Immature stages of the Brazilian crescent butterfly Ortilia liriope (Cramer) (Lepidoptera: Nymphalidae)

Abstract

We provide the first information on the morphology of the immature stages (egg, larva, and pupa), oviposition and larval behavior, and host plant, for the Brazilian crescent butterfly Ortilia liriope (Cramer), based on material from Santarém Municipality, Pará State, Northern Brazil. Females of O. liriope lay eggs in clusters. After hatching, larvae eat the exochorion and remain gregarious in all but the final instar. The host plant recorded in the study site is Justicia sp. (Acanthaceae). Despite the scarcity of data on the immature stages of Neotropical Melitaeini, we can already say that some morphological and behavioral traits observed in the immature stages of O. liriope are also present in all known genera in this tribe.

Acanthaceae; gregarious caterpillar; Justicia; Melitaeini; Phyciodina


SYSTEMATICS, MORPHOLOGY AND PHYSIOLOGY

Immature stages of the Brazilian crescent butterfly Ortilia liriope (Cramer) (Lepidoptera: Nymphalidae)

PL SilvaI; NP OliveiraI; EP BarbosaII; Y OkadaI; LA KaminskiII; AVL FreitasII

ILab de Zoologia, Programa de Biologia, Instituto de Ciências da Educação, Univ Federal do Oeste do Pará, Santarém, PA, Brasil

IIDepto de Biologia Animal, Instituto de Biologia, Univ Estadual de Campinas, Campinas, SP, Brasil

Correspondence

ABSTRACT

We provide the first information on the morphology of the immature stages (egg, larva, and pupa), oviposition and larval behavior, and host plant, for the Brazilian crescent butterfly Ortilia liriope (Cramer), based on material from Santarém Municipality, Pará State, Northern Brazil. Females of O. liriope lay eggs in clusters. After hatching, larvae eat the exochorion and remain gregarious in all but the final instar. The host plant recorded in the study site is Justicia sp. (Acanthaceae). Despite the scarcity of data on the immature stages of Neotropical Melitaeini, we can already say that some morphological and behavioral traits observed in the immature stages of O. liriope are also present in all known genera in this tribe.

Keywords: Acanthaceae, gregarious caterpillar, Justicia, Melitaeini, Phyciodina

Introduction

Melitaeini, one of the six recognized tribes of the Nymphalinae (Nymphalidae), is a relatively small group of ca. 250 butterfly species present only in the Holarctic and Neotropical regions (Wahlberg & Freitas 2007, Wahlberg et al 2009). The group is considered monophyletic (Zimmermann et al 1999, Freitas & Brown 2004, Wahlberg et al 2005), and the few clear synapomorphies consist of characters of male and female genitalia (Higgins 1981, Kons 2000).

The Melitaeini are divided into five distinct clades, including the subtribes Euphydryina, Melitaeina and Phyciodina, the Chlosyne-group, and the Gnathotriche-group (Wahlberg & Zimmermmann 2000, Wahlberg et al 2005). General information about Melitaeini is not evenly distributed among the five clades, being clearly biased towards the temperate Euphydryina and Melitaeina species (Wahlberg & Freitas 2007).

Phyciodina is composed mainly of tropical species, and alone comprises almost half of all species of Melitaeini. In spite of that, data on basic natural history for this subtribe, such as descriptions of early stages and host plants, are known for only a small fraction of the species (Beccaloni et al 2008).

The genus Ortilia Higgins was erected based on poorly defined characters of male genitalia, and originally included 10 species of typically orange-black melitaeines (Higgins 1981), which later were reorganized to represent nine species by Lamas (2004). Recently, a molecular study by Wahlberg & Freitas (2007) showed that Ortilia is in fact a polyphyletic assemblage, with their members distributed among three distinct clades within the Phyciodina. Thus far, immatures have not been described in detail for any species of Ortilia (sensu Lamas 2004), and information on host plant use remains scarce and uncertain (Beccaloni et al 2008, Neild 2008).

Ortilia liriope (Cramer) (Fig 1a), the type species of the genus, together with Ortilia gentina Higgins and Mazia amazonica (Bates) (Wahlberg & Freitas 2007) form a clearly distinct clade. The species occurs in northern South America, in Amazonia, usually in association with open sunny areas, such as tree gaps, forest edges and secondary forests. The present paper describes the early stages of O. liriope, compares the immatures with those of other known Melitaeini, and briefly discusses host plant use within the Phyciodina.

   

Material and Methods

Adults and immature of O. liriope were collected near the Urumari stream (2º27'S, 54º41'W), in the suburban area of Santarém Municipality, Pará State, Northern Brazil, in 2009-2010. Descriptions of immature stages are based on egg clusters collected in nature on the host plant Justicia sp. (Acanthaceae), and reared in laboratory following standard procedures for larval rearing (Freitas 1991) with food ad libitum using another species, Justicia brasiliana, that was well accepted by the larvae. Data were taken on behavior and development times for all stages. Measurements and general morphology were assessed using a Leica® MZ7.5 stereomicroscope equipped with a micrometric scale. Egg size was measured as height and width. The size of the larval head capsule was measured as the distance between the most external stemma (as in Freitas & Brown 2008). Head and body chaetotaxy were described following Stehr (1987). Immatures were fixed in Kahle solution (Triplehorn & Johnson 2005); all adults, preserved larvae, head capsules, and pupal skins were deposited at Unicamp (Museu de Zoologia, ZUEC).

Results

Natural history

At the study site, O. liriope was observed using Justicia sp. as its larval host plant. Females of O. liriope laid eggs in clusters of about 50-60 eggs (n = 2). Oviposition occurred with the female sitting on the upper surface of the leaf and curling the abdomen around the leaf edge so that eggs were deposited under the leaf.

After hatching, larvae ate the exochorion and remain aggregated until the final instar. Most larvae passed through five instars, but some have an extra, sixth stadium (18 out of 157 individuals). Final instars dispersed to feed solitarily until pupation. In the first two instars, larvae fed by scraping the under surface of the leaf, but in later instars they fed on the whole leaf, leaving only the largest veins. Prepupae hung from a support by the anal prolegs, curling the body in a ring with the head almost touching the apex of the abdomen (Fig 1j).

Description of immature stages

Egg (Fig 1b-c). Width (diameter) 0.46-0.56 mm, height 0.54-0.64 mm (n = 10). Light yellow, remaining unchanged until hatching. Pear-shaped with a conspicuously pointy apex; with 19-21 poorly defined vertical ridges and numerous inconspicuous horizontal ridges. Duration: five days (n = 15).

First instar (Figs 1d, 2, 3a). Head capsule width 0.30 mm (n = 10). Maximum body length 4.0 mm. Head capsule dark brown, without horns or spines. Body translucent, with dark green gut contents clearly visible; legs, prolegs and anal plate light beige; setae relatively long (ratio between setal length/segment height c. 1.2); setae above spiracles are black, and light below. Frontal head chaetotaxy and lateral body chaetotaxy are shown in Figs 2 and 3a, respectively; in the body the ventral group of setae is present, but is not shown. Duration: 3-5 days (n = 30).

   

Second instar (Fig 1e). Head capsule width 0.40-0.48 mm (n = 10). Maximum body length 6.0 mm. Head capsule light brown, with conspicuous long brown setae and without horns or spines. Body dark green dorsally, white ventrally; covered with short light brown scoli from T2 through A10; T1 without scoli, but bearing long black setae; legs brown, prolegs Third translucent, anal plate light brown. Scoli distribution remains the same until the final instar (Fig 3b). Duration: 2-3 days (n = 30).

Third instar (Fig 1f). Head capsule width 0.56-0.68 mm (n = 10). Maximum body length 11 mm. Head capsule orange-brown with black stemmata. Body dark greenish brown dorsally, light cream ventrally on abdominal segments; scoli dark brown, except for the subspiracular abdominal series, which is light cream; legs brown, prolegs translucent, anal plate brown. Duration: 3-4 days (n = 30).

Fourth instar (Fig 1g). Head capsule width 1.00-1.30 mm (n = 10). Maximum body length 16 mm. Head capsule color and shape as in previous instar. Body dark brown dorsally, light cream ventrally in abdominal segments; scoli dark brown, except for the subspiracular abdominal series, which is light cream; legs dark brown, prolegs translucent, anal plate brown. Duration: four days (n = 30).

Fifth (last) instar (Figs 1h-i). Head capsule width 1.90-2.04 mm (n = 6). Maximum body length 19 mm. Head capsule reddish brown with black stemmata; shape as in previous instar. Body dark brown dorsally, light cream ventrally in abdominal segments; scoli dark brown, except for the subspiracular abdominal series, which is light cream; legs dark brown, prolegs translucent, anal plate brown. Duration: six days (n = 30). Some larvae can have six instars; in these larvae, the fifth instar can reach 19 mm in length, but with the head capsule more similar in size to those of the fourth instar (head width 1.20 mm - 1.48 mm). Prepupa without marked changes in coloration (Fig 1j).

Pupa (Figs 1k-m). Length 11-12 mm (n = 14). Light brown with sparse darker marks all over the wing caps and abdomen. General profile elongated; ocular caps short and pointed like little cat ears. A series of short subdorsal pointed knobs from T2 through A7 segments as follows: T2-A1 with one subdorsal pair, those of T2 conspicuously enlarged and positioned over a pronounced bump; A2-A3 and A5-A7 with a single dorsal knob in addition to the subdorsal pair; A4 with a conspicuous transverse keel bearing five enlarged knobs, a single dorsal knob and two subdorsal pairs; all remaining segments without knobs (T1, A8-A10). Cremaster broad, dark brown. Abdominal segments beyond wing pad apices mobile. Duration: six days (n = 10).

Discussion

Host plant use

The genus Justicia used by O. liriope at the study site is used by several other species of Phyciodina (Beccaloni et al 2008). Unfortunately, reliable host plant records are available for very few species of Phyciodina, thus no additional discussion on patterns of host plant use in this subtribe is possible.

Although Nymphalinae displays a diversity of host plant use (Beccaloni et al 2008, Talsma et al 2008, Janzen & Hallwachs 2010), species of the subtribe Phyciodina have been reported on only a few host plants, mainly pertaining to Asteraceae and Acanthaceae, with scattered records on Verbenaceae and Scrophulariaceae (Scott 1986, Feldman & Haber 1998, Beccaloni et al 2008). Additional reports of other host plant families used by Phyciodina await confirmation (Beccaloni et al 2008).

Morphology of the immature stages

A number of morphological and behavioral traits observed in the immature stages of O. liriope are present in all known Melitaeini. These include egg clusters and gregarious larvae, absence of head horns, and the body scoli short and densely branched (Young 1973, DeVries 1987, Freitas 1991).

The pale yellow egg with weakly marked ridges is common to species spread throughout the Melitaeini (Young 1973, Freitas 1991, Wahlberg 2000). The number of vertical ridges appears to be quite variable among Melitaeini (from 18 to 23) (Scott 1973, Wahlberg 2000), and the eggs of O. liriope do fit the reported range. Pear-shaped eggs, with a conspicuously pointy apex, have been described for the following taxa of Phyciodina: Anthanassa frisia hermas (Hewitson) (D'Almeida 1941), Eresia ithomioides alsina Hewitson (Young 1973), Eresia lansdorfi (Godart), Ortilia ithra (Kirby) (AVLF unpublished data) and Tegosa claudina (Eschscholtz) (Toledo 1979, Freitas 1991). In all other known Melitaeini, the eggs have a flattened apex, including species of the genera Chlosyne Butler (Scott 1986, AVLF unpublished results), Euphydryas Scudder (Williams et al 1984, Wahlberg 2000), Melitaea Fabricius (Wahlberg 1997, 2000) and Phyciodes Hübner (McDunnough 1920, Genc et al 2003).

The setae present in the first instar of O. liriope are relatively long (longer than the segment height) compared with many other Nymphalidae groups (Freitas et al 1997, Freitas & Brown 2004). Long setae appear to be a widespread feature in Nymphalinae except for the Coeini (Scott 1973, Nakanishi 1988, Freitas 1999), and this character was considered a good synapomorphy of Nymphalinae (Freitas & Brown 2004). The distribution of body scoli in the remaining instars is similar to those of all known Melitaeini (Freitas 1991, Wahlberg 1997).

The pupa of O. liriope is very similar in general shape to those of Tegosa (Toledo 1979, Freitas 1991) and Phyciodes (McDunnough 1920, Scott 1986, Gatrelle 2004), both of which have a conspicuous keel on A4. This keel has not been observed in any of the other Melitaeini genera cited above, and might be of taxonomic importance.

Unfortunately, further comparisons regarding immature morphology and host plant use are not possible at the moment due to the general lack of information, especially for Neotropical species. Based on the sparse published information concerning the immature stages, Phyciodina have usually been considered a homogeneous group. The present results suggest that this picture could change easily once more information has been added to the few data available.

Acknowledgments

We are very grateful to Fosca P P Leite for allowing us to use the stereomicroscope for some larval measurements and to Chieno Suemitsu for the identification of the host plant species. We also thank Harri Lorenzi and Edgar F Souto from the Instituto Plantarum for the donation of host plants for rearing the larvae, and Daniela Rodrigues, Keith Willmott, Niklas Wahlberg, Annette Aiello and Marcelo Duarte for suggestions on the manuscript. AVLF thanks FAPESP (grant 04/05269-9) and the Brazilian CNPq (fellowship 300282/2008-7); LAK thanks CNPq for a fellowship (140183/2006-0); EPB thanks CAPES for a fellowship.

References

Beccaloni GW, Hall SK, Viloria AL, Robinson GS (2008) Catalogue of the hostplants of the Neotropical butterflies / Catálogo de las plantas huésped de las mariposas Neotropicales. In m3m - Monografias Tercer Milenio, Vol. 8. Zaragoza, S.E.A., RIBES-CYTED, The Natural History Museum, Instituto Venezolano de Investigaciones Científicas, 536p.

D'Almeida RF (1941) Contribuição para o conhecimento da biologia do Phyciodes hermas (Hew., 1864) (Lepidoptera, Nymphalididae). Arq Zool 2: 321-324 1 pl.

DeVries PJ (1987) The butterflies of Costa Rica and their natural history. Papilionidae, Pieridae, Nymphalidae. Princeton, Princeton University Press, 327p.

Feldman TS, Haber WA (1998) Oviposition behavior, host plant use, and diet breadth of Anthanassa butterflies (Lepidoptera: Nymphalidae) using plants in the Acanthaceae in a Costa Rican community. Fla Entomol 81: 396-406.

Freitas AVL (1991) Variação morfológica, ciclo de vida e sistemática de Tegosa claudina (Eschscholtz) (Lepidoptera: Nymphalidae: Melitaeinae) no estado de São Paulo, Brasil. Rev Bras Entomol 35: 301-306.

Freitas AVL (1999) Nymphalidae (Lepidoptera), filogenia com base em caracteres de imaturos, com experimentos de troca de plantas hospedeiras. PhD Thesis, Universidade Estadual de Campinas, Campinas, São Paulo. xii + 172p.

Freitas AVL, Brown Jr KS (2004) Phylogeny of the Nymphalidae (Lepidoptera). Syst Biol 53: 363-383.

Freitas AVL, Brown Jr KS (2008) Immature stages of Vila emilia (Nymphalidae: Biblidinae). Trop Lepid Res 18: 74-77.

Freitas AVL, Brown Jr KS, Otero LD (1997) Juvenile stages of Cybdelis, a key genus uniting the diverse branches of the Eurytelinae (Lepidoptera, Nymphalidae). Trop Lepid 8: 29-34.

Gatrelle RR (2004) Description of a multilevel cryptic new species of Phyciodes (Nymphalidae: Melitaeinae) from the Southern Appalachian Mountains. Tax Rep Int Lepid Surv 4: 1-19.

Genc H, Nation JT, Emmel TC (2003) Life history and biology of Phyciodes phaon (Lepidoptera: Nymphalidae). Fla Entomol 86: 445-449.

Higgins LG (1981) A revision of Phyciodes and related genera, with a review of the classification of the Melitaeinae. Bull Br Mus (Nat Hist) Entomol 43: 77-243.

Janzen DH, Hallwachs W (2010) Dynamic database for an inventory of the macrocaterpillar fauna and its food plants and parasitoids of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica (nn-SRNP-nnnnn voucher codes) <http://janzen.sas.upenn.edu>

Kons Jr HL (2000) Phylogenetic studies of the Melitaeini (Lepidoptera: Nymphalidae: Nymphalinae) and a revision of the genus Chlosyne Butler. PhD Thesis, University of Florida, 799p.

Lamas G (2004) Nymphalinae, p.249-257. In Lamas G (ed) Checklist: Part 4A. Hesperioidea-Papilionoidea. In Heppner JB (ed) Atlas of Neotropical Lepidoptera. Volume 5A. Gainesville, Association for Tropical Lepidoptera, Scientific Publishers. xxxiv + 439p.

McDunnough J (1920) Notes on the life history of Phyciodes batesi Reak. (Lepid.). Can Entomol 52: 56-59 1 pl.

Nakanishi A (1988) Study on the first instar larvae of the Subfamily Nymphalinae (Lepidoptera, Nymphalidae). Spec Bull Lep Soc Jap 6: 83-99.

Neild AFE (2008) The butterflies of Venezuela, Part 2: Nymphalidae II (Acraeinae, Libytheinae, Nymphalinae, Ithomiinae, Morphinae). Greenwich, London, Meridian Publications. 272p.

Scott JA (1973) Early stages and biology of Phyciodes orseis (Nymphalidae). J Res Lepid 12: 236-242.

Scott JA (1986) The butterflies of North America: a natural history and field guide. Stanford, Stanford University Press. xiii + 583p.

Stehr FW (1987) Order Lepidoptera. In Stehr FW (ed) Immature insects. Dubuque, Kendall/Hunt 1: 288-305.

Talsma JHR, Torri K, van Nouhuys S (2008) Host plant use by the Heath fritillary butterfly, Melitaea athalia: plant habitat, species and chemistry. Arthropod Plant Interac 2: 63-75. doi: 10.1007/s11829-008-9039-2.

Toledo ZDA (1979) Fauna del NOA. Contribución al conocimiento de los lepidópteros argentinos. VII. Phyciodes claudina (Eschscholtz) (Lepidoptera, Nymphalidae). Acta Zool Lilloana 33: 67-74.

Triplehorn CA, Johnson NF (2005) Borror and Delong's introduction to the study of the insects. 7th Edition. Belmont, C A. Thomson Brooks/Cole. 864p.

Wahlberg N (1997) The life history and ecology of Melitaea diamina (Nymphalidae) in Finland. Nota Lepidopterol 20: 70-81.

Wahlberg N (2000) Comparative descriptions of the immature stages and ecology of five Finnish melitaeine butterflies species (Lepidoptera: Nymphalidae). Entomol Fenn 11: 167-174.

Wahlberg N, Zimmermann M (2000) Pattern of phylogenetic relationships among members of the Tribe Melitaeini (Lepidoptera: Nymphalidae) inferred from mitochondrial DNA sequences. Cladistics 16: 347-363. doi:10.1006/clad.2000.0136

Wahlberg N, Freitas AVL (2007) Colonization of and radiation in South America by butterflies in the subtribe Phyciodina (Lepidoptera: Nymphalidae). Mol Phylogenet Evol 44: 1257-1272. doi:10.1016/j.ympev.2007.04.012.

Wahlberg N, Brower AVZ, Nylin S (2005) Phylogenetic relationships and historical biogeography of tribes and genera in the subfamily Nymphalinae (Lepidoptera: Nymphalidae). Biol J Linn Soc Biol 86: 227-251.

Wahlberg N, Leneveu J, Kodandaramaiah U, Peña C, Nylin S, Freitas AVL, Brower AVZ (2009) Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proc R Soc Biol Sci Ser B 276: 4295-4302. doi: 10.1098/rspb.2009.1303

Williams EH, Holdren CE, Ehrlich PR (1984) The life history and ecology of Euphydryas gillettii Barnes (Nymphalidae). J Lepid Soc 38: 1-12.

Young AM (1973) Notes on the biology of Phyciodes (Eresia) eutropia (Lepidoptera: Nymphalidae) in a Costa Rican Mountain Forest. J N Y Entomol Soc 81: 87-100.

Zimmermann M, Albert J, Descimon H (1999) Systemátique moléculaire des Mélitees. C R Acad Sci Serie III Sci Vie 322: 429-439.

Received 07 May 2010 and accepted 13 October 2010

Edited by Marcelo Duarte - MZ/USP

  • Beccaloni GW, Hall SK, Viloria AL, Robinson GS (2008) Catalogue of the hostplants of the Neotropical butterflies / Catálogo de las plantas huésped de las mariposas Neotropicales. In m3m - Monografias Tercer Milenio, Vol. 8. Zaragoza, S.E.A., RIBES-CYTED, The Natural History Museum, Instituto Venezolano de Investigaciones Científicas, 536p.
  • D'Almeida RF (1941) Contribuição para o conhecimento da biologia do Phyciodes hermas (Hew., 1864) (Lepidoptera, Nymphalididae). Arq Zool 2: 321-324 1 pl.
  • DeVries PJ (1987) The butterflies of Costa Rica and their natural history. Papilionidae, Pieridae, Nymphalidae. Princeton, Princeton University Press, 327p.
  • Feldman TS, Haber WA (1998) Oviposition behavior, host plant use, and diet breadth of Anthanassa butterflies (Lepidoptera: Nymphalidae) using plants in the Acanthaceae in a Costa Rican community. Fla Entomol 81: 396-406.
  • Freitas AVL (1991) Variação morfológica, ciclo de vida e sistemática de Tegosa claudina (Eschscholtz) (Lepidoptera: Nymphalidae: Melitaeinae) no estado de São Paulo, Brasil. Rev Bras Entomol 35: 301-306.
  • Freitas AVL (1999) Nymphalidae (Lepidoptera), filogenia com base em caracteres de imaturos, com experimentos de troca de plantas hospedeiras. PhD Thesis, Universidade Estadual de Campinas, Campinas, São Paulo. xii + 172p.
  • Freitas AVL, Brown Jr KS (2004) Phylogeny of the Nymphalidae (Lepidoptera). Syst Biol 53: 363-383.
  • Freitas AVL, Brown Jr KS (2008) Immature stages of Vila emilia (Nymphalidae: Biblidinae). Trop Lepid Res 18: 74-77.
  • Freitas AVL, Brown Jr KS, Otero LD (1997) Juvenile stages of Cybdelis, a key genus uniting the diverse branches of the Eurytelinae (Lepidoptera, Nymphalidae). Trop Lepid 8: 29-34.
  • Gatrelle RR (2004) Description of a multilevel cryptic new species of Phyciodes (Nymphalidae: Melitaeinae) from the Southern Appalachian Mountains. Tax Rep Int Lepid Surv 4: 1-19.
  • Genc H, Nation JT, Emmel TC (2003) Life history and biology of Phyciodes phaon (Lepidoptera: Nymphalidae). Fla Entomol 86: 445-449.
  • Higgins LG (1981) A revision of Phyciodes and related genera, with a review of the classification of the Melitaeinae. Bull Br Mus (Nat Hist) Entomol 43: 77-243.
  • Janzen DH, Hallwachs W (2010) Dynamic database for an inventory of the macrocaterpillar fauna and its food plants and parasitoids of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica (nn-SRNP-nnnnn voucher codes) <http://janzen.sas.upenn.edu>
  • Kons Jr HL (2000) Phylogenetic studies of the Melitaeini (Lepidoptera: Nymphalidae: Nymphalinae) and a revision of the genus Chlosyne Butler. PhD Thesis, University of Florida, 799p.
  • Lamas G (2004) Nymphalinae, p.249-257. In Lamas G (ed) Checklist: Part 4A. Hesperioidea-Papilionoidea.
  • In Heppner JB (ed) Atlas of Neotropical Lepidoptera. Volume 5A. Gainesville, Association for Tropical Lepidoptera, Scientific Publishers. xxxiv + 439p.
  • McDunnough J (1920) Notes on the life history of Phyciodes batesi Reak. (Lepid.). Can Entomol 52: 56-59 1 pl.
  • Nakanishi A (1988) Study on the first instar larvae of the Subfamily Nymphalinae (Lepidoptera, Nymphalidae). Spec Bull Lep Soc Jap 6: 83-99.
  • Neild AFE (2008) The butterflies of Venezuela, Part 2: Nymphalidae II (Acraeinae, Libytheinae, Nymphalinae, Ithomiinae, Morphinae). Greenwich, London, Meridian Publications. 272p.
  • Scott JA (1973) Early stages and biology of Phyciodes orseis (Nymphalidae). J Res Lepid 12: 236-242.
  • Scott JA (1986) The butterflies of North America: a natural history and field guide. Stanford, Stanford University Press. xiii + 583p.
  • Stehr FW (1987) Order Lepidoptera. In Stehr FW (ed) Immature insects. Dubuque, Kendall/Hunt 1: 288-305.
  • Talsma JHR, Torri K, van Nouhuys S (2008) Host plant use by the Heath fritillary butterfly, Melitaea athalia: plant habitat, species and chemistry. Arthropod Plant Interac 2: 63-75. doi: 10.1007/s11829-008-9039-2.
  • Toledo ZDA (1979) Fauna del NOA. Contribución al conocimiento de los lepidópteros argentinos. VII. Phyciodes claudina (Eschscholtz) (Lepidoptera, Nymphalidae). Acta Zool Lilloana 33: 67-74.
  • Triplehorn CA, Johnson NF (2005) Borror and Delong's introduction to the study of the insects. 7th Edition. Belmont, C A. Thomson Brooks/Cole. 864p.
  • Wahlberg N (1997) The life history and ecology of Melitaea diamina (Nymphalidae) in Finland. Nota Lepidopterol 20: 70-81.
  • Wahlberg N (2000) Comparative descriptions of the immature stages and ecology of five Finnish melitaeine butterflies species (Lepidoptera: Nymphalidae). Entomol Fenn 11: 167-174.
  • Wahlberg N, Zimmermann M (2000) Pattern of phylogenetic relationships among members of the Tribe Melitaeini (Lepidoptera: Nymphalidae) inferred from mitochondrial DNA sequences. Cladistics 16: 347-363. doi:10.1006/clad.2000.0136
  • Wahlberg N, Freitas AVL (2007) Colonization of and radiation in South America by butterflies in the subtribe Phyciodina (Lepidoptera: Nymphalidae). Mol Phylogenet Evol 44: 1257-1272. doi:10.1016/j.ympev.2007.04.012.
  • Wahlberg N, Brower AVZ, Nylin S (2005) Phylogenetic relationships and historical biogeography of tribes and genera in the subfamily Nymphalinae (Lepidoptera: Nymphalidae). Biol J Linn Soc Biol 86: 227-251.
  • Wahlberg N, Leneveu J, Kodandaramaiah U, Peña C, Nylin S, Freitas AVL, Brower AVZ (2009) Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proc R Soc Biol Sci Ser B 276: 4295-4302. doi: 10.1098/rspb.2009.1303
  • Williams EH, Holdren CE, Ehrlich PR (1984) The life history and ecology of Euphydryas gillettii Barnes (Nymphalidae). J Lepid Soc 38: 1-12.
  • Young AM (1973) Notes on the biology of Phyciodes (Eresia) eutropia (Lepidoptera: Nymphalidae) in a Costa Rican Mountain Forest. J N Y Entomol Soc 81: 87-100.
  • Zimmermann M, Albert J, Descimon H (1999) Systemátique moléculaire des Mélitees. C R Acad Sci Serie III Sci Vie 322: 429-439.

  • Correspondence:
    André V L Freitas
    Depto de Biologia Animal, Instituto de Biologia, Univ Estadual de Campinas
    CP 6109
    13083-970 Campinas, SP, Brasil

Publication Dates

  • Publication in this collection
    21 June 2011
  • Date of issue
    June 2011

History

  • Received
    07 May 2010
  • Accepted
    13 Oct 2010
Sociedade Entomológica do Brasil Sociedade Entomológica do Brasil, R. Harry Prochet, 55, 86047-040 Londrina PR Brasil, Tel.: (55 43) 3342 3987 - Londrina - PR - Brazil
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