231
ACTA ZOOLOGICA BULGARICA
Applied Zoology
Resea ch A icle
Ac a Zool. Bulg., June 2025, 77 (2): 231-241
Published online 14 June 2025
DOI: h ps://doi.o g/10.71424/azb77.2.002847
*Co esponding au ho : [email p o ec ed]
h ps://www.ac a-zoologica-bulga ica.eu/2025/002847
T ue Bugs (Hemip e a: He e op e a) Collec ed in an
Oil-Bea ing Rose Ag ocenosis in he Kazanlak Valley, Bulga ia
Desisla a S oiano a*, Tania Ka akiche a & Lyudmila Lozano a
Ins i u e o Biodi e si y and Ecosys em Resea ch, Bulga ian Academy o Sciences, 1 Tsa Os obodi el Bl d., 1000 So ia,
Bulga ia; E-mails: [email p o ec ed]; ania_ka akiche a@ab .bg; [email p o ec ed]
Academic edi o : D agan Chobano
Abs ac : We s udied he species composi ion and abundance o He e op e a in an oil-bea ing ose plan a ion in he
Kazanlak Valley, Sou he n Bulga ia. Insec s we e collec ed using wo ypes o aps – s icky and unnel
aps – combined wi h h ee ypes o isual s imuli ( luo escen yellow, anspa en and pu ple). O e a
ou -mon h pe iod (June o Sep embe 2023), a o al o 152 specimens ep esen ing 22 species o eigh
amilies we e collec ed. Ou esul s indica e ha some species a e signi ican ly mo e a ac ed o ce ain
colou s and ap ypes han o o he s. Insec s belonging o he subo de He e op e a, a e no among he
pes s causing economic losses in Bulga ian oil-bea ing ose p oduc ion. Howe e , he p esence o he
in asi e pes species, Halyomo pha halys (S ål, 1855), aises conce ns abou he damage his pes could
cause o ose plan a ions in Bulga ia. Addi ionally, ou indings sugges ha he p eda o De aeoco is u-
be , he mos abundan species in he samples, migh con ibu e o aphid popula ion con ol in he s udied
ag icul u al se ing. Fu he esea ch would be bene icial o assess i s e ec i eness as a biological con ol
agen in oil-bea ing ose plan a ions and o he cul i a ed c ops.
Key wo ds: biological agen s, oil-bea ing ose, colou ed aps, pes s, Rosa damascena Mill.
In oduc ion
Roses ha e been g own in Bulga ia since ancien
imes wi h he Th acians being he ea lies known
inhabi an s who cul i a ed hem (He odo us, VIII,
138: ca. 430BC; Za e 2018). The a ou able con-
di ions in he Sub-Balkan alleys and he low sou h-
e n slopes o he Balkan Moun ains (which ha e
acqui ed he name “Rose Valley”), wi h mode a e
ain all, a la ge numbe o sunny days and sui able
ligh - ex u ed soils, ha e been he p e equisi es o
he success ul cul i a ion o oses. The con empo-
a y comme cial ose p oduc ion in Bulga ia is con-
cen a ed in he same dis inc geog aphical egion
(Ko ache a e al. 2010) and oil-bea ing oses a e
he mos economically signi ican c ops among es-
sen ial oil-bea ing plan s in he coun y (Ma gina e
al. 1999, Rusano e al. 2020).
Rosa damascena Mill. (wi h common name
Damask ose) is p ima ily used o ose oil p oduc-
ion wo ldwide (Ko ache a e al. 2010). In Bulga -
ia, nowadays Rosa damascena Mill. . igin ipe ala
232
S oiano a D., Ka akiche a T. & Lozano a L.
Dieck. (Kazanlak ose) (Chalo a e al. 2017, Cais-
sa d e al. 2023) has been mainly used o cul i a-
ion pu poses. Some au ho s accep i as a sepa a e
axon, Rosa igin ipe ala Dieck. ex Koehne = R. ka-
zanlika V. T. 1978 (see Topalo 1978 a e Rusano
e al. 2020, Ma gina e al. 1999, Zla e e al. 2001).
In ou s udy we use he widely accep ed name Rosa
damascena Mill. . igin ipe ala o he Kazanlak
oil bea ing ose.
The oil-bea ing oses cul i a ed in Bulga ia a e
a acked by a ious pes s, leading o a signi ican e-
duc ion in ose yields (A anaso e al. 2008). This is
why, a e he mid-20 h cen u y, signi ican e o s
we e made o s udy insec s and o he in e eb a es
associa ed wi h oil-bea ing oses cul i a ed in he
coun y (Bu esh & Laza o 1956, Nikolo a & Na -
sko a 1965, Nikolo a & Na sko a 1968, Nikolo a
1967, 1969a,b, 1972).
In espec o Hemip e a, some o he majo
pes s o oil-bea ing oses in Bulga ia belong o he
subo de s Aucheno hyncha and S e no hyncha
(Nikolo a 1969a,b, Ma gina e al. 1999, A anaso
a al. 2008), among hem Edwa dsiana osae (Lin-
naeus, 1758) Mac osiphum osae (Linnaeus, 1758)
and Rhodococcus pe o na us (Cocke ell & Pa o ,
1899). Compa ed o he men ioned wo Hemip e a
subo de s, He e op e a (o ue bugs) – a g oup wi h
abou 40,000 desc ibed species wo ldwide (Schuh
& Wei auch 2020), has ecei ed signi ican ly less
a en ion in en omological s udies exclusi ely o-
cused on ose plan a ions in Bulga ia. In he book,
Nikolo a (1969b) epo ed ha , in he s udied ex-
pe imen al ose plan a ions, He e op e a was ep-
esen ed by 59 species o eigh amilies. Nikolo-
a (1969b) u he commen ed ha wo o hese
species, G aphosoma linea um (Linnaeus, 1758)
(Pen a omidae) and Co eus ma gina us (Linnaeus,
1758) (Co eidae), we e ha m ul o oses, eigh we e
lis ed as zoophages and 49 we e species wi h no
signi ican in luence on he a ge cul u e. Ne e -
heless, Nikolo a (1969b) lis s only he names o
15 species o He e op e a ( o mo e de ails see he
Discussion sec ion o his s udy). Also, in he same
book, Palomena p asina (Linnaeus, 1761) (Pen-
a omidae) is lis ed among he zoophages (bene i-
cial insec s), while he species is in ac phy opha-
gous (Rösch & Schmi z 2014). In a la e s udy o
pes s in ose plan a ions in Bulga ia, only one addi-
ional species o He e op e a is epo ed as a pes o
oil-bea ing oses (Ma gina e al. 1999) – Eu ydema
o na a (Linnaeus, 1758) (Pen a omidae). La e , Ba-
le ski e al. (2008) men ions species o He e op e a
as bene icial o ganisms in oil-bea ing ose plan a-
ions in Bulga ia.
Mo e da a on communi ies o He e op e a, in-
cluding bo h phy ophagous and zoophagous species
(po en ial biological agen s) and hei ela ionship
wi h oil-bea ing oses in Bulga ia would be use ul
o pes managemen in ose plan a ions in he coun-
y. The e o e, we ocused he p esen s udy on his
g oup o insec s.
Va ious me hods ha e been employed o s udy
insec abundance and species composi ion in ag o-
cenoses (McC a y 2018). Among hem, hose ely-
ing on s icky aps a e ela i ely e ec i e and inex-
pensi e in assessing he di e si y o ha m ul insec s
and hei na u al enemies (A akan e al. 2016). A
disad an age o his ype o aps is ha hey be-
come ine ec i e when he s icky su aces a e co -
e ed wi h insec s (Ahmad & Kama udin 2011). Fun-
nel aps mi iga e his issue and a e eusable, which
makes hem e y use ul in en omological esea ch
(Lindg en 1983). Howe e , hei e ec i eness can
a y depending on he a ge insec species and en-
i onmen al condi ions (Allison e al. 2014). The e-
o e, he combined use o bo h ap ypes seems
mo e easonable han employing only unnel aps
o only s icky aps.
In addi ion o he ype o ap, i s colou can
also a ec he composi ion o he caugh insec s.
Fo example, yellow aps p ima ily a ac whi e-
lies, lies, aphids and o he he bi o ous insec s
(Ilie a & Ka o a 2023). In con as , indi iduals
o Lygus ugulipennis Poppius, 1911 (Mi idae) a e
cap u ed mo e equen ly in blue s icky aps han
in yellow ones (Holopainen e al. 2001), while pu -
ple p ism aps e ec i ely collec species o amily
Pen a omidae (Pezzini e al. 2018). Addi ionally,
he use o di e en ypes o colou aps, including
pan ap, whi e colou ed modi ied Moe icke aps,
s icky aps and d y unnel aps allows esea ch-
e s o e alua e how a ac i e ce ain colou s a e
o speci ic insec g oups o species (Sakalian e
al. 1993, Kalushko & Dimo a 1997, Langou o
2001, Sakalian & Langou o 2004, Langou o
& Simo 2006, Guéo guie & Ljubomi o 2009,
Simo 2013, Subche e al. 2013, Tosho a e al.
2017, Lape a-Gjono a & Ljubomi o 2020, Pa -
lo a 2020).
In he p esen s udy, ecognising hei limi a-
ions and ad an ages, we employed bo h s icky and
unnel aps. We combined each ap ype wi h isual
s imuli ( luo escen yellow, anspa en and pu ple),
o assess he species composi ion and abundance
o He e op e a in ose plan a ions in S a a Zago a
P o ince. We also analysed he simila i ies among
assemblages o He e op e a, ela i e o he di e en
ap ypes.
T ue Bugs (Hemip e a: He e op e a) Collec ed in an Oil-Bea ing Rose Ag ocenosis in he Kazanlak...
233
Ma e ials and Me hods
Collec ion o Ma e ial and Taxonomic
Iden i ica ion
F om June o Sep embe 2023, a su ey was con-
duc ed o de e mine he species composi ion o
insec s in oil-bea ing ose (Rosa damascena Mill.
. igin ipe ala) plan a ions o e an a ea o en de-
ca es nea Gaba e o Village, Pa el Banya Munici-
pali y, S a a Zago a P o ince. Two ypes o colou
aps we e used: s icky (p ism ype, PALs and o h-
e s) and unnel (Lindg en ype, MUL and o he s),
bo h ypes ha e o en been employed in such s udies
(Im ei e al. 2020a,b, Pe ko ich e al. 2022, Pe ice
e al. 2023). We combined he aps wi h h ee ypes
o isual s imulus: luo escen -yellow, anspa en
and pu ple colou . The e we e six combina ions o
ap ype and colou , wi h h ee eplica es pe com-
bina ion, so in o al 18 aps we e se up (Fig. 1).
The luo escen -yellow and anspa en aps we e
ins alled on 4 h o June and he pu ple aps on 6 h o
July. The aps we e placed 7–10 me e s apa . T ap
ca ches we e collec ed e e y 7–14 days. No plan
p o ec ion p oduc s we e used du ing he s udy pe-
iod. The analysis was pe o med in R e sion 4.4.2
(R Co e Team 2025).
Iden i ica ion o he collec ed insec s was done
using he ollowing keys: Ke zhne & Yache sky
(1964), Wagne (1974), Josi o (1981), Pe ica
(1998). The da abase “Lea mine s and Plan Galls
o Eu ope” was used as he p ima y sou ce o die
in o ma ion o he collec ed species. Addi ional
sou ces a e ci ed in he species commen s in he Dis-
cussion sec ion.
Fig. 1. Types and colou s o aps: s icky aps (A–D); unnel aps (E–F); scheme o hei dis ibu ion in he ield (G).
234
S oiano a D., Ka akiche a T. & Lozano a L.
S a is ical analysis
We es ed whe he a speci ic species o He e op e a
is mo e s ongly a ac ed o a ype o aps wi h
ce ain colou , as well as independen ly o only he
colou o only he ap ype. Fo his pu pose, we
analysed da a on he p esence o absence o he
collec ed species in each sample using he unc-
ion mul ipa om he R package indicspecies (De
Cáce es & Legend e 2009). To quan i y he associa-
ion be ween a gi en species and a gi en ap ype
(o combina ion o ap ype and colou ) we used
he es s a is ic IndVal.g. This a ian o he o iginal
IndVal index accoun s o di e ences in g oup sizes.
In ou case, such di e ences come om he ac ha
he pu ple aps we e ins alled a mon h la e han he
es o he aps (see he subsec ion abo e).
To explo e pa e ns in insec specimen coun s
and species composi ion ac oss di e en ap ypes,
we used hie a chical clus e ing wi h he B ay-Cu is
dissimila i y index, wi h species abundance ( ecal-
cula ed pe 100 apping days) summa ized ac oss
all samples o each espec i e ap ype. The spe-
cies abundance used o he hie a chical clus e ing
was calcula ed as he numbe o indi iduals collec -
ed pe species in a gi en sample (see he able be-
low) di ided by he apping days o he espec i e
sample and hen mul iplied by 100.
We applied boo s apping wi h 9,000 eplica e
esampling. The clus e ing analysis was pe o med
using he p og am PAST 4.17 (Hamme & Ha pe
2001).
Resul s
Collec ed ma e ial
The numbe o collec ed specimens o each species
is p o ided below (in pa en heses) o each sampling
pe iod ( he pe iods o ap ins alla ion and collec ion)
and each ap ype: luo escen unnel (FF), luo es-
cen s icky (FS), pu ple unnel (PF), pu ple s icky
(PS), con ol unnel (CF) and con ol s icky (CS). The
amilies and species a e lis ed in alphabe ical o de .
Co eidae: Co eus ma gina us (Linnaeus,
1758): 06. VII–20. VII, PF (1); 16. VIII–9. IX, FF
(1); 24. VI–3. VII, FF (1).
Cydnidae: Oche os e hus sp.: 24. VI–3. VII,
FF (1). Sehi us mo io (Linnaeus, 1761): 24. VII–04.
VIII, PS (1). T i omegas sexmacula us (Rambu ,
1839): 12. VI–24.VI, CF (1).
Lygaeidae: Melanoco yphus albomacula us
(Goeze, 1778): 04. VIII–16. VIII, PS (1), CS (1); 06.
VII–20. VII, CS (2); 08. VI–12. VI, CF (1), CS (1);
12. VI–24.VI, FS (1), CS (2); 16. VIII–9. IX, PS (1);
20. VII–24. VII, CF (1); 24. VI–3. VII, FS (1), CS (1).
Mi idae: Adelphoco is lineola us (Goeze,
1778), CS (4); 04. VI–08. VI, CS (1); 12. VI–24.VI,
CS (2); 24. VI–3. VII, CS (1). Adelphoco is andali-
cus (Rossi, 1790), PS (1), CS (1); 20. VII–24. VII,
CS (1); 24. VII–04. VIII, PS (1). De aeoco is ube
(Linnaeus, 1758): 03. VII- 6. VII, FS (2); 04. VIII–
16. VIII, PS (3), CS (3); 06. VII–20. VII, FS (2), PF
(7), PS (5), CS (1); 20. VII–24. VII, PS (10), CF (2),
CS (11); 24. VII–04. VIII, PF (3), CF (1). Lygus u-
gulipennis Poppius, 1911: 20. VII–24. VII, PS (1).
Oxyca enidae: Me opoplax o igani (Kolena i,
1845): 08. VI–12. VI, FS (1).
Pen a omidae: Aelia acumina a (Linnaeus,
1758): 04. VIII–16. VIII, FS (1); 08. VI–12. VI, FF
(1); 20. VII–24. VII, PS (1), CF (1). Ca poco is sp.:
16. VIII–9. IX, FF (1). Dolyco is bacca um (Lin-
naeus, 1758): 03. VII- 6. VII, CF (1); 04. VIII–16.
VIII, PF (1), CF (1); 08. VI–12. VI, CF (2); 12.
VI–24.VI, CF (1); 16. VIII–9. IX, CF (1). Eu ydema
ole acea (Linnaeus, 1758): 20. VII–24. VII, PS (1).
Eu ydema o na a (Linnaeus, 1758): 04. VIII–16.
VIII, FS (4); 16. VIII–9. IX, PF (1); 20. VII–24.
VII, FS (3), PS (5), CS (4); 24. VII–04. VIII, PS (2),
CS (2). Eysa co is en alis (Wes wood, 1837): 24.
VII–04. VIII, CF (1). G aphosoma i alicum (O.F.
Mülle , 1766): 03. VII- 6. VII, CF (1); 06. VII–20.
VII, FF (1), PF (1); 12. VI–24.VI, FS (1); 20. VII–
24. VII, FS (1), CF (1); 24. VI–3. VII, CF (1); 24.
VII–04. VIII, PF (1), CF (1). Halyomo pha halys
(S ål, 1855): 20. VII–24. VII, PF (2). Neza a i id-
ula (Linnaeus, 1758): 12. VI–24.VI, CF (1), CS (1).
Pe ibalus s ic us (Fab icius, 1803): 04. VIII–16.
VIII, CS (1); 20. VII–24. VII, CS (1).
Redu iidae: Phyma a c assipes (Fab icius,
1775): 12. VI–24.VI, FS (1). Rhynoco is punc i en-
is (He ich-Schae e , 1846): 03. VII- 6. VII, CF
(1); 06. VII–20. VII, FF (1), PF (2), CF (1).
Rhypa och omidae: Aphanus oland i (Lin-
naeus, 1758): 04. VIII–16. VIII, CS (3). Beosus
ma i imus (Scopoli, 1763): 16. VIII–9. IX, PS (1),
CS (2). Emble his sp.: 04. VIII–16. VIII, CS (1).
Megalono us sp.: 24. VI–3. VII, CS (1); 20. VII–24.
VII, CS (1); 04. VIII–16. VIII, FS (1); 16. VIII–9.
IX, FS (2), PS (2), CS (2). Raglius sp.: 16. VIII–9.
IX, FS (1).
Species composi ion o he samples
The o al numbe o collec ed He e op e a was 152
indi iduals, belonging o eigh amilies, 27 gene a
and 22 species. Due o he poo condi ion o he
ma e ial om he s icky aps, wo specimens we e
iden i ied only a he amily le el (one o Mi idae
and one o Lygaeidae, bo h no included in he lis ed
T ue Bugs (Hemip e a: He e op e a) Collec ed in an Oil-Bea ing Rose Ag ocenosis in he Kazanlak...
235
abo e specimens) and i e only a he genus le el.
The mos abundan species was De aeoco is ube
(Linnaeus, 1758) (Mi idae), while Eu ydema o na a
(Linnaeus, 1758) (Pen a omidae) was he second
mos abundan species.
Among he collec ed species, he e we e bo h
p eda o s and phy ophages. The p eda o y species
we e o amilies Mi idae and Redu iidae. Phy-
ophages o hose wi h mixed eeding habi s we e
o Co eidae, Cydnidae, Lygaeidae, Mi idae, Oxy-
ca enidae, Pen a omidae and Rhypa och omidae.
In e ms o he numbe o cap u ed specimens,
phy ophages p edomina ed wi h 94 specimens. The
numbe o p eda o s was smalle – 56 specimens
and he e we e only wo specimens om species
wi h a mixed eeding ype.
Associa ion be ween speci ic species and ap ypes
In he p esen s udy, De aeoco is ube (IndVal.g
= 0.47, p = 0.03) was mos equen ly collec ed
wi h he pu ple s icky aps. The analysis in which
we used only he colou o he aps con i med ha
his species is mos ly a ac ed o he pu ple colou
(IndVal.g = 0.48, p = 0.04). Eu ydema o na a was
collec ed p edominan ly by he pu ple s icky aps
(IndVal.g = 0.44, p = 0.04). In he analysis based
solely on colou s, he e was no signi ican associa-
ion be ween Eu ydema o na a and he pu ple col-
ou . The analysis in which we used only he ype o
aps showed ha Dolyco is bacca um and Rhyno-
co is punc i en is (Redu iidae) we e mainly col-
lec ed in unnel aps (IndVal.g = 0.42 and IndVal.g
= 0.38, espec i ely and p = 0.01 o bo h species).
The esul s o he es o he species we e no s a is-
ically signi ican .
Simila i ies in assemblages o He e op e a,
ela i e o di e en ap ypes
The highes numbe o species – 11, was collec -
ed wi h con ol s icky aps, ollowed by pu ple s icky
and luo escen s icky – wi h nine species collec ed
by each. Among he unnel aps, eigh species we e
collec ed in con ol unnel, ollowed by pu ple un-
nel – six species and luo escen unnel – i e species.
The clus e ing showed ha he luo escen unnel
aps dis inc ly sepa a ed om he o he aps ypes –
low simila i y index wi h s ong suppo (100% boo -
s ap alue). The s icky aps we e g ouped oge he
and wo o he unnel aps we e also oge he (Fig.
2), bu bo h o hese g oups we e cha ac e ised wi h
low suppo (62% boo s ap alues).
Discussion
Species dis ibu ion, die and hos plan
p e e ences
Among he collec ed species, nine belong o he
Medi e anean complex (acco ding o Josi o 1999),
namely Adelphoco is andalicus, Aphanus oland i,
Fig. 2. Hie a chical clus e dend og am based on B ay-Cu is Index alues, showing he simila i y among ap ypes
in espec o assemblages o He e op e a. T ap ypes: con ol unnel (CF), con ol s icky (CS), luo escen unnel (FF),
luo escen s icky (FS), pu ple unnel (PF), pu ple s icky (PS). The pe cen age o eplica es, whe e each node is s ill
suppo ed, is also p esen ed.
236
S oiano a D., Ka akiche a T. & Lozano a L.
Beosus ma i imus, Eysa co is en alis, Melanoco -
yphus albomacula us, Me opoplax o igani, Phyma-
a c assipes, Rhynoco is punc i en is, T i omegas
sexmacula us (Rambu , 1839). The es o he spe-
cies (wi h he excep ion o wo alien species, com-
men ed below) a e om he Eu o-Sibe ian complex,
ep esen ed in ou s udy by Hola c ic, Holopalaea c-
ic and Wes Palaea c ic species (cha ac e ised ac-
co ding o Josi o 1986 o Josi o 1999).
The la ges numbe o indi iduals we e o am-
ily Mi idae, which is logical since i is he mos di-
e se and species- ich amily o subo de He e op-
e a (Ha izano e al. 2010, Kim e al. 2023). The
mos abundan species in he p esen s udy, De aeo-
co is ube , belongs o he sub amily De aeoco i-
nae (Mi idae). Rep esen a i es o his sub amily a e
p edominan ly p eda o s, eeding on a ious small
insec s such as aphids and la ae o h ips and mo hs
(Kim e al. 2023). The peak abundance o D. ube ,
in June and July, coincides wi h he peak popula ion
le els o he g een ose aphid Mac osiphum osae
(Linnaeus, 1758), a majo pes causing economic
losses in oil-bea ing ose p oduc ion in Bulga ia
(Nikolo a 1969b) and sugges s a ela ionship be-
ween he abundance o hese species. De aeoco is
ube has also been ound on o he plan s in es ed
by aphids (Yazici 2019) and may p ey on species
like Chae osiphon e a hodum (Walke , 1849),
Myzaphis buck oni H.R.L. Da is, 1919, Aphis abae
Scopoli, 1763, Mac osiphum eupho biae (Thomas,
1878), Myzus pe sicae (Sulze , 1776), which a e
ound on oses bu cause less damage (And ee
2018). Addi ionally, D. ube has been obse ed
eeding on he scale insec Eulecanium iliae (Lin-
naeus, 1758) in Se bia (De ise ic e al. 2024).
While i may help o con ol aphid popula ions in
ag icul u e, i s e ec i eness in ose plan a ions e-
mains undocumen ed, wa an ing u he esea ch.
Adelphoco is lineola us, Adelphoco is an-
dalicus and Lygus ugulipennis (Mi idae) we e p e-
sen wi hin and a ound he s udied a ea. These a e
phy ophagous species, associa ed wi h he baceous
plan s o he han oses (Holopainen e al. 2001,
Kmen & Bana 2012, Fen & Okya 2022).
The collec ed species o amily Pen a omidae
a e widely dis ibu ed h oughou he coun y. Eu-
ydema o na a was he second mos abundan spe-
cies in he samples. This species has ophic ela-
ionships wi h plan s o B assicaceae and Apiaceae
(g owing nea he plan a ion) a he han wi h oses
– his could be he eason o he abundance o E.
o na a. Ano he possible explana ion could be ha
he indi iduals we e a ac ed o he colou o he
aps du ing mig a ions (cap u ed in con ol s icky,
luo escen s icky, pu ple s icky and pu ple unnel
aps).
In he aps, wo in asi e alien phy ophagous
species, Halyomo pha halys and Neza a i idula
(Pen a omidae) we e ound. Halyomo pha halys
o igina es om Eas Asia (Zhu e al. 2012) and in
2016 was ound o he i s ime in Bulga ia (Simo
2016). This polyphagous species a ec s bo h local
and o namen al plan s (Hemala & Kmen 2017) and
has become a majo in asi e pes wi h implica ions
o plan p oduc ion in many egions (K i icos e
al. 2017, Mais ello e al. 2017, Vé ek & Ko anyi
2017, Pajač Beus e al. 2024). Be ween 2017 and
2024, he species sp ead apidly ac oss Eu ope and
o he egions, causing se e e damage o ui o -
cha ds and ege able c ops (Mais ello 2024). Spe-
cies dis ibu ion models ha e indica ed i s po en ial
o widesp ead colonisa ion, d i en by i s b oad hos
ange and i s high clima ic adap abili y (Zhu e al.
2012, K i icos, 2017). In I aly, in a s udy, combin-
ing c owdsou ced da a and spa ial modelling, he
in asion dynamics o his species ha e been acked
(Mais ello e al. 2018), indica ing he impo an
ole ha ci izen-science can play in ea ly de ec ion.
I should be men ioned, ha o his species mul iple
in oduc ion e en s ha e been sugges ed based on
gene ic s udies ac oss No h Ame ica and Eu ope
(Mo ison e al. 2017, Valen in e al. 2017). Halyo-
mo pha halys has been epo ed o cause damage o
a ious ag icul u al c ops in Bulga ia (H is ozo a
& Ha izano a 2022). In he ligh o he esul s o
he ci ed pape s, he p esence o H. halys in a ose
plan a ion is conce ning and i s ole as a po en ial
pes equi es u he s udy. In espec o his species’
na u al enemies, a ecen s udy ca ied ou in Bul-
ga ia, Plo di P o ince (H is ozo a & Ha izano a
2024), epo s i e species o egg pa asi oids na u-
ally occu ing in eggs o H. halys and he au ho s
sugges ha he adap a ion o his new hos will lead
o g adual inc ease o he pa asi isa ion a es in na -
u al popula ions o H. halys.
Neza a i idula is economically impo an pes
a ec ing many ag icul u al and wild plan s wo ld-
wide (Ma cu & G ozea 2020, P abhaka e al. 2023).
I likely o igina es om he Medi e anean egion o
A ica (Hokkanen, 1986, Jones 1988) and in 1959,
i was i s egis e ed in Bulga ia (S awinski 1959).
Recen ly, Neza a i idula has sp ead no hwa ds
(Simo e al. 2012).
In ou aps we ound he p eda o s Rhynoco-
is punc i en is and Phyma a c assipes o amily
Redu iidae. Bo h species a e associa ed wi h g assy
ege a ion, sh ubs and low ees. Gi en ha in India,
o example, o he species o Redu iidae, Rhynoco-
T ue Bugs (Hemip e a: He e op e a) Collec ed in an Oil-Bea ing Rose Ag ocenosis in he Kazanlak...
237
is ma gina us (Fab icius, 1794) and Rhynoco is
uscipes (Fab icius, 1787), ha e been ecognised
as bene icial o ag icul u al pes managemen (Sa-
haya aj 2014), he po en ial o R. punc i en is and
P. c assipes as biological con ol agen s equi es
u he in es iga ion.
Species o amilies Co eidae, Cydnidae,
Lygaeidae, Oxyca enidae and Rhypa och omidae,
ound in he aps, a e no di ec ly associa ed wi h
oil-bea ing ose plan a ions. The h ee species o
Cydnidae – T i omegas sexmacula us, Sehi us mo-
io and ep esen a i es o he genus Oche os e hus
– inhabi he li e and uppe soil laye (Lis 1999)
and a e associa ed wi h plan s o Bo aginaceae
and Lamiaceae (Aukema e al. 2007, Kolak 2015).
They ha e occasionally been ound on Rosa sp. and
Mo us sp. (Bolu 2020, Ali 2021).
The amilies Rhypa och omidae and Oxy-
ca enidae we e ep esen ed by he pe obion s (no
epo ed associa ion wi h oses) eeding on seeds
o a ious plan s (Swee 1960, Maleno ský e al.
2011, Kenzhegaliye e al. 2021). Co eus ma gina-
us (Co eidae), p ima ily eeding on plan s o amily
Polygonaceae (Kmen & Baňař 2012), was also ob-
se ed in he aps. Nikolo a (1969b) obse ed ha
nymphs o C. ma gina us ha m oil-bea ing oses in
Bulga ian plan a ions by eeding on hei lea es. In
he same s udy, she epo ed ha adul C. ma gina-
us eed on scale insec s o he genus Rhodococcus
and sugges s ha ac ually hei p esence migh be
mo e bene icial han ha m ul. This hypo hesis needs
u he con i ma ion, since i has no been men-
ioned elsewhe e ha he species has a mixed die .
Addi ionally, in Romania, he e a e epo s o C.
ma gina us being pes on Rosa sp., as well (G ozea
e al. 2023).
Nikolo a (1969b) ca ied ou a s udy mainly
in one expe imen al ose plan a ion in Bulga ia nea
Klisu a Village (Plo di P o ince) and epo ed 59
He e op e a species o eigh amilies, bu names o
only 15 we e p o ided: An hoco idae – An hoco is
pilosus (Jako le , 1877); Nabidae: Himace us mi -
micoides (O. Cos a, 1834), Nabis pseudo e us Re-
mane, 1949; Redu iidae – Rhynoco is i acundus
(Poda, 1761); Tingidae – Dic yla echii (Sch ank,
1782); Mi idae – De aeoco is ube , De aeoco is
u ilus (He ich-Schae e , 1838), De aeoco is lu e-
scens (Schilling, 1837), O hops campes is (Lin-
naeus, 1758) (as Lygus campes is L. in he pape );
Co eidae – Co eus ma gina us; Lygaeidae: Lygaeus
eques is (Linnaeus, 1758); Pen a omidae – Doly-
co is bacca um, Eu ydema ole acea, G aphosoma
linea um (Linnaeus, 1758), Palomena p asina (Lin-
naeus, 1761). Only ou o he species a e epo ed
bo h by Nikolo a (1969b) and in he p esen s udy –
C. ma gina us, D. ube , E. ole acea and Dolyco is
bacca um, sugges ing ha he species composi ion
o He e op e a in ose plan a ions may a y g ea ly,
mainly due o di e ences in bo h he opog aphy
o he pa icula egions and he cha ac e is ics o
he ege a ion wi hin he cul i a ed a ea and i s su -
oundings.
Associa ion be ween ap ypes and speci ic
species and simila i ies in he assemblages
ela i e o he di e en ap ypes
In he p esen s udy, he s a is ically signi ican
IndVal.g alues anged om 0.38 o 0.48, wi h p-
alues be ween 0.01 and 0.04. Acco ding o Du êne
and Legend e (1997), an IndVal.g alue exceeding
0.5 is conside ed indica i e o a s ong associa ion.
The e o e, ou esul s demons a e mode a e as-
socia ions be ween he species and he espec i e
ap ypes o colou s. Addi ionally, due o he small
numbe o cap u ed insec s, i is no possible o d aw
eliable conclusions abou he colou p e e ences o
he s udied species. Howe e , he p esen ed below
specula i e ends migh be use ul in he concep ual-
isa ion o u u e s udies on he a ac i eness o di -
e en colou s in espec o species o He e op e a.
In he p esen s udy, Dolyco is bacca um and
Rhynoco is punc i en is we e mos equen ly col-
lec ed using unnel aps, which aligns wi h he e-
sul s o Lindg en (1983), whe e unnel aps we e
e ec i e in collec ing a ious insec species, es-
pecially la ge ones. This can be explained by he
design o hese aps, which p o ides mo e e icien
cap u e o mo e ac i e and la ge indi iduals (Lind-
g en 1983).
Ou esul s abou he associa ion be ween D.
ube (Mi idae) and he aps wi h pu ple colou
we e simila o hose epo ed by Holopainen e al.
(2001), whe e Lygus ugulipennis (Mi idae) showed
a p e e ence o blue and pu ple aps compa ed
o yellow. These ac s sugges ha some p eda o y
species o Mi idae may be a ac ed o ce ain ligh
wa eleng hs associa ed wi h hese cool colou s.
Howe e , in he p esen s udy, D. ube was cap-
u ed in all ypes o aps excep o he luo escen
unnel ap.
I is no su p ising ha Eu ydema o na a was
collec ed p edominan ly in he pu ple s icky aps,
since o he phy ophagous insec s o amily Pen a o-
midae ha e also been collec ed using pu ple s icky
aps (Pezzini e al. 2018). Rela i ely ew s udies
ha e ocused on he in luence o ap colou on he
cap u e o species om his amily. Fo example,
adul s and nymphs o H. halys appea o p e e black
238
S oiano a D., Ka akiche a T. & Lozano a L.
py amid aps o e yellow, whi e, g een and ans-
pa en ones; his applies o bo h plas ic and wooden
aps (Leskey e al., 2012). Simila esul s we e ob-
ained by Joseph (2014) wi h black aps o Bag a-
da hila is (Bu meis e , 1835). Labo a o y and ield
s udies wi h he Ha lequin bug, Mu gan ia his i-
onica (Hahn, 1834), ha e shown ha his species is
mo e a ac ed o g een and black aps han o whi e,
yellow, ed o pu ple ones (DiMeglio e al. 2017).
I should be no ed ha he esponse o some
o he collec ed species o he colou o he aps in
he p esen s udy may be skewed due o di e ences
in he empe a u e o he aps, which likely a y
be ween ligh e and da ke aps unde ield condi-
ions. This could be an impo an ac o , conside -
ing ha a ecen s udy on Lep oglossus occiden alis
(Co eidae) showed ha his species uses in a ed
signals o loca e hos plan s (Takács e al. 2009).
No single ap ype (s icky o unnel) cap u ed
all species o He e op e a and none collec ed mo e
han hal o he species s udied. Clus e ing analysis
e ealed ha bo h he ype and colou o he aps
in luenced he species composi ion. These ind-
ings sugges ha o comp ehensi e s udies on he
composi ion and abundance o He e op e a, i is
essen ial o use a a ie y o ap ypes and colou s
o accoun o hese di e ences. In addi ion o he
s icky aps and unnel aps, he use o whi e col-
ou ed modi ied Moe icke aps (Langou o 2001) is
also ad isable, since hey ha e p o en e y e ec i e
in s udies on He e op e a (Simo 2013) and in sam-
pling o insec s om o he g oups (Langou o 2001,
Langou o & Simo 2006, Pa lo a 2020).
Conclusion
The collec ed species o He e op e a ha e no p ac i-
cal signi icance as pes s o cul i a ed oil-bea ing os-
es in he s udied egion. The species composi ion o
He e op e a in he s udied ag ocenosis is la gely de-
e mined by he p esence o he baceous plan s wi hin
he ag ocenosis o in he su ounding a ea. The dis-
co e y o he in asi e species Halyomo pha halys
aises he need o u u e moni o ing o his species
and imely ale s in case o a po en ial h ea o i
becoming an economically signi ican pes on oses.
Acknowledgemen s: The s udy was unded by he Bulga -
ian Minis y o Educa ion and Science: he Na ional Science
Fund g an numbe KП-06-H56/1 10.11.2021. We ex end ou
g a i ude o M s. To ka Bane a, o p o iding access o he ose
plan a ion and o he in aluable assis ance. We a e g a e ul o
Nikolay Simo o his expe ise in axonomic iden i ica ion and
assis ance wi h manusc ip p epa a ion and o Snejana G oze a
o he aluable commen s on he manusc ip .
Re e ences
Ahmad S. N. & Kama udin N. 2011. Phe omone apping in
con olling key insec pes s: p og ess and p ospec s. Oil
Palm Bulle in 62: 12-24.
Ali A. Y. 2021. Con ibu ion o Pen a omoidea (Hemip e a:
He e op e a: Pen a omomo pha) auna o Ta ous wi h a
new eco d o Sy ia. Jou nal o Insec Biodi e si y and
Sys ema ics 7 (4): 365-374.
And ee R. 2002-2018. Ag icul u al En omology o All. Com-
pu e e e ence book (a CD) Ag icul u al Uni e si y
Plo di . (In Bulga ian).
Allison J. D., Bhanda i B. D., McKenney J. L. & Milla J. G. 2014.
Design ac o s ha in luence he pe o mance o ligh
in e cep aps o he cap u e o longho ned bee les (Co-
leop e a: Ce ambycidae) om he sub amilies Lamiinae
and Ce ambycinae. PLoS One 9 (3): e93203.
A akan E., Pehli an S. & Sa a S. 2016. Response o some
bene icial insec species o colou ed s icky aps in ci us.
Tu kish Jou nal o En omology 40 (4): 385-396. (In Tu k-
ish wi h English summa y).
A anaso N., Mi ko a E., Diko a B., Bae a G., T enche G.,
Ma ino a M., Angelo a D., Dzhu manski A., Lambe
H. & Pa lo a D. 2008. A guide o In eg a ed Pes Man-
agemen oil-bea ing ose, min , la ende and co iande .
So ia: Na ional Plan P o ec ion Se ice h ps://www.mzh.
go e nmen .bg/ (In Bulga ian).
Aukema B., B ue J. & Visken G. 2007. Nieuwe en zeldzame
Belgische wan sen 11 (Hemip e a: He e op e a). Bulle in
Socié é oyale belge d’En omologie Koninklijke Belgische
Ve eniging oo En omologie 143: 83-91.
Bale ski N., Simo a S. & D agano a S. 2008. Biodi e si y
o bene icial o ganisms (en omopa ogens, p eda o s and
pa asi oids) in he biocoenoses o oil-bea ing ose (Rosa
damascena Mill.) in Bulga ia. Ag icul u al Academy, Plan
Science 45: 115-122.
Bolu H. 2020. Sou heas e n Ana olia Region Insec Fauna II
(O de Hemip e a I: Subo de He e op e a III: Pen a o-
moidea) o Tu key. Jou nal o he He e op e a o Tu key
2 (2): 81-101.
Bu esh I. & Laza o A. 1956. Pes insec s o ag icul u e and
o es y in Bulga ia. So ia: Bulga ian Academy o Science.
291 pp. (In Bulga ian).
Caissa d J. C., Ad a I., Cona C., Pa ami a S. N. & Baudino
S. 2023. Do we eally know he scen o oses? Bo any
Le e s 170 (1): 77-88.
Chalo a V. I., Manolo I. G. & Manolo a V. S. 2017. Challenges
o comme cial o ganic p oduc ion o oil-bea ing ose in
Bulga ia. Biological Ag icul u e & Ho icul u e 33 (3):
183-194. h ps://doi.o g/10.1080/01448765.2017.1315613
De Cáce es M. D. & Legend e P. 2009. Associa ions be ween
species and g oups o si es: indices and s a is ical in e ence.
Ecology 90 (12): 3566-3574. h ps://doi.o g/ 10.1890/08-
1823.1
De ise ic M., D obnjako ić T. & G ao a D. 2024. The p eda o s
a acking so scales (Hemip e a: Coccomo pha: Coccidae)
in Se bia. Eu opean Jou nal o En omology 121: 252-
259. h ps://doi.o g/10.14411/eje.2024.026.
DiMeglio A. S., Kuha T. P. & Webe D. C. 2017. Colou p e e -
ence o ha lequin bug (He e op e a: Pen a omidae). Jou nal
o economic en omology 110 (5): 2275-2277. h ps://doi.
o g/10.1093/jee/ ox179
T ue Bugs (Hemip e a: He e op e a) Collec ed in an Oil-Bea ing Rose Ag ocenosis in he Kazanlak...
239
Du êne M. & Legend e P. 1997. Species assemblages and
indica o species: he need o a lexible asymme ical ap-
p oach. Ecological monog aphs 67 (3): 345-366.
Fen M. & Okya Z. 2022. He e op e a (Hemip e a) species is-
i ing Ve bascum densi lo um Be ol. in Edi ne (Tü kiye).
Jou nal o he He e op e a o Tu key 4 (2): 169-183. h ps://
doi.o g/10.5281/zenodo.7358960
G ozea I., Molna L., Ca abe A., S e R., Bu na iu M., Dami-
ano S., G ozea A. & Vi eiu A. M. 2023. Upda ed hos
plan ange o phy ophagous insec Co eus ma gina us
(Hemip e a: Co eidae) in Romania. Resea ch Jou nal o
Ag icul u al Science 55 (1): 91-97. (h ps://www. jas. o/
pape _de ail/3833)
Guéo guie B. & Ljubomi o T. 2009. Coleop e a and Hyme-
nop e a (Insec a) om Bulga ian Sec ion o Maleshe ska
Planina Moun ain: S udy o an Un il Recen ly Unknown
Biodi e si y. Ac a Zoologica bulga ica 61 (3): 235-276.
Hamme O. & Ha pe D. A. 2001. Pas : paleon ological s a is ics
so wa e package o educa on and da a analysis. Palae-
on ologia elec onica 4 (1): 1. h p://palaeo-elec onica.
o g/2001_1/pas /issue1_01.h m
Ha izano A., Ha izano a V. & S oe a A. 2010. Biological plan
p o ec ion. So ia: Dionis. 196 p. (In Bulga ian).
Hemala V. & Kmen P. 2017. Fi s eco d o Halyomo pha halys
and mass occu ence o Neza a i idula in Slo akia.
Plan P o ec ion Science 53: 247-253. h ps://doi.o g/
10.17221/166/2016-PPS
He odo us [ca 430 BC] The His o ies, VIII, 138. In: Godley A.D.
(Ed. wi h an English ansla ion):He odo us. The His o ies.
Camb idge: Ha a d Uni e si y P ess, 1920
Hokkanen H. 1986. Polymo phism, pa asi es, and he na i e a ea
o Neza a i idula (Hemip e a, Pen a omidae). Annales
En omologici Fennici 52: 28-31.
Holopainen J. K., Raiskio S. & Wul A. 2001. Blue s icky aps
a e mo e e icien o he moni o ing o Lygus ugulip-
ennis (He e op e a: Mi idae) han yellow s icky aps.
Ag icul u al and Food Science 10 (3): 277-284. h ps://
doi.o g/10.23986/a sci.5698
H is ozo a M. & Ha izano a A. 2022. Labo a o y s udy o he
li ecycle pa ame e s o he b own ma mo a ed s ink bug
(Halyomo pha halys S ål.) – an alien pes es ablished in
Bulga ia. Ag icul u al Sciences 14 (32): 23-30.
H is ozo a M. V. & Ha izano a V. B. 2024 Pa asi oids o he
in asi e Halyomo pha halys (he e op e a: pen a omidae)
in Bulga ia and he a e o pa asi ism a ield condi ions.
Ag icul u al Uni e si y – Plo di , Ag icul u al Sciences 16
(43): 70-76. h ps://doi.o g/10.22620/ag isci.2024.43.007
Ilie a T. & Ka o a A. 2023. Implemen a ion o me hods
o moni o ing and con ol o enemies in ag icul u e. New
knowledge Jou nal o science 12 (2): 58-66. (In Bulga ian,
English Summa y).
Im ei Z., Lohonyai Z., Csóka G., Musko i s J., Szanyi S., Vé ek
G., Fail J., Tó h M. & Domingue M. J. 2020a. Imp o -
ing apping me hods o bup es id bee les o enhance
moni o ing o na i e and in asi e species. Fo es y: An
In e na ional Jou nal o Fo es Resea ch 93 (2): 254-264.
h ps://doi.o g/10.1093/ o es y/cpz071
Im ei Z., Lohonyai Z., Musko i s J., Ma ula E., Vu s J., Fail J.,
Gould P. J. L, Bi ke M. A., Tó h M. & Domingue M. J.
2020b. De eloping a non‐s icky ap design o moni o -
ing jewel bee les. Jou nal o Applied En omology 144 (3):
224-231. h ps://doi.o g/10.1111/jen.12727
Jones W. A. 1988. Wo ld e iew o he pa asi oids o he sou h-
e n g een s ink bug, Neza a i idula L. (He e op e a:
Pen a omidae). Annals o he En omological Socie y
o Ame ica 81 (2): 262-273. h ps://doi.o g/10.1093/
aesa/81.2.262
Joseph S. V. 2014. E ec o ap colou on cap u es o bag ada
bug, Bag ada hila is (Hemip e a: Pen a omidae). Jou nal
o En omological Science 49 (3): 318-321.
Josi o M. 1981. Fauna Bulga ica 12. He e op e a, Pen a omo-
idea. So ia: Bulga ian Academy o Sciences. 205 p. (In
Bulga ian).
Josi o M. 1986. Ve zeichnis de on de Balcanhalbinsel bekan-
n en He e op e ena en (Insec a, He e op e a). Faunis ische
Abhandlungen S aa liches Museum ü Tie kunde in
D esden 14 (6): 61-93.
Josi o M. 1999. He e op e ous insec s in he Sandanski-Pe ich
Ke le, Sou hwes e n Bulga ia. His o ia na u alis bulga ica
10: 35-66.
Kalushko P. & Dimo a V. 1997. Colou opism o sca abaeid
bee les. Ac a En omologica Bulga ica 3-4: 30-32. (In
Bulga ian, English summa y).
Kenzhegaliye A. M., Esenbeko a P. A., Zhaksybaye M. B.
2021. Ma e ials o he auna o Lygaeidae (Hemip e a,
He e op e a) o Sou h-Eas e n Kazakhs an. Repo s o he
Na ional Academy o sciences o he Republic o Kazakh-
s an 2 (336): 26-34. h ps://doi.o g/10.32014/2021.2518-
1483.26
Ke zhne I. M. & Yache sky T. L. 1964. O de He e op e a
(Hemip e a). Key o he insec s o he Eu opean pa o
he USSR. Vol. 1. Moscow-Lening ad: Publishing house
“Science”, pp. 655-845. (In Russian).
Kim J., Cassis G. & Jung S. 2023. Phylogene ic analysis o he
p eda o y plan bug sub amily De aeoco inae (Hemip e a:
He e op e a: Mi idae) based on molecula and mo phologi-
cal da a. Zoological Jou nal o he Linnean Socie y 197
(1): 246-266. h ps://doi.o g/10.1093/zoolinnean/zlac061
Kmen P. & Baňař P. 2012. T ue bugs (Hemip e a: He e op e a) o
he Bílé Ka pa y P o ec ed Landscape A ea and Biosphe e
Rese e (Czech Republic). Ac a Musei Mo a iae, Scien iae
Biologicae 96 (2): 323-628.
Kolak G. 2015. Nowe s anowisko T i omegas sexmacula us
(Rambu , 1839) (Hemip e a: He e op e a: Cydnidae) na
Gó nym Śląsku. Ac a en omologica silesiana 23: 1-5.
Ko ache a N., Rusano K. & A anasso I. 2010. Indus ial
cul i a ion o oil bea ing ose and ose oil p oduc ion in
Bulga ia du ing 21s cen u y, di ec ions and challenges.
Bio echnology & Bio echnological Equipmen 24 (2):
1793-1798. h ps://doi.o g/10.2478/V10133-010-0032-4
K i icos D. J., Kean J. M., Phillips C. B., Senay S. D., Acos a H.
& Haye T. 2017. The po en ial global dis ibu ion o he
b own ma mo a ed s ink bug, Halyomo pha halys, a c i ical
h ea o plan biosecu i y. Jou nal o Pes Science 90 (4):
1025-1034. h ps://doi.o g/10.1007/s10340-017-0869-5
Langou o M. 2001. Faunis ic, ecological and zoogeog aphic
s udies o he amily Pho idae (Dip e a, B achyce a) om
Vi osha Moun ain. Unpublished PhD hesis. Ins i u e o
Zoology, So ia, 1-171. (In Bulga ian).
Langou o M. & Simo N. 2006. S udy on he biodi e si y o
model g oups animals in communi ies o Que cus cocci e a
L. His o ia na u alis bulga ica 17: 166. (In Bulga ian).
Lape a-Gjono a A. & Ljubomi o T. 2020. Fi s Reco ds o Two
S umigenys An Species (Hymenop e a: Fo micidae) om
