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____________Mun. Ent. Zool. Vol. 9, No. 2, June 2014_________
783
VERBASCUM GAILLARDOTII BOISS. AND ITS NATURAL
ENEMY COMPLEX IN HATAY PROVINCE, TURKEY
Mikdat Doğanlar* and İlhan Üremiş**
* Honorary Professor, Research Station of Biological Control, Adana, TURKEY. E-
mail:mikdoganlar@yahoo.com
** Mustafa Kemal University, Agriculture Faculty, Plant Protection Department, Hatay,
TURKEY. E-mail:iuremis@mku.edu.tr
[Doğanlar, M. & Üremiş, İ. 2014. Verbascum gaillardotii Boiss. and its natural enemy
complex in Hatay province, Turkey. Munis Entomology & Zoology, 9 (2): 783-791]
ABSTRACT: Verbascum gaillardotii Boiss. and its natural enemy complex in Hatay
province, Turkey have been studied. Diagnostic characters and distribution in Turkey was
given. The natural enemy complex of the flat-margined mullein was given for the first time
from Hatay, Turkey. The natural enemies are: Rhinusa tenuirostris (Stierlin, 1888),
Rhinusa tetra (Fabricius, 1792) (Coleoptera: Curculionidae), Melitaea trivia (Denn. &
Schiff.) (Lepidoptera: Nymphalidae), Cucullia verbasci L., the mullein moth, (Lepidoptera:
Noctuidae), Asphondylia verbasci (Vallot, 1827) (Diptera: Cecidomyiidae). The hymenopter
parasites of plant-feeders are: Entedon sparetus Walker (Eulophidae), Calosota sp.
(Eupelmidae), and 2 spp. of Ichneumonidae (reared from galls of R. tenuirostris), Torymus
verbasci Ruschka, 1921 (Torymidae) (reared from galls of A. verbasci).
KEY WORDS: Verbascum gaillardotii natural enemies, Hatay, Turkey.
The gaillardot’s mullein, Verbascum gaillardotii Boissier, 1959,
(Scrophulariaceae) was first described from Lebanon. The species was recorded
from Turkey by Özçelik & Çetinkaya (2002 in Isparta, and TÜBİVES in Hatay).
Nesom (2012) recorded the species as Verbascum sinuatum L., ssp. gaillardotii
(Boissier) Bornmueller from Syria, Lebanon and Palestine, gave the differences
from Verbascum sinuatum L., ssp. sinuatum.
There is not any record on natural enemy of the gaillardot’s mullein, however
Caldara et al. (2012) stated that Rhinusa spp. in the R. tetra species group feeding
on several species of Verbascum, and gave an identification key for 5 species. Sert
& Çağatay (1999) gave Rhinusa tenuirostris (Stierlin, 1888) as a synonym of
Gymnetron asellus Gravenhorst, 1807. Caldara et al. (2010) carried out a
phylogenetic analysis of the species belonging to the weevil genus Rhinusa
Stephens, 1829 (Coleoptera: Curculionidae: Curculioninae: Mecinini), and
transferred Gymnetron bodenheimeri H. Wagner, 1926 to Rhinusa as a distinct
species, later Caldara (2013) synonymized it under R. tenuirostris.
Gokman & Gumovsky (2013) gave Entedon sparetus Walker as parasitoid of
Rhinusa asellus (Gravenhorst) on mullein, Verbascum sp.
Anonymous (2014) gave diagnostic characters, hosts and biological data of
Melitaea trivia (Denn. & Schiff.) and Cuculia verbasci L.
Larvae of Asphondylia verbasci (Vallot, 1827) change the flower buds of
Verbascum nigrum L. and V. sinuatum (Scrophulariaceae) to galls (Tavares,
1902, 1905; Cogolludo, 1921; Vilarrubia, 1936; Sukuhrava et al., 2006).
Aim of the current work is to find out the diagnostic characters of V.
gaillardotii, and the species in its natural enemy complex in Hatay province,
Turkey, and to give some morphological and biological aspects of the species
which will be helpful in biological control of V. gaillardotii,
____________Mun. Ent. Zool. Vol. 9, No. 2, June 2014_________
784
MATERIALS AND METHOD
The gaillardot’s mullein was collected to obtain the several stages in
development periods in 2012 and 2013, and their photos were taken for
taxonomic works.
In the period from September, 2012 to March, 2013, the galls of R.
tenuirostris on V. gaillardotii were collected from several regions of Hatay
province of Turkey. The regions are: Hatay: Altınözü, Hanyolu and Yanıkpınar
villages, Antakya, Yayladağ, Şenköy. The galls collected were brought to
laboratory, placed in the cages and kept under the conditions of 50-60% relative
humidity and about 15-20 0C. Some of galls were dissected to obtain specimens of
larvae and pupae. To rear adult midges in the bud galls of V. gaillardotii galls
were collected in April and May, 2013, and were brought to laboratory, placed in
the plastic bags under same conditions stated above. The adults came out of the
galls were killed in 97% ethanol and put into vials with ethanol. Taxonomic works
were carried out under microscopes, and photographs of diagnostic characters of
the species were taken by using a stereo-microscope with a digital camera
attached to it.
The identification of the gaillardot’s mullein was done by following the key of
Nesom (2012) by the second author; Rhinusa tenuirostris was identified by Dr.
Roberto Caldara (via Lorenteggio 37, 20146 Milano, Italy. E-mail
roberto.caldara@gmail.com); the other plant feeder species were identified by
Dr. Ivo Tosevski (Institute for Plant Protection and Environment, Banatska 33,
11080 Zemun, SERBIA, E-mail: tosevski_ivo@yahoo.com); the parasitoids were
identified by the first author.
RESULTS AND DISCUSSION
Verbascum gaillardotii Boissier, 1859
Syn. Verbascum sinuatum L., ssp. gaillardotii (Boissier) Bornmueller (Nesom,
2012).
The species very similar to Verbascum sinuatum L., the description of which
was given in detail by Nesom (2012). The plants in Hatay province should be V.
gaillardotii having narrower bracts and bracteoles, slightly smaller corollas, 4(--
5) stamens and flat-margined leaves (in V. sinuatum with broader bracts and
bracteoles, bigger corollas, 5(--4) stamens and wavy leaves) (Fig. 1).
The habitus, inflorescences and seed capsules as seen in Fig. 2.
Distribution: In Turkey: Hatay. In the world: Syria, Lebanon, Palestine.
Syn. Verbascum sinuatum L., ssp. gaillardotii (Boissier) Bornmueller (Nesom,
2012).
Natural enemy complex Verbascum gaillardotii
Rhinusa tenuirostris (Stierlin, 1888)
Syn. Gymnetron bodenheimeri H. Wagner, 1926. (Caldara, 2013)
Sert & Çağatay (1999) gave Rhinusa tenuirostris (Stierlin, 1888) as a synonym
of Gymnetron asellus Gravenhorst, 1807. Caldara et al. (2010) transferred
____________Mun. Ent. Zool. Vol. 9, No. 2, June 2014_________
785
Gymnetron bodenheimeri H. Wagner, 1926 to Rhinusa as a distinct species, later
Caldara (2013) synonymized it under R. tenuirostris.
Diagnosis: body with long rostrum (Figs. 3a,b); rostrum of male in lateral and
dorsal views of the same width from base to apex (Figs. 3a,b and 8-9 of Caldara et
al., 2012), in dorsal view striate-punctate without larger median sulcus; rostrum
of female in lateral and dorsal views parallel-sided (Fig. 3c); antenna clubbed with
4+3 flagellar segments (Fig. 3d); abdomen with 6 sternits (Fig. 3f); uncus of
metatibiae of male pointed at apex, and tibiae with outer margin distinctly curved
outwards near apex (Fig. 3e). Legs with claws fused basally (Fig. 3g); spiculum
ventrale almost Y-shaped (Fig. 4a); aedeagus very long, parallel-sided to near
apex (Fig. 4b); spermatheca and tip of gaster as in figs. 4c,d.
Material studied: Hatay, Turkey: 12 females; 7 males, Altınözü, Hanyolu, 05-23
March, 2012, 15 females, 11 males, Yanıkpınar villages, 27 February- 13 March,
2013; 3 females, 2 males, Center of Antakya, 10- 22 March, 2013. All of the
specimens were reared from galls on V. gaillardotii by M. Doğanlar.
Biology: Up to now there was not any biological data about this species under
both names. By this work its biology in Hatay province, Turkey was studied. The
results as follows:
The adults overwintered under shelters of debris. In early spring adults
started to feed on newly developed stems and branches by inserting very long
rostrum and open deep holes (Fig. 5).
After copulation the matured eggs were laid onto opening of the feeding holes.
Later hatching take place, the first instar larvae (5-12) start to feed on sides of the
hole, and induce gall, than stem thickening (Fig. 6a) which later become a
globular gall in several shapes (Figs. 6b-d).
Many weevil larvae in different stages can be found in the galls. Development
of the larvae has continued in Summer and Autumn. At the end of Autumn the
larvae have pupated and diaposed in Winter. The galls with pupae were collected
and brought to the laboratory in February. At the beginning of March, after a few
days the adults of R. tenuirostris come out from the galls by opening an exit hole,
3-4 mm in diameter (Fig. 7). The emergence of adults from galls has continued up
to the end of April. At the beginning of March the adults can also be seen on the
newly developed Verbascum stems in the field.
Parasitoids: Entedon sparetus Walker (Eulophidae), Calosota sp.
(Eupelmidae), and 2 spp. of Ichneumonidae. Entedon sparetus was also reared
from Rhinusa asellus (Gravenhorst, 1807) (Gokman & Gumovsky, 2013).
Rhinusa tetra (Fabricius, 1792)
Synonyms were given by Caldara et al. (2012).
Diagnosis: Rostrum of male in lateral and dorsal views gradually but distinctly
tapering from base to apex, moderately elongate (length/width at base 3.8–4.4,
average 4.0; rostrum length/pronotum length male 0.84–0.97, average 0.90
(Figs. 8a,b), in dorsal view at least at antennal insertion with large median sulcus
deeper than lateral ones; rostrum of female in lateral and dorsal views either
gradually narrowing from base to apex or parallel-sided, length/width of rostrum
at base 4.3–5.2, average 4.6; rostrum length/pronotum length 0.95–1.07,
(average 1.01) (Fig. 8c); aedeagus shorter, sinuous at middle and then gradually
narrowing to apex (Fig. 8d); female with scrobe distinctly visible in dorsal view
(Fig. 8c).
Biology: Larva and adult were quoted to be collected on various species of
Verbascum. Such as: V. blattaria, V. boerhavii, V. creticum, V. lychnitis, V.
____________Mun. Ent. Zool. Vol. 9, No. 2, June 2014_________
786
nigrum, V. phlomoides, V. phoeniceum, V. pulverulentum, V. speciosum, V.
thapsiforme, V. thapsus Sometimes adult R. tetra were collected also on
Scrophularia (S. auriculata, S. canina (Caldara et al. 2012). Introduced in North
America where it was proposed as a potential candidate for the biological control
of invasive common mullein, Verbascum thapsus L. (O'Brien & Wibmer 1982).
Distribution. Europe, Siberia, North Africa, Middle East, central Asia, northern
India (R. Caldara, pers. comm.).
Material studied: 6 females, 2 males, Hatay, Altınözü, Hanyolu village, 02
June, 2013, feeding on seed capsules of V. gaillardotii, by M. Doğanlar.
Asphondylia verbasci (Vallot, 1827)
Fedotova (2004) gave description of adults and the figures of diagnostic
characters.
Skuhrava et al. (2012) stated that larvae change the flower buds into galls of
Verbascum nigrum L. and V. sinuatum (Scrophulariaceae). In Hatay province the
midges lay its eggs on buds, after hatching the larva enter into the bud and feed
on the generative organs. The bud form the gall (Fig. 9) and larva pupated and
adult emerged from the gall. Infestation by A. verbasci was not so high, about 5-
10%.
Distribution: Hatay, Altınözü, Hanyolu village; Antakya and Harbiye; Yayladağ,
Şenköy.
Parasitoids: Torymus verbasci Ruschka, 1921 was reared on 11 females and 7
males from 70 galls collected from Harbiye. Parasitism level was about 25%, but
in other regions parasitism was not higher than 5%.
Beside of those species the following species of Lepidoptera feeding on leaves
and buds of V. gaillardotii in several parts of Hatay province: Melitaea trivia
(Dennis. & Schiffer.) (Lesser Spotted Fritillary), and Cucullia verbasci, The
mullein moth, (Lepidoptera: Noctuidae).
LITERATURE CITED
Boissier, P. E. 1856. Diagnoses plantarum novarum præsertim orientalium nonnullis Europæis boreali-
Africanisque additis, Ser. 2, 6: 128. 1859 [Jul-Dec, 1856].
Caldara, R. 2013. Curculionidae: Curculioninae. in Löbl, I. & Smetana, A. (editors). Catalogue of
Palaearctic Coleoptera, Volume 8, Curculionoidea II. Brill, Leiden, Boston. pp. 52.
Caldara, R., Casalini, R. & Baviera, C. 2012. Taxonomic and nomenclatural notes on the Rhinusa
tetra (Fabricius) species complex (Coleoptera: Curculionidae). Zootaxa, 3329: 31-40.
Caldara, R., Sassi, D. & Toševski, I. 2010. Phylogeny of the weevil genus Rhinusa Ste phens based
on adult morphological characters and host plant information (Coleoptera: Curc ulionidae). Zootaxa,
2627: 39-56.
Cogolludo, J. 1921. Contribución al conocimiento de las zoocecidias de España. Trab. Mus. Nac. Cienc.
Nat., Ser. Bot., 16: 1-117.
Fedotova, Z. A. 2004. A review of gall-midges (Diptera, Cecidomyiidae) developing on mullein
(Verbascum spp.) with description of new taxa from the middle Volga river basin. Zoologicheskii
Zhurnal, 83 (7): 809-825.
Gokman, V. E. & Gumovsky, A. V. 2013. New data on chromosomes of Chalcidoidea (Hymenoptera).
Entomological Review, 93 (1): 30-34.
____________Mun. Ent. Zool. Vol. 9, No. 2, June 2014_________
787
Nesom, G. L. 2012. Taxon eds.: Rabeler & Freeman, Verbascum (Scrophulariaceae). Flora of North
America, Provisional Publication. Flora of North America Association. September 14, 2007.
fna.huh.harvard.edu/files/Pittosporaceae.pdf. (Accessed March 27, 2014), 17: 9-10.
O'brien, C. W. & Wibmer, G. J. 1982. Annotated checklist of the weevils ( Curculionidae sensu lato) of
North America, Central America, and the West Indies (Coleoptera: Curculionoidea). Memoirs of the
American Entomological Institute, 43: 1-382.
Özçelik, H. & Çetinkaya, M. 2002. Kovada çayı arboretumu (Isparta) florası. Fen Bilimleri Enstitüsü
Dergisi, 6 (3): 125-140.
Sert, O. & Çağatay, N. 1999. İç Anadolu Bölgesi Gymnetron, Hypera, Sibinia ve Tychius (Coleoptera:
Curculionidae) türleri üzerinde taksonomik çalışmalar. Tr. J. of Zoology, 23 (2): 521-544.
Skuhravá, M., Skuhravý, V., Blasco-Zumeta, J. & Pujade-Villar J. 2006. Gall midges ( Diptera:
Cecidomyiidae) of the Iberian Peninsula, 2. Zoogeographical analysis of the gall midge fauna. Boln. Asoc.
esp. Ent., 30 (1-2): 93-159.
Tavares, J. da S. 1902. As zoocecídias Portuguezas. Ann. Sci. Nat. Porto, 7: 17-109.
Tavares, J. da S. 1905. Synopse das zoocecidias Portuguezas. Brotéria, 4: 1-123.
Vilarrúbia, A. 1936. Les zoocecídies de les plantes de Catalunya. Treb. Mus. Cienc. Nat. Barcelona, Ser.
entomol., 11 (10): 1-106.
Figure 1. Verbascum spp. a, b. V. sinuatum L., 1753, a. flowers with 5 anthers, b. first year of
plant with wavy leaves; c, d. V. gaillardotii Boissier, 1859, a. flowers with 4 anthers, b. first
year of plant with flat-margined leaves
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Figure 2. Several stages of Verbascum gaillardotii Boissier, 1859.
Figure 3. Rhinusa tenuirostris (Stierlin, 1888). Female. a, b. body. a. in lateral view, b. in
dorsal view; c. base of rostrum; d. antenna; e. fore leg, except coxa, in lateral view; f.
abdomen, in ventral view; g. claws, in dorsal view.
____________Mun. Ent. Zool. Vol. 9, No. 2, June 2014_________
789
Figure 4. Rhinusa tenuirostris (Stierlin, 1888). a-b. male. a. spiculum ventrale; b. aedeagus
in lateral view, with apical part in dorsal view; c-d. female. c. spermatheca; d. tip of gaster.
Figure 5. Feeding holes of Rhinusa tenuirostris (Stierlin, 1888). a, b. base of stem; c. apical
part of stem.
____________Mun. Ent. Zool. Vol. 9, No. 2, June 2014_________
790
Figure 6. Several stages of gall formation by Rhinusa tenuirostris (Stierlin, 1888). a.
early stage to f. mature galls.
Figure 7. Several galls with exit holes of Rhinusa tenuirostris (Stierlin, 1888).
____________Mun. Ent. Zool. Vol. 9, No. 2, June 2014_________
791
Figure 8. Rhinusa tetra (Fabricius, 1792). a, b. pronotum and head, a. in dorsal view, b. in
lateral view; c. body, in lateral view; d. apical part of aedeagus, in dorsal view.
Figure 9. Several galls developed by larva of Asphondylia verbasci (Vallot, 1827) on
Verbascum gaillardotii Boissier, 1859.
