Artículo

Checklist of butterflies from the rupestrian grasslands of Serra do Cipó, Minas Gerais, Brazil (Lepidoptera: Papilionoidea)

Levantamento de borboletas dos campos rupestres da Serra do Cipó, Minas Gerais, Brasil (Lepidoptera: Papilionoidea)

Listado de mariposas de los campos rurales de la Serra do Cipó, Minas Gerais, Brasil (Lepidoptera: Papilionoidea)

A. C. V. Pires
Universidade Federal de Minas Gerais, Brazil
M. V. Beirão
Universidade Federal de Minas Gerais, Brazil
G. W. Fernandes
Stanford University, USA
I. F. Oliveira
Universidade Federal do Rio Grande do Norte, Brazil
G. C. N. Pereira
Universidade Federal de Minas Gerais, Brazil
V. D. Silva
Centro Universitário Uma, Brazil
O. H. H. Mielke
Universidade Federal do Paraná, Brazil
M. Duarte
Universidade de São Paulo, Brazil

Checklist of butterflies from the rupestrian grasslands of Serra do Cipó, Minas Gerais, Brazil (Lepidoptera: Papilionoidea)

SHILAP Revista de Lepidopterología, vol. 46, no. 181, pp. 5-17, 2018

Sociedad Hispano-Luso-Americana de Lepidopterología

Received: 05 December 2016

Accepted: 02 February 2017

Abstract: The aim of this study is to provide a list of the butterflies (Lepidoptera: Papilionoidea) that occur in the rupestrian grasslands of Serra do Cipó, Minas Gerais, Brazil. Butterflies were sampled using VSR traps and entomological nets in seven undisturbed plots between 800 and 1400m above sea level. We collected 1,520 individuals belonging to 172 species. Among these species, four are on the Brazilian list of endangered species: Cunizza hirlanda planasia (Stoll, 1790), Magnastigma julia Nicolay, 1977, Strymon ohausi (Spitz, 1933) and Rhetus belphegor (Westwood, 1851).

KEY WORDS: Lepidoptera, Papilionoidea, conservation, threatened species, inventory, Brasil.

Resumo: O objetivo desse estudo é fornecer uma lista de borboletas (Lepidoptera: Papilionoidea) que ocorrem nos campos rupestres da Serra do Cipó, Minas Gerais, Brasil. As borboletas foram coletadas utilizando a armadilha VSR e rede entomológica em sete áreas não perturbadas entre 800 e 1400 metros de altitude. Coletamos 1520 indivíduos pertencentes a 172 espécies. Entre as espécies coletadas, quatro constam na lista nacional oficial de espécies da fauna ameaçadas de extinção: Cunizza hirlanda planasia (Stoll, 1790), Magnastigma julia Nicolay, 1977, Strymon ohausi (Spitz, 1933) and Rhetus belphegor (Westwood, 1851).

PALAVRAS CHAVE: Lepidoptera, Papilionoidea, conservação, espécies ameaçadas, levantamento, Brasil.

Resumen: El objetivo de este estudio es proveer una lista de mariposas (Lepidoptera: Papilionoidea) que se encuentran en las praderas herbáceas de la Serra do Cipó, Minas Gerais, Brasil. Las mariposas fueron colectadas usando trampas VSR y red entomológica en siete áreas no perturbadas entre los 800 y 1.400 metros de altitud. Colectamos 1.520 individuos pertenecientes a 172 especies. Entre estas especies, cuatro de ellas figuran en la lista brasileña de especies amenazadas: Cunizza hirlanda planasia (Stoll, 1790), Magnastigma julia Nicolay, 1977, Strymon ohausi (Spitz, 1933) y Rhetus belphegor (Westwood, 1851).

PALABRAS CLAVE: Lepidoptera, Papilionoidea, conservación, especies amenazadas, inventario, Brasil.

Introduction

The Cerrado (savanna-like vegetation) is one of the most threatened ecosystem due to urban expansion, agriculture, fire, afforestation, extraction of ornamental species, mining and road construction (BARBOSA et al., 2010; RIBEIRO & FREITAS, 2010; NEGREIROS et al., 2011; FERNANDES et al., 2014). The Espinhaço range comprises a group of mountains between the municipality of Ouro Branco (MG) and the southern part of the state of Bahia (Chapada de Diamantina), and extends for approximately 1200 km, with elevations greater than 800 m a.s.l.. Serra do Cipó is located in the southern part of the Espinhaço range, where there is a predominance of a complex ecosystem called the Rupestrian Grassland (FERNANDES, 2016; GIULIETTI, 1987). The plant species of this ecosystem have striking morpho-anatomical peculiarities that comprise a flora with high degree of morphological and behavioral convergence, diversity, and endemism (FERNANDES, 2016; ECHTERNAACHT et al., 2011; RAPINI et al., 2008; NEGREIROS et al., 2014).

Butterflies have been considered one of the best flagship species for conservation because most species are conspicuous and colorful (NEW, 1997). Other reasons that make butterflies Good environmental indicators are: short lifespan, diurnal habits, high diversity, easy sampling, identification and relatively well known taxonomy (BROWN & FREITAS, 1999; BHARDWAJ et al., 2012). Butterflies are involved in many ecological interactions, have close relationships with plants, and have been used as models in ecological and evolutionary studies. Butterflies are also used in many studies for habitat conservation because they are especially vulnerable to landscape and habitat fragmentation and loss, responding quickly to changes in vegetation and climate (BROWN & FREITAS, 1999; ROY & SPARKS, 2000).

A species checklist is of fundamental importance for conservation plans and environmental monitoring methods (MIELKE et al., 2008). The recognition of endemisms and local rarities are also important criteria to determine which areas have conservation potential (ROMERO & NAKAJIMA, 1999). Among the threatened Brazilian Lepidoptera, Rhetus belphegor (Westwood, 1851) (Riodinidae: Riodininae) is the only species recorded from Serra do Cipó (BROWN, 1993; MACHADO et al., 2008; NASCIMENTO & CAMPOS, 2011). However, this may be due to the lack of studies on Lepidoptera in the entire region. We expect that the number of endangered and endemic species will rise as more studies are carried out. Furthermore, we expect that these studies will lead to a better understanding of the butterfly fauna composition on the unique environment of the rupestrian grasslands. The aim of this study was to report the first list of butterfly species of the rupestrian grasslands in Serra do Cipó, a region that has been intensely studied for other groups of organisms (e.g., galling insects: LARA et al., 2002; ants: ARAÚJO & FERNANDES, 2003; freefeeding herbivores: RIBEIRO et al., 1998).

Materials and Methods

STUDY AREA

Serra do Cipó has a humid, subtropical climate with a dry winter and a temperate summer (Cwb in Köppen’s classification) (ALVARES et al., 2013), with mean temperatures between 17.4 and 19.8º C. The annual precipitation is about 1500 mm, with a wet season from November to January, a transitional period from February to April, and a dry season from May to September followed by another transitional post-dry period in October (MADEIRA & FERNANDES, 1999). The soil of Serra do Cipó is sandy, shallow, extremely oligotrophic and with high concentrations of aluminum and low capacity for water retention, (NEGREIROS et al., 2008; NEGREIROS et al., 2011). The study plots were located inside the National Park of Serra do Cipó and the Environmental Protection Area Morro da Pedreira, in the district of Serra do Cipó, Minas Gerais, Brazil (Fig. 1).

Map of Serra do Cipó with Parque Nacional da Serra do Cipó and Área de Proteção Morro da Pedreira limits, the sampling sites (black dots), other butterfly surveys in Minas Gerais (red dots) and the altitudinal gradient between 0 and 2000 m a.s.l.
Fig. 1
Map of Serra do Cipó with Parque Nacional da Serra do Cipó and Área de Proteção Morro da Pedreira limits, the sampling sites (black dots), other butterfly surveys in Minas Gerais (red dots) and the altitudinal gradient between 0 and 2000 m a.s.l.

SAMPLING

Butterflies were recorded in seven plots between 800 and 1400 m a.s.l.. In each plot three transects separated by 500m were sampled, for a total of 21 transects for the whole collecting area. Butterflies were sampled using both nets and traps. For sampling butterflies using nets, each transect was 250 m in length. Sampling employed two well-trained researchers sampling for two consecutive hours. Sampling took place 3 times during the day: soon after sun rise (at 08:00 am- 10:00 am), in the heat of the day (11:00 am-1:00 pm) and just before sun set (2:00 pm-4:00 pm). For sampling butterflies using traps, four Van Someren-Rydon (VSR) traps were placed in each transect separated by a distance of 50 m. Traps were baited with a mixture of banana and sugar cane that had been fermented for 48 hs. Traps were set on the first day while the next three days were reserved for daily butterfly collection at all traps.

Sampled individuals were immediately sacrificed and placed in entomological envelopes. Each envelope included the date, time of sampling (in case of net study), sampling point, trap number (for trap sampling) and the name of the collector. In the laboratory, the butterflies were identified using available field guides (D’ABRERA, 1981, 1984, 1987, 1994, 1995; CANALS, 2003; UEHARA-PRADO et al., 2004; SILVA et al., 2010) and the specimen collections of the Campinas University (Unicamp), Zoological Museum of São Paulo University (MZUSP), and Coleção Entomológica Pe. Jesus Santiago Moure at Paraná University (UFPR). Classification followed LAMAS (2004) and subsequent revisions (MIELKE, 2005; WAHLBERG et al., 2009; DUARTE & ROBBINS, 2010; WARREN et al., 2013). Sampling occurred in January, April, July and October 2012, and January, May, August and October 2013, encompassing the times of the year with the greatest differences in weather conditions (MADEIRA & FERNANDES, 1999).

ACCUMULATION CURVES

We constructed two accumulation curves, one for each method (entomological net and trap), in order to evaluate the sampling efficiency of both methods. Species curves were constructed using the Vegan package (2.2-1 version) (OKSANEN et al., 2015) in the R program environment (R CORE TEAM, 2015).

Results

Total butterfly sampling effort was 336 net hours and 252 trap days. The traps sampled only four subfamilies (Biblidinae, Charaxinae, Satyrinae and the satyroid lineage of the subfamily Nymphalinae) of the family Nymphalidae (DEVRIES et al., 2001; FREITAS & BROWN, 2004). We recorded 1,520 individual butterflies of 172 species belonging to 17 subfamilies (Table I). Six butterfly families were recorded and the number of species per family was: 59 species of Hesperiidae, 28 of Lycaenidae, 54 of Nymphalidae, 5 of Papilionidae, 12 of Pieridae, and 14 of Riodinidae. The most common species were Paryphthimoides sp2 (Nymphalidae) (N=135), Eurema elathea flavescens (Chavannes, 1850) (Pieridae: Coliadinae) (N=125), Hemiargus hanno (Stoll, 1790) (Lycaenidae: Polyommatinae) (N=122), Yphthimoides manasses (C. Felder & R. Felder, 1867) (Nymphalidae: Satyrinae) (N=92), and Pyrisitia nise tenella (Boisduval, 1836)(Pieridae: Coliadinae) (N=75). Together, these five species, represented 36% of the total sample. We recorded 71 (41%) species with only one capture (singletons). Only four species occurred in all seven studied areas: Hemiargus hanno, Junonia evarete (Cramer, 1779) (Nymphalidae: Nymphalinae), Eurema elathea flavescens (Chavannes, 1850) and Phoebis sennae marcellina (Cramer, 1777) (Pieridae: Coliadinae). One new species was found in this study: Paryphthimoides sp. 2 (Nymphalidae) (A. V. L. Freitas personal observation) was found between 800 and 1400 m a.s.l. The new species is deposited in Campinas University (Unicamp) museum. Some specimens cannot be identified at species level due to the damage suffered during the sampling or because of the wing scale loss that occurs naturally throughout the insect’s life. Others belong to a poorly studied butterfly group, the Satyrinae, which has many species with uncertain taxonomic position.

The accumulation curve for sampling by net butterfly richness per family did not indicate a tendency to asymptote. Although our sampling effort was similar to other studies in non-forest ecosystems (e.g. CARNEIRO et al., 2014; CARVALHO et al., 2015; MARCHIORI & ROMANOWSKI, 2006), the area studied showed a high richness of butterflies, indicating that we might be able to discover more butterfly species if more localities are sampled. The accumulation curve for sampling by trap exhibited a tendency towards asymptote (Fig. 2).

Accumulation curves for species of butterflies in Serra do Cipó (MG, Brazil). The gray curve is net sampling while the black curve is trap sampling.
Fig. 2
Accumulation curves for species of butterflies in Serra do Cipó (MG, Brazil). The gray curve is net sampling while the black curve is trap sampling.

Discussion

The number of species found in this study is similar to that found by other surveys of grassland habitats in Brazil (ISERHARD et al., 2010; DOLIBAINA et al., 2011; CARNEIRO et al., 2014; CARVALHO et al., 2015), but is lower than that of other types of locations, such as the Atlantic rain forest (652 species: BROWN, 1992) and Cerrado (839 species: MIELKE et al., 2008). However, in addition to the need for further sampling, as indicated by the accumulation curve, our study was restricted to a single area that was smaller than the areas in the other studies.

Among the sampled species, 107 (62.2%) are considered typical of open environments or have been recorded in other grassland environments (MIELKE et al., 2008; ISERHARD et al., 2010; DOLIBAINA et al., 2011; CARVALHO et al., 2015; BROWN, 1992; CALLAGHAN, 1982; KAMINSKI et al., 2015; MARCHIORI & ROMANOWSKI, 2006; KAMINSKI et al., 2012; KAMINSKI & CARVALHO-FILHO, 2012; PAZ et al., 2013; FREITAS & MARINI-FILHO, 2011; GOZZI et al., 2012; SILVA et al., 2015). Only 25 (14.5%) of the species found in this study had been previously recorded in the only other study done in the Espinhaço mountain range (NERY et al., 2014) (Table 1).

Table I
List of butterfly species from Serra do Cipó (MG, Brazil). S = number of species, * = registered species of nearby region [53] and + = species found in other grasslands.
Species AbundanceSpecies Abundance
Hesperiidae (S= 59)Chalcone sp. 6
Eudaminae (S= 14)Conga chydaea (Butler, 1877) + 1
Chioides catillus (Cramer, 1779) + 11Conga urqua (Weeks, 1909) + 23
Cogia azila Evans, 1953 3Copaeodes jean favor Evans, 1955 + 2
Cogia calchas (Herrich-Schäffer, 1869) 6Cumbre sp. 2
Cogia hassan evansi Bell, 1937 20Cymaenes warreni (Weeks, 1901) 2
Epargyreus sp. 2Euphyes eberti Mielke, 1972 6
Phocides polybius phanias (Burmeister, 1880) + 2Euphyes sp. 1
Typhedanus undulatus (Hewitson, 1867) + 2Hylephila phyleus (Drury, 1773) + 5
Udranomia spitzi Hayward, 1942 + 14Hylephila sp. 1
Urbanus carmelita barra Evans, 1952 2Lerema caraca Mielke, 1992 3
Urbanus cindra Evans, 1952 + 11Lerema veadeira Mielke, 1968 + 1
Urbanus dorantes (Stoll, 1790) + 2Lerodea erythrostictus (Prittwitz, 1868) + 1
Urbanus evenus (Ménétriès, 1855) + 5Lerodea eufala (Edwards, 1869) + 1
Urbanus procne (Plötz, 1881) + 2Nastra tanta Evans, 1955 + 1
Urbanus simplicius (Stoll, 1790) + 1Panoquina bola Bell, 1942 + 4
Hesperiinae (S= 30)Panoquina peraea (Hewitson, 1866) 7
Chalcone briquenydan (Weeks, 1901) + 2Polites vibex catilina (Plötz, 1886) + 2
Species AbundanceSpecies Abundance
Pompeius dares Plötz, (1883) + 1Rubroserrata ecbatana (Hewitson, 1868) 1
Quasimellana mielkei Burns, 1994 7Strymon cestri (Reakirt, [1867]) + 1
Synale metella (Plötz, 1882) + 1Strymon cyanofusca Johnson, Eisele & MacPherson,
Thespieus homochromus Mielke, 1978 51990 1
Vehilius inca (Scudder, 1872) + 5Strymon mulucha (Hewitson, 1867) 3
Vettius lucretius (Latreille, 1824) + 1Strymon ohausi (Spitz, 1933) 15
Vidius nostra nostra Evans, 1955 + 3Strymon oreala (Hewitson, 1868) + 2
Vidius similis Mielke, 1980 + 3Thereus sp. 1
Vidius sp. 8Theritas triquetra (Hewitson, 1865) + 1
Wallengrenia premnas (Wallengren, 1860) + 1Nymphalidae (S= 54)
Xeniades chalestra Hewiston, 1866 + 1Biblidinae (S= 10)
Pyrginae (S= 14)Biblis hyperia (Cramer, 1779) *+ 1
Chiomara basigutta Plötz, 1884 + 27Callicore astarte (Cramer, 1779) *+ 1
Elbella intersecta losca Evans, 1951+ 1Callicore sorana (Godart, [1824]) *+ 43
Elbella luteizona (Mabille, 1877) + 2Eunica cuvierii (Godart, 1819) *+ 12
Gesta gesta Prittwitz, 1868 + 1Eunica tatila (Herrich-Schäffer, [1855]) *+ 12
Gesta heteropterus (Plötz, 1884) + 1Hamadryas amphinome (Linnaeus, 1767) *+ 2
Gorgythion sp. 4Hamadryas februa (Hübner, [1823]) *+ 2
Heliopetes arsalte (Billberg, 1820) + 8Hamadryas feronia (Linnaeus, 1758) *+ 6
Heliopetes macaira orbigera (Mabille, 1888) + 7Temenis laothoe (Cramer, 1777) *+ 1
Heliopetes omrina (Butler, 1870) *+ 16Nica flavilla (Godart, [1824]) 1
Pyrgus orcus (Stoll, 1780) *+ 30Charaxinae (S= 3)
Pyrrhopyge amythaon Bell, 1931 1Memphis moruus (Fabricius, 1775) *+ 3
Sophista latifasciata (Spitz, 1930) + 3Siderone galanthis (Cramer, 1775) *+ 3
Timochreon doria (Plötz, 1884) 1Zaretis strigosus (Gmelin, [1790]) + 1
Viola violella (Mabille, 1897) + 5Danainae (S= 2)
Zopyrion evenor Godman & Salvin, 1901 + 5Danaus gilippus (Bates, 1863) + 9
Lycaenidae (S= 28)Danaus plexippus (Linnaeus, 1758) 1
Lycaeninae (S= 1)Heliconiinae (S= 3)
Arcas ducalis (Westwood, 1852) + 1Heliconius besckei (Ménétriés, 1857) * 1
Polyommatinae (S= 2)Heliconius erato phyllis (Fabricius, 1775) *+ 4
Hemiargus hanno (Stoll, 1790) + 124Heliconius ethilla nacarea (Godart, 1819) *+ 1
Leptotes cassius (Cramer, 1775) * 32Ithomiinae (S= 1)
Theclinae (S= 25)Placidina euryanassa (Felder & Felder, 1860) 1
Allosmaitia strophius (Godart, [1824]) 4Nymphalinae (S= 10)
Arawacus tarania (Hewitson, 1868) 2Anartia jatrophae (Linnaeus, 1763) + 2
Badecla badaca (Hewitson, 1868) 10Colobura dirce (Linnaeus, 1758) *+ 1
Calycopis caulonia (Hewitson, 1877) + 1Eresia lansdorfi (Godart, 1819) *+ 1
Calycopis janeirica (Felder, 1862) 1Euptoieta hegesia meridiania Stichel, 1938 3
Chlorostrymon telea (Hewitson, 1868) 2Junonia evarete (Cramer, 1779) *+ 43
Cyanophrys herodotus (Fabricius, 1793) 1Smyrna blomfildia (Fabricius, 1781) *+ 1
Evenus regalis (Cramer, 1775) 1Tegosa claudina (Eschscholtz, 1821) + 2
Gargina gargophia (Hewitson, 1877) 1Vanessa braziliensis (Moore, 1883) + 11
Magnastigma julia Nicolay, 1977 + 4Vanessa myrinna (Doubleday, 1849) + 7
Michaelus thordesa (Hewitson, 1867) 1Satyrinae (S= 25)
Nicolaea schausa (E. Jones, 1912) 3Caligo brasiliensis (Felder, 1862) + 2
Nicolaea socia (Hewitson, 1868) 2Cissia sp.1 6
Nicolaea sp. 1Eryphanis automedon (Cramer, 1775) 2
Ocaria ocrisia (Hewitson, 1868) 1Guaianaza pronophila (Butler, 1870)* 1
Pseudolycaena marsyas (Linnaeus, 1758) *+ 1Forsterinaria quantius (Godart, [1824])*+ 4
Rekoa marius (Lucas, 1857) 1Godartiana muscosa (Butler, 1870) *+ 3
Species AbundanceSpecies Abundance
Hermeuptychia atalanta (Butler, 1867) + 1Aphrissa statira (Cramer, 1777) + 1
Hermeuptychia maimoune (Butler, 1870) 1Eurema albula (Cramer, 1775) *+ 1
Moneuptychia itapeva (Freitas, 2007) *+ 14Eurema elathea flavescens (Chavannes, 1850) *+ 125
Moneuptychia soter (Butler, 1877) *+ 2Eurema phiale paula (Röber, 1909) *+ 3
Morpho helenor mielkei Blandin, 2007 *+ 11Phoebis sennae marcellina (Cramer, 1777) + 28
Opsiphanes invirae (Hübner, [1808]) *+ 3Pyrisitia leuce (Boisduval, 1836) + 5
Paryphthimoides melobosis (Capronnier, 1874) 41Pyrisitia nise tenella (Boisduval, 1836) + 75
Paryphthimoides phronius (Godart, [1824]) *+ 5Pierinae (S= 4)
Paryphthimoides poltys (Prittwitz, 1865) *+ 7Ascia monuste orseis (Godart, [1819]) *+ 1
Paryphthimoides sp.1 135Cunizza hirlanda planasia Fruhstorfer, 1910 + 1
Paryphthimoides sp.2 21Glutophrissa drusilla (Cramer, 1777) + 3
Pharneuptychia phares (Godart, [1824]) 2Hesperocharis anguitia (Godart, 1819) 2
Taygetina kerea (Butler, 1869) + 2Riodinidae (S= 15)
Taygetis laches (Fabricius, 1793) *+ 6Riodininae (S= 15)
Yphthimoides affinis (Butler, 1867) *+ 24Anteros lectabilis Stichel, 1909 + 1
Yphthimoides patricia (Hayward, 1957) 92Ariconias glaphyra (Westwood, 1851) 28
Yphthimoides ochracea (Butler, 1867) *+ 2Aricoris pasquita (Stichel 1910) 1
Yphthimoides renata (Stoll, 1780) *+ 4Aricoris propitia (Stichel, 1910) + 48
Yphthimoides sp.1 6Aricoris tutana (Godart, [1824]) + 12
Papilionidae (S= 5)Baeotis johannae Sharpe, 1890 8
Papilioninae (S= 5)Chalodeta theodora (Felder & Felder, 1862) 1
Battus polydamas (Linnaeus, 1758) + 1Dachetola azora (Godart, [1824]) + 4
Heraclides thoas brasiliensis (Rothschild &Emesis diogenia Prittwitz, 1865 13
Jordan, 1906) + 1Lemonias stalachtioides (Butler, 1867) 4
Parides anchises (Linnaeus, 1758) + 1Lyropteryx terpsichore Westwood, 1851 3
Parides bunichus diodorus (Hopffer,, 1865) + 37Rhetus belphegor (Westwood, 1851) + 3
Parides neophilus eurybates (Gray, [1853]) 1Stichelia bocchoris (Hewitson, 1876) 5
Pieridae (S= 12)Synargis axenus (Hewitson, 1876) + 7
Coliadinae (S= 8)Synargis calyce (Felder & Felder, 1862) 1
Anteos clorinde (Godart, [1824]) 1

Table I (Cont.)
List of butterfly species from Serra do Cipó (MG, Brazil). S = number of species, * = registered species of nearby region [53] and + = species found in other grasslands.
List of butterfly species from Serra do Cipó (MG, Brazil). S = number of species, * = registered species of nearby region [53] and + = species found in other grasslands.

Table I(Cont.)
List of butterfly species from Serra do Cipó (MG, Brazil). S = number of species, * = registered species of nearby region [53] and + = species found in other grasslands.
List of butterfly species from Serra do Cipó (MG, Brazil). S = number of species, * = registered species of nearby region [53] and + = species found in other grasslands.

The most abundant and species rich families were Hesperiidae (over one third of all collected species, 33.7%) and Nymphalidae (31.9%). These are the most species rich butterfly families in the Neotropics (LAMAS, 2004). They are also known to have a positive association with monocotyledons during their early life stage (DEVRIES, 1985; FERRER-PARIS et al., 2013), and since monocotyledons are dominant in the rupestrian grasslands of Serra do Cipó (RAPINI et al., 2008), they likely contribute to the wide distribution of these butterfly taxa. The most abundant butterfly species was a new species of Paryphthimoides, indicating the need for more inventories in the region of Serra do Cipó. The other abundant butterfly species in this study are known to be common in open, grassland, ruderal or even in disturbed areas (BROWN, 1992). The species that were found at all of the sampling points of this study have wide distributions and occur in many regions of Brazil (MOTTA, 2002).

In comparison to other surveys in Minas Gerais, the present study was fourth in the total number of butterfly species encountered, behind studies in Poços de Caldas (EBERT, 1969), São Francisco River (SOARES et al., 1999) and Uberlândia (MOTTA, 2002) (see Table II). Of all the species collected by us, 61 had not been previously recorded for Minas Gerais, with 32 (52.4%) species of Hesperiidae, 14 (22.9%) species of Lycaenidae, 22 (36%) species of Nymphalidae, 2 (3.2%) species of Pieridae, and 10 (16.4%) species of Riodinidae. Therefore, this study greatly expands knowledge of the butterfly fauna of Minas Gerais.

Butterflies of tropical mountains remain poorly known, which makes it difficult to recognize and determine the conservation and endemic status of these major taxa of herbivores. For example, the species Arcas ducalis (Westwood, 1852) (Lycaenidae: Theclinae), which was found in our study, was previously known to be restricted to mountaintop environments with preserved vegetation in southern and southeastern Brazil (NICOLAY, 1971; BROWN, 1992; BROWN, 1993).

Table II
Comparison of butterfly surveys in Minas Gerais, Brazil. * = studies with only fruit feeding butterflies (Nymphalidae)
Comparison of butterfly surveys in Minas Gerais, Brazil. * = studies with only fruit feeding butterflies (Nymphalidae)

This species is considered endangered in the states of São Paulo, Rio de Janeiro, and Espírito Santos (BROWN & FREITAS, 1999; OTERO et al., 2000; AZEVEDO et al., 2007). Another example is R. belphegor, with three individuals collected in one plot at 1300 m a.s.l. in the present study. This species is on the Brazilian red list of threatened species (MMA, 2014) and is classified as Endangered (EN) by the International Union for Conservation of Nature (IUCN). Another species reported here, M. julia and Strymon ohausi, both belonging to family Lycaenidae, are also classified as Endangered (EN) by the IUCN (FREITAS & MARINI-FILHO, 2011; MMA, 2014). Cunizza hirlanda planasia (Pieridae: Pierinae) is another species on the national red list of threatened species (MMA, 2014), and is listed as Vulnerable (VU) indicating that more information about its biology and distribution are required. This was the first record of M. julia, S. ohausi and C. hirlanda planasia in Serra do Cipó, all sampled outside the Serra do Cipó National Park (a full protection conservation unit); however, they were found in Morro da Pedreira Environmental Protection Area (a sustainable use conservation unit). Our record on the distribution of Hermeuptychia atalanta (Butler, 1867) (Nymphalidae: Satyrinae) represents a newrecord for southeastern Brazil (SERAPHIM et al., 2014).

Conclusión

Results have shown that rupestrian grasslands host a great diversity of butterflies, including species listed as endangered. Because it is a montane environment, particularly exposed to the consequences of global warming, conservationist efforts are needed in order to protect the integrity of this unique ecosystem.

Acknowledgments

We thank André Vitor Lucci Freitas, Diego Dolibaina and Fernando Dias for butterfly species identifications, Parque Nacional da Serra do Cipó, Pousada Serra Morena, Cedro Cachoeira Indústria Têxtil, Reserva Vellozia and Pousada Pedra do Elefante for logistic support. Instituto Chico Mendes license number 23234-3. We acknowledge the support provided by CNPq, and FAPEMIG. MD has been supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP grants 2002/13898-0, 2010/14682-8), and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq grants 563332/2010-7, 305905/2012-0). This is the contribution #074 of the PELD-CRSC-17.

BIBLIOGRAPHY

ALVARES, C. A., STAPE, J. L., SENTELHAS, P. C., GONÇALVES, J. L. M. & SPAROVEK, G., 2013.- Köppen’s climate classification map for Brazil.- Meteorologische Zeitschrift, 22: 711-728.

ARAÚJO, L. M. & FERNANDES, G. W., 2003.- Altitudinal patterns in a tropical ant assemblage and variation in species richness between habitats.- Lundiana, 4: 103-109.

ARAÚJO, M. C. & PAPROCKI, H., 2015.- Lista de Lepidoptera do Parque Ecológico Felisberto Neves, Betim, Minas Gerais.- Sinapse Múltipla, 4: 1-15.

AZEVEDO, C. O., VAZ-DE-MELLO, F. Z., TAVARES, M. T., BRESCOVIT, A. D., MARCO JUNIOR, P., FURIERI, K. S., BROWN JR, K. S. & FREITAS, A. V. L., 2007.- Os invertebrados terrestres ameaçados de extinção no estado do Espírito Santo.- In M. PASSAMANI & S. L. MENDES (org). Espécies da fauna ameaçadas de extinção no Estado do Espírito Santo: 105-120. Instituto de Pesquisas da Mata Atlântica, Vitória.

BARBOSA, N. P. U., FERNANDES, G. W., CARNEIRO, M. A. A. & JÚNIOR, L. A. C., 2010.- Distribution of non-native invasive species and soil properties in proximity to paved roads and unpaved roads in a quartzitic mountainous grassland of southeastern Brazil (rupestrian fields).- Biological Invasions, 12: 3745-3755.

BHARDWAJ, M., UNIYAL, V. P., SANYAL, A. K. & SINGH, A. P., 2012.- Butterfly communities along an elevational gradient in the Tons valley, Western Himalayas: Implications of rapid assessment for insect conservation.- Journal of Asia-Pacific Entomology, 15: 207-217.

BROWN JR, K. S., 1992.- Borboletas da Serra do Japi: diversidade, habitats, recursos alimentares e variação temporal.- In L. P. C. MORELLATO (ed). História Natural da Serra do Japi: ecologia e preservação de uma área florestal no Sudeste do Brasil: 142-187. Editora Unicamp, Campinas.

BROWN JR, K. S., 1993.- South America: Selected species.- In T. R. NEW (ed). Conservation Biology of Lycaenidae (Butterfly): 146-153. Information Press, Oxford.

BROWN JR, K. S. & FREITAS, A. V. L., 1999.-Lepidoptera.- InC. A. JOLY & C. E. M. BICUDO(eds.),Biodiversidade do Estado de São Paulo, Brasil: síntese do conhecimento ao final do século XXinvertebrados terrestres: 225-243. FAPESP, São Paulo.

CALLAGHAN, C. J., 1982.- A study of isolating mechanisms among Neotropical butterflies of the subfamily Riodininae.- Journal of Research on the Lepidoptera, 21: 159-176.

CANALS, G. R., 2003.- Butterflies of Missiones. Buenos Aires: 492 pp. L. O. L. A., Buenos Aires.

CARNEIRO, E., MIELKE, O. H. H., CASAGRANDE, M. M. & FIEDLER, K., 2014.- Skipper richness (Hesperiidae) along elevational gradients in Brazilian Atlantic Forest.- Neotropical Entomology, 43: 27-38.

CARVALHO, A. P. S., PIOVESAN, G. & MORAIS, A. B. B., 2015.- Butterflies (Lepidoptera: Papilionoidea) of grassland areas in the Pampa biome, southern Brazil.- Checklist, 11: 1-6.

D’ABRERA, B., 1981.- Butterflies of the Neotropical region. Part I Papilionidae & Pieridae: 188 pp. Hill House, Victoria.

D’ABRERA, B., 1984.- Butterflies of the Neotropical region. Part II Danaidae, Ithomiidae, Heliconidae & Morphidae: 223 pp. Hill House, Victoria.

D’ABRERA, B., 1994.-Butterflies of the Neotropical region. Part VI Riodinidae: 216pp.Hill House, Victoria.

D’ABRERA, B., 1995.-Butterflies of the Neotropical region. Part VII Lycaenidae: 183pp.Hill House, Victoria.

DEVRIES, P. J., 1985.-Hostplant records and natural history on Costa Rican butterflies (Papilionidae, Pieridae e Nymphalidae).-The Journal of Research on the Lepidoptera, 24: 290-333.

DEVRIES, P. J., 1987.- The Butterflies of Costa Rica and their natural history. Volume I: Papilionidae, Pieridae and Nymphalidae: 327 pp. Princeton University, New Jersey.

DEVRIES, P. J. & WALLA, T. R. 2001.- Species diversity and community structure in Neotropical fruit-feedingbutterflies.- Biological Journal of the Linnean Society, 74: 1-15.

DOLIBAINA, D. R., MIELKE, O. H. H. & CASAGRANDE, M. M., 2011.- Borboletas (Papilionoidea e Hesperioidea) de Guarapuava e arredores, Paraná, Brasil: um inventário com base em 63 anos de registros.- Biota Neotropica, 11: 341-354.

DUARTE, M. & ROBBINS, R. K., 2010.- Description and phylogenetic analysis of the Calycopidina (Lepidoptera, Lycaenidae, Theclinae, Eumaeini): a subtribe of detritivores.- Revista Brasileira de Entomologia, 54: 45-65.

EBERT, H., 1969. -On the frequency of butterflies in eastern Brazil, with a list of the butterfly fauna of Poços de Caldas, Minas Gerais.- Journal of the Lepidopterists’ Society, 23: 1-48.

ECHTERNACHT, L., TROVÓ, M., OLIVEIRA, C. T. & PIRANI, J. R., 2011.- Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil.- Flora, 206: 782-791.

FERNANDES, G. W., 2016.- Ecology and conservation of mountaintop grasslands in Brazil: 567 pp. Springer International Publishing.

FERNANDES, G. W., BARBOSA, N. P. U., NEGREIROS, D. & PAGLIA, A. P., 2014. Challenges for the conservation of vanishing megadiverse rupestrian grasslands.- Natureza & Conservação, 12: 162-165.

FERRER-PARIS, J. R., SÁNCHEZ-MERCADO, A., VILORIA, A. L. & DONALDSON, J., 2013.- Congruence and diversity of butterfly-host plant associations at higher taxonomic levels.- PlosOne, 8: 1-15.

FREITAS, A. V. L. & BROWN JR, K. S., 2004.- Phylogeny of the Nymphalidae.- Systematic Biology, 53: 363-383.

FREITAS, A. V. L. & MARINI-FILHO, O. J., 2011.- Plano de ação nacional para a conservação dos lepidópteros: 124 pp. Série Espécies Ameaçadas, 13. Instituto Chico Mendes de Conservação da Biodiversidade, ICMBio, Brasilia.

GIULIETTI, A. M., MENEZES, N. L., PIRANI, J. R., MEGURO, M. & WANDERLEY, M. G. L. 1987.- Flora da Serra do Cipó, Minas Gerais: caracterização e lista das espécies.- Boletim de Botânica da Universidade de São Paulo, 9: 1-151.

GOZZI, M. R., BEIRÃO, M. V., MEDEIROS, L. R., NEVES, F. S. & FAGUNDES, M., 2012.- Borboletas frugívoras em uma região de transição entre cerrado sensu stricto e caatinga no norte de Minas Gerais, Brasil.- MG Biota, 4: 25-37.

HALL, J. P. W., 2002.- A review of Chalodeta Stichel with a revision of the chelonis group (Lepidoptera: Riodinidae).- Proceedings of the Entomological Society of Washington, 104: 376-389.

ISERHARD, C. A., QUADROS, M. T., ROMANOWSKI, H. P. & MENDONÇA JR, M. S., 2010.- Borboletas (Lepidoptera: Papilionoidea e Hesperioidea) ocorrentes em diferentes ambientes na Floresta Ombrófila Mista e nos Campos de Cima da Serra do Rio Grande do Sul, Brasil.- Biota Neotropica, 10: 309-320.

KAMINSKI, L. A., SOARES, G. R., SERAPHIM, N., WAHLBERG, N., MARINI-FILHO, O. J. & FREITAS, A. V. L., 2015.- Natural history and systematic position of Rhetus belphegor (n. comb.) (Lepidoptera: Riodinidae), an endangered butterfly with narrow distribution in Southeast Brazil.- Journal of Insect Conservation, 19: 1141-1151.

KAMINSKI, L. A. & CARVALHO-FILHO, F. S., 2012.- Life history of Aricoris propitia (Lepidoptera: Riodinidae)-a myrmecophilous butterfly obligately associated with fire ants.- Psyche, 1: 1-10.

KAMINSKI, L. A., BARBOSA, E. P. & FREITAS, A. V. L., 2012.- Immature stages of the neotropical mistletoe butterfly Cunizza hirlanda planasia Fruhstorfer (Pieridae: Anthocharidini).- Journal of Lepidopterists’ Society, 66: 143-146.

LAMAS, G., 2004. -Checklist: Part 4A. Hesperioidea-Papilionoidea.- In J. B. HEPPNER (ed.). Atlas of Neotropical Lepidoptera 5A: 439 pp. Association for Tropical Lepidoptera, Gainesville.

LARA, A. C. F., FERNANDES, G. W. & GONÇALVES-ALVIM, S. J., 2002.- Tests of hypotheses on patterns of gall distribution along an altitudinal gradient.- Tropical Zoology, 15: 219-232.

MACHADO, A. B. M., DRUMMOND, G. M. & PAGLIA, A. P., 2008.- Livro Vermelho da Fauna Brasileira Ameaçada de Extinção, 1: 511 pp. Fundação Biodiversitas, Brasilia.

MADEIRA, J. A. & FERNANDES, G. W., 1999.- Reproductive phenology of sympatric species of Chamaecrista (Leguminosae) in Serra do Cipó, Brazil.- Journal of Tropical Ecology, 15: 463-479.

MARCHIORI, M. O. & ROMANOWSKI, H. P., 2006.- Borboletas (Lepidoptera, Papilionoidea e Hesperioidea) do Parque Estadual do Espinilho e entorno, Rio Grande do Sul, Brasil.- Revista Brasileira de Zoologia, 23: 1029-1037.

MIELKE, O. H. H., 2005.- Catalogue of the American Hesperioidea: Hesperiidae (Lepidoptera): 1536 pp. Sociedade Brasileira de Zoologia, Curitiba.

MIELKE, O. H. H., EMERY, E. O. & PINHEIRO, C. E. G., 2008.- As borboletas Hesperiidae (Lepidoptera, Hesperioidea) do Distrito Federal, Brasil.- Revista Brasileira de Entomologia, 52: 283-288.

MMA, 2014.- Portaria Nº 444, de 17 de dezembro de 2014. Diário Oficial da União, Brasília, DF. 18 dez. 2014. Seção 1, p. 121. Available from http://www.icmbio.gov.br/portal/images/stories/biodiversidade/faunabrasileira/ avaliacao-do-risco/PORTARIA_N%C2%BA_444_DE_17_DE_DEZEMBRO_DE_2014.pdf. (accessed 29 May 2015).

MOTTA, P. C., 2002.- Butterflies from the Uberlândia region, central Brazil: species list and biological comments.- Brazilian Journal of Biology, 62: 151-163.

NASCIMENTO, J. L. & CAMPOS, I. B., 2011.- Atlas da fauna brasileira ameaçada de extinção em unidades de conservação federais: 276 pp. Instituto Chico Mendes de Conservação da Biodiversidade, Brasilia.

NEGREIROS, D., FERNANDES, G. W., BERBARA, R. L. L., RODARTE, L. H. O. & BARBOSA, N. P. U., 2011.- Caracterização físico-química de solos quartzíticos degradados e áreas adjacentes de campo rupestre na Serra do Cipó, MG, Brasil.- Neotropical Biology and Conservation, 6: 156-161.

NEGREIROS, D., MORAES, M. L. B. & FERNANDES, G. W., 2008.- Caracterização da fertilidade dos solos de quatro leguminosas de campos rupestres, Serra do Cipó, MG, Brasil.- Journal of Plant Nutrition and Soil Science, 8: 30-39.

NEGREIROS, D., LESTRADIC, S., FERNANDES, G. W. & RENNÓ, H. C., 2014.- CSR analysis of plant functional types in highly diverse tropical grasslands of harsh environments.- Plant Ecology, 215: 379-388.

NERY, I., CARVALHO, N. & PAPROCKI, H., 2014.- Checklist of butterflies (Insecta: Lepidoptera) from Serra do Intendente State Park-Minas Gerais, Brazil.- Biodiversity Data Journal, 2: e3999. doi: 10.3897/BDJ.2.e3999

NEW, T. R., 1997.- Are Lepidoptera an effective “umbrella group” for biodiversity conservation?- Journal of Insect Conservation, 1: 5-12.

NICOLAY, S. S., 1971.-A review of the genus Arcas with descriptions of new species (Lycaenidae, Strymonini).-Journal of the Lepidopterist’s Society, 25: 87-108.

OKSANEN, J., BLANCHET, F. G., KINDT, R., LEGENDRE, P., MINCHIN, P. R., O’HARA, R. B., SIMPSON, G. L., SOLYMOS, P., STEVENS, M. H. H. & WAGNER, H., 2015.-Vegan: Community Ecology Package. R package version 2.3-4. Available from http://CRAN.R-project.org/package=vegan.

OTERO, L. S., BROWN JR., K. S., MIELKE, O. H. H., MONTEIRO, R. F., COSTA, J. M., MACEDO, M. V., MACIEL, N. C., BECKER, J., SALGADO, N. G., SANTOS, S. B., MOYA, G. E., ALMEIDA, J. M. & DUARTE, M., 2000.-Invertebrados terrestres.- InH. G. BERGALLO, C. F. D. ROCHA, M. A. S. ALVES & M. VANSLUYS(eds.).A fauna ameaçada de extinção do estado do Rio de Janeiro: 53-62. Editora da Universidade do Estado do Rio de Janeiro, Rio de Janeiro.

PAZ, A. L. G., ROMANOWSKI, H. P. & MORAIS, A. B. B., 2013.-Borboletas frugívoras do centro oeste do Rio Grande do Sul, Brasil (Lepidoptera: Nymphalidae).-SHILAP Revista de lepidopterología, 41: 1-14.

R CORE TEAM, 2015.- R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.R-project.org/.

RAPINI, A., RIBEIRO, P. L., LAMBERT, S. & PIRANI, J. B., 2008.- A flora dos campos rupestres da Cadeia do Espinhaço.- Megadiversidade, 4: 16-24.

RIBEIRO, K. T. & FREITAS, L., 2010.- Impactos potenciais das alterações no Código Florestal sobre a vegetação de campos rupestres e campos de altitude.- Biota Neotropica, 10: 239-246.

RIBEIRO, S. P., CARNEIRO, M. A. A. & FERNANDES, G. W., 1998.- Free-feeding insect herbivores along environmental gradients in Serra do Cipó: basis for a management plan.- Journal of Insect Conservation, 2: 1-12.

ROMERO, R. & NAKAJIMA, J. N., 1999.- Espécies endêmicas do Parque Nacional da Serra da Canastra, MG.- Revista Brasileira de Botânica, 22: 259-265.

ROY, D. B. & SPARKS, T. H., 2000.- Phenology of British butterflies and climate change.- Global Change Biology, 6: 407-416.

SERAPHIM, N., MARÍN, M. A., FREITAS, A. V. L. & SILVA-BRANDÃO, K. L., 2014.- Morphological and molecular marker contributions to disentangling the cryptic Hermeuptychia hermes species complex (Nymphalidae: Satyrinae: Euptychiina).- Molecular Ecology Resources, 14: 39-49.

SILVA, A. R. M., LANDA, G. G. & VITALINO, R. F., 2007.- Borboletas (Lepidoptera) de um fragmento de mata urbano em Minas Gerais, Brasil.- Lundiana, 8: 137-142.

SILVA, A. R. M., GUIMARÃES, M. P. M., VITALINO, R. F., BAGNI, A. S., MARTINS, Y. E., COREIRO, A. M. & OLIVEIRA, E. G., 2010.- Borboletas frugívoras do Parque Estadual do Rio Doce, MG.- MGBiota, 3(4): 5-21.

SILVA, A. R. M., CASTRO, C. O., MAFIA, P. O., MENDONÇA, M. O. C., ALVES, T. C. C. & BEIRÃO, M. V., 2012.- Borboletas frugívoras (Lepidoptera: Nymphalidae) de uma área urbana (Área de Proteção Especial Manancial Cercadinho) em Belo Horizonte, Minas Gerais, Brasil.- Biota Neotropica, 12: 292-297.

SILVA, A. R. M., PONTES, D. V., GUIMARÃES, M. P., OLIVEIRA, M. V., ASSIS, L. T. F. & UEHARAPRADO, M., 2015.- Fruit-feeding butterflies (Lepidoptera: Nymphalidae) of the Áea de Proteção Especial Manancial Mutuca, Nova Lima and Species list for the Region of Belo Horizonte, Minas Gerais, Brazil.- Biota Neotropica, 15(3): e20140118.

SOARES, A., JÚLIO, C. E. A., CAETANO, C. A., TANGERINI, N., FARIA, A. C. & COSTA, J. E., 1999.- Lista de lepidopterofauna diurna da região da calha do Rio São Francisco, estado de Minas Gerais, municípios de Itacarambi, Jaíba, Manga e Matias Cardoso.- Boletim do Museu Nacional, 402: 1-11.

SOARES, G. R., OLIVEIRA, A. A. P. & SILVA, A. R. M., 2012.- Borboletas (Lepidoptera: Papilionoidea e Hesperioidea) de um parque urbano em Belo Horizonte, Minas Gerais, Brasil.- Biota Neotropica, 12: 1-10.

UEHARA-PRADO, M., FREITAS, A. V. L., FRANCINI, R. B. & BROWN JR, K. S., 2004.- Guia das borboletas frugívoras da Reserva Estadual do Morro Grande e região de Caucaia do Alto, Cotia (São Paulo).- Biota Neotropica, 4: 1-9.

WAHLBERG, N., LENEVEU, J., KODANDARAMAIAH, U., PEÑA, C., NYLIN, S., FREITAS, A. V. L. & BROWER, A. V. Z., 2009.- Nymphalid butterflies diversity following near demise at the Cretaceous / Tertiary boundary.- Proceedings of the Royal Society B, 276: 4295-4302.

WARREN, A. D., DAVIS, K. J., STANGELAND, E. M., PELHAM, J. P. & GRISHIN, N. V., 2013.- Illustrated list of American butterflies. Available from http://www.butterfliesofamerica.com/ (accessed october 2015).

HTML generated from XML JATS4R by