CHALCIDOID PARASITOIDS (HYMENOPTERA: CHALCIDOIDEA) ASSOCIATED WITH SIBINIA SUBELLIPTICA (DESBROCHERS, 1873) (COLEOPTERA: CURCULIONIDAE) IN BULGARIA
Abstract
The weevil Sibinia subelliptica (Desbrochers, 1873) and a rich complex of associated chalcidoid parasitoids were reared from inflorescences of Dianthus giganteus d’Urv. (Caryophyllaceae) in Bulgaria. The following taxa were identified: Aprostocetus venustus (Gahan) and Baryscapus sp. near garganus (Domenichini, 1958) (Eulophidae); Eupelmus barai Fusu and E. microzonus Förster (Eupelmidae); Aximopsis augasmae (Zerova), A. collina (Zerova), Eurytoma coleophorae Zerova and E. coleopterae Zerova (Eurytomidae); Catolaccus crassiceps (Masi) and Pteromalus ochrocerus (Thomson) (Pteromalidae); and Exopristus trigonomerus (Masi) (Torymidae). Two of these, E. coleophorae and E. coleopterae, are new records for Bulgaria. All parasitoid-host relationships are documented here for the first time. New plant associations with D. giganteus are recorded here for all reared parasitoids except E. barai and E. microzonus. The new trophic association of S. subelliptica with D. giganteus is established here.
Keywords: Dianthus giganteus; parasitoid complex; new records; new host; new associations.
Resumen
Parasitoides calcidoides (Hymenoptera: Chalcidoidea) asociados con Sibinia subelliptica (Desbrochers, 1873) (Coleoptera: Curculionidae) en Bulgaria
El gorgojo Sibinia subelliptica (Desbrochers, 1873) y un rico complejo de parasitoides calcidoides asociados se criaron a partir de inflorescencias de Dianthus giganteus d’Urv. (Caryophyllaceae) en Bulgaria. Se identificaron los siguientes taxones: Aprostocetus venustus (Gahan) y Baryscapus sp. cercana a garganus (Domenichini, 1958) (Eulophidae); Eupelmus barai Fusu y E. microzonus Förster (Eupelmidae); Aximopsis augasmae (Zerova), A. collina (Zerova), Eurytoma coleophorae Zerova y E. coleopterae Zerova (Eurytomidae); Catolaccus crassiceps (Masi) y Pteromalus ochrocerus (Thomson) (Pteromalidae); y Exopristus trigonomerus (Masi) (Torymidae). Dos de éstos, E. coleophorae y E. coleopterae, son registrados como nuevos para Bulgaria. Todas las mencionadas relaciones parasitoide-hospedador se documentan por primera vez, así como se registra por primera vez la asociación de la planta D. giganteus con todos los parasitoides obtenidos, excepto en los casos de E. barai y E. microzonus. Se establece la nueva asociación trófica de S. subelliptica con D. giganteus.
Palabras clave: Dianthus giganteus; complejo parasitoide; nuevos registros; nuevo hospedador; nuevas asociaciones.
Introduction[Up]
The genus Sibinia Germar, 1817 (Coleoptera: Curculionidae: Curculioninae) includes three subgenera: Dichotychius Bedel, 1885, Microtychius Casey, 1910 and Sibinia s. str. (Skuhrovec et al., 2015). The Palaearctic S. (Sibinia) species develop in plant representatives of different genera belonging to family Caryophyllaceae [Arenaria L., Cerastium L., Dianthus L., Eremogone Fenzl, Gypsophila L., Lychnis L., Melandrium Röhl., Minuartia L., Petrorhagia (Ser.) Link, Psammophiliella Ikonn., Saponaria L., Silene L., Spergula L., Spergularia (Pers.) J. Presl & C. Presl] (Szénási, 2013; Yunakov et al., 2018). Species in subgenus Dichotychius live on Plumbaginaceae (Skuhrovec et al., 2015) and those in Microtychius have hosts belonging to different genera of family Fabaceae (Clark, 1978). Species of Sibinia are trophically associated with narrow host ranges. Some of them are monophagous whereas other are restricted to two or more plant species of a single genus. The larvae of most species feed mainly on the seeds of their hosts (Clark, 1978). Sibinia species are found in different types of habitats: salty lands, sands, xerothermic grasslands and meadows, steppes, dry and stony slopes, forest edges, agricultural habitats and salt marshes (Yunakov et al., 2018). Some species of the genus are considered as bioindicators of natural sandy habitats (Košťálová & Szénási, 2015).
Sibinia subelliptica (Desbrochers, 1873) is a Palaearctic curculionid species known from Europe, Anatolia, Siberia, East Asia (Russian Far East, N Korea, Japan, NE China) and N Africa (Algeria) (Balalaikins, 2013). It is a thermophilous oligophagous beetle that develops on plant species from the genus Dianthus, mostly in xerothermic habitats (Angelov, 1980). Its known hosts are: D. acicularis Fischer ex Ledebour (Dedyukhin & Martynenko, 2020), D. andrzejowskianus Kulcz. (Yunakov et al., 2018), D. armeria L. (Tempère & Péricart, 1989), D. balbisii Ser. (Clark, 1978), D. borbasii Vandas (Yunakov et al., 2018), D. carthusianorum L. (Cmoluch et al., 1975; Clark, 1978), D. ferrugineus Miller (Teodor, 2011), D. pratensis Bieb. (Dedyukhin, 2014), D. sylvestris Wulfen (Teodor, 2011), D. ?versicolor Fisch. ex Link (Dedyukhin, 2012). The females lay their eggs at the base of the flowers (Angelov, 1980). The complete development of the species from egg to imago takes place in the flowers of the host plant without the larva to enter the soil to pupate (Alziar, 1976), although pupation in the soil has been reported in the literature (Angelov, 1980; Tempère & Péricart, 1989). The species is common in Bulgaria from May to July from 200 to 1000 m a. s. l. (Angelov, 1980).
The genus Dianthus L. (Caryophyllaceae) is represented by annual, biennial and perennial herbaceous plants (Kirillov et al., 2016). It is widespread mainly in Europe, the Mediterranean region and in Asia, and a few species are known from Africa and America (Chandra et al., 2016). Dianthus giganteus d’Urv. is a perennial plant that grows on stony and grassy places in the lowlands and mountains. It occurs throughout Bulgaria up to 2100 m a. s. l. It is also distributed in Albania, former Yugoslavia, Greece, Italy, Romania, Turkey and SW Asia (Stojanov, 1966).
There is no information in the literature about parasitoids of the curculionid beetle S. subelliptica. The aim of this study is to provide the first data on a parasitoid complex probably associated with this weevil.
Material and methods[Up]
Over 2100 dry inflorescences of D. giganteus were collected on 1.VIII.2015 and on 15.VII. 2016 in Arbanasi Village near Veliko Tarnovo (43°05’50.1” N 25°40’38.3” E, 417 m). The collected material was stored in laboratory conditions in plastic bottles darkened with an aluminium foil and with an additional transparent tube at temperature 23-26° C. The tops of the bottles were cut out and covered with white cheesecloth. The material was stored for at least one year until all emergences had ceased. Emerged parasitoids were aspirated with a pooter, fixed in ethanol and later examined under a stereo microscope. During the dissection of at least 300 inflorescences, we found 500 imagos of S. subelliptica at the base of the flowers (Fig. 1). Only 12 specimens were observed outside the inflorescences.
Fig. 1.— Flores disecadas de Dianthus giganteus infectadas por Sibinia subelliptica. Escala = 1 mm.
The weevil and its parasitoids were identified following Graham (1969, 1987, 1991), Angelov (1980), Grissell (1995), Zerova & Seryogina (1999), Zerova (2010), Gibson & Fusu (2016), Fusu (2017) and Fursov et al. (2019).
The specimens are preserved in the authors’ collection (University of Plovdiv and Institute of Biodiversity and Ecosystems Research, Bulgarian Academy of Sciences).
Colour photographs were taken with a Canon 5D Mark III digital camera.
Results[Up]
During the study we reared 512 specimens of S. subelliptica, along with 905 specimens of hymenopteran parasitoids belonging to 11 species (Table 1) of five families of Chalcidoidea (Eulophidae, Eupelmidae, Eurytomidae, Pteromalidae and Torymidae), from inflorescences of D. giganteus (Fig. 2).
Tabla 1.– Parasitoides obtenidos a partir de inflorescencias de Dianthus giganteus d’Urv. de Arbanasi Village.
| Family | Parasitoid species | Number of individuals | |||
|---|---|---|---|---|---|
| 01.VIII.2015 | 15.VII.2016 | ||||
| ♀♀ | ♂♂ | ♀♀ | ♂♂ | ||
| Eulophidae | Aprostocetus venustus (Gahan, 1914) | 11 | 4 | 51 | 25 |
| Baryscapus sp. near garganus | 7 | 1 | – | – | |
| Eupelmidae | Eupelmus barai Fusu, 2017[*] | – | – | 6 | – |
| Eupelmus microzonus Förster, 1860[**] | 9 | – | 6 | – | |
| Eurytomidae | Aximopsis augasmae (Zerova, 1977) | – | – | 2 | 2 |
| Aximopsis collina (Zerova, 1984) | 63 | 30 | 39 | 42 | |
| Eurytoma coleophorae Zerova, 1977 | – | – | 3 | – | |
| Eurytoma coleopterae Zerova, 1978 | 45 | 7 | 52 | 25 | |
| Pteromalidae | Catolaccus crassiceps (Masi, 1911) | – | – | 2 | – |
| Pteromalus ochrocerus (Thomson, 1878) | 51 | 27 | 36 | 14 | |
| Torymidae | Exopristus trigonomerus (Masi, 1916) | 135 | 54 | 87 | 69 |
Fig. 2.— Inflorescencia de Dianthus giganteus con orificios de las emergencias de los parasitoides calcidoideos asociados con Sibinia subelliptica (vista desde la parte posterior). Escala = 1 cm.
Since only 1/7 of the inflorescences were dissected, the number of beetles in them can be expected to exceed 3500 individuals. In addition to these, we obtained hundreds of thrips (Thysanoptera) and four specimens of unidentified species of Chrysopidae (Neuroptera). Whilst S. subelliptica was not proven to be the host species of all these parasitoids, we believe that it was very probably the host (primary or secondary) of at least the most frequently reared Hymenoptera. Two of the parasitoid species, Eurytoma coleophorae and E. coleopterae, are recorded for the first time from Bulgaria. All parasitoids are suggested to be associated with S. subelliptica for the first time and, with the exception of E. barai and E. microzonus, all parasitoid species are newly associated with D. giganteus. Also, D. giganteus is recorded here as a new host plant of S. subelliptica.
Although we cannot conclusively confirm that all reared parasitoids are primary parasitoids of S. subelliptica, their large number (with the exception of C. crassiceps and E. coleophorae) suggests a more common than accidental association with this host.
Discussion[Up]
The review of the literature shows that there are no data about parasitoids of S. subelliptica. However, parasitoids belonging to four families of Chalcidoidea (Eulophidae, Eupelmidae, Eurytomidae and Pteromalidae) and one family of Ichneumonoidea (Braconidae) have been recorded on eight other Sibinia spp. (Table 2).
Tabla 2.– Lista de los parasitoides himenópteros conocidos y de sus hospedadores en Sibinia obtenidos a partir de: 1 – Rogers et al. (1975), 2 – Clark (1978), 3 – Gibson (2013), 4 – Beyarslan & Şahin (2019), 5 – Fursov et al. (2019).
| Sibinia spp. | Parasitoids |
|---|---|
| S. femoralis Germar | Bracon intercessor Nees (Braconidae)4 Eurytoma coleopterae Zerova (Eurytomidae)5 |
| S. inermis (Casey) | Eutrichosoma mirabile Ashmead (Pteromalidae)2 |
| S. pallida (Schaeffer) | Lyrcus sp. [= Zatropis sp.] (Pteromalidae)2 |
| S. seminicola Clark | Horismenus sp. (Eulophidae)2 Eupelmus sp. (Eupelmidae)2 Pteromalinae (Pteromalidae)2 |
| S. setosa (LeConte) [= S. sulcatula (Casey)] |
Eurydinoteloides perdubia (Girault) [= Zatropis perdubius (Girault)] (Pteromalidae)1 Lyrcus capitis (Burks) [= Zatropis capitis Burks] (Pteromalidae)1 Eutrichosoma mirabile Ashmead (Pteromalidae)2 Trimeromicrus maculatus Gahan (Pteromalidae)3 |
| S. simplex (Casey) | Eutrichosoma mirabile Ashmead (Pteromalidae)2 Tetrastichus sp. (Eulophidae)2 |
| S. variegata (Casey) | Urosigalphus breviovipositorus Gibson (Braconidae)2 |
| S. viscariae (Linnaeus) | Bracon variator Nees (Braconidae)4 |
Aprostocetus venustus is a parasitoid of species of Bruchophagus Ashmead (Hymenoptera: Eurytomidae) in seeds of Fabaceae (Graham, 1987; Boyadzhiev, 2006; Ribes Escolà & Askew, 2009) as well as of species of Contarinia Rondani (Diptera: Cecidomyiidae) in Sorghum (Poaceae) [as Tetrastichus venustus Gahan] (Wiseman et al., 1978) and Mango (Anacardiaceae) (Yefremova et al., 2007). It has been also reared from Dasineura oleae (Angelini) (Diptera: Cecidomyiidae) on Olea europaea L. (Oleaceae) (Doganlar, 1992). Recently, A. venustus was reared from flower heads of Xeranthemum annuum L. (Asteraceae) along with Larinus sibiricus Gyllenhal (Coleoptera: Curculionidae) and a rich complex of hymenopteran parasitoids associated with this beetle (Antov et al., 2020). We found no information in the literature for previous rearings of this eulophid species from D. giganteus.
Baryscapus Förster, 1856 is a large and biologically diverse genus in the subfamily Tetrastichinae (Eulophidae) (Graham, 1991) comprising 128 species with a cosmopolitan distribution (Noyes, 2019). Species of the genus develop mostly as gregarious or more rarely as solitary endoparasitoids of larvae or pupae of a wide variety of insect hosts belonging to Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera and Neuroptera. Some species of Baryscapus are secondary parasitoids of species of the families Braconidae and Ichneumonidae and of the superfamilies Chalcidoidea and Cynipoidea (Graham, 1991). We assume that Baryscapus sp. near garganus is an undescribed species and differs from females of B. garganus mainly in structure of antennae and thorax as well as the longer abdomen. Its taxonomic characterization will be a subject of further studies.
Eupelmus barai is a polyphagous parasitoid whose host range include various insects belonging to Coleoptera (Curculionidae), Diptera (Cecidomyiidae and Tephritidae), Hymenoptera (Cynipidae, Diprionidae and Eurytomidae) and Lepidoptera (Coleophoridae, Millieridae, Tortricidae and Yponomeutidae). In the family Curculionidae, only Scolytus rugulosus (Müller) has been recorded as its host from Moldova (Fusu, 2017).
Eupelmus microzonus is a polyphagous parasitoid attacking the larvae and pupae of a wide range of insect hosts that are usually concealed in galls, flower heads, seeds, grass stems or cocoons and belong to Coleoptera, Diptera, Hymenoptera and Lepidoptera (Bouček, 1977; Antov & Stojanova, 2020). The following curculionid beetles are known as its hosts: Anthonomus pomorum (Linnaeus) (Gibson & Fusu, 2016), Ceutorhynchus obstrictus (Marsham) (Haye et al., 2018), Curculio glandium Marsham (Kostjukov et al., 2018), Microlarinus lareynii (Jacquelin du Val) (Soydanbay-Tunçyürek, 1976), Pachytychius hordei (Brullé) (Gözüaçık & Şimşek, 2015), Tychius aureolus Kiesenwetter [= T. femoralis Brisout] and T. flavus Becker (Nikolskaya, 1952). Recently, the species was also associated with L. sibiricus (Antov et al., 2020). It has been recorded as a parasitoid of three weevil species of the family Brentidae: Catapion seniculus (Kirby) [= Apion seniculus Kirby] (Mambetova, 1975, as cited by Noyes, 2019), Hemitrichapion reflexum (Gyllenhal) (Muhtarova et al., 2009) and Oxystoma ochropus (Germar) (Lotfalizadeh & Hashemi, 2015).
Aximopsis augasmae has been recorded as a parasitoid of the larvae of Augasma atraphaxidellum Kuznetzov (Lepidoptera: Coleophoridae) on Atraphaxis spinosa L. (Polygonaceae) and some other moth species on Zygophyllum L. (Zygophyllaceae) (Zerova & Seryogina, 2006). It was also reported as a parasitoid of Etiella zinckenella (Treitschke) (Lepidoptera: Pyralidae) in pods of Sophora alopecuroides L. (Fabaceae) (Lotfalizadeh & Hosseini, 2014). There is no data for its rearing from D. giganteus.
Aximopsis collina has been recorded as a parasitoid in Diplolepis galls on Rosa spp. (Lotfalizadeh et al., 2006; Zerova, 2010; Mete & Mergen, 2017). Recently, it was associated with seeds of three Asphodelus spp. (Delvare et al., 2019). There is no data for its rearing from D. giganteus.
Eurytoma coleophorae has been reared from galls of Coleophora serinipennella Christoph (Lepidoptera: Coleophoridae) on Atriplex sp. (Amaranthaceae) and Ascalenia kabulella Kasy (Lepidoptera: Cosmopterigidae) on Myricaria alopecuroides Schrenk (Tamaricaceae) (Zerova, 2010). There is no data for its rearing from D. giganteus. The species is distributed in SE Europe and Kyrgyzstan (Zerova, 2010). This is the first record from Bulgaria.
Eurytoma coleopterae is a parasitoid attacking the larvae of small beetles whose development takes place in stems, galls and seeds of herbaceous plants (Fursov et al., 2019). The species has been reared from larvae of Lixus salsolae Faust. and Sibinia femoralis Germar (Coleoptera: Curculionidae) in galls on Silene wolgensis (Hornem.) Otth [= Otites wolgensis (Hornem.) Grossh.] (Caryophyllaceae) (Zerova, 1978). Recently, it was obtained from larvae of Metapion sp. (Coleoptera: Curculionidae) developing in seeds of Ruta sp. (Rutaceae) (Fursov et al., 2019). In the family Caryophyllaceae, this species is associated with S. wolgensis, but not with D. giganteus. It is known from Turkey, Turkmenistan and Ukraine (Fursov et al., 2019), but it has not been recorded from Bulgaria so far.
Catolaccus crassiceps is a polyphagous species that develops as a primary or secondary parasitoid on a wide variety of insect hosts belonging to Coleoptera (Curculionidae), Hymenoptera (Braconidae and Cynipidae), Lepidoptera (Coleophoridae, Crambidae, Gelechiidae, Noctuidae, Nolidae and Pieridae) and Neuroptera (Chrysopidae) (Dzhanokmen, 2017). It has been reared from cocoons of Coniatus indicus Marshall (Coleoptera: Curculionidae) on Tamarix dioica Roxb. ex Roth (Tamaricaceae) (Boućek et al., 1978). In the family Caryophyllaceae, this species is associated with Gypsophila struthium Loefl. (Askew et al., 2001), but not with D. giganteus.
Pteromalus ochrocerus is known as a parasitoid on species of Curculionidae (Coleoptera), Cynipidae (Hymenoptera) and Tephritidae (Diptera) (Cobo et al., 2016). Its host among the curculionid beetles is A. pomorum (Thompson, 1958). Plant associations include Asteraceae and Lamiaceae (Askew et al., 2006; Cobo et al., 2016), but not Caryophyllaceae.
Exopristus trigonomerus is a parasitoid of species of Coleoptera and probably Diptera concealed in galls and stems of herbaceous plants. Its known hosts among the curculionid beetles are: Rhinusa bipustulata (Rossi) [= Gymnetron bipustulatum (Rossi)] (Zerova & Seryogina, 1999), Larinus canescens Gyllenhal (Cobo et al., 2014), L. sibiricus (Antov et al., 2020) and P. hordei (Altınayar, 1981). It has been also obtained from larvae of the apple fruit weevil Tatianaerhynchites aequatus (L.) (Coleoptera: Rhynchitidae) in Turkey (Bolu, 2006). Plant associations include Asteraceae, Cistaceae, Fabaceae, Gnetaceae, Papaveraceae, Scrophulariaceae (Noyes, 2019) and Plantaginaceae (Bouček, 1977), but not Caryophyllaceae. In our study, E. trigonomerus is the most numerous parasitoid with 189 specimens reared in 2015 and 156 specimens in 2016.
Acknowledgements[Up]
We are very grateful to Dr. Yulian Marinov (Regional Natural History Museum – Plovdiv) for the identification of D. giganteus and useful comments related to it. We are thankful to Dr. Ognyan Todorov (Regional Natural History Museum – Plovdiv) for the photographing of the material. Sincere thanks to Dr. Nikolay Georgiev (Educational Horizons School – Sofia) for translating certain components of the paper in Spanish.
References[Up]
|
Altınayar, G., 1981. Studies on the insect fauna in cereal fields of Middle Anatolian Region. Bitki Koruma Bülteni, 21(2): 53-88 [in Turkish with English summary]. |
|
|
Alziar, G., 1976. Quelques observations sur la biologie de Sibinia subelliptica Desbr. (Coleoptera, Curculionidae). Riviera Scientifique, 1-2: 2. |
|
|
Angelov, P.A., 1980. Fauna Bulgarica, Volume 10: Coleoptera, Curculionidae Part IV Calandrinae. 2. Aedibus Academia Scientiarum Bulgarica. Sofia. 301 pp. [in Bulgarian]. |
|
|
Antov, M. & Stojanova, A., 2015. Published data and new records to the fauna of Eupelmidae (Insecta: Hymenoptera) in Bulgaria. ZooNotes, 83: 1-11. |
|
|
Antov, M. & Stojanova, A., 2020. Bulgarian Eupelmidae (Hymenoptera: Chalcidoidea): new records, phenology and habitat data. North-Western Journal of Zoology, 16(1): 36-49. |
|
|
Antov, M.I., Boyadzhiev, P.S., Todorov, I.A. & Stojanova, A.M., 2020. The parasitoid complex associated with Larinus sibiricus Gyllenhal, 1835 (Coleoptera: Curculionidae) in Bulgaria. Acta Zoologica Bulgarica, Supplement 15: 123-128. |
|
|
Askew, R.R., Blasco-Zumeta, J. & Pujade-Villar, J., 2001. Chalcidoidea and Mymarommatoidea (Hymenoptera) of a Juniperus thurifera L. forest of Los Monegros region, Zaragoza. Monografías Sociedad Entomológica Aragonesa, 4: 1-76 [in Spanish with English summary]. |
|
|
Askew, R.R., Plantard, O., Gómez, J.F., Nieves, M.H. & Nieves-Aldrey, J.L., 2006. Catalogue of parasitoids and inquilines in galls of Aylacini, Diplolepidini and Pediaspidini (Hym., Cynipidae) in the West Palaearctic. Zootaxa, 1301(1): 1-60. https://doi.org/10.11646/zootaxa.1301.1.1 |
|
|
Balalaikins, M., 2013. Latvian Curculioninae (Coleoptera: Curculionidae). 2. Tribe Tychiini Gistel, 1848. Latvijas Entomologs, 52: 99-118. |
|
|
Beyarslan, A. &Şahin, F., 2019. Ectoparasitoid Braconinae species (Hymenoptera: Braconidae) of plant pest (Coleoptera, Diptera, Lepidoptera and Hymenoptera) determined from Bingöl, Bitlis, Muş and Van provinces of Turkey. Munis Entomology & Zoology, 14(1): 136-147. |
|
|
Bolu, H., 2006. A new host [Tatianaerhynchites aequatus (L.) Coleoptera: Rhynchitidae] record for Bracon pectoralis Wesmael, Baryscapus bruchidii (Erdös), Eupelmus urozonus Dalman and Exopristus trigonomerus (Masi) from Turkey. Journal of the Entomological Research Society, 8(3): 51-62. |
|
|
Bouček, Z., 1977. A faunistic review of the Yugoslavian Chalcidoidea (parasitic Hymenoptera). Acta Entomologica Yugoslavica, Supplementum 13: 1-145. |
|
|
Boućek, Z., Subba Rao, B.R. & Farooqi, S.I., 1978. A preliminary review of Pteromalidae (Hymenoptera) of India and adjacent countries. Oriental Insects, 12(4): 433-468. https://doi.org/10.1080/00305316.1978.10432529 |
|
|
Boyadzhiev, P., 2006. Eulophidae (Hymenoptera: Chalcidoidea) of the Western Rhodopes (Bulgaria). In: P. Beron (ed.). Biodiversity of Bulgaria. 3. Biodiversity of Western Rhodopes (Bulgaria and Greece) I. Pensoft & National Museum of Natural History. Sofia: 561-579. |
|
|
Chandra, S., Rawat, D.S., Chandra, D. & Rastogi, J., 2016. Nativity, phytochemistry, ethnobotany and pharmacology of Dianthus caryophyllus. Research Journal of Medicinal Plant, 10(1): 1-9. https://doi.org/10.3923/rjmp.2016.1.9 |
|
|
Clark, W.E., 1978. The weevil genus Sibinia Germar: natural history, taxonomy, phylogeny, and zoogeography, with revision of the New World species (Coleoptera: Curculionidae). Quaestiones Entomologicae, 14(2): 91-387. |
|
|
Cmoluch, Z., Łętowski, J. & Minda, A., 1975. Weevils (Curculionidae, Coleoptera) of the Pieprzowe Mountains near Sandomierz. Annales Universitatis Mariae Curie-Skłodowska, Sectio C, 30(26): 193-208 [in Polish with Russian & English summaries]. |
|
|
Cobo, A., Ribes, A. & Pujade-Villar, J., 2016. Chalcidoid parasitoids (Hymenoptera: Chalcidoidea) associated with Isocolus melikai Pujade-Villar, 2014 (Hymenoptera: Cynipidae). Boletín de la Sociedad Entomológica Aragonesa, 59: 153-156 [in Spanish with English summary]. |
|
|
Cobo, A., Alonso-Zarazaga, M.A., Ribes, A., Selfa, J. & Pujade-Villar, J., 2014. First record of Larinus (Larinomesius) canescens Gyllenhal, 1835 (Coleoptera: Curculionidae) for the Community of Madrid and contributions of biology and parasitoidism. Butlletí de la Institució Catalana d’Història Natural, 78: 125-127 [in Spanish]. |
|
|
Dedyukhin, S.V., 2012. Beetles weevils (Coleoptera, Curculionoidea) of the Vyatka-Kama interfluve: fauna, distribution, ecology. Udmurt University. Izhevsk. 340 pp. [in Russian with English summary]. |
|
|
Dedyukhin, S.V., 2014. New data on the fauna and ecology of the weevils (Coleoptera, Curculionoidea) Vyatka-Kama region and Middle Preduralye. Bulletin of Udmurt University. Series Biology. Earth Sciences, 1: 73-84 [in Russian with English summary]. |
|
|
Dedyukhin, S.V. & Martynenko, V.B., 2020. Consortial associations of phytophagous beetles (Coleoptera: Chrysomeloidea, Curculionoidea) with plants on the unique Sterlitamak shikhans. Entomological Review, 100(4): 473-496. https://doi.org/10.1134/S0013873820040065 |
|
|
Delvare, G., Ribes Escolà, A., Stojanova, A.M., Benoit, L., Lecomte, J. & Askew, R.R., 2019. Exploring insect biodiversity: the parasitic Hymenoptera, chiefly Chalcidoidea, associated with seeds of asphodels (Xanthorrhoeaceae), with the description of nine new species belonging to Eurytomidae and Torymidae. Zootaxa, 4597(1): 1-90. https://doi.org/10.11646/zootaxa.4597.1.1 |
|
|
Doganlar, M., 1992. Notes on the species of the nominal subgenus Aprostocetus s. str. of Aprostocetus Westwood, 1833, from Europe and Turkey (Hymenoptera, Eulophidae, Tetrastichinae). Entomofauna, 13(31): 513-536. |
|
|
Dzhanokmen, K.A., 2017. Pteromalids (Hymenoptera, Chalcidoidea: Pteromalidae) of the Karatau Ridge and adjacent territories of the Talas Alatau Ridge in Western Tien Shan. Entomological Review, 97(6): 794-817. https://doi.org/10.1134/S0013873817060082 |
|
|
Fursov, V.N., Zerova, M.D. & Kodan, M., 2019. The first record of Eurytoma сoleopterae Zerova, 1978 (Hymenoptera: Eurytomidae) as larval parasitoid of weevils and jewel beetles (Coleoptera: Curculionidae, Buprestidae) in Turkey and Turkmenistan. Ukrainian Entomological Journal, 16(1): 16-20. https://doi.org/10.15421/281903 |
|
|
Fusu, L., 2017. An integrative taxonomic study of European Eupelmus (Macroneura) (Hymenoptera: Chalcidoidea: Eupelmidae), with a molecular and cytogenetic analysis of Eupelmus (Macroneura) vesicularis: several species hiding under one name for 240 years. Zoological Journal of the Linnean Society, 181(3): 519-603. https://doi.org/10.1093/zoolinnean/zlw021 |
|
|
Gibson, G.A.P., 2013. Revision of the species of Jaliscoa Bouček within a review of the identity, relationships and membership of Jaliscoa, Catolaccus Thomson, Eurydinoteloides Girault, Lyrcus Walker and Trimeromicrus Gahan (Hymenoptera: Pteromalidae). Zootaxa, 3612(1): 1-85. https://doi.org/10.11646/zootaxa.3612.1.1 |
|
|
Gibson, G.A.P. & Fusu, L., 2016. Revision of the Palaearctic species of Eupelmus (Eupelmus) Dalman (Hymenoptera: Chalcidoidea: Eupelmidae). Zootaxa, 4081(1): 1-331. https://doi.org/10.11646/zootaxa.4081.1.1 |
|
|
Gözüaçık, C. &Şimşek, Z., 2015. Larval parasitoids of the cereal weevil, Pachytychius hordei (Brullé, 1832) (Coleoptera: Curculionidae) at Mardin Province in Turkey. Egyptian Journal of Biological Pest Control, 25(1): 7-10. |
|
|
Graham, M.W.R. de V., 1969. The Pteromalidae of North-Western Europe (Hymenoptera: Chalcidoidea). Bulletin of the British Museum (Natural History). Entomology, Supplement 16: 1-908. https://doi.org/10.5962/p.258046 |
|
|
Graham, M.W.R. de V., 1987. A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain genera. Bulletin of the British Museum (Natural History), Entomology series, 55(1): 1-392. Available from https://www.biodiversitylibrary.org/page/41067129 [accessed 6 May 2022]. |
|
|
Graham, M.W.R. de V., 1991. A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae): revision of the remaining genera. Memoirs of the American Entomological Institute, 49: 1-322. |
|
|
Grissell, E.E., 1995. Toryminae (Hymenoptera: Chalcidoidea: Torymidae): a redefinition, generic classification, and annotated world catalog of species. Memoirs on Entomology, International, Volume 2, Associated Publishers. Gainesville. 470 pp. |
|
|
Haye, T., Olfert, O., Weiss, R., Mason, P.G., Gibson, G., Gariepy, T.D. & Gillespie, D.R., 2018. Bioclimatic analyses of Trichomalus perfectus and Mesopolobus morys (Hymenoptera: Pteromalidae) distributions, two potential biological control agents of the cabbage seedpod weevil in North America. Biological Control, 124: 30-39. https://doi.org/10.1016/j.biocontrol.2018.06.003 |
|
|
Kirillov, V., Stikhareva, T., Suleimen, Y., Serafimovich, M., Kabanova, S. & Mukanov, B., 2016. Chemical composition of the essential oil from carnation coniferous (Dianthus acicularis Fisch. ex Ledeb) growing wild in Northern Kazakhstan. Natural Product Research, 31(1): 1-7. https://doi.org/10.1080/14786419.2016.1214832 |
|
|
Košťálová, Z. & Szénási, V., 2015. Species of the weevil genus Sibinia Germar, 1817 (Coleoptera: Curculionidae) as bioindicators of natural sandy habitats. Entomofauna Carpathica, 27(2): 12-18. |
|
|
Kostjukov, V.V., Japoshvili, G., Shcherbakov, N.A., Podvarko, A.T., Vasil’ieva, L.A. & Varfolomeeva, O.R., 2018. Parasitoids of Curculio glandium Marsch. (Coleoptera, Curculionidae) in the forests of the North Caucasus. In: A.M. Asaturova (ed.). Proceedings of the International Conference “Biological plant protection is the basis of agroecosystems stabilization. Formation and prospects of the development of organic agriculture in the Russian Federation”, Issue 10, 11-13 September 2018. Granat. Krasnodar: 109-113 [in Russian with English summary]. |
|
|
Lotfalizadeh, H. & Hashemi, S.M., 2015. Parasitoids (Hymenoptera: Chalcidoidea) of the seed eater weevil, Oxystoma ochropus (Germar) (Coleoptera: Apionidae) in northwestern Iran. Acta Entomologica Serbica, 20: 145-150. https://doi.org/10.5281/zenodo.44652 |
|
|
Lotfalizadeh, H. & Hosseini, F., 2014. Chalcidoid parasitoids (Hymenoptera) of Etiella zinckenella (Treitschke) (Lep.: Pyralidae) on Sophora alopecuroides L. in Iran. North-Western Journal of Zoology, 10(2): 251-258. |
|
|
Lotfalizadeh, H., Rasplus, J-Y. & Delvare, G., 2006. Rose gall wasps and their associated fauna (Hymenoptera) in Iran. Redia, 89: 73-85. |
|
|
Mete, Ö. & Mergen, Y.O., 2017. The community components associated with two common rose gall wasps (Hymenoptera: Cynipidae: Diplolepidini) in Turkey. Turkish Journal of Zoology, 41(4): 696-701. https://doi.org/10.3906/zoo-1602-20 |
|
|
Muhtarova, G.M., Ephendieva, S.S. & Talibova, S.E., 2009. The materials to knowledge of bugs fauna of the family Apionidae (Coleoptera) of South Daghestan. South of Russia: ecology, development, 4(2): 143-149 [in Russian with English summary]. |
|
|
Nikolskaya, M.N., 1952. Chalcids of the fauna of the USSR (Chalcidoidea). Keys to the fauna of the USSR, published by the Zoological Institute of the Academy of Sciences of the USSR. Volume 44. Publishing House of the Academy of Sciences of the USSR. Moscow-Leningrad. 574 pp. [in Russian]. |
|
|
Noyes, J.S., 2019. Universal Chalcidoidea Database. World Wide Web electronic publication. Available from http://www.nhm.ac.uk/chalcidoids [accessed 18 Mar. 2021]. |
|
|
Ribes Escolà, A. & Askew, R.R., 2009. Chalcidoidea (Hymenoptera) reared from fruits of Juniperus phoenicea, with descriptions of three new species. Boletín de la Sociedad Entomológica Aragonesa, 45: 109-121. |
|
|
Rogers, C.E., Clark, W.E. & Burke, H.R., 1975. Bionomics of Sibinia sulcatula (Coleoptera: Curculionidae) on mesquite in Texas. The Southwestern Naturalist, 20(3): 303-314. https://doi.org/10.2307/3670034 |
|
|
Skuhrovec, J., Gosik, R., Caldara, R. & Košťál, M., 2015. Immatures of Palaearctic species of the weevil genus Sibinia (Coleoptera, Curculionidae): new descriptions and new bionomic data with suggestions on their potential value in a phylogenetic reconstruction of the genus. Zootaxa, 3955(2): 151-187. https://doi.org/10.11646/zootaxa.3955.2.1 |
|
|
Soydanbay-Tunçyürek, M., 1976. The list of natural enemies of some insect pests in Turkey – Part I. Bitki Koruma Bülteni, 16(1): 32-46 [in Turkish with English summary]. |
|
|
Stojanov, N., 1966. Dianthus L. In: D. Jordanov (ed.). Flora Reipublicae Popularis Bulgaricae. Volume 3. Aedibus Academiae Scientiarum Bulgaricae, Serdicae. Sofia: 409-434 [in Bulgarian]. |
|
|
Szénási, V., 2013. Sibinia beckeri (Desbrochers, 1873) in Hungary (Coleoptera: Curculionidae). Folia Entomologica Hungarica, 74: 111-121. |
|
|
Tempère, G. & Péricart, J., 1989. Faune de France 74. Coléoptères Curculionidae. Quatrième partie. Compléments aux trois volumes d’Adolphe Hoffmann. Corrections, Additions et Répertoire. Fédération Française des Sociétés de Sciences Naturelles. Paris. 534 pp. |
|
|
Teodor, L.A., 2011. Ecological studies regarding the snout-beetles (Coleoptera: Curculionoidea) from the Arieş River basin and the upper course of the Someşul Cald River. In: L. Rákosy & L. Momeu (eds.). Volum comemorativ –Bogdan Stugren. Presa Universitară Clujeană. Cluj-Napoca: 107-148 [in Romanian with English summary]. |
|
|
Thompson, W.R., 1958. A catalogue of the parasites and predators of insect pests. Section 2. Host parasite catalogue, Part 5. Commonwealth Agricultural Bureaux, Commonwealth Institute of Biological Control. Ottawa. 600 pp. |
|
|
Wiseman, B.R., Gross, H.R.Jr. & McMillian, W.W., 1978. Seasonal distribution of the sorghum midge and its hymenopterous parasites, 1975-77. Environmental Entomology, 7(6): 820-822. https://doi.org/10.1093/ee/7.6.820 |
|
|
Yefremova, Z., Ebrahimi, E. & Yegorenkova, E., 2007. The subfamilies Eulophinae, Entedoninae and Tetrastichinae in Iran, with description of new species (Hymenoptera, Eulophidae). Entomofauna, 28(30): 405-440. |
|
|
Yunakov, N., Nazarenko, V., Filimonov, R. & Volovnik, S., 2018. A survey of the weevils of Ukraine (Coleoptera: Curculionoidea). Zootaxa, 4404(1): 1-494. https://doi.org/10.11646/zootaxa.4404.1.1 |
|
|
Zerova, M.D., 1978. Fauna of Ukraine. Volume 11: Hymenoptera Parasitica. Issue 9. Chalcidoidea – Eurytomidae. Naukova Dumka. Kyiv. 465 pp. [in Ukrainian]. |
|
|
Zerova, M.D., 2010. Palaearctic species of the genus Eurytoma (Hymenoptera, Chalcidoidea, Eurytomidae): morphological and biological peculiarities, trophical associations and key to determination. Vestnik Zoologii, Supplement 24: 1-203 [in Russian with English & Ukrainian summaries]. |
|
|
Zerova, M.D. & Seryogina, L.Ya., 1999. Torymid chalcidoid wasps (Hymenoptera, Chalcidoidea, Torymidae) of tribes Podagrionini and Monodontomerini of the Ukrainian fauna. Vestnik Zoologii, Supplement 13: 3-130 [in Russian with English summary]. |
|
|
Zerova, M.D. & Seryogina, L.Ya., 2006. A review of the Palaearctic species of the genus Eurytoma, belonging to the E. robusta species-group (Hymenoptera, Eurytomidae), with description of two new species. Entomological Review, 86(6): 695-705. https://doi.org/10.1134/S001387380606008X |