Nhambikuara cerradensis Freitas, Barbosa & Zacca, 2018

Freitas, André V. L., Barbosa, Eduardo P., Zacca, Thamara, Marín, Mario Alejandro, Beirão, Marina V., Silva, André R. M., Casagrande, Mirna M., Espeland, Marianne & Willmott, Keith R., 2018, Before it is too late: description of a new genus and species of butterfly from a highly threatened Brazilian biome, Revista Brasileira de Entomologia 62 (2), pp. 148-158 : 150-153

Nhambikuara cerradensis Freitas, Barbosa & Zacca , sp. nov.

( Figs. 1 , 2 , 5 , 6)

Yphthimoides sp.1 ; Silva et al., 2012: 295

Satyrinae sp.1; Freire Júnior & Diniz, 2015: 1214

Type material. Holotype male deposited at ZUEC ( Figs. 1A, 1B ) with the following labels (separated by transverse bars): / Holotypus / Serra do Cipó , Santana do Riacho, Minas Gerais, Brasil, 08.III.2009, Kaminski L. A. leg./ ZUEC LEP 10071/ Nhambikuara cerradensis Freitas, Barbosa & Zacca det. 2018 /

Allotype female deposited at ZUEC ( Figs. 1C, 1D ) with the following labels (separated by transverse bars): / Allotypus /Serra do

Cipó , Santana do Riacho, Minas Gerais, Brasil, 11.III.2009, Kaminski L. A. leg. /ZUEC LEP 10073/ Nhambikuara cerradensis Freitas, Barbosa & Zacca det. 2018 /

Diagnosis. This species is characterized by the following combination of characters: 1) absence of ocelli in DW, 2) ochre wavy submedian, median, submarginal and marginal lines in VHW, 3) six small bipupilated ocelli in VHW between Rs and 2A, 4) valva with subtriangular developed costae and apex strongly serrated, 5) aedeagus with elongated paired cornutal patches and anterior region strongly curved upwards, 6) sterigma strongly sclerotized and developed, almost three times longer than wider, 7) ductus bursae membranous with a half-ring sclerotized plate and, 8) corpus bursae with dorsal paired signa. DNA sequence data suggest that its sister species is Nhambikuara mima comb. nov., and the differences between these two species are discussed further below, under the account for N. mima .

Description. Head: dark brown, frons with mixed creamy and light brown scales; eyes chestnust brown, with sparsely localized bristles; post-genal area creamy mixed with light brown scales; labial palpus curved upwards, dorsally short, creamy mixed with brown scales, laterally short, creamy scales, ventrally elongated with creamy mixed with light brown scales at first and second segment, short scales at third segment; antennae brown with apex dark brown, laterally with white scales in each side of the base of the flagellomeres. Thorax: dorsally brown, ventrally covered in long mixed creamy and brown scales; legs mixed with creamy and light brown scales. Wings: males FW: 17–19 mm (n = 7), HW: 14–15 mm (n = 5) (Holotype: FW: 19 mm; HW: 14 mm), females FW: 19–21 mm (n = 8), HW: 15–16 mm (n = 6) (Allotype: FW: 20 mm; HW: 15 mm). DFW: ground color brown, submarginal and marginal lines dark brown, marginal region light brown.DHW:similar to DFW. VFW: ground color light brown, four parallels brown ochre lines, submedian and median lines crossing from Radius to 1A + 2A, and submarginal and marginal lines crossing from R 4 to inner margin; two small ocelli in M 1 -M 2 and M 2 -M 3 in submarginal

0.5 mm

0.5 mm

region. VHW: ground color light brown, four parallels brown ochre lines crossing from costal margin to inner margin, median and submarginal lines irregular fused to each other at tornal area, a series of six ocelli at submarginal region in Rs-M 1, M 1 -M 2, M 2 - M 3, M 3 -Cu 1, Cu 1 -Cu 2, Cu 2 -1A + 2A, ocelli Rs-M 1 and Cu 2 -1A + 2A with only a silvery pupil, ocelli M 1 -M 2 to CuA 1 -CuA 2 bipupilated. Abdomen: dorsally brown, ventrally with mixed creamy and brown scales.

Male genitalia ( Figs. 2A–2E ). Tegumen dorsally flattened, anterior margin concave at median region; gnathos 2/3 the length of uncus, sinuous and curved upwards; uncus straight, apex curved downwards, basal third as long as the median region; appendices angulares reduced; anterior projection of saccus almost two times longer than valva; fultura superior absent; fultura inferior sclerotized in U-shape; valva with a developed costae, dorso-apical region serrated, basal region narrow; aedeagus with anterior region strongly curved upwards, posterior region about 1 ½ length of anterior region, elongated paired cornutal patches.

Female genitalia ( Figs 2F, 2G ). 8th tergite half-sclerotized, not fused with the lateral expansions of lamella antevaginalis, spiracle absent; papilla analis developed, sub-squared, basal half strongly sclerotized, setae sparsely distributed at distal region, apophysis posterior reduced; lamella antevaginalis fused to lamella postvaginalis forming the sterigma which is strongly sclerotized and developed, almost three times longer than wider; ductus bursae membranous, as long as corpus bursae, sclerotized half-ring between ductus bursae and corpus bursae, paired signa dorsally.

Variation ( Figs 1E, 1F ). Seasonal variation seems to occur in this species, as has also been reported for many other species of Euptychiina from the Brazilian savanna ( Freitas, 2007; Freitas et al., 2010; Siewert et al., 2013; Zacca et al., 2014). During the rainy season (October to March), the wing ventral ocelli are developed, filling in most of the intervenal spaces on the VHW, whereas these ocelli become strongly reduced in the dry season (April to September).

Distribution ( Fig. 6). This species is mostly associated to open vegetation, especially the Brazilian cerrado (States of Maranhão, Ceará, Bahia, Goiás, Distrito Federal, Mato Grosso, Mato Grosso do Sul, Minas Gerais and São Paulo ), a biome that presents a high richness of endemic species ( Ratter et al., 1997; Brown and Gifford, 2002).

Natural history. This species is restricted to open savannic vegetations in the cerrado biome, montane rocky fields (known locally as “ campos rupestres ”), flying both in open vegetation and at the edges of the riparian forests along small streams. In the region of Belo Horizonte, Minas Gerais, 46 out of the 48 sampled individuals were captured in the cerrado area, and only two in the adjacent riparian forest. In a cerrado area in Brasília (central Brazil), 72 out of the 104 sampled individuals were captured in the cerrado area and 32 in the adjacent riparian forest (Freire Júnior, 2015). Adults have a low flight, usually not flying more than 1.5 m above the ground. The species is usually localized and although it has been throughout the year, typically no more than 10 individuals are seen in a single day. However, the species was found to be common in some sites, such as Santana do Riacho, Minas Gerais, where from 30 to nearly 60 individuals were captured with bait traps in single months (MVB, unpublished; see also Freire Júnior, 2015 and Freire Júnior and Diniz, 2015). Males and females were observed feeding on animal feces and other decaying material and were easily attracted to traps baited with fermented fruits (AVLF, MVB and ARMS, pers. obs., Silva et al., 2012). The sex ratio was close to 1: 1 in two bait trap studies, with females being more common in both studies: 1) in Santana do Riacho, a total of 81 females and 64 males were captured (x 2 = 1.99, P = 0.18, DF = 1); 2) in Itirapina, a total of 10 females and four males were captured (x 2 = 2.57, P = 0.11, DF = 1). Individuals were more active during the morning, and no territorial behavior has been reported (AVLF pers. obs.).

Etymology. The name of this species is formed by adding the suffix -ensis to the toponym “cerrado” to form an adjective which means “from the cerrado”, alluding to its strong association with the savannic Brazilian cerrado biome. As mentioned before, the cerrado is one of the most threatened phytophysiognomies in Brazil ( Strassburg et al., 2017), suffering from high anthropic conversion rates every year, mostly to give place to extensive soybean and sugarcane plantations.

Paratypes. BRAZIL – Maranhão: Feira Nova – 26 km East, Fazenda Forquilha dos Brejos, 1 male, 13-16-IV-2011, Mielke & Casagrande leg., DZ 32.041 (DZUP); Imperatriz – 1 male, 9-VII-1974, Exc. Depto Zool., DZ 31.804 (DZUP). Ceará: Viçosa do Ceará – 3 km W, 750 m, 1 male, 28.V.2013, Dolibaina & Pessoa leg., DD 226* (DD). Bahia: Catolés – Abaíra, Chapada Diamantina, 1 male, 1.XI.2013, S. M. Kerpel & A. F. Junior leg., CLEIIC802 (CLEIC), 1 female, 2.XI.2013, S. M. Kerpel & A. F. Junior leg., CLEIIC803 (CLEIC), 1 male, 3.XI.2013, S. M. Kerpel & A. F. Junior leg., CLEIIC804 (CLEIC), 1 male, 31.X.2013, S. M. Kerpel & A. F. Junior leg., CLEIIC805 (CLEIC); Morro do Chapéu – Capão do Pinho, 1 male, 1 female, 22.VI.2009, T.Zacca leg., MZUEFS#5.0060, MZUEFS#5.0059 (MZFS); Pindobaçu – Cachoeira da Fumaça, 10 ◦ 28 l 43 llS 40 ◦ 12 l 27.6 llW, 1 male, XII.2009, T. Zacca leg., MZUEFS#46.805 (MZFS); Senhor do Bonfim – Serra da Maravilha, 1 male, 1 female, 20.VII.2009, T. Zacca leg., MZUEFS#45220, MZUEFS#45179 (MZFS). Distrito Federal: Brasília – 1000 m, 1 male, 8.IX.1969, H. Ebert leg., DZ 35.043 (DZUP), 4 females, 14.V.1969, ex-coll. H. Ebert, DZ 34.963, DZ 34.983, DZ 35.213, DZ 35.273 (DZUP), Parque do Gama, 1000 m, 1 male and 2 females, 17-VI-1972, Mielke & Brown leg., DZ 33.899*, DZ 35.113, DZ 35.073 (DZUP), 1 male, 4 females, 17.V.1969, ZUEC-LEP 10285, ZUEC-LEP 10286, ZUEC-LEP 10287, ZUEC-LEP 10288, ZUEC-LEP 10289 (ZUEC), 1 male, 20.VI.1972, K. S. Brown leg., ZUEC-LEP 10297 (ZUEC), Fazenda Água Limpa, 1 female, 11.VII.1976, K. S. Brown leg., ZUEC-LEP 10266 (ZUEC), Brasília Country Club, 1200 m, 1 female, 17.VI.1972, Mielke & Brown leg., DZ 35.173 (DZUP), 2 females, 19.VI.1972, DZ 35.183, DZ 35.193 (DZUP), 2 females, 18.VI.1972, K. S. Brown leg. ZUEC-LEP 10267, ZUEC-LEP 10269 (ZUEC); Planaltina – 15 ◦ 35 lS 47 ◦ 42 lW, 1000 m, 1 male, 4.XII.1982, Mielke & Becker leg., DZ 35.153 (DZUP). Goiás: 2 males, 31.VIII.1969, ex-coll. H. Ebert, DZ 34.953, DZ 35.243 (DZUP); Goiânia – 2 males and 1 female, 17.XII.1968, K. S. Brown leg., ZUEC-LEP 10282, ZUEC-LEP 10283, ZUEC-LEP 10284 (ZUEC); Rio Quente – Pousada do Rio Quente , 2 males, 12.II.1979, A. Raw leg., DZ 35.023, DZ 35.163 (DZUP); Iporá – 1 male, 21.VI.1972, K. S. Brown leg., ZUEC-LEP 10299 (ZUEC). Mato Grosso: Diamantino – Rio Arinos, Fazenda Diamantino , 300–400 m, 1 male (no abdome), 5.V.1986, H. & H. D. Ebert leg., DZ 35.103 (DZUP), 1 female, 26.VIII.1978, Mielke & Furtado leg., DZ 35.013 (DZUP), 1 female, 5-IX-1996, E. Furtado leg., DZ 33.900* (DZUP), 1 male, 7-IX-1978, Mielke & Furtado leg., DZ 31.884 (DZUP); São Vicente – São José da Serra , 700 m, 1 male, 24.VI.1972, Mielke & Brown leg., DZ 35.093 (DZUP), 1 female, 24.VI.1972, K. S. Brown leg., ZUEC-LEP 10295 (ZUEC). Mato Grosso do Sul: Aquidauana – 20 ◦ 25 l 59.23 llS –55 ◦ 39 l 30.28 llW, 2 females, no date, (DNA Vouchers YPH-0575,YPH-0576), J.Lener leg., ZUEC-LEP 10013, ZUEC-LEP 10014 (ZUEC). Minas Gerais: Belo Horizonte – 4 males, 5 females, Área de Proteção Especial Manancial

Cercadinho, 2007, 19 ◦ 58 l 18.4 llS 43 ◦ 54 l 30 llW, Silva A.R.M. leg., ZUEC-LEP 10076, ZUEC-LEP 10078, ZUEC-LEP 10080, ZUEC-LEP 10084, ZUEC-LEP 10077, ZUEC-LEP 10079, ZUEC-LEP 10080, ZUEC-LEP 10081, ZUEC-LEP 10082 (ZUEC); Letícia – Córrego leitão, 19 ◦ 06 l 38 llS 44 ◦ 32 l 14 llW, 1 male, 15.VI.1972, K. S. Brown leg., ZUEC-LEP 10296 (ZUEC); Paracatu – 1 female, 13.V.1969, K. S. Brown leg., ZUEC-LEP 10274 (ZUEC), 1 male, 16.V.1969, ex-coll. H. Ebert, DZ 35.003 (DZUP); Buritis – 1 female and 1 (no abdomen), 23.XII.1968, ex-coll. H. Ebert, DZ 34.993, DZ 35.233 (DZUP), 8 males and 4 females, 23.XII.1968, K. S. Brown leg., ZUEC-LEP 10268, ZUEC-LEP 10270, ZUEC-LEP 10271, ZUEC-LEP 10272, ZUEC-LEP 10273, ZUEC-LEP 10275, ZUEC-LEP 10276, ZUEC-LEP 10277, ZUEC-LEP10278, ZUEC-LEP 10279, ZUEC-LEP 10280, ZUEC-LEP 10281 (ZUEC), 1 male, 6.XI.1976, D. Gifford leg., DZ 35.033 (DZUP); São Gonçalo do Rio Preto – Parque Estadual do Rio Preto , 811 m, 1 male, 26.III.2015, I. Saraiva et al. leg. (ZUEC), 1 male, 27.V.2015 (PUC-MG), 1 male, 16.VII.2015 (ZUEC), 808 m, 2 males, 29.V.2015, I. Saraiva et al. leg. (PUC-MG), 899 m, 4 males, 16.VII.2015 (PUC-MG), 2 males, 18.VII.2015 (PUC-MG), 766 m, 3 males, 2 females, 19.VII.2015 (PUC-MG), 2 males, 19.IX.2015 (PUC-MG), 1 male, 20.IX.2015 (PUC-MG), 1 male, 28.V.2015 (PUC-MG), 1 male, 25.IX.2015 (PUC-MG), 1 male, 2 females, 23.II.2016 (PUC-MG), 1 male, 26.III.2016 (PUC-MG), 1 female, 19.IX.2016 (PUC-MG), 2 females, 25.XI.2016 (PUC-MG), 787 m, 1 male, 26.III.2016, I. Saraiva et al. leg. ZUEC-LEP 10016 (ZUEC), 899 m, 1 female, 16.VII.2015, I. Saraiva et al. leg. ZUEC-LEP 10017 (ZUEC), 801 m, 1 female, 28.VII.2016, Geanne leg., ZUEC-LEP 10571 (ZUEC), 904 m, 1 female, 29.VII.2016, Geanne leg., ZUEC-LEP 10572 (ZUEC), 914 m, 1 male, 27.VII.2016, Geanne leg., ZUEC-LEP 10573 (ZUEC), 752 m, 1 female, 27.VII.2016, Geanne leg., ZUEC-LEP 10574 (ZUEC), 882 m, 1 female, 27.VII.2016, Geanne leg., ZUEC-LEP 10575 (ZUEC); São João del Rei – Rio das Mortes , 800–1000 m, 1 (no abdomen), 16.IV.1955, H. Ebert leg., DZ 35.203 (DZUP); Santana do Riacho – Serra do Cipó, 1100 m, 1 male, 1 female, 7–10.V.2002, A. V. L. Freitas leg. (ZUEC-AVLF), APA Morro da Pedreira, 1 female, 14.IV.2012, 1 female, 24.X.2012, 1 male, 15.IV.2012, (DNA vouchers YPH-0572, YPH-0573, YPH-0574), M. Beirão leg., ZUEC-LEP 10010, ZUEC-LEP 10011*, ZUEC-LEP 10012* (ZUEC), 1 male, 08.III.2009, 1 male, 11.III.2009, Kaminski L.A. leg., ZUEC-LEP 10072, ZUEC-LEP 10074 (ZUEC); Santa Barbara – Serra do Caraça, 1300–1500 m, 1 male, 1–5-II-1985, Mielke & Casagrande leg., DZ 31806 (DZUP); Lagoa Santa : Serra do Cipó, 1000–1300 m, 1 female, 30-I-1985, Mielke & Casagrande leg., DZ 31.848 (DZUP); Cardeal Mota – Serra do Cipó, 19 ◦ 21 lS 43 ◦ 36 lW, 1 male, 07-XII-2005, Oliveira L. B. leg., ZUEC-LEP 10298 (ZUEC). São Paulo : Campo Alegre – Brotas, 750 m, 2 males, 1.V.1966, H. Ebert leg., DZ 35.223, DZ 35.263, 1 male, 21.V.1967, DZ 34.973 (DZUP); Santa Rita do Passa Quatro – Gleba Pé do Gigante, Parque Estadual da Vassununga, 21 ◦ 37 l 36.52 llS 47 ◦ 37 l 34.57 llW, 1 male, 1–3.V.2003, A.V.L. Freitas leg. (ZUEC-AVLF), 1 female, 1–3.V.2003, A.V.L. Freitas leg. (ZUEC), 1 female, IV.2003, A. V. L. Freitas leg., ZUEC-LEP 10265 (ZUEC), 1 female, IV.2003, (DNA Voucher YPH-0065), A.V.L. Freitas leg., ZUEC-LEP 10015 (ZUEC); Itirapina – Cerrado da Graúna, 1 female, 13.VIII.2010, D.G.M. Silva leg., (DNA voucher MGCL-LOAN-150) (ZUEC), 1 male, 31.VIII.2010, D.G.M. Silva leg., (DNA voucher MGCL-LOAN-134) (ZUEC).

Additional examined material. Minas Gerais: Santana do Riacho – Serra do Cipó, 1 female, 11.III.2009, Kaminski L.A. leg., ZUEC-LEP 10075 ( ZUEC); Belo Horizonte – Área de Proteção Especial Manancial Cercadinho , 19 ◦ 58 l 18.4 llS 43 ◦ 54 l 30 llW, 2007, 1 male, 8 females, Silva A.R.M. leg., ZUEC-LEP 10087, ZUEC-LEP 10083, ZUEC-LEP 10085, ZUEC-LEP 10086, ZUEC-LEP 10088, ZUEC-LEP 10089, ZUEC-LEP 10090, ZUEC-LEP 10091, ZUEC-LEP 10092 ( ZUEC) .

Figures

Fig. 1. Nhambikuara cerradensis gen. et sp. nov. A – holotype male, dorsal; B – holotype male, ventral; C – allotype female, dorsal; D – allotype female, ventral.

Fig. 2. Nhambikuara cerradensis gen. et sp. nov., male (YPH-0574) and female (DZ 33.900) genitalia. A – male lateral; B – male dorsal; C – male ventral; D – male aedeagus, lateral; E – male aedeagus, dorsal; F – female lateral; G – female ventral. Abbreviations: sa – saccus; te – tegumen; un – uncus; va – valva; gn – gnathos; ae – aedeagus; co – cornuti; bu – bursae coppulatrix; db – ductus bursae; pa – papilla anallis; st – sterigma; sg – signa.

Fig. 5. Natural habitats of Nhambikuara cerradensis gen. et sp. nov. in the Cerrado: A – Itirapina, São Paulo; B – Brasília, Distrito Federal and Nhambikuara mima comb. nov.: C – Sirinhaém, Pernambuco; D – an individual in its natural habitat in Guiana, Surama, north Rupuruni (Photo:David Geale).