Identification based on morphological and molecular characters of Phassus huebneri (Geyer) (Lepidoptera: Hepialidae), a ghost moth feeding on blackberry in Michoacán, Mexico: its biology and parasitoids-Reference-Cited by-同舟云学术

Identification based on morphological and molecular characters of Phassus huebneri (Geyer) (Lepidoptera: Hepialidae), a ghost moth feeding on blackberry in Michoacán, Mexico: its biology and parasitoids

Published:2022-12-05 Issue:4 Volume:5214 Page:496-506
ISSN:1175-5334
Container-title:Zootaxa
language:
Short-container-title:Zootaxa

Author:

ESQUIVEL-AYALA BLANCA A.^ORCID,MARTÍNEZ ANA M.^ORCID,ZAMORA NORMA^ORCID,RAMOS-ORTIZ SELENE^ORCID,MIELKE CARLOS C. G.^ORCID,FIGUEROA JOSÉ I.^ORCID,SILVA-ROJAS HILDA V.^ORCID,REBOLLAR-ALVITER ÁNGEL^ORCID,VALDEZ JORGE M.^ORCID,PINEDA SAMUEL^ORCID

Abstract

Larvae of an unidentified Lepidopteran hepialid were found boring stems and crown roots of blackberry (Rubus sp.) in Michoacán, Mexico. In this study, the morphological and molecular identification of larvae and adults of this insect was performed. Preliminary aspects of biology, including information on parasitoids associated to larval stage, are also recorded. A total of 109 larvae of various instars were collected and three were reared to adult. The two females and one male were identified as Phassus huebneri (Geyer) (Lepidoptera: Hepialidae) following morphological characters. This identification was corroborated by comparing the cytochrome oxidase I (COI) barcode of two field-collected larvae (IIAFL1 and IIAFL2) with sequences of Phassus spp. obtained from GenBank. A Neighbor-Joining similarity analysis yielded a phenogram with two subclades. The first subclade grouped the IIAFL1 and IIAFL2 sequences with two other Mexican sequences categorized as P. huebneri, whereas in the second subclade other species belonging to the genus Phassus from Guatemala and Costa Rica were grouped together. Larval development of nine instars took about 14 months. Larvae reached a maximum length of 10 cm. The pupal stage lasted 39–41 days. Each of the two females laid over 1,000 unfertilized eggs within a period of 48 h. Larvae were parasitized by Dinera grisescens Fallen (Diptera: Tachinidae) and another unidentified Dinera sp. This study provides additional evidences on the distribution pattern of P. huebneri in western Mexico and presents the first record of this species feeding on one of the most economically important crops in Mexico.

Publisher

Magnolia Press

Subject

Animal Science and Zoology,Ecology, Evolution, Behavior and Systematics

Reference2 articles.

Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402. https://doi.org/10.1093/nar/25.17.3389
Arguedas-Gamboa, M. & Rodríguez-Solís, M. (2015) Insectos barrenadores del xilema en especies forestales comerciales en Costa Rica. Revista Mexicana de Ciencias Forestales, 7 (35), 79–89. https://doi.org/10.29298/rmcf.v7i35.76
Bertin, S., Picciau, L., Acs, Z., Alma, A. & Bosco, D. (2010) Molecular differentiation of four Reptalus species (Hemiptera: Cixiidae). Bulletin of Entomological Research, 100 (5), 551–558. https://doi.org/10.1017/S0007485309990605
Brown, B., Emberson, R.M. & Paterson, A.M. (1999) Mitochondrial COI and II provide useful markers for Wiseana (Lepidoptera: Hepialidae) species identification. Bulletin of Entomological Research, 89, 287–293. https://doi.org/10.1017/S0007485399000437
Brown, B., Emberson, R.M. & Paterson, A.M. (2000) Phylogenetic relationships within the genus Wiseana (Lepidoptera: Hepialidae). New Zealand Journal of Zoology, 27 (1), 1–14. https://doi.org/10.1080/03014223.2000.9518203
Cameron, S.L. (2014) Insect mitochondrial genomics: implications for evolution and phylogeny. Annual Review of Entomology, 59, 95–117. https://doi.org/10.1146/annurev-ento-011613-162007
De Mandal, S., Chhakchhuak, L., Gurusubramanian, G. & Kumar, N.S. (2014) Mitochondrial markers for identification and phylogenetic studies in insects—A review. DNA Barcodes, 2 (1), 1–9. https://doi.org/10.2478/dna-2014-0001
Doyle, J. (1991) DNA Protocols for Plants. In: Hewitt, G.M., Johnston, A.W.B. & Young, J.P.W. (Eds.), Molecular Techniques in Taxonomy. Springer, Berlin, Heidelberg, 283–293. https://doi.org/10.1007/978-3-642-83962-7_18
Dugdale, J.S. (1994) Hepialidae (Insecta: Lepidoptera). In: Duval, C.T. (Ed.), Fauna of New Zealand/Ko te Aitanga Pepeke o Aotearoa. Vol. 30. Lincoln, Canterbury (Manaaki Whenua), pp. 1–164, 349 + 25 figs., 27 + 5 maps.
Escamilla-Prado, E., Escamilla-Femat, S., Gómez-Utrilla, J.M., Tuxtla, M.A., Ramos-Elorduy, J. & Pino, J.M. (2012) Uso tradicional de tres especies de insectos comestibles en agroecosistemas cafetaleros del estado de Veracruz. Tropical and Subtropical Agroecosystems, 15 (Supplement 2), 101–109.
Felsenstein, J. (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution, (39), 783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Flint, M.L. (1992) Integrated pest management for cole crops and lettuce. University of California, Statewide Integrated pest management project, Division of Agriculture and natural resources. Publication 3307, 112 pp.
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenjoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.
García, del P.F. & Haro, A. (1987) Cultivo en el laboratorio en una dieta artificial del taladro de la madera, Zeuzera pyrina L. (Lepidoptera: Cossidae). Boletín de Sanidad Vegetal Plagas, 12, 281–289.
Geyer, C. ([1838]) pl. [53] with legend. In: Hübner, J., Sammlung exotischer Schmettlinge [sic]. Vol. 3. J. Hübner, Augsburg, pls. 1–53.
Gómez, B., Junghans, C., Aldasoro, E.M. & Grehan, J.R. (2016) The ghost moth (Lepidoptera: Hepialidae) as food of indigenous people in Mexico. Journal of Insects Food and Feed, 2 (1), 53–59. https://doi.org/10.3920/JIFF2015.0092
Granados, E.F. (1999) Determinación, biología y daño del gusano barrenador (Lepidoptera: Hepialidae) del aliso (Alnus jorullensis HBK) en la parte alta de la cuenca del río Chixoy. Tesis de Licenciatura, Agronomía en Recursos Naturales Renovables., Universidad de San Carlos de Guatemala, Guatemala City, 54 pp.
Grehan, J.R. (1989) Larval feeding habits of the Hepialidae (Lepidoptera). Journal of Natural History, 23, 803–824. https://doi.org/10.1080/00222938900770421
Grehan, J.R. (2012) Morphological evidence for phylogenetic relationships within the Hepialidae (Lepidoptera: Exoporia). Bulletin of the Buffalo Society of Natural Sciences, 42, 33–61.
Grehan, J.R. & Ismavel, V.A. (2017) Forest ghost moth fauna of northeastern India (Lepidoptera: Hepialidae: Endoclita, Palpifer, and Hepialiscus). Journal of Threatened Taxa, 9 (3), 9940–9955. https://doi.org/10.11609/jott.3030.9.3.9940-9955
Grehan, J.R. & Mielke, C.G.C. (2020) Taxonomic revision and biogeography of Phassodes Bethune-Baker, 1905 (Lepidoptera: Hepialidae), ghost moth descendants of a subduction zone weed in the south-west Pacific. Bishop Museum Occasional Papers, 136, 1–37.
Grehan, J.R., Mielke, C.G.C, Garzón-Orduña, I., Cruz, A. & Velazco, C. (2022) New species of Phassus Walker ghost moth from northeastern Mexico and notes on its biogeographic significance (Lepidoptera: Hepialidae). Zoonova, Greeenford, 19, 1–18.
Grehan, J.R., Mielke, C.C.G. & Hilje, L. (2021) Observations on Phassus n-signatus Weymer (Lepidoptera: Hepialidae) feeding on Ligustrum lucidum in a suburban habitat of Heredia, Costa Rica. Journal of Insect Biodiversity, 023 (1), 001–008.
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.
Harvey, M.L., Dadour, I.R. & Gaudieri, S. (2003) Mitochondrial DNA cytochrome oxidase I gene: potential for distinction between immature stages of some forensically important fly species (Diptera) in Western Australia. Forensic Science International, 131 (2–3), 134–139. https://doi.org/10.1016/S0379-0738(02)00431-0
Hebert, P.D. & Gregory, T.R. (2005) The promise of DNA barcoding for taxonomy. Systematic Biology, 54 (5), 852–859. https://doi.org/10.1080/10635150500354886
Higgins, D.G., Blackshields, G. & Wallace, I.M. (2005) Mind the gaps: progress in progressive alignment. Proceedings of the National Academy of Sciences, 102 (30), 10411–10412. https://doi.org/10.1073/pnas.0504801102
Hodges, R.W., Powell, J. & Passoa, S. (2005) Order Lepidoptera, butterflies and months. In: Triplehorn, C.A. & Johnson, N.F. (Eds.), Borror and DeLong’s Introduction to the study of insects. 7th Edition. Thomson Books/Cole, Belmont, pp. 571–647.
Jimeno-Sevilla, H.D., Elizondo-Salas, A.C., Hernández-Atlahua, F.L. & Hernández-Rincón, J.A. (2021) Las popotocas, historia de vida, manejo y usos. Primera Edición. Instituto Tecnológico Superior de Zongolica, Tepetitlanapa, Zongolica, Veracruz, 26 pp.
Jung, S., Duwal, R.K. & Lee, S. (2011) COI barcoding of true bugs (Insecta, Heteroptera). Molecular Ecology Resources, 11 (2), 266–270. https://doi.org/10.1111/j.1755-0998.2010.02945.x
López, E., Gómez, B., Sánchez, M.S., Junghans, C. & Martínez, L.V. (2015) Insectos útiles entre los tsotsiles del municipio de San Andrés Larráinzar, Chiapas, Mexico. Etnobiología, 13, 72–84.
López, J.A., Mariaca, R. & Gómez, B. (2013) Conocimiento tradicional y antropoentomofagía del chanulte’ en Oxchuc, Chiapas, Mexico. Etnobiología, 11, 69–80.
Luna-Barradas, M.M., Escalante-Luna, M.R.D. & Gallardo-Monterrosas, D. (2016) Actividad antifúngica de extractos: etanolico, metanolico, y etéreo del gusano Phassus triangularis sobre Candida albicans. Revista Latinoamericana de Química, 44 (Suplemento Especial), 59.
Mielke, C.G.C. & Casagrande, M.M. (2013) A new Cibyra Walker, 1856 from southern Brazil (Lepidoptera: Hepialidae). Nachrichten des Entomologischen Vereins Apollo, Neue Folge, 34 (1/2), 73–86.
Mielke, C.G.C. & Grehan, J.R. (2012) Catalogue of the Latin American Hepialidae with taxonomic remarks (Lepidoptera). Nachrichten des Entomologischen Vereins Apollo, Neue Folge, 32, 131–158.
Mielke, C.G.C. & Grehan, J.R. (2015) Description of a new species of Phassus Walker, 1856 from Costa Rica, Pallas, gen. n., with a new species from Guatemala, and taxonomic notes on Sthenopis Packard, [1865] (Lepidoptera, Hepialidae). The European Entomologist, 7, 113–134.
Mielke, C.G.C., Grehan, J.R. & Monzón-Sierra, J. (2020) Taxonomic revision of Schausiana Viette with two new species from Guatemala and notes on biogeography and correlated tectonics (Lepidoptera: Hepialidae). Zootaxa, 4860 (1), 67–91. https://doi.org/10.11646/zootaxa.4860.1.3
Moreno, Ch.G. (1989) Biología de las especies de la familia Hepialidae en las localidades de elevación media Costa Rica. Tesis de Licenciatura. Universidad Nacional de Costa Rica, Heredia, Costa Rica, 161 pp.
Nielsen, E., Robinson, G. & Wagner, D. (2000) Ghost moths of the world: a global inventory and bibliography of the Exoporia (Mnesarchaeoidea and Hepialoidea) (Lepidoptera). Journal of Natural History, 34, 823–878. https://doi.org/10.1080/002229300299282
Panorama Agroalimentario (2020) Datos de un campo que avanza sin dejar a nadie atrás. Secretaría de Agricultura y Desarrollo Rural. Servicio de Información Agroalimentaria y Pesquera. Available from: https://www.inforural.com.mx/wp-content/uploads/2020/11/Atlas-Agroalimentario-2020.pdf (accessed 22 September 2022)
Poitout, S. & Bues, R. (1974) Elevage de chenilles de veingt-huit especes de lepidopteres. Noctuidae et de deux especes d’ elevage selon les especes d’Artiidae sur milieu artificiel simple. Particularités de I´ elevage selon les especes. Annales de Zoologie Ecologie Animale, 6, 341–411.
Prokopy, R. & Kogan, M. (2009) Integrated pest management. In: Encyclopedia of insects. 2nd Edition. Academic Press, San Diego, California, pp. 523–528. https://doi.org/10.1016/B978-0-12-374144-8.00148-X
Pusz-Bochenska, K., Perez-Lopez, E., Dumonceaux, T.J., Olivier, C. & Wist, T.J. (2020) A rapid, simple, laboratory and field-adaptable DNA extraction and diagnostic method suitable for insect-transmitted plant pathogen and insect identification. Plant Health Progress, 21 (1), 63–68. https://doi.org/10.1094/PHP-09-19-0063-FI
Ramos-Elorduy, J. (1982). Los insectos como una fuente de proteínas en el futuro. Editorial Limusa, Mexico, 144 pp.
Ramos-Elorduy, J. & Pino, J.M. (1988) The utilization of insects in the empirical medicine of ancient Mexicans. Journal of Ethnobiology, 8, 195–202.
Rathee, M. & Dalal, P. (2018) Emerging insect pests in Indian agriculture. Indian Journal of Entomology, 80 (2), 267–281. https://doi.org/10.5958/0974-8172.2018.00043.3
Regier, J.C., Mitter, Ch., Kristensen, N.P., Davis, D.R., van Nieukerken, E.J., Rota, J., Simonsen, T.J., Mitter, K.T., Kawahara, A.Y., Yen, S.-H., Cummings, M.P. & Zwick, A. (2015) Molecular phylogeny for the oldest (nonditrysian) lineages of extant Lepidoptera, with implications for classification, comparative morphology and life-history evolution. Systematic Entomology, 40 (4), 671–704. [https://resjournals.onlinelibrary.wiley.com/doi/abs/10.1111/syen.12129] https://doi.org/10.1111/syen.12129
Richards, N.K., Mansfield, S., Townsend, R.J. & Ferguson, C.M. (2017) Genetic variation within species and haplotypes of the Wiseana (Lepidoptera: Hepialidae) complex and development of non‐sequenced based identification tools to aid field studies. Pest Management Science, 73 (11), 2334–2344. https://doi.org/10.1002/ps.4620
Saitou, N. & Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.
Sandoval, L. & Nishida, K. (2015) The first record of an audible sound produced by a ghost moth, Phassus (Hepialidae) from Costa Rica. The Journal of Research on the Lepidoptera, 48, 45–49. https://doi.org/10.5962/p.266471
SIAP—Servicio de Información Agroalimentaria y Pesquera (2020) Anuario estadístico de la producción agrícola. Available from: http://www.siap.gob.mx (accessed 22 September 2022).
Simonsen, T.J. (2018) Splendid ghost moths and their allies, a revision of Australian Abantiades, Oncopera, Aenetus, Archaeoaenetus and Zelotypia (Hepialidae). Vol. 12. Monographs on Australian Lepidoptera. CSIRO Publishing, Melbourne, 300 pp. https://doi.org/10.1071/9781486307487
Stehr, F.W. (1987) Immature Insects. Vol. I. Kendall/Publishing Co., Dubuque, Iowa, 754 pp.
Strand, E. (1916) Lepidoptera Niepeltiana 2. In: Niepelt, W. (Ed.), Abbildungen und Beschreibungen neuer und wenig bekannter Lepidoptera aus der Sammlung W. Niepelt. Zirlau. Urban & Co, Leipzig, pp. [2] + 1–26, pls. xiii–xvii.
Tamura, K., Nei, M. & Kumar, S. (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences, 101, 11030–11035. https://doi.org/10.1073/pnas.0404206101
Thompson, E.H. (1895) Insect and fungus pests of field, farm and garden. Tasmanian Department of Agriculture Bulletin, 6 (Part 2), 1–34.
Tindale, N.B. (1932) Revision of the Australian ghost moths (Lepidoptera Homoneura, family Hepialidae). Part I. Records of the South Australian Museum, 4, 497–536.
Vázquez, Y.M., Martínez, A.M., Valdez, J.M., Figueroa, J.I., Rebollar, Á., Chavarrieta, J.M., Sánchez, J.A., Viñuela, E. & Pineda, S. (2014) Life history, diagnosis, and parasitoids of Zale phaeograpta (Lepidoptera: Erebidae). Annals of the Entomological Society of America, 107 (1), 170–177. https://doi.org/10.1603/AN13093
Wagner, D.L., Tobi, D.R., Parker, B.L., Wallner, W.E. & Leonard, J.G. (1989) Immature stages and natural enemies of Korscheltellus gracilis (Lepidoptera: Hepialidae). Annual of Entomological Society of America, 82 (6), 717–724. https://doi.org/10.1093/aesa/82.6.717
Waterhouse, D.F. & Sands, D.P.A. (2001) Classical biological control of arthropods in Australia. Monograph No. 77. Australian Centre for International Agricultural Research, Canberra, 560 pp.
Wood, D.M. (1987) Chapter 110. Tachinidae. In: McAlpine, J.F., Peterson, B.V., Shewell, G.E., Teskey, H.J., Vockeroth, J.R. & Wood, D.M. (Eds.), Manual of Nearctic Diptera. Vol. 2. Agriculture Canada Monograph 28. Research Branch, Agriculture Canada, Ottawa, pp. 1193–1269.
Yang, X-H., Yu, Y.-H., Wu, Y.-J., Qin, J.-L. & Luo, Y.-Q. (2013) First report of Endoclita signifer (Lepidoptera: Hepialidae) as a new pest on Eucalyptus. Journal of Economical Entomology, 106 (2), 866–873. https://doi.org/10.1603/EC12310
Waller, J.B. (1966) Sexing of pupae of Wiseana cervinata (Walker) Hepialidae. New Zealand Entomologist, 3, 5. https://doi.org/10.1080/00779962.1966.9722852
Walker, F. (1856) s.n. In: List of the specimens of lepidopterous insects in the collection of the British Museum. Part VII. Lepidoptera Heterocera. Trustees of NHMUK, London, pp. [4] + [1509]–1808.
Wilson, J.J. (2012) DNA barcodes for insects. In: Krees, W.J. & Erickson, D.L (Eds.), DNA Barcodes: Methods and protocols, methods in molecular biology. Vol. 858. Humana Press, Totowa, New Jersey, pp. 17–46. https://doi.org/10.1007/978-1-61779-591-6_3
Zhang, C.-T. & Shima, H. (2006) Systematic study of the genus Dinera Robineau-Desvoidy from the Palaearctic and Oriental regions (Diptera: Tachinidae). Zootaxa, 1243 (1), 1–60. https://doi.org/10.11646/zootaxa.1206.1.1