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349
ISSN 1863-7221 (print)
|
eISSN 1864-8312 (online)
© Senckenberg Gesellschaft für Naturforschung, 2018.
76
(2): 3 49 – 376
18.7.2018
Systematics of the butterfly genus Cissia Doubleday,
1848 (Lepidoptera: Nymphalidae: Satyrinae) using
an integrative approach
T Z
*, 1, M M. C 2, O. H.H. M 2, B
H 3, E P. B 1, A V.L. F 1, L M. M 1,
M E 4, S N 5, 6 & K R. W 5
1 Departamento de Biologia Animal and Museu de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, Rua Monteiro Lobato,
255 – Cidade Universitária Zeferino Vaz – Barão Geraldo, CEP 13083-862, Campinas, São Paulo, Brazil; Thamara Zacca * [zacca.butterfly@
gmail.com] — 2 Universidade Federal do Paraná, Laboratório de Estudos de Lepidoptera Neotropical, Curitiba, Paraná, Brazil — 3 Life Sci-
ences Department, Natural History Museum, London, UK — 4 Zoological Research Museum Alexander Koenig, Adenauer Allee 160, 53113
Bonn, Germany — 5 McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville,
Florida, USA — 6 Entomology and Nematology Department, University of Florida, Gainesville, Florida, USA — * Corresponding author
Accepted 19.iv.2018.
Published online at www.senckenberg.de/arthropod-systematics on 29.vi.2018.
Editors in charge: Brian M. Wiegmann & Klaus-Dieter Klass
Abstract. The genus Cissia Doubleday, 1848 is revised and its monophyly is tested using Maximum Likelihood analysis based on three
genes (COI, GAPDH and RpS5). A new taxonomic arrangement is proposed based on molecular and morphological evidence, and Cissia
now comprises six species, C. penelope (Fabricius, 1775), C. pompilia (C. Felder & R. Felder, 1867), C. proba (Weymer, 1911), C. eous
(Butler, 1867) comb.n., C. phronius (Godart, [1824]) comb.n. and C. rubricata (W.H. Edwards, 1871) comb.n., distributed from the
Southern US to Argentina. The remaining species previously treated in Cissia are here cited as “Cissia” until they can be removed to
undescribed genera in upcoming papers. Euptychia moneta Weymer, 1911, E. austera Butler, 1867 and Paryphthimoides kiliani Anken,
1999 are new synonyms of Cissia penelope, C. pompilia and C. eous, respectively. Neotypes of Euptychia moneta, Satyrus phronius and
Neonympha rubricata are designated, as well as the lectotypes of Neonympha pompilia, N. thelete Snellen, 1887, Euptychia usitata Butler,
1867, E. pieria Butler, 1867, E. erigone f. proba Weymer, 1911 and E. eous. The results conrm that is possible to distinguish most of the
species of Cissia based on both morphological and molecular data, althougth C. rubricata shows some differences in the male genitalia
compared to its sibling species.
Key words. Euptychiina, Megisto, molecular phylogeny, morphology, Paryphthimoides, seasonal polyphenism, taxonomy, Yphthimoides.
1. Introduction
Euptychiina is a subtribe of the diverse buttery subfam-
ily Satyrinae, which has been the focus of signicant
research in the last couple of decades, from both phy-
logenetic and biogeographic perspectives (Murray &
Prowel 2005; Peña et al. 2006, 2010; Marín et al. 2017)
to descriptions of new genera and species (e.g. BarBosa
et al. 2015, 2016; BenMesBah 2015; Cong & grishin
2014; Costa et al. 2016; Fratello et al. 2015; Freitas
2003; Freitas & Peña 2006; Freitas et al. 2013, 2015,
2016a; huertas et al. 2016; nakahara et al. 2015a,b,
2016a,b, 2017; neild et al. 2014, 2015; seraPhiM et al.
2013; siewert et al. 2013; ZaCCa et al. 2013, 2017). A
broader collaborative effort to revise the systematics of
the subtribe has been underway since 2013, involving
some 30 researchers from around the world, and result-
ing in approximately 40 papers published on this subtribe
(see details in http://www.mnh.u.edu/museum-voices/
euptychiina/).
One of the oldest genera in the subtribe, Cissia Dou-
bleday, 1848, has been shown to be polyphyletic in both
Z et al.: Systematics of butterfly genus Cissia
350
molecular and morphological phylogenies (Murray &
Prowell 2005; Peña et al. 2006; Marín et al. 2017).
Prior to the present study, Cissia comprised 17 species
restricted to the Neotropical region (laMas 2004; Brévi-
gnon 2005; BenMesBah 2015): C. cleophes (Godman &
Salvin, 1889), C. confusa (Staudinger, 1887), C. joyceae
Singer, DeVries & Ehrlich, 1983, C. labe (Butler, 1870),
C. lesbia (Staudinger, [1886]), C. moneta (Weymer,
1911), C. myncea (Cramer, 1780), C. palladia (Butler,
1867), C. penelope (Fabricius, 1775) (and its synonym
Papilio clarissa Fabricius, 1780, the type species of
the genus), C. pompilia (C. Felder & R. Felder, 1867),
C. proba (Weymer, 1911), C. pseudoconfusa Singer,
DeVries & Ehrlich, 1983, C. similis (Butler, 1867),
C. terrestris (Butler, 1867), C. themis (Butler, 1867),
C. maripa Brévignon, 2005 and C. touloulou Benmes-
bah, 2015. The yellowish patch in the submarginal re-
gion of the ventral forewing surface is a character that
has presumably been widely used to group these species
within Cissia, although there is variation in size, intensity
and position of the patch among the species within the
genus. Nevertheless, a number of other Euptychiina spe-
cies show a similar patch, such as Inbio hilara (C. Felder
& R. Felder, 1867), Euptychia neblina Warren & Naka-
hara, 2015, Magneuptychia agnata (Schaus, 1913) and
Magneuptychia drymo (Schaus, 1913). In museum col-
lections it is not unusual to nd specimens of these gen-
era with each other, reecting the current confusion sur-
rounding their taxonomy.
Given the polyphyly of Cissia in existing phylo genies
and the appearance of what was thought to be a diagnostic
character in other genera, the limits of the genus clearly
need revision. Furthermore, the taxonomy of Cissia spe-
cies remains poorly understood and several species are
phenotypically similar to other euptychiine butteries.
The present study provides a taxonomic revision of the
genus based on an integrative approach using molecular
and morphological data.
2. Material and methods
We examined over 3500 specimens, including the types,
from the following collections (acronyms as used in the
text): AN – Andrew Neild collection, London, United
Kingdom; BM – Booth Museum, Brighton, United King-
dom; CMNH – Carnegie Museum of Natural History,
Pittsburgh, Pennsylvania, United States; DD – Diego R.
Dolibaina collection, Paraná, Brazil; DZUP – Coleção
Entomológica Pe. Jesus de Santiago Moure, Universidade
Federal do Paraná, Paraná, Brazil; FD – Fernando M.S.
Dias collection, Paraná, Brazil; IML – Instituto Miguel
Lillo, Tucumán, Argentina; IOC – Instituto Oswaldo
Cruz, Rio de Janeiro, Brazil; MB – Mohamed Benmesbah
collection, Toulouse, France; MNHN – Muséum national
d’Histoire naturelle, Paris, France; MTD – Senckenberg
Museum für Tierkunde, Dresden, Germany; MZUJ –
Muzeum Zoologiczne Uniwersytetu Jagiellonskiego,
Krakow, Poland; NHMUK – Natural History Museum,
London, United Kingdom; RA – Ralf H. Anken collec-
tion, Germany; RMNH – Rijksmuseum voor Natuurli-
jke Historie, Leiden, Netherlands; USNM – Smithsonian
National Museum of Natural History, Washington, D.C.,
United States; ZMHU – Museum für Naturkunde der
Humboldt-Universität, Berlin, Germany; ZMUC– Natu-
ral History Museum of Denmark, Copenhagen, Denmark;
ZSM – Zoologische Staatssammlung München, Munich,
Germany; ZUEC – Museu de Zoologia da Universidade
Estadual de Campinas, São Paulo, Brazil.
Photographs of Neotropical buttery type specimens
taken by Gerardo Lamas and available in warren et
al. (2017) were consulted, especially for those relevant
names and recognized species of Cissia.
Nomenclature used herein follows laMas (2004) and
subsequent works (Brévigon 2005; BenMesBah 2015).
In the present study, we opted to refer as “Cissia” those
species herein removed from the genus, but that will be
transferred to undescribed genera in upcoming papers
(Zacca et al. in prep.). The following abbreviations are
used throughout the text: FW – forewing; HW – hind-
wing; DW – dorsal wings; VW – ventral wings; DFW –
dorsal forewing; VFW – ventral forewing; DHW – dor-
sal hindwing; VHW – ventral hindwing; HT – holotype;
AT – allotype. In the section “Type material”, the labels
are separated from one another by transverse bars.
We attempted to review all publications including
members of Cissia, although given the broad distribution
and abundance of several species, some publications will
inevitably have been missed. This is particularly true for
the North American literature relating to Cissia rubri-
cata, since that species has already been the subject of a
modern taxonomic revision (see Miller 1976).
Distribution maps were produced using the free soft-
ware QGIS (Qgis develoPMent teaM 2016). Geograph-
ical data were obtained from label data in collections and
the literature, including available information on host
plants and immature stages.
2.1. Morphological study
Male and female specimens studied had their abdomen
detached and soaked in a heated test tube with 10% po-
tassium hydroxide solution (KOH) for about ve min-
utes to facilitate the dissection of the genitalia. Dissected
specimens are marked with an asterisk after the voucher
number in the “Examined material” section. Images of
genitalia were obtained in Leica LAS 3D view and LAS
montage version 4.7 with the aid of a video camera Leica
DFC 500 attached to a stereoscopic microscope Leica
MZ16. Illustrations were prepared with the aid of a cam-
era lucida attached to a stereoscopic microscope and sub-
sequently vectorised by using the software GIMP version
2.8.10 (giMP teaM 2016).
Male and female genitalia terminology follow mostly
klots (1970), but the term “gnathos” is applied sensu
351
ARTHROPOD SYSTEMATICS & PHYLOGENY — 76
(2) 2018
Table 1. Species of Euptychiina with sampling site data, code, and GenBank accession numbers from specimens used for phylogenetic
analysis.
Taxa Locality Code COI GAPDH RPS5
Cissia eous Brazil, São Paulo, Jundiaí, Serra do Japi BLU573 MG209743 — —
Cissia eous Brazil, Bahia, Reserva de Una BLU667 MG209748 — —
Cissia eous Brazil, São Paulo, Picinguaba, Casa da Farinha BLU658 MG209744 — —
Cissia eous Brazil, Bahia, Vitória da Conquista BLU664 MG209747 — —
Cissia eous Brazil, São Paulo, Cebimar, São Sebastião BLU618 KU340893 — —
Cissia eous Brazil, Bahia, Reserva de Una BLU660 MG209745 — —
Cissia eous Brazil, Minas Gerais, Serra do Cipoó, Santana do Riacho BLU621 KU340896 — —
Cissia eous Brazil, São Paulo, Campinas, Unicamp, Mata da Zoologia YPH0104 KU340856 KU340901 KU340934
Cissia eous Brazil, Bahia, Reserva de Una BLU661 MG209746 — —
Cissia eous Brazil, Paraná, Foz do Iguaçu BLU619 KU340894 — —
Cissia eous Brazil, Paraná, Foz do Iguaçu BLU620 KU340895 — —
Cissia eous Brazil, Rio Grande do Sul, Alegrete YPH0422 KU340872 KU340920 KU340955
Cissia phronius Brazil, São Paulo, Ribeirão Grande, Trilha do Capinzal BLU378 KU340890 — —
Cissia phronius Brazil, São Paulo, Ribeirão Grande, Trilha do Capinzal BLU380 KU340892 — —
Cissia phronius Brazil, São Paulo, Atibaia NW126-7 DQ338807 GU205973 GU206034
Cissia phronius Brazil, São Paulo, Ribeirão Grande, Trilha do Capinzal BLU379 KU340891 — —
Cissia penelope Peru, Junin, La Solitaria-Quebrada Siete Jeringas CP07-58 GU205833 GU205945 GU206005
Cissia penelope Ecuador, Napo DNA99-028 AY508530 — —
Cissia rubricata
cheneyorum
USA, Arizona, Southwestern Research Station, Portal LEP-19315 MG209757 MG546314 MG546327
Cissia proba Ecuador, Zamora-Chinchipe, E of Zumba, km 2.6 El Pite-Río Mayo rd. KW-140622-01 MG209751 MG546309 MG546319
Cissia proba Peru, Madre de Dios, Tambopata Research Center CP01-30 GQ864751 GQ864945 GQ865416
Cissia pompilia Costa Rica, Area de Conservacion Guanacaste, Sector San Cristobal,
Estacion San Gerardo
07-SRNP-100013 JQ573901 — —
Cissia pompilia Mexico, Yucatan, Valladolid, carretera a Xocen MAL-02577 GU659737 — —
Carminda paeon Brazil, São Paulo B-17-41 DQ338801 — —
Carminda paeon Brazil, São Paulo, Ribeirão das Pedras NW126-11 GQ864792 GQ865004 GQ865473
Carminda paeon Brazil, São Paulo, Jundiaí, Serra do Japi BLU324 MG209740 — —
Carminda paeon Brazil, São Paulo, Jundiaí, Serra do Japi BLU325 MG209741 — —
Carminda paeon Brazil, São Paulo, Jundiaí, Serra do Japi BLU326 MG209742 — —
Carminda paeon Brazil, Paraná, Foz do Iguaçu, Trilha Poço Preto YPH0357 MG209761 MG546318 MG546323
Carminda umuarama Brazil, Minas Gerais, Pq. Itatiaia, Itamonte YPH0437 KU340873 KU340921 KU340956
Carminda umuarama Brazil, Espírito Santo, Caparaoó YPH0459 KU340874 KU340922 KU340957
“Cissia” labe
(= sp Janzen13)
Costa Rica, Area de Conservacion Guanacaste, Sector Pitilla, Sendero
Nacho
11-SRNP-30733 JQ526864 — —
“Cissia” labe Ecuador, Carchi, Lita, ridge east of Río Baboso KW-140721-04 MG209753 MG546311 MG546325
“Cissia” palladia Brazil, São Paulo, Campinas, Unicamp MGCL-LOAN-191 MG209759 MG546316 MG546328
Carminda griseldis Brazil, Mato Grosso, Extrema NW127-17 GU205853 GU205965 GU206025
Carminda griseldis Brazil, São Paulo, Alto do Capivari, Campos do Jordão YPH0394 KU340869 KU340917 KU340952
Carminda griseldis Brazil, Espírito Santo, Caparaoó YPH0462 KU340875 KU340923 KU340958
Yphthimoides pacta Brazil, Mato Grosso, Diamantino MGCL-LOAN-355 MG209760 MG546317 MG546322
Graphita griphe Colombia, Cali, San Antonio YPH0361 KU340866 KU340915 KU340948
Graphita griphe Colombia, Cali, San Antonio YPH0362 KU340867 — KU340949
Stegosatyrus ocelloides Brazil, Minas Gerais, Serra do Cipoó YPH0527 KU340879 — KU340966
Stegosatyrus ocelloides Brazil, Minas Gerais, Serra do Cipoó YPH0543 KU340883 KU340928 KU340970
Stegosatyrus ocelloides Brazil, Minas Gerais, Serra do Cipoó YPH0530 KU340880 KU340925 KU340967
Stegosatyrus periphas Argentina, Buenos Aires Province, Ituzaingó LEP-18718 MG209756 MG546313 MG546326
Megisto cymela USA, Rhode Island, Valley Falls CP21-04 GQ357208 GQ357439 GQ357569
Paleonympha opalina Taiwan, Pingtung County, Hsiaokuehu, Wutai Shiang EW25-21 DQ338880 GQ865010 GQ865479
“Cissia” myncea Peru, Madre de Dios DNA99-009 AY508556 — —
“Cissia” myncea Brazil, São Paulo, Ubatuba, Picinguaba NW108-6 DQ338581 GQ357427 GQ357556
“Cissia” myncea Peru, Madre de Dios, Tambopata Research Center CP01-58 GU205832 GU205944 GU206004
“Cissia” confusa Costa Rica, Area de Conservacion Guanacaste, Sector Pitilla, Sendero
Tierra Blanca
11-SRNP-30020
(DHJ02)
JQ526869 — —
“Cissia” confusa DNA99-082 AY508533 — —
Magneuptychia agnata Ecuador, Esmeraldas, km 42 San Lorenzo-Lita rd., Finca Cypris LEP-15103 MG209755 MG546312 MG546321
Magneuptychia libye Ecuador, Zamora-Chinchipe, km 6 Los Encuentros-El Panguí LEP-14777 MG209754 MF192728 MG546320
“Cissia” similis Costa Rica, Area de Conservacion Guanacaste, Sector Horizontes,
Laguna Bejuco
07-SRNP-14171 JQ538434 — —
Z et al.: Systematics of butterfly genus Cissia
352
PierCe (1909), “fultura superior” and “fultura inferior”
sensu Petersen (1904), “combination of ventral arm of
tegumen and dorsal arm of saccus” sensu austin and
Mielke (2008). The intromittent male organ in butteries
is usually reffered as “aedeagus”, but here we use the term
“phallus”, since Agathiphagidae are the only Lepidoptera
with a true aedeagus (see kristensen 1979, 2003). The
nomenclature of the wing venation mostly follows CoM-
stoCk & needhaM (1898–99) and CoMstoCk (1918), and
for broad regions of the wing we follow neild (1996).
The extra band located at the submarginal region on both
ventral wings between the median and submarginal lines
is called “umbra”, as proposed by sChwanwitsCh (1924),
and followed by ForBes (1941). The ocelli are referred
to in the text as “complete” or “incomplete”; an ocellus
is considered “complete” when it has all elements of the
eyespot (ocellar ring, ocellar spot and pupil), while it is
“incomplete” when any of these elements are missing.
2.2. DNA sampling and analysis
Phylogenetic relationships and genetic distances among
species of Cissia and appropriate outgroups were esti-
mated to verify the monophyly of the redened genus
and assess the status of taxa.
Genomic DNA was extracted from one to two legs
of adults using the DNeasy Blood & Tissue Kit with
standard protocol (QIAGEN, Düsseldorf, Germany) or
the Omniprep kit (G-BioSciences). DNA was stored in
TE buffer at –20°C. We amplied the 658 bp barcode
region of the mitochondrial gene COI as well as the nu-
clear genes GAPDH and RPS5, which have been shown
to be useful in phylogenetic studies (wahlBerg & wheat
2008). Primers and PCR reaction conditions follows
nakahara et al. (2015, 2017) and silva-Brandão et al.
(2005). All sequences were aligned using MAFFT v. 7
(katoh & stanley 2013) with sequences obtained previ-
ously and available on GenBank (see Table 1). The nal
matrix comprised 67 specimens and 2,772 bp. Based on
previous molecular phylogenies (Peña et al. 2006, 2010)
and on our unpublished data from additional euptychiine
species, we chose sixteen species as outgroups, and Eu-
ptychia westwoodi Butler, 1867 to root the phylogenetic
tree.
The data were divided into codon positions, and
substitution models (see Electronic Supplement 2) and
partitioning scheme were inferred using ModelFinder
in IQ-TREE 1.5.4 nguyen et al. 2015). This was fol-
lowed by 250 likelihood searches and 2000 nonpara-
metric bootstrap replicates, also in IQ-TREE. Bayesian
analysis was also performed for the combined data set
under the model jumping (nst-=mixed), using the pro-
gram MrBayes 3.2 (ronQuist et al. 2012) on the CIPRES
Science Gateway (Miller et al. 2010). The matrix was
divided in three partitions associated with the genes. As
analysis of combined data by Bayesian methods permits
partition-specic substitution models and parameters, all
substitution model parameters (gamma shape, character
state frequencies, substitution rates of GTR model) were
allowed to vary across partitions (= genes). Four simul-
taneous chains were run for 10×106 generations for two
runs, sampling trees every 1,000 cycles. The rst 10 per-
cent trees were discarded as xed “burn in”. Consider-
ing the similarities between the results found in ML tree
(Fig. 1) and Bayesian tree (see Electronic Supplement 3),
we choose the ML tree to show and discuss our results.
Genetic distances (see Tables 2, 3) among species
of Cissia were determined by using the Kimura-2-para-
meters substitution model (kiMura 1980) in the program
MEGA v. 6.0 (taMura et al. 2013).
Table 1 continued.
Taxa Locality Code COI GAPDH RPS5
“Cissia” similis DNA97-014 AY508529 — —
Hermeuptychia hermes
(= sp. Janzen04)
Costa Rica, Area de Conservacion Guanacaste, Sector Mundo Nuevo,
Quebrada Tibio Perla
07-SRNP-55888 JQ535699 — —
“Cissia” terrestris Panama, Isla Barro Colorado YB-BCI2873 HM406607 — —
“Cissia” pseudoconfusa Mexico, Quintana Roo, Ejido X-maben: camino a Noh-cancab MAL-02559 HQ990161 — —
“Cissia” pseudoconfusa Panama, Isla Barro Colorado YB-BCI11849 HM416553 — —
Amphidecta calliomma Peru, Madre de Dios, Los Amigos Biological Station LEP-19579 MG209758 MG546315 MG546329
Atlanteuptychia
ernestina
Brazil, São Paulo, Jundiaí, Serra do Japi EE002 MG209750 MG546308 —
Atlanteuptychia
ernestina
Brazil, São Paulo, Serra do Japi YPH0191 KP994863 KU340904 KU340937
Atlanteuptychia
ernestina
Brazil, São Paulo, Jundiaí, Serra do Japi EE001 MG209749 MG546307 —
Paramacera xicaque Brazil, Distrito Federal, Magdalena Contreras, Cañada de los Dinamos CP15-08 GQ357210 GQ357442 GQ357571
Cyllopsis pertepida Mexico, Guanajuato. Mpio. San Felipe/Leon 8 km NE El Zuaco NW165-3 GQ357204 GQ357428 GQ357557
Euptychia westwoodi Ecuador, Esmeraldas, km 17 San Lorenzo-Ibarra rd., San Francisco ridge KW-140718-03 MG209752 MG546310 MG546324
Table 2. Mean genetic distances among the species of Cissia.
12345
1 Cissia rubricata
2 Cissia proba 13.4
3 Cissia pompilia 11.7 7.0
4 Cissia penelope 13.6 14.8 15.5
5 Cissia phronius 12.0 11.4 13.0 10.3
6 Cissia eous 10.3 9.3 8.0 11.0 6.4
353
ARTHROPOD SYSTEMATICS & PHYLOGENY — 76
(2) 2018
3. Results
3.1. Molecular phylogeny and genetic
distances
Maximum Likelihood (ML) analysis indicates that C. pe-
nelope (whose synonym Papilio clarissa is the type spe-
cies for the genus) forms a clade with two species pre-
viously placed in the genus Paryphthimoides (C. eous
comb.n. and C. phronius comb.n.), which were sister to
one another (Fig. 1), with all of these relationships strong-
ly supported (bootstrap support [bs] = 100). Although
some differences in the male genitalia are observed (see
discussion in “Taxonomy” section), C. rubricata (former-
ly placed in Megisto) is placed as sister to C. penelope +
(C. eous + C. phronius), also with high support (bs = 98).
This clade is sister (bs = 89) to one containing the sister
species C. pompilia and C. proba (bs = 100) (Fig. 1).
Ten of the remaining 13 species formely placed in
Cissia (laMas 2004; Brévigon 2005; BenMesBah 2015)
are scattered more distantly across the Euptychiina phy-
logeny (see Fig. 1 – collapsed clades labelled as “Taxa re-
moved from Cissia” and “Magneuptychia + taxa removed
from Cissia”), including “Cissia” confusa (Staudinger,
1887), “C.” labe (Butler, 1870), “C.” lesbia (Stauding-
er, [1886]), “C.” myncea (Cramer, 1780), “C.” palladia
(Butler, 1867), “C.” pseudoconfusa Singer, DeVries &
Ehrlich, 1983, “C.” similis (Butler, 1867), “C.” terrestris
(Butler, 1867), “C.” themis (Butler, 1867) and “C.” mari-
pa Brévignon, 2005. Three former Cissia species, “C.”
cleophes (Godman & Salvin, 1889), “C.” joyceae Singer,
DeVries & Ehrlich, 1983 and “C.” touloulou Benmesbah,
2015 have yet to be included in our molecular dataset (M.
Espeland unpubl. data), although genitalic morphology is
clearly distinct from all members of the redened Cissia.
Interspecic genetic distances among the six species
that form a clade with C. penelope range from 6.4% to
15.5% (Table 2). Historically, C. eous and C. phronius
have been confused with each other in several collec-
tions, but their genetic distances range from 6.0% to
6.6% (Table 3) supporting their status as distinct species
(in addition to the morphological evidence discussed un-
der Taxonomy section). Conversely, intraspecic genetic
distances are highest among the individuals of C. pe-
nelope (3.5%), intermediate in individuals of C. eous
(0.2%–1.7%) and lowest (0 – 0.2%) among the individu-
als of C. phronius (Table 3).
3.2. Taxonomy
Cissia Doubleday, 1848
Cissia Doubleday, 1848: 33; type-species Papilio clarissa Cram-
er, 1775, by monotypy; a synonym of Papilio penelope Fab-
ricius, 1775. – heMMing 1967: 116. – Miller 1968: 92; syn.
Argyreuptychia. – singer et al. 1983: 101. – laMas 2004: 218;
syn.: Vareuptychia. – Peña et al. 2006: 31.
Argyreuptychia Forster, 1964: 123; type-species Papilio penelope
Fabricius, 1775, by original designation.
Diagnosis. Species of Cissia are characterized by the fol-
lowing set of characters: (1) glabrous eyes, (2) bipupil-
lated ocellus in Cu1-Cu2 in DHW, (3) silvery ocelli in M2-
M3 and M3-Cu1 in VHW, (4) submarginal and marginal
lines crenulated in VFW and VHW, (5) uncus arched
downwards (Fig. 4A), (6) gnathos hook-like and short
(except in C. rubricata that is sinuous and developed), (7)
Table 3. Pairwise genetic distances among the species of Cissia.
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
1 Cissia rubricata LEP19315
2 Cissia proba CP01-30 13.4
3 Cissia pompilia 07-SRNP-100013 11.1 6.3
4 Cissia pompilia MAL-02577 12.3 7.7 1.2
5 Cissia penelope DNA99-028 12.9 14.9 14.9 15.8
6 Cissia penelope CP07-58 14.4 14.6 15.2 16.1 3.5
7 Cissia phronius NW126-7 12.0 11.4 12.3 13.8 10.1 10.6
8 Cissia phronius BLU378 12.0 11.4 12.3 13.8 10.1 10.6 0.0
9 Cissia phronius BLU379 12.0 11.4 12.3 13.8 10.1 10.6 0.0 0.0
10 Cissia phronius BLU380 12.0 11.4 12.3 13.8 10.1 10.6 0.0 0.0 0.0
11 Cissia eous YPH-0422 10.3 9.8 7.3 8.7 11.4 11.2 6.9 6.9 6.9 6.9
12 Cissia eous BLU619 10.3 9.8 7.3 8.7 11.1 10.9 6.6 6.6 6.6 6.6 0.2
13 Cissia eous BLU620 10.3 9.8 7.3 8.7 11.1 10.9 6.6 6.6 6.6 6.6 0.2 0.0
14 Cissia eous BLU573 10.3 9.2 7.3 8.7 11.1 10.9 6.3 6.3 6.3 6.3 1.5 1.7 1.7
15 Cissia eous BLU618 10.3 9.2 7.3 8.7 11.1 10.9 6.3 6.3 6.3 6.3 1.5 1.7 1.7 0.0
16 Cissia eous BLU621 10.3 9.2 7.3 8.7 11.1 10.9 6.3 6.3 6.3 6.3 1.5 1.7 1.7 0.0 0.0
17 Cissia eous BLU658 10.3 9.2 7.3 8.7 11.1 10.9 6.3 6.3 6.3 6.3 1.5 1.7 1.7 0.0 0.0 0.0
18 Cissia eous BLU660 10.3 9.2 7.3 8.7 11.1 10.9 6.3 6.3 6.3 6.3 1.5 1.7 1.7 0.0 0.0 0.0 0.0
19 Cissia eous BLU661 10.0 8.9 7.6 8.9 10.9 10.6 6.0 6.0 6.0 6.0 1.7 2.0 2.0 0.2 0.2 0.2 0.2 0.2
20 Cissia eous BLU664 10.3 9.2 7.3 8.7 11.1 10.9 6.3 6.3 6.3 6.3 1.5 1.7 1.7 0.0 0.0 0.0 0.0 0.0 0.2
21 Cissia eous BLU667 10.3 9.2 7.3 8.7 11.1 10.9 6.3 6.3 6.3 6.3 1.5 1.7 1.7 0.0 0.0 0.0 0.0 0.0 0.2 0.0
22 Cissia eous YPH-0104 10.3 9.2 7.3 8.7 11.1 10.9 6.3 6.3 6.3 6.3 1.5 1.7 1.7 0.0 0.0 0.0 0.0 0.0 0.2 0.0 0.0
Z et al.: Systematics of butterfly genus Cissia
354
phallus with anterior region bottle-shaped and posterior
region with apex dorsally bid (Fig. 4D,E), (8) absence
of vesical cornuti in phallus, (9) lamella antevaginalis lat-
erally expanded and orbicular or obovate in ventral view
(Fig. 5A,B), (10) ductus bursae membranous and paired
signa at corpus bursae.
History of classication. Cissia Doubleday, 1848 was
described without any diagnosis, including only its type
species Cissia clarissa (Cramer, 1782). Papilio crantor
Fabricius, 1791 was included doubtfully in Cissia by
Doubleday, being ineligible to be the type species of the
genus under Article 67(h) of the ICZN. laMas (2004)
treated this species as a junior synonym of “C.” myncea
(Cramer, 1780). godart ([1824]) considered Papilio cla-
rissa as a junior synonym of Papilio penelope Fabricius,
1775, which was also followed by sCudder (1875).
dyar ([1903]) treated in Cissia the Neartic species
Papilio cymela Cramer, 1777 (replacement name for P.
eurytus Fabricius, 1775), Neonympha rubricata, N. mitch-
elli French, 1889 and P. sosybius Fabricius, 1793; the
rst two species were placed by laMas (2004) in Megisto
Hübner, [1819], and the last in Hermeuptychia Forster,
1964. Barnes & lindsey (1922) suggested that the name
Megisto should replace Cissia, based on the sCudder’s
(1875) inclusion of P. penelope Fabricius, 1775 and P.
eurytus Fabricius, 1775, the type species of Megisto, in
Cissia. However, molecular data show that the type of
Megisto is not closely related to true Cissia species (Peña
et al. 2006, 2010), as redened in the present study.
The rst systematic arrangement to include some
species of Cissia was proposed by Butler (1867a), who
placed them in “Division 1” of Euptychia Hübner, 1818
characterized by “Alae supra fuscae, rarissime albo
violaceove variae; posticae plerumque ocello subanali
distincto: subtus pallidiores, ocellis forma regularibus,
plerumque distinctis, lineis duabus medii, interna anti-
carum raro obsoleta”. In this category, Butler included
Papilio myncea Cramer, 1780, Euptychia palladia But-
ler, 1867, Euptychia terrestris Butler, 1867, Euptychia
themis Butler, 1867, Euptychia similis Butler, 1867,
Papilio clarissa Cramer, 1780, Euptychia usitata Butler,
1867 and Euptychia pieria Butler, 1867. laMas (2004)
followed Godart ([1824]) and sCudder (1875) in treat-
ing P. clarissa as a junior synonym of C. penelope, while
E. usitata and E. pieria were placed as synonyms of
C. pompilia (C. Felder & R. Felder, 1867).
In his “Catalogue of Diurnal Lepidoptera of the
family Satyridae”, Butler (1868) erected the “Section
Fig. 1. Phylogeny of the genus Cissia based on the Maximum Likelihood analysis of combined COI, GAPDH and RpS5 gene sequences.
Bootstrap values < 75 not shown.
355
ARTHROPOD SYSTEMATICS & PHYLOGENY — 76
(2) 2018
Megisto”, a category without diagnostic characters, and
included 102 species, 10 of which were treated by laMas
(2004) in Cissia, including E. clarissa, E. crantor (Fab-
ricius, 1793), E. myncea, E. palladia, E. pieria, E. pom-
pilia, E. similis, E. terrestris, E. themis and E. usitata.
Butler (1877) proposed the “Euptychia ocypete species
group” to contain 31 species that he considered allied to
each other by their wing phenotypes. Among them, eight
Fig. 2. Species of Cissia. A – D: C. penelope: A – Male, dorsal; B – Male, ventral; C – Female, dorsal; D – Female, ventral. E – H:
C. pompilia: E – Male, dorsal; F – Male, ventral; G – Female, dorsal; H – Female, ventral. I – L: C. proba: I – Male, dorsal; J – Male,
ventral; K – Female, dorsal; L – Female, ventral. M – P: C. eous: M – Male, dorsal; N – Male, ventral; O – Female, dorsal; P – Female,
ventral. Q – T: C. phronius: Q – Neotype male, dorsal; R – Neotype male, ventral; S – Female, dorsal; T – Female, ventral. U – X: C. ru-
bricata rubricata: U – Male, dorsal; V – Male, ventral; W – Female, dorsal; X – Female, ventral. — Arrows indicate diagnostic characters
of the wing patterns to the species (see text). Scale = 1 cm.
Z et al.: Systematics of butterfly genus Cissia
356
species placed in Cissia by laMas (2004), were includ-
ed: E. labe Butler, 1870, E. myncea, E. palladia, E. ter-
restris, E. penelope, E. themis, E. usitata, E. undina But-
ler, 1870.
Mostly based on slight characters of the wing colora-
tion and venation, godMan & salvin (1879 – 1901) di-
vided the genus Euptychia in eight groups, named from
“a” to “h”. “Group d” was characterized by the “wings
of male opaque brown, of female paler, the markings of
the underside sometimes showing faintly above; upper
discocellular of primaries very short, directed outwards,
middle discocellular strongly convex” (p. 78) and com-
prised by 17 species, including E. labe, E. pieria, E. ter-
restris and E. similis; of which the rst three former were
allocated in “subgroup a”, dened by the “rst subcostal
branch emitted before the end, the second at the end of
the cell” (p. 78), while E. similis belonged to “subgroup
b”, characterized by the “rst subcostal branch of prima-
ries emitted before the end of the cell, the second beyond
it” (p. 81).
In his introduction to the genus Euptychia, weyMer
(1911) explained his decision to treat within that genus
all of the species that other authors had placed in Cissia
and Neonympha: “The American authors place the seven
species occurring there in the genera Neonympha Hübner
and Cissia Doubleday. But as these species have exactly
similar allies in Mexico and in tropical Central and South
America, I follow Butler and Godman & Salvin in re-
ferring them all to Euptychia”. Still in this same work,
Weymer proposed the “ocypete group” comprising 36
species, some of them not cited in Butler (1877), with-
out any explanation. However, Weymer treated all of
the Cissia species previously cited by Butler, and made
some recommendations about their taxonomic status, as
follows: 1) E. pieria, E. pompilia and E. thelete (Snellen,
1887) were treated as forms of E. usitata, 2) E. themis
and E. undina as forms of E. similis, and 3) E. pytheus
Möschler, 1883 as a form of E. penelope.
Forster (1964) described the genera Argyreuptychia
and Vareuptychia to a number of species placed by laMas
(2004) in Cissia. The genus Argyreuptychia comprised 10
species, of which seven were placed in Cissia by laMas
(2004) (A. penelope, A. proba, A. labe, A. palladia, A. py-
theus, A. moneta Weymer, 1911 and A. lesbia Staudinger,
[1886]), and stated that the genus was characterized by
its “small size when compared to Megeuptychia Forster,
1964 and Magneuptychia Forster, 1964, silvery eyespots
in M2-M3 and M3-Cu1 on ventral hindwings, slender un-
cus, and short and narrow aedeagus [= phallus]” (For-
ster 1964: 123). In contrast, Vare uptychia, containing
V. similis and V. usitata, was erected based on “differ-
ences in the male genitalia structures when compared to
the closely related genus Argyreuptychia and the com-
pletely different pattern and coloration of the wing un-
derside, with straighter bands” (Forster 1964: 125).
Although Forster (1964) did not provide a detailed
description of the male genitalia, when comparing his il-
lustrations of V. similis and V. usitata (p. 125, gs. 145,
146), the only character that is shared by both species is
the presence of cornutal patches on the phallus. The dif-
ferences in wing pattern mentioned by Forster are likely
the median and/or submedian line(s) on the underside of
the wings, which are straighter in the species he placed in
Vareuptychia. It is known (Freitas 2004; Peña & laMas
2005; BarBosa et al. 2015) that the limits of most of the
genera proposed by Forster are very wide and based on
vaguely dened features that also can be found in other
Euptychiina genera, with no clear distinguishing dia-
gnostic characters.
However, two important points must be considered
here: 1) by studying only Bolivian specimens, Forster ig-
nored the existence of Cissia Doubleday, 1848, a genus
with the same type species that he had chosen for Ar-
gyreuptychia, and 2) the close relationship between Ar-
gyreuptychia and Vareuptychia. The rst point was noted
by Miller (1968) who placed Argyreuptychia as an ob-
jective synonym of Cissia, later followed by singer et
al. (1983) and laMas (2004). When describing the diag-
nostic characters of Euptychiini (= Euptychiina), Miller
(1968) stated that Cissia species are characterized by
having a spiny midtibia, while in the remaining genera of
the tribe the spines are slight or lacking (p. 91).
singer et al. (1983) provided the rst taxonomic re-
view of Cissia and proposed the most recent systematic
arrangement of this genus. Considering only species from
Costa Rica and Trinidad, the authors concluded that Cis-
sia species do not show clear characters in wings pattern
and male genitalia that enable them to be distinguished
from other genera (singer et al. 1983: 106). In that study,
Cissia was mainly dened based on morphological fea-
tures of immatures, which led the authors to subdivided
the genus into four subgroups: 1) “labe subgroup” – com-
prising C. labe, C. palladia and C. penelope; 2) “confusa
subgroup” – C. myncea, C. confusa and C. pseudocon-
fusa; 3) “gomezi subgroup” – only C. gomezi Singer,
Fig. 3. Wing venation of Cissia penelope. A – Male; B – Female.
— Abbreviations: Sc – subcostal vein; R – radial vein; Rs – sector
radial vein; M – median vein; Cu – cubital vein; A – anal vein. —
Scale = 1 cm.
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ARTHROPOD SYSTEMATICS & PHYLOGENY — 76
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DeVries & Ehrlich, 1983; and 4) “subgroup incertis” –
C. drymo Schaus, 1913, C. agnata Schaus, 1913 and
C. joyceae Singer, DeVries & Ehrlich, 1983. However,
even after this study, some authors opted to treat Cissia
as a catch-all genus (see devries 1987) including a num-
ber of what we now know to be unrelated.
d’aBrera (1988) placed most species of Euptychiina
in the genus Euptychia, including some species placed
in Cissia by laMas (2004), such as: E. cleophes, E. pal-
ladia, E. labe, E. confusa, E. myncea, E. terrestris,
E. lesbia, E. penelope, E. usitata and E. similis. laMas
(2004) followed Miller’s (1968) and singer et al.’s
(1983) concept of Cissia, but also included eight more
species: C. cleophes, C. lesbia, C. moneta, C. pompilia,
C. proba, C. similis, C. terrestris and C. themis. In addi-
tion, laMas (2004) transferred C. agnata, C. drymo and
C. gomezi to Magneuptychia Forster, 1964, and treated
Cissia ucumariensis Andrade, 1991 as a junior synonym
of Euptychoides griphe (C. Felder & R. Felder, 1867) (=
Graphita griphe). This classication of laMas (2004) is
the one currently used, with Cissia comprising 15 spe-
cies. Two Amazonian species from French Guiana were
Fig. 4. Male genitalia of species of Cissia. A: C. penelope (from left to right): lateral, dorsal, ventral, phallus lateral, phallus dorsal.
B: C. pompilia: lateral, dorsal, ventral, phallus lateral, phallus dorsal. C: C. proba: lateral, dorsal, ventral, phallus lateral, phallus dorsal.
D: C. eous: lateral, dorsal, ventral, phallus lateral, phallus dorsal. E: C. phronius: lateral, dorsal, ventral, phallus lateral, phallus dorsal.
F: C. rubricata: lateral, dorsal, ventral, phallus lateral, phallus dorsal. — Abbreviations: t – tegumen; u – uncus; g – gnathos; aa – appendix
angularis; s – saccus; v – valvae. — Arrows indicate diagnostic characters to the genus (see text).
Z et al.: Systematics of butterfly genus Cissia
358
described in Cissia after Lamas’ publication, namely
C. maripa Brévignon, 2005 and C. touloulou Benmes-
bah, 2015, and no formal taxonomic alteration has been
made until the present paper.
Taxonomy. The genus Cissia is redened here to include
six species: C. penelope, C. pompilia, C. proba, C. eous
comb.n., C. phronius comb.n. and C. rubricata comb.n..
Based on molecular data, the genus is a member of the
‘Megisto clade’ as dened by Peña et al. (2010), whereas
morphological data failed to recover Cissia within this
clade, but placed it as a nearby branch (Marín et al.
2017). The Megisto clade contains genera which are
typically most diverse in more temperate regions of the
Americas, and our data suggest that the genus is sister
to a clade comprising the genera Carminda, Graphita,
Stegosatyrus, Megisto, Paleonympha and several former
Cissia species which will need to be placed into other
genera. In addition to our molecular results, several mor-
phological features support the new taxonomic arrange-
ment of Cissia, including the the absence of setae on the
eyes, wing pattern characters and venation, as well as
the genitalia morphology. singer et al. (1983) stated that
the wings and male genitalia did not provide clear char-
acters to delimit Cissia, but the genus as redened here
does show a consilience of such characters that facili-
tate its recognition. Genitalic morphology remains one
of the most useful tools in the delimitation of genera and
species of Euptychiina (e.g.: siewert 2013; ZaCCa et al.
2013, 2014, 2016; Freitas et al. 2015, 2016a; nahakara
et al. 2015), in combination with molecular data that sup-
port systematic evolutionary hypotheses.
The remaining species previously treated in Cissia
(laMas 2004; Brévigon 2005; BenMesBah 2015) include:
“C.” confusa, “C.” labe, “C.” lesbia, “C.” myncea, “C.”
pal ladia, “C.” pseudoconfusa, “C.” similis, “C.” terres-
tris, “C.” themis, “C.” maripa, “C.” cleophes, “C.” joyce-
ae, and “C.” touloulou. Although the last three of these
species have no DNA sequence data are yet available,
we are condent (based on morphological evidence) that
these are not closely related to the six species we treat
Fig. 5. Female genitalia of species of Cissia. A: C. penelope: lateral (above), ventral (below). B: C. pompilia: lateral (above), ventral (be-
low). C: C. proba: lateral (above), ventral (below). D: C. eous: lateral (above), ventral (below). E: C. phronius: lateral (left), ventral (right).
F: C. rubricata: ventral. — Abbreviations: t8 – 8th tergum; pa – papilla analis; la – lamellae antevaginalis; db – ductus bursae; cb – corpus
bursae; sg – signa. — Arrows indicate diagnostic characters to the genus (see text).
359
ARTHROPOD SYSTEMATICS & PHYLOGENY — 76
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here in our redened concept of Cissia. Some of them
will shortly be moved into a redened Paryphthimoides
Forster, 1964 (Zacca et al. in prep.), while the most ap-
propriate generic classication for the remainder is under
study, with new genera being needed to accommodate at
least some species (Zacca et al. in prep.). Since the ICZN
requires that valid species names be binomens, we leave
these species for the moment as “Cissia” until they can
be moved into suitable genera, with the understanding
that our use of the generic name Cissia throughout the re-
mainder of the paper refers to the six species that will ul-
timately remain within the genus as newly dened here.
Synonymic checklist of Cissia species
(- indicates a synonym)
Cissia Doubleday, 1848
Argyreuptychia Forster, 1964
Cissia penelope (Fabricius, 1775)
- Papilio clarissa Cramer, 1782
- Euptychia moneta Weymer, 1911 syn.n.
Cissia pompilia (C. Felder & R. Felder, 1867)
- Euptychia usitata Butler, 1867
- Euptychia usitata pieria Butler, 1867
- Euptychia austera Butler, 1867 syn.n.
- Euptychia usitata pompilia C. Felder & R. Felder, 1867
- Neonympha thelete Snellen, 1887
- Euptychia usitata thelete Weymer, 1911
Cissia proba (Weymer, 1911)
Cissia eous (Butler, 1867) comb.n.
- Paryphthimoides bahneri Anken, 1994 syn.n.
- Paryphthimoides kiliani Anken, 1999 syn.n.
Cissia phronius (Godart, [1824]) comb.n.
Cissia rubricata (W.H. Edwards, 1871) comb.n.
Cissia rubricata rubricata (W.H. Edwards, 1871) comb.n.
Cissia rubricata smithorum (Wind, 1946) comb.n.
Cissia rubricata cheneyorum (R. Chermock, 1949) comb.n.
Cissia rubricata anabelae (L. Miller, 1976) comb.n.
Cissia rubricata pseudocleophes (L. Miller, 1976) comb.n.
Key to species of Cissia
1 DFW and DHW with orange patches ........................
......................................... C. rubricata (Fig. 2U – X)
1’ DFW and DHW totally brown ............................... 2
2 VW with well-marked dark brown scattered dots at
the submarginal region (Fig. 2A); VHW with one
developed incomplete silvery ocellus in Rs-M1 (Fig.
2B) ................................... C. penelope (Fig. 2A – D)
2’ VW without dark brown scattered dots (or, if present,
just a few and faded); VHW with one complete sil-
very ocellus in Rs-M1 (or, if incomplete, is always
small) ...................................................................... 3
3 VW with submedian and median lines straight ...... 4
3’ VW with submedian and median lines crenulated … 5
4 VW without umbra (or, if present it is almost the
same colour as the ground colour); VW with a nar-
row median line ................ C. pompilia (Fig. 2E – H)
4’ VW with umbra darker than the ground colour; VW
with a wide median line (approximately 1 mm) .......
................................................. C. proba (Fig. 2I – L)
5 DHW with developed and well-marked ocellus at
Cu1-Cu2 (Fig. 2M); VHW with outer margin crenu-
lated along its entire length; VHW with developed
ocelli at M1-M2 and Cu1-Cu2 (in general, with a well-
marked ochre ocellar ring) ..... C. eous (Fig. 2M – P)
5’ DHW with reduced or absent ocellus at Cu1-Cu2;
VHW with outer margin slightly crenulated and pro-
nounced at Cu1; VHW with reduced ocelli (in gen-
eral, noticed only by the silvery pupils and the pale
ocellar ring) ..................... C. phronius (Fig. 2Q – T)
Cissia penelope (Fabricius, 1775)
(Figs. 2A – D, 3A,B, 4A – E, 5A,B, 8)
Papilio penelope Fabricius, 1775: 493; syntype: America. – FaB-
riCius 1793: 96. – singer et al. 1983: 110, g. 4D; neotype:
America (photograph examined); ZMUC. – Miller 1968: 93.
– ZiMsen 1964: 515.
Papilio clarissa Cramer, 1782: pl. 293, gs. D, E; syntype: Suri-
name. – singer et al. 1983: 110; neotype: Suriname; NHMUK
(examined); syn. P. penelope. – Miller 1968: 92. – laMas
2004: 218.
Euptychia clarissa; hüBner [1819]: 54. – westwood 1851 in dou-
Bleday: 373. – Butler 1867a: 462. – Butler 1868: 16.
Satyrus penelope; godart [1823]: 489.
Cissia clarissa; douBleday 1848: 33.
Neonympha clarissa; herriCh-sChäFFer 1864: 59.
Euptychia penelope; kirBy 1871: 48. – MösChler 1877: 323. –
Butler 1877: 118. – kirBy 1879: 134. – sharPe 1890: 568.
– kaye 1904: 179. – weyMer 1911: 200, pl. 47b. – aurivil-
lius 1929: 158. – gaede 1931: 459. – BarCant 1970: 143,
161, pl. 13, g. 10 (male). – wesley & eMMel 1975: 24, 30.
– d’aBrera 1988: 772 (male). – eMMel & austin 1990: 10. –
vargas-ZaPata et al. 2011: 51.
Argyreuptychia penelope; Forster 1964: 123. – lewis 1973: pl. 54,
g. 2.
Cissia penelope; Miller 1968: 123. – singer et al. 1983: 110. –
aCkery 1988: 114, table 9. – Mielke & Casagrande 1992: 181.
– singer & ehrliCh 1993: 252. – laMas 1994a: 165. – Brown
& hutChings 1997: 106. – laMas [1997b]: 65. – Mielke &
Casagrande 1998: 468. – wood & gillMan 1998: 609, 613.
– t. raCheli & l. raCheli 1998: 111. – devries & walla
1999: 347. – raMos 2000: 40. – t. raCheli & l. raCheli 2001:
213. – Brown & Freitas 2002: pl. 15. – laMas 2003: appendix
3, 203. – lande et al. 2003: 153. – laMas 2004: 218. – Mur-
ray & Prowell 2005: 69. – Brown et al. 2007 (appendix): 10.
– Pinheiro & eMery 2007: 72. – BeCCaloni et al. 2008: 329.
– Brévignon 2008: 72. – kaMinski & Freitas 2008: 171. – Bar-
low et at. 2009: 174. – Marín & uriBe 2009: 25. – Marín et
al. 2009: 242. – Mielke et al. 2010: 289. – Peña et al. 2010:
246. – salaZar et al. 2011: 166. – willMott et al. 2011: 2,
g. 15 (male). – Casagrande et al. 2012: 25. – Montero &
ortiZ 2013: 58. – CoCk 2014: 11. – garwood 2014: 24, gs.
253, 254. – garwood 2015: 57, gs. 727 – 729. – garwood &
JaraMillo 2016: 107, gs. 1219 – 1222.
Euptychia moneta Weymer, 1911: 200, pl. 47b; neotype herein des-
ignated: [French Guiana] Cayenne; NHMUK; syn.n. – gaede
1931: 455.
Euptychia maepius [misidentication]; lewis 1973: pl. 58, g. 10.
Cissia moneta; laMas 2004: 218.
Diagnosis. Cissia penelope has a distinctive feature of
the wing pattern that makes its identication easy when
compared to all other Euptychiina species: the presence
of dark brown scattered dots on the ventral wings in the
Z et al.: Systematics of butterfly genus Cissia
360
submarginal region between R5-Cu2 on VFW and Rs-Cu2
on the VHW. Additionally, the VHW has three silvery in-
complete ocelli, each one in Rs-M1, M2-M3 and M3-Cu1.
The VHW submarginal and marginal lines are irregular
and thin, widening between 1A + 2A and the tornus.
Male genitalia (Fig. 5A – E). Tegumen slightly at-
tened, laterally subtriangular; uncus arched downward,
about 2 × length of tegumen, covered by small setae,
smoothly dilated at median region in dorsal view, apex
laterally curved downwards and dorsally truncated;
gnathos hook-like, wide at base and tapering at apex,
½ – ⅔ × length of uncus; combination of ventral arm of
tegumen and dorsal arm of saccus slightly sinuous; ap-
pendix angularis short; anterior projection of saccus de-
veloped, cylindrical, and almost same length as gnathos;
fultura inferior present; fultura superior absent; valva
sub-rectangular covered by long hair-like setae latero-
ventrally, and short setae at inner side, costa developed
and sub-square, dorsal margin slightly projected at me-
dian region, ventral margin slightly projected at median
region, apex wide and serrated; phallus straight, shorter
than valva, cylindrical, anterior region bottle-shaped,
posterior region about 2 × longer than anterior region,
with bid apex in dorsal view, distal opening ventral and
longer than proximal opening.
Female genitalia (Fig. 4A,B). 8th tergite rectangular;
papilla analis somewhat triangular and covered by long
hair-like setae at distal region, apophysis posterior short;
lamella antevaginalis fused to lamella postvaginalis with
one spiracle located at upper margin of lateral expansions
of lamella antevaginalis; lamella postvaginalis obovate
in ventral view; ductus bursae membranous; corpus bur-
sae about same length as ductus bursae, with paired signa
dorsally.
Variation. In general, males are smaller (FW length:
17 – 20 mm) than females (FW length: 18 – 22 mm), with
a straight FW outer margin (rounded in females). The
subapical ocellus on the DFW is larger in females than
in males, and the VFW yellowish-ochre patch is larger
in females. weyMer (1911) suggested that the absence
of the silvery pupil at the apical ocellus on VFW could
be used to distinguish males and females, but this fea-
ture can be present or absent in both sexes. The width of
the median and submedian lines on ventral wings is in-
traspecically variable. The median line on the VHW can
be strongly concave in Cu2-1A + 2A, close to the inner
margin. Sometimes, the three silvery incomplete ocelli
located in R5-M1, M2-M3 and M3-Cu1 on VFW are faded,
although it can be possible to see these elements by mov-
ing the specimens against the light. Ocelli ring colora-
tion varies from pale-ochre to golden or orange. Some
structures of the male genitalia can show intraspecic
variation, such as the degree of concavity at the supe-
rior region of the gnathos, the anterior portion of saccus
varying between straight and smoothly curved upwards,
and the anterior region of the phallus being straight or
slightly curved downward.
Distribution. This species occurs in Central and South
America in Guatemala, Costa Rica, Colombia, Ecuador,
Peru, Bolivia, Venezuela, Guyana, Surinam, French Gui-
ana and Brazil, plus the islands of Curaçao and Trinidad,
mainly in association with Amazon and Atlantic forests,
but being also found in dry forests in Central America
and midwestern Brazil (Fig. 8). Cissia penelope is com-
mon and widely distributed in the cis-Andean region,
with only one record (garwood & JaraMillo 2016) in
the valley drained by the river Cauca, between the An-
dean Cordilleras Occidental and Central in Colombia.
It is found from sea level to about 2000 m. Regarding
phenotypically similar species, C. penelope is sympatric
in (1) Colombia with C. pompilia and C. proba; (2) Ven-
ezuela – C. pompilia; (3) Ecuador, Peru, Bolivia and Bra-
zil – C. proba. It is syntopic with C. proba in Meta and
Putumayo (Colombia), Napo and Orellana (Ecuador),
Amazonas, Acre, Maranhão, Mato Grosso and Rondônia
(Brazil), Junín, Loreto and Madre de Dios (Peru), and
Santa Cruz (Bolivia).
Although CoCk (2013: 83) mentioned that speci-
mens supposedly collected by Ralph du Boulay Evans
in Trinidad could be mislabelled (e.g.: male specimen at
NHMUK – voucher number BMNH(E) 1421881) and
might have come from western Venezuela or Curaçao,
we found additional specimens of C. penelope from
Trinidad collected by other naturalists, such as F. Birch,
T.T. Dyer and A. Hall, as well as being included in pub-
lications (kaye 1921; BarCant 1970; singer et al. 1983;
singer & ehrliCh 1993), which conrm its occurrence
on that island.
Biology and phenology. In general, C. penelope is found
at the forest edge and in nearby open areas such as grass-
land or pasture, avoiding deep shade in forests (singer et
al. 1983), and it has been considered an indicator of dis-
turbed areas (singer & ehrliCh 1993; Brown & hutCh-
ings 1997; wood & gillMan 1998; raMos 2000; lande
et al. 2003). It is multivoltine and ies year around.
Adults are attracted by rotting fruits and other decay-
ing material, and are consequently often captured in bait
traps (Mielke & Casagrande 1992; Brown & hutChings
1997; Casagrande et al. 2012).
Host plants and immature stages. Larvae of Cissia
penelope have been recorded feeding on Cyperus L.
and Seleria B. (Poales: Cyperaceae), and some species
of Poaceae, such as Ichnanthus pallens (Sw.), Lasiacis
sloanei (Griseb.), Panicum pilosum Sw., P. polygonatum
Schrad., Paspalum conjugatum P.J. Bergius, Pasp. de-
cumbens Sw., Setaria paniculifera (Steud.), and Tripsa-
cum sp. (singer et al. 1983; aCkery 1988; BeCCaloni et
al. 2008). The only information on the immature stages is
found in singer et al. (1983).
Type material, neotypes designation and taxonomic
history. FaBriCius (1775) described this species based
on an unstated number of specimens from an impre-
cise locality in America, collected by Drury. singer et
al. (1983) designated the neotype of Papilio penelope
Fabricius, 1775 (Fig. 58) in the ZMUC, with the follow-
ing labels: /Penelope ex. Am: Ma: Schmid’, ex Sehested
& Tonder Collection [handwritten]/ Mus. Leh. e T. L.
[handwritten]/ NEOTYPE Papilio penelope Fabricius,
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ARTHROPOD SYSTEMATICS & PHYLOGENY — 76
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1775, Singer et al., 1983: 110 [red label]/ photographed
[handwritten] R. I. Vane-Wright. 197/8/.
Papilio clarissa Cramer, 1782 was described based
on an unstated number of specimens from Surinam, col-
lected by Stoll. Godart ([1823]) noted that P. clarissa is a
junior synonym of P. penelope, and treated it in Satyrus
Latreille, 1810. The neotype female of Papilio clarissa
Cramer, 1782 (g. 59) is in the NHMUK and also desig-
nated in singer et al. (1983) with the following labels:
/N° 110. CLARISSA. Cr[amer]. IV. 293. D. E. [hand-
written]/ Linnep. Surin[ame]. [handwritten]/ FELDER
COLL[ECTIO]N./ Rothschild Bequest B. M. 1939-1/
NEOTYPE/ Papilio clarissa Cramer NEOTYPE det. R.
I. Vane-Wright 1983/.
Euptychia moneta Weymer, 1911 was described and
gured based on an unstated number of specimens from
Cayenne, French Guiana (weyMer 1911: 200, pl. 47b).
Syntypes of E. moneta have not been found after an ex-
haustive search in the ZMHU, ZSM, MTD or NHMUK
collections, which house the majority of the type mate-
rial of Weymer (nekrutenko 2001; PyrCZ 2006). Among
the Weymer types deposited at the ZSM, one specimen
was found identied as E. moneta from “San Ramons
[sic] [Junín]”, Peru, but it was collected in 1956 by F.
König, 45 years after the original description of this spe-
cies. Several of Weymer’s types went missing during
World War II and neotype designations are needed for
many names to permit their unambiguous identication
and clarify their taxonomic status, such as E. moneta.
Herein, the neotype of Euptychia moneta is designated,
which agrees completely with the original illustration
provided by Weymer; this neotype has the following la-
bels: /Cayenne [French Guiana]/ Ex Oberthür Coll. Brit.
Mus. 1927 – 3./ BMNH(E) #786267/; and two others will
be added later: /Neotypus/ Neotypus Euptychia mon-
eta Weymer, 1911. T. Zacca & B. Huertas, det. 2016/.
NHMUK.
Furthermore, E. moneta is placed as a new synonym
of C. penelope, since no other similar looking specimens
of E. moneta have been found in French Guiana or sur-
rounding countries, even though researches have been
conducting extensive eld works in these areas (A. Neild
and M. Benmesbah pers. comm.), and no inventories
have yet documented this species (e.g.: Brévignon 2005;
Brévignon & BenMesBah 2012). We therefore regard the
specimen used to represent E. moneta by Weymer, and
the neotype designated here, as aberrant forms of C. pe-
nelope, as already suggested in Brévignon (2008: 71).
Remarks. Forster (1964) erected the genus Argyreu-
ptychia to include E. penelope and six additional species,
based on morphological characters of the male genita-
lia and some wings features, such as the silvery marked
ocelli on the VHW. However, Argyreuptychia is a subjec-
tive junior synonym of Cissia Doubleday, 1848 since the
types of the two genera are currently regarded as neing
synonymous (see discussion in “History of classica-
tion”).
Examined material. See Electronic Supplement 1.
Cissia pompilia (C. Felder & R. Felder, 1867)
(Figs. 2E – H, 4F – J, 5C,D, 6A – D, 7A,B, 9)
Neonympha pompilia C. Felder & R. Felder, [25.IV].1867: 479;
syntypes: [Colombia] Bogotá and Mexico. Lectotype herein
designated: [Colombia] Bogotá; NHMUK (examined).
Euptychia usitata Butler, [30.IV.]1867a: 463, pl. 39, g. 2; syn-
types: Venezuela and Guatemala. Lectotype herein designated:
Venezuela; NHMUK (examined). – Butler 1868: 17. – kirBy
1871: 48. – Butler & druCe 1874: 336. – kirBy 1879: 132.
– weyMer 1890: 35. – weyMer 1911: 201, pl. 47e. – devries
1987: 272, pl. 48, gs. 22, 23 (male) [misidentication]. –
d’aBrera 1988: 773 (female). – santini 2004: 1056.
Euptychia pieria Butler, 1867a: 463, pl. 39, g. 3; syntype: Hon-
duras. Lectotype male here designated: Honduras; NHMUK
(examined). – Butler 1868: 17. – Butler 1870: 252. – kirBy
1871: 48. – Butler & druCe 1874: 336. – godMan & salvin
1880: 79 – 80. – weyMer 1890: 9. – godMan 1901 in godMan
& salvin: 654.
Euptychia austera Butler, 1867a: 464, pl. 39, g. 4; holotype: [Co-
lombia] Bogotá; NHMUK (examined). syn.n.
Neonympha thelete Snellen, 1887: 18, pl. 1, g. 3; lectotype: [Neth-
erlands] Curaçao; RMNH (examined).
Euptychia usitata pieria; Butler 1870: 252. – weyMer 1911: 201.
Euptychia usitata pompilia; weyMer 1911: 201, pl. 47e.
Euptychia usitata thelete; weyMer 1911: 201
Vareuptychia usitata; Forster 1964: 125, g. 146 (male genitalia).
– aCkery 1988: 115, table 9. – lewis 1973: 65, g. 9. – austin
et al. 1996: 33.
Vareuptychia pieria; llorente-BousQuets et al. 1986: 24.
Cissia usitata pieria; raguso & llorente-BousQuets 1991: 132.
Cissia usitata; MeerMan & BooMsMa 1993: 42.
Cissia pompilia; luis-MartíneZ et al. 1995: 119. – laMas 1996:
53. – laMas 2003: appendix 3, 203. – laMas 2004: 218; syn.:
usitata, thelete. – luis-MartíneZ et al. 2004: 349. – BeCCaloni
et al. 2008: 329. – PoZo et al. 2008: 415. – lóPeZ 2009: 28. –
Marín & uriBe 2009: 25. – Marín et al. 2009: 237. – BalaM
& león 2010: 531. – luis-MartíneZ et al. 2011: 23. – Marín et
al. 2012: 209. – Miller et al. 2012: 58. – garwood 2014: 58,
gs. 742 – 746. – garwood 2015: 38, gs. 448 – 453. – gar-
wood & JaraMilo 2016a: 107, gs. 1223 – 1228. – garwood
& JaraMilo 2016b: 103, gs. 1155 – 1160. – luis-MartíneZ et
al. 2016: 214.
Vareuptychia usitata pieria; PoZo et al. 2003: 516.
Yphthimoides austera; laMas 2004: 224.
Diagnosis. Compared to all other species of Cissia,
C. pompilia most closely resembles C. proba in its wing
shape and element pattern, but it can be distinguished
from this species by its paler ground color on both ventral
wings surfaces and the narrower submedian and median
lines.
Male genitalia (Fig. 4F – J). Tegumen slightly attened
in dorsal view, laterally subtriangular; uncus arched
downwards, about 2 × length of tegumen, covered by
small setae, not dilated at median region, apex curved
downwards and truncated in dorsal view; gnathos hook-
like, half length of uncus; combination of ventral arm
of tegumen and dorsal arm of saccus straight; appendix
angularis short and curved downwards; anterior projec-
tion of saccus developed, cylindrical, and longer than
gnathos; fultura superior absent; fultura inferior present;
valva sub-rectangular covered by long hair-like setae lat-
ero-ventrally, with short setae at inner side, costa devel-
oped and rectangular, dorsal and ventral margins slightly
Z et al.: Systematics of butterfly genus Cissia
362
projected at median region, apex pointed and serrated;
phallus straight, almost same length of valva, cylindrical,
anterior region bottle-shaped, posterior region about 2 ×
longer than anterior region with bid apex in dorsal view,
distal opening ventral and longer than proximal opening.
Female genitalia (Fig. 5C,D). 8th tergite rectangular; pa -
pilla analis somewhat triangular and covered by long
hair-like setae at distal region, apophysis posterior absent;
lamella antevaginalis fused to lamella postvaginalis with
one spiracle located at upper margin of its lateral expan-
sions; lamella postvaginalis orbicular in ventral view;
ductus bursae membranous; corpus bursae 0.5 – 1.0 ×
length of ductus bursae, with a short paired signa dorsally.
Variation. Females are mostly larger (FW length: 20 – 22
mm) than males (FW length: 17 – 21 mm) and have a
small subapical ocellus in M1-M2 on DFW. Females of
C. pompilia sometimes have small ocelli in R4 + 5-M1, M2-
M3 and M3-Cu1 on DFW and others similar in M1-M2,
M2-M3, M3-Cu1 and Cu2-1A + 2A on the DHW. If males
have one ocellus in M1-M2 on DFW, it is never larger
than that in females. A few specimens collected during
the wet seasons showed extremelly well-developed ocelli
on VW (Fig. 6A). Some structures of the male genitalia
can be variable, such as the shape of the tegumen varying
from attaned to slightly convex in lateral view, and the
length of the anterior projection of the saccus.
Distribution. This species is widely distributed through-
out Central America to South America, where it is re-
stricted to western Colombia, Venezuela and Ecuador
(Fig. 9). Cissia pompilia (Fig. 7A,B) is found in both
rain and dry forests, especially along forest edges, and
has also been documented in second-growth vegetation,
riparian forests and pastures (devries et al. 1997; lóPeZ
& MCneelly 2009). Cissia pompilia occurs up to altitude
of 1600 m (godMan & salvin 1901: 80; devries 1987;
specimen labels), The species is sympatric with C. penel-
ope in Colombia and Venezuela, and syntopic in Titiribí,
Antioquia (Colombia) (JaraMillo & garwood 2016a).
Biology and phenology. This species occurs through-
out the year, although PoZo et al. (2008) recorded its
highest abundance peak in October and its lowest abun-
dance in January, May and June, in the Calakmul region,
Campeche, Mexico. In Honduras, C. pompilia has been
documented only in the rainy season, between May and
September (Miller et al. 2012). Individuals have also
been captured by bait traps in Honduras (MeerMan &
BooMsMa 1993).
Host plants and immature stages. Recorded larval host
plants include species of Eleusine Gaertn. (Chloridoide-
ae, Poaceae) (devries 1987; aCkery 1988; santin 2004;
BeCCaloni et al. 2008). The only information on the im-
mature stages is found in devries (1987) and JanZen &
hallwaChs (2009).
Type material, lectotypes designation and taxonomic
history. Neonympha pompilia C. Felder & R. Felder,
1867 was described based on unstated number of speci-
mens from Colombia (Bogotá) and Mexico, collected
by [Alexander] Lindig and [Auguste] Sallé, respec-
tively. Four male syntypes of N. pompilia were found
at NHMUK, two from Bogotá and two from Mexico.
To x the identity of the name, herein is designated the
lectotype of this taxon; this specimen has the follow-
ing labels: /TYPE/ Bogotá, Lindig, type/ Neon.[ympha]
pompilia Feld/ = Euptychia pieria Butler (1866)/ Type
of N. pompilia Feld[er] = E. pieria Butl[er]. comp[ared].
w[ith]. type 10.XII.12, NDR [Norman D. Riley]/ Roths-
child Bequest B.M. 1939-1./ BMNH(E)#1267129/; and
two other labels will be added later: /Lectotypus/ Lecto-
typus Neonympha pompilia C. Felder & R. Felder, 1867.
T. Zacca & B. Huertas det. 2016/. NHMUK. The other
three syntypes are here designated as paralectotypes and
will be labelled accordingly.
Euptychia usitata Butler, 1867 was described based
on an unstated number of specimens from Venezuela and
Guatemala. godMan & salvin (1901: 80) stated that the
identity of this Venezuelan form (E. usitata) of E. pie-
ria need further consideration, as they did not have suf-
cient specimens to solve this puzzle. Only one female
syntype was found at the NHMUK that agrees with the
original description and illustration. To x the identity of
the name, this female syntype is designated herein as the
lectotype of this taxon; this specimen has the following
labels: /TYPE/ Euptychia usitata Butler Monog[raphy]./
B. M. TYPE No. Rh. 3299, Euptychia usitata Butl[er]./
Venezuela/ Venezuela Pur[chased]. from Dyson 47-9/;
and two other labels will be added later: /Lectotypus/
Lectotypus Euptychia usitata Butler, 1867. T. Zacca &
B. Huertas det. 2016/. NHMUK.
Euptychia pieria Butler, 1867 was described based
on an unstated number of specimens from Honduras.
Only one male syntype was found at the NHMUK that
agrees with the original description and illustration. To
x the identity of the name, this male syntype is desig-
nated herein as the lectotype of this name; this specimen
has the following labels: /TYPE/ Euptychia pieria Butler
Monog[raphy]./ B. M. TYPE No. Rh. 3199, Euptychia
pieria ♂ Butl[er]./ Honduras/ Honduras Pur[chased].
from Dyson 45-123/; and two others labels will be added
later: /Lectotypus/ Lectotypus Euptychia pieria Butler,
1867. T. Zacca & B. Huertas det. 2016/. NHMUK.
Euptychia austera Butler, 1867 was described based
on a single female [holotype] from Bogotá, Colombia.
Currently this species is placed in Yphthimoides Forster,
1964 (laMas 2004) and it is only known from the holo-
type deposited at NHMUK. No additional specimens
have been found in several collections examined for the
present study or in recent buttery inventories performed
in Colombia (e.g.: donegan & huertas 2005; Monte-
ro et al. 2009; Calero-MeJía et al. 2013; rodrígueZ &
Miller 2013; Marín et al. 2014). The holotype specimen
has the median and submedian bands fused into a single
broad band on both wings, and similar blurring and fu-
sion of the submarginal lines, strongly suggestive of a
type of aberration that is observed rarely in other species.
These observations, together with the otherwise simi-
lar morphology between the holotype of E. austera and
specimens of C. pompilia, led us to place the former as
synonym of the latter (syn.n.).
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ARTHROPOD SYSTEMATICS & PHYLOGENY — 76
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Neonympha thelete Snellen, 1887 was described
based on two syntypes from Curaçao Islands [Nether-
lands]. Snellen provided a very precise illustration of this
species that undoubtedly agrees with N. pompilia, and
N. thelete was correctly synonymized by laMas (2004).
The Snellen collection is currently housed at the Natu-
ralis Biodiversity Center, Leiden, Netherlands (RMNH).
Only one syntype was found there; the second syntype is
probably missing (E.G. Miracle pers. comm.). Although
this syntype has a lectotype label afxed by G. Lamas in
1995, it was never published. This syntype is designated
herein as the lectotype of this taxon to x the identity
of the name; this specimen has the following labels: /
Curaçao [Netherlands] R. P. Janson/ Neonympha thelete
Snell. nov. sp./ Lectotype ♂Neonympha thelete Snellen,
1887, G. Lamas des[ignated]. 1995; and two other labels
will be added later: /Lectotypus/ Lectotypus Neonympha
thelete Snellen, 1887. T. Zacca det. 2016/. RMNH.
Remarks. Determing the correct date of publication But-
ler’s “Monograph on the genus Euptychia” is important in
a series of decisions related to the priority of euptychiine
names. According to dunCan (1937), the work was read in
1866 during the meeting of the Zoological Society of Lon-
don. The proceedings of this meeting were divided into
three issues, and Butler’s paper appeared in the third issue
(pp. 377 – 645) published in April 1867, and therefore the
correct year of publication is 1867 and not 1866. The cor-
rect month should be April without any specic date since
this was never stated, and the default date therefore be-
comes April 30, the last day of the month. laMas (1996),
following higgins (1963), claried that the correct date
of publication of C. Felder & r. Felder’s (1867) work
was 25 April 1867, just ve days before Butler’s publica-
tion. godMan (1901: 564) was therefore incorrect when
he stated that E. pieria had priority over N. pompilia.
Butler (1867a) described E. usitata with two vari-
ations, one from Venezuela and the second from Guate-
mala. The former had a large ocellus in M3-Cu1 on DHW,
and the latter had a rufous median line on DW. In the
same work, Butler also described E. pieria from Hon-
duras. Interestingly, Butler considered E. pieria closely
related to E. similis (to be transferred to another genus
– Zacca et al. in prep.), and not to E. usitata. Three years
later, Butler (1870) published a work entitled “On new
and recently described species of diurnal Lepidoptera”
reporting his own mistake when considering E. pieria
and E. usitata as distinct species, and treated E. pieria as
a simple variety of E. usitata (Butler 1870: 252). wey-
Mer (1911: 201) considered E. pieria, E. pompilia and
E. thelete as forms of E. usitata.
The descriptions and illustrations of N. pompilia,
E. usitata and E. pieria agree in many aspects; laMas
([1997a]) came to the same conclusion, and synonymized
E. pieria and E. usitata with N. pompilia. The types of
these names differ only by their size, the expression of the
ocelli, and the coloration of the ventral lines. After exam-
ining a large series of specimens from localities in Central
and South America (see “Examined material” section), it
is apparent that C. pompilia exhibits seasonal polymor-
phism, which could account for taxonomic disagreements
over the years. For example, despite the absence of date
on the labels of syntypes of E. usitata from Polochic Val-
ley (Guatemala), the two specimens have a very charac-
teristic phenotype of the dry season, with ocelli less ap-
parent, and weak and rufous lines on the wings underside,
similar to other specimens collected between January and
April (dry season) in Mexico and Nicaragua (Fig. 6D).
One specimen from Panama in the NHMUK (Fig. 6C),
collected in July, displays a large ocellus and well-marked
dark brown lines on the underside of the wings, similar to
other specimens collected in the wet season.
Forster (1964: 125, g. 146) illustrated the male gen-
italia of this species (considered by him as Vareuptychia
usitata), but the cornuti were probably erroneously illus-
trated in the phallus. In all specimens of C. pompilia here
examined, there are no cornuti, and all other structural
features agree with Forster’s illustration. The absence of
cornuti is one of the most important features of all spe-
cies now allocated in Cissia.
snellen (1887) considered N. thelete to be pheno-
typically similar to E. liturata Butler, 1867, but the wing
elements of these two species are completely different, as
are the structures of male and female genitalia. Recently,
E. liturata was proposed as junior synonym of Prae-
faunula armilla (ZaCCa et al. 2017 – see also illustrations
of the genitalia for comparison).
Cissia pompilia was not included in the taxonomic
review of Cissia by singer et al. (1983).
Examined material. See Electronic Supplement 1.
Cissia proba (Weymer, 1911)
(Figs. 2I – L, 4K – O, 5E,F, 7C, 10)
Euptychia erigone f. proba Weymer, 1911: 203, pl. 47d, g. 5;
syntypes: Peru. Lectotype male herein designated: Peru; MTD
(examined).
Fig. 6. Seasonal polyphenism in Cissia pompilia: A,B: Costa Rica,
Puntarenas, Osa, collected in February: male: A – dorsal, B – ven-
tral; C: Panama, collected in July (wet season): male; D: Mexico,
collected in January (dry season): male. — © Trustees of the Natu-
ral History Museum, London.
Z et al.: Systematics of butterfly genus Cissia
364
Euptychia mariameliae Hayward, 1957: 109; holotype: Bolivia,
Santa Cruz; IML.
Argyreuptychia proba; Forster 1964: 124; syn.: mariameliae.
Cissia proba; laMas 1991: 10. – laMas 1994: 165. – devries et al.
1997: 355. – laMas [1997b]: 65. – Brown & Freitas, 2002: pl.
15. – laMas 2004: 218; syn.: mariameliae. – Marín & uriBe
2009: 25. – wahlBerg et al. 2009: table 1s (suppl.). – Mielke
et al. 2010: 290. – Peña et al. 2010: 246. – Piñas-ruBio 2010:
31, gs. 233 – 238. – CheCa et al. 2013: 486.
Cissia terrestris [misidentication]; willMott et al. 2011: 2, g.
16.
Diagnosis. Cissia proba is distinguished from its con-
geners by the (1) remarkable grayish-brown ground col-
our on VW, (2) differentiated scales that gives the VW
a “velvety texture”, (3) presence of a strong umbra on
both VW surfaces, and (4) creamy band between the me-
dian and submarginal bands on both VW. Cissia proba
might be confused with Cissia terrestris and Yphthi-
moides maepius, being differentiated from the former by
the VHW submarginal line being rounded and crenulated
between M1-Cu2 (pointed and crenulated in E. terrestris),
and from the latter by the presence of 3 rounded ocelli on
VHW (5 rounded ocelli in Y. maepius).
Male genitalia (Fig. 4K – O). Tegumen attened, later-
ally subtriangular; uncus arched downward, about 1.5 ×
length of tegumen, covered by small setae, not dilated
at median region in dorsal view, apex laterally curved
downwards and truncated in dorsal view; gnathos hook-
like, ⅔ – ½ length of uncus; combination of ventral arm
of tegumen and dorsal arm of saccus slightly sinuous; ap-
pendix angularis short; anterior projection of saccus de-
veloped, cylindrical, and almost same length as gnathos;
fultura superior absent; fultura inferior present; valva
sub-rectangular covered by long hair-like setae latero-
ventrally, and short ones at inner side, costa developed
and rectangular, dorsal margin straight at median region,
ventral margin slightly projected at median region, apex
pointed and serrated; phallus straight, longer than valva,
cylindrical, anterior region bottle-shaped, posterior re-
gion about two times longer than anterior region with bi-
d apex in dorsal view, distal opening ventral and longer
than proximal opening.
Female genitalia (Fig. 5E,F). 8th tergite rectangular; pa-
pilla analis somewhat oblong and covered by long hair-
like setae in distal region, apophysis posterior short; la-
mella antevaginalis fused to lamella postvaginalis with
one spiracle located at upper margin of its lateral expan-
sions; lamella postvaginalis orbicular in ventral view and
extremely well-developed; ductus bursae membranous;
corpus bursae 1.5 × length of ductus bursae, with paired
signa dorsally.
Variation. Sexual dimorphism related to the wingspan
is not evident in C. proba. Females can be easily dis-
tinguished from males by having a subapical, well-de-
veloped ocellus in M1-M2 on DFW. The dorsal ground
colour of the wings varies from brown to dark brown,
being lighter in some old specimens in collections. The
same occurs with the creamy band between the median
and submarginal bands on both VW, which can be faded
in old specimens. Additionally, the length of the anterior
projection of the saccus can be short (the same length of
the gnathos) or long (almost the same length of the un-
cus), but it is always large and cylindrical.
Distribution. This species has a trans-Andean distribu-
tion, occurring from Colombia to Bolivia, and to north-
ern and midwest Brazil (Fig. 10), in altitudes not higher
than 1450 m. Cissia proba is found almost exclusively in
the Amazon rainforest, but there are some records from
xerophytic vegetation in Bolivia and northern-midwest-
ern Brazil. Cissia proba is sympatric with phenotypically
similar species in (1) Colombia and Ecuador with C. pe-
nelope and pompilia (in the former country), (2) Peru,
Bolivia and Brazil with C. penelope, being syntopic
with the latter in Morona-Santiago, Pastaza, Sucumbíos,
Zamora-Chinchipe, Napo and Orellana (Ecuador), Lo-
reto and Madre de Díos (Peru), Buenavista, Santa Cruz
de la Sierra (Bolivia), and all those Brazilian states previ-
ously cited.
Biology and phenology. Cissia proba is multivoltine and
ies throughout the year (Fig. 7C). Adults are attracted
by rotting fruits and other decaying material, and con-
sequently frequently captured in bait traps (AVLF pers.
obs.). The species is common in disturbed areas and sec-
ondary growth near forest.
Host plants and immature stages. Unknown.
Type material, lectotype designation and taxonomic
history. Euptychia erigone f. proba Weymer, 1911 was
described based on an unstated number of specimens
from Peru, and two syntypes were found deposited in
the MTD. These syntypes are tagged with unpublished
lectotype and paralectotype labels. To x the identity
Fig. 7. Individuals in situ: A,B – Cissia pompilia, male (Colombia); C – Cissia proba, male (Junín, Peru). — Photos A,B: Juan Guillermo
Jaramillo; C: David Geale.
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ARTHROPOD SYSTEMATICS & PHYLOGENY — 76
(2) 2018
of the name, one of the syntypes is designated herein
as the lectotype of this taxon; this specimen has the fol-
lowing labels: /proba Weym. [handwritten]/ Hillapani
[Illapani Viejo, Cuzco] Peru [handwritten]/ Lectotype
♂ Euptychia erigone f. proba Weymer by G. Lamas
‘91/ Stauding[er]. & Bang-Haas Dresden. Ankauf 1961/
Staatl. Museum für Tierkunde Dresden/ GART specimen
ID: 02428 Exemplar + Etiketten/; and two others labels
will be added later: /Lectotypus/ Lectotypus Euptychia
erigone f. proba Weymer, 1911. T. Zacca det. 2016/. The
lectotype photo is also available in warren et al. (2017).
Euptychia mariameliae Hayward, 1957 was described
based on a single female [holotype] from Santa Cruz,
Bolivia. The description of this species agrees with
Euptychia erigone f. proba Weymer, 1911, and Forster
(1964) correctly treated E. mariameliae as a junior syno-
nym of the latter species.
Remarks. According to weyMer (1911), the Peruvian
E. erigone f. proba is distinguished from E. erigone (cur-
rently in Yphthimoides Forster, 1964) by a few charac-
ters of the VHW, such as the silvery incomplete ocelli in
M2-M3 and M3-Cu1, and the wide submedian and median
lines. Euptychia erigone f. proba was raised to species
by Forster (1964), who transferred it to his new genus
Argyreuptychia. This species was not treated in singer
et al. (1983), but it was correctly transferred to Cissia by
laMas (1991).
Examined material. See Electronic Supplement 1.
Cissia eous (Butler, 1867) comb.n.
(Figs. 2M – P, 4P – T, 5G,H, 11)
Euptychia eoüs [sic] Butler, 1867a: 477, pl. 39, g. 15; syntypes:
Brazil, Pará. Lectotype male herein designated: Brazil, Rio de
Janeiro; NHMUK (examined); incorrect original spelling (ICZN
1999, Art. 32.5.2). – Butler 1868: 24.
Euptychia eous; kirBy 1871: 580. – weyMer 1911: 208, pl. 48a. –
aurivillius 1929: 157. – gaede 1931: 445. – köhler 1935:
213. – BieZanko et al. 1957: 117. – BieZanko 1960a: 3. – Bie-
Zanko 1960b: 2. – BieZanko et al. 1962: 93. – BieZanko et al.
1966: 33. – d’aBrera 1988: 774 (male). – iserhard & roMa-
nowski 2004: 652.
Paryphthimoides eous; Forster 1964: 107, g. 109 (male genita-
lia). – Brown & Mielke 1967: 91. – BieZanko et al. 1974: 112. –
krüger & silva 2003: 40. – laMas 2004: 221; syn.: kiliani. – Bar
et al. 2008: 336. – núñeZ-Bustos 2008: 82. – PaZ et al. 2008:
145. – teston & Corseuil 2008: 47. – BentanCur-viglione 2009:
35. – núñeZ-Bustos 2009: 75. – doliBaina et al. 2011: 349. –
núñeZ-Bustos et al. 2011: 40. – Mielke et al. [2012]: 301. – gi-
aCoMet et al. 2012: 118. – silva et al. 2013: 90. – PaZ et al. 2013:
420. – garCia-salik et al. 2014: 279. – thiele et al. 2014: 7.
Paryphthimoides phronius [misidentication]: Brown 1992: 152,
153, g. 5. – Freitas & Brown 2004: 365. – FranCini et al. 2011:
65.
Paryphthimoides bahneri Anken, 1994: 348, gs. 1 (male), 2 (male
genitalia); holotype: Brazil, Mato Grosso do Sul, Navirai, Bar-
ranco do Rio Amambai; RA. syn.n.
Paryphtimoides kiliani Anken, 1999: 108 – 110, gs. 1 – 8 (male,
female, genitalia); holotype: Brazil, Minas Gerais, Poté; RA.
Diagnosis. Cissia eous is distinguished from its conge-
ners by the (1) DHW with a well-developed, rounded
ocellus in Cu1-Cu2, and circled by a well-marked golden
ring, (2) VHW with dark brown, ochre and crenulated
submedian, median, submarginal and marginal lines,
(3) in general, the median line on VHW is pronunced
inwards between Cu2 and the inner margin, and (4) the
space between the marginal line and the outer margin
is pale yellow ochre on VHW. The dorsal wing pheno-
type of C. eous is similar to C. proba, with no subapical
ocellus on DFW, but C. eous can be differentiated from
C. proba by the ocellus on DHW occupying half the
space between Cu1-Cu2 (while this ocellus occupies the
entire space in C. proba). Cissia eous is readily distin-
guished from C. phronius comb.n. by the median line be-
ing shifted inwards between Cu2 and the inner margin on
VHW, and by having males with the wings totally brown
(while these have a greasy-brown aspect in C. phronius
comb.n.)
Male genitalia (Fig. 4P – T). Tegumen slightly attened,
laterally subtriangular; uncus arched downward, about
1.5 × length of tegumen, covered by small setae, smooth-
ly dilated at median region, apex curved downwards and
truncated in dorsal view; gnathos hook-like (but not too
accentuated as in C. pompilia and C. proba), half length
of uncus; combination of ventral arm of tegumen and
dorsal arm of saccus sinuous; appendix angularis short
and curved downwards; anterior projection of saccus de-
veloped, cylindrical, longer than gnathos; fultura inferior
present; fultura superior absent; valva sub-rectangular
covered by long hair-like setae latero-ventrally, and short
setae at inner side, costa developed and rectangular,
dorsal and ventral margins slightly projected at median
region, apex wide and serrated; phallus straight, about
same length as valva, cylindrical, anterior region bottle-
shaped, posterior region about 2 × longer than anterior
region with bid apex in dorsal view, distal opening ven-
tral and longer than proximal opening.
Female genitalia (Fig. 5G,H). 8th tergite rectangular;
papilla analis somewhat triangular and covered by long
hair-like setae at distal region, apophysis posterior short;
lamella antevaginalis fused to lamella postvaginalis with
one spiracle located at upper margin of lateral expansions
of lamella antevaginalis; lamella postvaginalis orbicular
in ventral view; ductus bursae membranous; corpus bur-
sae about same length as ductus bursae, with paired signa
latero-ventrally.
Variation. Females are normally larger (FW length:
18 – 21 mm) than males (FW length: 15 – 19 mm), and
the distance between the median and submarginal lines
is wider on the VFW. The number of ocelli on the VFW
varies from three to four. The number of pupils in the
rst, third and fourth ocelli on the VHW can also vary
from one to two. The size of the ocelli on the VHW is
another variable feature, but even if the second and the
fth ocelli are reduced, the ochre-circled ring and the
pupil(s) are always evident, which easily distinguishes
C. eous from C. phronius. Seasonal polyphenism is also
observed in C. eous (as also reported in anken 1999),
with the ocelli extremely reduced and ventral dark lines
paler in the dry season.
Z et al.: Systematics of butterfly genus Cissia
366
Distribution. This species is restricted to South Ameri-
ca, occurring in Brazil, Uruguay, Paraguay and Argentina
(Fig. 11), and it has been found in several vegetational
formations, such as riparian forests, open woods and
second-growth forests, to anthropogenic areas (BieZanko
et al. 1960a; Brown & Mielke 1967; anken 1994; PaZ
et al. 2013). It is mainly found in lowland areas, but
can sometimes be found in mountainside forests (D.R.
Dolibaina pers. comm.), at altitudes below 1100 m. In
Brazil, C. eous is widely distributed in the northern, mid-
west and southern regions, with only one old record from
Manaus, Amazonas (aurivillius 1929) that is regarded
Figs. 8–13. Geographical distribution of Cissia species. 8: C. penelope. 9: C. pompilia. 10: C. proba. 11: C. eous. 12: C. phronius. 13:
C. rubricata and its subspecies.
8
10
12
9
11
13
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ARTHROPOD SYSTEMATICS & PHYLOGENY — 76
(2) 2018
as erroneous. Cissia eous is sympatric with C. penelope,
C. proba and C. phronius in midwestern Brazil, and only
with C. phronius in all other places where it occurs as
mentioned above, where both can also be found ying
together.
Biology and phenology. Cissia eous is commonly found
in moist and shady places of several different vegetal
formations, including secondary forests and forest edges
in coastal Brazil. Adults are attracted to fermented fruits
and other decaying materials (BieZanko et al. 1960a;
AVLF pers. obs.), being commonly collected in bait traps
(garCia-salik et al. 2014). It is multivoltine and ies
throughout the year.
Host plants and immature stages. Larvae of Cissia eous
have been recorded feeding on Poa L. species (hayward
1969; aCkery 1988), more specically in Poa annua L.
(BieZanko et al. 1957), and also in Digitaria sanguinalis
(L.) and Stenotaphrum secundatum (Walt.) (BieZanko et
al. 1960a; silva et al. 1968).
Type material, lectotype designation and taxonomic
history. Euptychia eous Butler, 1867 was described
based on an unstated number of specimens from Pará,
Brazil. After exhaustive searches at the NHMUK col-
lection, no syntypes from this type locality were found.
Nevertheless, two specimens from Rio de Janeiro, Brazil
were found at NHMUK, and they have the typical blu-
ish identication labels of Butler. One of these specimens
was chosen as the lectotype of Euptychia eous to x the
identity of the name; this specimen has the following la-
bels: /Type/ Rio de Janeiro/ Rio/ Euptychia eous Butler.
Monog[raph]./ B. M. Type No. Rh 3210 Euptychia eous
♂Butl[er]./ BMNH(E) 1267063/; and two other labels
will be added later: /Lectotypus/ Lectotypus Euptychia
eous Butler, 1867. T. Zacca & B. Huertas det. 2016/.
NHMUK.
Remarks. According to William T.M. Forbes (in let-
ter – BieZanko et al. 1960a), Euptychia eous differs from
E. poltys in having two larger and darker ocelli (at M1-M2
and Cu1-Cu2). Forbes also regarded Euptychia punctata
Weymer, 1911 as an extreme form of E. eous. However,
Freitas et al. (2016) recently demonstrated that E. punc-
tata is a valid species, currently placed in Sepona Freitas
& Barbosa, 2016. Comparing S. punctata and E. eous
there are clear differences between these species, such as
the smaller size in C. eous (16 – 19 mm), ocelli generally
bipupillated (always with only one pupil in S. punctata),
short gnathos (longer in S. punctata) and the narrow and
arched downward uncus (straight and wide in S. punc-
tata).
weyMer (1911) treated Euptychia zeredatha Butler,
1869 as a form of E. eous, stating that the former species
was distinguished from the latter by the small and puncti-
form ocelli on the ventral surface. Interestingly, BieZanko
et al. (1960b) found that E. eous and its E. zeredatha
form were syntopic, being also very common in Rio
Grande do Sul, Brazil. Cissia eous comb.n. and E. zere-
datha are distinguished by the less dense scales (giving
a translucide aspect) on the wings of the latter (BieZanko
et al. 1960b) and by all the ocelli on the underside be-
ing very small and punctiform (weyMer 1911). laMas
(2004) raised Paryphthimoides zeredatha to species, and
considered P. bahneri to be its synonym. However, mor-
phological evidence supports P. zeredatha as a synonym
of Paryphthimoides poltys (Zacca et al. in prep.).
Paryphthimoides bahneri Anken, 1994 was described
based on only one specimen [holotype] from Navirai,
Mato Grosso do Sul, Brazil. According to anken (1994),
this species is characterized by its reduced wings mark-
ings, DHW with two small ocelli in Cu1-Cu2 and Cu2-
1A + 2A, apex of the valva serrated and cornutal patch
located on the vesica. It has been observed that the two
former characters are strongly variable among individu-
als of C. eous. The illustration of the genitalia provided
by Anken shows strong similarities between his new
species and C. eous. Although Anken described P. bah-
neri as having a cornutal patch, his illustration is not ac-
curate concerning this structure, especially considering
that the cornuti are generally located on the vesica in all
Euptychiina genera that have this feature. Also, while
Anken’s text afrms that the diagnostic character of the
phallus of P. bahneri is the location of the cornutal patch,
in the illustration of the phallus there is an arrow indicat-
ing the posterior region of phallus as a diagnostic feature.
This arrow could also be interpreted as indicating the
‘cornuti’ to which he refers, or indicating that the pos-
terior region is bid, which it most likely is. If the latter
option is considered, the genitalia are clearly the same as
in C. eous, for which reason we synonymize P. bahneri
with C. eous, and not with C. phronius as suggested by
laMas (2004). In fact, C. eous, C. phronius and P. poltys
are phenotypically similar to each other concerning their
wing pattern, but their genitalia help reliably identify
them.
anken (1999) stated that P. kiliani differs from P.
eous by having less crenulated lines on both ventral
wings. Two male paratypes showed a distinct phenotype
that Anken treated as a variation of P. kiliani. One of
these paratypes is illustrated (p. 111, gs. 5, 6), and it is
clearly a species of Hermeuptychia. One might suspect
that Anken very probably choose to compare with the
“true” P. eous, the genitalia of one of those misidentied
paratypes. But curiously, the genitalia of the holotype il-
lustrated in his work (Fig. 7) agrees in all aspects with
C. eous, and does not support that explanation for An-
ken’s misinterpretation. As it was not possible to access
the types of P. kiliani, there is no other option than basing
the present taxonomic decision on the Anken’s paper and
well-illustrated male holotype. Paryphthimoides kiliani
was considered a synonym of P. eous by laMas (2004).
Examined material. See Electronic Supplement 1.
Cissia phronius (Godart, [1824]) comb.n.
(Figs. 2Q – T, 4U – Y, 5I,J, 12)
Satyrus phronius Godart, [1824]: 466, 496; holotype: Brazil. Neo-
type here designated: Brazil, Paraná, São José dos Pinhais;
DZUP.
Neonympha phronius; westwood 1851, in douBleday: 376.
Z et al.: Systematics of butterfly genus Cissia
368
Euptychia phronius; Butler 1867a: 470. – weyMer 1911: 206, pl.
48. – BieZanko et al. 1960a: 5. – BieZanko et al. 1962: 94. –
eBert 1969: 47. – d’aBrera 1988: 774.
Paryphthimoides phronius; Forster 1964: 107. – Brown & Miel-
ke 1967: 92. – Mielke 1994: 772. – Brown & Freitas 2000:
104. – Motta 2002: 157. – uehara-Prado et al. 2004: 14. –
eMery et al. 2006: 90. – MaChiori & roManowski 2006a:
447. – MaChiori & roManowski 2006b: 1032. – Pinheiro &
eMery 2006: 12. – dessuy & Morais 2007: 113. – Morais et
al. 2007: 42. – Pinheiro & eMery 2007: 72. – núñeZ-Bustos
2008: 82. – giovenardi et al. 2008: 603. – PaZ et al. 2008:
145. – Peixoto & Benson 2008: 1069. – Pinheiro et al. 2008:
142. – teston & Corseuil 2008: 47. – BetanCur-viglione
2009: 35. – núñeZ-Bustos 2009: 75. – Peixoto & Benson
2009: 1 – 14. – graZia et al. 2010: 187. – iserhard et al. 2010:
312. – núñeZ-Bustos 2010: 120. – Peña et al. 2010: 248. –
silva et al. 2010: 10. – BonFantti et al. 2011: 250. – doliBaina
et al. 2011: 349. – núñeZ-Bustos et al. 2011: 40. – Pedrotti et
al. 2011: 387. – ritter 2011: 5. – rosa et al. 2011: 3. – santos
et al. 2011: 272. – Bellaver et al. 2012: 185. – giaCoMet et al.
2012: 118. – silva et al. 2012: 295. – uehara-Prado & riBeiro
2012: 174. – MaChiori et al. 2013: 7. – PaZ et al. 2013: 420. –
garCía-salik et al. 2014: 279. – PaZ et al. 2014: 413. – thiele
et al. 2014: 7. – CaPorale et al. 2015: 5. – sPaniol & Morais
2015: 39. – graCiotiM & Moraes 2016: 120.
Diagnosis. Compared to all other species of Cissia,
C. phronius closely resembles C. eous, from which it can
be distinguished by its (1) angular hindwing shape with
the outer margin being produced distally at Cu1, (2) males
with greasy wings and less dense scales that are partly
translucent, and (3) ventral ocelli extremely reduced
(sometimes the only elements seen are the silvery pupils).
Male genitalia (Figs. 5U – Y). Tegumen attened in dor-
sal view, laterally subtriangular; uncus arched downward,
about 1.5 × length of tegumen, covered by small setae,
smoothly dilated at median region in dorsal view, apex
laterally curved downwards and truncated in dorsal view;
gnathos hook-like, half length of uncus; combination of
ventral arm of tegumen and dorsal arm of saccus sinuous,
appendix angularis short and curved downwards; anteri-
or projection of saccus developed, cylindrical, with same
length of gnathos; fultura superior absent; fultura infe-
rior present; valva sub-rectangular covered by long hair-
like setae latero-ventrally, and short ones at inner side,
costa developed and rectangular, dorsal margin straight
at median region, ventral margin projected at median
region, apex wide and serrated; phallus straight, about
same length as valva, cylindrical, anterior region bottle-
shaped, posterior region about 2 × longer than anterior
region with bid apex in dorsal view, distal opening ven-
tral and longer than proximal opening.
Female genitalia (Figs. 5I,J). 8th tergite rectangular;
papilla analis somewhat triangular and covered by long
hair-like setae at distal region, apophysis posterior short;
lamella antevaginalis fused to lamella postvaginalis, with
spiracle located at upper margin of its lateral expansions;
lamella postvaginalis orbicular and projected distally at
median region; ductus bursae membranous; corpus bur-
sae about ⅓ smaller than ductus bursae, with paired signa
ventrally.
Variation. Males are mostly smaller (14 – 18 mm) than
females (18 – 21 mm) and their wings are greasy. In-
traspecic variation can be noticed in the width of the
apex of the valva, which can vary from wide to narrow,
similar to the apex of C. proba.
Distribution. This species is restricted to South Ameri-
ca, specically Brazil, Uruguay, Paraguay and Argentina
(Fig. 12). Cissia phronius is found in open grasslands,
riparian forests, forest edge, and even antropogenic areas
(Brown & Mielke 1967; eBert 1969; Motta 2002; Mo-
rais et al. 2007; Bustos 2008; Peixoto & Benson 2008;
Pinheiro et al. 2008; núñeZ-Bustos 2010; ritter et al.
2011; rosa et al. 2011; Bellaver et al. 2012; silva et al.
2012; CaPorale et al. 2015); also in native forests and
reforested areas of Araucaria, in mixed ombrophilous
forest in Rio Grande do Sul, Brazil (iserhard et al. 2010;
santos et al. 2011). In Brazil, C. phronius is widely dis-
tributed from Goiás to Rio Grande do Sul, in altitudes
up to 1500 m, but it is most common in elevations up to
800 m (D.R. Dolibaina pers. comm.). It is sympatric and
syntopic with C. eous in a few localities, and sympatric
with C. penelope only in Goiás.
Biology, phenology and behaviour. Males of C. phro-
nius are territorialist and defend their areas by chasing off
conspecic rivals (Peixoto & Benson 2008). According
to Peixoto & Benson (2009), the increase in the tempera-
ture during the dry and wet seasons is directly related to
the increase of abundance of C. phronius in eld. Cissia
phronius is multivoltine and ies year round, and simi-
larly to several other euptychiines, this species ies close
to the ground. Adults are attracted by rotting fruits and
other decaying material, and consequently are often cap-
tured in bait traps (PaZ et al. 2014; sPaniol & Morais
2015; AVLF pers. obs.), being one of the most abundant
species of Euptychiina in inventories (dessuy & Moraes
2007; thiele et al. 2014).
Host plants and immature stages. Larvae of Cissia
phronius have been recorded feeding on species of Poa-
ceae, such as Poa annua L., Digitaria sanguinalis L.,
Paspalum distichum L., P. notatum Flüggé and Steno-
taphrum secundatum Kuntze (núneZ-Bustos 2010). The
only information on immature stages is that the eggs are
rounded and yellow (núneZ-Bustos 2010).
Type material, neotype designation and taxonomic
history. Satyrus phronius Godart, [1824] was described
based on only one specimen [holotype] which had only
the wings sent from a non-specic locality in Brazil.
The description of this species species (as is the case
with many other Euptychiina species described by J.B.
Godart) is very broad, not precisely dening S. phronius.
The only character mentioned by Godart that permits
discrimination between S. phronius and the phenotypi-
cally similar C. eous is the ventral ocelli not surrounded
by yellowish ring, with the last two extreme ringed with
black. The other characters mentioned by Godart, such
as the 1) DW with the outer area darker, 2) VW yellow-
ish, 3) three transversal dark brown waved lines, 4) outer
line convoluted (crenulated) also t with the description
of E. eous. The VFW with a single white pupil, cited by
Godart, is an intraspecically variable feature in this spe-
cies.
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ARTHROPOD SYSTEMATICS & PHYLOGENY — 76
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Considering that the wings [holotype] used to de-
scribe Satyrus phronius has neither been found at the
Muséum national d’Histoire naturelle, Paris, France
(O.H.H. Mielke, R. Rougeri, pers. comm.), nor at the
NHMUK, a neotype of Satyrus phronius is designated
herein; this specimen has the following labels: /Neoty-
pus/ 19.III.1979, S.[ão] José dos Pinhais, PR [Paraná],
[Brazil], 850 m, Mielke leg./ DZ 28.625/ Neotypus
Satyrus phronius Godart, [1824]. T. Zacca det. 2016/.
DZUP.
Examined material. See Electronic Supplement 1.
Cissia rubricata (W.H. Edwards, 1871) comb.n.
(Figs. 2U – X, 4Z – AD, 5K, 13)
Euptychia rubricata W.H. Edwards, 1871: 212. Neotype desig-
nated by F. Brown, 1964: Waco, Texas; CMNH. – M. Brown
1964: 334, g. 2.
Megisto rubricata; Miller 1976: 9, gs. 21 – 25.
Diagnosis. Cissia rubricata comb.n. is easily distin-
guished from its congeners by the reddish patches on
both DFW and VWH.
Remarks. Euptychia rubricata was described based on at
least three specimens, a male and two females, collected
by G.W. Belfrage in Waco, Texas, USA (edwards 1871).
In his catalogue on the types of Satyrinae butteries de-
scribed by E.W. Edwards, M. Brown (1964) did several
nomenclatural acts, including the designation of the neo-
type of E. rubricata based on a male specimen from the
original type-locality, currently deposited at the CMNH
(for further information see M. Brown 1964: 334, 335).
According to Miller (1976), this species contains ve
subspecies, C. rubricata rubricata comb.n., C. rubricata
smithorum (Wind, 1946) comb.n., C. rubricata cheneyo-
rum (Chermock, 1949) comb.n., C. rubricata anabelae
(Miller, 1976) comb.n. and C. rubricata pseudocleophes
(Miller, 1976) comb.n., distributed from southern USA
to Honduras (Miller 1976; lotts & naBerhaus 2017)
(Fig. 13). A detailed comparative study of the morpho-
logy of the subspecies of C. rubricata, and information
on their respective distribution and phenology, is found
in Miller (1976), but illustration of female genitalia is
given herein for the rst time (Fig. 5K). Although ed-
wards (1871) indicated that this species was closely re-
lated to Pharneuptychia phares (Godart, [1824), based
on the similarities of the wing elements pattern, molecu-
lar evidence presented herein strongly supports its inclu-
sion in Cissia as redened here.
Examined material. See Electronic Supplement 1.
4. Discussion
Both molecular and morphological phylogenies of Eu-
ptychiina (Murray & Prowell 2005; Peña et al. 2010;
Marín et al. 2017) have shown Cissia as dened by
previous authors to be a polyphyletic genus. Sampling
six species of Cissia (C. penelope, C. confusa, C. myn-
cea, C. similis, C. terrestris and an unidentied species),
Murray & Prowell (2005) showed that C. penelope was
not related to the other ve species then included in the
genus, but was more closely related to the genera Megis-
to, Cyllopsis R. Felder, 1869 and Paramacera Butler,
1868 (all of them with species occurring in the Neartic
region), or even the Neotropical Yphthimoides Forster,
1964. The results obtained by Peña et al. (2010) placed
C. phronius as the sister of C. penelope, and both as sis-
ter of C. proba. This clade, also including Megisto and
Paleonympha Butler, 1871, constitutes one of the rst
branches in the Euptychiina tree. The results obtained
by Marín et al. (2017) also indicate C. penelope as sister
of C. pompilia, and that this clade is closely related to
Megisto and Paleonympha. The molecular phylogenetic
analysis performed in the present study mostly corrobo-
rates the results found in the previous studies. Our re-
sults (Fig. 1) show that Cissia is more closely related to
a clade composed of species of Carminda Dias, 1998,
Yphthimoides, Graphita Nakahara, Marín & Barbosa,
2016, Stegosatyrus Zacca, Mielke & Pyrcz, 2013, and a
new genus that will be described to contain some of the
species removed from Cissia (Zacca et al. in prep.).
Although the genus Atlanteuptychia Freitas, Barbosa
& Mielke, 2013 seems morphologically similar to Cis-
sia, sharing glabrous eyes and a short, hooked gnathos
in the male genitalia (see Freitas et al. 2013: 664, g. 7),
molecular evidence shows that these genera are distantly
related (Fig. 1), with Atlanteuptychia more closely re-
lated to Paramacera and Cyllopsis, as already indicated
by nakahara et al. (2015). Conversely, C. rubricata is
the only species of Cissia that does not have this short
and hooked gnathos, with genitalia that are more similar
to those found in some species of Magneuptychia For-
ster 1964 or Paryphthimoides Forster, 1964. According
to DNA sequence data, gnathos morphology does not
reect the evolutionary history of extant species of Cis-
sia.
Among all the species of Cissia, C. pompilia stands
out by its remarkable seasonal polyphenism that histori-
cally has led to the description of three names for the
same species. This species occurs in dry, forested regions
in Central and South America, with a severe to absolute
dry season for most part of the year, and rains falling
sporadically. Seasonal polyphenism in satyrine butter-
ies has been documented in some Brazilian, African and
Australian species (BrakeField & larsen 1984; Brake-
Field 1987; roskaM & BrakeField 1999; Freitas 2007;
Freitas et al. 2010; ZaCCa et al. 2014). This phenomenon
seems related to temperature variation during the wet/
dry seasons experienced by the larvae prior to pupation
(BrakeField & reitsMa 1991; BrakeField & Frankino
2009; siMPson et al. 2012). In Euptychiina, it seems to
directly affect the coloration and size of the wing ele-
ments, but their shape and location are not affected by the
environmental factors (niJhout 1991).
Z et al.: Systematics of butterfly genus Cissia
370
A detailed review of the immature stages is beyond
of the scope of the present study, but it is worth noting
that recent studies have indicated that the occurrence
of four larval instars formerly considered to be exlu-
sively found in Cissia (as suggested by singer et al.
1983), is also present in other phylogenetically distant
euptychiine genera (wahlBerg et al. 2009; Peña et al.
2010; Marín et al. 2017), such as Posttaygetis Forster,
1964 (Murray 2003), Taygetis Hübner, [1819] (Murray
2001; Freitas 2017), Forsterinaria Gray, 1973 (Freitas
& Peña 2006), Hermeuptychia Forster, 1964 (CosMo et
al. 2014) and Pareuptychia Forster, 1964 (Freitas et al.
2016b,c). The number of larval instars does not seem to
be a reliable feature to exclusively dene the genera of
Euptychiina, especially considering that some of them,
such as Taydebis Freitas, 2003, Magneuptychia and
Moneuptychia Forster, 1964 may have ve larval instars
(Freitas 2003, 2007; kaMinski & Freitas 2008; Freitas
et al. 2015). On the other hand, morphological charac-
ters related to egg, body colour, size and shape of the
cephalic horns or scoli of the larvae, and pupae, seems
to be more informative at the interspecic level. Future
studies should focus on providing detailed comparative
morphological studies of the immature stages of Cissia,
Magneuptychia and Paryphthimoides to verify if the
number of larval instars is congruent for each genus or if
it is a variable character.
5. Acknowledgments
The authors would like to express their gratitude to Wolfram Mey
(ZMHU), Tomasz Pyrcz (MZUJ), Jane Costa and Aline Vieira
(IOC) for providing access to the specimens deposited in the col-
lections under their care; to Ole Karsholt for sharing with us the
photos of the neotype of Papilio clarissa deposited at ZMUC; to
Alex Hausmann and Ulf Buchsbaum for the valuable informa-
tion on the types of G. Weymer deposited at ZSM and for sharing
photos of those types; to Marianne Elias and Rodolphe Rougerie
for their valuable information on the types of J.B. Godart depos-
ited at MNHN; to Mohamed Benmesbah and Andrew Neild for
the records, data and discussions on the geographical distribution
of the species of Cissia from French Guyana and Venezuela, re-
spectively; to John Kochalka, Carlos Aguilar-Julio and Mohamed
Benmesbah for the data of Cissia eous collected in Paraguay; to
Gerardo Lamas for valuable help with the bibliography and photos
of Cissia deposited at UNMSM. Vladimir Blagoderov (NHMUK)
assisted in the use of the automontage equipment at the Sackler
Biodiversity Imaging Laboratory, and Franciele L. Bettim helped
at TaxonLine-UFPR. We thank the Trustees of the Natural His-
tory Museum and Sophie Ledger for assisting with obtaining
photos of type specimens. The Conselho Nacional de Desenvolvi-
mento Cientíco e Tecnológico (CNPq), Brazil, granted a fellow-
ship to TZ (140225/2013-7), OHHM (304639/2014-10), MMC
(308247/2013-2) and AVLF (grants 303834/2015-3 and SIBIO-
TA-CNPq 563332/2010-7). TZ thanks the Coordenação de Aper-
feiçoamento Pessoal de Nível Superior (CAPES) for the PDSE
scholarship (99999.002879/2014-00). TZ (2017/02264-6) and EPB
(2016/15873-8) thanks FAPESP for post-doc fellowships. We ac-
knowledge support from the National Science Foundation (DEB-
1256742), and AVLF acknowledges the ICMBIO for providing a
research permit (SISBIO n° 10802-5), the FAPESP (Biota-Fapesp
grants 2011/50225-3, 2012/50260-6 and 2013/50297-0), and US-
AID and the U.S. National Academy of Sciences (NAS) under the
PEER program (Mapping and Conserving Buttery Biodiversity in
the Brazilian Amazon – PEER Cycle 4-478).
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Electronic Supplement Files
at http://www.senckenberg.de/arthropod-systematics
File 1: zacca&al-cissiasatyrinae-asp2018-electronicsupplement-1.
doc — List of examined material.
File 2: zacca&al-cissiasatyrinae-asp2018-electronicsupplement-2.
nex — Partition and substitutions models.
File 3: zacca&al-cissiasatyrinae-asp2018-electronicsupplement-3.
tif — Phylogeny of the genus Cissia based on Bayesian Inference
of combined COI, GAPDH and RpS5 gene sequences.
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