Functional Morphology of the Thorax of the Click Beetle Campsosternus auratus (Coleoptera, Elateridae), with an Emphasis on Its Jumping Mechanism
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
31802004
National Natural Science Foundation of China
6020271010K
Post-doctoral Later-stage Foundation Project of Shenzhen Polytechnic
2021xjkk0605
the Third Xinjiang Scientific Expedition Program
2020GDASYL-20200102021
the GDAS Special Project of Science and Technology Development
2020GDASYL-20200301003
the GDAS Special Project of Science and Technology Development
PubMed
35323546
PubMed Central
PMC8955093
DOI
10.3390/insects13030248
PII: insects13030248
Knihovny.cz E-zdroje
- Klíčová slova
- 3D reconstruction, clamping, click beetles, clicking, function, locking, musculature,
- Publikační typ
- časopisecké články MeSH
We investigated and described the thoracic structures, jumping mechanism, and promesothoracic interlocking mechanism of the click beetle Campsosternus auratus (Drury) (Elateridae: Dendrometrinae). Two experiments were conducted to reveal the critical muscles and sclerites involved in the jumping mechanism. They showed that M2 and M4 are essential clicking-related muscles. The prosternal process, the prosternal rest of the mesoventrite, the mesoventral cavity, the base of the elytra, and the posterodorsal evagination of the pronotum are critical clicking-related sclerites. The destruction of any of these muscles and sclerites resulted in the loss of normal clicking and jumping ability. The mesonotum was identified as a highly specialized saddle-shaped biological spring that can store elastic energy and release it abruptly. During the jumping process of C. auratus, M2 contracts to establish and latch the clicking system, and M4 contracts to generate energy. The specialized thoracic biological springs (e.g., the prosternum and mesonotum) and elastic cuticles store and abruptly release the colossal energy, which explosively raises the beetle body in a few milliseconds. The specialized trigger muscle for the release of the clicking was not found; our study supports the theory that the triggering of the clicking is due to the building-up of tension (i.e., elastic energy) in the system.
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Bennet-Clark H.C., Lucey E.C.A. The jump of the flea: A study of the energetics and a model of the mechanism. J. Exp. Biol. 1967;47:59–76. doi: 10.1242/jeb.47.1.59. PubMed DOI
Sutton G.P., Burrows M. Biomechanics of jumping in the flea. J. Exp. Biol. 2011;214:836–847. doi: 10.1242/jeb.052399. PubMed DOI
Heitler W.J. The locust jump. J. Comp. Physiol. 1974;89:93–104. doi: 10.1007/BF00696166. DOI
Bennet-Clark H.C. The energetics of the jump of the locust Schistocerca gregaria. J. Exp. Biol. 1975;63:53–83. doi: 10.1242/jeb.63.1.53. PubMed DOI
Wan C., Hao Z., Feng X. Structures, properties, and energy-storage mechanisms of the semi-lunar process cuticles in locusts. Sci. Rep. 2016;6:35219. doi: 10.1038/srep35219. PubMed DOI PMC
Bonsignori G., Stefanini C., Scarfogliero U., Mintchev S., Benelli G., Dario P. The green leafhopper, Cicadella viridis (Hemiptera, Auchenorrhyncha, Cicadellidae), jumps with near-constant acceleration. J. Exp. Biol. 2013;216:1270–1279. doi: 10.1242/jeb.076083. PubMed DOI
Burrows M., Ghosh A., Sutton G.P., Yeshwanth H.M., Rogers S.M., Sane S.P. Jumping in lantern bugs (Hemiptera, Fulgoridae) J. Exp. Biol. 2021;224:jeb243361. doi: 10.1242/jeb.243361. PubMed DOI PMC
Nadein K., Betz O. Jumping mechanisms and performance in beetles. I. Flea beetles (Coleoptera: Chrysomelidae: Alticini) J. Exp. Biol. 2016;219:2015–2027. doi: 10.1242/jeb.140533. PubMed DOI
Nadein K., Betz O. Jumping mechanisms and performance in beetles. II. Weevils (Coleoptera: Curculionidae: Rhamphini) Arthropod Struct. Dev. 2018;47:131–143. doi: 10.1016/j.asd.2018.02.006. PubMed DOI
Ruan Y., Konstantinov A.S., Shi G., Tao Y., Li Y., Johnson A.J., Luo X., Zhang X., Zhang M., Wu J., et al. The mechanical mechanism of the flea beetle jump, its application to bionics and preliminary design for a robotic jumping leg. ZooKeys. 2020;915:87–105. doi: 10.3897/zookeys.915.38348. PubMed DOI PMC
Muona J., Chang H., Ren D. The clicking Elateroidea from Chinese Mesozoic deposits (Insecta, Coleoptera) Insects. 2020;11:875. doi: 10.3390/insects11120875. PubMed DOI PMC
Kundrata R., Packova G., Prosvirov A.S., Hoffmannova J. The fossil record of Elateridae (Coleoptera: Elateroidea): Described species, current problems and future prospects. Insects. 2021;12:286. doi: 10.3390/insects12040286. PubMed DOI PMC
Evans M.E.G. The jump of the click beetle (Coleoptera, Elateridae)—A preliminary study. J. Zool. 1972;167:319–336. doi: 10.1111/j.1469-7998.1972.tb03115.x. DOI
Binaghi G. Sulla meccanica del salto degli Elateridi. Boll. Soc. Ent. Ital. 1942;74:1–6.
d’Aguilar J. Recherches sur l’thologie des imagos d’Agriotes (Col. Elateridae) Annals Ểpiphyt. 1961;11:1–95.
Larsén O. On the morphology and function of locomotor organs of the Gyrinidae and other Coleoptera. Opusc. Entomol. 1966;30:1–241.
Evans M.E.G. The jump of the click beetle (Coleoptera: Elateridae)—Energetics and mechanics. J. Zool. 1973;169:181–194. doi: 10.1111/j.1469-7998.1973.tb04553.x. DOI
Ribak G., Weihs D. Jumping without using legs: The jump of the click-beetles (Elateridae) is morphologically constrained. PLoS ONE. 2011;6:e20871. doi: 10.1371/journal.pone.0020871. PubMed DOI PMC
Ribak G., Mordechay O., Weihs D. Why are there no long distance jumpers among click-beetles (Elateridae)? Bioinspir. Biomim. 2013;8:036004. doi: 10.1088/1748-3182/8/3/036004. PubMed DOI
Ribak G., Reingold S., Weihs D. The effect of natural substrates on jump height in click-beetles. Funct. Ecol. 2012;26:493–499. doi: 10.1111/j.1365-2435.2011.01943.x. DOI
Bolmin O., Duan C., Urrutia L., Abdulla A.M., Hazel A.M., Alleyne M., Dunn A.C., Wissa A. Pop! Observing and modeling the legless self-righting jumping mechanism of click beetles. In: Mangan M., Cutkosky M., Mura A., Verschure P.F.M.J., Prescott T., Lepora N., editors. Living Machines. Springer; Cham, Switzerland: 2017. pp. 35–47.
Bolmin O., Wei L., Hazel A.M., Dunn A.C., Wissa A., Alleyne M. Latching of the click beetle (Coleoptera: Elateridae) thoracic hinge enabled by the morphology and mechanics of conformal structures. J. Exp. Biol. 2019;222:jeb196683. doi: 10.1242/jeb.196683. PubMed DOI
Bolmin O., Socha J.J., Alleyne M., Dunn A.C., Fezzaa K., Wissa A. Nonlinear elasticity and damping govern ultrafast dynamics in click beetles. Proc. Natl. Acad. Sci. USA. 2021;118:1–8. doi: 10.1073/pnas.2014569118. PubMed DOI PMC
Fukushima A., Kawaguchi Y. Click beetle-like jumping device for entertainment; Proceedings of the SIGGRAPH Asia 2014 Emerging Technologies; Shenzhen, China. 3–6 December 2014; pp. 1–3. DOI
Chen G., Tu J., Ti X., Hu H. A single-legged robot inspired by the jumping mechanism of click beetles and its hopping dynamics analysis. J. Bionic. Eng. 2020;17:1–17. doi: 10.1007/s42235-020-0099-z. DOI
Cate P.C., Sánchez-Ruiz A., Löbl I., Smetana A. Elateridae. In: Löbl I., Smetana A., editors. Catalogue of Palaearctic Coleoptera. Volume 4. Apollo Books; Stenstrup, Denmark: 2007. pp. 89–209.
Kundrata R., Gunter N.L., Janosikova D., Bocak L. Molecular evidence for the subfamilial status of Tetralobinae (Coleoptera: Elateridae), with comments on parallel evolution of some phenotypic characters. Arthropod Syst. Phylogeny. 2018;76:137–145.
Douglas H.B., Kundrata R., Brunke A.J., Escalona H.E., Chapados J.T., Eyres J., Richter R., Savard K., Ślipiński A., McKenna D., et al. Anchored phylogenomics, evolution and systematics of Elateridae: Are all bioluminescent Elateroidea derived click beetles? Biology. 2021;10:451. doi: 10.3390/biology10060451. PubMed DOI PMC
Matsuda R. Morphology and evolution of the insect thorax. Mem. Entomol. Soc. Can. 1970;102:5–431. doi: 10.4039/entm10276fv. DOI
Verhoeff K.W. Zur vergleichenden Morphologie des Abdomens der Coleopteren und über die phylogenetische Bedeutung desselben, zugleich ein zusammenfassender kritischer Rückblick und neuer Beitrag. Z. Wiss. Zool. 1918;117:130–204.
Horst A. Zur Kenntnis der Biologie und Morphologie einiger Elateriden und ihrer Larven. Arch. Nat. 1922;88:1–90.
Douglas H.B. Revision of Cardiophorus (Coleoptera: Elateridae) species of eastern Canada and United States of America. Can. Entomol. 2003;135:493–548. doi: 10.4039/n02-003. DOI
Šípek P., Fabrizi S., Eberle J., Ahrens D. A molecular phylogeny of rose chafers (Coleoptera: Scarabaeidae: Cetoniinae) reveals a complex and concerted morphological evolution related to their flight mode. Mol. Phylogenet. Evol. 2016;101:163–175. doi: 10.1016/j.ympev.2016.05.012. PubMed DOI
Sugimoto M., Ogawa N., Yoshizawa K. Morphology of the elytral base sclerites. Arthropod Struct. Dev. 2018;47:423–429. doi: 10.1016/j.asd.2018.02.004. PubMed DOI
Kukalová-Peck J., Lawrence J.F. Relationship among coleopteran suborders and major endoneopteran lineages: Evidence from hind wing characters. Eur. J. Entomol. 2004;101:95–144. doi: 10.14411/eje.2004.018. DOI
Lawrence J.F., Beutel R.G., Leschen R.A.B., Ślipiński A. Glossary of morphological terms. In: Beutel R.G., Lawrence J.F., Leschen R.A.B., editors. Handbook of Zoology—Arthropoda: Insecta—Coleoptera, Beetles. Volume 2. De Gruyter; Berlin, Germany: 2010. pp. 9–20.
Gurjeva E.L. Stroenie grudnogo otdela zhukov-shchelkunov (Coleoptera, Elateridae) I znachenie ego priznakov dlya sistemy semeistva [Thoracic structure of click beetles (Coleoptera, Elateridae) and the significance of the structural characters for the system of the family] Ent. Obozr. 1974;53:96–113. (In Russian)
Friedrich F., Beutel R.G. The pterothoracic skeletomuscular system of Scirtoidea (Coleoptera: Polyphaga) and its implications for the relationships of the beetle suborders. J. Zool. Syst. Evol. Res. 2006;44:290–315. doi: 10.1111/j.1439-0469.2006.00369.x. DOI
Crowson R.A. The Natural Classification of the Families of Coleoptera. EW. Classey Ltd.; Middlesex, UK: 1967. p. 214.
Calder A.A. Click Beetles: Genera of the Australian Elateridae (Coleoptera) CSIRO Publishing; Clayton, Australia: 1996. p. 401. Monographs on Invertebrate Taxonomy.
Douglas H.B. Phylogenetic relationships of Elateridae inferred from adult morphology, with special reference to the position of Cardiophorinae. Zootaxa. 2011;2900:1–45. doi: 10.11646/zootaxa.2900.1.1. DOI
Douglas H.B. World reclassification of the Cardiophorinae (Coleoptera, Elateridae), based on phylogenetic analyses of morphological characters. ZooKeys. 2017;655:1–130. doi: 10.3897/zookeys.655.11894. PubMed DOI PMC
Baehr M. Zur Funktionsmorphologie und evolutiven Bedeutung der elytralen Sperrmechanismen der Scaritini (Coleoptera: Carabidae) Entomol. Gen. 1980;6:311–333.
Friedrich F., Beutel R.G. The thorax of Zorotypus (Hexapoda, Zoraptera) and a new nomenclature for the musculature of Neoptera. Arthropod Struct. Dev. 2008;37:29–54. doi: 10.1016/j.asd.2007.04.003. PubMed DOI
Belkaceme T. Skelet und Muskulatur des Kopfes und Thorax von Noterus laevis Sturm. Ein Beitrag zur Morphologie und Phylogenie der Noteridae (Coleoptera: Adephaga) Stuttg. Beitr. Naturk. 1991;462:1–94.
Lawrence J.F., Ślipiński A., Seago A.E., Thayer M.K., Newton A.F., Marvaldi A.E. Phylogeny of the Coleoptera based on morphological characters of adults and larvae. Ann. Zool. 2011;61:1–217. doi: 10.3161/000345411X576725. DOI
Jordan A., Broad G.R., Stigenberg J., Hughes J., Stone J., Bedford I., Penfield S., Wells R. The potential of the solitary parasitoid Microctonus brassicae for the biological control of the adult cabbage stem flea beetle Psylliodes chrysocephala. Entomol. Exp. Appl. 2020;168:360–370. doi: 10.1111/eea.12910. PubMed DOI PMC
Patek S.N., Korff W.L., Caldwell R.L. Biomechanics: Deadly strike mechanism of a mantis shrimp. Nature. 2004;428:819–820. doi: 10.1038/428819a. PubMed DOI
Patek S.N., Rosario M.V., Taylor J.R. Comparative spring mechanics in mantis shrimp. J. Exp. Biol. 2013;216:1317–1329. doi: 10.1242/jeb.078998. PubMed DOI
Tadayon M., Amini S., Wang Z.A., Miserez A. Biomechanical design of the mantis shrimp saddle: A biomineralized spring used for rapid raptorial strikes. iScience. 2018;8:271–282. doi: 10.1016/j.isci.2018.08.022. PubMed DOI PMC
Potter J. Woodpeckers and head injury. Lancet. 1976;307:640. doi: 10.1016/S0140-6736(76)90441-4. DOI
May P.R., Fuster J.M., Haber J., Hirschman A. Woodpecker drilling behavior: An endorsement of the rotational theory of impact brain injury. Arch. Neurol. 1979;36:370–373. doi: 10.1001/archneur.1979.00500420080011. PubMed DOI
Wang L., Cheung J.T.M., Pu F., Li D., Zhang M., Fan Y. Why do woodpeckers resist head impact injury: A biomechanical investigation. PLoS ONE. 2011;6:e26490. doi: 10.1371/journal.pone.0026490. PubMed DOI PMC
Kundrata R., Bocak L. The phylogeny and limits of Elateridae (Insecta, Coleoptera): Is there a common tendency of click beetles to soft-bodiedness and neoteny? Zool. Scr. 2011;40:364–378. doi: 10.1111/j.1463-6409.2011.00476.x. DOI