Immature stages of the threatened butterfly Euptychia boulleti (Le Cerf, 1919) (Nymphalidae: Satyrinae) from the Brazilian Atlantic Forest and its conservation perspectives

ABSTRACT

The present paper describes the immature stages of the Neotropical satyrine butterfly Euptychia boulleti (Le Cerf, 1919) from the Brazilian Atlantic Forest. Eggs were laid singly on the under surface of the fronds of its host plant, Selaginella muscosa Spring (Lycopodiopsida: Selaginellaceae). Larvae are solitary in all instars, with a color pattern and shape that make them cryptic on their host plants. The pupa is short and smooth, green with black and white markings. Although the adults are very divergent in wing pattern, the immature stages are very similar to those of other species in the genus Euptychia Hübner, 1818. The present study added over 20 more records of E. boulleti, adding two additional sites for this species. Based on all available records, the EOO (extent of occurrence) has an increase of 13% and AOO (area of occupancy) an increase of 20% compared to previous estimates. Identifying additional E. boulleti populations could be important for conservation efforts of this species, especially if these are in fully protected areas.

Keywords:  Butterfly; Camouflage; Euptychiina; Lepidoptera; Selaginella

Introduction

In the last Brazilian Red List, 63 butterfly taxa were listed as threatened, out of which 59 taxa (93.6%) are present in the Atlantic Forest (MMA, 2022). This biome, highly fragmented and threatened itself (Myers et al., 2000; Vancine et al., 2024), also includes most locality records for endangered butterflies (Rosa and Freitas, 2024). Conservation actions are even more critical and urgent considering most of these records are located outside fully Protected Areas (PAs) (sensuRosa and Freitas, 2024).

The small euptychiine Euptychia boulleti (Le Cerf, 1919) (Nymphalidae: Satyrinae), assessed as a Critically Endangered (CR) species (MMA, 2022), is restricted to very few localities of montane forest in the Atlantic Forest (Freitas et al., 2012). Very little information on the natural history and behavior of this species is available, hampering potential actions toward its conservation (Freitas and Marini-Filho, 2011; Freitas et al., 2012). In addition, five out of the 12 locality records are outside PAs, indicating suboptimal conservation opportunities for the species (Rosa and Freitas, 2024).

The genus Euptychia Hübner, 1818 includes about 37 described and 15 undescribed species (Warren et al., 2024; Zacca et al., 2024). It is worth noting that there is a lack of complete biological information for most Euptychia species (Freitas et al., 2019). For instance, there are only partial descriptions or pictures of immature stages of Euptychia for a handful of species (Purves and Orians, 1983; Singer et al., 1983; DeVries, 1987; Brévignon, 2008; Hamm and Fordyce, 2016; Janzen and Hallwachs, 2024;), and a single publication that provides detailed descriptions of all immature stages of Euptychia mollina Hübner, 1818 from the Brazilian Amazon (Freitas et al., 2019). Larvae of all species are reported feeding on species of Selaginella (Lycopodiopsida: Selaginellaceae); a single exception, Euptychia insolata A. Butler & H. Druce, 1872, was reported using the moss Neckeropsis undulata (Hedw.) Reichardt (Bryopsida: Neckeraceae) (see Singer et al., 1971, 1983; DeVries, 1987; Freitas et al., 2019).

In the present paper, we present a detailed description of the immature stages of Euptychia boulleti and data on its behavior, natural history, geographical distribution, and conservation perspectives. This is the first paper illustrating in detail all life stages for this threatened butterfly species, and also the first describing the immature stages for a species of Euptychia from the Atlantic Forest.

Material and methods

Adults and immature stages of E. boulleti were studied in three localities of montane Atlantic Forest in the State of Rio de Janeiro, Southeastern Brazil: 1) Parque Nacional do Itatiaia (PNI), Itatiaia (22°25'S 44°37'W), 900-1400 m (Figs. 1A, B); 2) Reserva Ecológica de Guapiaçu (REGUA), Cachoeiras de Macacu, Trilha Vermelha, (22°27'S 42°46'W), 990-1000 m; 3) Reserva Particular do Patrimônio Natural Alto da Figueira (RPPN Alto da Figueira), Nova Friburgo, (22°22'S 42°29'W), 1100-1400 m (Figs. 1C, D).

Figure 1
Habitat and host plants of E. boulleti: (A, B). Itatiaia National Park, Itatiaia, Rio de Janeiro; (C, D) RPPN Alto da Figueira, Nova Friburgo, Rio de Janeiro; (E, F). Two views of Selaginella muscosa Spring, the larval host plant of E. boulleti.

Eggs and larvae were obtained in the field by searching the host plants (after the observation of an ovipositing female) in the RPPN Alto da Figueira in November 2023. In addition, eggs were also expressed from wild-caught females (as in Freitas, 2004). The plant on which eggs were found, Selaginella muscosa Spring (Lycopodiopsida: Selaginellaceae) (Fig. 1E, F), was potted and maintained in the laboratory to feed the larva. The eggs and larvae were reared in plastic containers cleaned daily and provided with fresh plant material every two or three days (following Freitas et al., 2019). Data were recorded on morphology and development time for all stages. Dry head capsules and the pupal case were retained in glass vials. Voucher specimens of the immature stages and adults were deposited in the Zoological Collection (ZUEC) of the Museu de Diversidade Biológica (MDBio), Universidade Estadual de Campinas, Campinas, São Paulo, Brazil.

Measurements were taken and general aspects of morphology were observed using a Leica®MZ7.5 stereomicroscope equipped with a micrometric scale. Scanning electron microscopy (SEM) was conducted using a JEOL^® JSM-5800 microscope, and samples were prepared in accordance with the following protocol: Sample critical point dried using Bal-tec^® - CPD030 equipment and attached with double stick tape to aluminum stubs; gold/palladium coated with a Bal-tec^® - SCD050 sputter coater. Egg size is presented as height and diameter, and head capsule size is the distance between the most external stemmata (as in Freitas, 2007). Terminology for early stages descriptions follows García-Barros and Martín (1995) for eggs and Stehr (1987) for larvae and pupae. For the distribution map, localities and categories of Protected Areas (fully protected or not) were obtained from Rosa and Freitas (2024).

Geographical range (extent of occurrence EOO and area of occupancy AOO) was estimated based on all known sites of E. boulleti. The EOO is the area contained within the shortest continuous boundary (minimum convex polygon) that includes all known distribution points of a species, and the AOO is the area within its EOO that is actually occupied by a given taxon (IUCN, 2012, 2022). The EOO as recommended by IUCN includes all areas across the taxon’s geographical distribution to measure the degree to which risks from threatening factors are spread spatially, even if this is on land and/or ocean. Both EOO and AOO were estimated using the online open-source program GeoCAT (Geospatial Conservation Assessment Tool, available at http://geocat.kew.org) (Bachman et al., 2011). As recommended by IUCN for AOO analyses, a 2 km grid of all cells (area of 4 km²), which contain distribution points for the species, was used (IUCN, 2012, 2022).

Results

Egg (Figs. 2A, B). Yellow, round without visible markings. Height 0.64 – 0.70 mm (mean = 0.66 mm, SD = 0.022) and diameter 0.64 – 0.66 mm (mean = 0.65 mm, SD = 0.011, n=5); duration 12-13 days (n = 4).

Figure 2
Immature stages of E. boulleti: (A, B) Egg, dorsal and lateral; (C, D) First instar, lateral and dorsal; (E, F) Second instar, lateral and dorsal; (G, H) Third instar, lateral and dorsal; (I, J) Fourth instar, lateral and dorsal; (K, L) Fifth (last) instar, lateral and dorsal; (M, N, O) Pupa, lateral, ventral and dorsal; (P) Reared adult male.

First instar (Figs. 2C, D, 3A, B, C). Head capsule width 0.42 – 0.48 mm (mean = 0.46 mm, SD = 0.023); head scoli 0.06 mm (n = 6). Head black, bearing a pair of short scoli on vertex. Third stemma larger than other stemmata. Body light green with several small protuberances; caudal filaments short. Legs and prolegs light green. Setae light green; most dorsal and subdorsal setae clubbed at tip (Fig. 3C). Maximum length 3.5 mm. Duration 4-10 days (n = 6).

Figure 3
Scanning electron microscopy of first instar of E. boulleti: (A) General view (bar = 200 µm); (B) Lateral view of head (bar = 100 µm); (C) Detail of a body seta (bar = 20 µm).

Second instar (Figs. 2E, F). Head capsule width 0.60 – 0.62 mm (mean = 0.61 mm, SD = 0.010); head scoli 0.28 – 0.34 mm (mean = 0.32 mm, SD = 0.020, n = 6). Head black, with two short pointed scoli on vertex. Body green, with poorly marked whitish longitudinal stripes and covered with small protuberances giving a rough appearance to the larva; caudal filaments short. Legs and prolegs light green. Maximum length 5 mm. Duration 6-8 days (n = 6).

Third instar (Figs. 2G, H). Head capsule width 0.78 – 0.88 mm (mean = 0.84 mm, SD = 0.033); head scoli 0.50 – 0.58 mm (mean = 0.53 mm, SD = 0.030, n = 7). Very similar to second instar in color and general shape. Maximum length 7 mm. Duration 6-10 days (n = 6).

Fourth instar (Figs. 2I, J). Head capsule width 1.02 – 1.30 mm (mean = 1.20 mm, SD = 0.081); head scoli 0.60 – 0.70 mm (mean = 0.64 mm, SD = 0.032, n = 8). Head green, with brown areas on lateral head and scoli, with two diverging short pointed scoli on vertex. Body green, with several short dorsal and lateral white chalazae, with oblique dark/light markings converging dorsally; legs and prolegs green; caudal filaments short. Maximum length 11 mm. Duration 9-12 days (n = 7).

Fifth (last) instar (Figs. 2K, L). Head capsule width 1.74 – 1.86 mm (mean = 1.77 mm, SD = 0.063); head scoli 0.70 – 0.80 mm (mean = 0.76 mm, SD = 0.043, n = 8). Head green, with light brown areas on lateral head and scoli, with two diverging short scoli on vertex. Body green, with several short dorsal and lateral white chalazae, with oblique dark/light markings converging dorsally; legs and prolegs green; caudal filaments short, white, green at base. Maximum length 16 mm. Duration 13-17 days (n = 7).

Pupa (Figs. 2M, N, O). Short and smooth; mostly green with several black areas and mottled with white markings, with short ocular caps; cremaster broad, dark in ventral portion; dorsal abdomen with elevated ridges in each segment, black and outlined with a white stripe. Total length 7-8 mm (n = 7). Duration 14-16 days (n = 4).

Behavior and natural history.Euptychia boulleti (Fig. 1P) is very localized in some montane habitats above 1100 m. Males and females are seldom observed together, and show marked differences in behavior and habitat preference. Males are usually observed on mountain tops with clearings (or covered with low vegetation), above 1500 m, where they display an apparent territorial behavior from 12:00 to 13:00 (Freitas et al., 2012; present study) (Fig. 1D). Males resemble some Lycaenidae, particularly the sympatric Arawacus meliboeus (Fabricius, 1793) (a similarity already noted by Le Cerf, 1919) and Arawacus separata (Lathy, 1926); besides the similar wing pattern, hilltopping males remain perched on leaves and present a similar behavior of flying and frequently spinning in circles during the flight when disturbed (observations made by the authors on REGUA and RPPN Alto da Figueira; and also by R. K. Robbins and A. Caldas in PNI, pers. comm.). It is known that jumping spiders (Salticidae) avoid attacking some hairstreaks (Lycaenidae) (Sourakov, 2013). In this case, E. boulleti could gain protection by being similar to the above-mentioned Lycaenidae species. Also, the pattern of dark stripes converging towards a red spot at the anal angle of the hindwings is somewhat similar to the “false head” described for several lycaenids and could provide protection by deflecting attacks towards this non-vital area (Robbins, 1980). However, if these similarities in behavior and color pattern are to some extent related to mimicry or the “false head” hypothesis, that is a subject for future studies. Females are more often observed at lower altitudes (1100-1300 m) flying near the ground in ravines and slopes where the larval host plant, Selaginella muscosa, is locally abundant (Figs. 1A, C). The larvae are solitary in all instars and their color pattern and shape make them cryptic on the fronds of their host plant. In the wild, eggs were laid individually underneath the leaves and strobili (the reproductive organs of S. muscosa) of the host plants growing in low densities in partially shaded areas. In the laboratory, larvae placed on different species of Selaginella from Rio de Janeiro began to feed within the first two days, but then stopped and rejected the host plant.

Habitat, distribution and geographical range. Based on all available information, E. boulleti occurs at 12 localities in the montane Atlantic Forest in the Brazilian states of Rio de Janeiro and Espírito Santo (Freitas et al., 2012; Rosa and Freitas, 2024, ^{Table S1}, Fig. 4), with a small distribution gap from Itatiaia to Petrópolis municipalities (about 150 km), and a large gap from central Rio de Janeiro to south Espírito Santo States (about 320 km). Most of these localities are wet forests above 1000 m, except for the region of Santa Teresa municipality and vicinities, where E. boulleti occurs at much lower elevations ranging from 600 to 800 m, with at least one reliable record at 300 m on the slopes of the nearby mountains. However, even with this exception, it is quite clear that E. boulleti is typically a montane species. All localities of E. boulleti share a common characteristic - they are covered by wet forests. This could be related to the persistence of its larval host plants, as species of Selaginella are strongly associated with high-humidity environments (Setyawan et al., 2016). Based on all available records, the EOO was estimated to be 33,356.57 km² and the AOO was estimated to be 48 km².

Figure 4
Map showing the known geographical distribution of E. boulleti.

Discussion

Natural History and immature stages

Euptychia boulleti is a species of the genus Euptychia with a unique and noticeable wing pattern that led to its description three times in three different genera in the first half of the twentieth century (Le Cerf, 1919; Joicey and Talbot, 1924; Gagarin, 1936). Its placement in the genus Euptychia was proposed almost a century later based on morphology and molecular data (Freitas et al., 2012; see also Espeland et al., 2023). In this study, the larval host plant and immature stages reinforce this placement in the genus Euptychia; although the adults of E. boulleti are quite divergent in wing pattern, the immature stages are very similar to those of other known species of Euptychia (Freitas et al., 2019 and references therein). Several previous studies also showed that immature stages of butterflies are conservative and help to unveil taxonomic questions (e.g. Brown Junior and Freitas, 1994; Freitas et al., 1997, 2002; Freitas and Brown Junior, 2004). In short, the present results reinforce the idea that the immature stages are an important source of information in studies of butterfly taxonomy and systematics.

In general, the immature stages of E. boulleti resemble those described for other Euptychia species (Freitas et al., 2019 and references therein). The yellow eggs of E. boulleti is a novelty, known eggs of other species of Euptychia are white or green (Singer and Mallet, 1986; DeVries, 1987; Freitas et al., 2019). However, information about the eggs is available for only four species (including this study), making it impossible to identify any patterns until more data is obtained. The larvae of E. boulleti are similar to those of all other Euptychia, with the chalazae a bit more developed than those of E. mollina, E. westwoodi A. Butler, 1867 and E. neildi Brévignon, 2005 (DeVries, 1987; Brévignon, 2008; Freitas et al., 2019), but not as developed as in E. insolata (DeVries, 1987). Pupae are also similar in shape but lack the dorsal shelf present on pupae of E. mollina, E. westwoodi and E. neildi (see references above). It is important to note that the present study contributes to filling the gaps of knowledge of immature stages in the phylogeny of Euptychia, as all other species with known immatures belong to different lineages of Euptychia (see Espeland et al., 2023). However, without a comprehensive phylogeny of Euptychia and knowledge of immature stages, hypotheses of morphological evolution cannot be made. Therefore, the search and description of the immature stages of additional species of Euptychia are highly encouraged.

Conservation perspectives of E. boulleti

The present study added over 20 more records of E. boulleti, in addition to those published by Freitas et al. (2012). However, only two records represent sites previously unknown for this species, the first in Petrópolis municipality, and the second in RPPN Alto da Figueira in Nova Friburgo municipality, both in Rio de Janeiro State. However, these new records did not significantly expand the known regions of occurrence, as they are from localities nearby to previously known areas of occurrence of E. boulleti (Fig. 4, ^{Table S1}). Based on all available records, the EOO has an increase of 13% and AOO an increase of 20% compared to previous estimates (Rosa et al., 2023b). Nevertheless, both records are present in two PAs (RPPN Alto da Figueira, a private reserve, and Parque Nacional da Serra dos Órgãos, a national park), the latter being a fully protected area that may offer new opportunities for the conservation of this species.

However, some large areas of suitable habitats for E. boulleti are still present in the large distribution gap from central Rio de Janeiro and south Espírito Santo. Although a large part of this area consists of lowlands (not suitable for E. boulleti), this gap includes the mostly unknown Parque Estadual do Desengano (Desengano State Park), in north Rio de Janeiro, a large block of more than 25,000 hectares of well-preserved forests, including large extensions of montane forests at altitudes of 1100 to 1500 m (Soffiati, 2009). A second region is the south portion of Espírito Santo, where a mosaic of montane forests with different degrees of conservation, small cities, and crops mostly restricted to small properties create a complex landscape that favors the local biodiversity. In this region, two other rare montane butterfly species that occur in sympatry with E. boulleti were previously reported, namely the clearwing Episcada vitrea R.F. d'Almeida & O. Mielke, 1967 (Nymphalidae: Danainae) and the metalmark Petrocerus catiena (Hewitson, 1875) (Riodinidae) (Rosa et al., 2023a, 2023b). In both areas, however, butterfly inventories are low or absent, and identifying E. boulleti populations in these two regions could be important for conservation efforts of this species, especially in a fully protected area such as the Desengano State Park. Other important steps to improve the knowledge of this species are: 1) to carry out detailed behavioral studies of both sexes, including the putative male territorial behavior and female choice for oviposition sites; 2) to infer the effective population sizes based on genomic data in different regions; 3) to identify potential areas of occurrence based on analyses of distribution modeling; and 4) propose new conservation areas where this species is present. Ultimately, the maintenance of large extensions of well-preserved montane forests is the only way to ensure the persistence of this species in the future.

Supplementary Material

The following online material is available for this article:

Table S1

Data for individuals of Euptychia boulleti (all from Brazil) from collections and field observations. The table presents only data not included in the previous study of Freitas et al. (2012).

Acknowledgements

Thanks to Alexandre Antonelli and Thomas Berg for all their support during fieldwork in RPPN Alto da Figueira and to Jorge Bizarro for support in REGUA. Shinichi Nakahara revised the last version and made valuable contributions. To Stina Weststrand (Gothenburg Botanical Garden) for the Selaginella species identification. To Keith Willmott and an anonymous referee for carefully revising and giving valuable suggestions on the submitted version of the manuscript.

• Funding
  AVLF acknowledges support from FAPESP (grants 2011/50225-3 and 2021/03868-8), from the Brazilian Research Council – CNPq (421248/2017-3 and 304291/2020-0), and from the National Science Foundation (DEB-1256742). AHBR thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 and Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq (151203/2024-5). JYOC acknowledges support from Antonelli Foundations. EPB acknowledges support from FAPESP (2016/15873-8 and 2018/21432-0) and CNPq (174863/2023-3) for post-doc fellowships. This publication is part of the RedeLep ‘Rede Nacional de Pesquisa e Conservação de Lepidópteros’ SISBIOTA-Brasil/CNPq (563332/2010-7). The present study is registered at the SISGEN (A1B92D5).

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Edited by

• Associate Editor:
  Thamara Zacca

Publication Dates

• Publication in this collection
  04 Nov 2024
• Date of issue
  2024

History

• Received
  19 July 2024
• Accepted
  16 Sept 2024