Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 47 No. 1: 13 Mar. 2024
Type: Review Article
Published: 2024-03-01
DOI: 10.12976/jib/2024.47.1.1
Page range: 1-17
Abstract views: 12
PDF downloaded: 0

Gall-inducing and building habit in Lixinae weevils (Coleoptera: Curculionidae)

Ukrainian Entomological Society, Pryazovskyi National Nature Park
##plugins.generic.jatsParser.article.authorBio##
×

SEMYON V. VOLOVNIK

Science Department

Adaptivity gall-forming larval constructions lixine weevils

Abstract

Among the Lixinae, at least 35 species are gall inducers. Twenty six species have larvae with building activity (lists of both are provided). Fifteen species are root gallers (tribe Cleonini) and 20 species are stem gallers (Lixini). Their gall morphology (shape, colour, size), habitat peculiarities and typical gall development are described. A new classification of galls according to their inhabitants and formation is proposed. The data obtained suggest that galling depends on the thickness of the transformed plant parts. The potential benefits and costs of galling to gall inducers are discussed. Data on the diversity of parasitoids indirectly support a protective role for galls. A summary of information on special larval constructions is presented. Two types of such constructions are—the ground capsules and the trehalas. These are closed chambers whose walls consist of a small soil and plant particles bound with sticky larval secretions. Capsules and trehalas are attached to the plant and serve to complete preimaginal development. Both are functionally similar to galls.

References

  1. Aleeva M. N. 1953а. Dolgonosiki vrediashchie sakharnoi sviokle v Djambulskoi oblasti Kazakhskoi SSR. Trudy Respublikanskoi stantsii zashchity rastenii (Alma-Ata) 1: 14–43. (in Russian)
  2. Aleeva M. N. 1953b. Materialy k biologii dolgonosikov (Coleoptera, Curculionidae), vrediashchikh sakharnoi sviokle v Kazakhstane. Entomologicheskoe Obozrenie 33(3): 103–108 (in Russian)
  3. Alonso-Zarazaga M. A., Barrios H., Borovec R., Bouchard P., Caldara R., Colonnelli E., Gültekin L., Hlaváč P., Korotyaev B., Lyal C. H. C., Machado A., Meregalli M., Pierotti H., Ren L., Sánchez-Ruiz M., Sforzi A., Silfverberg H., Skuhrovec J., Trýzna M., Velázquez de Castro A. J. & Yunakov N. N. 2023. Cooperative Catalogue of Palaearctic Coleoptera Curculionoidea. 2nd Edition. Monografías electrónicas de la Sociedad Entomológica Aragonesa S.E.A., Zaragoza, Spain, 14: 1–780.
  4. Anderson D. M. 1970. Dodder weevils in simultaneous association with parasitic plants and their hosts. Science 168: 132–133. https://doi.org/10.1126/science.168.3927.132
  5. Arnol’di L. V. 1955. Novyj rod dolgonosikov-galloobrazovatelej iz Turkmenii. Trudy Zoologicheskogo instituta AN SSSR 21: 301–305. (in Russian)
  6. Baudyš E. 1955. O hálkotvorných nosatcich. Acta universitatis agriculturae et Silviculturae (Brno) 4: 301–320.
  7. Beutenmuller W. 1893. On the food-habits of North American Rhynchophora. Journal of the New York Entomological Society 1: 36–43.
  8. Boehm R.1908. Notes biologiques sur quelques Coléoptéres de la faune désertique. Bulletin de la Société Entomologique d’Égypte 2: 57–69. https://doi.org/10.5962/bhl.part.5612
  9. Brandhorst C. T. 1977. Plant galls of the vicinity of Seward, Nebraska. Transactions of the Nebraska Academy of Sciences and Affiliated Societies 444: 12–20.
  10. Brun L. A., Sheppard A. W. & Carrara A. 1993. Host range of Pachycerus cordiger (= P. scabrosus) (Col., Curculionidae). Entomophaga 38(4): 537–539. https://doi.org/10.1007/BF02373088
  11. Cawthra E. V. 1958. The ocurence of Cleonus piger Scop. (Col., Сurculionidae) at Aberlady Bay, East Lothian, with some notes upon its larval instars. Entomology Monthly Magazine 94(1132): 204–206.
  12. Davletshina A. G. 1970. K faune pustynnopastbishchnogo rastenia karraka (Cousinia resinosa). Pp. 145–149. In: Vrediteli selskokhosiajstvennykh kultur Uzbekistana i ikh entomofagi. Jakhontov VV [ed.] Fan,Tashkent. (in Russian)
  13. Davletshina A. G, Avanesova G. A & Mansurov A. K. 1979. Entomofauna Yugo-zapadnogo Kyzylkuma. Fan, Tashkent. 128 pp. (in Russian)
  14. Dieckmann L. 1983. Beiträge zur Insektenfauna der DDR: Coleopterahttp//res2.agr.ca/lethbridge/weedbio/agents/acypach_e.htm.Curculionidae (Tanymecinae, Leptopiinae, Cleoninae, Tanyrhynchinae, Cossoninae, Raymondionyminae, Bagoinae, Tanysphyrinae). Beiträge Entomologie 33(2): 257–381.
  15. Eluwa M. C. 1979. Biology of Lixus camerunus Kolbe (Coleoptera: Curculionidae): A major pest of the edible vernonias (Compositae) in Nigeria. Revue de Zoologie Africaine 93(1): 223–240.
  16. Fabre J. H. 1922. The Life of the Weevil. New York, Dodd, Mead & Co. 341 pp. https://doi.org/10.5962/bhl.title.56720
  17. Felt E. P. 1940. Plant galls and gall makers. Comstock Publishing Company, Inc., Ithaka-New York. 364 pp.
  18. Fernandes G. W., Carneiro M. A. A. & Isaias R. M. S. 2012. Gall-Inducing Insects: From Anatomy to Biodiversity, pp. 369–395. In: Insect Bioecology and Nutrition for integrated Pest management. Panizi A.R. and Parra J.R.P. [eds.]. CRC Press, Boca Raton. https://doi.org/10.1201/b11713-19
  19. Fishkis I. S. & Beriozovyi A. S. 1936. Polosatyi khromoderus—vreditel’ sakharnoi sviokly. Oblknizhizdat, Voronezh. 24 pp. (in Russian)
  20. Fletcher T. B. 1920. Annotated list of Indian crop-pest. Pp. 23–314. In: Report of the proceedings of the third entomological meeting held at Pusa on the 3rd to 15th February 1919. Volume 1. Superintendent Government Printing, Calcutta. 417 pp. https://doi.org/10.5962/bhl.title.7897
  21. GBIF: Global Biodiversity Information Facility. 2023. Available from: https://www.gbif.org/ (Accessed 24 Dec, 2023).
  22. Gerling D., Kugler J. & Lupo A. 1976. The galls and gall insects of Tamarix spp. in Israel and the Sinai. Bollettino del Laboratorio di Entomologia Agraria 33: 53–79.
  23. Gültekin L. 2008. Taxonomic review of the stem-inhabiting trehala-constructing Larinus Dejean, 1821 (Coleoptera: Curculionidae): New species, systematics and ecology. Zootaxa 1714: 1–18. https://doi.org/10.11646/zootaxa.1714.1.1
  24. Gültekin L. 2012. New data on Conorhynchus hololeucus (Pallas, 1781) (Coleoptera: Curculionidae). Florida Entomologist 95: 500–502. https://doi.org/10.1653/024.095.0241
  25. Gültekin L. & Korotyaev B. A. 2012. New data on Cosmobaris discolor (Boheman) and Hypolixus pica (F.) (Coleoptera: Curculionidae) associated with Amaranthus (L.) (Amaranthaceae). The Coleopterists Bulletin 66(3): 226–232. https://doi.org/10.1649/072.066.0308
  26. Gültekin N. 2022. First biological data on Cleonini weevil Conorhynchus lacerta Chevrolat, 1873 (Coleoptera: Curculionidae) from Tuzluca – Iğdır territory. Munis Entomology & Zoology 17(1): 530–534.
  27. Gültekin L. & Shahreyary-Nejad S. 2015. A new trehala-constructing Larinus Dejean (Coleoptera: Curculionidae) from Iran. Zoology in the Middle East: 1–6. https://doi.org/10.12976/jib/2016.4.24
  28. Gültekin N., Gürbüz R. & Gözüaçik C. 2021. Biological observations on the Salsola tragus L. weed feeder Conorhynchus kindermanni Faust, 1904 (Coleoptera: Curculionidae) in Ağrı Mountain lowland area. Transaction of American Entomological Society 147: 921– 928. https://doi.org/10.3157/061.147.0407
  29. Harris P. 2005. Cyphocleonus achates (Fåhr.). Root-core feeding weevil. Available from: http//res2.agr.ca/lethbridge/weedbio/agents/acypach_e.htm. (Accessed 20 Jan, 2007).
  30. Harris, P. & Shorthouse J. D. 1996. Effectiveness of gall inducers in weed biological control. The Canadian Entomologist 128:1021–1055. https://doi.org/10.4039/Ent1281021-6
  31. Hoffmann A. 1950. Coléoptères Curculionides. (Faune de France, Vol. 52. P. 1). Lechevalier, Paris, 486 pp.
  32. Hoffmann A. 1954. Coleoptera: Curculionidae. Lechevalier, Paris. 1208 p. (Faune de la France Vol. 59. P. 2). Pp. 487–1207.
  33. Hooper, G. B. & Holdaway, B. E. 2007. Observations on an association between the weevil Scaphosomus trivittatus (Say) and two Astragalus species on selenium-rich soils in Carbon County, Utah. Western North American Naturalist, 67(4): 605–608. https://doi.org/10.3398/1527-0904(2007)67[605:OOAABT]2.0.CO;2
  34. Houard C. 1908. Les Zoocécidies des Plantes d’Europe et du Bassin de la Méditerranée. V. 1. Paris, pp. 387–394. https://doi.org/10.5962/bhl.title.8967
  35. Houard C. 1909. Les Zoocécidies des Plantes d’Europe et du Bassin de la Méditerranée. V. 2. Paris, pp. 779–1064. https://doi.org/10.5962/bhl.title.8967
  36. Huber J. T. & Vayssieres J. F. 1990. Life cycle and host specificity of the heliotrope weevil, Pachycerus cordiger (= madidus auct.) [Col.: Curculionidae]. Entomophaga, 35(3): 475–484. https://doi.org/10.1007/BF02375273
  37. Isaev A. Ju. 1994. Ekologo-faunisticheskij obzor zhukov-dolgonosikov (Coleoptera: Apionidae, Rhynchophoridae, Curculionidae) Ulianovskoi oblasti. Ulianovsk, 77 s. (Priroda Ulianovskoi oblasti, vipusk 4). (in Russian).
  38. Isart J. 1972. Observaciones bioecológicas sobre Cleonus mendicus (Gyllenhal, 1834) (Col. Curculionidae). Graellsia 28: 177–202.
  39. Ivannikov A. I. & Baytenov M. S. 1979. Zhuki-dolgonosiki (Col. Curculionidae) fitofagi sornykh rastenyi semeistva slozhnotsvetnykh Kazakhstana, pp. 53–64. In: Novosti entomologii Kazakhstana. Trudy Kazakhstanskogo otdeleniya Vsesojuznogo entomologicheskogo obshchestva. Dep. v VINITI, № 3415-79 Dep. (in Russian)
  40. Jacobs J. S., Sing Sh. E. & Martin J. M. 2006. Influence of herbivory and competition in invasive weed fitness: observed effects of Cyphocleonus achates (Coleoptera: Curculionidae) and Grass-Seeding Treatments on Spotted Knapweed Perfomance. Environmental Entomolology 35(6): 1590–1596. https://doi.org/10.1603/0046-225X(2006)35[1590:IOHACO]2.0.CO;2
  41. Jeffries M. J. & Lawton J. H. 1984. Enemy free space and ecological structure of ecological communities. Biological Journal of the Linnean Society 23: 269–286. https://doi.org/10.1111/j.1095-8312.1984.tb00145.x
  42. Khnzoryan S. M. 1951. Zametki po faune dolgonosikov Armenii (Coleoptera, Curculionidae). Izvestiya Akademii nauk ArmSSR, biologia i selskokhozyaistvennye nauki 4(9): 827–831. (in Russian)
  43. Kieffer J.-J. 1901. Synopsis des zoocécidies d’Europe. Annales Societes Entomologiques France 70: 238– 578.
  44. Korotyaev B. A., Gültekin L., Volkovitsh M. G., Dorofeyev V. I. & Konstantinov A. S. 2016. Bioindicator beetles and plants in desertified and eroded lands in Turkey. Journal of Insect Biodiversity 4(1): 1–47. https://doi.org/10.12976/jib/2016.4.1
  45. Korotyaev B. A., Konstantinov A. S., Lingafelter S. W., Mandelshtam M. Yu. & Volkovitsh M. G. 2005. Gall-inducing Coleoptera. Vol. 1: 239–271. In: Biology, ecology and evolution of gall-inducing Arthropods. Raman A., Schaefer C. W., Withers T. M. (Eds), Enfield (NH), USA; Plymouth, UK., Science Publishing Inc. 429 pp.
  46. Krivosheina N. P. 1975. K biologii dolgonosikov, (Coleoptera, Curculionidae), razvivaiushchikhsia v peskoukrepitelnikh rasteniiakh Turkmenii. Entomologisheskoe Obozrenie 54(1): 117–126 (in Russian)
  47. Kumachiov I. S. 1979. Dolgonosiki (Coleoptera, Curculionidae) fitofagi sornykh rastenij Taukumov na Yugo-vostoke Kazakhstana. In: Novosti entomologii Kazakhstana. Trudy Kazakhskogo Otdelenija Vsesojuznogo entomologicheskogo obshchestva. Deponirovano v VINITI № 3415-79:48–52 (in Russian)
  48. Mani M. S. 1964. Ecology of plant galls. W. Junk Publishers, The Hague, The Netherlands. https://doi.org/10.1007/978-94-017-6230-4
  49. Mani M. S. 1965. Key to plant galls from India. Bulletin of Botanical Survey of India 7: 89–127.
  50. Marshall G. A. K. 1923. On new species of Curculionidae from India (Coleoptera). The Annales and Magazine of Natural History 9(12): 281–300. https://doi.org/10.1080/00222932308632947
  51. Meng F., Bar-Shmuel N., Shavit R., Behar A. & Segoli M. 2019. Gut bacteria of weevils developing on plant roots under extreme desert conditions. BMC Microbiology 19, 311: 1–13. https://doi.org/10.1186/s12866-019-1690-5
  52. Meregalli M. 2014. Lixinae. In: Handbook of Zoology, Coleoptera, Beetles. Leschen RAB, Beutel RG. [Eds], Volume 3. De Gruyter, Göttingen, 523–529.
  53. Meyer J. 1987. Plant Galls and Gall-Inducers. Gebrüder and Borntraeger. Berlin, Stuttgart, 291 pp.
  54. Miller D. G. & Raman A. 2019. Host–plant relations of gall-inducing insects. Annals of the Entomological Society of America 112(1): 1–19. https://doi.org/10.1093/aesa/say034
  55. Mitiaev I. D. & Iashchenko R.V. 2007. Nasekomye—vrediteli tamariksa v Iugo-Vostochnom Kazakhstane. Thetis, Almaty, 184 pp. (in Russian)
  56. Molliard M. 1904. Virescens and proliferations florales produites par des parasites agissant à distance. Comptes Rendus des Séances de l’Academie des Sciences 139: 930–932.
  57. Mordkovich V. G. 2014. Stepnye ecosystemy. Akadem. izdatelstvo “Geo”, Novosibirsk. 170 pp. (in Russian)
  58. Nasirzadeh A. R., Javid-Tash I. & Riasat M. 2005. Identification of Echinops species and study on some biological characteristics of Larinus vulpes Oliv. as manna producer in Fars Province. Iranian Journal of Medicinal and Aromatic Plants Research 21(3): 335–346. (in Persian; cited after English resume)
  59. Nikulina O. N. 1989. K biologii zhukov-dolgonosikov roda Lixus (Coleoptera, Curculionodae) razvivaiushchikhsia v polukustarnikakh i travianistoj rastitel’nosti Tajikistana. Entomologicheskoe Obozrenie 68(3): 510–521. (in Russian) https://doi.org/10.3382/ps.0680510
  60. O’Brien, C. W. & Marshall G. B. 1987. Unusual larval “sand tube” in the weevil genus Cleonidius in West Texas. The Southwestern Entomologist 12(4): 357–360.
  61. Pierce W. D. 1907. On the biologies of the Rhynchophora of North America, pp. 249–319. In: Annual Report Nebraska State Board of Agriculture for the year 1906–1907. [Mellor W.R prep.] State Journal Company, Lincoln, Nebraska.
  62. Pourtaherzarei R. A., Shishebor P. & Eslamizadeh R. 2011. A study of the biology of amaranth stem-boring weevil, Hypolixus pica (Fabricius) on red root pigweed, Amaranthus retroflexus L. in Dezful. Iranian Journal of Plant Protection Science 41(2): 225–232.
  63. POWO. 2023. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Available from: http://www.plantsoftheworldonline.org. (Accessed 25 Dec, 2023).
  64. Price P. W., Waring G. L. & Fernandes G. W. 1986. Hypotheses on the adaptive nature of galls. Proceedings of the Entomological Society of Washington 88(2): 361–363.
  65. Price P. W., Fernandes G. W. & Waring G. L. 1987. Adaptive nature of insect galls. Environmental Entomology 16:15–24. https://doi.org/10.1093/ee/16.1.15
  66. Quilichini A. & Debussche M. 2000. Seed dispersal and germination patterns in a rare Mediterranean island endemic (Anchusa crispa Viv., Boraginaceae). Acta Oecologica 21(6): 303−313. https://doi.org/10.1016/S1146-609X(00)01089-4
  67. Richardson R. A., Body M., Warmund M. R., Schultz J. C. & Appel H. M. 2017. Morphometric analysis of young petiole galls on the narrow-leaf cottonwood, Populus angustifolia, by the sugarbeet root aphid, Pemphigus betae. Protoplasma 254: 203–216. https://doi.org/10.1007/s00709-015-0937-8
  68. Rohfritsch O. 1992. Patterns in Gall Development, pp. 60–86. In: Biology of Insect-Induced Galls. J. D. Shorthouse & O. Rohfritsch [eds.] New York: Oxford University Press. 296 pp.
  69. Ross H. 1932. Praktikum der Gallenkunde (Cecidologie). Entstehung, Entmawicklung, Bau der durch Tiere, und Pflanze hervorgerufenen Gallbildungen sowie Ökologie der Gallenerreger. Biologische Studienbücher. W. Schönichen, Berlin. Julius Springer, 312 pp.
  70. Scherf H. 1964. Die Entwicklungsstadien der mitteleuropäischen Curculioniden (Morphologie, Bionomie, Ökologie). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, Band 506. Verlag W. Kramer, Frankfurt a. M., 335 pp.
  71. Schmidt H. 1910. Notizen zur Biologie unserer gallenbildenden Rüsselkäfer. Entomologische Rundschau 27: 111.
  72. Seni A. 2018. Insect pests of amaranthus and their management. International Journal of Environment, Agriculture and Biotechnology (IJEAB) 3(3): 1100–1103. https://doi.org/10.22161/ijeab/3.3.50
  73. Şengonca Ç. 1981. Untersuchungen über den Saflorschaedling—Lixus speciosus (Col.: Curculionidae) in der kilikischen Ebene Südostanatoliens. Medizinal Fakultät Landbouwwetenschappen, Rijksuniv, Gent (Belgium) 46 (2): 623–628.
  74. Shaw M. R. & Wahl, D. B. 1989. The biology, egg and larvae of Acaenitus dubitator (Panzer) (Hymenoptera, Ichneumonidae: Acaenitinae). Systematic Entomology 14: 117–125. https://doi.org/10.1111/j.1365-3113.1989.tb00269.x
  75. Shelef O., Helman Y, Friedman A.-L.-L., Behar A. & Rachmilevitch S. 2013. Tri-Party Underground Symbiosis between a Weevil, Bacteria and a Desert Plant. PLoS ONE 8(11): e76588. https://doi.org/10.1371/journal.pone.0076588
  76. Skuhrovec J., Volovnik S. & Gosik R. 2017. Description of the immature stages of Larinus vulpes (Coleoptera: Curculionidae: Lixinae) and notes on its biology. Zookeys 679: 107–137. https://doi.org/10.3897/zookeys.679.12560
  77. Skuhrovec J., Volovnik S., Gosik R., Stejskal R. & Trnka F. 2019. Cleonis pigra (Scopoli, 1763) (Coleoptera: Curculionidae: Lixinae): morphological re-description of the immature stages, keys, tribal comparisons and biology. Insects 10, 325: 1–25. https://doi.org/10.3390/insects10100325
  78. Soiunov O. 1991. Kompleksy nasekomykh Severnykh Karakumov. Ylym, Ashkhabad, 455 pp. (in Russian)
  79. Steinger Th. & Müller-Schärer H. 1992. Physiological and growth responses of Centaurea maculosa (Asteraceae) to root herbivory under varying levels of interspecific plant competition and soil nitrogen availability. Oecologia 91: 141–149. https://doi.org/10.1007/BF00317253
  80. Tara J. S., Azam M., Ayri Sh., Feroz M. & Ramamurthy V. V. 2009. Bionomics of Hypolixus truncatulus (F.) (Coleoptera: Curculionidae: Lixinae: Lixini), a major pest of Amaranthus caudatus L. Munis Entomology & Zoology 4(2): 510–518.
  81. Thelen G. S., Vivanco G. M., Newingham B., Good W., Bais H. P., Landres P., Caesar A. & Callaway R. M. 2005. Insect herbivory stimulates allelopathic exudation by an invasive plant ant the supression of natives. Ecology Letters 8: 209–217. https://doi.org/10.1111/j.1461-0248.2004.00713.x
  82. Tokgaev T. & Nepesova M. 1964. Materialy k faune i ekologii dolgonosikov (Coleoptera, Curculionidae) jugo-vostochnoj Turkmenii. Izvestija AN TurkmSSR. Seria biologicheskikh nauk 1: 53–59. (in Russian)
  83. Tooker J. F. & Giron D. 2020. The evolution of endophagy in herbivorous insects. Frontiers in Plant Science, hal-03101309: 1–20. https://doi.org/10.3389/fpls.2020.581816
  84. Trnka F., Stejskal R. & Skuhrovec J. 2015. Biology and morphology of immature stages of Adosomus roridus (Coleoptera: Curculionidae: Lixinae). Zootaxa 4021(3): 433–446. https://doi.org/10.11646/zootaxa.4021.3.3
  85. Van Hezewijk B. H. & Bourchier R. S. 2012. Impact of Cyphocleonus achates on diffuse knapweed and its interaction with Larinus minutus. Biological Control 62(2): 113–119. https://doi.org/10.1016/j.biocontrol.2012.03.008
  86. Volovnik S. V. 2010. Weevils Lixinae (Coleoptera, Curculionidae) as gall formers. Entomological Review 90(5): 585–590. https://doi.org/10.1134/S0013873810050052
  87. Volovnik S. V. 2022. Synoptic catalogue of insect parasitoids associated with Lixinae (Coleoptera: Curculionoidea: Curculionidae). Journal of Insect Biodiversity 35(1): 1–37. https://doi.org/10.12976/jib/2022.35.1.1
  88. Volovnik S.V. 2023. On the distribution and biology of Bothynoderes affinis, one of the pests of sugar beet. Munis Entomology and Zoology 8 (supplement): 2027–2036.
  89. Wanat M. 2011. Biology and distribution of Lixus punctiventris Boheman, 1835 (Coleoptera, Curculionidae) in Poland. Weevil News: http://www.curci.de, 64: 5 pp.
  90. Yothers M. A. & Lancing E. 1910. Notes of Lixus marginatus Say. The Canadian Entomologist 42(3): 70–71. https://doi.org/10.4039/Ent4269-3
  91. Zerova M. D., Tolkanitz V. I., Kotenko A. G., Seriogina L. Ja., Diakonchuk L. A., Melika Zh. G., Gumovskij A. V., Fursov V. N., Simutnik S. A., Narol’skij N. B. & Stetzenko I. T. 2006. The Types of Ichneumonoidea, Cynipoidea and Chalcidoidea (Hymenoptera, Apocrita) Deposited in the Collection of the Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine. Vestnik Zoologii, Supplement 20(5–6): 136 pp.
  92. Zotov A. A. 2011. Morfologia preimaginalnykh stadij dolgonosikov triby Cleonini sensu lato (Coleoptera: Curculionidae). Caucasian Entomological Bulletin 7(2): 153–162. (in Russian) https://doi.org/10.23885/1814-3326-2011-7-2-153-162
  93. Zwölfer H. 1988. Evolutionary and ecological relationships of the insect fauna of thistles. Annual Review of Entomology 33: 103–122. https://doi.org/10.1146/annurev.en.33.010188.000535
  94. Zwölfer H., Frick K. E. & Andres L. A. 1971. A study of the host plant relationship of European members of the genus Larinus (Col.: Curculionidae). Commonwealth Institute of Biological Control, Technical Bulletin 14: 97–143.