Abstracts
This study describes and compares the diverse dorsal and ventral wing color patterns of Brassolini butterflies. Thirty-three species are illustrated, where pattern elements of the nymphalid ground plan are labeled in color. In general, a larger number of pattern elements can be identified on the ventral than on the dorsal surface of both wings, and the forewing has a larger number of discernible pattern elements than the hind wing. The dorsal elements are broad, diffuse, and more difficult to identify against the typically brown brassoline wing background color. Species with a light colored dorsal background served as a guide for our proposal that fewer pattern elements are present dorsally, particularly on the hind wing. Colorful bands or markings generally present on the dorsal surface seem to be associated with specific pattern elements and have correspondence to the ventral pattern. We refer to these as trailing bands, and they constitute a predominant feature of the brassoline dorsal coloration. We propose a subordinate groundplan for brassolines and interpret some of the ventral pattern variation in light of their phylogeny. Dorsal color pattern variation that leads to sexual dimorphism and mimetic resemblance are also discussed.
butterfly; wing color; nymphalid ground plan; eyespots; ocelus; Caligo
Este estudo descreve e compara os diversos padrões de coloração dorsal e ventral das borboletas da tribo Brassolini. Com o objetivo de demarcar os elementos do padrão de base dos ninfalídeos (‘pattern elements of the nymphalid ground plan’), 33 espécies são ilustradas. De maneira geral, o número de elementos-padrão identificados na face ventral é maior do que o da face dorsal em ambas as asas, e a asa anterior contém um número maior de elementos visíveis do que a posterior. Os elementos da face dorsal são mais largos e difusos, e também mais difíceis de identificar devido à usual coloração de fundo marrom escuro dos brassolíneos. Espécies que apresentam coloração de fundo clara serviram como guia para a nossa interpretação de que a superfície dorsal das asas apresenta um número reduzido de elementos-padrão, especialmente a da asa posterior. Faixas ou manchas coloridas que geralmente aparecem na superfície dorsal estão aparentemente associadas com elementos-padrão específicos, e apresentam correspondência com faixas que aparecem na face ventral. Estas faixas (‘trailing bands’) se alastram a partir da borda de certos elementos e constituem uma característica predominante da coloração dorsal dos brassolíneos. Nós propomos um padrão de base para os brassolíneos que é subordinado ao dos ninfalídeos, e utilizamos a filogenia do grupo para interpretar alguns aspectos da variação de elementos-padrão da superfície ventral. As variações de padrão e cor que resultam em dimorfismo sexual e mimetismo são discutidas.
borboleta; coloração das asas; padrão de base dos ninfalídeos; manchas ocelares; ocelo; Caligo
Introduction
Wing colors play vital and diverse roles in Lepidoptera, spanning from physiology (e.g., thermoregulation) to inter and intraspecific interactions. Camouflage, large eyespots for startle or deflection, aposematism and mimicry are notable adaptations that reduce predation risk (e.g., Vane-Wright & Ackery 1984VANE-WRIGHT, R.I., & ACKERY, P.R. 1984. The biology of butterflies. Princeton University Press, Princeton, 429p., Chai 1990CHAI, P. 1990. Relationships between visual characteristics of rainforest butterflies and responses of a specialized insectivorous bird. In Proceedings of a Symposium sponsored by the American Society of Zoologists. College Station, Texas, p.31-60.). Although different in their evolutionary outcome, all of these phenotypic defenses involve impressive modifications of wing pattern elements (Nijhout 1991NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington.). For example, some nymphalid butterflies closely resemble dead leaves, a useful appearance at rest of when feeding on fallen rotting fruit (e.g., Zaretis itys (Cramer, 1777), Nymphalidae, Charaxinae; Kallima inachus (Boisduval, 1846), Nymphalidae, Nymphalinae; see http://biology.duke.edu/nijhout/patterns2.html for a demonstration; last accessed 7 March 2013). In contrast, brightly colored butterflies incur a predation risk that can only be defused if they are chemically protected, mimetic, or too difficult to catch. Among these, mimicry is a particularly complex defense because wing colors play a role in both predator-prey and model-mimic interactions while being also used to mediate male-female, intraspecific communication. In fact, mate-choice experiments suggest that assortative mating based on wing color led to genetic divergence and speciation of the sister taxa Heliconius cydno Doubleday, 1847 and H. melpomene (Linnaeus, 1748) (Nymphalidae, Heliconiinae), which belong to separate mimicry rings (Jiggins et al. 2001JIGGINS, C.D., NAISBIT, R.E., COE, R.L. & MALLET, J. 2001. Reproductive isolation caused by colour pattern mimicry. Nature 411:302-305. http://dx.doi.org/10.1038/35077075
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). Furthermore, instances of female-limited mimicry also demonstrate the importance of color for mate recognition in butterflies (e.g., Kunte 2008KUNTE, K. 2008. Mimetic butterflies support Wallace's model of sexual dimorphism. Proc. R. Soc. B 275:1617-1624. http://dx.doi.org/10.1098/rspb.2008.0171
http://dx.doi.org/10.1098/rspb.2008.0171...
, 2009KUNTE, K. 2009. The diversity and evolution of batesian mimicry in Papilio swallowtail butterflies. Evolution 63:2707-2716. http://dx.doi.org/10.1111/j.1558-5646.2009.00752.x
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), implying a potential tradeoff between defensive coloration and mating success in the male sex.
The utility of color for intraspecific interactions likely depends on light levels in the environment. Not surprisingly, nocturnal moth wing colors do not play a role in mate location, recognition, or courtship; chemical communication is favored instead (e.g., Birch 1970BIRCH, M. 1970. Pre-courtship use of abdominal brushes by the nocturnal moth, Phlogophora meticulosa (L.) (Lepidoptera: Noctuidae). Anim. Behav. 18:310-316. http://dx.doi.org/10.1016/S0003-3472(70)80043-4
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), which also seems to be the case in day-flying moths (e.g., Eisner & Meinwald 1995EISNER, T. & MEINWALD, J. 1995. The chemistry of sexual selection. Proc. Natl. Acad. Sci. USA, 92:50-55. http://dx.doi.org/10.1073/pnas.92.1.50
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). In contrast, butterfly wing colors are commonly used for male-male and male-female interactions, and the highly visible, territorial male Morpho butterflies (Nymphalidae, Satyrinae, Morphini) provide a fitting example of both. While dorsal blue colors have a role in male-male and perhaps male-female interactions (Fruhstorfer 1912FRUHSTORFER, H. 1912. Family: Brassolidae. In Die Gross-Schmetterlinge der Erde (A. Seitz, ed.). Stuttgart, v.5, p.285-332., Penz & DeVries 2002PENZ, C.M. & DEVRIES, P.J. 2002. Phylogenetic analysis of Morpho butterflies (Nymphalidae, Morphinae): implications for classification and natural history. Am. Mus. Novitates, 3374:1-33. http://dx.doi.org/10.1206/0003-0082(2002)374%3C0001:PAOMBN%3E2.0.CO;2
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, DeVries et al. 2010DEVRIES, P.J., PENZ, C. & HILL, R. 2010. Vertical distribution, flight behavior, and evolution of wing morphology in Morpho butterflies. J. Anim. Ecol. 79:1077-1085. http://dx.doi.org/10.1111/j.1365-2656.2010.01710.x
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), the dark and camouflaged ventral wing coloration likely protects both sexes at rest. Thus, the Morpho dorso-ventral differentiation seems to fit the situation described by Oliver et al. (2009)OLIVER, J.C., ROBERTSON, K.A. & MONTEIRO, A. 2009. Accomodating natural and sexual selection in butterfly wing pattern evolution. Proc. R. Soc. B. 276:2369-2375. http://dx.doi.org/10.1098/rspb.2009.0182
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for Bicyclus (Nymphalidae, Satyrinae, Satyrini), where the dorsal color pattern is shaped by sexual selection, while natural selection operates on the camouflaged ventral surface. Members of the Satyrinae tribe Brassolini, sister group to Morphini (Wahlberg et al. 2009WAHLBERG, N., LENEVEU, J., KODANDARAMAIAH, U., PEÑA, C., NYLIN, S., FREITAS, A.V.L. & BROWER, A.V.Z. 2009. Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proc. R. Soc. B. 276:4295-4302. http://dx.doi.org/10.1098/rspb.2009.1303
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), might be under similar selection regimes given the remarkable color pattern differences between their dorsal and ventral wing surfaces.
With few exceptions, Brassolini butterflies are crepuscular. While they may be found feeding or puddling during the day, reproductive activities (mating behavior and oviposition) typically occur at dawn or dusk. Most brassolines are relatively dull colored dorsally, and if their colors have a role in male-female interactions in this butterfly group, then they must be discernible at low light levels of crepuscular hours. Although pattern elements of the nymphalid ground plan are easily recognizable on the ventral surface across the tribe, they are subdued in some taxa and striking in others (e.g., Penetes vs. Caligo). Ventral ripple patterns, striations that resemble windblown sand, are common throughout the Satyrinae (Nijhout 1991NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington.), and excepting Penetes all brassolines have ripple patterns. Ventral eyespots also occur across the tribe exhibiting a wide range of sizes and complexity. With the wings folded at rest some brassolines are camouflaged (e.g., Dynastor napoleon Doubleday, 1849 resembles a dead leaf) while others are quite visible (e.g., some Caligo species have conspicuous eyespots). The richness of color patterns, coupled with differing activity periods (crepuscular vs. diurnal) and flight behaviors, constitute an open field of investigation for this butterfly tribe.
This study represents the first broad survey of color pattern diversity in Brassolini. Here we provide a framework for understanding color pattern variation among genera, which constitutes a required foundation for future work on evolution, development and genetics of wing color patterns in this butterfly group. Ventral patterns are described in detail and dorsal patterns are explained here for the first time. We identify and illustrate pattern elements using the nymphalid ground plan proposed by Schwanwitsch (1924)SCHWANWITSCH, B.N. 1924. On the groundplan of wing-pattern in nymphalids and certain other families of rhopalocerous Lepidoptera. Proc. Zool. Soc. Lond. B. 34:509-528. and Süffert (1927)SÜFFERT, F. 1927. Zur vergleichende analyse der schmetterlingszeichnung. Biol. Zent. Bl. 47:385-413., and modified by Nijhout (1991)NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington.. We then propose a subordinate groundplan for the Brassolini that is placed in a phylogenetic context. Finally, we briefly discuss instances of sexual dimorphism and color convergence across genera.
Material and Methods
1.Specimens, species and illustrations
Appendix 1 lists locality data and museum deposition of 554 specimens from 75 species that were examined directly (73% of the Brassolini species diversity), plus sources of photographs of additional taxa. Thirty-three species are illustrated here (usually male). For economy of space, not all species mentioned in the text are included in the figures, but male and female photographs of most brassolines can be found at http://fs.uno.edu/cpenz/Brassolini.html (last accessed 12 August 2013). Photographs were taken with a Cannon G9 digital camera and processed in Adobe Photoshop (Adobe Systems Inc.). Figures with a color-coded key identifying wing pattern elements were prepared using either the type species or an alternative representative of each genus depending on availability of material and /or particular characteristics of their wing patterns. To document variation, multiple species of the same genus were sometimes illustrated. Although body size varies broadly within Brassolini, all images used to describe pattern elements were converted to a similar size to facilitate comparison (Figures 1-7). Images that illustrate sexual dimorphism and color resemblance across genera are scaled proportionately to life size (Figure 9).
Male wings in ventral view plus a schematic drawing showing color-coded pattern elements. Scale bars: 1 cm. A, Bia actorion, Suriname; B, Narope cyllastros, no data; C, Brassolis sophorae, French Guiana; D, Aponarope sutor, Brazil, Rondônia; E, Dynastor napoleon, Brazil, Santa Catarina; F, Dynastor macrosiris macrosiris, French Guiana.
Male wings in ventral view plus a schematic drawing showing color-coded pattern elements. Scale bars: 1 cm. A, Dasyophthalma rusina, South Brazil; B, Opoptera syme, Brazil, São Paulo; C, Caligopsis seleucida, Peru, Madre de Dios; D, Opoptera aorsa, Brazil, Paraná; E, Eryphanis automedon, Ecuador, Sucumbios; F, Eryphanis bubocula, Costa Rica, Guanacaste.
Male wings in ventral view plus a schematic drawing showing color-coded pattern elements. Scale bars: 1 cm. A, Caligo eurilochus, Ecuador, Sucumbios; B, Caligo atreus, Colombia, Antiochia; C, Caligo martia, Brazil, Santa Catarina; D, Selenophanes cassiope, Peru, Chanchamayo; E, Penetes pamphanis, Brazil, Paraná; F, Catoblepia xanthus, Brazil, Pará.
Male wings in ventral view plus a schematic drawing showing color-coded pattern elements. Scale bars: 1 cm. A, Catoblepia orgetorix championi, Panama, Chiriqui; B, Catoblepia berecynthia, Central Peru; C, Mielkela singularis, Mexico, Chiapas; D, Orobrassolis ornamentalis, Brazil, São Paulo; E, Blepolenis bassus, Brazil; F, Opsiphanes sallei, Peru, Pasco.
Wings in dorsal view (except for A, left side) indicating color-coded pattern elements and trailing bands. Mostly males, except when indicated. Scale bars: 1 cm. A, Opoptera syme, Brazil, São Paulo, ventral view on the left; B, Bia actorion, Suriname; C, Brassolis sophorae, French Guiana; D, Narope cyllastros, no data; E, Dynastor napoleon, Brazil, Santa Catarina; F, Dasyophthalma rusina, female on the left and male on the right, both from South Brazil.
Wings in dorsal view (except for G, left side) indicating color-coded pattern elements and trailing bands. Mostly males, except when indicated. Scale bars: 1 cm. A, Caligopsis seleucida, male on the left and female on the right, both from Peru, Madre de Dios; B, Eryphanis zolvizora, Bolivia; C, Eryphanis bubocula, Costa Rica, Guanacaste; D, Caligo eurilochus, male on the left and female on the right, both from Ecuador, Sucumbios; E, Caligo atreus, Colombia, Antiochia; F, Caligo martia, Brazil, Santa Catarina; G, Caligo oileus, male on the left (in ventral and dorsal views) and female on the right, from Peru, Huanuco and Ayacucho, respectively; H, Caligo arisbe, Brazil; I, Caligo beltrao, Brazil, Santa Catarina.
Male wings in dorsal view (except for E and H, left side) indicating color-coded pattern elements and trailing bands. Scale bars: 1 cm. A, Selenophanes cassiope, Peru, Chanchamayo; B, Selenophanes supremus, Peru, Chanchamayo; C, Penetes pamphanis, Brazil, Paraná; D, Catoblepia xanthus, Brazil, Pará; E, Mielkela singularis, Mexico, Chiapas, ventral view on the left; F, Orobrassolis ornamentalis, Brazil, São Paulo; G, Blepolenis bassus, Brazil; H, Opsiphanes sallei, Peru, Pasco, ventral view on the left; I, Opsiphanes cassina, Ecuador, Sucumbios; J, Opsiphanes boisduvallii, Mexico.
Homology and the identification of pattern elements
Pattern elements of the nymphalid ground plan (NGP) are discrete components of wing color differentiation expressed on the wing surface (Nijhout 1991NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington. and references therein). Within the comparative context of the NGP, the term ‘homology’ is generally used to indicate the repetition of a pattern element among cells on the same wing (serial homology), the mirror image of elements between wing surfaces (dorso-ventral homology), and the equivalence of pattern elements across species. Although the latter clearly corresponds to evolutionary homology (i.e., characters shared by common ancestry), the identification of NGP pattern elements is somewhat subjective and should therefore be considered a hypothesis of homology that might be tested through a genetic or phylogenetic framework. As such, the coding of pattern elements for species included in this study constitutes a set of working hypotheses.
Our method for the identification of NGP pattern elements followed three steps. First, we studied the pattern element variation across nymphalid subfamilies to build a framework for size and color diversity, as well as the sequential location of individual pattern elements along wing cells (topographical correspondence can be used to infer homology; e.g., DePinna 1991DEPINNA, M.C.C. 1991. Concepts and tests of homology in the cladistic paradigm. Cladistics 7:367-394. http://dx.doi.org/10.1111/j.1096-0031.1991.tb00045.x
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, Rieppel & Kearny 2002RIEPPEL, O. & KEARNY, M. 2002. Similarity. Biol J. Linn. Soc. 75:59-82. http://dx.doi.org/10.1046/j.1095-8312.2002.00006.x
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). We did this to be consistent with previous work (Nijhout 1991NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington., 1994NIJHOUT, H.F. 1994. Symmetry systems and compartments in lepidopteran wings: the evolution of a patterning mechanism. Development (Suppl.) 225-233., 2001NIJHOUT, H.F. 2001. Elements of butterfly wing patterns. J. Exp. Zool. (Mol. Dev. Evol.) 291:213-225. http://dx.doi.org/10.1002/jez.1099
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) that formed the basis of more recent research on evolution of development. Second, we examined and compared a large number of species, including all brassoline genera. To account for variation within species, specimens from various localities were studied whenever possible. A large sample size allowed us to use intermediate phenotypes as clues for the identification of pattern elements within and between genera (as suggested by Nijhout 1991NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington.). Finally, after pattern elements were color-coded for each species, we checked our identifications of pattern elements for consistency throughout the Brassolini.
Terminology and character optimization
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Wing background: The background corresponds to the canvas upon which patterns elements are expressed, and background color may or may not be homogeneous across the wing surface (Nijhout 1991NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington.);
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Nymphalid ground plan (NGP) pattern elements: The nine pattern elements found in Brassolini are indicated by letters b to j from the wing base to the distal edge, following Nijhout (1991NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington., p.43);
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Pattern element h, ocelus, and eyespot: Pattern element h corresponds to a series of oceli, and given this fact, the letter h is used here in reference to the whole series while the terms ocelus and oceli are used when referring to specific units (within particular cells). The term ‘eyespot’ does not necessarily correspond to NGP pattern element h across butterflies (Nijhout 1991NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington.) and it is not used in the descriptions below. Oceli can be simple (one solid spot) or complex (a spot encircled by rings);
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Ripple patterns: These correspond to striations or granular markings typically found on the ventral wing surface of satyrines. Development of ripple patterns precedes that of NGP pattern elements (Nijhout 2001NIJHOUT, H.F. 2001. Elements of butterfly wing patterns. J. Exp. Zool. (Mol. Dev. Evol.) 291:213-225. http://dx.doi.org/10.1002/jez.1099
http://dx.doi.org/10.1002/jez.1099... ), and our descriptions and discussion take this into account; -
Trailing bands: The space between certain pattern elements may contain a bright band (white, cream, yellow or orange) that contrasts the dorsal or ventral wing background. We coined the term ‘trailing bands’ for these because, on the ventral surface, they are usually contiguous to one pattern element and diffuse at the opposite side (see Figures 5A for identification on the ventral and dorsal surfaces, and 8A for a schematic representation). Nonetheless, they can also fill the entire space between two flanking elements, or be diffuse in both the distal and proximal edges. It is, therefore, possible that they are developmentally associated with various pattern elements. Dorsal and ventral trailing band homologues vary in width and color, and may be expressed in the same, or slightly offset, locations. The trailing bands differ from, and should not be confused with, “patterned background colors” described by Nijhout (1991NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington., p.38);
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Wing venation nomenclature follows the Comstock-Needham system (indicated in Figure 8A).
A, Subordinate groundplan for the Brassolini ventral and dorsal wing surfaces. Continuous lines (or a large circle for element h) indicate pattern elements or trailing bands that are usually present, and small dots or dotted lines denote those that are often absent. The wing outline corresponds to Opoptera syme. B, Annotated Brassolini phylogeny on which selected wing color characters have been optimized.
We used MacClade (Maddison & Maddison 2005MADDISON, D.R. & MADDISON, W.P. 2005. MacClade 4.08. Sinauer, Sunderland.) to optimize variation of selected pattern elements onto a genus-level phylogeny (annotated from Penz 2007PENZ, C.M. 2007. Evaluating the monophyly and phylogenetic relationships of Brassolini genera (Lepidoptera, Nymphalidae). Sys. Entomol. 32:668-689. http://dx.doi.org/10.1111/j.1365-3113.2007.00391.x
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; the slight differences in topology between the tree used here and that in Penz et al. 2013PENZ, C.M., FREITAS, A.V.L., KAMINSKI, L.A., CASAGRANDE, M.M., & DEVRIES, P.J. 2013. Adult and early-stage characters of Brassolini contain conflicting phylogenetic signal (Lepidoptera, Nymphalidae). Sys. Entomol. 38:316-333. http://dx.doi.org/10.1111/syen.12000
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did not affect character optimization).
Results
Pattern elements of the nymphalid ground plan were easily identified in most brassolines, although some species had reduced patterns. Color-coded identification diagrams in Figures 1-7 together with Tables 1 and 2 facilitate comparison across genera. Individual pattern elements are more readily recognized on the ventral surface of the wings. Therefore, we address the ventral coloration first, and use it as a guide for the identification of dorsal pattern elements and trailing bands. Based on our comparative study of 75 species, we then propose a subordinate groundplan for Brassolini and place the variation in key characteristics in a phylogenetic context (Figure 8), noting that some taxa depart from the groundplan. Finally, we describe instances of sexual dimorphism and color pattern convergence among genera (Figure 9).
Sample of brassoline species showing sexual dimorphism and color convergence. Scale bar for all images: 1 cm. A, Bia actorion male, Suriname and female, Ecuador, Sucumbios; B, Opoptera syme male, Brazil, São Paulo and female (no data); C, Dasyophthalma rusina male on the left and female on the right, both from South Brazil; D, Caligopsis seleucida male on the left and female on the right, both from Peru, Madre de Dios; E, Caligo oileus male on the left and female on the right, from Peru, Huanuco and Ayacucho, respectively; F, Caligo illioneus male, Ecuador Sucumbios; G, Eryphanis automedon male on the left and female on the right, from Colombia, Cali and Paraguay, San Juan Caballero, respectively; H, Catoblepia orgetorix championi male, Panama, Chiriqui and C. orgetorix magnalis female Ecuador, Pastaza; I, Caligo atreus male, Colombia, Antiochia; J, Opoptera staudingeri male, Costa Rica, Heredia; K, Mielkela singularis male on the left and female on the right, both from Mexico, Chiapas; L, Opsiphanes cassina male on the left and female on the right, both from Ecuador, Sucumbios.
1.
Ventral wing surface
The diversity of ventral patterns within Brassolini is illustrated in Figures 1-4 and described in Table 1. The number of visible ventral pattern elements varies broadly between and sometimes within genera, and the ventral forewing (VFW) usually contains a larger number of visible elements than the ventral hind wing (VHW). The VFW typically includes elements b to j. Element e and g are usually obscured by ripple patterns, being vestigial or absent in several taxa as a result (see Figures 1-4). Two VFW submarginal bands (i and j) are visible in most species, but one or both can be absent (e.g., Orobrassolis ornamentalis (Stichel, 1906), Figure 4D; Bia actorion (Linnaeus, 1763), Figure 1A). The VHW typically includes elements c, d, f, h, i and j, and although very reduced b and e are also present in some taxa (see Figures 1-4). Element g is absent from the VHW of all species examined. The VHW submarginal bands (i and j) can be absent or present (e.g., absent in Dynastor darius (Fabricius, 1775), Figure 1E; present, sharp in Opoptera syme (Hübner, 1821), Figure 2B; blurred in Caligo eurilochus (Cramer, 1775), Figure 3A).
The position and appearance of pattern elements varies between the VFW and VHW, as it could be expected from their different shape ( Figures 1-4). The elements of the central symmetry system (d, e, f) and border oceli (h) are located more distally on the VFW than on the VHW. Element f is usually more visible and expressed across a larger number of wing cells on the VFW than the VHW. The serial expression of element h on the VFW usually includes simple spots anterior to vein M1 and a complex ocelus in the cell below this vein, but some taxa also have an additional ocelus in the cell below M2 (Dynastor, Figure 1F; Caligopsis and Eryphanis, Figure 2C, E, F). From veins M2 or M3 to the posterior portion of the VFW, h can be absent, fragmented, continuously diffuse, or form a uniquely broad band as in Blepolenis (Figure 4E).
Element h, suitably referred to as border oceli, constitutes a notable and easily recognizable wing color component in satyrine butterflies. Within Brassolini, the different manifestations of h on the VHW can be divided in three categories: (1) Narope and Aponarope have a small spot in most cells (Figure 1B, D); (2) some Catoblepia have a complex ocelus of similar size in most cells (Figure 4B); and (3) the majority of brassolines have two large, usually complex oceli located below Sc+R1 and Cu1 (anterior and posterior oceli), which are sometimes accompanied by one or two (infrequently three) additional markings. While these markings are usually located below M1 or M2 (Figures 1C, 2E, 3A), Caligopsis (Figure 2C) and Eryphanis (Figure 2E, F) are unique in having a well-developed ocelus below M3. Within category (3) above, the anterior ocelus of the VHW may diverge from the usual, round shape (e.g., Selenophanes cassiope (Cramer, 1775), Figure 3D), and the posterior ocelus may be quite large, expanding across veins Cu1 and Cu2 (e.g., Caligo, Figure 3A-C). The location of the posterior ocelus varies in the proximal-distal axis of the Cu1 cell: it is positioned at the base of the tail near the wing margin in Bia (Figure 1A), very near the discal cell in Dasyophthalma (Figure 2A), Caligopsis (Figure 2C), Eryphanis (Figure 2E, F) and Caligo (Figure 3A, B, C), and approximately at mid-length of the Cu1 cell in the remaining genera. When present, the submarginal bands (i and j) are always thin and distinctive on the VFW, but those on the VHW can be either thin (e.g., Opoptera syme, Figure 2B), or broad and diffuse (e.g., Caligo eurilochus, Figure 3A).
The presence, width, color and intensity of trailing bands vary between genera (Figures 1-4). In several species, the contrast between the dark NGP pattern elements and the white trailing bands produces a striking contrast (e.g., Eryphanis bubocula (Butler, 1872), Figure 2F), and in others the ventral expression of such band is faint (e.g., Catoblepia xanthus (Linnaeus, 1758), Figure 3F). A trailing band may also be located in an area of the VFW that is not visible when the butterfly is at rest (e.g., Penetes pamphanis Doubleday, 1849; Figure 3E). Trailing bands constitute a key feature of the dorsal color pattern and will be addressed in more detail below.
Three attributes of the ripple patterns are worth emphasizing. First, they vary from granular (Narope, Figure 1B; Aponarope, Figure 1D; Brassolis, Figure 1C) to striated (e.g., Dynastor macrosiris (Westwood, 1851), Figure 1F), and can be well-defined or blurry (Dynastor napoleon, Figure 1E). Second, they can either be prevalent on both wings (Figure 2A), or be expressed on the VHW but reduced to a localized portion of the VFW, usually between f and h (Figure 4E). Although most genera are uniform in this regard, species of Caligo and Catoblepia vary in the VFW expression of ripple pattern (compare Caligo in Figure 3A, B, C and Catoblepia in Figures 3F, 4A, B). Finally, the ripple pattern can be absent from a specific region of the VHW. Caligopsis seleucida (Hewitson, 1877), all Eryphanis and some Caligo species lack ripple pattern in the area between the anterior and posterior oceli, which is sometimes outlined by pale-colored trailing bands (Figures 2C, E, F and 3C). The lack of ripple pattern in that area makes element d clearly visible, and this dark “ripple-free” area is a prominent visual component of the VHW because it highlights the anterior and posterior oceli. In contrast, Mielkella singularis (Weymer, 1907) and all Opsiphanes have a small and inconspicuous VHW area lacking ripple patterns close to the wing base (Figure 4C, F), which is not present in Blepolenis or Orobrassolis.
2.Dorsal wing surface
The dorsal color patterns are simpler than those on the ventral surface. They typically include a reduced number of pattern elements, trailing bands, and iridescent patches that are not part of the NGP (Table 2). We selected Opoptera syme (Figure 5A) as a starting point for the identification of dorsal pattern elements and trailing bands for three reasons: (1) its dorsal pale brown background allowed us to identify dark brown pattern elements, (2) its ventral color patterns are well defined and easy to recognize, and (3) dorsal pattern elements are almost perfectly aligned with their ventral homologues. The four pattern elements that can be identified on the DFW of O. syme are f, h, i, and j (the latter being barely visible in some specimens, absent in others), and elements i and j are visible on the DHW (Figure 5A, see also Figure 9B). Some of the ventral, pale yellow trailing bands have orange dorsal homologues. By comparing the ventral and dorsal images in Figure 5A, note that the two orange bands on the DFW correspond to VFW trailing bands distal to f and proximal to i (see horizontal lines connecting the images). The trailing band distal to f is shorter and more diffuse on the DFW than on the VFW. A diffuse and broken band is located distal to i on DHW, and its ventral homologue is better defined. Opoptera syme females show a faint iridescent patch on the DHW that is not associated with any of the NGP pattern elements (Figure 9B). The fortuitous dorsal coloration of this species allowed us to build a comparative framework used to interpret the dorsal patterns of other brassolines (Figures 5-7).
Few pattern elements can be identified on the dorsal wing surface (Table 2). Visible pattern elements are broad and diffuse, usually blending with the brown wing background (Figures 5-7). Therefore, in species with predominantly dark brown wings, identification of pattern elements was not possible (e.g., Bia, Figure 5B; Penetes; Figure 7C; Table 2). Orobrassolis constitutes an exception where the pale wing background allowed for the identification of six pattern elements on the DFW (c, d, e, f, h, and i; Figure 7F). Element f and those distal to it are generally expressed on the DFW except for g, and the homogeneously dark distal half of the DFW of some taxa suggests that such pattern elements blend together (e.g., Opsiphanes, Figure 7H, I). Nonetheless, elements c and d are visible on the DFW of some taxa (Brassolis, Figure 5C; Caligopsis, Figure 6A; Orobrassolis, Figure 7F; Blepolenis, Figure 7G). Element h usually appears as a series of two or three anterior, simple spots and one diffuse ocelus below M1. However, additional spots are found in some species (e.g., Selenophanes supremus Stichel, 1901; Figure 7B), or h may be extended across the entire DFW in others (e.g., Caligo eurilochus and C. oileus C. Felder & R. Felder, 1861; Figure 6D, G). Most brassolines seem to lack pattern elements proximal to i on the DHW, but e is present in a few taxa (Narope, Figure 5D; Orobrassolis, Figure 7F). In contrast to other brassolines, element e is present on both the DFW and DHW of most species of Narope (Figure 5D). The dark distal portion of the DHW of some species of Caligo (e.g., C. eurilochus, Figure 6D) expands over an area that includes element h on the ventral surface. Although it is possible that h might be present on the dorsal surface of such species, we conservatively interpreted all brassolines as lacking h on the DHW.
Light-colored trailing bands constitute a highly visible component of the dorsal brassoline coloration because they contrast the brown wing background. As shown in Figures 5-7 (see also Table 2), these bands are found on both wings, varying in position, width, length, amalgamation, color, and intensity. Most brassolines have a band across the DFW, and the two main components of this band can be easily identified in Opoptera syme (Figure 5A); i.e., the trailing bands distal to f and proximal to i. Amalgamation of the same two DFW trailing bands in Opoptera staudingeri (Godman & Salvin, 1894) (Figure 9J) result in a single, continuous, curved band, an arrangement that is also found in Catoblepia (example in Figure 7D). Some taxa have a band distal to element d that blends with that distal to f (e.g., Brassolis, Figure 5C; Caligo martia (Godart, 1824), Figure 6F; Selenophanes cassiope, Figure 7A). A band between DFW elements c and d is present in a few species (e.g., Mielkella singularis, Figure 7E). Regarding the DHW, when a trailing band is present, it usually corresponds to that distal to element i (Figures 5A, C, E; 6B, E; 7A, D to H), and sometimes a faded band distal to j is also visible (Figure 7A, G). Dasyophthalma is unusual in having a trailing band located proximal to element i (Figure 5F).
Dorsal iridescence is present in species of seven genera, in both sexes or one sex only (Table 2). Among the species and specimens examined here, iridescence is found in both sexes of some species of Bia, Dasyophthalma, Eryphanis, Caligo and Catoblepia orgetorix (Hewitson, 1870), being more intense in males. Female-limited faint iridescence is visible on the DHW of Opoptera syme (Figure 9B) and both wings of O. aorsa (Godart, 1824) and O. hilaris Stichel, 1901 (not illustrated), Caligopsis seleucida (Figure 9D; but an iridescent male is illustrated by D'Abrera 1987D'ABRERA, B. 1987. Butterflies of the Neotropical Region. Part III Brassolidae, Acraeidae & Nymphalidae (partim). Hillhouse, p.386-525.), and Catoblepia soranus (Westwood, 1851) (not illustrated).
3.Subordinate groundplan for Brassolini
Figure 8A summarizes the proposed subordinate groundplan for Brassolini. Pattern elements and trailing bands represented by solid lines or large circles are typically present, and those indicated by dotted lines are often absent. Pattern elements are narrower and more clearly defined on the ventral than on the dorsal wing surfaces, where they are broad and diffuse. While the ventral wing coloration is derived mostly from pattern elements and ripple patterns, trailing bands constitute the most visible component of the dorsal surface.
The number of visible pattern elements decreases progressively from the VFW to the VHW, and DFW to the DHW. Pattern elements c, d, f, h, i and j are usually expressed on the VFW, and e and g were visible in fewer of the examined species. Elements c and d vary from straight lines to a complex web of interlocking lines, and they fill a large portion of the wing surface together with f. Round oceli are typically visible above vein M2, and h may be irregularly shaped or absent below that vein. Elements i and j are typically thin and may fade towards the VFW tornus. Pattern element h is the dominant feature of the VHW. It can be expressed as a series of simple or complex round oceli, but most species display two complex oceli (anterior and posterior) that flank several irregular markings. Although f, i and j are often expressed, element f is usually visible on the anterior portion of the wing only, and i and j interact with the ripple pattern and appear more diffuse than their VFW counterparts. The DFW groundplan includes few pattern elements, typically f and those distal to it, except for g. We hypothesize that element g is absent from the DFW based on the dorsal patterns of Opoptera syme (Figure 5A) and other species that have a light background color (e.g., Figures 5D; 6D, G, H; 7F, G, J), and also because g is often missing from the VFW. Finally, most pattern elements are absent from the DHW, and most species display a combination of elements i and j plus a trailing band (e is found in a few taxa).
The ventral color patterns of Narope, Aponarope and Penetes are unusual within Brassolini, and depart from the groundplan. While well developed in other members of the tribe, the border oceli of Narope and Aponarope appear as small spots that blend with their unique, finely granular ripple pattern, and the pattern elements are highly fragmented in these genera (Figure 1B, D). In Penetes, the few pattern elements present are diffuse and barely noticeable, and ripple patterns are also lacking (Figure 3E). Intervenous stripes that are not part of the NGP are visible inside Penetes VFW discal cell (3 stripes) and VHW discal cell (one stripe). Incidentally, the dark intervenous stripes in Penetes are indicative of unpigmented intervenous stripes that distort certain pattern elements in other brassolines. For example, in the VFW discal cell of Selenophanes (Figure 3D) element c appears as a series of four contiguous circles that possibly result from distortions from three intervenous stripes.
The wing background color of most brassolines is brown, but some taxa are notably different. We hypothesize that the vivid dorsal coloration of some species of Narope (Figure 5D), the two Orobrassolis (Figure 7F), Opsiphanes blythekitzmillerae Austin & A. Warren, 2007 (not illustrated) and O. boisduvallii Doubleday, 1849 (Figure 7J) results from a change in background color, with an extreme reduction in the expression of dorsal pattern elements in the two Opsiphanes. The dorsal colors of some species of Caligo (e.g., Figure 6H) and all Blepolenis (Figure 7G) can also be interpreted as a change in background coloration, and the bold dorsal pattern elements f to j (minus g) are particularly well developed and bold in Blepolenis. This fortuitous variation in background color further supports our hypothesis that many pattern elements are absent from the dorsal wing surface of brassolines, especially the DHW.
4.Dorsal sexual dimorphism and color pattern convergence
In most brassoline species, males and females are only mildly dimorphic in their dorsal colors, and have similar wing shape (Table 2). Mild color dimorphism results from females having more clearly defined dorsal pattern elements and / or trailing bands than males. For example, in some Caligo (e.g., C. oileus; Figures 6G, 9E) both the dorsal pattern elements and trailing bands are more visible in females. The slight iridescence of some female Opoptera (Figure 9B) and Catoblepia (not illustrated), or slightly wider and paler trailing bands of Opsiphanes (Figure 9L) can also be considered mild color dimorphism.
There are instances in which dorsal colors and wing shape are clearly different between the sexes (Table 2). The genus Bia is an interesting case in which obvious sexual differences can occur on both the dorsal and ventral wing surfaces. The DFW orange trailing band and iridescent patch are positioned more distally in the males, and females have a less intense, but larger iridescent patch extending through the discal cell in the medial area of the wing (Figure 9A; male iridescence may be absent in some forms). In some locations, the female VFW has reduced ripple patterns distal to element f such that the distal portion of the hind wing has a predominantly yellow appearance (not illustrated). Within Narope, N. guilhermei Casagrande, 1989 (not illustrated) is the most notable for color differences between the sexes, but males and females differ in wing shape in all species. Sexual dimorphism in Dasyophthalma results from differences in the DFW trailing band distal to f that is present in females only, and also the larger, more intense iridescent patches in males of two species (Figures 5F, 9C). In some Eryphanis, males are much more intensely iridescent than females (Figure 9G). Differences in wing shape plus the colors and width of trailing bands produces strong sexual dimorphism in Mielkella singularis (Figure 9K).
In a few cases, strong sexual dimorphism is intertwined with dorsal color convergence across genera. Female Catoblepia orgetorix orgetorix, C. orgetorix magnalis Stichel, 1902 and C. orgetorix championiBristow, 1981BRISTOW, C.R. 1981. A revision of the brassoline genus Catoblepia (Lepidoptera: Rhopalocera). Zool. J. Linnean Soc. 72:117-163. http://dx.doi.org/10.1111/j.1096-3642.1981.tb01655.x
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(Figure 9H), and both sexes of C. orgetorix rothschildi Casagrande & Lamas, 2004, resemble Caligo atreus (Kollar, 1850) and depart strongly from the typical Catoblepia phenotype (Figure 9I). This resemblance to C. atreus can be achieved with few phenotypic modifications: (1) all dorsal female trailing bands become lighter in color, (2) the DFW trailing bands are amalgamated and positioned closer to the medial area of the wing, (3) a patch of iridescent scales is superimposed onto the DFW trailing band, and (4) the DHW trailing band becomes wider, reaching the wing edge. The monomorphic Opoptera staudingeri differs from close relatives in the aorsa-group by lacking hind wing tails and in the continuous, relatively wide DFW and DHW trailing bands. Such modifications yield a resemblance to species of Catoblepia (compare Figure 9J and H). Finally, due to their dorsal iridescence, Caligopsis seleucida females (Figure 9D) more closely resemble some Caligo (Figure 9F) than the conspecific male.
Discussion
This study represents the first comprehensive examination of color pattern diversity in the tribe Brassolini. Here we describe the expression of pattern elements across all genera, and propose a subordinate groundplan for the tribe (Figure 8A). Much variation was found on the ventral forewing surface, with the number of visible pattern elements ranging from one to nine. Except for Penetes, ripple patterns were prevalent on the ventral hind wing and expressed to a lesser extent on the ventral forewing, varying from sharply striated, to blurry, or granular. On the dorsal wing surface pattern elements are broader and more diffuse than on the ventral surface (bold, sensuNijhout & Wray 1986NIJHOUT, H.F. & WRAY, G.A. 1986. Homologies in the colour patterns of the genus Charaxes (Lepidoptera, Nymphalidae). Biol. J. Linn. Soc. 28:387-410. http://dx.doi.org/10.1111/j.1095-8312.1986.tb01766.x
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), and are often amalgamated. Furthermore, fewer pattern elements are identifiable on the dorsal than on the ventral surface (Figure 8A). The dorsal forewing typically includes f, h, i and j, but e and d are sometimes visible. The dorsal hind wing lacks most pattern elements, usually displaying only i and j. We hypothesize that the dorsal white, yellow or orange trailing bands might be associated with particular pattern elements, and they constitute an important feature of the brassoline groundplan. Finally, iridescent bands do not correspond to NGP elements, but may be superimposed onto them. The presence and intensity of iridescence is quite variable, appearing in different areas of the wing, and evolving independently in four separate Brassolini lineages (sensuPenz 2007PENZ, C.M. 2007. Evaluating the monophyly and phylogenetic relationships of Brassolini genera (Lepidoptera, Nymphalidae). Sys. Entomol. 32:668-689. http://dx.doi.org/10.1111/j.1365-3113.2007.00391.x
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) when optimized onto the tree using parsimony (Bia-clade, Opoptera-clade, Caligo-clade and Opsiphanes-clade; Figure 8B).
The dorsal and ventral wing surfaces of brassolines differ in the number of identifiable pattern elements, and occasionally in their background color. Similar to what Nijhout & Wray (1986)NIJHOUT, H.F. & WRAY, G.A. 1986. Homologies in the colour patterns of the genus Charaxes (Lepidoptera, Nymphalidae). Biol. J. Linn. Soc. 28:387-410. http://dx.doi.org/10.1111/j.1095-8312.1986.tb01766.x
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described for Charaxes (Charaxinae, sister to Satyrinae which includes Brassolini; Wahlberg et al. 2009WAHLBERG, N., LENEVEU, J., KODANDARAMAIAH, U., PEÑA, C., NYLIN, S., FREITAS, A.V.L. & BROWER, A.V.Z. 2009. Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proc. R. Soc. B. 276:4295-4302. http://dx.doi.org/10.1098/rspb.2009.1303
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), brassoline ventral pattern elements are narrower, better defined and easier to identify than the dorsal ones, which are broad and sometimes diffuse. While dorsal and ventral surfaces contain the same set of pattern elements in Charaxes (Nijhout & Wray 1986NIJHOUT, H.F. & WRAY, G.A. 1986. Homologies in the colour patterns of the genus Charaxes (Lepidoptera, Nymphalidae). Biol. J. Linn. Soc. 28:387-410. http://dx.doi.org/10.1111/j.1095-8312.1986.tb01766.x
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, p.400), we hypothesize that in most brassolines fewer elements are present dorsally, particularly on the hind wing (Figure 8A). This hypothesis is based on an inter-related series of comparative observations. First, the yellow or orange dorsal wing background color of some species markedly differs from the typical brown. This greatly facilitated the identification of pattern elements that were present, and also revealed that some were absent (e.g., Narope cyllastros Doubleday, 1849, Figure 5D; Opsiphanes boisduvallii, Figure 7J). Second, only distal pattern elements could be identified in several species that have pale brown dorsal background (e.g., Opoptera syme, Figure 5A; Caligopsis seleucida, Figure 6A; Caligo oileus, Figure 6G). Third, in some species the distal half of the wings is darker than the proximal half, suggesting that distal pattern elements are bold/amalgamated as in Charaxes (Nijhout & Wray 1986NIJHOUT, H.F. & WRAY, G.A. 1986. Homologies in the colour patterns of the genus Charaxes (Lepidoptera, Nymphalidae). Biol. J. Linn. Soc. 28:387-410. http://dx.doi.org/10.1111/j.1095-8312.1986.tb01766.x
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), while proximal ones are not expressed (e.g., Brassolis, Figure 5C; Opsiphanes sallei Doubleday, 1849; Figure 7H). As an alternative hypothesis, it may be that the dorsal background color changes as a gradient across the wing as in C. eurilochus (Figure 6D). However, the dorsal pattern of C. eurilochus seems to constitute a dull version of C. arisbe Hübner, 1822 (Figure 6H), where the yellow background highlights the same dorsal elements also present in C. eurilochus, especially the female.
Many nymphalid species have different dorsal and ventral background colors, and this is also the case in some brassolines. Opsiphanes blythekitzmillerae and O. boisduvallii constitute an interesting example because their orange-yellow dorsal background color is strikingly different from other species in the genus. Furthermore, while the ventral background color of O. blythekitzmillerae conforms to that of other Opsiphanes, O. boisduvallii has an orange-yellow ventral background similar to its dorsal color. Rountree & Nijhout (1995)ROUNTREE, D.B. & NIJHOUT, H.F. 1995. Genetic control of a seasonal morph in Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 41:1141-1145. http://dx.doi.org/10.1016/0022-1910(95)00051-U
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described the genetic control of ventral hind wing background color in Junonia coenia Hübner, 1822 (=Precis coenia; Nymphalinae). This species exhibits seasonal polyphenism (light vs. dark ventral hind wing color), but a recessive allele at a single locus restricts the phenotype to a dark ventral hind wing background color. This suggests the change in ventral background color in O. boisduvallii may have a simple genetic control.
Within Brassolini, the expression of border oceli (h) varies between the forewing and hind wing, and between the antero-posterior axis and dorso-ventral surfaces of each wing. The ventral forewing element h typically appears as a series of distinctive light colored spots and / or complex oceli anterior to vein M2, and is either absent or composed of brown spots, blotches, diamonds or lines posterior to that vein. As an exception, a complex ocelus posterior to M2 is only found on the ventral surface of Dynastor and Caligopsis + Eryphanis, representing a developmental parallel given that these genera belong to two separate clades (Penz 2007PENZ, C.M. 2007. Evaluating the monophyly and phylogenetic relationships of Brassolini genera (Lepidoptera, Nymphalidae). Sys. Entomol. 32:668-689. http://dx.doi.org/10.1111/j.1365-3113.2007.00391.x
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; Figure 8B). The antero-posterior modifications of h support the proposal that reduced covariance and genetic correlations between wing cells allow differential expression of serial homologues (Paulsen 1994PAULSEN, S.M. 1994. Quantitative genetics of butterfly wing patterns. Dev. Genet. 15:79-91. http://dx.doi.org/10.1002/dvg.1020150109
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; Nijhout 1994NIJHOUT, H.F. 1994. Symmetry systems and compartments in lepidopteran wings: the evolution of a patterning mechanism. Development (Suppl.) 225-233., 2001NIJHOUT, H.F. 2001. Elements of butterfly wing patterns. J. Exp. Zool. (Mol. Dev. Evol.) 291:213-225. http://dx.doi.org/10.1002/jez.1099
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; but see also Monteiro et al. 1997MONTEIRO, A., BRAKEFIELD, P.M. & FRENCH, V. 1997. Butterfly eyespots: the genetics and development of the color rings. Evolution 51:1207-1216. http://dx.doi.org/10.2307/2411050
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, Monteiro 2008MONTEIRO, A. 2008. Alternative models for the evolution of eyespots and of serial homology on lepidopteran wings. BioEssays 30:358-366. http://dx.doi.org/10.1002/bies.20733
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). Although diffuse and subdued, the ventral forewing expression of element h is mirrored on the dorsal forewing. In contrast, the prominent ventral hind wing oceli lack dorsal homologues, thus demonstrating dorso-ventral independence of pattern formation.
We observed considerable variation in the number and size of the ventral hind wing oceli and their putative interaction with adjacent pattern elements or other color components. In the majority of brassolines, the ventral hind wing oceli located below veins Sc+R1 and Cu1 (anterior and posterior oceli) are the largest and most complex, while those in other cells are smaller, simpler, vestigial, or absent. The absence of oceli below veins M3 and Cu2 seems to have preceded and facilitated the increase in size of the posterior ocelus in several taxa, Caligo being the most obvious example (Figure 3A, B, C). Furthermore, differences in the organization of the posterior ocelus suggest independent evolution of increased size. For instance, in some species the dark ocelar center crosses veins M3 and Cu2 (e.g., Caligo atreus, Figure 3B), while in others the outermost ring only expands cell boundaries (e.g., Catoblepia orgetorix, Figure 4A). The unique fusion of posterior oceli in the sister genera Caligopsis and Eryphanis is also noteworthy because it shows that serial homologues can interact to form novel designs (see Nijhout 2001NIJHOUT, H.F. 2001. Elements of butterfly wing patterns. J. Exp. Zool. (Mol. Dev. Evol.) 291:213-225. http://dx.doi.org/10.1002/jez.1099
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for several examples of such interaction). Finally, the posterior ocelus is contained inside cell cu1 in Bia, Narope, Brassolis and Dynastor, early lineages in the Brassolini phylogeny (Penz 2007PENZ, C.M. 2007. Evaluating the monophyly and phylogenetic relationships of Brassolini genera (Lepidoptera, Nymphalidae). Sys. Entomol. 32:668-689. http://dx.doi.org/10.1111/j.1365-3113.2007.00391.x
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; Figure 8B). Although a larger posterior ocelus seems to have evolved at the ancestor of the Opoptera + Caligo + Opsiphanes-clades (Figure 8B), this character is not homogeneous between or within the 12 genera in these lineages (compare Figure 2E and F plus Figure 4A and B) and variation is size is continuous.
The ventral hind wing of several species in the Caligo-clade combines a ripple-free, dark medial area with a large posterior ocelus; intriguing from both developmental and ecological perspectives. If the ripple pattern is determined before the NGP pattern elements (Nijhout 1991NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington., 2001NIJHOUT, H.F. 2001. Elements of butterfly wing patterns. J. Exp. Zool. (Mol. Dev. Evol.) 291:213-225. http://dx.doi.org/10.1002/jez.1099
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), a ripple-free “window” can only be produced if ripple pattern expression is blocked at that specific site early in pattern development (see Figures 2C, E, F; 3C). The large ventral hind wing oceli of Caligo are quite obvious when these butterflies feed on the ground or rest on vertical tree trunks (pers. obs.), and the ripple-free medial area enhances visibility of the oceli. There are two main hypotheses for the evolution of conspicuous oceli in Lepidoptera (reviewed in Stevens 2005STEVENS, M. 2005. The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera. Biol. Rev. 80:573-588. http://dx.doi.org/10.1017/S1464793105006810
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): they can be used as a deflection point (target) that directs predator attacks to non-essential body parts, or function as a startling display. In support of the deflection hypothesis, it has been demonstrated that the posterior hind wing tornus is more noticeable yet structurally weaker than the surrounding areas in a sample of African species (DeVries 2002DEVRIES, P.J. 2002. Differential wing-toughness among palatable and unpalatable butterflies: direct evidence supports unpalatable theory. Biotropica 34:176-181., 2003DEVRIES, P.J. 2003. Tough models versus weak mimics: new horizons in evolving bad taste. J. Lep. Soc. 57:235-238.) and South American Pierella astyoche (Erichson, 1849) (Nymphalidae, Satyrinae; Hill & Vaca 2004HILL, R.I. & VACA, J.F. 2004. Differential wing strength in Pierella butterflies (Nymphalidae, Satyrinae) supports the deflection hypothesis. Biotropica 36:362-370.). Although untested, Stradling (1976)STRADLING, D.J. 1976. The nature of the mimetic patterns of the brassolid genera, Caligo and Eryphanis. Ecol. Entomol. 1:135-138. http://dx.doi.org/10.1111/j.1365-2311.1976.tb01214.x
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hyothesized that in some Eryphanis and Caligo the posterior ocelus plus a dark band across the wing look like a reptile in profile to function as a startle display.
Field experiments and observations demonstrated that ventral oceli play a role in mate selection. Choice trials showed that male Lycaeides idas (Linnaeus, 1761) (Lycaenidae) selected females based on the size of their ventral hind wing aurorae and spots (Fordyce et al. 2002FORDYCE, J.A., NICE, C.C., FORISTER, M.L. & SHAPIRO, A.M. 2002. The significance of wing pattern diversity in the Lycaenidae: mate discrimination by two recently diverged species. J. Evol. Biol. 15:871-879. http://dx.doi.org/10.1046/j.1420-9101.2002.00432.x
http://dx.doi.org/10.1046/j.1420-9101.20...
), and male and female Bicyclus anynana show a seasonal preference for ocelus size (Prudic et al. 2011PRUDIC, K.L., JEON, C., CAO, H. & MONTEIRO, A. 2011. Developmental plasticity in sexual roles of butterfly species drives mutual sexual ornamentation. Science, 331:73-75. http://dx.doi.org/10.1126/science.1197114
http://dx.doi.org/10.1126/science.119711...
). During courtship, male Pierella astyoche hover by decoupling forewing from hind wing movement, and clearly display the large hind wing white spots to the potential mate (CMP pers. obs.), an additional function to anti-predator defense (see above). Male Caligo form mating leks at forest edges (Freitas et al. 1997FREITAS, A.V.L., BENSON, W.W., MARINI-FILHO, O.J. & CARVALHO, R.M. 1997. Territoriality by the dawn's early light: the Neotropical butterfly Caligo idomeneus (Nymphalidae: Brassolinae). J. Res. Lepid. 34:14-20., Srygley & Penz 1999SRYGLEY, R.B. & PENZ, C.M. 1999. The lek mating system in Neotropical owl butterflies: Caligo illioneus and C. oileus (Lepidoptera, Brassolinae). J. Insect Behav. 12:81-103. http://dx.doi.org/10.1023/A:1020981215501
http://dx.doi.org/10.1023/A:102098121550...
). Upon arrival at the lek site, female C. illioneus (Cramer, 1775) appear to detect perched males visually (CMP pers. obs.). When approached, males take off and initiate aerial courtship behavior. It therefore seems possible that the ventral hind wing oceli of Caligo play a role in mate location, and also function as a startle display in both sexes. Given the diversity in size, color and number of oceli in brassolines, we might expect that oceli may serve multiple purposes.
Brassolines defy classical definitions of Batesian and Müllerian mimicry. There are examples of color resemblance among genera, but there is no evidence of chemical protection (see Chai 1990CHAI, P. 1990. Relationships between visual characteristics of rainforest butterflies and responses of a specialized insectivorous bird. In Proceedings of a Symposium sponsored by the American Society of Zoologists. College Station, Texas, p.31-60.). The most notable case involves the convergence of Catoblepia orgetorix onto Caligo atreus with which it overlaps geographically (Figure 9H, I). Four lines of evidence support this assertion: (1) the dorsal phenotype of orgetorix departs from the typical Catoblepia; (2) ventral hind wing oceli are the largest in the genus, and resemble Caligo; (3) convergence is limited to females in the subspecies orgetorix, championi and magnalis, fitting the expectations of sex-limited mimicry (Turner 1984TURNER, J.R.G. 1984. Mimicry: the palatability spectrum and its consequences. In The biology of butterflies (R.I. Vane-Wright and P.R. Ackery, ed.). Princeton University Press, Princeton, p.141-161., Silberglied 1984SILBERGLIED, R. 1984. Visual communication and sexual selection in butterflies. In The biology of butterflies (R.I. Vane-Wright and P.R. Ackery, ed.). Princeton University Press, Princeton, p.207-223.) and appearing to be the ancestral condition; and (4) both sexes of C. orgetorix rothschildi (endemic to the Magdalena Valley, Colombia) have the mimetic phenotype, suggesting that evolution of male color convergence followed that of the female. If Caligo and Catoblepia lack chemical defenses, then the resemblance could potentially be explained by an “arithmetic” effect (safety in numbers; Vane-Wright 1976VANE-WRIGHT, R.I. 1976. A unified classification of mimetic resemblances. Biol. J. Linn. Soc. 8:25-56. http://dx.doi.org/10.1111/j.1095-8312.1976.tb00240.x
http://dx.doi.org/10.1111/j.1095-8312.19...
, after Van Someren & Jackson 1959VAN SOMEREN, V.G.L. & JACKSON, T.H.E. 1959. Some comments on protective resemblance amongst African lepidoptera (Rhopalocera). J. Lep. Soc. 13:121-147.). Whether the similarity among these species confers a fitness-related advantage is unknown, and fieldwork is needed to assess if predators recognize and avoid them. The resemblance between Opoptera staudingeri and Catoblepia orgetorix (Figure 9J and H), and some geographical races of Brassolis sophorae (Linnaeus, 1758) and Selenophanes cassiope (Figures 5C and 6G) also catch the eye, but remain inexplicable. These examples demonstrate that remarkable similarity can be accomplished with relatively few modifications of the trailing bands (color, width, position) and the addition of iridescence (see Results).
Some instances of color resemblance in brassolines might be due to phylogenetic relatedness or male color divergence. Bristow (1981BRISTOW, C.R. 1981. A revision of the brassoline genus Catoblepia (Lepidoptera: Rhopalocera). Zool. J. Linnean Soc. 72:117-163. http://dx.doi.org/10.1111/j.1096-3642.1981.tb01655.x
http://dx.doi.org/10.1111/j.1096-3642.19...
, 1991)BRISTOW, R. 1991. A revision of the brassoline genus Opsiphanes (Lepidoptera: Rhopalocera). Zool. J. Linnean Soc. 101:203-293. http://dx.doi.org/10.1111/j.1096-3642.1991.tb00282.x
http://dx.doi.org/10.1111/j.1096-3642.19...
noted that geographical races of Catoblepia and Opsiphanes converge locally in color pattern. Although we have not examined sufficient specimens to verify this suggestion, these genera belong to the same clade (Penz 2007PENZ, C.M. 2007. Evaluating the monophyly and phylogenetic relationships of Brassolini genera (Lepidoptera, Nymphalidae). Sys. Entomol. 32:668-689. http://dx.doi.org/10.1111/j.1365-3113.2007.00391.x
http://dx.doi.org/10.1111/j.1365-3113.20...
) and their archetypal dorsal colors closely fit the groundplan in Figure 8. Similarity due to common ancestry is therefore a valid alternative explanation for their color resemblance. Members of the Caligo-clade (sensu Penz 2007PENZ, C.M. 2007. Evaluating the monophyly and phylogenetic relationships of Brassolini genera (Lepidoptera, Nymphalidae). Sys. Entomol. 32:668-689. http://dx.doi.org/10.1111/j.1365-3113.2007.00391.x
http://dx.doi.org/10.1111/j.1365-3113.20...
) also share dorsal color patterns through common ancestry. The similarity among females of Caligopsis seleucida (Figure 9D), Eryphanis automedon (Cramer, 1775) (Figure 9G, plus others not illustrated), and some species of Caligo (e.g., C. illioneus, Figure 9F) might be due to the maintenance of ancestral patterns, while the male sex diverged though sexual selection. This suggestion is, nonetheless, tentative and requires further examination.
Much research has been done on the development, genetics, and evolution of nymphalid wing pattern elements, particularly the border oceli. Nonetheless, the most in-depth studies have focused on Bicyclus anynana, Junonia coenia, and some Heliconius (for reviews, see Monteiro et al. 1997MONTEIRO, A., BRAKEFIELD, P.M. & FRENCH, V. 1997. Butterfly eyespots: the genetics and development of the color rings. Evolution 51:1207-1216. http://dx.doi.org/10.2307/2411050
http://dx.doi.org/10.2307/2411050...
, Beldade & Brakefield 2002BELDADE, P. & BRAKEFIELD, P.M. 2002. The genetics and evo-devo of butterfly wing patterns. Nature Rev. Genet. 3(2002):442-452., Monteiro 2008MONTEIRO, A. 2008. Alternative models for the evolution of eyespots and of serial homology on lepidopteran wings. BioEssays 30:358-366. http://dx.doi.org/10.1002/bies.20733
http://dx.doi.org/10.1002/bies.20733...
, Beldade et al. 2008BELDADE, P., McMILLAN, W.O. & PAPANICOLAOU, A. 2008. Butterfly genomics eclosing. Heredity 100:150-157. http://dx.doi.org/10.1038/sj.hdy.6800934
http://dx.doi.org/10.1038/sj.hdy.6800934...
), and the general relevance of such work relies on the evolutionary homology of wing pattern elements across taxa. Although the long early stage development time of brassolines is a limitation for laboratory research (e.g., 70 days for Caligo illioneus; Penz et al. 1999PENZ, C.M., AIELLO, A. & SRYGLEY, R.B. 1999. Early stages of Caligo illioneus and C. idomeneus (Nymphalidae, Brassolinae) from Panama, with remarks on larval food plants for the subfamily. J. Lep. Soc. 53:142-152.), some of these butterflies are locally abundant (DeVries et al. 2011DEVRIES, P.J., ALEXANDER, L.G., CHACON, I.A. & FORDYCE, J.A. 2011. Similarity and difference among rainforest fruit-feeding butterfly communities in Central and South America. J. Anim. Ecol. 81:472-482. http://dx.doi.org/10.1111/j.1365-2656.2011.01922.x
http://dx.doi.org/10.1111/j.1365-2656.20...
) and easily maintained in enclosures (CMP pers. obs.). The objective of this investigation was to provide a comparative framework of wing color pattern variation that can be useful for research on genetics and development of brassolines, but mostly as an impetus for fieldwork that focuses on the function of wing color patterns in the context of intra and interspecific ecological interactions. The diversity of brassoline color patterns, time of activity and mating behaviors, plus recent phylogenetic analyses, constitute the perfect ingredients for research on a key question that relates to all Lepidoptera: what are forces that drive the evolution of color pattern diversity?
This research would not have been possible without the specimen loans provided by several museum curators, to whom we extend our thanks: D. Grimaldi (AMNH), B. Huertas (BMNH), J. Rawlins (CMNH), I. Chacón (InBio), B. Brown (LACM), F. Meyer (MAPA), S. Borkin (MPM), B. van Bekkum-Ansari (NMNL), M. Duarte (MZSP), G. Austin (in memoriam) and A. Warren (UFL), M. Hernandez (UFSC), R. Robbins (USNM) and P. DeVries (private collection). We thank F. Nijhout (Duke University) for inspiration and many useful suggestions, and P. DeVries (University of New Orleans) and an anonymous reviewer for comments on the manuscript. The University of New Orleans Work Study Program provided funding for N. Mohammadi. This work is dedicated to the memory of our fathers Rubem Paulo Penz (1935-2006) and Aliakbar Mohammadi (1951-2006).
References
- BELDADE, P. & BRAKEFIELD, P.M. 2002. The genetics and evo-devo of butterfly wing patterns. Nature Rev. Genet. 3(2002):442-452.
- BELDADE, P., McMILLAN, W.O. & PAPANICOLAOU, A. 2008. Butterfly genomics eclosing. Heredity 100:150-157. http://dx.doi.org/10.1038/sj.hdy.6800934
» http://dx.doi.org/10.1038/sj.hdy.6800934 - BIRCH, M. 1970. Pre-courtship use of abdominal brushes by the nocturnal moth, Phlogophora meticulosa (L.) (Lepidoptera: Noctuidae). Anim. Behav. 18:310-316. http://dx.doi.org/10.1016/S0003-3472(70)80043-4
» http://dx.doi.org/10.1016/S0003-3472(70)80043-4 - BRISTOW, C.R. 1981. A revision of the brassoline genus Catoblepia (Lepidoptera: Rhopalocera). Zool. J. Linnean Soc. 72:117-163. http://dx.doi.org/10.1111/j.1096-3642.1981.tb01655.x
» http://dx.doi.org/10.1111/j.1096-3642.1981.tb01655.x - BRISTOW, R. 1991. A revision of the brassoline genus Opsiphanes (Lepidoptera: Rhopalocera). Zool. J. Linnean Soc. 101:203-293. http://dx.doi.org/10.1111/j.1096-3642.1991.tb00282.x
» http://dx.doi.org/10.1111/j.1096-3642.1991.tb00282.x - CASAGRANDE, M.M. 2002. Naropini Stichel, taxonomia e imaturos (Lepidoptera, Nymphalidae, Brassolinae). Rev. Bras. Zool. 19:467-569. http://dx.doi.org/10.1590/S0101-81752002000200012
» http://dx.doi.org/10.1590/S0101-81752002000200012 - CHAI, P. 1990. Relationships between visual characteristics of rainforest butterflies and responses of a specialized insectivorous bird. In Proceedings of a Symposium sponsored by the American Society of Zoologists. College Station, Texas, p.31-60.
- D'ABRERA, B. 1987. Butterflies of the Neotropical Region. Part III Brassolidae, Acraeidae & Nymphalidae (partim). Hillhouse, p.386-525.
- DEPINNA, M.C.C. 1991. Concepts and tests of homology in the cladistic paradigm. Cladistics 7:367-394. http://dx.doi.org/10.1111/j.1096-0031.1991.tb00045.x
» http://dx.doi.org/10.1111/j.1096-0031.1991.tb00045.x - DEVRIES, P.J. 2002. Differential wing-toughness among palatable and unpalatable butterflies: direct evidence supports unpalatable theory. Biotropica 34:176-181.
- DEVRIES, P.J. 2003. Tough models versus weak mimics: new horizons in evolving bad taste. J. Lep. Soc. 57:235-238.
- DEVRIES, P.J., ALEXANDER, L.G., CHACON, I.A. & FORDYCE, J.A. 2011. Similarity and difference among rainforest fruit-feeding butterfly communities in Central and South America. J. Anim. Ecol. 81:472-482. http://dx.doi.org/10.1111/j.1365-2656.2011.01922.x
» http://dx.doi.org/10.1111/j.1365-2656.2011.01922.x - DEVRIES, P.J., PENZ, C. & HILL, R. 2010. Vertical distribution, flight behavior, and evolution of wing morphology in Morpho butterflies. J. Anim. Ecol. 79:1077-1085. http://dx.doi.org/10.1111/j.1365-2656.2010.01710.x
» http://dx.doi.org/10.1111/j.1365-2656.2010.01710.x - EISNER, T. & MEINWALD, J. 1995. The chemistry of sexual selection. Proc. Natl. Acad. Sci. USA, 92:50-55. http://dx.doi.org/10.1073/pnas.92.1.50
» http://dx.doi.org/10.1073/pnas.92.1.50 - FORDYCE, J.A., NICE, C.C., FORISTER, M.L. & SHAPIRO, A.M. 2002. The significance of wing pattern diversity in the Lycaenidae: mate discrimination by two recently diverged species. J. Evol. Biol. 15:871-879. http://dx.doi.org/10.1046/j.1420-9101.2002.00432.x
» http://dx.doi.org/10.1046/j.1420-9101.2002.00432.x - FREITAS, A.V.L., BENSON, W.W., MARINI-FILHO, O.J. & CARVALHO, R.M. 1997. Territoriality by the dawn's early light: the Neotropical butterfly Caligo idomeneus (Nymphalidae: Brassolinae). J. Res. Lepid. 34:14-20.
- FRUHSTORFER, H. 1912. Family: Brassolidae. In Die Gross-Schmetterlinge der Erde (A. Seitz, ed.). Stuttgart, v.5, p.285-332.
- HILL, R.I. & VACA, J.F. 2004. Differential wing strength in Pierella butterflies (Nymphalidae, Satyrinae) supports the deflection hypothesis. Biotropica 36:362-370.
- JIGGINS, C.D., NAISBIT, R.E., COE, R.L. & MALLET, J. 2001. Reproductive isolation caused by colour pattern mimicry. Nature 411:302-305. http://dx.doi.org/10.1038/35077075
» http://dx.doi.org/10.1038/35077075 - KUNTE, K. 2008. Mimetic butterflies support Wallace's model of sexual dimorphism. Proc. R. Soc. B 275:1617-1624. http://dx.doi.org/10.1098/rspb.2008.0171
» http://dx.doi.org/10.1098/rspb.2008.0171 - KUNTE, K. 2009. The diversity and evolution of batesian mimicry in Papilio swallowtail butterflies. Evolution 63:2707-2716. http://dx.doi.org/10.1111/j.1558-5646.2009.00752.x
» http://dx.doi.org/10.1111/j.1558-5646.2009.00752.x - MADDISON, D.R. & MADDISON, W.P. 2005. MacClade 4.08. Sinauer, Sunderland.
- MONTEIRO, A. 2008. Alternative models for the evolution of eyespots and of serial homology on lepidopteran wings. BioEssays 30:358-366. http://dx.doi.org/10.1002/bies.20733
» http://dx.doi.org/10.1002/bies.20733 - MONTEIRO, A., BRAKEFIELD, P.M. & FRENCH, V. 1997. Butterfly eyespots: the genetics and development of the color rings. Evolution 51:1207-1216. http://dx.doi.org/10.2307/2411050
» http://dx.doi.org/10.2307/2411050 - NIJHOUT, H.F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institute Press, Washington.
- NIJHOUT, H.F. 1994. Symmetry systems and compartments in lepidopteran wings: the evolution of a patterning mechanism. Development (Suppl.) 225-233.
- NIJHOUT, H.F. 2001. Elements of butterfly wing patterns. J. Exp. Zool. (Mol. Dev. Evol.) 291:213-225. http://dx.doi.org/10.1002/jez.1099
» http://dx.doi.org/10.1002/jez.1099 - NIJHOUT, H.F. & WRAY, G.A. 1986. Homologies in the colour patterns of the genus Charaxes (Lepidoptera, Nymphalidae). Biol. J. Linn. Soc. 28:387-410. http://dx.doi.org/10.1111/j.1095-8312.1986.tb01766.x
» http://dx.doi.org/10.1111/j.1095-8312.1986.tb01766.x - OLIVER, J.C., ROBERTSON, K.A. & MONTEIRO, A. 2009. Accomodating natural and sexual selection in butterfly wing pattern evolution. Proc. R. Soc. B. 276:2369-2375. http://dx.doi.org/10.1098/rspb.2009.0182
» http://dx.doi.org/10.1098/rspb.2009.0182 - PAULSEN, S.M. 1994. Quantitative genetics of butterfly wing patterns. Dev. Genet. 15:79-91. http://dx.doi.org/10.1002/dvg.1020150109
» http://dx.doi.org/10.1002/dvg.1020150109 - PENZ, C.M. 2007. Evaluating the monophyly and phylogenetic relationships of Brassolini genera (Lepidoptera, Nymphalidae). Sys. Entomol. 32:668-689. http://dx.doi.org/10.1111/j.1365-3113.2007.00391.x
» http://dx.doi.org/10.1111/j.1365-3113.2007.00391.x - PENZ, C.M. & DEVRIES, P.J. 2002. Phylogenetic analysis of Morpho butterflies (Nymphalidae, Morphinae): implications for classification and natural history. Am. Mus. Novitates, 3374:1-33. http://dx.doi.org/10.1206/0003-0082(2002)374%3C0001:PAOMBN%3E2.0.CO;2
» http://dx.doi.org/10.1206/0003-0082(2002)374%3C0001:PAOMBN%3E2.0.CO;2 - PENZ, C.M., AIELLO, A. & SRYGLEY, R.B. 1999. Early stages of Caligo illioneus and C. idomeneus (Nymphalidae, Brassolinae) from Panama, with remarks on larval food plants for the subfamily. J. Lep. Soc. 53:142-152.
- PENZ, C.M., FREITAS, A.V.L., KAMINSKI, L.A., CASAGRANDE, M.M., & DEVRIES, P.J. 2013. Adult and early-stage characters of Brassolini contain conflicting phylogenetic signal (Lepidoptera, Nymphalidae). Sys. Entomol. 38:316-333. http://dx.doi.org/10.1111/syen.12000
» http://dx.doi.org/10.1111/syen.12000 - PRUDIC, K.L., JEON, C., CAO, H. & MONTEIRO, A. 2011. Developmental plasticity in sexual roles of butterfly species drives mutual sexual ornamentation. Science, 331:73-75. http://dx.doi.org/10.1126/science.1197114
» http://dx.doi.org/10.1126/science.1197114 - RIEPPEL, O. & KEARNY, M. 2002. Similarity. Biol J. Linn. Soc. 75:59-82. http://dx.doi.org/10.1046/j.1095-8312.2002.00006.x
» http://dx.doi.org/10.1046/j.1095-8312.2002.00006.x - ROUNTREE, D.B. & NIJHOUT, H.F. 1995. Genetic control of a seasonal morph in Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 41:1141-1145. http://dx.doi.org/10.1016/0022-1910(95)00051-U
» http://dx.doi.org/10.1016/0022-1910(95)00051-U - SILBERGLIED, R. 1984. Visual communication and sexual selection in butterflies. In The biology of butterflies (R.I. Vane-Wright and P.R. Ackery, ed.). Princeton University Press, Princeton, p.207-223.
- SCHWANWITSCH, B.N. 1924. On the groundplan of wing-pattern in nymphalids and certain other families of rhopalocerous Lepidoptera. Proc. Zool. Soc. Lond. B. 34:509-528.
- SRYGLEY, R.B. & PENZ, C.M. 1999. The lek mating system in Neotropical owl butterflies: Caligo illioneus and C. oileus (Lepidoptera, Brassolinae). J. Insect Behav. 12:81-103. http://dx.doi.org/10.1023/A:1020981215501
» http://dx.doi.org/10.1023/A:1020981215501 - STEVENS, M. 2005. The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera. Biol. Rev. 80:573-588. http://dx.doi.org/10.1017/S1464793105006810
» http://dx.doi.org/10.1017/S1464793105006810 - STRADLING, D.J. 1976. The nature of the mimetic patterns of the brassolid genera, Caligo and Eryphanis. Ecol. Entomol. 1:135-138. http://dx.doi.org/10.1111/j.1365-2311.1976.tb01214.x
» http://dx.doi.org/10.1111/j.1365-2311.1976.tb01214.x - SÜFFERT, F. 1927. Zur vergleichende analyse der schmetterlingszeichnung. Biol. Zent. Bl. 47:385-413.
- TURNER, J.R.G. 1984. Mimicry: the palatability spectrum and its consequences. In The biology of butterflies (R.I. Vane-Wright and P.R. Ackery, ed.). Princeton University Press, Princeton, p.141-161.
- VAN SOMEREN, V.G.L. & JACKSON, T.H.E. 1959. Some comments on protective resemblance amongst African lepidoptera (Rhopalocera). J. Lep. Soc. 13:121-147.
- VANE-WRIGHT, R.I. 1976. A unified classification of mimetic resemblances. Biol. J. Linn. Soc. 8:25-56. http://dx.doi.org/10.1111/j.1095-8312.1976.tb00240.x
» http://dx.doi.org/10.1111/j.1095-8312.1976.tb00240.x - VANE-WRIGHT, R.I., & ACKERY, P.R. 1984. The biology of butterflies. Princeton University Press, Princeton, 429p.
- WAHLBERG, N., LENEVEU, J., KODANDARAMAIAH, U., PEÑA, C., NYLIN, S., FREITAS, A.V.L. & BROWER, A.V.Z. 2009. Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proc. R. Soc. B. 276:4295-4302. http://dx.doi.org/10.1098/rspb.2009.1303
» http://dx.doi.org/10.1098/rspb.2009.1303
Appendix 1 Examined specimens and useful links (last accessed 1 April 2013). All photographs in D’Abrera (1987) and Casagrande (2002) were also examined. Abbreviations: M, male; F, female; AMNH, American Museum of Natural History, US; BMNH, The Natural History Museum, UK; CMNH, Carnegie Museum of Natural History, US; InBio, Instituto Nacional de Biodiversidad, Costa Rica; LACM, Natural History Museum of Los Angeles County, US; MAPA, Museu Anchieta (Porto Alegre), Brazil; MECN, Museo Ecuatoriano de Ciencias Naturales, Ecuador; MPM, Milwaukee Public Museum, US; NMNL, National Museum of Natural History Naturalis, The Netherlands; MZSP, Museu de Zoologia, Universidade de São Paulo, Brazil; PJD, Phil DeVries, private collection; UFL, University of Florida, US; UFSC, Universidade Federal de Santa Catarina, Brazil; USNM, United States National Museum, Smithsonian Institution, US.
Bia Hübner, 1819
Two species examined directly; see also http://fs.uno.edu/cpenz/bia.html
Bia actorion-complex (Linnaeus, 1763)
1 M, Peru, Loreto, Iquitos (MPM); 5 M, Ecuador, Sucumbios, Garza Cocha, 7 Mar 1994, 6 Apr 1994, 17 Jan 1995, 9 Jul 1995, 10 Dec 1995 (PJD); 1 M, Venezuela, Alto Orinoco, 19 Nov 1951 (USNM); 1 M, British Guiana, Kangaruma, Potaro, 2 Nov 1908 (CMNH); 1 M, Suriname, 25 Oct 1969 (NMNL); 3 M, Brazil, Amazonas, Manaus, 6 Dec 1993, 10 Dec 1993, 15 Jul 1985 (USNM); 1 F, Peru Satipo (MPM); 4 F, Ecuador, Sucumbios, La Selva Biological Station, 6 Jan 1993, 5 Aug 1994, 7 Jul 1995, and 4 Feb 1994 (PJD); 1 F, Brazil, Amazonas, Manaus, Dec 1993 (USNM); 1F, Brazil, no date (USNM); 3 F, Peru, Madre de Dios, Manu, 15 Nov 1990, 2 May 1991, and 14 May 1991 (USNM); 2 F, Venezuela, Suapure, no date and 22 Dec 1899 (CMNH); 2 F, Brazil, Nova Olinda, Rio Purus, Jun 1922 and Mar 1922 (CMNH); 1 F, Brazil, Arima, Rio Purus, Mar 1922 (CMNH); 3 F, Bolivia, Yapacani River Feb 1915, Marc 1915, Sep 1914 (CMNH)
Bia actorion decaerulea Weymer, 1911
7 M, French Guiana, Mana River, June 1917 (CMNH); 1 M, Brazil, Amazonas, Tonantins, Aug 1923 (CMNH); 4 M, Brazil, Amazonas, Manacapuru Apr 1925 (CMNH); 1 F, French Guyana, Pied Saut, Oyapok River, Jan 1918 (CMNH); 3 F, French Guyana, Mana River, Jun 1917 (CMNH); 3 F, Brazil, Manacapuru, Mar 1925, Apr 1925, and Sep 1923
Bia peruana Röber, 1904
1 M, Peru, Chuchurras, no date (BMNH); 1 M, Peru, Pasco Pan de Azucar 25 Jul 1961 (LACM); 1 M, Peru, Huanuco, Rio Pichis, no date (UFL); 1 F, Peru, Pachitea, 7 Feb (BMNH)
Narope Doubleday, 1849
Six species examined directly, 11 through photographs in Casagrande (2002)CASAGRANDE, M.M. 2002. Naropini Stichel, taxonomia e imaturos (Lepidoptera, Nymphalidae, Brassolinae). Rev. Bras. Zool. 19:467-569. http://dx.doi.org/10.1590/S0101-81752002000200012
http://dx.doi.org/10.1590/S0101-81752002...
; see also http://fs.uno.edu/cpenz/narope.html
Narope cyllabarus Westwood, 1851
1 M, Bolivia, no date (MPM)
Narope cyllarus Westwood, 1851
1 M, Brazil, Paraná, Sep 1952 (MPM)
Narope cyllastros Doubleday, 1849
1 M, no data (MPM); 1 M, Brazil, Paraná, Rio das Cobras, Feb 1942 (MPM); 1 F, Brazil, Santa Catarina, Nova Teutônia 14 Feb 1961 (MPM); 1 F, Paraguay, no date (MPM); 1 F, Brazil, Minas Gerais, no date (AMNH)
Narope nesope Hewitson, 1869
1 M, Bolivia, no date (MPM)
Narope panniculus Stichel, 1904
2 M, Ecuador, no date (AMNH); 1 M, Bolivia, Santa Cruz, Buenavista Ichilo, Mar 1954 (MPM); 1 M, Bolivia, Santa Cruz, Ichilo, Mar 1955 (UFL); 1 F, Brazil, Minas Gerais (AMNH)
Narope anartes Hewitson, 1874
1 M, Colombia, Cali 12 May 1963 (MPM)
Aponarope Casagrande, 1982
One species examined directly, nested within Narope (Penz 2007PENZ, C.M. 2007. Evaluating the monophyly and phylogenetic relationships of Brassolini genera (Lepidoptera, Nymphalidae). Sys. Entomol. 32:668-689. http://dx.doi.org/10.1111/j.1365-3113.2007.00391.x
http://dx.doi.org/10.1111/j.1365-3113.20...
); see also http://fs.uno.edu/cpenz/aponarope.html
Aponarope sutor (Stichel, 1916)
1 M, Brazil, Rondônia, Fazenda Rancho Grande, 17 Apr 1992 (UFL)
Brassolis Fabricius, 1807
Six species examined directly, see also http://fs.uno.edu/cpenz/brassolis.html
Brassolis sophorae (Linnaeus, 1758)
1 M, Guiana Française (UFL); 1 M, British Guiana, Georgetown, 1959 (MPM); 1 M, Trinidad (UFL); 1 M, Ecuador, Napo Prov., Jatun Sacha Biol. Sta., 1988 (UFL); 1 M, Peru, Loreto, 1961, Pucallpa (UFL); 1 M, Bolivia, Santa Cruz (UFL); 1 M, Bolivia, Santa Cruz, 1972 (UFL); 1 M, Paraguay, Villarica, 1951 (MPM); 1 M, Brazil, Sta. Catarina, Nova Teutônia, 1960 (MPM); 1 F, Guiana Française (UFL); 1 F, Trinidad, Moruga (UFL); 1 F, Ecuador, Apuya, Napo Province, 1993; 1 F, Ecuador, Puyo, Oriente, 1950 (MPM); 1 F, Peru, Loreto, 1981 (UFL); 1 F, Bolivia, Beni Riveralta, 1986 (UFL); 1 F, Bolivia, Sta. Cruz Mineros, 1956 (MPM); 1 F, Paraguay, Villarica, 1949 (MPM); 1 F, Brazil, Nova Friburgo, Rio de Janeiro (MPM); 1 F, Brazil, São Paulo, São Carlos, 1979 (UFL).
Brassolis dinizi d'Almeida, 1956
3 M, Brazil, Ceará, Fortaleza 1956, 1958 and 1959 (MPM); 1 M, North Brazil, 1973 (MPM); 1 M, Paraíba, Brazil, (MPM); 1 F, Brasil, Paraisa [sic] (MPM); 2 F, Brazil, Ceará Fortaleza, 1959 (MPM)
Brassolis haenschi Stichel, 1902
1 M, Ecuador, Balzapamba (UFL); 1 M, Ecuador, Balzapamba (BMNH); 1 F, Ecuador, Los Rios Province, Rio Palenque (UFL); 1 F, Ecuador, Los Rios Province, Rio Palenque (UFL)
Brassolis isthmia Bates, 1864
1 M, Costa Rica, Limon province, Puerto Viejo, 1989 (UFL); 1 M, Panama, Canal Zone, 1973 (MPM); 1 M, Panama, Balboa, 1966 (UFL); 1 F, Panama, Tocumen, 1976 (UFL)
Brassolis granadensis Stichel, 1902
1 M, Colombia Cali, 1956 (MPM); 1 M, no data (UFL); 1 F, Colombia, Tolima, Payande, Mina Vieja area, 1974 (UFL).
Brassolis astyra Godart, 1824
1 M, Brazil, 1939 (MPM); 1 M, Brazil, Pará, Obidos, 1952 (MPM); 1 M, Brazil, Rio de Janeiro, Gávea, 1960 (MPM); 1 M, Brazil, Corcovado, Rio [de Janeiro], 1910 (UFL); 1 M, Brazil, [Santa Catarina], Corupa (MPM); 1 M, Brazil, Santa Catarina (MPM); 1 M, Brazil, Gravatai, 1966 (MAPA); 1 M, Brazil, Gravatai, 1966 (MAPA); 1 F, Brazil, 1932 (MPM); 1 F, [Brazil], Rio [de] Janeiro (UFL); 1 F, Brazil, Rio de Janeiro, 1960 (MPM); 1 F, Brazil, Corcovado, Rio [de Janeiro], 1910 (UFL); 1 F, Brazil, Itaci, São Paulo, 1960 (MPM); 1 F, Brazil, Santa Catherina, Rio Tirubo, 1937 (MPM); 1 F, Brazil, Gravatai, 1966 (MAPA); 1 F, Brazil, Gravatai, 1966 (MAPA).
Dynastor Doubleday, 1849
Three species examined directly, see also http://fs.uno.edu/cpenz/dynastor.html
Dynastor darius (Fabricius, 1775)
1 M, Paraguay, 1973 (MPM); 1 M, Nicaragua, Managua dept., Managua, 1858 (MPM); 1 F, Brazil, Paraná, Ponta Grossa, XI 1947 (MPM); 1 F, Brazil, Santa Catarina, “Mansa Humbolt” [sic] (MPM).
Dynastor napoleon Doubleday, 1849
1 M, Brazil, Santa Catarina, XI 1954 (MPM); 1 M, Brazil, Santa Catarina, IX 1964 (MPM); 1 M, Brazil, Santa Catarina, 1956 (UFL); 1 F, Brazil, Rio de Janeiro, 1920 (MPM); 1 F, no data (UFL)
Dynastor macrosiris (Westwood, 1851)
1 M, Guiana Française (UFL); 1 M, El Salvador, Finca El Refugio, Ahuachapan, Sep 2006 (PJD); 1 F, Mexico, Chiapas, 1973 (UFL); 1 F, El Salvador, Finca El Refugio, Ahuachapan, Sep 2006 (PJD).
Opoptera Aurivillius, 1882
Eight species examined directly, see also http://fs.uno.edu/cpenz/opoptera.html
Opoptera syme (Hübner, 1821)
1 M, Brazil, R.J., Nova Friburgo, 22 Feb 1961; 1 M, Brésil, Etat de Sao Paolo, no date (UFL); 1 M, Sumaní, Guanabara [RJ], Parque da Tijuca, Brazil, Aug 14 1972 (UFL); 1 F, South America, no date (UFL); 1 F, Petropolis [RJ], Brazil, no date (USNM); 1 F, Brazil, Rio de Janeiro St., no date (USNM)
Opoptera sulcius (Staudinger, 1887)
1 M, Brazil, Pinhal [São Paulo], Feb 1950 (MPM); 1 M, Brazil, Santa Catarina, Taió, Feb 1959 (MPM); 1 M, Brazil, Santa Catarina, São Bento do Sul, Mar 10 1984 (UFL); 1 M, Brazil, Santa Catarina, Gaio (sic) [likely Taió], Feb 1986 (UFL); 1 F, Brazil, Santa Catarina, Feb 1964 (MPM); 1 F, South Brazil, no date (MPM); 1 F, Brazil, Joinville, 14 Mar 1964 (UFL); 1 F, Brazil, São Luis do Puruná, Paraná, 16 Mar 1984 (UFL)
Opoptera fruhstorferi (Röber, 1896)
1 M, Brazil, St. Catherines, no date (AMNH); 1 M, South Brazil, no date (MPM); 1 M, Brazil, Taió, St. Cath., Feb 1956 (MPM); 2 F, Itaporanga [São Paulo, Brazil], Feb 1948 and Mar 1948 (AMNH); 1 F, Brazil, Santa Catarina, 6 Feb 1963 (MPM); 1 F, South Brazil, no date (MPM)
Opoptera aorsa (Godart, 1824)
1 M, Brazil, Toledo, Paraná, Nov 1969 (MPM); 1 M, Espírito Santo, Brazil, no date (AMNH); 5 M Brazil, Espírito Santo, no date (AMNH); 1 M, Brazil, North Paraná, no date (AMNH); 1 M, Brazil, Paraná, no date (AMNH); 1 F, Brazil, Nova Friburgo, R.J., 3 Mar 1961 (MPM); 1 F, Brazil, North Paraná, no date (AMNH); 1 F Espírito Santo, Brazil, no date (AMNH)
Opoptera hilaris Stichel, 1901
1 M, Ecuador, Río Huagra-yacu, Oriente, 3 Apr 1941 (AMNH); 2 M, Ecuador, Río Huagra-yacu, Oriente, 12 and 14 Apr 1941 (AMNH); 2 M, Ecuador, no date (AMNH); 1 M, Middle Ecuador, no date (AMNH); 2 M, Oriente Ecuador, no date (AMNH); 1 M, Ecuador, Sucumbios, La Selva Biological Station, 2 Aug 1993 (PJD); 1 M, Peru, Puerto Maldonado, Los Amigos Biological Station, 13 Feb 2004 (PJD); 1 M, Peru, Chanchamayo, no date (AMNH); 1 M, Peru, Jepelacio, North no date (AMNH); 1 M, Bolivia, no date; 1 M, Brazil, Puraquequara, Amazonas, 10 Apr-10 May 1945 (AMNH); 1 F, Ecuador, Sucumbios, La Selva Biological Station, 10 Dec 1997 (PJD)
Opoptera staudingeri (Godman & Salvin, 1894)
1 M, Costa Rica, Heredia, Puerto Viejo, Feb 1970 (MPM); 1 F, Costa Rica, Heredia, Puerto Viejo, Feb 1970 (MPM)
Opoptera arsippe (Hopffer, 1874)
3 M, Peru, Pasco, Chuchurras, no date (UFL); 2 M, Peru, Huanuco, ca. 15 kms. N of Tingo Maria on Rio Huallaga, 15-22 Aug 1981 and Aug 1981 (UFL); 1 M, Peru, Tingo Maria, 19-24 Jul 1978 (LACM); 2 M, Peru, Huánuco, Tingo Maria, Dec 1984 (LACM); 2 M, Bolivia, no date (LACM); 2 M no data (LACM); 1 M, Peru, Juanjui, Iquitos, 7-19 May 1961 (UFL); 4 M, Chanchamayo, Peru, no date (AMNH)
Opoptera bracteolata Stichel, 1901
1 M, Bolivia, no date (MPM); 1 M, Bolivia, Cochabamba, Chapare, Alto Palmar, Dec 1956 (UFL)
Dasyophthalma Westwood, 1851
Four species examined directly, see also http://fs.uno.edu/cpenz/dasyophthalma.html
Dasyophthalma rusina (Godart, 1824)
1 M, Brazil, Santa Catarina 26 Dec 1957 (MPM); 1 M, South Brazil, no date (MPM); 1 M, Brazil, Espírito Santo, Santa Teresa, 4-7 March 1973 (UFL); 1 M, Brazil, Rio de Janeiro, Petrópolis, Independência, 16 Jan 1972 (UFL); 1 M, Brazil, Rio de Janeiro, Petrópolis, 9-12 Jan 1971 (UFL); 1 M, Brazil, Minas Gerais, Parque Rio Doce, 26 Mar1972 (UFL); 2 M, Brazil, Santa Catarina, São Bento do Sul, 10 Mar 1984 (UFL); 1 M, Brazil, Santa Catarina, 1 Jan 1968 (UFL); 1 M [Brazil] Sta. Catharina, no date (AMNH); 1 F, Brazil, Santa Catarina, São Bento do Sul, 25 Jan 1966 (MPM); 1 F, South Brazil, no date (MPM)
Dasyophthalma geraensis Rebel, 1922
1 M, Brazil, Minas Geraes, no date (MZSP); 1 M, [Brazil] Minas Geraes, no date (AMNH); 1 M Brazil, Espírito Santo, Castello, 21 Feb 1922 (UFL); 1 M, Brazil, Rio de Janeiro, Parque Nacional do Itatiaia, 13-14 Jan 1973, (UFL); 1 M, Brazil, Brazil, Rio de Janeiro, Itatiaia, 21 Mar 1972 (UFL)
Dasyophthalma creusa (Hübner, 1821)
1 M, South Brazil, no date, (MPM); 1 M, Brazil, Santa Catarina, São Bento do Sul, 13 Feb 1966 (MPM); 1 M, Brazil, Santa Catarina, São Bento do Sul, 10 Feb (UFL); 1 M, Brazil, Santa Catarina, São Bento do Sul, 10 Feb 1984 (UFL); 1 M, Brazil, Rio de Janeiro, Dec 1943 (UFL); 1 M, Brazil, Guanabara [Rio de Janeiro], Jacarepaguá, 20 Feb 1971 (UFL); 1 F, South Brazil, no date, (MPM); 1 F, Brazil, Santa Catarina, São Bento do Sul, 13 Feb 1966 (MPM)
Dasyophthalma vertebralis Butler, 1869
1 M, Brazil, Espírito Santo (MZUSP); 1 F, [Brazil] East Amazonas, no date (MZUSP)
Caligopsis Seydel, 1924
One species examined directly, see also http://fs.uno.edu/cpenz/caligopsis.html
Caligopsis seleucida (Hewitson, 1877)
2 M, Peru, Puerto Maldonado, Los Amigos Biological Station, 10 Sep 2004 and 12 Oct 2004 (PJD); 1 M, Bolivia, Cochabamba, San Francisco, Apr 1976 (MPM); 2 F, Peru, Puerto Maldonado, Los Amigos Biological Station, 9 Apr 2004 and 14 Oct 2004 (PJD); 1 F, Brazil, Amazonas, Madeira River, no date (USNM)
Eryphanis Boisduval, 1870
Nine species examined directly, see also http://fs.uno.edu/cpenz/eryphanis.html
Eryphanis automedon (Cramer, 1775)
1 M, Venezuela, Waterworks, Puerto Cabello, Carabobo, 22 Jul 1979 (UFL); 1 M, Trinidad, BWI, Mar 1937 (UFL); 2 M, Trinidad [18]98 (UFL); 1 M, Trinidad, Arima Valley, SIMLA Research Station, 27 Jun-3 Jul 1978 (UFL); 1 M, British Guyana, Kamarung, 10-14 Oct 1977 (UFL); 1 M, Surinam, Jan 2001 (PJD); 2 M, French Guiana, R. Orapu (UFL); 1 M, Colombia, Cali 19 Dec 1966 (MPM); 1 M, Colombia, Vaupes, San Jose del Guaviare, Dec [19]91 (UFL); 1 M, Colombia, Villavicencio, Ocoa, 27 Oct 1943 (UFL); 2 M, Ecuador, Sucumbios, Garza Cocha, La Selva Biological Station, 17 Jan 1995 and 9 Jan 1998 (PJD); 1 M, Ecuador, Napo, Limoncocha, 10 Oct 1971 (UFL); 1 M, Ecuador, Napo, Misahualli, 28 Apr 1971 (UFL); 1 M, Ecuador, Balzapampa, no date (UFL); 2 M, Peru, Puerto Maldonado, Los Amigos Biological Station, 13 May 2004 and 15 Oct 2004 (PJD); 1 M, Peru, Huanuco, Tingo Maria, Rio Huallaga, 15-22 Aug 1981 (UFL); 1 M, Peru, Mogotta (sic), 14 May 1955 (UFL); 1 M, Peru, Tingo Maria, 30 Jul 1980 (UFL); 1 M, Brazil, Para, Obidos, Mar 1976 (MPM); 1 M, Brazil, Rondonia, Jaru, 9 Aug 1976 (UFL); 1 M, Brazil, Rondonia, Caucalandia 13 nov 1990 (UFL); 1 M, Brazil, Rondonia, Fazenda Rancho Grande 9 Nov 1990 (UFL); 3 M, Brazil, Minas Gerais, Uberaba, no date (UFL); 1 M, Brazil, Guanabara [=Rio de Janeiro], Gávea, 6 Feb 1973 (UFL); 1 M, Brazil, Santa Catarina, Blumenau, no date (UFL); 1 M, Bolivia, Santa Cruz, 29 Apr 1959 (MPM); 1 M, Bolivia, Santa Cruz, Buenavista, Ichilo, Feb 1946 (UFL); 1 M, Bolivia, no date (UFL); 2 M, Paraguay, Amambay, Pedro Juan Caballero, 4 Feb 1969 (MPM); 1 F, Trinidad, Maquerippe Bay, 22 Aug 1974 (UFL); 1 F Trinidad, St. Amis, 23 Nov 1920 (UFL); 1 F, Surinam, Lelydorp, no date (PJD); 1 F, French Guiana, R. Orapu (UFL); 2 F, Ecuador, Napo, Misahualli, 3 Sep 2000 (UFL); 1 F, Peru, Puerto Maldonado, Los Amigos Biological Station, 14 Jul 2004 (PJD); 1 F Peru, Tingo Maria, 30 Jul 1980 (UFL); 1 F, Brazil, Rondonia, Fazenda Rancho Grande, 22 Mar 1991 (UFL); 1 F, Brazil, Minas Gerais, Uberaba, no date (UFL); 1 F, Paraguay, Pedro Juan Caballero, 4 Feb 1969 (MPM)
Eryphanis lycomedon (Meerburgh, 1780)
1 M, Guatemala, no date (UFL); 1 M, Costa Rica, Puntarenas, Pto. Cortez 23 Nov 2003 (INBio); 1 M, Costa Rica, Heredia, Santa Clara, 5 Sep 1987 (UFL); 1 M, Costa Rica, Alajuela, Rio Virilla, 5.5 km SW Guacima, 2 Oct 1967 (UFL); 1 M, Panama, Canal zone, Madden Forest, 21 Aug 1969 (UFL); 1 M, Panama, Las Cumbres, Oct 1960 (UFL); 1 M, Colombia, Cali, 19 Dec 1966 (MPM); 1 M, Colombia, Cali, 20 Oct 1965 (MPM); 1 M, Colombia, Cauca, Pescador, 29 Jan 1974 (UFL); 11 M, Colombia, Boyaca, Muzo, no date (UFL); 2 M, Colombia, Valle de Cauca, Cali (Cañas Gordas), 1 Oct 1973 and 21 Feb 1974 (UFL); 1 M, Colombia, Rio Guatiquia, Apr 1917 (UFL); 2 M, Colombia, Yacopi, 1936 and 12 Apr 1938 (UFL); 1 M, Ecuador, Pichincha, Santo Domingo de los Colorados, 8 May 1988 (UFL); 1 M, Ecuador, Tonchigue, Apr 1964 (MPM); 1 M, Ecuador, Los Rios, Rio Palenque, no date (UFL); 1 M, Ecuador, Pichincha, Hotel Tinalandia, Santo Domingo de los Colorados, 10 May 1988 (UFL); 1 M, Bolivia, no date (UFL); 1 M, Bolivia, no date (UFL); 7 M, Brazil, Santa Catarina, Blumenau (UFL); 1 F, Costa Rica, Puntarenas, Corcovado National Park, Apr 1989 (INBio); 1 F, Costa Rica, Heredia, Pueblo Nuevo Sarapiqui 24 Jul- 22 Aug 1992 (INBio); 1 F, Costa Rica, Cartago, Turrialba, 13 Jul 1965 (UFL); 1 F, Costa Rica, Alajuela, Atenas, 16 Dec 1984 (UFL); 1 F, Panama, Canal Zone, Madden Forest, 2 Dec 1969 (UFL); 1 F, Panama, Las Cumbres, 25 Jan 1964 (UFL); 1 F, Colombia, Cali, 27 May 1966 (MPM); 1 F, Colombia, Cali, 2 Nov 1966 (MPM); 2 F, Colombia, Valle de Cauca, Cali (Cañas Gordas), 13 Jan 1974 (UFL); 2 F, Colombia, Cali, Pance, Valle, 22 and 25 Jan 1987 (UFL); 1 F, Colombia, Cali, Valle, 9 Aug 1979 (UFL); 1 F, Ecuador, Tonchigue, Apr 1964 (MPM); 1 F, Ecuador, Pichincha, Alluriquin, 16 Aug 1972 (UFL); 1 F, Ecuador, Pichincha, Hotel Tinalandia, Santo Domingo de los Colorados, 8 May 1988 (UFL); 1 F, Ecuador, Pichincha, Tinalandia, Santo Domingo, 5 May 1992 (UFL); 1 F, Brazil, Santa Catarina, Blumenau, no date (UFL)
Eryphanis aesacus (Herrich-Schäffer, 1850)
1 M, Mexico, San Luis Potosi 23 Jul 1937 (MPM); 1 M, Mexico, Catemaco, Nov 1965 (MPM); 2 M, Mexico, Oaxaca, Monteflor Jun 1978 (UFL); 1 M, Mexico, Oaxaca, Chiltepec, 3 Sep 1976 (UFL); 1 M, Mexico, South of Tampico, 1 Nov 1975 (UFL); 1 M, Mexico, Escarcega, Campeche 2 and 5 May 1969 (UFL); 1 M, Mexico, Taumalipas, Taumazunchale, no date (UFL); 1 M, Mexico, El Pujal, San Luis Potosi, 18 Jun 1939 (UFL); 1 M, Guatemala, Chacoj, Pelochic, no date (BMNH); 1 M, Guatemala, Alta Verapaz, Baleu Mpio., San Cristobal, Verapaz, 24 Sep 1966 (UFL); 1 M, El Salvador, Ahuachapan, El Refugio Sep 2003 (PJD); 1 M, El Salvador, Ahuachapan, La Fincona El Imposible, 13 Sep 1984 (UFL); 1 M, Belize, Cayo Distr., Green Hills 29 Jul 2007 (PJD); 1 F, Mexico, no date (MPM); 1 F Mexico, Oaxaca, Tuxtepec, 4 Sep 1976 (UFL); 2 F, Mexico, Presidio, Jun 1951 (UFL); 2 F Mexico, Catemaco, Sep 1956 (UFL); 1 F, Guatemala, Central Valleys, no date, #802305, (BMNH); 1 F, Guatemala, Petén, Parque Nacional Tikal, 20 Sep 1993 (UFL); 1 F, El Salvador, Ahuachapan, El Refugio Sep 2003 (PJD); 1 F, El Salvador V.C. Santa Ana, D.C. Santa Ana, Nov 1997 (PJD); 1 F, El Salvador, San Salvador, 13 Nov 1984 (UFL)
Eryphanis bubocula (Butler, 1872)
1 M, Costa Rica, Guanacaste, Rio San Lorenzo, Tierras Morenas Aug 1992 (INBio); 1 F, Costa Rica, Cartago, Tapanti 9 Apr 1983 (INBio); 1 F, Colombia, Val. Del Cauca, Calima Valley, 14 Feb 1989 (UFL)
Eryphanis gerhardi (Weeks, 1902)
1 M, Ecuador, Balzapampa, no date (UFL); 1 M, Bolivia, no date (MPM); 1 M, Bolivia, Cochabamba Mar 1955 (MPM); 1 M, Bolivia, Chapare, Alto Palmar, Sep 1954 (MPM); 1 M, Bolivia, Cochabamba, El Palmar Chapare, Apr 1947 (UFL); 1 M, Bolivia, Cochabamba, Alto Palmar Chapare, Oct 1958 (UFL); 1 M, Bolivia, Santa Cruz, Buenavista, Ichilo, 21 Feb 1994 (UFL); 1 M, Brazil, Rondonia, Jaru 9 Aug 1976 (UFL); 1 F, Brazil, Rondonia, Jaru, 6 Aug 1976 (UFL)
Eryphanis reevesii (Doubleday, 1849)
1 M, Brazil, São Paulo, Pinhal Apr 1955 (MPM); 1 M Brazil, São Paulo, Itaici 3 Sep 1961 (MPM); 1 M, Brazil, Meatana [maybe Mendanha, Minas Gerais] 20 Jul 1968 (UFL); 1 M, Brazil, [São Paulo], Pinhal, Mar 1952 (UFL); 1 M, Brazil, Santa Catarina, Blumenau, no date (UFL); 4 M, Brazil, Santa Catarina, São Bento do Sul, 10 Mar 1984 (UFL); 1 M, Brazil, Santa Catarina, Trombudo Alto, 28 Mar 1957 (UFL); 2 M, Argentina, Parque Nacional Iguasu, Misiones, 18 Jun 1973; 1 M, Argentina, Misiones, Rio Uruguay 19 Jun 1973 (UFL); 1 F, Brazil, Rio de Janeiro, Nova Friburgo Oct 1958 (MPM); 1 F, Brazil, São Paulo, Pinhal Apr 1955 (MPM); 2 F, Brazil, Minas Gerais, Uberaba, no date (UFL); 1 F Brazil, Santa Catarina, Trombudo Alto, 26 Mar 1956 (UFL)
Eryphanis zolvizora (Hewitson, 1877)
1 M, Bolivia, Cochabamba Mar 1955 (MPM); 1 M, Bolivia, no date (MPM); 1 M, Bolivia, Cochabamba, El Palmar Apr 1947 (UFL); 1 M, Bolivia, Cochabamba, El Palmar Chapare, Apr 1947; 1 M, Bolivia, Las Yungas, Nov 1990 (UFL); 1 F, Bolivia, Cochabamba, Alto Palmas Sep 1958 (UFL)
Eryphanis opimus (Staudinger, 1887)
1 M, Colombia, Cali 29 Sep 1964 (MPM)
Eryphanis greeneyi Penz & DeVries, 2008
1 M, Ecuador, Napo, Yanayacu Biological Station, 5km W of Cosanga, May 2007, HOLOTYPE (BMNH); 1 M, Ecuador, Napo Prov., Yanayacu Biological Station (MECN); 1 M, Ecuador, Provincia Napo, YYBS, 5-Feb-[20]02 (AMNH); 1 M, Ecuador, Provincia Napo, 12-Apr-[20]00 (PJD); 1 M, Ecuador, Rio Blanco, near Baños, Abril 17/[19]56 (MPM); 1 M, Ecuador, Balzapampa, (UFL); 1 M, Ecuador, Zamora-Chinch. Province, Zumba-Loja 21-23 Sep 1993 (UFL); 1 F, Ecuador, Napo, Yanayacu Biological Station, May 2007 (BMNH); 1 F, Ecuador: Napo Prov., Yanayacu Biological Station (MECN); 1 F, Ecuador, Napo, Biol. Yanayacu, no date (AMNH); 1 F, Ecuador, Provincia Napo, San Isidro, 21-Dec-[19]99 (PJD).
Caligo Hübner, 1819
Thirteen species examined directly, see also http://fs.uno.edu/cpenz/caligo.html
Caligo arisbe Hübner, 1822
2 M, Brazil, Paraná, São Luis do Puruna, 16 Mar 1984 (UFL); 1 M, Brazil, no date (UFL)
Caligo atreus (Kollar, 1850)
1 M, Colombia, Antioquia, Zaragosa (MPM); 1 M, Costa Rica, Heredia, Puerto Viejo, Finca La Selva, 1968-1970 (MPM); 1 M, Costa Rica, Heredia, Puerto Viejo, Finca La Selva, 1968-1970 (MPM); 1 F, no data (MPM)
Caligo beltrao (Illiger, 1801)
1 M, Brazil, Stuporanza, Dec 1950 (MPM); 1 M, Brazil, Santa Catarina, Joinvile Mar 1972 (MPM); 1 F, Brazil, Stuporanza, Jan 1951 (MPM); 1 F, Brazil, Santa Catarina, Joinvile, Feb 1969 (MPM)
Caligo eurilochus (Cramer, 1775)
1 M, Costa Rica, Heredia, Puerto Viejo, Finca La Selva, 17 Feb 1978 (MPM); 1 F, Costa Rica, Heredia, Puerto Viejo, Finca La Selva, Feb 1969 (MPM)
Caligo idomeneus (Linnaeus, 1758)
1 M, East Peru, no date (MPM); 1 M, Colombia, no date (MPM); 1 F, East Peru, no date (MPM), 1 F, Peru, Satipo, Nov 1952 (MPM)
Caligo illioneus (Cramer, 1775)
1 M, Costa Rica, Heredia, Finca La Tirimbina 17 Feb 1978 (MPM); 1 F, Costa Rica, Heredia, Finca La Selva Feb 1969 (MPM)
Caligo martia (Godart, 1824)
1 M, Brazil, Pinhal, no date (MPM); 1 M, Brazil, São Bento, SC, Jan 1969 (MPM); 1 F, Brazil (MPM), 1 F, Brazil, Santa Catarina, 2 Jan 1963 (MPM)
Caligo oberthuri (Deyrolle, 1872)
1 M, Ecuador, Riobamba, no date (UFL); 1 F, Ecuador, Riobamba, no date (UFL)
Caligo oileus C. Felder & R. Felder, 1861
1 M, Peru, Huanuco, Tingo Maria, Mar 1981 (UFL); 1 F, Peru, Ayacucho May 1936 (UFL)
Caligo telamonius (C. Felder & R. Felder, 1862)
1 M, Colombia, Cauca, May 1917 (UFL); 1 F, Colombia, Cauca Valley, no date (UFL)
Caligo teucer (Linnaeus, 1758)
1 M, Peru, Tingo Maria, Jul 1980 (UFL); 1 F, Peru, Tingo Maria, 25 May 1972 (UFL)
Caligo Uranus Herrich-Schäffer, 1850
1 M, Mexico, Chiapas, Bonampak, Jul-Aug 1976 (UFL); 1 F, Mexico, Santa Rosa Comitán, Apr 1962 (UFL)
Caligo zeuxippus H. Druce, 1902
1 M, Ecuador, Pichincha, Santo Domingo de los Colorados, 10 May 1988 (UFL); 1 F, Ecuador, Pichincha, Santo Domingo de los Colorados, 9 May 1988 (UFL)
Selenophanes Staudinger, 1887
Three species examined directly, see also http://fs.uno.edu/cpenz/selenophanes.html
Selenophanes cassiope (Cramer, 1775)
1 M, Brazil, Paraná, Rolandia, Dec 1942 (AMNH), 1 M, Peru, Chanchamayo, no date (AMNH), 2 M, Peru, Puerto Maldonado, Los Amigos Biological Station, 15 Jun 2004 and 12 Sep 2004 (PJD); 1 F, Peru, Rio Huallaga (AMNH), 2 F, Peru, Puerto Maldonado, Los Amigos Biological Station, 11 Oct 2004 and 15 Oct 2004 (PJD), 1 F, no località, 20 Sep 1922 (USNM)
Selenophanes josephus (Godman & Salvin, 1881)
1 M, Panama, Canal Zone, Madden Forest, 20 Jul 1970 (USNM); 1 F, Panama, Darién, Caña, 5 Jul 1981 (USNM)
Selenophanes supremus Stichel, 1901
2 M, Peru, Chanchamayo, no date (UFL)
Penetes Doubleday, 1849
One species examined directly, see also http://fs.uno.edu/cpenz/penetes.html
Penetes pamphanis Doubleday, 1849
1 M, Brazil, Paraná, Curitiba (MPM); 1 M, Paraguay, Villarica, Nov. 1948 (MPM); 1 F, Brazil, no date (MPM); 1 F, Brazil, Rio Grande do Sul, no date (USNM)
Catoblepia Stichel, 1901
Seven species examined directly, see also http://fs.uno.edu/cpenz/catoblepia.html
Catoblepia amphirhoe (Hübner, 1825)
1 M, Brazil, Santa Catarina, São Bento do Sul, 10 Mar 1984 (UFL); 1 M, Brazil, Santa Catarina, São Bento do Sul, 10 Feb (UFL); 1 M, Brazil, São Paulo, Araçatuba (UFL); 1 F, Brazil, São Paulo, Mendes, no date (UFL)
Catoblepia berecynthia (Cramer, 1777)
1 M, Central Peru, no date (MPM); 2 M, Peru, Puerto Maldonado, Los Amigos Biological Station, 10 Oct 2004 and 14 Oct 2004 (PJD); 1 F, Paraguay, no date (MPM),
Catoblepia orgetorix (Hewitson, 1870)
1 M, Colombia, Antioquia, Zaragosa, 18 Feb 1977 (MPM); 1 M, Ecuador, Oriente (AMNH); 1 M, Panama, Chiriqui, no date (UFL); 1 F, Colombia, Antioquia, Zaragosa, 18 Feb 1977 (MPM), 1 F, Ecuador, Pichincha, Santo Domingo de los Colorados (AMNH); 1 F, Ecuador, Canelos, no date (UFL)
Catoblepia soranus (Westwood, 1851)
1 M, Colombia, Amazonas, Rio Tacana, 1-13 Nov 1946 (AMNH); 1 M, Ecuador, Sucumbios, Garza Cocha, La Selva Biological Station, 26 Apr 1995 (PJD); 1 M, Peru, Rio Huallaga, no date (AMNH); 1 M, Brazil, Rondônia, Fazenda Rancho Grande, 29 Nov 1991 (UFL); 1 F, Peru, no date (USNM); 1 F, Colombia, Amazonas, Rio Tacana, 26-31 Oct 1946 (AMNH); 1 F, Peru, Iquitos, no date (AMNH); 1 F, Brazil, Rondônia, Fazenda Rancho Grande, 1 Sep 1991 (UFL)
Catoblepia versitincta Stichel, 1901
1 M, French Guiana, St. Jean Maroni, no date (UFL); 1 F, French Guiana, Gourdonville, no date (UFL)
Catoblepia xanthus (Linnaeus, 1758)
1 M, Brazil, Pará, Obidos, Nov 1965 (MPM); 2 M, Ecuador, Sucumbios, Garza Cocha, La Selva Biological Station, 10 Jul 1999 and 9 Nov 1993 (PJD); 1 F, British Guiana, Georgetown, Jan 1960 (MPM); 1 F, Ecuador, Sucumbios, Garza Cocha, La Selva Biological Station, 10 Dec 1996 (PJD)
Catoblepia xanthicles (Godman & Salvin, 1881)
1 M, Ecuador, Sucumbios, Garza Cocha, La Selva Biological Station, 5 May 1996 (PJD)
Mielkella Casagrande, 1982
One species examined directly, see also http://fs.uno.edu/cpenz/mielkella.html
Mielkella singularis (Weymer, 1907)
1 M, Mexico, Chiapas, no date (AMNH); 1 M, Mexico, Chiapas June 1977 (AMNH); 1 F, [Mexico] Santa Rosa Comitán 19 Jun 37 (AMNH); 1 F, Mexico, Chiapas, no date (AMNH); 1 F, Mexico, Chiapas, no date (USNM); 1 F, Mexico, Chiapas, Santa Rosa Comitán, Mar 1966 (MPM)
Orobrassolis Casagrande, 1982
One species examined directly, see also http://fs.uno.edu/cpenz/orobrassolis.html
Orobrassolis ornamentalis (Stichel, 1906)
1 M and 1 F, Brazil, São Paulo, Umuarama (MPM)
Blepolenis Röber, 1906
Three species examined directly, see also http://fs.uno.edu/cpenz/blepolenis.html
Blepolenis bassus (C. Felder & R. Felder, 1867)
2 M, Brazil (MPM); 1 M, Brazil, S. Paulo, no date (MZSP 13713); 2 M, Brazil, E. Paraná, Murtinho, Jan 1916 and 29 Jan 1916 (MZSP 13712 and 13711); 1 F, Brazil, Campos do Jordão-Lagoinha (MZSP 13714); 1 F, Brazil, C. Jordão-Lagoinha, Jan 28 1967 (MZSP 13715); 1 F, Brazil, São Bento [do Sul], [Rio Grande do Sul], Jan 1955 (MPM).
Blepolenis batea (Hübner, 1821)
1 M, Brazil, Serra do Caraça, Minas Gerais, 24 Mar 1972 (MZSP 13717); 1 M, Brazil, Itatiaia, E. Rio [de Janeiro], (MZSP 13604); 1 M, Brazil, Nova Friburgo, Rio de Janeiro, Nov 1957 (MPM); 1 M, Brazil, C. Jordão-Lagoinha, 28 Jan 1967 (MZSP 13721); 1 M, Brazil, Est. Biol. Boracéia, Salesópolis, São Paulo, 8 Mar 1968 (MZSP 13720); 1 M, Brazil, São Paulo, Salesópolis, Boracéia, Jan 1952 (MZSP 13723); 1 M, Brazil, Itatiba, São Paulo, Dec 1935 (MZSP 13719); 1 M, Brazil, S. Paulo, no date (MZSP 13718); 1 M, Brazil, S. Paulo, no date (MZSP 13716); 1 M, Brazil, S. Paulo, Botanica, 12 Mar 1952 (MZSP 13605); 1 M, Brazil, Santa Catarina, Nova Teutônia, 19 Jan 1961 (MPM); 1 M, Brazil, Santa Catarina, no date (AMNH); 1 M, Brazil, Santa Catarina, no date B.M. 1937-285 (BMNH); 1 M, Brazil, Porto Alegre, no date (MZSP 13709); 1 M, Brazil, Pelotas, Rio Grande do Sul, 20 Jan 1967 (AMNH); 1 F, Brazil, no date (MPM); 1 F, Brazil, Est. Biol. Boracéia, Salesópolis, São Paulo, 14 Feb 1968 (MZSP 13607); 1 F, Brazil, Est. Biol. Boracéia, Salesópolis, São Paulo, 2 Mar 1968 (MZSP 13606); 1 F, Brazil, Ypiranga, São Paulo, Jan 1929 (MZSP 13722); 1 F, Brazil, S. Paulo, 5 Feb 1939 (MZSP 13724); 2 F, Brazil, Santa Catarina, no date (AMNH)
Blepolenis catharinae (Stichel, 1902)
1 M, no locality, no date, B.M. 1937-285, (BMNH); 1 M, no locality, no date (MZSP 13 710); 3 M, Brazil, Lagoa do Peri, Florianopolis-SC, Jan 2008 (UFSC); 2 F, Brazil, Lagoa do Peri, Florianópolis-SC, Jan 2008 and Feb 2008 (UFSC)
Opsiphanes Doubleday, 1849 [13]
Six species examined directly, see also http://fs.uno.edu/cpenz/opsiphanes.html
Opsiphanes boisduvallii Doubleday, 1849
1 M, no data (MPM); 1 M, Mexico, no date (MPM); 1 F, Mexico (MPM); 1 F, Mexico, San Luis Potosi, 29-31 Jul 1941 (MPM)
Opsiphanes invirae (Hübner, 1808)
1 M, Paraguay, San Salvador (MPM); 1 M, Brazil, no date (MPM); 1 F, Brazil, Espírito Santo, Linhares (MPM); 1 F, Brazil Feb 1950 (MPM)
Opsiphanes quiteria (Stoll, 1780)
2 M, Peru, Puerto Maldonado, Los Amigos Biological Station, 11 May 2004 and 12 Oct 2004 (PJD); 1 F, Peru, Puerto Maldonado, Los Amigos Biological Station, 12 Nov 2004 (PJD)
Opsiphanes tamarindi C. Felder & R. Felder, 1861
1 M, Colombia, Cali, 15 Feb 1965 (MPM); 1 F, Colombia, Cali, 15 Feb 1965 (MPM); 1 F, Nicaragua, Managua, Managua 24 Feb 1958 (MPM)
Opsiphanes sallei Doubleday, 1849
1 M, Peru, Paaco, Oxapampa, no date (UFL); 1 M, Huanoabamba, Peru, no date (AMNH); 1 F, Colombia, Rio Negro, no date (USNM); 1 F, Colombia, Bogota, no date (UFL)
Opsiphanes cassia (Linnaeus, 1758)
1 M, Catemaco, Sep 1962 (MPM)
Publication Dates
-
Publication in this collection
Sept 2013
History
-
Received
1 Apr 2013 -
Reviewed
13 Aug 2013 -
Accepted
13 Sept 2013