica, Boljetinska reka and
Mala Moštanica the waspsTrichogramma sp.(Hymenoptera:
Trichogrammatidae) were reared from winter
moths eggs. Parasitized eggs are distinguished by their
almost black colour. In this way, we can assess the parasitism
even after the eclosion of parasitic wasps.The
winter moth eggs were parasitized between 16.33% at
Boljetinska Reka, compartment 44, to 33.95% at Zlatica,
compartment 96. It was found out that the majority
of eggs died from other causes (e.g. predators).At
Zlatica, compartment 59, the total mortality of eggs


DISCUSSION
Many authors give the data on population dynamic
of E. defoliaria (Patočka et al.,1968; Glavendekić,
1988, 1999). During our study, mottled umber
moth was recorded in all localities, most often in a
lower population density except in East Serbia, where
it was dominant compared to the populations of other
early-season defoliators.
Winter moth population dynamics has been studied
in different forest types. Based on our own data and literature,
it is evident that frequent outbreaks of 9 winter


moth species are of chronic type and characteristic for
the following forest types: forest ofTurkey oak and sessile
oak (Quercetum petraeae-cerris) on brown and les


sive brown soil on serpentinite at the locality Brankovac;
forests of sessile oak (Quercetum montanum typicum) on
acid brown soil in the locality Porečke šume, compartment
54 f; in the forest of Hungarian oak andTurkey oak
with Eastern hornbeam (Quercetum frainetto-cerris carpinetosum
orientalis) on dystric and eutric brown soils
on Bukovik; in the association Orno-Quercetum pubescentis-
virgilianae in Košutnjak and in the artificially
established stand of mixed oaks at Mala Moštanica.
Plantations of pedunculate oak mixed with hornbeam in
forest unitVisoka šuma Lošinci are also under threat of
winter moths outbreaks.


Winter moths occur regularly, but as a rule there are
no outbreaks in the forest of sessile oak, Turkey oak
and hornbeam (Carpino-Quercetum petraeae-cerris)
onbrown forest soil and lessive brown forest soil.


The study of parasitoids and hyperparasitoids ofE.
defoliariashows that parasitic wasps fam. Braconidae
are not narrowly specific for theE. defoliaria


The fauna of parasitic wasps in the fam. Ichneumonidaeisrelatively
poor also if compared to the fauna of
other European countries, Slovakia and the former
was 58.49%. In Zlatica, compartment 96 egg mortality
was 44.65%.


The level of egg parasitism of winter moths in natural
population in the management unit Zlatica, compartment
59 was 33%. Larval eclosion was recorded
from 41.51% of eggs, whereas 25.47% eggs died during
the embryonic development. In the Forest unit Zlatica,
compartment 96, the parasitized eggs were almost
34%.The mortality during the embryonic development
was 10.7%According to the report of the Diagnose-forecasting
service, a mass occurrence of winter moths
was forecast for the spring in 1992 in these compartments,
but it failed.The efficiency of egg parasitoids in
the management unit Boljetinska Reka, compartment
44, was somewhat lower, there were altogether 16.33%
parasitized eggs. Egg mortality during embryonic development
was 14.28%.


– Rasprava
USSR (Herting, 1965, 1976; Čapek, and Čepelak,
1981;Čapek,1985). One of the reasons is that
winter moths in the study period were in pre-culmination,
culmination or in the first post-culmination years,
when parasitoid populations in the fam. Ichneumonidaeare
usually low.They dominate in the phase of latency,
while in the culmination phase they retreat
before Tachinidae.


Eulophus larvarum is the most frequent and the
most numerous representative of parasitic wasps in the
superfamily Chalcidoidaea.In the conditions of winter
moth outbreaks, it is a dominant representative of parasitic
Hymenoptera.In the host culmination phase, this
species also showed a great upswing of abundance.


Egg parasitoids Trichogramma sp. and Telenomus
minutushave been described.The research was performed
in the entire study area, but egg parasitoids were
detected only at the locality Mala Moštanica, Zlatica and
Miroč. Egg parasitoidT. minutuswas so far recognized
only as the parasitoid ofOrthosia miniosa(Lepi doptera,
Noctuidae) (Kozlov and Kononova, 1983), and
Operophtera spp.(Glavendekić&Gruppe,1992).


Tachinidae are the most significant winter moth parasitoids
on many localities. The dominance and frequency
of B. nigripes, P. nemea are expected and in
harmony with the results of the studySisojević and
Čepelak,(1998).TachinidsP. magnicornis, andP. fissicorniswere
found individually. In the study of population
dynamics of early-season defoliators in the
Management unit Kožica in the period 1992–1994, a
high population density was recorded in 1992, and already
in the following year there was a drastic decrease
of population density.This was caused, first of all by caterpillar
parasitoids, which reduced ca. 67%.The most
represented parasitoids wereTachinidae. On that occa




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sion, the above tachinid parasitized 69% of host caterpillars.
Parasitoids are mainly dependent on the stage of caterpillars;
Braconidae and Chalcidoidaea prefer the
younger stages, while Ichneumonidae and Tachinidae
more often attack the third instars and older caterpillars.


Some of hyperparasitoids are very broad polyphages


(G. areator,Habrocytus chrysos, andPediobius folio rum),


so they were the subject of the study of the parasitoid complex
of various hosts: gypsy moth, brown-tail moth, leaf
rollers, etc.As it can be concluded from the above study
results, parasitoids and hyperparasitoids are predominantly
polyphagous. Population density ofE.defoliariadepends
largely on its natural enemies, because they have a
significant influence on the population reduction.


CONCLUSIONS – Zaključci


1. The parasitoids in the following families were recorded
on E. defoliaria: Braconidae, Ichneumonidae,
Eulophidae, Torymidae, Trichogrammatidae,
Scelionidae andTachinidae. There are altogether 16
species reared from various stages of the host.
2. Abundance of parasitoids depends on the phase of
host outbreak. In the phase of culmination, the markedly
dominant species areTachinidae; the abundance
of Eulophiadae is elevated, while Ichneumonidae dominate
in the latency.
3. Regarding their trophic characteristics, they are
mainly polyphagous with a wide spectre of hosts in
the group winter moths and order Lepidoptera.


4. Total parasitism of winter moths in natural conditions
varied from 16,33% to 33%.Total parasitism
in exposed conditions was from 27,27% to 43,75%.
5. Five species of hyperparasitoids ofE. defoliariafall
into the families Ichneumonidae,Perilampidae, Pteromalidae
and Eulophidae and they are polyphagous
species.
6. Recorded parasitoid-hyperparasitoid complex is related
to the host species in the belt of oak forests.
This indicates their co-evolutive relationship. The
coevolution between parasitoids and hyperparasitoids
toE. defoliariaoffers an ideal theoretic foundation
for the biological control.


ACKNOWLEDGEMENT– Zahvala
I would like to acknowledge tothank Prof. Dr. K. tification of particular species. Financial support for
Horstmann, Prof. Dr. J. Kolarov, Prof. Dr. L. Mihajlo-the research was given by Ministry of Sciences and
vić, Dr. Kozlov, Dr. Čapek and Dr.Tschorsnig for iden-Technologies Republic of Serbia.


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............ .. ..... ....,
.......... ............. .......... ... .....
.... ...., “.....”, ..........




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SAŽETAK: Istraživanja biologije i ekologije velikog mrazovca – Erannis defoliaria
Clerck, 1759 (Lepidoptera, Geometridae) provedena su u razdoblju 1985–2009 g. u hrastovim
šumama u Srbiji. Veliki mrazovac je za vrijeme istraživanja pretežno pretežito bio
u latenci. Jedino u Gazdinskoj Gospodarskoj jedinici Miroč i Zlatica bio je dominantna
vrsta u kompleksu ranih defolijatora hrasta. Prirodni neprijatelji, posebice parazitoidi i
hiperparazitoidi odnosima ishrane vezani su za stadije ličinke i kukuljice E. defoliaria i
važan su čimbenik njegovog mortaliteta.


Istraživanjima su obuhvaćeni svi razvojni stadiji velikog mrazovca. Primijenjene su
odgovarajuće metode u laboratoriju i u prirodi, u različitim šumskim zajednicama. Rad
na terenu proveden je standardnim metodama entomoloških istaživanja. Metoda ekspozicije
u prirodnim uvjetima primijenjena je na stadiju jajeta i ličinke primjenom ljepljivihpojasa pojaseva u vrijeme aktivnosti ženki. Ženke su polagale jaja u pukotine kore ispod
ljepljivih pojasapojaseva. Komadi kore s jajima izrezani su i odnošeni u laboratorij na
daljnji uzgoj i obradu. Ljepljivi pojasevi upotrjebljeni su i za ekspoziciju gusjenica, pa su
stoga obnavljani u travnju i svibnju. Gustoća populacije gusjenica utvrđivana je kada su
bile pretežito u drugom larvalnom stadiju i djelomično u trećem larvalnom stadiju. Apsolutna
abundanca domaćina utvrđena je brojanjem listova ili otvorenih pupoljaka i gusjenica
u uzorku. Relativna abundanca utvrđena je na temelju proračuna broja gusjenica na
1000 listova.


Veliki mrazovac zabilježen prisutan je na svim lokalitima, najčešće u niskoj gustoći populcije.
U šumskim upravama Miroč i Zlatica, međutim, on je bio dominantan (65% ranih
defolijatora). Gusjenice mogu varirati u boji (slika 1). Jajni parazitoidTrichogrammasp.
(Hym., Trichogrammatidae) utvrđen je na nekoliko lokaliteta u širem području Nacionalnog
parka Djerdap i u okolini Beograda. Rod Trichogramma je polifagan i nije specifičan
samo za velikog mrazovca. Nešto uže specijaliziran je jajni parazitoid Telenomus
minutus, koji je utvđen u istočnoj Srbiji na lokalitetu Miroč. Larvalni parazitoidi su: Protapanteles
immunis,Cotesia limbata,C. jucunda(slika 2) (Hym., Braconidae),Casinaria
ischnogaster,C. moesta,Phobocampe crassiuscula,P. pulchella,Phobocampe sp. (Hym.,
Ichneumonidae) (slika 3). Euplectrus bicolor, Eulophus larvarum (Hym., Eulophidae),
Blondelia nigripes,Phryxe magnicornis,P. nemea,Peribaea fissiconis(Diptera, Tachinidae).
Ustanovljeno je i 5 vrsta hiperparazitoida:Gelis areator,Bathythrix lamina(Hym.,
Ichneumonidae), Perilampus ruficornis (Hym., Perilampidae); Habrocytus chrysos
(Hym., Pteromalidae), Tetrastichussp. (Hym., Eulophidae).


Ključne riječi:Quercusspp., hrast,Erannis defoliaria, veliki mrazovac, parazitoid,
hiperparazitoid