Butterflies ( Lepidoptera : Papilionoidea ) of an urban park in northeastern Brazil

Despite being one of the groups most well studied in Brazil, the butterfly fauna of northeastern Brazil, especially north of the mouth of São Francisco River, is poorly known. The aim of this study was to inventory the butterfly fauna in a remnant of Atlantic Forest in the state of Pernambuco as a contribution to understanding the distribution of these insects. The study was carried out in a 384.7 hectares fragment of Parque Estadual Dois Irmãos, in the metropolitan region of Recife. The butterflies were sampled monthly with insect nets from August 2011 to July 2012 and from January to August 2016. Additional records were obtained from two entomological collections and from two previous visits to the area in July 2003 and August 2006. A total of 273 species was sampled in 464 hours, with an additional 15 species recorded from the Entomological Collections, totaling 288 butterfly species recorded. The richest family was Hesperiidae (108 species), followed by Nymphalidae (80), Lycaenidae (43) Riodinidae (37), Pieridae (16) and Papilionidae (4). The fauna was dominated by generalist species with a broad geographical distribution, many of them commonly found on open areas, forest edges and secondary vegetation. Roeberella lencates (Hewitson, 1875) and Pheles atricolor atricolor (Butler, 1871) (Riodinidae) represent new records for northeastern Brazil.


Introduction
Although the butterfly fauna of Brazil is relatively well sampled, there is still a "knowledge gap" in northeastern Brazil (Santos et al. 2008).The entire region is relatively under-sampled and poorly known, especially in the highly fragmented forests north of the mouth of São Francisco River (Freitas & Marini-Filho 2011, Iserhard et al. 2017).This region, which is known as the "Pernambuco Center of Endemism" (Brown Jr. 1977, Santos et al. 2007), is the most endangered sector of the Atlantic Forest, with less than 12% of the original vegetation remaining (Ribeiro et al. 2009), almost half as fragments smaller than 10 ha (Ranta et al. 1998).
The purpose of the present study was to inventory the butterfly species found in "Parque Estadual Dois Irmãos", a forest fragment in the metropolitan region of Recife, Pernambuco, northeastern Brazil, and to compare the results with those of previous inventories in the same region.These baseline results will also serve as a point of comparison for future inventories as ecological succession proceeds in this park.

Study area
Parque Estadual Dois Irmãos (PEDI) (08º 00' 48" S, 34º 56' 42.9" W) is a state park in Recife, Pernambuco, northeastern Brazil (Figure 1).PEDI was created by State Law nº 11.622 of December 29, 1998 with ca.384.7 ha, and has recently expanded (state decree nº 40.547 of March 28, 2014) with the inclusion of adjacent forest (the "Fazenda Brejo dos Macacos"), now totaling 1,157.72 ha.This coastal Atlantic Forest consists of a mix of successional regenerating stages.The present study was carried out in the 384.7 ha area now called "Mata de Dois Irmãos".This area is the original part of the Park, including a 14 ha zoo.The climate is tropical monsoon (Am of Köppen), hot and humid, with a monthly average temperature of 25.8ºC.Rainfall, with an annual precipitation up to 2,400 mm, is seasonal, with a wet season from March to August and a dry season from September to February (Coutinho et al. 1998, Alvares et al. 2014).The predominant soils are dystrophic red-yellow latosols (Coutinho et al. 1998), and the vegetation is classified as ombrophilic dense lowland forest (Veloso et al. 1991).

Sampling and identification
Sampling was carried out monthly from August 2011 to July 2012, following the protocol described in Brown Jr. (1972), Brown Jr. & Freitas (2000) and Iserhard et al. (2013), with four sampling days each month, totaling 48 field trips.In addition, occasional visits were conducted between January and August 2016, totaling 17 additional field trips.The daily sampling period was from 9:00 to 16:00 hours, with a total sampling effort of 455 hours.Sampling was conducted along pre-existing trails (up to 2 linear km) covering a variety of habitats by one collector using an insect net (with a handle 1 m in length).Special attention was devoted to forest edges, water bodies or their banks, rich soil and flower patches, small clearings, and other heterogeneous environments.Areas with notable concentrations of butterflies were observed until no additional species had been recorded for a period of five to ten minutes.Additional data were obtained from two previous visits by AVLF (July 29, 2003 andAugust 10, 2006, totaling 9 samplings hours) and from material deposited in the Entomological Collection, Biology Department, Universidade Federal Rural de Pernambuco (UFRPE), and the Entomological Collection, Universidade Federal de Pernambuco (UFPE).Specimens were mounted and deposited in the following Brazilian institutions: 1) Universidade Federal de Pernambuco, Recife, PE; 2) Museu de Zoologia, Universidade Estadual de Campinas, Campinas, SP; and 3) Coleção Entomológica Padre Jesus Santiago Moure, UFPR, Curitiba, PR.
The authors identified species using the literature, the museum collections for which they are responsible, and their taxonomic expertise, which is partly based on years of fieldwork in Brazil and other Neotropical countries.The Discussion is based on these same information sources.The nomenclature in Table 1 follows Lamas (2004), but higher taxonomic categories for Nymphalidae were updated from Wahlberg et al. (2009), for Riodinidae from Seraphim et al. (2018) and Hall (2018), for Hesperiidae from Warren et al. (2009).The higher classification of butterflies was updated from Heikkilä et al. (2012).All families were sampled, except for the Hedylidae.
A number of unusual riodinid species were found.The species Roeberella lencates (Hewitson, 1875) and Pheles atricolor atricolor (Butler, 1871) were recorded for northeastern Brazil for the first time (Table 1).A single individual of R. lencates was captured when resting in a "pitangueira" tree (Eugenia uniflora, Myrtaceae) in an open sunny area known as "Chapéu do Sol".A single individual of P. atricolor atricolor was found on a trail along a forest edge.It made short flights followed by landing on a leaf.A third riodinid Eurybia gonzaga Dolibaina, Dias, Mielke & Casagrande, 2014 is a recently described endemic for Pernambuco.It was observed frequently in PEDI.This species flies near the ground at dusk.It lands on the underside of leaves.

Species richness
The 288 butterfly species recorded at PEDI is considerably lower than at sites in SE Brazil (800+ species, Francini et al. 2011) and the Amazon Basin (up to 1700 species in Robbins et al. 1996 andBrown 2005), but is similar in richness to other inventories for the Atlantic Forest of northeastern Brazil.Kesselring & Ebert (1982) found 291 butterfly species in the urban park "Mata do Buraquinho" in João Pessoa, Paraíba after five years of sampling.Paluch et al. (2011Paluch et al. ( , 2016) ) recorded 197 species in a forest area in Caruaru, Pernambuco (216 sampling hours) and 260 species in Itanagra, Bahia (288 sampling hours), respectively.Cardoso (1949) recorded 218 butterfly species in the forest of Maceió, Alagoas after many years of sampling.Even though PEDI is located in an urban area of Recife that is close to a large highway, its butterfly fauna is comparable in richness to these other sites in northeastern Brazil.
The richness of Hesperiidae and Lycaenidae in PEDI was similar to that recorded by Kesselring & Ebert (1982), but higher than other localities in the region (Cardoso 1949, Paluch et al. 2011, 2016) Pieridae, the number of recorded species is similar to most inventories conducted in the region (Cardoso 1949, Kesselring & Ebert 1982, Paluch et al. 2011, 2016).The richness of Papilionidae is low compared to that in southern Atlantic Forest sites (see Brown Jr. & Freitas 2000), though similar to other well-sampled sites on the Atlantic Forest of northeastern Brazil (Kesselring & Ebert 1982, Paluch et al. 2011, 2016).Finally, the number of Riodinidae species was similar to those in Kesselring & Ebert (1982) and Paluch et al. (2016), but was greater than the numbers reported in Cardoso (1949) and Paluch et al. (2011).

Taxonomic composition
The relative contribution of each butterfly family in PEDI mirrors the pattern reported in the list of Brazilian butterflies and in all well sampled sites in Brazil.Hesperiidae is the richest family, followed by Nymphalidae (Brown Jr. & Freitas 1999, 2000, Francini et al. 2011).Lycaenidae and Riodinidae are equivalent in richness in PEDI, a pattern similar to that observed in most southern Atlantic Forest sites and in montane forests.However, it diverges from that observed in the lowland forests of Rio de Janeiro and Espírito Santo (Brown Jr. & Freitas 2000, Francini et al. 2011), where Riodinidae surpasses Lycaenidae.Clearly, additional surveys in other sites in the Pernambuco Center of Endemism and in the forests of Bahia are needed to better document these patterns.
In the Atlantic Forest, Nymphalidae is considered a reliable surrogate of the total butterfly fauna, generally making up 25-29% of the total butterfly fauna (Brown Jr. & Freitas 2000).Based on this indicator, the fauna of PEDI would be expected to vary between 276 and 320 species, which is consistent with the 288 recorded species.

Habitat
The fauna of PEDI is dominated by species commonly found along forest edges, in open habitats and disturbed forests.As an example, all species of Pieridae recorded in the study site are typical of secondary forests and disturbed areas with the possible exception of Leucidia elvina (Godart, 1819).The same is true for Hesperiidae and Papilionidae, except for Parides zacynthus polymetus (Godart, 1819), and the major groups of Nymphalidae.The tribe Ithomiini (Nymphalidae: Danainae) is poorly represented, as noted, with most of those in PEDI associated with open disturbed habitats and forest edges (with the exception of Napeogenes inachia ssp.).

Biogeography
The biogeographic composition of the PEDI fauna shows a large contribution of widely distributed species, as illustrated with the Lycaenidae, Papilionidae and Pieridae.For Lycaenidae for example, many of the species have wide geographic distributions; with 24 of 43 species (56%) occurring from Central America to Brazil.Alternately, some species are primarily Amazonian and penetrate the Atlantic Forest only in the north.Examples are Nesiostrymon hyccara (Hewitson, 1868), Ostrinotes tarena (Hewitson, 1874), and Thereus enenia (Hewitson, 1867).Others are endemic to the Atlantic Forest, such as Panthiades hebraeus (Hewitson, 1867) and Theritas triquetra (Hewitson, 1865).Although none of the Lycaenidae, Pieridae and Papilionidae at PEDI are endemic to the Pernambuco Center of Endemism, this is not true for Riodinidae.For example, the recently described Eurybia gonzaga is known only from Pernambuco (Dolibaina et al. 2014).It was also recorded in "RPPN Frei Caneca", Jaqueira (as type material, see Dolibaina et al. 2014)

Conservation
No threatened butterflies are recorded in PEDI, but there is a historical record (about 50 years ago) of Morpho menelaus eberti Fischer, 1962 (Nymphalidae: Satyrinae: Morphini) in the "Chapéu do Sol", deposited in the National Museum of Natural History in Paris (Blandin 2007).Although habitat loss, years of logging and other urban related disturbances could explain the local extinction of M. melenaus eberti, this butterfly could still persist in the area in low densities.Another threatened morphine that could be present in the area is Morpho epistrophus nikolajewna Weber, 1951.This butterfly has been recorded to the south in Maceió (Cardoso 1949), to the north in Igarassu (Carlos E. B. Nobre pers.comm.) and in João Pessoa (Kesselring & Ebert 1982), which are Atlantic Forest fragments near urban areas.Further sampling is needed before stating that both species of Morpho Fabricius, 1807 are absent in forested areas around Recife.
The reported results showed that PEDI possesses a relatively rich butterfly community.Considering the degree of threat to the fauna of the Atlantic Forest of northeastern Brazil, PEDI is of enormous importance for conserving butterflies, as it is for vertebrates such as birds and mammals (Machado et al. 1998).Conservation strategies should be developed in conjunction with public entities, such as the Environment Secretariat of Recife, and non-governmental organizations such as the "Centro de Pesquisas Ambientais do Nordeste" (CEPAN), and with the local communities surrounding the whole area.Priority actions for PEDI should include the proposition of a sustainable management plan focused on reintroduction of locally extinct species of plants and animals, an effective plan for restoring heavily disturbed areas, and establishment of programs of ecological monitoring and management of the surrounding environments so that the area can persist as an important Atlantic Forest remnant.

Table 1 .
Butterflies (Lepidoptera) from the "Parque Estadual Dois Irmãos", Recife, Pernambuco, Brazil.Number of species are noted within parenthesis for each major taxon. 1 Data from the UFPE Entomological Collection; 2 Data from the UFRPE Entomological Collection; 3 new record for northeastern Brazil.