Comparative Antennal Morphology of Agriotes (Coleoptera: Elateridae), with Special Reference to the Typology and Possible Functions of Sensilla
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
57378441
Deutscher Akademischer Austauschdienst
287664 and 285948
Tempus Public Foundation
PubMed
32098184
PubMed Central
PMC7074560
DOI
10.3390/insects11020137
PII: insects11020137
Knihovny.cz E-resources
- Keywords
- chemoreceptors, click-beetles, crop pest, pest control, pheromones, scanning electron microscopy, wireworm,
- Publication type
- Journal Article MeSH
Species of the click-beetle genus Agriotes Eschscholtz are economically important crop pests distributed mainly in the Northern Hemisphere. They can inflict considerable damage on various field crops. Therefore, the detection, monitoring, and control of Agriotes include the adult trapping using species-specific sex pheromones, which is a critical component of pest research. To obtain a better understanding of the detailed antennal morphology as background information for subsequent chemical ecology research, we conducted a scanning electron microscopy study of the antennal sensilla of both sexes in 10 European Agriotes species. We identified 16 different sensilla in Agriotes, belonging to six main types: sensilla chaetica (subtypes C1 and C2), sensilla trichodea, sensilla basiconica (subtypes B1-B9), dome-shaped sensilla (subtypes D1 and D2), sensilla campaniformia, and Böhm sensilla. We discuss their possible functions and compare the sensilla of Agriotes with those of other Elateridae in order to consolidate the sensillum nomenclature in this family. Additionally, our study reveals the remarkable interspecific variability in sensillar equipment of Agriotes and identifies several characters of potential importance for future use in systematic studies. The present study provides a strong preliminary framework for subsequent research on the antennal morphology of this crop pest on a wider scale.
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Hill D.S. Agricultural Insect Pests of Temperate Regions and Their Control. Cambridge University Press; Cambridge, UK: 1987. 272p
Parker W.E., Howard J.J. The biology and management of wireworms (Agriotes spp.) on potato with particular reference to the U.K. Agric. For. Entomol. 2001;3:85–98. doi: 10.1046/j.1461-9563.2001.00094.x. DOI
Barsics F., Haubruge E., Verheggen F.J. Wireworms’ management: An overview of the existing methods, with particular regards to Agriotes spp. (Coleoptera: Elateridae) Insects. 2013;4:117–152. doi: 10.3390/insects4010117. PubMed DOI PMC
Ritter C., Richter E. Control methods and monitoring of Agriotes wireworms (Coleoptera: Elateridae) J. Plant Dis. Protect. 2013;120:4–15. doi: 10.1007/BF03356448. DOI
Keiser A., Häberli M., Stamp P. Quality deficiencies on potato (Solanum tuberosum L.) tubers caused by Rhizoctonia solani, wireworms (Agriotes ssp.) and slugs (Deroceras reticulatum, Arion hortensis) in different farming systems. Field Crop Res. 2012;128:147–155. doi: 10.1016/j.fcr.2012.01.004. DOI
Traugott M., Benefer C.M., Blackshaw R.P., van Herk W.G., Vernon R.S. Biology, ecology, and control of elaterid beetles in agricultural land. Annu. Rev. Entomol. 2015;60:313–334. doi: 10.1146/annurev-ento-010814-021035. PubMed DOI
Cate P. Elateridae. In: Löbl I., Smetana A., editors. Catalogue of Palaearctic Coleoptera. Volume 4. Apollo Books; Stenstrup, Denmark: 2007. pp. 89–209.
Kabalak M., Sert O., Özgen İ., Platia G. A new species of the Agriotes nuceus species group from Turkey. J. Insect Sci. 2013;13:17. doi: 10.1673/031.013.1701. PubMed DOI PMC
Johnson P.J. Elateridae Leach 1815. In: Arnett R.H., Thomas M.C., Skelley P.E., Frank J.H., editors. American Beetles, Volume 2, Polyphaga: Scarabaeoidea through Curculionoidea. CRC Press; Boca Raton, FL, USA: 2002. pp. 160–173.
Furlan L., Tóth M., Parker W.E., Ivezić M., Pancic S., Brmez M., Dobrinčić R., Barčić J.I., Mureşan F., Subchev M., et al. The efficacy of the new Agriotes sex pheromone traps in detecting wireworm population levels in different European countries; Proceedings of the XXI IWGO Conference; Legnaro, Italy. 27 October–3 November 2001; Legnaro, Italy: Veneto Agricoltura; 2001. pp. 293–303.
Tóth M., Furlan L., Xavier A., Vuts J., Toshova T., Subchev M., Szarukan I., Yatsynin V. New sex attractant composition for the click beetle Agriotes proximus: Similarity to the pheromone of Agriotes lineatus. J. Chem. Ecol. 2008;34:107–111. doi: 10.1007/s10886-007-9398-7. PubMed DOI
Staudacher K., Pitterl P., Furlan L., Cate P.C., Traugott M. PCR-based species identification of Agriotes larvae. Bull. Entomol. Res. 2011;101:201–210. doi: 10.1017/S0007485310000337. PubMed DOI
Vuts J., Tolasch T., Furlan L., Csonka É.B., Felföldi T., Márialigeti K., Toshova T.B., Subchev M., Xavier A., Tóth M. Agriotes proximus and A. lineatus (Coleoptera: Elateridae): A comparative study on the pheromone composition and cytochrome c oxidase subunit I gene sequence. Chemoecology. 2012;22:23–28. doi: 10.1007/s00049-011-0091-5. DOI
Benefer C.M., van Herk W.G., Ellis J.S., Blackshaw R.P., Vernon R.S., Knight M.E. The molecular identification and genetic diversity of economically important wireworm species (Coleoptera: Elateridae) in Canada. J. Pest Sci. 2013;86:19–27. doi: 10.1007/s10340-012-0454-x. DOI
Tóth M., Furlan L., Yatsynin V.G., Ujvary I., Szarukan I., Imrei Z., Tolasch T., Francke W., Jossi W. Identification of pheromones and optimization of bait composition for click beetle pests (Coleoptera: Elateridae) in Central and Western Europe. Pest Manag. Sci. 2003;59:417–425. doi: 10.1002/ps.629. PubMed DOI
Vernon R.S., Tóth M. Evaluation of pheromones and a new trap for monitoring Agriotes lineatus and Agriotes obscurus in the Fraser valley of British Columbia. J. Chem. Ecol. 2007;32:345–351. doi: 10.1007/s10886-006-9217-6. PubMed DOI
Tóth M. Pheromones and attractants of click beetles: An overview. J. Pest Sci. 2013;86:3–17. doi: 10.1007/s10340-012-0429-y. DOI
Blackshaw R.P., van Herk W.G., Vernon R.S. Determination of Agriotes obscurus (Coleoptera: Elateridae) sex pheromone attraction range using target male behavioural responses. Agric. For. Entomol. 2018;20:228–233. doi: 10.1111/afe.12249. DOI
Tóth M., Furlan L., Szarukán I., Nagy A., Vuts J., Toshova T., Velchev D., Lohonyai Z., Imrei Z. The addition of a pheromone to a floral lure increases catches of females of the click beetle Agriotes ustulatus (Schaller) (Coleoptera: Elateridae) J. Chem. Ecol. 2019;45:667–672. doi: 10.1007/s10886-019-01087-z. PubMed DOI PMC
Borg-Karlson A.-K., Agren L., Dobson H., Bergström G. Identification and electroantennographic activity of sex-specific geranyl esters in an abdominal gland of female Agriotes obscurus (L.) and A. lineatus (L.) (Coleoptera, Elateridae) Experientia. 1988;44:531–534. doi: 10.1007/BF01958940. DOI
Merivee E., Erm A. Studies on sex pheromone gland morphology and pheromone components in female elaterid beetles Agriotes obscurus L. and Agriotes lineatus L. (Coleoptera, Elateridae) Eesti. NSV Tead. Akad. Toim. Biol. 1993;42:108–117.
Yatsynin V.G., Rubanova E.V., Okhrimenko N.V. Identification of female-produced sex pheromones and their geographical differences in pheromone gland extract composition from click beetles (Col., Elateridae) J. Appl. Entomol. 1996;120:463–466. doi: 10.1111/j.1439-0418.1996.tb01636.x. DOI
Tóth M., Furlan L., Yatsynin V.G., Ujvary I., Szarukan I., Imrei Z., Subchev M., Tolasch T., Francke W. Identification of sex pheromone composition of click beetle Agriotes brevis Candèze. J. Chem. Ecol. 2002;28:1641–1652. doi: 10.1023/A:1019984714858. PubMed DOI
Tolasch T., von Fragstein M., Steidle J.L. Sex pheromone of Agriotes acuminatus (Stephens, 1830) (Coleoptera: Elateridae) J. Chem. Ecol. 2010;36:314–318. doi: 10.1007/s10886-010-9767-5. PubMed DOI
Vuts J., Furlan L., Tóth M. Female responses to synthetic pheromone and plant compounds in Agriotes brevis Candèze (Coleoptera: Elateridae) J. Insect Behav. 2018;31:106–117. doi: 10.1007/s10905-018-9668-y. DOI
Merivee E. Antennal sensilla of the female and male elaterid beetle Agriotes obscurus L. (Coleoptera: Elateridae) Proc. Estonian Acad. Sci. Biol. 1992;41:189–215.
Merivee E., Rahi M., Luik A. Distribution of olfactory and some other antennal sensilla in the male click beetle Agriotes obscurus L. (Coleoptera: Elateridae) Int. J. Insect Morphol. Embryol. 1997;26:75–83. doi: 10.1016/S0020-7322(97)00013-5. DOI
Merivee E., Rahi M., Bresciani J., Ravn H.P., Luik A. Antennal sensilla of the click beetle, Limonius aeruginosus (Olivier) (Coleoptera: Elateridae) Int. J. Insect Morphol. Embryol. 1998;27:311–318. doi: 10.1016/S0020-7322(98)00023-3. DOI
Merivee E., Rahi M., Luik A. Antennal sensilla of the click beetle, Melanotus villosus (Geoffroy) (Coleoptera: Elateridae) Int. J. Insect Morphol. Embryol. 1999;28:41–51. doi: 10.1016/S0020-7322(98)00032-4. DOI
Peng G., Shu J., Zhang A., Wang J., Xu T., Wang H. Antennal sensilla of the click beetle, Melanotus cribricollis (Coleoptera: Elateridae) Sci. Silvae Sin. 2012;48:106–112.
Ren L.-L., Wu Y., Shi J., Zhang L., Luo Q. Antennal morphology and sensilla ultrastructure of Tetrigus lewisi Candèze (Coleoptera: Elateridae) Micron. 2014;60:29–38. doi: 10.1016/j.micron.2014.01.005. PubMed DOI
Zauli A., Maurizi E., Carpaneto G.M., Chiari S., Merivee E., Svensson G.P., Di Giulio A. Scanning electron microscopy analysis of the antennal sensilla in the rare saproxylic beetle Elater ferrugineus (Coleoptera, Elateridae) Ital. J. Zool. 2016;83:338–350. doi: 10.1080/11250003.2016.1211766. DOI
Faucheux M.J., Kundrata R. Comparative antennal morphology of male Drilini with special reference to the sensilla (Coleoptera: Elateridae: Agrypninae) Zool. Anz. 2017;266:105–119. doi: 10.1016/j.jcz.2016.11.002. DOI
Zacharuk R.Y. Ultrastructure and function of insect chemosensilla. Ann. Rev. Entomol. 1980;25:27–47. doi: 10.1146/annurev.en.25.010180.000331. DOI
Altner H., Prillinger L. Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and its functional significance. Internat. Rev. Cytol. 1980;67:69–139.
Faucheux M.J. Biodiversité et Unité des Organes Sensoriels des Insectes Lépidoptères. Société des Sciences Naturelles de l’Ouest de la France; Nantes, France: 1999. pp. 1–296.
Chen J.M., Qiao H.L., Xhen J., Xu C.Q., Lian Z.M., Guo K. Observation of antennal sensilla in Xylotrechus grayii (Coleoptera: Cerambycidae) with scanning electron microscopy. Microsc. Res. Tech. 2014;77:264–273. doi: 10.1002/jemt.22338. PubMed DOI
Faucheux M.J. Persistence of larval characteristics on the antennae of the neotenic female of Drilus mauritanicus Lucas, 1849 (Coleoptera, Elateridae, Agrypninae, Drilini) Bull. Inst. Sci. Rabat Sect. Sci. Vie. 2014;36:65–76.
Faucheux M.J., Beaulieu G. Antennal sensilla in the male imago of Drilus mauritanicus Lucas 1849. Comparison with Malacogaster passerinii Bassi 1833 (Coleoptera: Elateridae: Agrypninae: Drilini) Bull. Soc. Sci. Nat. Ouest Fr. (N.S.) 2016;38:149–163.
Altner H. Insect sensillum specificity and structure: An approach to a new typology. In: Le Magnen J., MacLeod P., editors. Olfaction and Taste. Volume 6. Information Retrieval; London, UK: 1977. pp. 295–303.
Zacharuk R.Y. Antennae and sensilla. In: Kerkut G.A., Gilbert L.I., editors. Comparative Insect Physiology, Biochemistry and Pharmacology. Volume 6. Pergamon Press; London, UK: 1985. pp. 1–69.
Faucheux M.J. Sensilles antennaires du mâle du Ver luisant, Lampyris noctiluca (Linnaeus, 1767) (Coleoptera: Elateroidea: Lampyridae) Bull. Soc. Sci. Nat. Ouest Fr. (N.S.) 2015;37:145–152.
Dyer L.J., Seabrook W.D. Sensilla on the antennal flagellum of the sawyer beetles Monochamus notatus (Drury) and Monochamus scutellatus (Say) (Coleoptera: Cerambycidae) J. Morphol. 1975;146:513–532. doi: 10.1002/jmor.1051460407. PubMed DOI
Dai H.-G., Honda H. Sensilla on the antennal flagellum of the yellow spotted longicorn beetle, Psacothea hilaris (Pascoe) (Coleoptera: Cerambycidae) Appl. Entomol. Zool. 1990;25:273–282. doi: 10.1303/aez.25.273. DOI
Faucheux M.J. Le Grand Capricorne, Cerambyx cerdo Linné. In: Faucheux M.J., Lebrun D., Sadorge A., editors. Les Insectes du Bois: Capricornes, Vrillettes, Termites et Autres Xylophages. Société des Sciences Naturelles de l’Ouest de la France; Nantes, France: 2001. pp. 115–134.
Faucheux M.J. Antennal sensilla of the yellow beetle Phoracantha recurva Newman, 1840: Distribution and comparison with Phoracantha semipunctata (Fabricius, 1775) (Coleoptera: Cerambycidae) Bull. Inst. Sci. Rabat, Sect. Sci. Vie. 2011;33:19–29.
Hatfield L.D., Frazier J.L., Coons L.B. Antennal sensilla of the pecan weevil, Curculio caryae (Horn) (Coleoptera: Curculionidae) Int. J. Insect Morphol. Embryol. 1976;5:279–287. doi: 10.1016/0020-7322(76)90028-3. DOI
Faucheux M.J. Distribution and abundance of antennal sensilla from two populations of the pine engraver beetle, Ips pini (Say) (Coleoptera: Scolytidae) Ann. Sci. Nat. Zool. 1994;15:15–31.
Merivee E., Ploomi A., Rahi M., Luik A., Sammelselg V. Antennal sensilla of the ground beetle Bembidion lampros Hbst. (Coleoptera, Carabidae) Acta Zool. 2000;81:339–350. doi: 10.1046/j.1463-6395.2000.00068.x. DOI
Merivee E., Ploomi A., Luik A., Rahi M., Sammelselg V. Antennal sensilla of the ground beetle Platynus dorsalis (Pontoppidan, 1763) (Coleoptera, Carabidae) Microsc. Res. Tech. 2001;55:339–349. doi: 10.1002/jemt.1182. PubMed DOI
Schneider D. Electrophysiological investigation of the olfactory specificity of sexual attracting substances in different species of moths. J. Insect Physiol. 1962;8:15–30. doi: 10.1016/0022-1910(62)90051-3. DOI
Tóth M., Szöcs G., Löfstedt C., Hansson B.S., Subchev M. Sex pheromone components of Mamestra suasa: Chemical analysis, electrophysiological activity, wind tunnel activity and field tests in two European countries. Entomol. Exp. Appl. 1986;42:291–299. doi: 10.1111/j.1570-7458.1986.tb01035.x. DOI
Greenfield M.D. Sexual selection. In: Allison J.D., Cardé R.T., editors. Pheromone Communication in Moths. Evolution, Behavior, and Application. University of California Press; Oakland, CA, USA: 2016. pp. 79–88.
Cook B.J., Shelton W.D., Staten R.T. Antennal responses of the pink bollworm to gossypiella. Southwest. Entomol. 1978;3:141–146.
Van der Pers J.N.C. Responses from olfactory receptors in females of three species of small ermine moths (Lepidoptera: Yponomeutidae) to plant odours. Entomol. Exp. Appl. 1978;24:394–398.
Lopes O., Barata E.N., Mustaparta H., Araújo J. Fine structure of antennal sensilla basiconica and their detection of plant volatiles in the eucalyptus woodborer, Phoracantha semipunctata Fabricius (Coleoptera: Cerambycidae) Arthropod Struct. Dev. 2002;31:1–13. doi: 10.1016/S1467-8039(02)00011-7. PubMed DOI
Sun L., Xiao H., Gu S.H., Zhou J.J., Guo Y.Y., Liu Z.W., Zhang Y.J. The antenna-specific odorant binding protein AlinOBP13 of the alphalpha plant bug Adelphocoris lineolatus is expressed specifically in basiconic sensilla and has high binding affinity to terpenoids. Insect Mol. Biol. 2014;23:417–434. doi: 10.1111/imb.12089. PubMed DOI
Zhang Y., Ren L., Zhang L., Luo Y. Ultrastructure of antennal and posterior abdominal sensilla in Chlorophorus caragana females. Micron. 2015;75:45–57. doi: 10.1016/j.micron.2015.04.014. PubMed DOI
Hallberg E. Sensory organs in Ips typographus (Insecta: Coleoptera)—Fine structure of antennal sensilla. Protoplasma. 1982;111:206–214. doi: 10.1007/BF01281968. DOI
Monteforti G., Angeli S., Petacchi R., Minnocci A. Ultrastructural characterization of antennal sensilla and immunocytochemical localization of a chemosensory protein in Carausius morosus Brünner (Phasmida: Phasmatidae) Arthropod Struct. Dev. 2002;30:195–205. doi: 10.1016/S1467-8039(01)00036-6. PubMed DOI
Faucheux M.J. The larviform females of Malacogaster nigripes Schaufuss 1867. Antennal sensilla: Persistence and significance of larval characteristics (Coleoptera: Elateridae: Agrypninae: Drilini) Bull. Soc. Sci. Nat. Ouest Fr. (N.S.) 2016;38:287–310.
Faucheux M.J. La sensille campaniforme des insectes: La vraie et les fausses. Bull. Soc. Sci. Nat. Ouest Fr. (N.S.) 2019;41:155–159.
Nurme K., Merivee E., Must A., Di Giulio A., Muzzi M., Williams I., Mänd M. Bursty spike trains of antennal thermo- and bimodal hygro-thermoreceptor neurons encode noxious heat in elaterid beetles. J. Therm. Biol. 2018;72:101–117. doi: 10.1016/j.jtherbio.2018.01.008. PubMed DOI
Stange G., Stowe S. Carbon-dioxide sensing structures in terrestrial arthropods. Microsc. Res. Tech. 1999;47:416–427. doi: 10.1002/(SICI)1097-0029(19991215)47:6<416::AID-JEMT5>3.0.CO;2-X. PubMed DOI
McIver S.B. Mechanoreception. In: Kerkut G.A., Gilbert L.I., editors. Comprehensive Insect Physiology, Biochemistry and Pharmacology. Volume 6. Pergamon Press; London, UK: 1985. pp. 71–132.
Ritcey G.M., McIver S.B. External morphology of antennal sensilla of four species of adult flea beetles (Coleoptera: Chrysomelidae: Alticinae) Int. J. Insect Morphol. Embryol. 1990;19:141–153. doi: 10.1016/0020-7322(90)90024-J. DOI
Fischer D.C., Kogan M. Chemoreceptors of adult Mexican bean beetles. External morphology and role in food preference. Entomol. Exp. Appl. 1986;40:3–12. doi: 10.1111/j.1570-7458.1986.tb02149.x. DOI
Schneider D. Insect antennae. Ann. Rev. Entomol. 1964;9:103–122. doi: 10.1146/annurev.en.09.010164.000535. DOI
Faucheux M.J., Mason F. Les antennes des Némotélinés (Insecta: Diptera: Stratiomyidae). I: Nemotelus Geoffroy et Cluninemotelus Mason. Bull. Soc. Sci. Nat. Ouest Fr. (N.S.) 2000;22:49–70.
Faucheux M.J. Sensilles auricilliformes multipores sur l’antenne de l’adulte femelle de Liposcelis decolor (Pearman 1925) (Psocoptera: Troctomorpha: Liposcelididae) Bull. Soc. Sci. Nat. Ouest Fr. (N.S.) 2012;34:233–242.
Gurjeva E.L. A review of the Palearctic species of the genus Agriotes Esch. (Coleoptera, Elateridae) Entomol. Obozr. 1972;51:859–877.