The last instar larva and pupa of Eucoeliodes mirabilis (A. Villa & G. B. Villa, 1835) (Curculionidae: Ceutorhynchini) are described using drawings and SEM images and are compared and keyed with already described larvae of 58 other ceutorhynchinae taxa. The larval body has an effective combination of morphological adaptations that assist a unique biological defensive strategy. All larval stages of E. mirabilis feed ectophytically on leaves of Euonymus europaeus L. (Celastraceae), and the larval body is covered with a thick faecal shield. The fixation of this protective shield on the larval back is performed by a peculiar dorsal microsculpture composed of a dense carpet of microtrichia on the thorax and abdomen, which serves effectively as a velcro system. Because of this strategy, macrosetae on the larval and pupal body of E. mirabilis are completely reduced. Larvae of E. mirabilis also have distinct morphological adaptations for protecting the spiracles against intrusion of faeces and avoiding occlusion of the tracheal system: a) microtrichia around spiracles are slightly shorter, distinctly stronger and are arranged with high-density and in clusters and b) spiracles are protected by an external safety valve. This strategy of E. mirabilis larvae is unique, although somewhat similar to that of Criocerinae and Blepharida-group leave beetles (Galerucinae) (both Coleoptera: Chrysomelidae), but with distinctly different morphological adaptations.

Administration of Podyji National Park Znojmo Czech Republic

Department of Ecology and Environmental Sciences Faculty of Science Palacký University Olomouc Olomouc Czech Republic

Department of Science University Roma Tre Rome Italy

Group Function of Invertebrate and Plant Biodiversity in Agro Ecosystems Crop Research Institute Praha 6 Ruzyně Czech Republic

See more in PubMed

Price PW, Denno RF, Eubanks MD, Finke DL. Insect ecology: Behavior, populations and communities. Cambridge University Press, Cambridge; 2011.

Ruxton GD, Sherratt TN, Speed MP. Avoiding attack. Oxford University Press, New York; 2004.

Weiss M. Defecation behavior and ecology of insects. Annu Rev Entomol. 2006; 51: 635–661. 10.1146/annurev.ento.49.061802.123212 PubMed DOI

Eisner T, Tassel E, Carrel JE. Defensive use of ‘fecal shield’ by a beetle larva. Science 1967; 158: 1471–1473. PubMed

Root RB, Messina FJ. Defensive adaptations and natural enemies of a case bearing beetle,

Damman H, Cappuccino N. Two forms of defence in a chrysomelid beetle: egg clumping and excrement cover. Ecol Entomol. 1991; 16: 163–167.

Olmstead KL. Waste products as chrysomelid Defences In: Jolivet PH, Cox ML, Petitpierre E, editors. Novel Aspects of the Biology of Chrysomelidae. Kluver Academic Publishers, Dordrecht; 1994. pp. 311–318.

Morton TC, Vencl FV. Larval leaf beetles form a defense from recycled host plant chemicals discharged in fecal wastes. J Chem Ecol. 1998; 24: 765–786.

Vencl FV, Morton TC. Macroevolutionary aspects of larval shield defences In: Cox ML, editor. Advances in Chrysomelidae Biology. Volume 1 Backhuys, Leiden; 1999. pp. 217–238.

Nogueira-de-Sa´ F. Defensive strategies of two cassidine larvae: the role of fecal shields and chemical substances. Chrysomela Newsletter 2004; 43: 6–8.

Nogueira-de-Sa´ F, Trigo JR. Do fecal shields provide physical protection to larvae of the tortoise beetles

Nogueira-de-Sa´ F, Trigo JR. Fecal shield of the tortoise beetle

Chaboo CS, Grobberlaar E, Larsen A. Fecal Ecology in Leaf Beetles: Novel Records in the African Arrow-Poison Beetles,

Chaboo CS, Brown CG, Funk DJ. Faecal case architecture in the gibbosus species group of

Borowiec L, Świętojańska J. 2.7.2 Cassdinae Gyllenhal, 1813 In: Leschen RAB, Beutel RG, editors. Handbook of Zoology, Arthropoda: Insecta, Coleoptera, Beetles. Volume 3: Morphology and Systematics (Phytophaga). Walter de Gruyter, Berlin/Boston; 2014. pp. 198–217.

Chamorro ML. 2.7.4 Lamprosomatinae Lacordaire, 1848 In: Leschen RAB, Beutel RG, editors. Handbook of Zoology, Arthropoda: Insecta, Coleoptera, Beetles. Volume 3: Morphology and Systematics (Phytophaga). Walter de Gruyter, Berlin/Boston; 2014. pp. 226–230.

Chamorro ML. 2.7.5 Cryptocephalinae Gyllenhal, 1813 In: Leschen RAB, Beutel RG, editors. Handbook of Zoology, Arthropoda: Insecta, Coleoptera, Beetles. Volume 3: Morphology and Systematics (Phytophaga). Walter de Gruyter, Berlin/Boston; 2014. pp. 230–236.

Vencl FV, Leschen RAB. 2.7.6 Criocerinae Latreille, 1807 In: Leschen RAB, Beutel RG, editors. Handbook of Zoology, Arthropoda: Insecta, Coleoptera, Beetles. Volume 3: Morphology and Systematics (Phytophaga). Walter de Gruyter, Berlin/Boston; 2014. pp. 237–242.

Agrain FA, Buffington ML, Chaboo CS, Chamorro ML, Scholler MS. Leaf beetles are ant-nest beetles: the curious life of the juvenile stages of case-bearers (Coleoptera, Chrysomelidae, Cryptocephalinae). ZooKeys. 2015; 547: 133–164. PubMed PMC

Chaboo CS, Chamorro-Lacayo L, Schöller M. Catalog of known immature stages of Camptosomate leaf beetles (Coleoptera: Chrysomelidae: Cryptocephalinae and Lamprosomatinae). Proc Entomol Soc Wash. 2016; 118(2): 150–217.

Vencl FV, Nogueira-de-Sá F, Allen BJ,Windsor DM, Futuyma DJ. Dietary specialization influences the efficacy of larval tortoise beetle shield defenses. Oecologia 2005; 145: 404–414. 10.1007/s00442-005-0138-9 PubMed DOI

Vencl FV, Gómez NE, Ploss K, Boland W. The chlorophyll catabolite, pheophorbide PubMed DOI PMC

Keefover-Ring K. Making scents of defense: do fecal shields and herbivore-caused volatiles match host plant chemical profiles? Chemoecology. 2013; 23: 1–11.

Prathapan KD, Chaboo CS. Biology of Blepharida-group flea beetles with first notes on natural history of PubMed PMC

Aiello A, Vencl FV. One plant, two herbivore strategies:

Colonnelli E. Ceutorhynchinae In: Löbl I, Smetana A, editors. Catalogue of Palaearctic Coleoptera, Vol. 8 Brill, Leiden; 2013. pp. 176–214.

Smreczyński S. Podrodziny Curculioninae. Klucze do oznaczania owadów Polski; Cz. XIX: Coleoptera. Zeszyt 98e: Curculionidae. Państwowe Wydawnictwo Naukowe, Warszawa; 1974. (in Polish).

Lohse GA. Unterfamilie Ceutorhynchinae In: Freude H, Harde KW, Lohse GA, editors. Die Käfer Mitteleuropas. Vol. 11 Goecke & Evers, Krefeld: 11; 1983. pp. 180–253.

Colonnelli E. Catalogue of Ceutorhynchinae of the World, with a key to Genera (Insecta, Coleoptera, Curculionidae). Argania editio, Barcelona; 2004.

Stüben PE, Müller G, Krátký J, Bayer Ch, Behne L, Sprick P. Digital-Weevil-Determination der westpaläarktischen Curculionoidea: Transalpina: Ceutorhynchinae (2. Teil). (Ceuthorhynchini: Amalorrhynchus, Drupenatus, Poophagus, Coeliodes, Pseudocoeliodes, Coeliodinus, Eucoeliodes, Neoxyonyx, Thamiocolus, Micrelus, Zacladus, Phrydiuchus, Stenocarus, Nedyus, Ceutorhynchus: Marklissus). Snudebiller 2013; 14(209): 1–24.

Podlussány A Curculionoidea (Coleoptera) of Örség Landscape Conservation Area. In: Vig K, editor. Natural History of Örség Landscape Conservation Area II. Savaria Múzeum, Szombathely, 23/2 (Pars historico-naturalis); 1996. pp. 203–273.

Oberprieler RG, Anderson RS, Marvaldi AE. 3 Curculionoidea Latreille, 1802: Introduction, Phylogeny In: Leschen RAB, Beutel RG, editors. Handbook of Zoology, Arthropoda: Insecta, Coleoptera, Beetles. Volume 3: Morphology and Systematics (Phytophaga). Walter de Gruyter, Berlin/Boston; 2014. pp. 285–300.

May BM. An introduction to the immature stages of Australian Curculionoidea In: Zimmerman EC, editor. Australian weevils (Coleoptera: Curculionidae). Vol, 2 CSIRO, Melbourne; 1994. pp. 533–535.

Marvaldi AE, Sequeira AS, Brien CW, Farrell BD. Molecular and morphological phylogenetics of weevils (Coleoptera, Curculinoidea): do nitche shifts accompany diversification? Syst Biol. 2002; 51: 761–785. 10.1080/10635150290102465 PubMed DOI

Marvaldi AE. Key to larvae of the South American subfamilies of weevils (Coleoptera, Curculinoidea). Rev Chil Hist Nat. 2003; 76: 603–612.

Scherf H. Die Entwicklungstadien der Mittleeuropäischen Curculioniden (Morphologie, Bionomie, Ökologie). Abh Seckenb Naturforsch Ges. 1964; 506: 1–335.

May BM. Immature stages of Curculionidae: larvae of soil dwelling weevils of New Zealand. J R Soc N Z. 1977; 72: 189–228.

Marvaldi AE. Larvae of Entiminae (Coleoptera: Curculionidae): Tribal diagnoses and phylogenetic key, with a proposal about natural groups within Entimini. Entomol Scand. 1998; 29: 89–98.

Marvaldi AE. Morfología larval en Curculionidae (Insecta: Coleoptera). Acta Zool Lilloana 1999; 45(1): 7–24.

Marvaldi AE, Lanteri AA, Guadalupe del Río M, Oberprieler RG. 3.7.5 Entiminae Schoenherr, 1823 In: Leschen RAB, Beutel RG, editors. Handbook of Zoology, Arthropoda: Insecta, Coleoptera, Beetles. Volume 3: Morphology and Systematics (Phytophaga). Walter de Gruyter, Berlin/Boston; 2014. pp. 503–522.

Oberprieler RG, Marvaldi AE, Anderson RS. Weevils, weevils, weevils everywhere. Zootaxa. 2007; 1668: 491–520.

Oberprieler RG. 3.7.4 Cyclominae Schoenherr, 1826 In: Leschen RAB, Beutel RG, editors. Handbook of Zoology, Arthropoda: Insecta, Coleoptera, Beetles. Volume 3: Morphology and Systematics (Phytophaga). Walter de Gruyter, Berlin/Boston; 2014. pp. 483–502.

Gunter NL, Oberprieler RG, Cameron SL. Molecular phylogenetics of Australian weevils (Coleoptera: Curculionoidea): exploring relationships in a hyperdiverse lineage through comparison of independent analyses. Aust Entomol. 2016; 55(2): 217–233.

Oberprieler RG, Caldara R, Skuhrovec J. 3.7.2 Bagoini Thomson, 1859; Gonipterini Lacordaire, 1863; Hyperini Marseul, 1863 In: Leschen RAB, Beutel RG, editors. Handbook of Zoology, Arthropoda: Insecta, Coleoptera, Beetles. Volume 3: Morphology and Systematics (Phytophaga). Walter de Gruyter, Berlin/Boston; 2014. pp. 452–476.

Skuhrovec J, Bogusch P. The morphology of the immature stages of PubMed PMC

Costa JT, Fitzgerald TD, Pescador-Rubio A, Mays J, Janzen DH. Social Behavior of Larvae of the Neotropical Processionary Weevil

Gosik R, Sprick P, Skuhrovec J, Deruś M, Hommes M. Morphology and identification of the mature larvae of several species of the genus PubMed DOI

Räther M. Notes on four weevils in the tribe Cionini (Coleóptera: Curculionidae) associated with

Dieckmann L. Beiträge zur Insektenfauna der DDR: Coleoptera—Curculionidae: Ceutorhynchinae. Beitr Entomol. 1972; 22: 3–128.

Cunningham P. Biology of

Prena J, Colonnelli E, Hespenheide HA. 3.7.9 Conoderinae Schoenherr, 1833 In: Leschen RAB, Beutel RG, editors. Handbook of Zoology, Arthropoda: Insecta, Coleoptera, Beetles. Volume 3: Morphology and Systematics (Phytophaga). Walter de Gruyter, Berlin/Boston; 2014. pp. 577–588.

Wanat M. New records on larval exophagy in the subfamilies Bagoinae and Ceutorhynchinae (Coleoptera: Curculionidae). Weevil News 2011; 67: 1–5.

Tzanakakis ME. The biology of

Lawson FA. Chrysomelidae (Chrysomelioidea) (= Cassididae, Cryptocephalidae, Megalopodidae, Sagridae, etc.) In: Stehr FW, editor. Immature Insects. Volume 2 Kendall,/Hunt Publishing company, Iowa; 1992. pp. 568–585.

Miller F. Zemědělská entomologie. ČSAV, Praha, 1956. (in Czech).

Anderson DM. A review of the known larvae and pupae of the genus

Anderson DM. Curculionidae (broad sense) (Curculionoidea) In: Stehr FW, editor. Immature Insects. Volume 2 Kendall,/Hunt Publishing company, Iowa; 1992. pp. 594–612.

Vayssieres J-F. The Immature Stages of Two

May BM. Fauna of New Zealand, 28 Larvae of Curculionoidea (Insecta: Coleoptera): a systematic overview. Manaaki Whenua Press, Lincoln, New Zealand; 1993.

Lee C-Y, Morimoto K. Larvae of the Weevil Family Curculionidae of Japan: Part 4. Ceutorhynchinae to Molytinae (Insecta: Coleoptera). J Fac Agr, Kyushu Univ. 1996; 40 (3–4): 307–331.

Orlova-Bieńkowskaya MJ. Immature stages and biology of the freshwater weevil

Gosik R. Comparative morphology of the development stages of Poophagus hopffgarteni Tournier, 1873 and P. sisymbrii (Fabricius, 1776), with comments on their biology (Coleoptera: Curculionidae). Genus 2008; 19 (1): 103–112.

Gosik R. Description of the larva and pupa of

Gosik R. Description of the mature larvae of four species of the genus

Nikulina ON. Larval Morphology of the Weevil Genus

Stejskal R, Trnka F, Skuhrovec J. Biology and morphology of immature stages of

Skuhrovec J, Gosik R, Caldara R. Immatures of Palaearctic species of the weevil genus PubMed DOI

Trnka F, Stejskal R, Skuhrovec J. Biology and morphology of immature stages of PubMed DOI

Skuhrovec J, Gosik R, Caldara R, Košťál M. Immatures of Palaearctic species of the weevil genus PubMed DOI