Abstract
In most species of Gyrinidae, the immature stages are unknown, especially due to the difficulty in collecting the juveniles and assigning them to a particular species. Molecular association is a feasible technique that may solve this problem. Recent studies have used DNA sequence data, specifically the gene cytochrome oxidase subunit I (COI), to associate immature and adult stages, thus enabling the description of the former. The objectives of this study were (1) to describe and illustrate the immature stages of Gyrinus (Neogyrinus) rozei Ochs, 1953 including morphometric, chaetotaxic and bionomic information, and (2) to assess the usefulness of the gene COI to associate immatures and adults of Gyrinus. The studied specimens were collected in Roraima state, northern Brazil. The association of immature and adult stages was done either by rearing adults under laboratory conditions or by using DNA sequence data (COI). Eggs were described based on scanning electron microscopy; they are distinguished mainly by several features of chorion, micropyle and reticulation. Larvae of G. (N.) rozei can be distinguished from those of other Neotropical Gyrinidae by a combination of several characters, including the stipes with five robust hook-like additional setae on the dorsointernal margin, and the lacinia roughly hook-shaped. The pupa is similar to that of G. argentinus Steinhel, 1869, except for the number of setae on the body. The first record of the parasitoid wasp Melanosmicra sp. (Hymenoptera: Chalcididae) on a Gyrinus species is also provided.
References
Archangelsky, M. & Michat, M.C. (2007) Morphology and chaetotaxy of the larval stages of Andogyrus seriatopunctatus Régimbart (Coleoptera: Adephaga: Gyrinidae). Zootaxa, 1645, 19–33.
https://doi.org/10.11646/zootaxa.1645.1.2
Ashmead, W.H. (1904) Classification of the chalcid-flies of the superfamily Chalcidoidea, with descriptions of new species in the Carnegie Museum, collected in South America by Herbert H. Smith. Memoirs of the Carnegie Museum, 1, i–xi, 225–551.
Aube, C. (1838) Species général des Hydrocanthares et Gyriniens, par le docteur Ch. Aubé; pour faire suite au species general des Coléoptères de la collection de M. Le Comte Dejean. Mequignon Pere et fils, Libraires-editeurs, Paris, 803 pp.
Bachmann, A.O. (1961) Apuntes para una hidrobiología argentina. I. Andogyrus seriatopunctatus (Régimb.) en la Argentina. Descripción de la larva, pupa y capullo y observaciones biológicas (Coleopt. Gyrinidae. Enhydr.). Actas y Trabajos del Primer Congreso Sudamericano de Zoología, pp. 3–10.
Baker, G.T. & Wai, K. Ma. (1987) Chorionic structure of Dineutes hornii Rbts. (Coleoptera: Gyrinidae). Italian Journal of Zoology, 54, 209–212.
Bertrand, H. P. (1977) Gyrinidae. In: Larves et nymphes des coléoptères aquatiques du globe. pp. 203–204.
Boucek, Z. (1993) New taxa of North American Pteromalidae and Tetracampidae (Hymenoptera), with notes. Journal of Natural History 27, 1239–1313.
Brullé, M.A. (1835) Histoire Naturelle des Insectes. Vol. 5. Coléoptères. Vol. 2. F. D. Pillot, Paris, 436 pp.
Butcher, F.G. (1930) Notes on the cocooning habits of Gyrinus. J. Kansas Entomology. Society, 3, 64–66.
Čiampor, F. & Ribera, I. (2006) Hedyselmis opis: Description of the larva and its phylogenetic relation to Graphelmis (Coleoptera: Elmidae: Elminae). Journal of Entomology, 103, 627–636.
Colpani, D., Benetti, C.J., Hamada, N., Andrade-Souza, V. & Michat, M.C. (2018) Gyretes Brullé (Coleoptera: Gyrinidae) from Brazil: Morphology of eggs and early instars. Zootaxa, 4526 (3), 331–346.
https://doi.org/10.11646/zootaxa.4526.3.3
Costa, C., Vanin, S.A. & Casari-Chen, S.A. (1988) Gyrinidae. In: Larvas de Coleoptera do Brasil. Museu de Zoologia, Universidade de São Paulo, São Paulo, pp. 83–84.
Crespo, F.A. (1989a) Descripción de los estados preimaginales de Gyrinus (Oreogyrinus) argentinus Steinheil, 1869 (Coleoptera, Gyrinidae). Revista de la Sociedad Entomológica Argentina, 45, 163–172.
Crespo, F.A. (1989b) Descripción de los estados preimaginales de Neogyrinus ovatus (Aubé, 1838) comb. nov. (Coleoptera, Gyrinidae). Revista de la Sociedad Entomológica Argentina, 45, 237–240.
Curiel, J. & Morrone, J.J. (2012) Association of larvae and adults of Mexican species of Macrelmis (Coleoptera: Elmidae): a preliminary analysis using DNA sequences. Zootaxa, 3361, 56–62.
https://doi.org/10.11646/zootaxa.3361.1.5
Cushman, R.A. (1930) New parasitic Hymenoptera. Proceedings U.S. Natural Museum, 76 Art (25), 19 pp.
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–297.
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series, 41, 95–98.
Harris, R.A. (1979) A glossary of surface sculpturing. Occasional Papers in Entomology, California Department of Food and Agriculture, 28, 1–31.
Hebert, P.D.N., Cywinska, A., Ball, S. & Waard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B, Biological Sciences, 270, 313–321.
Geoffroy E.-L. (1762) Coleoptera, Gyrinidae. In: Histoire abrégée des insectes qui se trouvent aux environs de Paris, dans laquelle ces animaux sont rangés suivant un ordre méthodique. Durand, Paris, 523 pp. + 510 pl.
Gustafson, G.T. & Short, A.E.Z. (2017) Review of the whirligig beetle genus Gyrinus of Venezuela (Coleoptera: Gyrinidae). Acta Entomologica Musei Nationalis Pragae, 57 ( 2), 479–520.
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series, 41, 95–98.
Hatch, M.H. (1925) The phylogeny and phylogenetic tendencies of Gyrinidae. Paper of the Michigan Academy of Science, Arts and Letters, 5, 429–467.
Hillis, D.M. & Bull, J.J. (1993) An empirical test bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42, 182e192.
Kawada, R. & Buffington, M.L. (2016) A scalable and modular dome illumination system for scientific microphotography on a budget. PLoS ONE, 11 (5), e0153426.
https://doi.org/10.1371/journal.pone.0153426
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.
Komatsu, S., & Kobayashi, Y. (2012) Embryonic development of a whirligig beetle, Dineutus mellyi, with special reference to external morphology (Insecta: Coleoptera, Gyrinidae). Journal of morphology, 273, 541–560.
Laporte, F.L. de. (1834) Études entomologiques, ou description d’insectes nouveaux et observations sur leur synonymie. Par F. L. de Laporte Comte de Castelnau. Méquignon-Marvis, Paris, 94 pp + 2 pls.
Madaric, B.B., Stankovic, V.M., Corak, M., Ugarkovic, D. & Komarek, A. (2013) Contribution to molecular systematics of water scavenger beetles (Hydrophilidae, Coleoptera). Journal of Zoological Systematics and Evolutionary Research, 51, 165–171.
Michat, M.C., Archangelsky, M. & Fernández, L.A. (2010) Larval description and chaetotaxic analysis of Gyrinus monrosi Mouchamps, 1957 (Coleoptera: Gyrinidae). Koleopterologische Rundschau, 80, 1–14.
Michat, M., Alvarenga, T.M., Silva, M.S. & Alarie, Y. (2016) First larval description and chaetotaxic analysis of the neotropical whirligig beetle genus Enhydrus Laporte (Coleoptera, Gyrinidae). Revista brasileira de Entomologia, 60, 231–237.
Michat, M.C. & Gustafson, G.T. (2016) Larval morphology and chaetotaxy of Macrogyrus oblongus (Boisduval, 1835) (Coleoptera: Gyrinidae). Aquatic Insects, 37, 87–98.
Michat, M.C., Gustafson, G.T. & Bergsten, J. (2017) Larval morphology and chaetotaxy of Dineutus sinuosipennis Laporte, 1840, with a key for the identification of larvae of the tribe Dineutini (Coleoptera, Gyrinidae). ZooKeys, 718, 95–114.
Miller, K.B., Alarie, Y., Wolfe, G.W. & Whiting, M.F. (2005) Association of insect life stages using DNA sequences: The larvae of Philodytes umbrinus (Motschulsky) (Coleoptera: Dytiscidae). Systematic Entomology, 30, 499–509.
Miller, K.B., Alarie, Y. & Withing, M.F. (2007) Description of the larva of Notaticus fasciatus (Coleoptera: Dytiscidae) associated with adults using DNA sequence data. Annals of the Entomological Society of America, 100, 787–797.
Mouchamps R. (1957) Sur quelques Gyrinus de l’Amérique du Sud [Coleoptera Gyrinidae] (dixième note). Revue Française dʼEntomologie, 24, 244–252.
Nilsson, A.N. (1988) A review of primary setae and pores on legs of larval Dytiscidae (Coleoptera). Canadian Journal of Zoology, 66 (10), 2283–2294.
Noyes, J.S. (2019) Universal Chalcidoidea Database. World Wide Web electronic publication. [http://www.nhm.ac.uk/chalcidoids]
Oba, Y., Ôhira, H., Murase, Y., Moriyama, A. & Kumazawa, Y. (2015) DNA barcoding of Japanese click beetles (Coleoptera, Elateridae). PLoS ONE, 10 (1), e0116612.
Ochs, G. (1924) Über neue und interessante Gyriniden aus dem British Museum in London. Entomologische Blätter, 20, 228–244.
Ochs, G. (1935) Die brasilianische Artengruppe der Gattung Gyrinus, untergattung Neogyrinus Hatch. Revista de Entomologia, 5, 124-132.
Ochs G. (1953) Der jetzige Stand unserer Kenntnise über die Gyriniden-Fauna von Venezuela. Acta Biologica Venezuelica, 1, 181–208.
Ochs, G. (1965) Vierter Beitrag zur Kenntnis der Taumelkäfer des Amazonas-Gebiets (Col., Gyrinidae). Amazoniana, 1, 36–73.
Ochs, G. (1967) Fünfter Beitrag zur Kenntnis der Taumelkäfer des Amazonas-Gebiets (Col., Gyrinidae). Amazoniana, 1, 135–171.
Pentinsaari, M., Hebert, P.D. & Mutanen, M. (2014) Barcoding beetles: a regional survey of 1872 species reveals high identification success and unusually deep interspecific divergences. PLoS One, 9 (9), e108651.
Régimbart, M. (1882) Essai monographique de la famille des Gyrinidae. Annales de la Société Entomologique de France,VI, 2, 379–400.
Ruschka, F. (1914) No title - an account of aquatic Hymenoptera exhibited at meeting of 3th February 1914 ‘Wasserhymenopteren’. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 64, 206–209.
Saxod, R. (1964) L’oeuf, l’eclosion, la cuticle embryonnaire, et la larve neonate de Gyrinus substriatus Steph. Travaux Laboratoire Piscic.Université Grenoble, 56, 17–28.
Saxod, R. (1965) Larves et nymphes de quatre espéces françaises de Gyrinidae. Bulletin de la Société Entomologique de France, 90, 163–174.
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved Polymerase Chain Reaction primers. Annals of the Entomological Society of America, 87, 651–701.
Staudacher, K., Pitterl, P., Furlan, L., Cate, P.C. & Traugott, M. (2011) PCR-based species identification of Agriotes larvae. Bulletin of entomological research, 101 (2), 201–210.
Steinheil, E. (1869) Symbolae ad historiam Coleopterorum Argentiniae meridionalis, ossia elenco dei coleotteri raccolti dal parofessore Pellegrino Strobel, durante il suo soggiorno in Buenos Aires e mei viaggi di la intrepresi a Mendoza e nel Chili, indi a Bahia Blanca ed al Carmen de los Patagones; e descrizione delle specie nuove. Atti della Societa Italiana di Scienze Naturali e del Museo Civico di Storia Naturale in Milano, 12, 238–260.
Stephens, J.F. (1835) Illustrations of British entomology. Mandibulata, Vol. 5, London, pp. 366-440.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis. Molecular Biology and Evolution, 30, 2725–2729.
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.
Walker, F. (1833) Monographia Chalcidum. Entomology Monthly Magazine, 1, 115–142.
Wickham, H.F. (1894) On some aquatic larvae, with notice of their parasites. Canadian Entomologist, 26, 39–41.
Zaitsev, F.A. (1908) Uebersicht der paläarktischen Vertreter der Gattung Gyrinus (Linn.) Rég. (Coleoptera, Gyrinidae). Russkoe Entomologicheskoe Obozrenie, 7 (1907), 238–244.
Zhou, X., Kjer, K.M. & Morse, J.C. (2007) Associating larvae and adults of Chinese Hydropsychidae caddisflies (Insecta: Trichoptera) using DNA sequences. Journal of the North American Benthological Society, 26, 719–742.