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Morphological variability and teratologies in the stag beetle Lucanus cervus (Coleoptera: Lucanidae) from Romania

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Abstract

In the present study 423 Lucanus cervus individuals belonging to the entomological collection of the” Grigore Antipa” National Museum of Natural History (MNINGA) were checked for the presence of morphological differences and anomalies. Various malformations were identified in 16 specimens. This study also presents the first cases of bilateral symphysocery 2 + 3 and unilateral symphysocery 2 + 3 + 4 at the antennal clubs for L. cervus, as revealed by scanning electron microscopy. The teratological cases were more prevalent on the left rather than the right antenna (36.3% vs. 18.18%). The normal structural variations in L. cervus were classified as follows: different number of lamellate antennomeres of the antennal club, different number of pores on the last lamella and different shapes of the clypeus. More than 94% of the examined individuals had four antennomeres at the antennal club for both left and right antennae. The rounded shape (72%) with a uniporous sensilla (98%) of the last lamellate antennomere was the most common morph in the analysed samples. Among variations, V-shaped clypeus form was prevalent (37.3%) in L. cervus analysed males. Some structural modifications could have been caused by environmental factors producing alterations in the pupation or eclosion stages. For a better understanding of the causes of teratology and the presence of morphological changes in populations of L. cervus, further investigations are needed.

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Data Availability

All the samples are preserved in the MNINGA museum entomological collections.

References

  • Abdullah M, Abdullah A (1969) Abnormal elytra, wings and other structures in a female Trirhabda virgata (Chrysomelidae) with a summary of similar teratological observations in the Coleoptera. Deutsch Entomol Z 16:405–409. https://doi.org/10.1002/mmnd.19690160412

    Article  Google Scholar 

  • Antoine M (1912) Notes entomologiques. 1. Coléoptères anormaux. Bulletin de la Société Linnéenne du Nord de la France 41:175–183

    Google Scholar 

  • Asiain J, Marquez J (2009) New teratological examples in Neotropical Staphylinidae (Insecta: Coleoptera), with a compilation of previous teratological records. Rev Mex Biodiv 80:129–139

    Google Scholar 

  • Asmuss HM (1835) Monstrositates coleopterorum. Commentatio Pathologico-entomologica, Paris

    Google Scholar 

  • Balazuc J (1948) La Tératologie des Coléoptères et expériences de transplantation chez Tenebrio molitor L. Mémoires du Muséum National d’Histoire Naturelle (nouvelle série), Paris 25:1–193

  • Balazuc J (1952) Un Ergates faber L. gynandromorphe (Col. Cerambycidae). Bull Soc Entomol France 3:34–38

  • Balazuc J (1969) Supplément à la tératologie des Coléoptères. Redia 59:39–111

    Google Scholar 

  • Balbi E (1897) Difformitates et monstrositates Coleopterorum in collectione Balbii. Il Naturalista Siciliano 2:150–156

  • Bardiani M et al (2017) Guidelines for the monitoring of Lucanus cervus. J Nat Conserv 20:37–78 doi.org/10.3897/natureconservation.20.12687

    Article  Google Scholar 

  • Buckley D, Molnár V, Németh G, Petneházy O, Vörös J (2013) Monster… -omics: on segmentation, resegmentation, and vertebrae formation in amphibians and other vertebrates. Front Zool 10:17. https://doi.org/10.1186/1742-9994-10-17

    Article  PubMed  PubMed Central  Google Scholar 

  • Burke AF, Sole CL, Scholtz CH (2018) A remarkable teratological case for Eucymatodera parva Schenkling, 1908 (Cleridae: Tillinae) from Namibia. Afr Entomol 26:250–253. https://doi.org/10.4001/003.026.0250

    Article  Google Scholar 

  • Caruso D, Savini V (2012) Tres casos teratológicos de Gioia georgia en Choroní, Venezuela. Venezuela Entomotropica 27:89–91

    Google Scholar 

  • Chapman RF (1998a) The insects: structure and function. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Chapman RF (1998b) Mechanoreception. In: Chapman RF (ed) The insects: structure and function, 4th edn. Cambridge University Press, Cambridge, pp 610–652

    Chapter  Google Scholar 

  • Clark JT (1977) Aspects of variation in the stag beetle Lucanus cervus (L.) (Coleoptera: Lucanidae). Syst Entomol 2:9–16

    Article  CAS  Google Scholar 

  • Clark SM, Belo Neto LA (2010) A remarkable teratological specimen of Pseudoluperus longulus (Leconte) (Coleoptera: Chrysomelidae) from Utah, U. S. A. Coleopt Bull 64:383–385

    Article  Google Scholar 

  • Cox K, Thomaes A, Antonini G et al (2013) Testing the performance of a fragment of the COI gene to identify western Palaearctic stag beetle species (Coleoptera, Lucanidae). Zookeys 365:105–126. https://doi.org/10.3897/zookeys.365.5526

    Article  Google Scholar 

  • de Albuquerque NR, Arruda WS, Costa AS, Galharte RCV, Vargas LGH, Moreno IH (2010) A dicephalic yellow anaconda snake, Eunectes notaeus (Serpentes: Boidae), from southern Pantanal, Brazil. J Nat Hist 44:1989–1994. https://doi.org/10.1080/00222931003764105

    Article  Google Scholar 

  • de Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897. https://doi.org/10.1007/s10886-008-9485-4

    Article  CAS  PubMed  Google Scholar 

  • Della Beffa D (1990) Casi di teratologia in alcune specie di Coleotteri Lucanidi. Riv Coleott Ital 7:135

    Google Scholar 

  • Dziengo-Czaja M, Koss J, Matuszak A (2008) Teratological forms of diatoms (Bacillariophyceae) as indicators of water pollution in the western part of Puck Bay (southern Baltic Sea). Oceanol Hydrobiol Stud 37:119–132. https://doi.org/10.2478/v10009-007-0042-1

    Article  Google Scholar 

  • Fernández-Álvarez FA, Recuero E, Martínez-Solano I, Buckley D (2011) First record of bicephaly in Lissotriton boscai (Amphibia, Caudata, Salamandridae). North-West J Zool 7:161–163

    Google Scholar 

  • Ferrer J, Fernández-López J, González AF, Menéndez DF, Torralba-Burrial A (2014) Unusual teratology for a Tenebrionid: antennal Schistomelia in Probaticus granulatus (Allard, 1876) (Coleoptera: Tenebrionidae). Coleopt Bull 68:139–142 https://www.jstor.org/stable/24773302

    Article  Google Scholar 

  • Fremlin M (2013) Results of the “stag beetle ‘larval incidents’ in private gardens” survey. Essex Naturalist (New Series) 30:94–106

    Google Scholar 

  • Friedrich F, Matsumura Y, Pohl H, Bai M, Hörnschemeyer T, Beutel RG (2014) Insect morphology in the age of phylogenomics: innovative techniques and its future role in systematics. Entomol Sci 17:1–24. https://doi.org/10.1111/ens.12053

    Article  Google Scholar 

  • Frolov AV, Akhmetova LA (2016) Revision of the subgenus Orphnus (Phornus) (Coleoptera, Scarabaeidae, Orphninae). Eur J Taxon 241:1–20. https://doi.org/10.5852/ejt.2016.241

    Article  Google Scholar 

  • Gadeau de Kerville H (1886) Séance du 24 novembre 1886. Annales de la Société Entomologique de France 6:CLXXIX-CLXXX

  • Gamboa RF, Garzón A (2009) Primer registro de Lucanus cervus (Linné, 1758) f. pontbrianti (Mulsant, 1839) (Coleoptera: Lucanidae) para la Península Ibérica. Boletín de la Sociedad Entomológica Aragonesa 44:533–534

  • Gasca-Álvarez HJ, Deloya C, Reyes-Castillo P (2016) Teratological cases in five species of Cotinis Burmeister (Coleoptera: Scarabaeidae: Cetoniinae: Gymnetini), with a compilation of teratologies in Scarabaeoidea. Coleopt Bull 71:329–338. https://doi.org/10.1649/0010-065X-71.2.329

    Article  Google Scholar 

  • Gerard M, Layet V, Costa T, Roumazeilles Y, Chenal P, Cailliez D, Gerard B (2012) Sirenomelia and caudal malformations in two families. Am J Med Genet A 158A:1801–1807. https://doi.org/10.1002/ajmg.a.35408

    Article  PubMed  Google Scholar 

  • Ghannem S, Zrelli S, Boumaiza M (2015) New teratological record in Carabidae (Insecta: Coleoptera) from Tunisia. Arquivos Entomolóxicos 14:127–129

    Google Scholar 

  • Hendriks P (2011) De ondergrondse metamorfose van het Vliegend hert. De Levende Natuur 112:27–28

  • Hendriks P, Fremlin M (2012) How stag beetle Lucanus cervus larvae pupate. http://maria.fremlin.de/stagbeetles/pupation/pupation_captivity.html. Accesed 15 Dec 2007

  • Huang JP, Lin CP (2010) Diversification in subtropical mountains: Phylogeography, Pleistocene demographic expansion, and evolution of polyphenic mandibles in Taiwanese stag beetle, Lucanus formosanus. Mol Phylogenet Evol 57:1149–1161. https://doi.org/10.1016/j.ympev.2010.10.012

    Article  PubMed  Google Scholar 

  • Kalter H (2003) Teratology in the 20th century: environmental causes of congenital malformations in humans and how they were established. Neurotoxicol Teratol 25:131–282. https://doi.org/10.1016/j.ntt.2003.09.002

    Article  CAS  PubMed  Google Scholar 

  • Keil TA (1999) Morphology and development of the peripheral olfactory organs. In: Hansson BS (ed) Insect olfaction. Springer, Berlin, pp 5–47

    Chapter  Google Scholar 

  • Kizub IV, Leshchenko MV (2019) New cases of teratology in Lucanidae and Geotrupidae (Coleoptera: Scarabaeoidea) from the Palearctic region. Munis Entomol Zool 14:108–112

  • Klimaszewski J, Watt JC (1997) Coleoptera: family–group review and keys to identification. In: Duval CT (ed) Fauna of New Zealand, vol 37. Manaaki Whenua Press, New Zealand, pp 1–199

    Google Scholar 

  • Lacroix JP (1969) Contribution à l'étude des Lucanides - A propos de Lucanus cervus récoltés au Bois de Boulogne. L'Entomologiste 25:119–129

  • Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. Holmiae [= Stockholm]: L. Salvii, pp 1– 824

  • Mocquerys S (1880) Recueil de Coléoptères anormaux par feu M. S. Mocquerys avec introduction par M. J. Bourgeois, Rouen

    Google Scholar 

  • Monty J (1974) Teratological effects of the virus Rhabdionvirus oryctes on Oryctes rhinoceros (L.) (Coleoptera, Dynastidae). Bull Entomol Res 64:633–636. https://doi.org/10.1017/S0007485300035926

    Article  Google Scholar 

  • Narita S, Pereira RAS, Kjellberg F, Kageyama D (2010) Gynandromorphs and intersexes: potential to understand the mechanism of sex determination in arthropods. Terr Arthropod Rev 3:63–69. https://doi.org/10.1163/187498310X496190

    Article  Google Scholar 

  • Nazarenko VY (2014) Morphological anomalies in Molytinae weevils (Coleoptera, Curculionidae). Ukr Entomol J 1:69–72. https://doi.org/10.3897/zookeys.714.21112

  • Nowak-Chmura M (2012) Teratological changes in tick morphology in ticks feeding on exotic reptiles. J Nat Hist 46(15–16):911–921. https://doi.org/10.1080/00222933.2011.651635

    Article  Google Scholar 

  • Nowińska A, Brożek J (2017) Morphological study of the antennal sensilla in Gerromorpha (Insecta: Hemiptera: Heteroptera). Zoomorphology 136:327–347. https://doi.org/10.1007/s00435-017-0354-y

    Article  PubMed  PubMed Central  Google Scholar 

  • Nowińska A, Brożek J (2019) Antennal sensory structures in water bugs of Nepoidea (Insecta: Hemiptera: Nepomorpha), their morphology and function. Zoomorphology 138:307–319. https://doi.org/10.1007/s00435-01900446-4

    Article  Google Scholar 

  • Olsen RG (1977) Insect teratogenesis in a standing-wave irradiation system. Radio Sci 12:199–207. https://doi.org/10.1029/RS012i06Sp00199

    Article  Google Scholar 

  • Olsen RG (1982) Constant-dose microwave irradiation of insect pupae. Radio Sci 17:145S–148S. https://doi.org/10.1029/RS017i05Sp0145S

    Article  Google Scholar 

  • Ortuño VM, Hernández JM (1993) Several teratological cases in Coleoptera. Bol R Soc Esp Hist Nat Secc Biol 89:163–179

  • Ortuño VM, Ramos Abuin JA (2008) Reflexiones sobre la teratología y descripciones de cuatro teratosis apendiculares en Coleoptera. Boletín de la Sociedad Entomológica Aragonesa 43:435–439

  • Osuna E (1992) Fenómeno teratológico en Psalidognathus sp. (Coleoptera: Cerambycidae). Bol Entomol Venez 7:145–156

    Google Scholar 

  • Planet LM (1896) Note sur deux Lucanus cervus anomaux. Bull Soc Entomol France 6:168–169

  • Proches Ş (1997) Stag beetles (Lucanidae, Coleoptera) of Romania a biogeographical and ecological review. In: Analele Universităţii Bucureşti, XLVI. Biologie, Bucuresti, pp 99–104

    Google Scholar 

  • Romiti F, Redolfi DL, Piras P, Carpaneto GM (2016) Shape variation of mandible and head in Lucanus cervus (Coleoptera: Lucanidae): a comparison of morphometric approaches. Biol J Linn Soc Lond 120:836–851. https://doi.org/10.1093/biolinnean/blw001

    Article  Google Scholar 

  • Savini V, Furth D (2004) Teratología en Coleoptera: un caso en Gioia bicolor (Blake 1969) (Chrysomelidae, Alticinae) de Jamaica. Entomotropica 19:165–167

    Google Scholar 

  • Schneider D (1964) Insect antennae. Annu Rev Entomol 9:103–122

    Article  Google Scholar 

  • Schulz UH, Martins-Junior H (2001) Astyanax fasciatus as bioindicator of water pollution of Rio dos Sinos, RS, Brazil. Braz J Biol 61:615–622. https://doi.org/10.1590/S1519-69842001000400010

    Article  CAS  PubMed  Google Scholar 

  • Solano E, Thomaes A, Cox K et al (2016) When morphological identification meets genetic data: the case of Lucanus cervus and L. tetraodon (Coleoptera, Lucanidae). J Zool Syst Evol Res 54:197–205. https://doi.org/10.1111/jzs.12124

    Article  Google Scholar 

  • Taboada-Verona C, Faúndez EI, Sierra-Serrano O (2016) Reporte de un caso teratológico en Pelidnota polita Latreille, 1812 (Coleoptera: Scarabaeidae: Rutelinae) en Colombia. Boletín de la Sociedad Entomológica Aragonesa 59:303–304

  • Vermeulen AC (1995) Elaborating chironomid deformities as bioindicators of toxic sediment stress: the potential application of mixture toxicity concepts. Ann Zool Fenn 32:265–285

    Google Scholar 

  • Vitali F (2007) Anomalies multiples chez un exemplaire tératologique d’ Acanthinodera cumingii (Hope, 1833) (Coleoptera: Cerambycidae). L’Entomologiste 63:79–80

    Google Scholar 

  • Wagner CM, Rice PH, Pease AP (2013) First record of dicephalia in a bull shark Carcharhinus leucas (Chondrichthyes: Carcharhinidae) foetus from the Gulf of Mexico. U.S.A J Fish Biol 82:1419–1422. https://doi.org/10.1111/jfb.12064

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Guan L, Ren B (2011) Fine structure and distribution of antennal sensilla of longicorn beetles Leptura arcuata and Leptura aethiops (Coleoptera: Cerambycidae). Ann Entomol Soc Am 104:778–787. https://doi.org/10.1603/AN10188

    Article  Google Scholar 

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Acknowledgments

The author would like to thank Ionut Iorgu, Scientific Researcher, “Grigore Antipa” National Museum of Natural History, for his kind help in photographing the specimens and for the help in processing the photos. We are also grateful to Andrei Ștefan, Scientific Researcher, “Grigore Antipa” National Museum of Natural History, for the editing of the map of the study areas. We also thank Tiberiu Sahlean, Scientific Researcher, “Grigore Antipa” National Museum of Natural History, for his advice in certain aspects of using Photoshop 10.1 (Adobe Systems, Mountain View, CA, USA) and for the help in processing the photos.

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  1. “Grigore Antipa” National Museum of Natural History, Şos. Kiseleff no. 1, 011341, Bucharest, Romania

    Alexandra-Florina Popa, Rozalia Magda Motoc, Elena Iulia Iorgu & Luis Ovidiu Popa

  2. Faculty of Biology, University of Bucharest, Splaiul Independentei 91-95, R-050095, Bucharest, Romania

    Alexandra-Florina Popa & Marieta Costache

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  1. Alexandra-Florina Popa
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All authors contributed to the study conception and design. Material preparation and data collection: Alexandra-Florina Popa and Rozalia Magda Motoc. Analysis were performed by Alexandra-Florina Popa, Rozalia Magda Motoc and Elena-Iulia Iorgu. The first draft of the manuscript was written by Alexandra-Florina Popa and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Alexandra-Florina Popa.

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Popa, AF., Motoc, R.M., Iorgu, E.I. et al. Morphological variability and teratologies in the stag beetle Lucanus cervus (Coleoptera: Lucanidae) from Romania. Biologia 76, 2181–2193 (2021). https://doi.org/10.1007/s11756-021-00685-1

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