First Comprehensive Study of a Giant Among the Insects, Titanus giganteus: Basic Facts from Its Biochemistry, Physiology, and Anatomy

. 2020 Feb 12 ; 11 (2) : . [epub] 20200212

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32059419

Grantová podpora
CENAKVA (LM2018099) Ministerstvo Školství, Mládeže a Tělovýchovy
RVO 60077344 undefined <span style="color:gray;font-size:10px;">undefined</span>

Titanus giganteus is one of the largest insects in the world, but unfortunately, there is a lack of basic information about its biology. Previous papers have mostly described Titanus morphology or taxonomy, but studies concerning its anatomy and physiology are largely absent. Thus, we employed microscopic, physiological, and analytical methods to partially fill this gap. Our study focused on a detailed analysis of the antennal sensilla, where coeloconic sensilla, grouped into irregularly oval fields, and sensilla trichoidea were found. Further, the inspection of the internal organs showed apparent degeneration of the gut and almost total absence of fat body. The gut was already empty; however, certain activity of digestive enzymes was recorded. The brain was relatively small, and the ventral nerve cord consisted of three ganglia in the thorax and four ganglia in the abdomen. Each testis was composed of approximately 30 testicular follicles filled with a clearly visible sperm. Chromatographic analysis of lipids in the flight muscles showed the prevalence of storage lipids that contained 13 fatty acids, and oleic acid represented 60% of them. Some of our findings indicate that adult Titanus rely on previously accumulated reserves rather than feeding from the time of eclosion.

Zobrazit více v PubMed

Raye de Breukelerwaert J. Catalogue du cabinet célèbre et très renommé d’objets d’Histoire Naturelle delaissé par le très noble sieur Joan Raye seigneur de Breukelerwaert à Amsterdam. Van Cleef; Amsterdam: 1827. pp. 68–71.

Lameere A.A.L. Révision des Prionides. Dixième mémoire. Titanines Ann. de la société Entomol. de Belg. Brux. 1904;48:309–352.

Le Moult E. Captures et Biologie. Bull. Soc. Entomol. Fr. 1909:55–56.

Bleuzen P. Les coleopteres du monde: Prioninae 1. Sci. Nat. Venette. 1994;21:1–92.

Tavakilian G. Base de données Titan sur les cerambycidés ou longicornes. [(accessed on 12 May 2019)];2018 Available online: http://titan.gbif.fr/index.html.

Monné M.A. Catalogue of the Cerambycidae (Coleoptera) of the neotropical region. Part II. Subfamilies Lepturinae, Necydalinae, Parandrinae, Prioninae, Spondylidinae and families Oxypeltidae, Vesperidae, and Disteniidae. [(accessed on 12 May 2019)];2018 Available online: http://cerambyxcat.com/Parte3_Prioninae_Lepturinae_2018.pdf.

Lacordaire J.T. Notice sur l’entomologie de la Guyane française. Ann. de la société Entomol. de Fr. Paris. 1832;1:348–366.

Drury D., Westwood J.O. In: Illustrations of Exotic Entomology, Containing Upwards of Six Hundred and Fifty Figures and Descriptions of Foreign Insects Interspersed with Remarks and Reflections on Their Nature and Properties. 1st ed. Henry G., editor. Bohn; London, UK: 1836.

Sturm J. Catalog der Käfer-Sammlung von Jacob Sturm. Gedruckt auf Kosten des Verfassers; Nürnberg, Germany: 1843.

Thomson J. Systema Cerambycidarum ou exposé de tous les genres compris dans la famille des Cérambycides et familles limitrophes. Mémoires de la Société R. des Sci. de Liège. 1864;19:1–540.

Bates H.W., IX Contributions to an Insect Fauna of the Amazon Valley (Coleoptera, Prionides) Trans. Entomol. Soc. Lond. 1869;I:37–58. doi: 10.1111/j.1365-2311.1869.tb01097.x. DOI

Schloss P.D., Delalibera I., Handelsman J., Raffa K.F. Bacteria associated with the guts of two woodboring beetles: Anoplophora glabripennis and Saperda vestita (Cerambycidae) Environ. Entomol. 2006;35:625–629. doi: 10.1603/0046-225X-35.3.625. DOI

Mohammed W.S., Ziganshina E.E., Shagimardanova E.I., Gogoleva N.E., Ziganshin A.M. Comparison of intestinal bacterial and fungal communities across various xylophagous beetle larvae (Coleoptera: Cerambycidae) Sci. Rep. 2018;8:10073. doi: 10.1038/s41598-018-27342-z. PubMed DOI PMC

Weber M., Darzens D., Coulombel C., Foglietti M.J., Charas C. Purification and some properties of two amylases from Phoracantha semipunctata larvae. Comp. Biochem. Physiol. B. 1985;80:57–60. doi: 10.1016/0305-0491(85)90422-5. DOI

Patil N.K., Raut G.A., Gaikwand S.M. Activity of midgut amylase in Aeolesthes holosericea Fabricius (Coleoptera: Cerambycidae) J. Entomol. Zool. Stud. 2016;4:5–48.

Scrivener A.M., Watanabe H., Noda H. Diet and carbohydrate digestion in the yellowspotted longicorn beetle Psacothea hilaris. J. Insect Physiol. 1997;43:1039–1052. doi: 10.1016/S0022-1910(97)00063-2. PubMed DOI

Bian X., Shaw B.D., Han Y., Christeller J.T. Midgut proteinase activities in larvae of Anoplophora glabripennis (Coleoptera: Cerambycidae) and their interaction with proteinase inhibitors. Arch. Insect Biochem. Physiol. 1996;31:23–37. doi: 10.1002/(SICI)1520-6327(1996)31:1<23::AID-ARCH2>3.0.CO;2-Y. DOI

Johnson K.S., Rabosky D. Phylogenetic distribution of cysteine proteinases in beetles: Evidence for an evolutionary shift to an alkaline digestive strategy in Cerambycidae. Comp. Biochem. Physiol. B. 2000;126:609–619. doi: 10.1016/S0305-0491(00)00232-7. PubMed DOI

Torres-Castillo J.A., Aguirre-Mancilla C.L., Gutierréz-Diéz A., Sinagawa-García S.R., Torres-Acosta R.I., García-Zambrano E.A., Aguirre-Arzola V., Zavala-García F. Intestinal proteases of Moneilema armatum (Coleoptera: Cerambycidae) fed with Opunthia cladodes. Rev. Colomb. Entomol. 2015;41:249–256.

Kukor J.J., Martin M.M. Cellulose digestion in Monochamus marmorator Kby. (Coleoptera: Cerambycidae): Role of acquired fungal enzymes. J. Chem. Ecol. 1986;12:1057–1070. doi: 10.1007/BF01638996. PubMed DOI

Park D.S., Oh H.W., Jeong W.J., Kim H., Park H.Y., Bae K.S. A culture-based study of the bacterial communities within the guts on nine longicorn beetle species and their exo-enzyme producing properties for degrading xylan and pectin. J. Microbiol. 2007;45:394–401. PubMed

Chang C.J., Wu C.P., Lu S.C., Chao A.L., Ho T.H.D., Yu S.M., Chao Y.C. A novel exo-cellulase from white spottted longhorn beetle (Anoplophora malasiaca) Insect Biochem. Mol. Biol. 2012;42:629–636. doi: 10.1016/j.ibmb.2012.05.002. PubMed DOI

Pauchet Y., Kirsch R., Giraud S., Vogel H., Heckel D.G. Identification and characterization of plant cell wall degrading enzymes from three glycoside hydrolase families in the cerambycid beetle Apriona japonica. Insect Biochem. Mol. Biol. 2014;49:1–13. doi: 10.1016/j.ibmb.2014.03.004. PubMed DOI

Silva I. Morfologia do tubo digestivo da larva de Oncideres saga saga (Dalman, 1823) (Coleoptera, Cerambycidae) Acta Biol. Par. 1975;4:227–239. doi: 10.5380/abpr.v4i0.844. DOI

Silva I., Souza V.B.V. Ultrastructural aspects of the anterior mid gut of Oncideres saga saga (Dalman, 1823)—larva (Coleoptera, Cerambycidae) Rev. Bras. Entomol. S. P. 1981;25:103–112.

Haack R.A. Feeding biology of Cerambycids. In: Wang O., editor. Cerambycidae of the World; Biology and Pest Management. CRC Press Boca; Boca Raton, FL, USA: 2017. pp. 105–124.

Yi D.A., Kuprin A.V., Lee Y.H., Bae Y.J. Newly developed fungal diet for artificial rearing of the endangered long-horned beetle Callipogon relictus (Coleoptera: Cerambycidae) Entomol. Res. 2017;47:373–379. doi: 10.1111/1748-5967.12234. DOI

Lee S.G., Kim C., Choi I.J., Kuprin A.V., Lim J. A review of host plants of Callipogon (Eoxenus) relictus Semenov (Coleoptera: Cerambycidae: Prioninae), a Korea natural monument, with a new host, Quercus aliena Blume. J. Asia-Pac. Entomol. 2010;22:353–358. doi: 10.1016/j.aspen.2019.01.016. DOI

Edwards J.S. Observation on the ecology and behaviour of the Huhu beetle, Prionoplus reticularis White (Col. Ceramb.) Trans. R. Soc. N. Z. 1961;88:727–731.

Edwards J.S. On the reproduction of Prionoplus reticularis (Coleoptera: Cerambycidae), with general remarks on reproduction in the Cerambycidae. J. Cell. Sci. 1961;102:519–522.

Mansour K., Mansour-Bek J.J. On the digestion of wood by insects. J. Exp. Biol. 1933;11:243–256.

Benham G.S. Gross morphology and transformation of the digestive tract of Prionus laticollis (Coleoptera: Cerambycidae) Ann. Entomol. Soc. Am. 1970;63:1413–1419. doi: 10.1093/aesa/63.5.1413. DOI

Benham G.S.R., Farrar J. Notes on the biology of Prionus laticollis (Coleoptera: Cerambycidae) Can. Entomol. 1976;108:569–576. doi: 10.4039/Ent108569-6. DOI

Rodstein J., McElfresh J.S., Barbour J.D., Ray A.M., Hanks L.M., Millar J.G. Identification and synthesis of a female-produced sex pheromone for the cerambycid beetle Prionus californicus. J. Chem. Ecol. 2009;35:590–600. doi: 10.1007/s10886-009-9623-7. PubMed DOI

Kaiser A., Klok J., Socha J.J., Lee W.K., Quinlan M.C., Harrison J.F. Increase in tracheal investment with beetle size supports hypothesis of oxygen limitation on insect gigantism. Proc. Natl. Acad. Sci. USA. 2007;104:13198–13203. doi: 10.1073/pnas.0611544104. PubMed DOI PMC

Levine J.D., Sauman I., Imbalzano M., Reppert S.M., Jackson F.R. Period protein from the giant silkmoth Antheraea pernyi functions as a circadian clock element in Drosophila melanogaster. Neuron. 1995;15:147–157. doi: 10.1016/0896-6273(95)90072-1. PubMed DOI

Bernfeld P. Amylases, α and β. In: Colowick S.P., Kaplan N.O., editors. Methods in Enzymology. Volume 1. Academic Press; New York, NY, USA: 1955. pp. 49–58.

Kodrík D., Vinokurov K., Tomčala A., Socha R. The effect of adipokinetic hormone on midgut characteristics in Pyrrhocoris apterus L. (Heteroptera) J. Insect Physiol. 2012;58:194–204. doi: 10.1016/j.jinsphys.2011.11.010. PubMed DOI

Frugoni J.A.C. Tampone universale di Britton e Robinson a forza ionica costante. Gazz. Chim. Ital. 1957;87:403–407.

Elpidina E.N., Vinokurov K.S., Gromenko V.A., Rudenskaya Y.A., Dunaevsky Y.E., Zhuzhikov D.P. Compartmentalization of proteinases and amylases in Nauphoeta cinerea midgut. Arch. Insect Biochem. Physiol. 2012;48:206–216. doi: 10.1002/arch.10000. PubMed DOI

Roberts I.M. Hydrolysis of 4-methylumbelliferyl butyrate: A convenient and sensitive fluorescent assay for lipase activity. Lipids. 1985;20:243–247. doi: 10.1007/BF02534195. DOI

Folch J., Lees M., Stanley G.H.S. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957;226:497–509. PubMed

Tomčala. A., Kyselová V., Schneedorferová I., Opekarová I., Moos M., Urajová P., Kručinská J., Oborník M. Separation and identification of lipids in the photosynthetic cousins of Apicomplexa Chromera velia and Vitrella brassicaformis. J. Sep. Sci. 2017;40:3402–3413. PubMed

Appelqvist L.A. Rapid methods of lipid extraction and fatty acid methyl ester preparation for seed and leaf tissue with special remarks on preventing accumulation of lipid contaminants. Chem. Sci. 1968;28:551–570.

Williams D.M. Book of Insect Records. University of Florida; Gainesville, FL, USA: 2001. [(accessed on 21 June 2019)]. Chapter 30: Largest. Available online: http://entnemdept.ufl.edu/walker/ufbir/chapters/chapter_30.shtml.

Monné M.A. Catalogue of the Cerambycidae (Coleoptera) of the neotropical region. Part III. Subfamilies Parandrinae, Prioninae, Anoplodermatinae, Aseminae, Spondylidinae, Lepturinae, Oxypeltinae, and addenda to the Cerambycinae and Lamiinae. Zootaxa. 2006;1212:1–244. doi: 10.11646/zootaxa.1212.1.1. DOI

Shanbhag S.R., Müller B., Steibrecht R.A. Atlas of olfactory organs of Drosophila melanogaster. 1. Types, external organization, innervation and distribution of olfactory sensilla. Int. J. Insect Morphol. Embryol. 1999;28:377–397. doi: 10.1016/S0020-7322(99)00039-2. DOI

Altner H., Prillinger L. Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and its functional significance. Int. Rev. Cytol. 1980;67:69–139.

Altner H., Routil C., Loftus R. The structure of bimodal chemo-, thermo-, and hygroreceptive sensilla on the antenna of Locusta migratoria. Cell Tissue Res. 1981;215:289–308. doi: 10.1007/BF00239116. PubMed DOI

Hunger T., Steinbrecht R.A. Functional morphology of a double-walled multiporous olfactory sensillum: The sensillum coeloconicum of Bombyx mori (Insecta, Lepidoptera) Tissue Cell. 1998;30:14–29. doi: 10.1016/S0040-8166(98)80003-7. PubMed DOI

Steinbrecht R.A. Olfactory receptors. In: Eguchi E., Tominaga Y., editors. Atlas of Arthropod Sensory Receptors-Dynamic Morphology in Relation to Function. Springer Verlag; Tokyo, Japan: 1999. pp. 155–176.

Di Palma A., Pistillo M., Griffo R., Garonna A.P., Germinara G.S. Scanning electron microscopy of the antennal sensilla and their secretion analysis in adults of Aromia bungii (Faldermann, 1835) (Coleoptera, Cerambycidae) Insects. 2019;10:88. doi: 10.3390/insects10040088. PubMed DOI PMC

Schneider E.S., Römer H. Sensory structures on the antennal flagella of two katydid species of the genus Mecopoda (Orthoptera, Tettigonidae) Micron. 2016;90:43–58. doi: 10.1016/j.micron.2016.08.001. PubMed DOI

Weyda F., Štys P. Coxal setal organs of Machilidae and their homologues on the genitalia. Acta Entomol. Bohemoslov. 1974;71:51–52.

Eilers E.J., Talarico G., Hansson B., Hilker M., Reinecke A. Sensing the underground – ultrastructure and function of sensory organs in root-feeding Melolontha melolontha (Coleoptera: Scarabaeinae) larvae. PLoS ONE. 2012;7:e41357. doi: 10.1371/journal.pone.0041357. PubMed DOI PMC

Voigt D., Takanashi T., Tsuchihara K., Yazaki K., Kuroda K., Tsubaki R., Hosoda N. Strongest grip on the rod: Tarsal morphology and attachment of Japanese pine sawyer beetles. Zool. Lett. 2017;3:16. doi: 10.1186/s40851-017-0076-5. PubMed DOI PMC

Gorb E.V., Hosoda N., Miksch C., Gorb S.N. Slippery pores: Anti-adhesive effect of nanoporous substrates on the beetle attachment system. J. R. Soc. Interface. 2019;7:1571–1579. doi: 10.1098/rsif.2010.0081. PubMed DOI PMC

Bullock J.M.R., Federle W. Division of labour and sex differences between fibrillar, tarsal adhesive pads in beetles: Effective elastic modulus and attachment performance. J. Exp. Biol. 2009;212:1876–1888. doi: 10.1242/jeb.030551. PubMed DOI

Niederegger S., Gorb S., Jiao Y.K. Contact behaviour of tenent setae in attachment pads of the blowfly Calliphora vicina (Diptera, Calliphoridae) J. Comp. Physiol. A. 2002;187:961–970. doi: 10.1007/s00359-001-0265-7. PubMed DOI

Büscher T.H., Buckley T.R., Grohmann C., Gorb S.N., Bradler S. The evolution of tarsal adhesive microstructures in stick and leaf insects (Phasmatodea) Front. Ecol. Evol. 2018;6:1–11. doi: 10.3389/fevo.2018.00069. DOI

Chapman R.F. The Insects, Structure and Function. 4th ed. Cambridge University Press; Cambridge, UK: 1998. pp. 1–770.

Sehadová H., Šauman I., Sehnal F. Immunocytochemical distribution of pigment dispersing hormone in the cephalic ganglia of polyneopteran insects. Cell Tissue Res. 2003;312:113–125. doi: 10.1007/s00441-003-0705-5. PubMed DOI

Mitchell R.F., Hall L.P., Reagel P.F., McKenna D.D., Baker T.C., Hildebrand J.G. Odorant receptors and antennal lobe morphology offer a new approach to understanding the olfactory biology of the Asian longhorned beetle. J. Comp. Physiol. A. 2017;203:99–109. doi: 10.1007/s00359-016-1138-4. PubMed DOI PMC

Gokan N., Hosobuchi Y. Fine structure of the compound eyes of longicorn beetles (Coleoptera: Cerambycidae) Appl. Entomol. Zool. 1979;14:12–27. doi: 10.1303/aez.14.12. DOI

Wachmann E. Untersuchungen zur Feinstruktur der Augen von Bockka fern (Coleoptera, Cerambycidae) Zoomorphology. 1979;92:19–48. doi: 10.1007/BF00999833. DOI

Meyer-Rochow V.B., Mishra M. A six-rhabdomere, open rhabdom arrangement in the eye of the chrysanthemum beetle Phytoecia rufiventris: Some ecophysiological predictions based on eye anatomy. Biocell. 2009;33:115–120. PubMed

Crowson R.A. The Biology of the Coleoptera. Academic Press; New York, NY, USA: 1981. pp. 1–802.

Caveney S. The phylogenetic significance of ommatidium structure in the compound eye of polyphagan beetles. Can. J. Zool. 1986;64:1787–1819. doi: 10.1139/z86-270. DOI

Meyer-Rochow V.B. The dioptric system of beetle compound eyes. In: Horridge G.A., editor. The Compound Eye and Vision of Insects. Clarendon Press; Oxford, UK: 1975. pp. 299–313.

Mishra M., Meyer-Rochow V.B. Fine structure of the compound eye of the fungus beetle Neotriplax lewisi (Coleoptera, Cucujiformia, Erotylidae) Invertebr. Biol. 2006;125:265–278. doi: 10.1111/j.1744-7410.2006.00059.x. DOI

Jia L.P., Liang A.P. An apposition-like compound eye with a layered rhabdom in the small diving beetle Agabus japonicus (Coleoptera, Dytiscidae) J. Morphol. 2014;275:1273–1283. doi: 10.1002/jmor.20300. PubMed DOI

Niven J.E., Graham C.M., Burrows M. Diversity and evolution of insect nervous cord. Annu. Rev. Entomol. 2008;53:253–271. doi: 10.1146/annurev.ento.52.110405.091322. PubMed DOI

Crowson R.A. The phylogeny of Coleoptera. Annu. Rev. Entomol. 1960;5:111–134. doi: 10.1146/annurev.en.05.010160.000551. DOI

Calder A.A. The alimentary canal and nervous system of Curculionidae (Coleoptera): Gross morphology and systematic significance. J. Nat. Hist. 1989;23:1205–1265. doi: 10.1080/00222938900770671. DOI

Mohammadi H., Venkataraman Ramamurthy V., Subrahmanyam B. Configuration of nerve cord and characterization of brain neurosecretory cells in adult firefly, Luciola gorhami (Coleoptera: Lampyridae) J. Crop. Prot. 2016;5:179–187. doi: 10.18869/modares.jcp.5.2.179. DOI

Penteado-Dias A.M. Comparative study of the neural cord in the – Cerambycidae (Coleoptera) Rev. Bras. Entomol. 1984;28:223–243.

Snodgrass R.E. Principles of Insect Morphology. McGraw-Hill; New York, NY, USA: 1935. pp. 1–667.

Martin M.M. Invertebrate-Microbial Interactions. Ingested Fungal Enzymes in Arthropod Biology. Cornell University Press; Ithaca and London, UK: 1987. pp. 1–148.

Crook D.J., Prabhakar S., Oppert B. Protein digestion in larvae of the red oak borer Enaphalodes rufulus. Physiol. Entomol. 2009;34:152–157. doi: 10.1111/j.1365-3032.2008.00667.x. DOI

Sharifi M., Chitgar M.G., Ghadamyari M., Ajamhasani M. Identification and characterization of midgut digestive proteases from the rosaceous branch borer, Osphranteria coerulescens Redtenbacher (Coleoptera: Cerambycidae) Rom. J. Biochem. 2012;49:33–47.

Zibaee A. Digestive proteolytic profile in Stromatium fulvum Villers (Coleoptera: Cerambycidae) Rom. J. Biochem. 2014;51:17–30.

Canavoso L.E., Jouni Z.E., Karnas K.J., Pennington J.E., Wells M.A. Fat metabolism in insects. Annu. Rev. Nutr. 2001;21:23–46. doi: 10.1146/annurev.nutr.21.1.23. PubMed DOI

Howard R.W., Stanley-Samuelson D.W. Fatty acid composition of fat body and Malpighian tubules of the tenebrionid beetle, Zophobas atratus: Significance in eicosanoid-mediated physiology. Comp. Biochem. Physiol. B. 1996;115:429–437. doi: 10.1016/S0305-0491(96)00161-7. DOI

Tomčala A., Bártů I., Šimek P., Kodrík D. Locust adipokinetic hormone mobilizes diacylglycerols selectively. Comp. Biochem. Physiol. B. 2010;156:26–32. doi: 10.1016/j.cbpb.2010.01.015. PubMed DOI

Canavoso L.E., Frede S., Rubiolo E.R. Metabolic pathways for dietary lipids in the midgut of hematophagous Panstrongylus megistus (Hemiptera: Reduviidae) Insect. Biochem. Mol. Biol. 2004;34:845–854. doi: 10.1016/j.ibmb.2004.05.008. PubMed DOI

Stanley-Samuelson D.W., Jurenka R.A., Cripps C., Blomquist G.J., de Renobales M. Fatty acids in insects: Composition, metabolism, and biological significance. Arch. Insect Biochem. Physiol. 1988;9:1–33. doi: 10.1002/arch.940090102. DOI

Diefenbach L.M.G., Redaelli L.R., Gassen D.N. Characterization of the internal reproductive organs and their state as diapause indicator in Phytalus sanctipauli Blanchard, 1850 (Coleoptera, Scarabaeidae) Rev. Brasil. Biol. 1998;58:541–546. doi: 10.1590/S0034-71081998000300019. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...