Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2023-08-15
Page range: 151-200
Abstract views: 216
PDF downloaded: 23

Exochorion in the tribe Nymphalini (Lepidoptera: Nymphalidae): the genus Hypanartia Hübner, [1821] and comparison with related genera

Museo de Zoología (Entomología); Departamento de Biología Evolutiva; Facultad de Ciencias; Universidad Nacional Autónoma de México; México; 04510; CDMX; México
Museo de Zoología (Entomología); Departamento de Biología Evolutiva; Facultad de Ciencias; Universidad Nacional Autónoma de México; México; 04510; CDMX; México; Posgrado en Ciencias Biológicas; Unidad de Posgrado de la Universidad Nacional Autónoma de México; Edificio D; 1° Piso; Circuito de Posgrados; Ciudad Universitaria; 04510; CDMX; México
Museo de Zoología (Entomología); Departamento de Biología Evolutiva; Facultad de Ciencias; Universidad Nacional Autónoma de México; México; 04510; CDMX; México; Posgrado en Filosofía de la Ciencia; Universidad Nacional Autónoma de México; México
Lepidoptera Nymphalinae Antanartia Papilionoidea chorion ridges micropyle

Abstract

We describe and compare the exochorion of six species of Hypanartia (H. paullus, H. bella, H. lethe, H. godmanii, H. dione disjuncta, and H. trimaculata autumna) using specimens collected in the field and deposited in entomological collections. We used a standard staining technique and scanning electron microscopy to visualize and describe the main exochorionic characters, especially the ridges and the differentiation in the micropylar, perimicropylar, and transition zones in the apical region. We included plates with photographs, drawings, and schemes for clearer visualization of these structures, which are tabulated for comparison. For our characterization, we considered the ridges in colonnade as the main exochorionic feature in the Nymphalini. Thus, we made brief comparisons of these features among several species of the tribe, particularly with the genus Antanartia. The exochorionic characters agree with the separation of groups (paullus group and dione group). By examining the characteristics of H. paullus, the basal species of the paullus group, we found that ridges with conspicuous columns (e.g., in one section only) appears to be the plesiomorphic state, while those with elongated shafts and walls only in the intercolumn represent the apomorphic state.

 

References

  1. Ackery P.R. (1988) Hostplants and classification: a review of nymphalid butterflies. Biological Journal of the Linnean Society, 33 (2), 95–203. https://doi.org/10.1111/j.1095-8312.1988.tb00446.x
  2. Alexiuk, M.R., Lalonde, M.M.L. & Marcus, J.M. (2021a) Phylogenetic analysis of the complete mitochondrial genome of the Japanese peacock butterfly Aglais io geisha (Stichel 1907) (Insecta: Lepidoptera: Nymphalidae). Mitochondrial DNA, Part B, 6 (10), 3082–3084. https://doi.org/10.1080/23802359.2021.1981168
  3. Alexiuk, M.R., Lalonde, M.M.L. & Marcus, J.M. (2021b) Phylogenetic analysis of the complete mitochondrial genome of the Blomfild’s Beauty butterfly Smyrna blomfildia (Fabricius 1781) (Insecta: Lepidoptera: Nymphalidae). Mitochondrial DNA, Part B, 6 (11), 3199–3201. https://doi.org/10.1080/23802359.2021.1989337
  4. Arbogast, R.T. & Van Byrd, R. (1981) External morphology of the eggs of the meal moth Pyralis farinalis (L.), and the murky meal moth, Aglossa caprealis (Hübner) (Lepidoptera: Pyralidae). Journal of the Insect Morphology & Embriology, 10 (5/6), 419–423. https://doi.org/10.1016/0020-7322(81)90022-2
  5. Arbogast, R.T., Van Byrd, R., Chauvin, G. & Strong, R.G. (1984) The egg of Hofmannophila pseudospretella (Oecophoridae): fine structure of the chorion. Journal of the Lepidopterists’ Society, 38 (3), 202–208.
  6. Brower, A.V. (2000) Phylogenetic relationships among the Nymphalidae (Lepidoptera) inferred from partial sequences of the wingless gene. Proceedings of the Royal Society B: Biological Sciences, 267 (1449), 1201–1211. https://doi.org/10.1098/rspb.2000.1129
  7. Brown, K.S.Jr. & Freitas, A.V.L. (1994) Juvenile stages of Ithomiinae: overview and systematics (Lepidoptera: Nymphalidae). Tropical Lepidoptera, 5 (1), 9–20.
  8. Brown, K.S.Jr., Freitas, A.V.L., Wahlberg, N., Von Schoultz, B., Saura, A.O. & Saura, A. (2007) Chromosomal evolution in the South American Nymphalidae. Hereditas, 144 (4), 137–148. https://doi.org/10.1111/j.2007.0018-0661.02015.x
  9. Campos-González, E., Nieves-Uribe, S. & Llorente-Bousquets, J. (2020) Descripción del exocorion de tres especies de Coeini. Southwestern Entomologist, 45 (4), 1091–1120. https://doi.org/10.3958/059.045.0427
  10. Chapman, T.A. (1896a) The characters of the egg of Lepidoptera, as affording a basis for classification. The Entomologist’s Record and Journal of Variation, 8 (12), 287–289.
  11. Chapman, T.A. (1896b) XV. On the phylogeny and evolution of the Lepidoptera from a pupal and oval standpoint. Transactions of the Entomological Society of London, 44, 567–587. https://doi.org/10.1111/j.1365-2311.1896.tb00969.x
  12. Clark, F.D. (1900) Photographing the eggs of Lepidoptera (with plate). The Entomologist’s Record and Journal of Variation, 12 (11), 281–282.
  13. Dell’Erba, R., Kaminski, L.A. & Moreira, G.R.P. (2005) O estágio de ovo dos Heliconiini (Lepidoptera, Nymphalidae) do Rio Grande do Sul, Brasil. Iheringia, Série Zoologia, 95 (1), 29–46. https://doi.org/10.1590/S0073-47212005000100006
  14. Döring, E.K.H. (1955) Zur Morphologie der Schmetterlingseier. Akademie-Verlag, Berlin, 154 pp., 61 pls.
  15. Ellis, E.A., Storer, C.G. & Kawahara, A.Y. (2021) De novo genome assemblies of butterflies. Gigascience, 10 (6), 1–8. https://doi.org/10.1093/gigascience/giab041
  16. Espeland, M., Breinholt, J., Willmott, K.R., Warren, A.D., Vila, R., Toussaint, E.F.A., Maunsell, S.C., Aduse-Poku, K., Talavera, G., Eastwood, R., Jarzyna, M.A., Guralnick, R., Lohman, D.J., Pierce, N.E. & Kawahara, A.Y. (2018) A Comprehensive and dated phylogenomic analysis of butterflies. Current Biology, 28 (5), 770–778. https://doi.org/10.1016/j.cub.2018.01.061
  17. Fehrenbach, H. (2003) 18. Eggs. In: Kristensen, N.P. (Ed.), Handbook of Zoology: Vol. IV. Arthropoda: Insecta. Part 36. Lepidoptera, Moths and Butterflies. Vol. 2. Morphology, Physiology and Development. Walter de Gruyter, New York, New York, pp. 469–493. https://doi.org/10.1515/9783110893724.469
  18. Fic, Z., Konvicka, M. & Zrzavy, J. (2004) Red & black or white & black? Phylogeny of the Araschnia butterflies (Lepidoptera: Nymphalidae) and evolution of seasonal polyphenism. Journal of Evolutionary Biology, 17 (2), 265–278. https://doi.org/10.1111/j.1420-9101.2003.00681.x
  19. Fic, Z.F., Martinkova, B., Rindos, M., Bartonova, A.S., Wahlberg, N. & Maresova, J.P. (2022) Molecular phylogeny and biogeography of the genus Symbrenthia (Lepidoptera, Nymphalidae) correlates with the past geography of the Oriental region. Molecular Phylogenetics and Evolution, 177 (Art. 1076605), 1–10. https://doi.org/10.1016/j.ympev.2022.107605
  20. Field, W.D. (1971) Butterflies of the genus Vanessa and of the resurrected genera Bassaris and Cynthia (Lepidoptera: Nymphalidae). Smithsonian Contributions to Zoology, 84, 1–105. https://doi.org/10.5479/si.00810282.84
  21. Flores-Gallardo, A., Nieves-Uribe, S. & Llorente-Bousquets, J. (2021) Caracteres exocoriónicos en sistemática de Papilionoidea (Insecta: Lepidoptera): importancia de las técnicas de producción de imágenes. Dugesiana, 28 (2), 147–173. https://doi.org/10.32870/dugesiana.v28i2.7162
  22. Flores-Gallardo, A., Llorente-Bousquets, J. & Nieves-Uribe, S. (2022) Estilos y virtudes epistémicas en la representación esquemática de un sistema de caracteres: un ensayo sobre el exocorion de Papilionoidea (Insecta: Lepidoptera). Dugesiana, 29 (2), 225–243. https://doi.org/10.32870/dugesiana.v29i2.7265
  23. Freitas, A.V. & Brown, K.S. Jr. (2004) Phylogeny of the Nymphalidae (Lepidoptera). Systematic Biology, 53 (3), 363–383. https://doi.org/10.1080/10635150490445670
  24. García-Barros, E. (2000) Egg size in butterflies (Papilionoidea and Hesperiidae): a summary of data. Journal of Research on the Lepidoptera, 35, 90–136. https://doi.org/10.5962/p.280588
  25. García-Barros, E. & Martín, J. (1995) The eggs of the European satyrine butterflies (Nymphalidae): external morphology and its use in systematics. Zoological Journal of the Linnean Society, 115 (1), 73–115. https://doi.org/10.1111/j.1096-3642.1995.tb02324.x
  26. Giannopoulos, N.G., Michalopoulos, I., Papandreou, N.C., Malatras, A., Iconomidou, V.A. & Hamodrakas, S.J. (2013) LepChorionDB, a database of Lepidopteran chorion proteins and a set of tools useful for the identification of chorion proteins in Lepidopteran proteomes. Insect Biochemistry and Molecular Biology, 43 (2), 189–196. https://doi.org/10.1016/j.ibmb.2012.12.001
  27. Grados, J. (2014) Hypanartia splendida Rothschild, 1903 (Lepidoptera, Nymphalidae, Nymphalinae) una rara especie de la selva central de Perú. Revista Peruana de Biología, 21 (2), 183–186. https://doi.org/10.15381/rpb.v21i2.9824
  28. Greeney, H.F. & Chicaiza Aguirre, C. (2009) The life history of Hypanartia dione dione (Lepidoptera: Nymphalidae) in northeastern Ecuador. Journal of Research on the Lepidoptera, 41, 1–4. https://doi.org/10.5962/p.266520
  29. Harvey, D.J. (1991) Higher classification of the Nymphalidae. Appendix B. In: Nijhout, H.F. (Ed.), The development and evolution of butterfly wing patterns. Smithsonian Institution Press, Washington, D.C., pp. 255–273.
  30. Hernández-Mejía, B.C., Flores-Gallardo, A. & Llorente-Bousquets, J. (2013) Comparación morfológica del corion de especies de los géneros Pieriballia, Itaballia y Perrhybris (Lepidoptera: Pieridae: Pierinae), y sus implicaciones filogenéticas. Southwestern Entomologist, 38 (2), 275–292. https://doi.org/10.3958/059.038.0211
  31. Hernández-Mejía, B.C., Flores-Gallardo, A. & Llorente-Bousquets, J. (2014a) Morfología del corion en especies de los géneros Ascia y Ganyra y su comparación con otros géneros próximos de Pierinae (Lepidoptera: Pieridae). Southwestern Entomologist, 39 (1), 119–134. https://doi.org/10.3958/059.039.0112
  32. Hernández-Mejía, B.C., Flores-Gallardo, A. & Llorente-Bousquets, J. (2014b) Morfología del corion en la subfamilia Coliadinae (Lepidoptera: Pieridae). Southwestern Entomologist, 39 (4), 853–886. https://doi.org/10.3958/059.039.0416
  33. Hernández-Mejía, C., Flores-Gallardo, A. & Llorente-Bousquets J. (2015) Morfología del corion en Leptophobia (Lepidoptera: Pieridae) e importancia taxonómica. Southwestern Entomologist, 40 (2), 351–368. https://doi.org/10.3958/059.040.0210
  34. Hernández-Roldán, J.L., Munguira, M.L., Wagner, W. & Vila, R. (2012) Comparative analysis and taxonomic use of the morphology of immature stages and natural history traits in European species of Pyrgus Hübner (Lepidoptera: Hesperiidae, Pyrginae). Zootaxa, 3470 (1), 1–71. [monograph] https://doi.org/10.11646/zootaxa.3470.1.1
  35. Hinton, H.E. (1981) Biology of insect eggs. Vols. I–III. Pergamon, Oxford, 1125 pp.
  36. Hooke, R. (1665) Micrographia, or, some physiological descriptions of minute bodies made by magnifying glasses, with observations and inquiries thereupon. Printed by J. Martyn and J. Allestry, London, 273 pp. https://doi.org/10.5962/bhl.title.904
  37. Howarth, T.G. (1966) Revisional notes on the genus Antanartia (Lepidoptera; Nymphalidae). Bulletin of the British Museum (Natural History) Entomology, 18 (2), 21–43.
  38. Howe, W.H. (1975) The butterflies of North America. Doubleday & Company, Garden City, New York, 633 pp.
  39. Kaminski, L.A. & Freitas, A.V.L (2009) Fabaceae, a new host plant family for Hypanartia and for the Neotropical Nymphalinae (Lepidoptera: Nymphalidae). Journal of Research on the Lepidoptera, 41, 76–77. https://doi.org/10.5962/p.266531
  40. Kawaguchi, Y., Kusakabe, T. & Koga, K. (2002) Morphological variation of micropilar apparatus in Bombix mori eggs. Journal of Insect Biotechnology and Sericology, 71, 49–54.
  41. Kawahara, A.Y, Storer, C., Carvalho, A.P.S., et al. (2023) A global phylogeny of butterflies reveals their evolutionary history, ancestral hosts and biogeographic origins. Nature Ecology and Evolution, 7 (6), 903–913. https://doi.org/10.1038/s41559-023-02041-9
  42. Kristensen, N.P. (Ed.) (1998) Handbook of Zoology: Vol. IV. Arthropoda: Insecta. Part 35. Lepidoptera, moths and butterflies. Vol. 1. Evolution, systematics, and biogeography. Walter de Gruyter, New York, New York, 487 pp.
  43. Klots, A.B. (1960) Vida y costumbres de las mariposas/Vie et moeurs des Papillons. Segunda Edición, Garriga Impresiones S.A., Mallorca, Barcelona, 204 pp., 64 pls.
  44. Küppers, H. (1996) Atlas de los colores, más de 5500 matices con su caracterización y las instrucciones para su mezcla. Blume, Barcelona, 161 pp.
  45. Llorente-Bousquets, J.E. & Castro-Gerardino, J. (2007) Estudios en sistemática de Dismorphiini (Lepidoptera: Pieridae) I. Morfología de huevos y su importancia taxonómica. Revista de la Academia Colombiana de Ciencias Físicas y Exactas, 31 (118), 145–164.
  46. Llorente-Bousquets, J.E. & Castro-Gerardino, J. (2008) Morfología del corion en Dismorphiini (Lepidoptera: Pieridae). In: Llorente-Bousquets, J. & Lanteri, A. (Eds.), Contribuciones taxonómicas en órdenes de insectos hiperdiversos. Las Prensas de Ciencias, UNAM, México, D.F. pp. 72–90.
  47. Llorente-Bousquets, J., Nieves-Uribe, S., Flores-Gallardo, A., Hernández-Mejía, B.C. & Castro-Gerardino, J. (2018) Chorionic sculpture in the Dismorphiinae subfamily (Lepidoptera: Pieridae). Zootaxa, 4429 (2), 201–246. https://doi.org/10.11646/zootaxa.4429.2.1
  48. Malpighi, M. (1669) Dissertatio epistolica de Bombyce. Regiae Societatis Typographos, Londini, 100 pp., 12 pls. https://doi.org/10.5962/bhl.title.158896
  49. Mehra, D., Kirti, J. S. & Sidhu, A.K. (2018) Taxonomic review of the tribe Nymphalini (Lepidoptera: Nymphalidae: Nymphalinae) from western Himalaya, India with special emphasis on external genitalic attributes. Entomon, 43 (3), 237–256. https://doi.org/10.33307/entomon.v43i4.404
  50. Motta, P.C. (1989) Análise Filogenética de Ithomiinae (Lep.: Nymphalidae) com base nos ovos: relação com plantas hospedeiras. M.Sc. Thesis, SP, UNICAMP, Campinas, 294 pp.
  51. Müller, W. (1886) Südamerikanische Nymphalidenraupen: Versuch eines natürlichen Systems der Nymphaliden. Zoologische Jahrbücher, 1, 417–678. https://doi.org/10.5962/bhl.title.109410
  52. Munguira, M.L., Martín, J., García-Barros, E., Shahbazian, G. & Cancela, J.P. (2015) Morphology and morphometry of lycaenid eggs (Lepidoptera: Lycaenidae). Zootaxa, 3937 (2), 201–247. https://doi.org/10.11646/zootaxa.3937.2.1
  53. Nieves-Uribe, S., Flores-Gallardo, A., Hernández-Mejía, B. C. & Llorente-Bousquets, J. (2015) Exploración morfológica del corion en Biblidinae (Lepidoptera: Nymphalidae): aspectos filogenéticos y clasificatorios. Southwestern Entomologist, 40 (3), 589–648. https://doi.org/10.3958/059.040.0318
  54. Nieves-Uribe, S., Castro-Gerardino, J., Flores-Gallardo, A. & Llorente-Bousquets, J. (2016a) Corion en los géneros Anteos y Rhabdodryas: su significado e implicaciones. Southwestern Entomologist, 41 (2), 485–504. https://doi.org/10.3958/059.041.0218
  55. Nieves-Uribe, S., Castro-Gerardino, J., Flores-Gallardo, A. & Llorente-Bousquets, J. (2016b) Microrretícula coriónica en los géneros Nathalis Boisduval y Kricogonia Reakirt: implicaciones taxonómicas y tendencias evolutivas. Southwestern Entomologist, 41 (3), 716–733. https://doi.org/10.3958/059.041.0314
  56. Nieves-Uribe, S., Castro-Gerardino, J., Flores-Gallardo, A. & Llorente-Bousquets, J. (2016c) Estudio del corion de tres especies del género Colias Fabricius, 1807 y Zerene cesonia cesonia (Stoll, 1790). Southwestern Entomologist, 41 (4), 1121–1141. https://doi.org/10.3958/059.041.0411
  57. Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2016d) Morfología coriónica de once especies de Biblidinae de México y Colombia: un examen de predicciones. Southwestern Entomologist, 41 (2), 505–532. https://doi.org/10.3958/059.041.0219
  58. Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2017a) Corion de Ectima thecla thecla (Fabricius, 1796) y su comparación con el género Hamadryas. Southwestern Entomologist, 42 (3), 851–864. https://doi.org/10.3958/059.042.0324
  59. Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2017b) Corion de Orophila cardases campaspe (Hewitson, 1869) y caracterización coriónica de la subtribu Callicorina. Southwestern Entomologist, 42 (3), 865–878. https://doi.org/10.3958/059.042.0325
  60. Nieves-Uribe, S. Flores-Gallardo, A. & Llorente-Bousquets, J. (2018a) Corion de Leucidia brephos (Hübner, [1809]), comparaciones con otros géneros de Coliadinae y tendencias reticulares. Southwestern Entomologist, 43 (1), 239–255. https://doi.org/10.3958/059.043.0115
  61. Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2018b) Estructura exocoriónica en tres especies de Colias Fabricius, 1807 (Lepidoptera: Pieridae, Coliadinae). Southwestern Entomologist, 43 (2), 485–503. https://doi.org/10.3958/059.043.0220
  62. Nieves-Uribe, S., Flores-Gallardo, A., Llorente-Bousquets, J., Luis-Martínez, A. & Pozo, C. (2019) Use of exochorion characters for the systematics of Hamadryas Hübner and Ectima Doubleday (Nymphalidae: Biblidinae: Ageroniini). Zootaxa, 4619 (1), 77–108. https://doi.org/10.11646/zootaxa.4619.1.3
  63. Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2020a) Estructura exocoriónica de dos especies de Colias Fabricius de México. Southwestern Entomologist, 45 (3), 733–751. https://doi.org/10.3958/059.045.0316
  64. Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2020b) Chorion exploration in the tribe Anthocharidini (Lepidoptera: Pieridae) and their possible importance in its systematics. Zootaxa, 4868 (2), 151–207. https://doi.org/10.11646/zootaxa.4868.2.1
  65. Nieves-Uribe, S., Flores-Gallardo, A. & Llorente-Bousquets, J. (2021a) Micropylar and perimicropylar regions of the egg exochorion in six genera of Dismorphiinae (Lepidoptera: Pieridae). Zootaxa, 4966 (3), 251–289. https://doi.org/10.11646/zootaxa.4966.3.1
  66. Nieves-Uribe, S., Llorente-Bousquets, J. & Flores-Gallardo, A. (2021b) Toward standards in practices and techniques on ootaxonomy in the Pieridae (Lepidoptera: Papilionidae). Zootaxa, 4985 (3), 301–344. https://doi.org/10.11646/zootaxa.4985.3.1
  67. Nieves-Uribe, S. & Llorente-Bousquets, J. (2022) Rehidratación abdominal con hidróxido de amonio en Lepidoptera: obtención del corion para estudios taxonómicos. Southwestern Entomologist, 47 (2), 481–498. https://doi.org/10.3958/059.047.0224
  68. Nieves-Uribe, S., Llorente-Bousquets, J. & Flores-Gallardo, A. (2022) Morfología coriónica en dos subespecies de Eurema elathea y su comparación con E. daira sidonia. Southwestern Entomologist, 47 (1), 215–231. https://doi.org/10.3958/059.047.0121
  69. Nylin, S. & Wahlberg, N. (2008) Does plasticity drive speciation? Host-plant shifts and diversification in Nymphalinae butterflies (Lepidoptera: Nymphalidae) during the tertiary. Biological Journal of the Linnean Society, 94 (1), 115–130. https://doi.org/10.1111/j.1095-8312.2008.00964.x
  70. Payment, J.E., Marcus, J.M. & Lalonde, M.M.L. (2020) Phylogenetic analysis of the complete mitochondrial genome of the white peacock butterfly Anartia jatrophae saturata (Insecta: Lepidoptera: Nymphalidae). Mitochondrial DNA Part B, 5 (3), 3690–3692. https://doi.org/10.1080/23802359.2020.1832929
  71. Peterson, A. (1960) Photographing eggs of insects. The Florida Entomologist, 43 (1), 1–7. https://doi.org/10.2307/3492514
  72. Peterson, A. (1970) Eggs from miscellaneous species of Rhopalocera— Lepidoptera. The Florida Entomologist, 53 (2), 65–71. https://doi.org/10.2307/3493448
  73. Rezende, G.L., Vargas, H.C.M., Moussian, B. & Cohen, E. (2016) Composite eggshell matrices: chorionic layers and sub-chorionic cuticular envelopes. In: Cohen, E. & Moussian, B. (Eds.), Extracellular composite matrices in arthropods. Springer International Publishing, Cham, pp. 325–366. https://doi.org/10.1007/978-3-319-40740-1_9
  74. Rivera-Galicia, S., Nieves-Uribe, S. & Llorente-Bousquets, J. (2020) Estudio del exocorion en tres especies de Heliconiinae de México. Southwestern Entomologist, 45 (3), 753–779. https://doi.org/10.3958/059.045.0317
  75. Rothschild, W. & Jordan, K. (1903) Lepidoptera collected by Oscar Neuman in North-East Africa. Noviates Zoologicae: a Journal of Zoology in Connection with the Tring Museum, 10 (3), 491–542.
  76. Salkeld, E.H. (1973) The chorionic architecture and shell structure of Amathes c-nigrum (Lepidoptera: Noctuidae). The Canadian Entomologist, 105 (1), 1–10. https://doi.org/10.4039/Ent1051-1
  77. Salkeld, E.H. (1984) A catalogue of the eggs of some Canadian Noctuidae (Lepidoptera). Memoirs of the Entomological Society of Canada, 116 (Supplement 127), 1–167. https://doi.org/10.4039/entm116127fv
  78. Scudder, S.H. (1889) The butterflies of the eastern United States and Canada: with special reference to New England in three volumes. Published by the author, Cambridge, 1958 pp. https://doi.org/10.5962/bhl.title.40436
  79. Shi, Q.H., Sun, X.Y., Wang, Y.L., Hao, J.S. & Yang, Q. (2015) Morphological characters are compatible with mitogenomic data in resolving the phylogeny of nymphalid butterflies (Lepidoptera: Papilionoidea: Nymphalidae). PLoS One, 10 (4), 1–19. https://doi.org/10.1371/journal.pone.0124349
  80. Su, C., Shi, Q., Sun, X., Ma, J., Li, C., Hao, J. & Yang, Q. (2017) Dated phylogeny and dispersal history of the butterfly subfamily Nymphalinae (Lepidoptera: Nymphalidae). Scientific Reports, 7 (1), Art. 8799, 1–11. https://doi.org/10.1038/s41598-017-08993-w
  81. Suludere, Z. (1988a) Studies on the external morphology of the eggs of some Argynninae species (Satyridae [sic]: Lepidoptera). Communications of the Faculty of Sciences University of Ankara Series C Biology and Geological Engineering, 6, 9–28. https://doi.org/10.1501/Commuc_0000000125
  82. Suludere, Z. (1988b) Description of the eggs of Rhodostrophia meonaria Guenée from North Pakistan (Geometridae: Lepidoptera). Communications of the Faculty of Sciences University of Ankara Series C Biology and Geological Engineering, 6, 47–52. https://doi.org/10.1501/Commuc_0000000127
  83. Suludere, Z. (1988c) Studies on the external morphology of the eggs of some Melitaea species (Satyridae [sic]: Lepidoptera). Communications of the Faculty of Sciences University of Ankara Series C Biology and Geological Engineering, 6, 73–84. https://doi.org/10.1501/Commuc_0000000129
  84. Telfer, W.H. (2009) Egg formation in Lepidoptera. Journal of Insect Science, 9 (1), Art. 50, 1–21. https://doi.org/10.1673/031.009.5001
  85. Trougakos, I.P. & Margaritis, L.H. (2008) Novel morphological and physiological aspects of insect eggs. In: Hilker, M. & Meiners, T. (Eds.), Chemoecology of insect eggs and egg deposition. Blackwell Publishing Company, Berlin, pp. 3–36.
  86. Van Son, G. (1979) The butterflies of Southern Africa. Part. IV Nymphalidae: Nymphalinae. The Transvaal Museum Memoir, 22 (1), 1–286. https://doi.org/10.10520/AJA0000012_253
  87. Wahlberg, N. & Nylin, S. (2003) Morphology versus molecules: resolution of the positions of Nymphalis, Polygonia, and related genera (Lepidoptera: Nymphalidae). Cladistics, 19 (3), 213–223. https://doi.org/10.1016/S0748-3007(03)00027-6
  88. Wahlberg, N., Weingartner, E. & Nylin, S. (2003) Towards a better understanding of the higher systematics of Nymphalidae (Lepidoptera: Papilionoidea). Molecular Phylogenetics and Evolution, 28 (3), 473–84. https://doi.org/10.1016/S1055-7903(03)00052-6
  89. Wahlberg, N., Brower, A.V.Z. & Nylin, S. (2005) Phylogenetic relationships and historical biogeography of tribes and genera in the subfamily Nymphalinae (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society, 86 (2), 227–251. https://doi.org/10.1111/j.1095-8312.2005.00531.x
  90. Wahlberg, N., Leneveu, J., Kodandaramaiah, U., Peña, C.A., Nylin, S., Freitas, A.V. & Brower, A.V. (2009) Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proceedings of the Royal Society B: Biological Sciences, 276, 4295–4302. https://doi.org/10.1098/rspb.2009.1303
  91. Wheeler, D.E. (2009) Egg coverings. In: Resh, V.H. & Cardé, R.T. (Eds.), Encyclopedia of insects. Academic Press, Amsterdam, pp. 312–313. https://doi.org/10.1016/B978-0-12-374144-8.00093-X
  92. Willmott, K.R., Hall, J.P.W. & Lamas, G. (2001) Systematics of Hypanartia (Lepidoptera: Nymphalidae: Nymphalinae), with a test for geographical speciation mechanisms in the Andes. Systematic Entomology, 26 (4), 369–399. https://doi.org/10.1046/j.1365-3113.2001.00157.x
  93. Young, A.M. (1976) Notes on the life cycle of the butterfly Hypanartia kefersteini (Nymphalidae: Nymphalinae; Nymphalini) in Costa Rica. Brenesia, 1976 (9), 61–69.
  94. Zhang, M., Cao, T.W., Zhong, Y., Ren, Z.M., Guo, Y.P. & Ma, E.-B. (2008) Molecular phylogenetic analysis of the main lineages of Nymphalinae (Nymphalidae: Lepidoptera) based on the partial mitochondrial COI gene. Agricultural Sciences in China, 7 (6), 731–739. https://doi.org/10.1016/S1671-2927(08)60108-X
  95. Zhang, J., Cong, Q., Shen, J., Opler, P.A. & Grishin, N.V. (2021) Genomics-guided refinement of butterfly taxonomy. The Taxonomic Report of the International Lepidoptera Survey, 9 (3), 1–55. https://doi.org/10.5281/zenodo.5630311