Abstract
On the basis of comparative-morphological analysis of 43 genera and 92 species of Palaearctic Notodontidae, as well as the study of the eggs of outgroup species, complexes of characters that are diagnostic, taxonomic or phylogenetic are singled out. It is shown that the egg characteristics are of great taxonomic value at species and generic levels. Some characters are useful for grouping genera. In general, a complex of characters should be used, because different species or genera often share the same characters. Possible apomorphic and plesiomorphic states of the different characters are discussed in relation to the different taxa. The results of this study are discussed with reference to recently published classifications of Notodontidae. As a result of the studies, the keys for identification to the eggs of 43 genera and 92 species of notodontid moths from the Palaearctic region are presented. Reliable diagnostic characters that do not disappear with the injury of eggs or with eggs preserved in alcohol were used. Characters including egg shape, egg and chorion colour, the shape of gnawed holes in eggs when caterpillars hatched, chorionic sculpture, the type of oviposition, foodplants, and geographic distribution of the genera and species were applied. Occasionally, characters that are typical for live eggs, which vary during development, were used. These are characters of egg colour and pattern. The keys are illustrated with photographs made using a digital camera and a scanning electron microscope.
References
Arbogast, R.T., Chauvin, G., Strong, R.G. & Byrd, R.V. (1983) The egg of Endrosis sarcitrella (Lepidoptera: Oecophoridae): Fine structure of the chorion. Journal of Stored Products Research, 19 (2), 63–68.
https://doi.org/10.1016/0022-474X(83)90027-9
Arbogast, R.T., Byrd, R.V., Chauvin, G. & Strong, R.G. (1984) The egg of Pseudospretella (Lepidoptera: Oecophoridae): Fine structure of the chorion. Journal of Lepidopterists’ Society, 38 (3), 202–208.
Barbier, R. & Chauvin, G. (1974) The Aquatic Egg of Nymphula nymphaeata (Lepidoptera: Pyralidae). On the Fine Structure of the Egg Shell. Cell and Tissue Research, 149, 473–479.
https://doi.org/10.1007/BF00223026
Battisti, A., Avci, M., Avtzis, D.N., Jamaa, M.L.B., Berardi, L., Berretima, W., Branco, M., Chakali, G., El Fels, M.A.E.A., Frérot, B., Hódar, J.A., Ionescu-Mălăncuş, I., Ipekdal, K., Larsson, S., Manole, T., Mendel, Z., Meurisse, N., Mirchev, P., Nemer, N., Paiva, M.- R., Pino, J., Protasov, A., Rahim, N., Rousselet, J., Santos, H., Sauvard, D., Schopf, A., Simonato, M., Yart, A. & Zamoum, M. (2015) Natural history of the processionary moths (Thaumetopoea spp.): new insights in relation to climate change. In: Roques, A. (Ed.), Processionary moths and climate change: an update. Hardcover, Springer, pp. 15–79.
Calvo, D. & Molina, J.M. (2008) Morphological aspects of developmental stages of Streblote panda (Lepidoptera: Lasiocampidae). Annales de la Société Entomologique de France, 44 (1), 37–46.
https://doi.org/10.1080/00379271.2008.10697542
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, 29–46.
https://doi.org/10.1590/S0073-47212005000100006
Dolinskaya, I.V. (1984) Chrysalid morphology of certain notodontid moth species (Lepidoptera, Notodontidae). Vestnik zoologii, 4, 54–60. [in Russian]
Dolinskaya I.V. (1986) Chrysalid morphology of certain Notodontid moth species (Lepidoptera, Notodontidae) of the fauna of the USSR. Vestnik zoologii, 2, 59–66. [in Russian]
Dolinskaya, I.V. (1987a) Morphology of the eggs of the Notodontidae (Lepidoptera) of the fauna of the USSR. Communication 1. Vestnik zoologii, 1, 65–74. [in Russian]
Dolinskaya, I.V. (1987b) Morphology of the eggs of the Notodontidae (Lepidoptera) of the fauna of the USSR. Communication 2. Vestnik zoologii, 2, 50–60. [in Russian]
Dolinskaya, I.V. (1987c) Morphology of the eggs of certain Notodontid moth species (Lepidoptera, Notodontidae). In: Savchenko E.N. (Ed.), Fauna i biocenoticheskie svjazi nasekomykh Ukrainy. Naukova dumka, Kiev, pp. 40–42. [in Russian; English summary]
Dolinskaya, I.V. (1989) Morphology of the pupae of the Notodontidae (Lepidoptera) from Russian Far East. Vestnik zoologii, 5, 60–67. [in Russian]
Dolinskaya, I.V. (1990) Egg morphology of Notodontid moths of the USSR. Entomological Review, 69 (2), 67–80.
Dolinskaya I.V. (1993) Characteristics of Notodontid moth (Lepidoptera, Notodontidae). Communication 1. Key to Genera based on pupal characters. Vestnik zoologii, 5, 39–43. [in Russian]
Dolinskaya, I.V. (2008) Taxonomic variation in larval mandibular structure in Palaearctic Notodontidae (Noctuoidea). Nota lepidopterologica, 31 (2), 179–191.
Dolinskaya, I.V. (2010) The chorionic sculpture in eggs of some Hadeninae from Ukraine (Lepidoptera, Noctuidae). Ukrainska Entomofaunistyka, 1 (3), 3–15.
Dolinskaya, I.V. (2011a) Larval head microsculpture in Palaearctic Notodontidae (Noctuoidea) and its significance for the systematics of the family. Nota lepidopterologica, 34 (1), 11–28.
Dolinskaya, I.V. (2011b) The chorionic sculpture of the eggs of some Xyleninae (Lepidoptera, Noctuidae). Vestnik zoologii, 45 (1), 41–56.
https://doi.org/10.2478/v10058-011-0002-9
Dolinskaya, I.V. (2012) Species composition and biological peculiarities of Ukrainian Notodontidae (Lepidoptera). Euroasian Entomological Journal, 11(5), 465–485. [in Russian]
Dolinskaya, I.V. (2013) Diversity of the larval cranial setae in Palearctic Notodontidae (Noctuidae) and their taxonomic distribution. Vestnik zoologii, 47 (1), 27–37.
https://doi.org/10.2478/vzoo-2013-0002
Dolinskaya, I.V. (2014a) Egg morphology of some Noctuidae (Lepidoptera). Vestnik zoologii, 48 (4), 353–364.
https://doi.org/10.2478/vzoo-2014-0043
Dolinskaya, I.V. (2014 b) Egg morphology of some Nolidae and Erebidae (Lepidoptera, Noctuoidea). Vestnik zoologii, 48 (6), 553–561.
https://doi.org/10.2478/vzoo-2014-0066
Dolinskaya, I.V. (2016 a) Comparative morphology on the egg chorion characters of some Noctuidae (Lepidoptera). Zootaxa, 4085 (3), 374–392.
http://dx.doi.org/10.11646/zootaxa.4085.3.3
Dolinskaya, I.V. (2016 b) Key to the species of Ukrainian Notodontid Moths (Lepidoptera, Notodontidae) on the egg characters. Vestnik Zoologii, 50 (6), 517–532.
https://doi.org/10.1515/vzoo-2016-0059
Dolinskaya, I.V. & Pljushch, I.G. (1999) Surface structure of the eggshell of some Vapourer moths (Lepidoptera, Lymantriidae). Lambillionea, XC1X (4), 489–502.
Dolinskaya, I.V. & Pljushch, I.G. (2000) External morphology of the eggs of some Lappet-moth (Lepidoptera, Lasiocampidae). Vestnik zoologii, 34, 3, 49–60.
Dolinskaya, I.V. & Pljushch, I.G. (2003) Review of the main morphological characters of the palaearctic notodontid larvae (Lepidoptera, Notodontidae). Communication 1. Lambillionea, CIII, 4, 607–624.
Dolinskaya, I.V. & Geryak, Yu.N. (2010) The chorionic sculpture of the eggs of some Noctuinae (Lepidoptera, Noctuidae) from Ukraine. Vestnik zoologii, 44 (5), 421–432.
https://doi.org/10.2478/v10058-010-0028-4
Dolinskaya, I.V. & Ponomarenko, M.G. (2013) The chorionic sculpture in eggs of some Noctuidae (Lepidoptera). Vestnik zoologii, 47 (5), 431–439.
https://doi.org/10.2478/vzoo-2013-0046
Döring, E. (1955) Zur Morphologie der Schmetterlingseier. Berlin, Akademie-Verlag, 154 pp.
Downey, J.C. & Allyn, A.C. (1980) Eggs of Riodinidae. Journal of the Lepidopterists’ Society, 34 (2), 133–145.
Fehrenbach, H. (2003) 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, NY, pp. 469–493.
Fehrenbach, H., Dittrich, V. & Zissler, D. (1987) Eggshell fine structure of three lepidopteran pests: Cydia pomonella (L.) (Tortricidae), Heliothis virescens (Fabr.), and Spodoptera littoralis (Boisd.) (Noctuidae). International Journal of Insect Morphology and Embryology, 16 (3-4), 201–219.
https://doi.org/10.1016/0020-7322(87)90021-3
Freitas, A.V.L. & Brown, K.S. (2004) Phylogeny of the Nymphalidae (Lepidoptera). Systematic Biology, 53, 363–383.
https://doi.org/10.1080/10635150490445670
García-Barros, E. & Martín, J. (1995) The eggs of European satyrine butterflies (Nymphalidae): external morphology and its use in systematics. Zoological Journal of the Linnean Society, 115, 73–115
http:s//doi.org/10.1111/j.1096-3642.1995.tb02324.x
Gautam, S.G., Opit, G.P., Margosan, D. Tebbets, J.S. & Walse, S. (2014) Egg Morphology of Key Stored-Product Insect Pests of the United States. Annals of the Entomological Society of America, 107 (1), 1–10.
https://doi.org/10.1603/AN13103
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
Hinton, H.E. (1981) Biology of Insect eggs. 3 Vols. Pergamon Press, Oxford, 1125 pp.
Kitching,. I.J. (1985) Early stages and the classification of the milkweed butterflies (Lepidoptera: Danainae). Zoological Journal of the Linnean Society, 85, 1–97.
https://doi.org/10.1111/j.1096-3642.1985.tb01516.x
Kitching, I.J. & Rawlins, J.E. (1999) The Noctuoidea. In: Kristensen, N.P. (Ed.), Lepidoptera: moths and butterflies. Vol. 1. Evolution, systematics, and biogeography. Walter de Gruyter, Berlin, pp. 355–401.
Kobayashi, Y. & Gibb, G.W. (1995) The Early Embryonic Development of the Mnesarchaeid Moth, Mnesarchaea fusilella Walker (Lepidoptera: Mnesarchaeidae) and its Phylogenetic Significance. Australian Journal of Zoology, 1995, 43, 479–488.
https://doi.org/10.1071/ZO9950479
Kobayashi, H. & Nonaka, M. (2016) Molecular phylogeny of the Notodontidae: Subfamilies inferred from 28S rRNA sequences (Lepidoptera, Noctuoidea, Notodontidae). Tinea, 23 (Supplement 1), 83 pp.
Korycinska, A. (2012) A description of the eggs of seven species of Noctuidae (Lepidoptera) commonly transported by plant trade to the UK, and their separation using stereomicroscopy and scanning electron microscopy. Tijdschrift voor Entomologie, 155, 15–28.
https://doi.org/10.1163/221194312X651391
Kumar, V. & Kamble, C.K. (2008) Scanning electron microscope study on the egg chorion of silkmoth, Antheraea assamensis Helf. (Lepidoptera : Saturniidae). Animal Biology, 58, 235–244.
https://doi.org/10.1163/157075608X328071
Llanderal-Cázares, C., Castro-Torres, R. & Miranda-Perkins, K. (2017) Bionomics of Comadia redtenbacheri (Hammerschmidt, 1847) (Lepidoptera: Cossidae), Shilap Revista de Lepidopterología, 45 (179), 373–383.
Llorente-Bousquets, J. & 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 Exactas, 31 (18), 145–164.
Llorente-Bousquets, J., Nieves-Uribe, S., Flores-Gallardo, A., Hernández-Mejia, B.C. & Castro-Gerardino, J. (2018) Chorionic sculpture of eggs in the subfamily Dismorphiinae (Lepidoptera: Papilionoidea: Pieridae). Zootaxa, 4429 (2), 201–246.
https://doi.org/10.11646/zootaxa.4429.2.1
Margaritis, L.H. (1985) Structure and physiology of the eggshell. In: Kerkut, G.A. & Gilbert, L.I. (Eds.), Comprehensive Insect Phisiology Biochemistry and Pharmacology. Vol. I. Pergamon, Elmsford, New York, pp. 1583–230.
Margaritis, L.H. & Mazzini, M. (1998) Structure of the egg. In: Harrison, F.W. & Locke, M. (Eds.), Microscopic Anatomy of Invertebrates. Vol. 11b. Insecta. Wiley-Liss, New York, pp. 995–1037.
Marini, M. & Trentini, M. (1989) SEM morphological observations of Papilio hospiton Gn. 1839 and P. machaon L. 1758 eggs (Lepidoptera: Papilionidae). Nota lepidopterologica, 12 (3), 175–178.
Markin, G.P., Nagata, R.F. & Taniguchi, G. (1989) Biology and behavior of the South American moth, Cyanotricha necyria (Felder) (Lepidoptera: Notodontidae), a potential biocontrol agent in Hawaii of the forest weed, Passiflora mollissima (HBK) Bailey. Proceedings of the Hawaiian Entomological Society, 29, 115–123.
Masoodi, M.A. (1991) Biological studies on Lymantria obfuscata Walker (Lepidoptera: Lymantriidae) in Kashmir. Indian Forester, 117, 644–651.
Matov, A.Yu., Dubatolov, V.V. (2008) Notodontidae. In: Sinev, S. Yu. (Ed.), Catalogue of the Lepidoptera of Russia. KMK Scientific Press, Moscow, pp. 233–237. [in Russian; English summary]
Matsunura, S. (1929) Generic revision of the Palaearctic Notodontidae. Insecta Matsumurana, 4, 78–93.
McFarland, N. (1972) Egg photographs depicting 40 species of Southern Australian moths. Journal of Research on the Lepidoptera, 10 (3), 215–247.
Miller, G.L. & Williams, M.L. (1986) Ultrastructure of the egg of the Azalea caterpillar, Datana major Grote & Robinson (Notodontidae). Journal of the Lepidopterists’ Society, 40 (4), 318–321.
Miller J.S. (1991) Cladistics and classification of the Notodontidae (Lepidoptera: Noctuoidea) based on larval and adult morphology. Bulletin of the American Museum of Natural History, 204, 1–230, 541 figs., 8 tbls.
Miller, J.S. (1992) Pupal morphology and the subfamily classification of the Notodontidae (Lepidoptera: Noctuoidea). Journal of the New York Entomological Society, 100, 228–256.
Miller, J.S. (2009) Generic Revision of the Dioptinae (Lepidoptera: Noctuoidea: Notodontidae) Part 1: Dioptini. Bulletin of the American Museum of Natural History, 321, 1–1022.
Miller, J.S. & Otero, L.D. (1994) Immature stages of Venezuelan Dioptinae (Notodontidae) in Josia and Thirmida. Journal of the Lepidopterists’ Society, 48, 338–372.
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
Nakamura, M. (2007) Pupae of Japanese Notodontidae (Lepidoptera). Tinea, 19, 293–328.
Nakatomi, K. (1987) Notodontidae. In: Sugi, S. (Ed.), Larvae of Larger Moths in Japan. Kodansha, Tokyo, pp. 1–453, 120 pls. [in Japanese with English summary]
Nassig, W.A. (1988) A rearing of the caterpillars of Cerura malaysiana Holloway 1982 (Lep., Notodontidae). Heterocera Sumatrana, 2 (6), 59–66.
Ng Yuk Chau (1939) Notes on Melalopha anastomosis (L.) and M. anachoreta (F.) (Lep., Notodontidae). Lingnan Science Journal. 17, 1, 63–69.
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
Pascual, J.A. (1988) Descripción morfológica de los estados preimaginales (puesta, larva y crisálida) de Thaumetopoea processionea L. (Lep. Thaumetopoeidae). Boletín de Sanidad Vegetal Plagas, 14, 249–263.
Peterson, A. (1963) Some eggs of moths among the Amatidae, Arctiidae, and Notodontidae—Lepidoptera. The Florida Entomologist, 46 (2), 169–182.
https://doi.org/10.2307/3493627
Pinheiro, L.R., Silva, R.O. & Duarte, M. (2011) Immature stages of the moth Lobeza dentilinea (Lepidoptera: Notodontidae), with redescription of the species based on male and female morphology. Zoologia, 28 (4), 517–524.
https://doi.org/10.1590/S1984-46702011000400014
Pljushch, I.G. & Dolinskaya, I.V. (2000a) External morphology of the eggs of some Tiger-moths (Lepidoptera, Arctiidae). Lambillionea, C (1), 33–41.
Pljushch, I.G. & Dolinskaya, I.V. (2000 b) Eggshell fine structure of some species of Lithosiinae (Arctiidae) of Far East Russia. Nota lepidopterologica, 23 (1), 50–63.
Pljushch, I.G. & Dolinskaya, I.V. (2001) The features of chorionic surface structures of some species of Saturniidae, Brahmaeidae and Sphingidae of Far East Russia (Lepidoptera, Bombycoidea). Lambillionea, CI (1), 11–22.
Povel, G.D.E. (1984) The identification of the European small ermine moths, with special reference to the Yponomeuta padellus-complex (Lepidoptera, Yponomeutidae). Proceedings of the Koninklijke Nederlandse Akademie Van Wetenschappen, Series C, 87 (2), 149–180.
Pratt, P.D., Herdocia, K., Valentin, V., Makinson, J., Purcell, M.F., Mattison, E., Rayamajhi, M.B., Moran, P. & Raghu, S. (2016) Development rate, consumption, and host fidelity of Neostauropus alternus (Walker, 1855) (Lepidoptera: Notodontidae). The Pan-Pacific Entomologist, 92 (4), 200–209.
https://doi.org/10.3956/2016-92.4.200
Regier, J.C., Paukstadt, U., Paukstadt, L.H., Mitter, C. & Peigler, R.S. (2005) Phylogenetics of Eggshell Morphogenesis in Antheraea (Lepidoptera: Saturniidae): Unique Origin and Repeated Reduction of the Aeropyle Crown. Systematic Biology, 54 (2), 254–267.
https://doi.org/10.1080/10635150590923281
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
Rougerie, R. & Estradel, Y. (2008) Morphology of the Preimaginal Stages of the African Emperor Moth Bunaeopsis licharbas (Maassen and Weyding): Phylogenetically Informative Characters within the Saturniinae (Lepidoptera: Saturniidae). Journal of Morphology, 269, 207–232.
https://doi.org/10.1002/jmor.10562
Salkeld, E.H. (1984) A catalogue of the eggs of some Canadian Noctuidae (Lepidoptera), with comments. Memoirs of the Entomological Society of Canada, 127, 1–167.
Schimitschek, V.E. (1955) Zur Kenntnis des Pappelschädlings Pygaera anastomosis L. (Lep.—Fam. Notodontidae). Anzeiger für Schädlingskunde, 28 (10), 153–156.
Schintlmeister A. (1989) Zoogeographie der palaearktischen Notodontidae (Lepidoptera). Neue Entomologische Nachrichten, 25, 3–117.
Schintlmeister, A. (2008) Notodontidae. Palaearctic Macrolepidoptera. Vol. 1. Apollo Books, Stenstrup, 1–482, 40 pls.
Schintlmeister, A. (2013) Notodontidae and Oenosandridae (Lepidoptera). In: World Catalogue of Insect. Vol. 11. Brill, Leiden, pp. 1–605.
Skudlik, J., Poprawa, I. & Rost, M.M. (2005) The egg capsule of Spodoptera exiqua Hübner, 1808 (Insecta, Lepidoptera, Noctuidae): morphology and ultrastructure. Zoologica Poloniae, 50 (1–4), 25–31.
Suludere, Z. (1991) External morphology of the eggs of Clethrogyna dubia ssp. turcica (Lederer) (Lepidoptera, Lymantriidae). Centre for Entomological Studies Ankara, 12, 1–8.
Takhtajan, A. (1987) Systema Magnoliophytorum. Officina Editoria “Nauka”, Leninopoli, 438 pp. [in Russian].
Templado, J. & Ortiz, E. (1969) Caracteres comparativos entre Dicranura vinula L. y Dicranura iberica Templ.et Ort. (Lep. Notodontidae). Eos, Madrid, 45, 335–347.
Tikhomirov, A.M. (1981) Taxonomic structure of the family Notodontidae and its position in the system of Lepidoptera with regard of functional morphology of genitalia of species from the Far East . Trudy zoologicheskogo Instituta AN SSSR, Leningrad, 103, 62–72. [in Russian]
Weller, S.J. (1987) Litodonta hydromeli Harvey (Notodontidae): description of life stages. Journal of the Lepidopterists’ Society, 41, 187–194.
Wolf, K.W., Murphy, C., Reid, W. & Garraway, E. (2000) Fine structure of the eggshell in Utetheisa ornatrix (Lepidoptera: Arctiidae). Invertebrate Reproduction and Development, 38 (2), 85–94.
https://doi.org/10.1080/07924259.2000.9652442
Zolotuhin, V.V. & Kurshakov, P.A. (2011) Fine sculpture and phylogenetic implications of egg shell morphology in the Lasiocampidae (Lepidoptera, Lasiocampidae). Neue Entomologische Nachrichten, 67, 3–21.
Zolotuhin, V.V., Pygaev, S.N., Sinjaev, V.V. & Witt, T. (2011) The biology of Mirinidae with description of preimaginal instars of Mirina confusius Zolotuhin &Witt, 2000 (Lepidoptera, Mirinidae). Tinea, 21 (4), 189–198.