Brazilian Journal of and Environmental Research 3248 ISSN: 2595-573X

Butterflies (: Papilionoidea) in the Arboretum of Alagoas State,

Borboletas (Lepidoptera: Papilionoidea) no Arboretum de Alagoas, Brasil

DOI: 10.34188/bjaerv4n3-037

Recebimento dos originais: 04/03/2021 Aceitação para publicação: 30/06/2021

Lucas Teles Bezerra Graduando em Engenharia Florestal pela Universidade Federal de Alagoas (UFAL) Instituição: Universidade Federal de Alagoas (UFAL) Endereço: BR 104, Km 85, s/n, Rio Largo - AL, Brasil E-mail: [email protected]

Elmadã Pereira Gonzaga Doutoranda em Proteção de Plantas pelo Campus de Engenharias e Ciências Agrárias (CECA), da Universidade Federal de Alagoas (UFAL) Instituição: Universidade Federal de Alagoas (UFAL) Endereço: BR 104, Km 85, s/n, Rio Largo - AL, Brasil E-mail: [email protected]

Mayara Dalla Lana Doutora em Ciências Florestais pela Universidade Federal Rural de Pernambuco (UFRPE) Instituição: Universidade Federal de Alagoas (UFAL) Endereço: BR 104, Km 85, s/n, Rio Largo - AL, Brasil E-mail: [email protected]

Mariana Oliveira Breda Doutora em Entomologia Agrícola pela Universidade Federal Rural de Pernambuco (UFRPE) Instituição: Universidade Federal de Alagoas (UFAL) Endereço: BR 104, Km 85, s/n, Rio Largo - AL, Brasil E-mail: [email protected]

Marcelo Duarte Doutor em Ciências Biológicas (Entomologia) pela Universidade Federal do Paraná (UFPR) Instituição: Museu de Zoologia da Universidade de São Paulo (MZUSP) Endereço: Avenida Nazaré, 481. Ipiranga, São Paulo - SP, Brasil E-mail: [email protected]

ABSTRACT The deforestation of areas due to the expansion of cities and urban zones have directly affected natural habitats, causing negative changes, biodiversity loss and reducing populations size of native flora and fauna. In this context, are considered excellent organisms for monitoring environmental quality as they are involved in extremely specific ecological relationships with their habitats. Thus, this research aimed to carry out a survey of the (Lepidoptera: Papilionoidea) fauna in the Arboretum of Alagoas State. Weekly samplings were carried out from September 2019 to March 2020. During 140 sampling hours, 415 individuals were collected, being observed the occurrence of 44 species distributed in six families. The low number of recorded taxa reflects an

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Brazilian Journal of Animal and Environmental Research 3249 ISSN: 2595-573X expected poor richness as, in general, the closer the analyzed fragment is to an urban area, the smaller the number of species. was the most well represented family, being recorded seven subfamilies. Based on these results, it was possible to state that the butterfly fauna in the Arboretum of Alagoas State comprises species commonly found in anthropic environments and/or areas under high anthropogenic influence.

Keywords: Entomology, Environmental Refuge, Lepidopterofauna, Survey.

RESUMO O desmatamento de florestas para o avanço das cidades e perímetros urbanos tem afetado diretamente esses habitats ocasionando modificações negativas, perda da biodiversidade e redução no tamanho de populações da flora e da fauna. Neste contexto, as borboletas (Lepidoptera: Papilionoidea) são consideradas excelentes organismos para monitoramento da qualidade ambiental pois desenvolvem relações ecológicas bastante específicas com seu habitat. Portanto, esta pesquisa teve como objetivo efetuar um levantamento da Lepidopterofauna de borboletas (Lepidoptera: Papilionoidea) do Arboretum de Alagoas. Foram realizadas coletas semanais de setembro de 2019 a março de 2020. Em 140 horas de coleta, um total de 415 indivíduos foram obtidos, sendo observadas a ocorrência de 44 espécies distribuídas em seis famílias de Lepidoptera (Papilionoidea). O baixo número de táxons registrados reflete uma riqueza pouco expressiva já esperada pois, em geral, quanto mais próximo de área urbana for o fragmento analisado, menor o número de espécies encontradas. Nymphalidae foi a família mais bem representada com a ocorrência de sete subfamílias no local. Com base nos resultados desta pesquisa foi possível concluir que, de forma geral, as espécies encontradas no Arboretum de Alagoas são características de ambientes antropizados, e/ou áreas sob a influência antrópica.

Palavras-chave: Entomologia, Lepidopterofauna, Levantamento, Refúgio Ambiental.

1 INTRODUCTION Changes in natural landscapes due to anthropic actions and accelerated urbanization have caused disturbance, destruction, fragmentation and isolation of the ecosystems and natural habitats (Silva et al., 2007). In the state of Alagoas, Northeastern Brazil, the fragmentation of natural vegetation is provoked mainly by the deforestation for implementation of crops, such as eucalyptus and sugar cane (Andrade et al., 2019; Bezerra et al., 2020). In urban environments, the importance of green areas such as woods, parks, squares, and urban forests is quite remarkable because these places act as refuges, contribute to biodiversity conservation, provide the maintenance of environmental quality, reduce air pollution, and also have aesthetic and leisure functions (Dias, 2015; Steenberg et al., 2019). The development of studies in green areas of the urban zones is important in providing information about the local biodiversity, allowing the development of conservation strategies and the management of natural resources (Gaudereto et al., 2019). The Arboretum of Alagoas State located at the Federal University of Alagoas (UFAL), is an example of an urban green area, which suffers the influence of anthropization. The Arboretum is characterized by a 4.2 hectares forest

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Brazilian Journal of Animal and Environmental Research 3250 ISSN: 2595-573X implemented by the Botany Department of UFAL with the support of the Pro-rectory of Extension (PROEX/UFAL), and the Brazilian Institute of Environment and Renewable Natural Resources/IBAMA, for seedling production of native species in the region (Santos, 2011). The role of a biological indicator (bioindicator) gets to focus on the provision of fast analyzes on the biological quality of the environment (Pereira & Soares, 2020). Butterflies (Lepidoptera: Papilionoidea) are known for its potential as excellent bioindicators, by developing extremely specific ecological relationships with their habitats, intrinsic associations with host plants and being extremely sensitive and quickly responding to changes in the environment (Soares et al., 2012). Thus, surveys and faunistic analyzes of the butterfly fauna in urban green areas have become essential tools for recording and identifying the presumably isolated biodiversity in these urban environments. Also, these surveys are necessary for the identification of potential bioindicator species for the assessment of anthropogenic impact, and to assist the development of conservation strategies (Isehard et al., 2010; Cordeiro & Richardo, 2019). Furthermore, studies aiming the knowledge and inventory of these should be encouraged, especially for the northeastern Brazil, where the lepidopteran fauna is quite undersampled (Lima & Zacca, 2014), and there is a large gap on the knowledge about the diversity of butterflies due to the reduced number of specialists. Therefore, the objective of this study was to carry out the first survey of butterfly species (Lepidoptera: Papilionoidea) in the Arboretum of Alagoas State (UFAL).

2 MATERIAL AND METHODS 2.1 STUDY AREA The study was carried out in the Arboretum of Alagoas State, located at the Aristóteles Calazans Simões Campus of the Federal University of Alagoas (UFAL) (09º33'13.80" S and 35º46'07.80" W, 80 m a.s.l.), in the municipality of Maceió, state of Alagoas, Brazil. According to Köppen's climate classification, this area is classified as tropical wet coastal, with an average annual temperature of 25.6 °C and annual precipitation of 1,713 mm (Alvares et al., 2013). The area is in the open ombrophilous forest formation domain. The Arboretum of Alagoas is a green urban area of 4.2 hectares, created out of an environmental recovery project. In the past, this space was widely used for agricultural purposes and constant garbage disposal. Due to the initiative of the Botany Department of the Institute of Biological and Health Sciences (ICBS/UFAL) in 2002, with the support of the Pro-Rectory of Extension (PROEX/UFAL), and the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA), under the leadership of Maria Cecília Bello, professor and biologist, seedlings

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Brazilian Journal of Animal and Environmental Research 3251 ISSN: 2595-573X of native species from around the region were implanted, aiming the recovery of the area (Santos, 2011).

2.2 DATA SAMPLING The samplings were carried out weekly from September/2019 to March/2020. Each sampling was performed from 8 a.m. to 12:00 p.m. Thus, 35 samplings days were performed, in a total of 140 hours of sampling. Butterflies were collected by a single collector with the aid of an entomological net, following pre-existing trails all through the vegetation or conducting direct searches to capture the insects during flight or when they were resting on either flowers or leaves in the vegetation. All individuals collected during this study were stored in individual envelopes and then taken to the Laboratory of Agricultural and Forestry Entomology (LEAF), located in the Campus of Engineering and Agricultural Sciences (CECA), Federal University of Alagoas (UFAL), where specimens were spread and taxonomic identification was provided.

2.3 TAXONOMIC IDENTIFICATION The taxonomic identification of the collected species was carried out to the most precise taxonomic level by consulting data from the Lepidoptera collection of the Museum of Zoology of the University of São Paulo (MZUSP) and the website Butterflies of America (Warren et al., 2018). The species were also classified according to the Trophic Guild (TG) as Fruit-feeding (Ff) or Nectar-feeding (Nf). Additionally, they were classified according to their preferred habitat as Forest (Fo), Forest edge (Fe) or Open field (Of).

2.4 ABUNDANCE FLUCTUATION Variations in species abundance among the different families of butterflies sampled throughout the study were analyzed using an abundance fluctuation curve. Subsequently, a climate graph was created based on data collected on the INMET website (National Institute of Meteorology/Brazil) to compare with the abundance fluctuation curve, and to verify whether there was an interference of temperature and rainfall in the population fluctuation of the butterfly families in the studied area.

2.5 SPECIES ACCUMULATION CURVE A species accumulation curve was performed to verify whether a greater sampling effort would result in more sampled species for the studied area. This is an excellent procedure to assess

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how close an inventory/survey came to capturing the real number of species in a given locality (Gotelli & Colwell, 2001). The curve was formulated using the PAST (Paleontological Statistics) software (Hammer et al., 2001). The calculation of the first order Jackknife and Chao1 estimators was also performed based on the number of species occurring in only one sample (Burnham & Overton, 1978, 1979; Heltshe & Forrestor, 1983; Chao, 1987), as it is shown in the following equations:

Consider, Sobs: the number of taxa observed; Q1: the number of species found in only one sample (“uniques”); m: the number of samples analyzed; F1: number of species observed with a single specimen (singletons); F2: number of species observed represented by only two specimens (doubletons).

3 RESULTS AND DISCUSSION 3.1 RICHNESS AND ABUNDANCE In 140 hours of sampling, 415 individuals were collected, with the occurrence of 44 species, distributed in 13 subfamilies, belonging to the families Nymphalidae, , Hesperiidae, , and Papilionidae (Table 1). Although currently classified as Papilionoidea (Mitter et al., 2017), Hedylidae was not recorded in this study, probably due to the nocturnal habits of this enigmatic group of Neotropical butterflies (Kawahara et al., 2018).

Table 1. List of butterfly species (Lepidoptera: Papilionoidea) collected in the Arboretum of Alagoas State (UFAL), sampled from September 2019 to March 2020. Consider: TG = Trophic Guild, Ff = Fruit-feeding, Nc = Nectar-feeding. NI = Number of Individuals per Species, NS = Number of Samplings. PH = Preferred Habitat, Fo = Forest, Fe = Forest edge, Of = Open field. Family Taxa TG PH NS NI (S = 6) Biblis hyperia nectanabis (Fruhstorfer, 1909) Ff Fe/Fo 2 2 postverta postverta (Cramer, 1779) Ff Fe/Of 1 2 Hamadryas amphinome amphinome (Linnaeus, 1767) Ff Fe 18 21 Hamadryas feronia feronia (Linnaeus, 1758) Ff Fe 18 24 Hamadryas februa februa (Hübner, 1823) Ff Fe 12 16

Mestra hersilia hypermestra (Hübner, [1825]) Ff - 2 4 Nymphalidae (S = 3) (S = 23) Scada reckia reckia (Hübner, 1808) Nf Fe/Of 8 8 Dannaus gillipus gillipus (Cramer, 1775) Nf Fe/Of 3 3 lysimnia nesaea (Hübner, 1820) Nf Fe 30 71 Heliconiinae (S = 5) Agraulis vanillae maculosa (Stichel, [1908]) Nf Of 6 7 Dryas iulia alcionea (Fabricius, 1779) Nf Fe/Of 3 3

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Eueides isabella dianasa (Hübner, [1806]) Nf Fe/Of 7 7 Euptoieta hegesia meridiania (Stichel, 1938) Nf Fe 5 5 Heliconius erato phyllis (Linnaeus, 1775) Nf Fe 18 22 Nymphalinae (S = 4) Anartia jatrophae jatrophae (Linnaeus, 1763) Nf Of 4 4 Historis odius dious (Lamas, 1995) Ff Fo 1 1 Junonia evarete evarete (Cramer, 1779) Nf Of 9 10 Siproeta stelenes meridionalis (Fruhstorfer, 1909) Ff/Nf Fo 3 3 Satyrinae (S = 3) Caligo ilioneus ilioneus (Cramer, 1775) Ff Fo 3 3 atalanta (A. Butler, 1867) Ff Fo 3 3 Opsiphanes invirae remoliatus (Fruhstorfer, 1907) Ff Fe 1 1 Cyrestinae (S = 1) Marpesia petreus petreus (Cramer, 1776) Nf Fe/Fo 3 3 Libytheinae (S = 1) Libytheana carinenta carinenta (Cramer, 1777) Nf Fe/Fo 2 3 Coliadinae (S = 7) menippe (Hübner, 1818) Nf Fe/Of 17 17 albula albula (Cramer, 1775) Nf Fe/Of 10 12 Pyrisitia leuce leuce (Boisduval, 1836) Nf Fe/Of 10 12

Eurema elathea flavescens (Chavannes, 1850) Nf Fe/Of 3 4 Pieridae Phoebis sennae marcellina (Cramer, 1777) Nf Of 10 22 (S = 9) Phoebis philea philea (Linnaeus, 1763) Nf Of 4 4 Aphrissa statira statira (Cramer, 1777) Nf Fe/Of 4 4 Pierinae (S = 2) Ascia monuste orseis (Godart, 1819) Nf Of 15 35 Glutophrissa drusilla drusilla (Cramer, 1777) Nf Fe/Of 5 5 Theclinae (S = 4) marius (Lucas, 1857) Nf - 1 1 Lycaenidae

Badecla badaca (Hewitson, 1868) Nf - 3 4 (S = 4) Strymon astiocha (Prittwitz, 1865) Nf - 2 6 Evenus regalis (Cramer, 1775) Nf Fo 1 1 Pyrginae (S = 4) dorantes dorantes (Stoll, 1790) Nf Fe/Of 18 19 Hesperiidae Urbanus simplicius (Stoll, 1790) Nf Fe/Of 15 18 (S = 4) Urbanus proteus proteus (Linnaeus, 1758) Nf Fe/Of 1 1 Pyrgus orcus (Stoll, 1780) Nf Fe/Of 3 3 (S = 2) Riodinidae Aricoris campestris (H.W. Bates, 1868) Nf Fe 9 16 (S = 2) Synargis calyce (C. Felder & R. Felder, 1862) Nf - 1 1 Papilioninae (S = 2) Papilionidae Heraclides thoas brasiliensis (Rothschild & Jordan, 1906) Nf Fe/Of 2 2 (S = 2) Battus polydamas polydamas (Linnaeus, 1758) Nf Fe/Of 2 2 S Total 44

The diversity of butterflies in urban zones is quite lower compared to natural areas because areas under anthropogenic influence have been known to cause negative effects on the richness and abundance of these insects (Lazzeri et al., 2011). These negative effects may lead to local extinctions of species more sensitive to changes caused by deforestation (Ramírez-Restrepo & MacGregor- Fors, 2017). Furthermore, other factors commonly evidenced in urban green areas, such as the high homogenization of vegetation, the reduced supply of resources (Ruszczyk, 1987), and the high

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Brazilian Journal of Animal and Environmental Research 3254 ISSN: 2595-573X degree of isolation, directly affect lepidopteran communities reducing the number of species in these areas. Some authors, when carrying out surveys of lepidopterofauna in urban environments, forest fragments inserted in anthropogenic areas or close to urban regions, also recorded reduced numbers of species richness and abundance as described in Andrade & Teixeira (2017), Pereira & Soares (2020), Porath & Aranda, (2020) and Matias & Comeli (2020). However, different butterfly families respond in distinct ways to the disturbance of their habitats (Caitano et al., 2020). As it is discussed in previous studies (e.g. Ramírez-Restrepo & Halffter, 2013), highly urbanized areas may contain lower numbers of butterfly species belonging to certain families, however, there may be high abundance of other species more adapted to the same areas (Favretto et al., 2015). Regarding species richness among the recorded families, the highest number of species was observed in Nymphalidae, with 23 species, representing 52% of the total taxa, followed by Pieridae with nine species (20% of the total). The families with the lowest richness values were Papilionidae and Riodinidae with only two species each (5% of the total) (Table 2). When it comes to the abundance, Nymphalidae had the highest representation of specimens, with 226 individuals, equivalent to 54.46% of the total, followed by Pieridae with 115 individuals, (27.71% of the total). The families with the lowest abundance values were Lycaenidae and Papilionidae, with 12 (2.98%) and four individuals (0.96%), respectively (Table 2).

Table 2. Percentage of Richness and Abundance of butterfly families (Lepidoptera: Papilionoidea) sampled in the Arboretum of Alagoas State (UFAL), from September/2019 to March/2020. Consider: r% = Richness in percentage, N = Abundance and N% = Abundance in percentage. Families Subfamilies Genera Species r% N N% Nymphalidae 7 21 23 52 226 54.46 Pieridae 2 8 9 20 115 27.71 Hesperiidae 1 2 4 9 41 9.88 Lycaenidae 1 4 4 9 12 2.89 Riodinidae 1 2 2 5 17 4.10 Papilionidae 1 2 2 5 4 0.96 Total 13 39 44 100 415 100

3.1.1 Nymphalidae Nymphalidae has 12 subfamilies, ten of then recorded for Brazil: Libytheinae, Danainae, Limenitidinae, Heliconiinae, Apaturinae, Biblidinae, Cyrestinae, Nymphalinae, Charaxinae and Satyrinae (Wahlberg et al., 2009). In the world there are 6,300 species known for this family (Wahlberg et al., 2009) and, except for the poles, nymphalids have a cosmopolitan distribution (Powel, 2009). However, the greatest diversity of species for Nymphalidae is found in the neotropics, with approximately 2,430 species recorded. In Brazil, Nymphalidae comprises about 790 species (Orlandin, 2016).

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In the present study, Nymphalidae is distributed in seven subfamilies: Biblidinae (S = 6), Heliconiinae (S = 5), Nymphalinae (S = 4), Danainae (S = 3), Satyrinae (S = 3), Cyrestinae (S = 1), and Libytheinae (S = 1). The greatest richness and abundance observed for Nymphalidae is probably due to being the richest family of diurnal butterflies in the Neotropical region, especially in Brazil (Bogiani et al., 2012). According to Duarte et al. (2012), Nymphalidae is one of the most diversified families regarding habitats, which favors its occurrence and abundant distribution in all tropical and subtropical regions. Moreover, as highlighted by Lamas (2004), most Neotroprical nymphalid communities may be found in distinct habitats, formed by anthropic environments interconnected or not to natural habitats of different sizes, shapes and stages of disturbance. This characteristic makes Nymphalidae a widespread group, with variety of morphological traits, which, in turn, may be correlated with the adaptation to different ecological niches. Among the subfamilies of Nymphalidae recorded in this study, the greatest richness was observed in Biblidinae and may be justified by the fact that these butterflies are highly tolerant of environmental fragmentation (Uehara-Prado et al., 2007; Santos, 2020).

3.1.2 Pieridae In Brazil Pieridae is represented by the subfamilies Dismorphiinae, Pierinae and Coliadinae (Duarte et al., 2008; Heppner, 2008a). With around 1,200 described species distributed worldwide and 65 species estimated for Brazil (Leite et al., 2007; Duarte et al., 2008). In this study, Pieridae is represented by two subfamilies, Coliadinae (S = 7) and Pierinae (S = 2). In Brazil Pieridae is one of the most widely distributed families, despite the low number of species (Iserhard et al., 2017), with most of these taxa found in modified habitats with a high degree of anthropization (Zacca et al., 2011; Morais et al., 2012; Martins et al., 2017). The subfamily Coliadinae (S = 7) comprises the largest number of sampled species and was diagnosed as the one with the greatest frequency in areas with high degree of disturbance (Paluch et al., 2011). Therefore, this subfamily is considered to be one of the most tolerant and well-adapted groups of butterflies to urban environments (Kerpel et al., 2014). Thus, the abundant presence of Pieridae in open areas and in regions with spaced trees, such as squares, is quite characteristic, where the taxa can be constantly observed throughout the year (Arce et al., 2014).

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3.1.3 Hesperiidae Hesperiidae has a widespread distribution, except in the poles and in New Zealand. It is well represented in the Neotropical region, with approximately 2,300 species. Brazil houses around 1,160 species distributed in four subfamilies, Pyrrhopyginae, Pyrginae, Heteropterinae and Hesperiinae (Duarte et al., 2012; Mielke et al., 2012). In the present study only Pyrginae was recorded, represented by four species. Many Hesperiidae species are known as good bioindicators (Mielke et al., 2012) and true “flags” for the conservation of several ecosystems as they respond quickly to environmental changes (Dessuy & Moraes, 2007), especially in regularity and abundance of floral resources (Brown Jr & Freitas, 2000). Therefore, the low representation of individuals in this family may indicate alterations or disturbances in the studied area.

3.1.4 Lycaenidae and Riodinidae Lycaenidae has a worldwide distribution, yet it is more diversified in the Neotropical region, where it is found 40% of the species diversity (Heppner, 2008b). Even though morphological and molecular data corroborate the hypothesis that Riodinidae is a subfamily of Lycaenidae (Cong et al., 2017), most authors agree that they are two distinct families; however, they are phylogenetically closer to each other than to other families of Papilionoidea. Thus, they will be discussed together. Among the diurnal butterflies, Lycaenidae has the second highest species richness after Nymphalidae (Duarte et al., 2008), being widely considered as an important indicator of environmental quality because they may respond quickly to disturbances in their natural environment. They may be loyal to their microhabitat and some species are highly specialists in a few host plants (Ritter et al., 2011). Thus, the low richness of Lycaenidae observed in this study may be related to the sensitivity of this family to urban environments and its demand for food resources (Soares et al, 2012). Riodinidae has five subfamilies: Styginae, Hamearinae, Euselasiinae, Corrachiinae and Riodininae (Duarte et al., 2012), occurring almost exclusively in the Neotropical region, where approximately 95% of the richness for this family is recorded (Hall, 2002; Duarte et al., 2012; Siewert et al., 2014; Seraphim et al., 2018). These butterflies have different patterns of color and shapes, with sizes ranging from small to medium compared to specimens of other families of butterflies (Lemes, 2018). As for Lycaenidae, the low richness of Riodinidae in the studied area may be understood because these butterflies are known to be very narrowly distributed in some specific habitats, which can vary even between similar and close environments. It makes them very sensitive to variations

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Brazilian Journal of Animal and Environmental Research 3257 ISSN: 2595-573X and disturbances in their natural habitats (Nobre et al., 2008). Moreover, many riodinids are found only during certain periods of the day and in some months of the year. This fact may clarify why there is a lack of representation for this family in surveys and in most butterfly samplings (Hall, 2004).

3.1.5 Papilionidae Papilionidae is considered as one of the butterfly families with the smallest number of species (Duarte et al., 2008) and with few species in Brazil (Francini et al., 2011; Martins et al., 2017). Even though the vast majority of papilionids are considered widely distributed all throughout the country (Zacca et al., 2011; Morais et al., 2012; Martins et al., 2017), the number of species may still have been underestimated, as individuals of this family are exceedingly difficult to capture. Only two species of the subfamily Papilioninae were recorded, Heraclides thoas brasiliensis (Rothschild & Jordan, 1906) and Battus polydamas polydamas (Linnaeus, 1758). The former is easily found in naturally disturbed environments and cities (Schwartz & Di Mare, 2001; Sackis & Morais, 2008). Regarding the low representation of Papilionidae, Gonzalez (2008) suggests that butterflies with larger body sizes, such as papilionids, may be more sensitive to environmental variations due to habitat fragmentation, being indicators both directly of the effects on the landscape and indirectly of the effects in biotic changes. In addition, the small number of Papilionidae in the UFAL’s Arboretum is probably still related to the lack of water resources in the area. Also, it may be due to the small size of the studied area, once that according to Brown Jr & Freitas (1999), the species of this family are usually found in preserved forests with an abundance of water resources.

3.2 ABUNDANCE FLUCTUATION We noticed that, in overall, there were variations in the abundance of butterfly species throughout the months sampled, with lowest values being recorded in January/2020 and the peak in March/2020 (Figure 1).

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70 Nymphalidae 60 Pieridae

50 Hesperiidae

Lycaenidae 40 Riodinidae

30 Papilionidae

20

Number of specimens sampled Families sampled of / Number specimens 10

0 sep/19 oct/19 nov/19 dec/19 jan/20 feb/20 mar/20 Months of sampling

Figure 1. Abundance curves of butterfly families (Lepidoptera: Papilionoidea) sampled in the Arboretum of Alagoas State, over 7 months of sampling.

Expressive drops were registered in the abundance curves for the families Nymphalidae, Pieridae, Hesperiidae and Papilionidae, from October/2019 to January/2020, when the lowest value of abundance of collected individuals was observed. Growths in the number of individuals for all families, except Papilionidae, were observed in February/2020, being registered in this month, the occurrence of individuals of new families for the studied area, these being Lycaenidae and Riodinidae. The maximum taxon abundance for all families, except Papilionidae, was seen in March/2020, period in which, Nymphalidae and Pieridae recorded the highest abundance values. One of the explanations for theses fluctuations in abundance values is probably related to climatic variations through the sample period. When observing the average precipitation values (Figure 2), the abundance of the butterfly families strongly correlates with the variations in rainfall in the studied area. With sharp drops recorded from October/2019 to January/2020, the month in which the minimum rainfall values was observed (5 mm), and growth from February/2020 on, reaching the maximum rainfall values (198 mm) in March/2020. On the other hand, the abundance for the families correlates with an inverse growth trend to the average temperature over the sampling months (Figure 2), which presented a continuous growth from September/2019 to the maximum temperature value (28.51 °C) recorded in February/2020.

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29 250

200

) 28

150

27 Temperature(°C

100 (mm) Precipitation

26 50

25 0 sep/19 oct/19 nov/19 dec/19 jan/20 feb/20 mar/20

Average Precipitation (mm) Average Temperature (°C)

Figure 2. Climate Graph - Average temperature (°C) and Average precipitation (mm) in the city of Maceió - Alagoas State, over 7 months of sampling (from September/2019 to March/2020). Created in accordance with INMET – National Institute of Meteorology - Brazil.

Therefore, it is possible to see that the fluctuation in the population curves was directly proportional to rainfall and showed growth trends in milder temperatures. Recording minimum values as rainfall decreased and temperature rose, and a growth of values as humidity rose and temperature decreased. Bernardi et al. (2011) state that temperature and precipitation directly affect the abundance fluctuation of Lepidoptera (Papilionoidea), indicating that these insects can increase their populations under favorable environmental conditions and decrease under unfavorable conditions. Thus, some lepidopteran species may present seasonality, with peaks of abundance in certain seasons of the year (Santos, 2012), correlating with temperature (Brown Jr & Freitas, 2000) and rainfall as described by Nobre et al. (2008) and Zacca & Bravo (2012), which indicated a greater diversity of butterflies during rainy periods in the Caatinga biome. Based on the data of this research, the same trends possibly occurs in the Atlantic Forest of the coastal zone of Maceió - Alagoas State. These abiotic factors still might interfere in the abundance of butterfly families by influencing the availability of floral resources (Lima & Zacca, 2014).

3.3 SPECIES ACCUMULATION CURVE We noticed that the values of species collected were remarkably close to the values estimated by the diversity indicators, with cases in which the accumulation curve reached the same result as those suggested by the applied indicators. As it was seen for Pieridae and Papilionidae that featured

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Brazilian Journal of Animal and Environmental Research 3260 ISSN: 2595-573X a number of sampled species that coincides with the values suggested by the Jackknife1 and Chao1 estimators. In other families such as Nymphalidae and Hesperiidae, the number of sampled species was remarkably close to the number suggested by the applied estimators (Figure 3).

Figure 3. Cumulative species curve, Jackknife1 and Chao1 estimators recorded for six butterfly families in the Arboretum of Alagoas State, over 7 months of samplings (from September/2019 to March/2020).

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Ernesto (2013) explains that in cases where the curve stabilizes, it means that approximately all the richness of the area was sampled. If the curve shows a tendency to grow, the number of samplings is not enough to record the total number of species in the studied area. Therefore, the results evidenced by this study indicate that the sampling effort employed in the studied area possibly has been reached, however, the local richness of the butterfly fauna is still underestimated, and more species shall be added with greater sampling effort. One efficient way to verify whether the number of sampled species approaches the estimated number for the studied area is through the analysis of the first-order Jackknife and Chao1 estimators, which define the number of individuals that would be found with a greater sampling effort. For our data, the extension of the samplings would probably register a total of 50 (Jackknife1) or 47 species (Chao1), numbers considerably close to that achieved for the studied area (44 species). Some studies have suggested that Jackknife1 and Chao1 estimators are quite efficient to estimate the number of butterfly species with a greater sampling effort as in Lima & Zacca (2014) and Pereira et al. (2018).

4 CONCLUSIONS In general, the species collected in the Arboretum of Alagoas State (UFAL) are commonly found in anthropized environments and open green areas, such as squares and parks. Despite the small size of the Arboretum and the fact that it is surrounded by urban areas under constant anthropization, it is possible to state that many butterfly species were sampled. This value would probably increase with a greater sampling effort, as it is indicated by the cumulative curve of species, the Jackknife1 and Chao1 estimators. It was also observed that the species abundance of the studied area showed correlations to rainfall with growth trends in mild temperatures. Therefore, the Arboretum of Alagoas State may be considered an important environment for the conservation of butterfly species, pointing it out as an important environmental refuge place for the butterfly fauna in Maceió, state of Alagoas. Thus, it is stated that small green areas in urban zones are of great biological value for the maintenance and composition of the butterfly fauna.

ACKNOWLEDGEMENTS Marcelo Duarte is grateful to FAPESP (grants 2002/13898-0, 2003/13985-3 and 2016/50384-8), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (PROTAX II – grant 440597/2015- 3), Conselho Nacional de Desenvolvimento Científico e Tecnológico (grants 305905/2012-0, 311083/2015-3 and 312190/2018-2), and Universidade de São Paulo (Projeto 1, Pró-Reitoria de

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Pesquisa). Lucas Teles Bezerra is grateful to Universidade Federal de Alagoas (UFAL), Museu de Zoologia da Universidade de São Paulo (MZUSP) and to the Coordenação do Arboretum de Alagoas. We also thank Dr. Simeão Moraes (State University of Campinas, São Paulo, Brazil) for reviewing and editing this manuscript.

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