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Saturniid moths (Lepidoptera: Bombycoidea) from an Atlantic Rain Forest fragment in southeastern Brazil

The light-attracted silk moths (Lepidoptera: Saturniidae) of the Boraceia Biological Station in the municipality of Salesópolis, state of São Paulo, southeastern Brazil have been sampled over more than seven decades (1942-2013). A total of 6,288 individuals (including a gynandromorph) belonging to five subfamilies, 46 genera and 133 species were identified. Hemileucinae was the most abundant and speciesrich subfamily, followed by Ceratocampinae, Arsenurinae, Saturniinae, and Oxyteninae. Hylesia Hübner, Automeris Hübner, and Dirphiopsis Bouvier (Hemileucinae) were the dominant genera in abundance and species richness. Only Automeris illustris (Walker), Gamelia remissoides Lemaire, and Hidripa paranensis (Bouvier) (Hemileucinae) were recorded in all months of sampling. Hylesia metapyrrha (Walker) was the most abundant saturniid species recorded at the station, with 375 specimens, followed by Hylesia oratex Dyar with 265 specimens, Dirphia muscosa Schaus with 261 specimens (all Hemileucinae); Copaxa canella Walker (Saturniinae) with 232 specimens, and Lonomia cf. obliqua Walker (Hemileucinae) with 106 specimens. Fifteen additional species were each represented by more than 100 specimens. The importance of the Boraceia Biological Station to the maintenance of the saturniid moth diversity in the Atlantic Forest is discussed.


INTRODUCTION
Moths and butterflies are important organisms in tropical ecosystems because they interact widely with the vegetation and local fauna (Gilbert 1984, Miller 1993, Bonebrake et al. 2010, Johnson et al. 2017, Goldstein 2017. Their feeding habits, great diversity, ease of sampling, and the relatively well known taxonomy of some groups, such as Saturniidae, make them potentially important organisms for use in monitoring the biological diversity in different communities (Brown and Freitas 1999, 2000a, b, Basset et al. 2017, Mitter et al. 2017.
Saturniidae is comprised of 2,349 species worldwide in 169 genera, and is the most speciesrich family of Bombycoidea (van Nieukerken et al. 2011). Saturniidae has been divided into nine subfamilies: Agliinae, Arsenurinae, Ceratocampinae, Cercophaninae, Hemileucinae, FABIANO F. ALBERTONI, CARLOS G.C. MIELKE and MARCELO DUARTE Ludiinae, Oxyteninae, Salassinae, and Saturniinae (Minet 1994, Regier et al. 2008, van Nieukerken et al. 2011. Of these, five are represented in the Brazilian fauna (Lemaire and Minet 1998, Duarte et al. 2012: the most speciose subfamily, Hemileucinae, consists of 630 species in 51 genera; the cosmopolitan Saturniinae is represented by 480 species in 59 genera; Ceratocampinae has 170 species in 27 genera; and the Neotropical endemic Arsenurinae and Oxyteninae are represented by 60 species in 10 genera and 35 species in three genera, respectively (Lemaire and Minet 1998). More than one-third of the species estimated for Saturniidae occur in the Neotropics (Lemaire and Minet 1998, Duarte et al. 2012. In Brazil, approximately 500 species have been recorded (Camargo et al. 2017). Recently, over 500 saturniid species from the Neotropics were described by Brechlin and Meister in the journal Entomo-Satsphingia, which would add many species to the family, despite these authors' dubious method of splitting previous available names into cryptic groups (Nässig et al. 2010, St. Laurent et al. 2015. Adult saturniid moths are mostly nocturnal, except for males of several species in Saturniinae, Hemileucinae, Agliinae, and Ceratocampinae (e.g., Anisota spp., see also Lemaire and Minet 1998). The females of Heliconisa Walker, 1855 are essentially diurnal, as well as the females of Ithomisa Oberthür, 1881, which fly at the end of the day and also at night. The mouthparts of these insects are inchoate and they do not feed during their short 5-12-day adult life (Janzen 1984). Strong sexual dimorphism is observed in species of Ceratocampinae, Hemileucinae, and Oxyteninae; females can weigh more than twice as much as males, usually bear filiform antennae (pectinate in males), and are larger with more rounded wings than in males (Janzen 1984).

BRAZILIAN INVENTORIES OF SATURNIIDAE
The southern states of Brazil, Rio Grande do Sul, Santa Catarina, and Paraná, have partially inventoried their saturniid fauna. After approximately a decade of investigations in Rio Grande do Sul, 113 species in four subfamilies were recorded: Hemileucinae (61 species, 54%), Ceratocampinae (30, 27%), Arsenurinae (12, 11%), and Saturniinae (10, 9%) (Nunes et al. 2004, Specht et al. 2005a, b, Prestes et al. 2009). Although we have some efforts of sampling in Rio Grande do Sul, mainly focusing on groups of medical importance, there is still a need for long-term and systematic inventories to know the composition and distribution of the saturniids in different vegetation formations (e.g., grasslands, dense ombrophilous and seasonal deciduous forests, Araucaria forest) in this region of Brazil (see also vegetation map of Buriol et al. 2007).
To determine the Santa Catarina saturniid fauna, Siewert et al. (2010) used data from six important Brazilian lepidopteran collections, as well as geographic distributions provided by Lemaire (1978Lemaire ( , 1980Lemaire ( , 1988Lemaire ( , 2002. They recorded a total of 149 species in 50 genera, including 90 (60%) species of Hemileucinae, 32 (21%) of Ceratocampinae, 16 (11%) of Arsenurinae, and 11 (7%) of Saturniinae. We can state that the saturniid fauna of Santa Catarina is still poorly sampled. Only eight municipalities in the entire state have been sampled to date (see the map in Siewert et al. 2010), and it is necessary to intensify sampling efforts in the main vegetation formations in the state (e.g., deciduous, dense ombrophilous, and subtropical ombrophilous forests).
Knowledge of the lepidopteran fauna of Paraná is certainly the most extensive of the southern states of Brazil. However, with regard to the saturniids, long-term surveys of these moths have intensified only recently. During an entomological survey conducted between 1986 and 1987 in SATURNIIDS FROM AN ATLANTIC RAIN FOREST FRAGMENT 2829 and northeastern São Paulo and northern Paraná (Filardi et al. 2007). The Cerrado borders three other biomes and is considered a world biodiversity hotspot (Myers et al. 2000). Although extensive efforts have been made to sample saturniids in the Brazilian Cerrado, these moths remain little known in some states that still contain remnants (strongly threatened by human action) of this biome. In addition, as part of an extensive entomological catalog, Zikán and Zikán (1968) listed the lepidopteran (not all suborders) fauna from the Itatiaia region, which included the family Saturniidae (Saturnioidea in Zikán and Zikán 1968). This region is located between the states of Rio de Janeiro and Minas Gerais and varies widely in altitude, from approximately 500 m to more than 2,400 m (Zikán and Zikán 1940). Zikán and Zikán (1968) listed 125 species from 33 genera: Hemileucinae, 70 species (56%); Ceratocampinae, 33 (26%); Arsenurinae, 7 (6%); Saturniinae, 12 (10%); and Oxyteninae, 3 (3%), with 28 undetermined species, totaling 153 species. However, their determinations should be revised with the current nomenclature, in order to develop an accurate survey.
As we can see, the Brazilian Saturniidae are still unsatisfactorily understood with respect to species distribution, taxonomy, and biological information (e.g., Albertoni and Duarte 2015), although some knowledge is available for species with medical or economic value (Lemaire 2002, Specht et al. 2008. Undeniably, faunal inventories are vital to understanding and monitoring local biodiversity (Silveira et al. 2010). Saturniid moths were efficiently attracted at night via light trap, and we report herein a species list from longterm survey data (more than 70 years) collected in a strategically located fragment of Atlantic Rain Forest (Boraceia Biological Station) in the state of São Paulo, southeastern Brazil.
The saturniid fauna in the Cerrado (Brazilian savanna) has been documented by Camargo and Becker (1999) and A. Camargo et al. (unpublished data). Data from several entomological collections in Brazil were extensively searched. As a result, 202 species from 74 localities in 10 states and the Federal District were recorded (A. Camargo et al., unpublished data). Of these, 119 (58.9%) were Hemileucinae, 48 (23.7%) Ceratocampinae, 22 (10.9%) Arsenurinae, 11 (5.4%) Saturniinae, and 2 (1%) Oxyteninae. Of the six terrestrial biomes in Brazil (Amazon Forest, Atlantic Forest, Cerrado, Caatinga, Pampa, and Pantanal; see also Instituto Brasileiro de Geografia e Estatística 2004), the Cerrado is the second largest. This biome covers approximately 2,000,000 km 2 , with a continuous distribution throughout the entire Central-West region, western Bahia and Minas Gerais, as well as disjunct distribution areas in northern FABIANO F. ALBERTONI, CARLOS G.C. MIELKE and MARCELO DUARTE understanding of Brazilian biodiversity, allowing eventual amplification of the predictive capacity of lepidopteran fauna responses to global changes, particularly changes in land use and land cover and climate changes. The large extent of the reserve within which the Boraceia Biological Station is located, and because it contains mostly primary forest, two rare characteristics in fragments of Atlantic Rain Forest, make the biological station highly important for studies of the biodiversity of this biome. The importance of standardized local biological inventories and studies of community composition is evident, as in the case of the present study. Longino and Colwell (1997) emphasized the importance of biological inventories for conservation purposes, since they allow descriptions and characterizations of communities in terms of species richness, abundance and complementarity with other communities. Obtaining such information is important, for example, in setting priorities for monitoring and conservation actions. The Saturniidae, which is usually prominent among the lepidopteran fauna due to the diversity and ecological importance of its members, and is commonly among the best-studied moth families in a given locality (Santos et al. 2015), has been the target of a number of previous inventories in Brazil.

STUDY AREA
The survey of saturniid moths was conducted at the Boraceia Biological Station (BBS) (23º39′S, 45º53′W, elevation 850 m), located in the municipality of Salesópolis, state of São Paulo, in southeastern Brazil. The Biological Station is managed by the Museu de Zoologia of the Universidade de São Paulo (MZSP) and has an area of 96 ha. The station is located within the largest fragment of Brazilian Atlantic Rain Forest, which includes several parks and other types of conservation units (Travassos Camargo 1958, Custodio Filho 1989) (Figure 1). The climate is wet tropical, Cfa in Köppen's classification (Köppen 1948). Measurements from 1925 to 1944 identified Boraceia as one of the most humid regions in Brazil, with a mean annual rainfall of 3,058 mm (Setzer 1946).

MOTH SAMPLING
Sampling of saturniid moths in the BBS started in 1942, with the entomologist Romualdo Ferreira D'Almeida. A few years later, the entomologists Lauro Travassos, Lauro Travassos Filho, Ernesto Xavier Rabello, and several associates continued the series, with extensive collections spanning decades (Travassos Filho and Camargo 1958). A recent inventory was conducted by the senior author, over 13 consecutive months in 2012 and 2013 (see also Table I).
Nocturnal moths were attracted and collected using mercury-vapor mixed bulbs placed near the white wall of one of the scientists' residences (Duarte et al. 2008). Specimens collected after 2004 were killed by injection of aqueous ammonia solution in the thorax. We have no records about how specimens were killed in expeditions carried out before 2004. Most specimens sampled from September 1942 to June 2013 were stored, identified and labeled with a registration number in addition to the previous labels. All records were stored in a digitalized database, which is intended to be of free public access through the World Wide Web. All material is deposited in the MZSP, but some of the specimens collected by Lauro Travassos were deposited in the Entomological Collection of the Oswaldo Cruz Institute, Rio de Janeiro, Brazil, and those species not represented in the MZSP were included in our list, as a complement to the number of saturniid species recorded for the BBS (Miranda et al. 2015).
Previous identifications of the specimens deposited in the MZSP collection were verified, and nomenclature was checked using Lemaire (1978,1980,1988,2002 (2011). In addition to this literature, we used the content and associated data available in the member-restricted area of the website http://www.silkmoths.bizland. com/indexos.htm. To obtain more precise identification of specimens, 63 males of several morphospecies were dissected and data concerning the genitals were compared with literature and/ or with that from previously extracted organs. Dissections were conducted as follows: the abdomen was cut at segments IV-V and placed in a boiling 10% KOH solution for approximately 10 min. The tegument and internal contents were removed, the abdomen was placed in chlorazol black solution for approximately 1 min, and the genitals were separated from the abdomen. All parts were preserved in a container with glycerin, labeled, and given a unique code.
Most moths were pinned and dried, but a few were identified and placed in entomological envelopes, on which the sample origin and species identification were annotated.

RESULTS AND DISCUSSION
The lepidopteran collection of the MZSP hosts 6,288 specimens of Saturniidae (5,735 males, 552 females, and one gynandromorph) captured at the BBS between 1942 and 2013. More than   94% of the specimens examined were identified to the species level, and consisted of 43 genera and 126 species. The greatest abundance and number of species were observed for Hemileucinae, with 3,645 specimens (58%) of 77 species (61.1%), followed by Ceratocampinae with 1,298 specimens (20.6%) of 23 species (18.4%), Arsenurinae with 659 specimens (10.5%) of 14 species (11.2%), Saturniinae with 557 specimens (8.9%) of 10 species (7.9%), and Oxyteninae with 129 specimens (2.1%) of two species (1.6%) ( Tables  II and III). Besides the species deposited at MZSP, Miranda et al. (2015) recorded seven other species (one Arsenurinae, three Ceratocampinae, and three Hemileucinae, also listed in Table III) belonging to three genera from the BBS and apparently deposited only in the Entomological Collection of the Oswaldo Cruz Institute. Therefore, a total of 46 genera and 133 species are recorded from this biological station.
The distribution of the saturniid species among subfamilies in the BBS follows the pattern in most South American surveys (Ecuador: Racheli and Racheli 2005, 2006, Brazil: Marinoni et al. 1997, Camargo and Becker 1999, Nunes et al. 2004, Prestes et al. 2009, Siewert et al. 2010. Hemileucinae is the most speciose subfamily, followed by Ceratocampinae, Arsenurinae, Saturniinae, and Oxyteniinae (not infrequently, surveys do not include this subfamily because it has been raised to family rank). Worldwide, Hemileucinae is the subfamily with the largest number of species; Saturniinae, the only subfamily distributed worldwide, is next in species richness. However, although this pattern has also been observed in the Brazilian Cerrado, Camargo and Becker (1999) demonstrated that, as a percentage, Ceratocampinae and Arsenurinae together amount to almost the same proportion as Hemileucinae in this biome (48.2% Hemileucinae vs. 47.0% Ceratocampinae plus Arsenurinae). They explained this importance of Ceratocampinae and Arsenurinae in the Cerrado by the biology of these moths. It seems that the caterpillars, which bury in the soil to pupate, have higher survival in environments with a pronounced dry season.
The most abundant genera with the most species in the BBS belonged to the subfamily Hemileucinae. The genus Hylesia Hübner, [1820] was represented by 1,433 specimens in 17 species, including Hylesia sp. 1, sp. 2, and sp. 3. The next most speciose genera were Automeris Hübner, [1819] (Hemileucinae) with 404 specimens from nine species, and Dirphiopsis Bouvier, 1928 with 266 specimens from seven species. Dirphia Hübner, [1819], with six species, was the second most abundant genus with 432 specimens. Rothschildia Grote, 1897 (Saturniinae) was the only genus not belonging to Hemileucinae to be represented by six species, with 226 specimens.
The genus Hylesia is usually markedly dominant in surveys of Saturniidae in Brazil. In Paraná and Rio Grande do Sul, for example, 14 (16.3% of all species) and nine (8%) species of this genus were recorded, respectively. For BBS, 17 species (13.5% of all species) were recorded, including three morphospecies, in addition to a set of 40 specimens identified only at the genus level.
Hylesia is among the genera with the most complex taxonomy in Saturniidae due to the its phenotypic homogeneity and wide geographic distribution, covering the entire Neotropical region, from Mexico to Argentina (Lemaire 2002). Knowing that this genus is one of the most problematic in the family, the remarkable density of species and specimens sampled in the BBS makes this biological station a promising area for further studies on these saturniids. Dissections of the genitalia from 26 specimens showed that it is difficult to use the information from this part of the body for species separation (Wheeler 2008, Schlik-Steiner et al. 2010. Studies involving different tools to contribute to the delimitation of species of the genus are extremely important, both  Miranda et al. (2015).    (Lemaire, 1975).

CONCLUSIONS
The number of species among the subfamilies of Saturniidae recorded from the Boraceia Biological Station followed a similar pattern to that observed in most inventories conducted in Brazil and other countries of South America. Although the number of species increased sporadically with an increasing number of samples at a given location, collections from different altitudes or phytophysiognomies of the matrix region may greatly increase the species number. In total, 133 saturniid species were recorded, with no endemism to the BBS.
We found it prudent not to compare statistically our results on species richness with other surveys, because clearly the sampling efforts were not the same, and also because the phytophysiognomies are quite different from those in the BBS. The collection of Saturniidae from the BBS deposited in the MZSP is the result of more than 70 years of sampling accumulation, and thus it is not perfectly suitable for such comparisons. However, the number of species (133 species) recorded in the present study was obtained in a single sampling site (see details in the Materials and Methods section), and is comparatively high in relation to the number of species inventoried for the Brazilian Cerrado biome (202 species), the Itatiaia region (125 species), and Rio Grande do Sul (113 species), Santa Catarina (149 species), and Paraná (131 species).
The importance of the BBS for the Saturniidae assemblage of the Atlantic region of São Paulo is due especially to its location, within a context of well-preserved Atlantic Rain Forest that extends along the northern to southern coast of the state, including the Serra do Mar State Park (Figure 1). For this reason, the BBS and its facilities are located in a strategic position and are therefore highly valuable for the knowledge and conservation of the FABIANO F. ALBERTONI, CARLOS G.C. MIELKE and MARCELO DUARTE Taxa TABLE IV (continuation)