Orthoptera: Grylloidea: Phalangopsidae) from Caves of Eastern Brazil: Evidence of Isolation in the Subterranean Realm and Discussion About Troglomorphisms

Zootaxa 4032 (3): 297–308 ISSN 1175-5326 (print edition) www.mapress.com/zootaxa/ Article ZOOTAXA Copyright © 2015 Magnolia Press ISSN 1175-5334 (online edition) http://dx.doi.org/10.11646/zootaxa.4032.3.5 http://zoobank.org/urn:lsid:zoobank.org:pub:E72D6FD7-3369-401F-95AA-D19866972B2B Endecous peruassuensis n. sp. (Orthoptera: Grylloidea: Phalangopsidae) from caves of Eastern Brazil: evidence of isolation in the subterranean realm and discussion about troglomorphisms

MARCIO P. BOLFARINI1, 2 & MARIA ELINA BICHUETTE1 1Laboratório de Estudos Subterrâneos, Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de São Carlos, rod.Washington Luis, km 235, 13565-905, São Carlos, SP, Brazil 2Corresponding author. E-mail: [email protected]

Abstract

We describe a new species of the genus Endecous Saussure (1878), recorded at the Lapa do Cipó and Olhos d’Água caves, which are located in the Itacarambi municipality, Minas Gerais state, Eastern Brazil. Another species, E. aguassay Mews, 2008 was recordedin the surroundings of the caves. The genus Endecous corresponds to the most common cricket in Bra- zilian hypogean environments. In general, these crickets inhabit the areas around cave entrances up to the aphotic zones of caves. The genus Endecous is the only cave cricket to present troglobiomorphosis, i.e., an apterous condition. The distribution of the new species is limited to these two caves, which suggests an endemism in this karst system similar to the distribution of other endemic animals, such as harvestmen and amblypygid arachnids. This species is the sixth troglobitic one described for Olhos d’Água cave, which sets this cave as a spot of subterranean fauna in Brazil.

Key words: new species, cave cricket, subterranean environment, Peruaçu Caves National Park

Introduction

Gorochov (2014) proposed a classification for the subfamily Phalangopsinae (regarded here as the family Phalangopsidae) and synonymized the tribe Luzarini Hebard, 1928 with the tribe Phalangopsini Blanchard, 1845. The author proposed several subtribes for the Luzarini tribe and included the genus Endecous Saussure, 1878 in the subtribe Modestozarina Gorochov, 2014 based on the following characters: maxillary palpi thinner and longer, hind tibia with dorsal inner apical spur, longest and ectophallic fold (rachis) of male genitalia long or moderately long and with a finger-like or angular apex. In that study, the author also divided the genus into three subgenera: the subgenus Pedroecous Gorochov, 2014, monotypic, for the species E. Apterus Bolfarini & Souza-Dias, 2014; the subgenus Notendecous Gorochov, 2014 for the species E. Onthophagus (Berg, 1891) and E. Lizeri Rehn, 1918; and the subgenus Endecous Saussure, 1878 for the remaining species, namely E. abbreviates Piza, 1960; E. aguassay Mews, 2008; E. alejomesai Zefa, 2010; E. arachnopsis Saussure, 1878; E. betariensis de Mello & Pellegatti- Franco, 1998; E. cavernicolus Costa Lima, 1940; E. itatibensis Rehn, 1918; E. ferruginosis Bruner, 1916; E. hubbelli Liebermann, 1965; E. onthophagus (Berg, 1891); E. lizeri Rehn, 1918; and E. ubajarensis Zefa, 2014. This subgenus was proposed mainly based on the characters of the phallic complex and tegmina (e. g., wings absent in both sexes of E. apterus). The genus Endecous is common in Brazilian caves and is mentioned in several lists of cave fauna (Trajano, 1987; Pinto-da-Rocha, 1996b; Trajano & Bichuette, 2010) in taxonomic descriptions (Saussure, 1878; Berg, 1891; Bruner, 1916; Rehn, 1918; Costa Lima, 1940; Piza, 1960; Liebermann, 1965; de Mello & Pellegatti-Franco, 1998; Mews & Sperber, 2008; Zefa et al. 2010, 2014; Souza-Dias et al., 2014), in cytotaxonomy (Zefa et al. 2010, 2014) and in evolutionary biology studies (Trajano & Bichuette, 2010). The genus Endecous comprises species with troglophilic populations found in burrows, holes and natural cavities, which frequently leave these sites towards the surface.

Accepted by D. Rentz: 21 Sept. 2015; published: 16 Oct. 2015 297 Seven species of the genus Endecous have populations described in hypogean environments: E. onthophagus (Berg, 1891); E. itatibensis Rehn, 1918; E. cavernicolus Costa Lima, 1938; E. betariensis Pellegatti & Mello- Franco, 1998; E. alejomesai Zefa, 2010; E. apterus Bolfarini & Souza-Dias, 2014; and E. ubajarensis Zefa, 2014. In addition, there are other five species tha thave troglophilic populations, i.e., species with source populations in both epigean and hypogean environments, where the individuals move between these habitats and promote gene flow. These inferences are in agreement with the ecological-evolutive classification proposed by Schiner-Racovitza (Schinner, 1854; Racovitza 1907) modified by other authors (Barr & Holsinger, 1985; Holsinger & Culver, 1988, Trajano, 2012). According to this classification, others groups are defined as trogloxenes because a fraction of the source population occurs in epigean habitats but use subterranean resources (to date, there are no known populations of trogloxene crickets in Brazil) and the troglobites correspond exclusively to subterranean source populations (Trajano, 2012). Desutter-Grandcolas (1997) proposed a classification for the taxa that live, reproduce and forage exclusively in subterranean habitats, such as troglobites. Other populations do not use an exclusive habitat andare characterized according to their own natural habitat (e.g.,cavicolous, straminicolous, and dendrophyles; Desutter, 1995). Mews & Sperber (2008) described E. aguassay based on specimens from the Viçosa municipality and redescribed E. cavernicolus from the Lapinha cave, in the Lagoa Santa municipality, both locations in Minas Gerais State. In that study, the authors referred to E. cavernicolus as a true cavernicolous animal (troglobitic) and to E. aguassay as cavicolous/straminicolous. Later, Souza-Dias et al. (2014) noted that E. cavernicolus comprises cavicolous species with several troglophilic populations,while Zefa et al. (2014) did not mention the position of E. ubajarensis according to the ecological-evolutive classification; they only described its occurrence at two hundred meters inside the Ubajara cave, in a touristic area under artificial light. In this study, we describe a new cave cricket species of the Endecous genus from Olhos d’Água cave. In addition, we include a discussion about troglobiomorphisms and the isolation of this new species in the caves.

Material and methods

Study area. The Peruaçu Valley is located at the Peruaçu Caves National Park (PCNP), in a transitional area between the Cerrado (Brazilian savannah) and the Caatinga (mesophytic and xeromorphic forests) of the morphoclimatic domains (Ab'Saber, 1977). In an area of limestone karst of the PCNP, the Peruaçu River runs over 17 km in a canyon that, according to Rodet et al. (2009), gave the name to the watershed. The Peruaçu Valley region consists of large rocky outcrops with a predominance of calcareous rocks of the Bambuí group and lesser amounts of sandstones of the Urucuai training (Karmann et al., 2003). According to the Koppen-Geiger classification, the climate of the region is classified as Aw, tropical wet and dry winter (Peel et al., 2007); the rainy season is concentrated between March and November, and the dry season between April and September (Nimer, 1979). The average annual temperature is 24°C, the minimum temperature is 16°C, and the maximum is 34°C; the hottest months are October and November, and the coldest are June and July (Brandão & Magalhães, 1991). The Peruaçu caves are located in the karst plateau of San Francisco at 500–700 mof altitude. The Olhos d’Água cave (23S 589230.979 mE 8328963.592 mN) was explored and mapped in 1984 and is one of 138 caves in the municipalities of Januária, Itacarambi and São João das Missões. The cave has 9,100 m of horizontal projection and is considered the longest cave in the state of Minas Gerais (CNC, 2015). The cave consists of a long main tunnel (Fig. 04 C) with extensive stretches of low ceiling and a few large chambers, side channels and higher level snippets. The main entrance is located at 500 m of altitude with an unlevelled surface of approximately 126 meters; the main conduit ends in a small lake, Duffin lake (Trajano, 1997). The Lapa do Cipó cave (23S 587658.464 mE; 8335305.908 mN) is located approximately 6.5 km northwest from the Olhos d’Água cave entrance. Both caves correspond to different drainages. The resurgence of Olhos d’Água cave is not perennial, which can constitute an isolation factor for aquatic invertebrates but not necessarily for terrestrial cave invertebrates (Fig. 4C). Methods. The specimens were collected manually at the Lapa do Cipó and Olhos d’Água caves, fixed and immersed in 70% ethanol. In the laboratory, the male phallic complexes were removed and treated with an aqueous solution of 10% KOH for 24 h to remove membranes and muscular tissues. We examined, described, compared and photographed the specimens using a LeicaDFC295©video camera attached to a Leica M205C stereomicroscope

298 · Zootaxa 4032 (3) © 2015 Magnolia Press BOLFARINI & BICHUETTE with a Planapo 1.0x objective. The figures were produced from stacks of images using LAS (Leica Application Suite) v3.7. The images were subsequently edited in Adobe Photoshop CS6©. The habitus and field photographs were taken with a Canon EOS T5i digital camera with an 18–135 mm Canon lens. The epigean collections were carried out in the surroundings of the caves to assure the cave status of the species (troglobitic). The holotype and paratypes were deposited in the collection of the Museu de Zoologia da Universidade de São Paulo (MZSP). We deposited a couple of paratypes in the collection of the Laboratório de Estudos Subterrâneos of the Universidade Federal de São Carlos (LES/UFSCar). For character comparison, we used E. aguassay, an epigean species collected near the entrance of a Olhos d’Água cave. To study the species distribution, we used identified materials from 36 caves in the Bambui and Quadrilatero Ferrifero karst systems. Abbreviations. General morphology. I, II, III, anterior, median, posterior (leg, tarsomere); FW, forewing; F, femur; T, tibia; apical spurs of TIII: iad, iam, iav, inner apical dorsal, medium and ventral; oad, oam, oav, outer apical dorsal, medium and ventral; subapical spurs of TIII: is1, inner subapical 1. TIII subapical and apical spurs formula indicated as x/y, for inner/outer spurs, respectively (model proposed by Souza-Dias et al. 2015); Male genitalia. Arc, ectophallic arc; Ect. Ap., ectophallicapodeme; Ect. F., ectophallic fold; End. Sc.,endophallic sclerite; Ps. Arm, pseudepiphallic arm; Ps. Sc., pseudepiphallic sclerite; Ps.P., pseudepiphallic paramere, r, rami. Repositories. MZSP, Museu de Zoologia da Universidade de São Paulo;LES/UFSCar, Coleção Zoológica do Laboratório de Estudos Subterrâneos, Universidade Federal de São Carlos.

Results

Family Phalangopsidae Blanchard, 1845

Subfamily LuzarinaeHerbard, 1928

Tribe Phalangopsini Blanchard, 1845

SubtribeModestozarinaGorochov, 2014

Genus Endecous Saussure, 1878

Endecous (Endecous) peruassuensis Bolfarini, n. sp. (Figures1G–L; 2C, C, D, F, G, I; 3D–F; 4E, F, H. Table 1) http://lsid.speciesfile.org/urn:lsid:Orthoptera.speciesfile.org:TaxonName:471756

Type material. 1 male holotype, 3 males paratypes, 1 female paratype, Brazil, Minas Gerais state, Itacarambi, Olhos d’Água cave (23S 589246.803 mE; 8328939.507 mN). Bolfarini, M.P. & do Monte, B. G. O. leg.1 female paratype, Brazil, Minas Gerais state, Itacarambi, Olhos d’Água cave (23S 589246.803 mE; 8328939.507 mN). do Monte, B; Gallão J.D. & von Schimonsky, D. M. leg, 23–24.x.2013. 2 males paratypes, 1 female paratype, Brazil, Minas Gerais state, Januária, Lapa do Cipó cave (23S 587658.464 mE; 8335305.908 mN), 05.vi.2014, Bolfarini, M.P. & do Monte, B. G. O. leg. Specimens examined. 6 adult males, 3 adult females, 13 juveniles, same data as the type material. Etymology. Toponimic, allusive to the Peruaçu Caves National Park, north of Minas Gerais state, eastern Brazil. "Peruaçu" in the native Brazilian Tupi-Guarani means "Great River" by combining the terms peru ("river") and açu ("great"). Diagnosis. Male. FWs with triangular, elongated mirror, formed by three cells, with a transversal vein in the apical cell (Fig. 2D II); chord formed by two elongated, straight cells; harp with four diagonals veins forming five uniform fields in width, with no secondary veins (Fig. 2D I); lateral field with two longitudinal veins, not reaching the mirror (Fig. 2D IV); anal field with close cells (Fig. 2D III); pars stridents with 72 teeth. Phallic complex with pseudepiphallic arms thin and flattened, curved; pseudepiphallic parameres short, distant from one another, presence of a membranous region in the middle that connects the proximal and apical parts; pseudepiphallic sclerite thin, sub straight; ectophallic apodeme few sclerotized, short; rami thin and straight, triangular in lateral view; ectophallic arc curved; endophallic sclerite well developed.

ENDECOUS PERUASSUENSIS N. SP. Zootaxa 4032 (3) © 2015 Magnolia Press · 299 FIGURE 1. Male general morphology. E. aguassay A—head in front view; B—maxillary palpi; C—Lateral view of head, pronotum and wings; D—habitus; E—Supra-anal plate; F—subgenital plate; E. peruassuensis sp. n. G—head in front view; H—maxillary palpi; I—lateral view of head, pronotum and wings; J—habitus; K—Supra-anal plate; L—subgenital plate.

300 · Zootaxa 4032 (3) © 2015 Magnolia Press BOLFARINI & BICHUETTE FIGURE 2. Male general morphology. E. aguassay: A—FWs (B—scheme); E—TIII; H—eyes in lateral view. E. peruassuensis sp. n. C—FWs (D—scheme); F—TIII; G—metanotal structure; I—eyes in lateral view.

ENDECOUS PERUASSUENSIS N. SP. Zootaxa 4032 (3) © 2015 Magnolia Press · 301 FIGURE 3. Male phallic complex. E. aguassay in dorsal view (A), ventral (B), and lateral (C). E. peruassuensis sp. n. in dorsal view (D), ventral (E) and lateral (F).

302 · Zootaxa 4032 (3) © 2015 Magnolia Press BOLFARINI & BICHUETTE FIGURE 4. Study area and habitats. A—surroundings of the cave in dry season (Cerrado—brazilian savannah); B—entrance of the Olhos D’ água cave; C—main conduit; D—Lapa do Cipó cave; E—E. peruassuensis sp. n. male; F—E. peruassuensis sp. n. female; G—E. aguassay; H—male court.

Description. Male holotype: body elongated, pubescent, general coloration yellow (Fig. 1J).Measurements shown in Table 1.Head: frons and clypeus yellow; gena yellow with inferior portion brown; labrum pale yellow; epicranial suture area glabrous; vertex and occiput marbled light brown (Fig. 1G). Antennal scape yellow, pilose; interantennal space same sized as scape (Fig. 1G). Distal margin of mandible yellow with dark apex. Maxillary palpi light yellow, fifth joint the longest, with dilated apex (ratio 4th joint/5th joint = 0, 78; Fig. 1H). Eyes elongated, flattened, inferior border acuminated, border of ommatidia lightly depigmented (Fig. 2I). Ocelli absent. Thorax: Disk of pronotum wider than long, yellowish, lateral lobes with same color. Cephalic margin almost straight; caudal margin slightly convex; (Fig. 1K). Male’s FWs as figures 2C, D: Mirror triangular, elongated, formed by three cells, with a transversal vein in the apical one (Fig. 2D II); chord formed by two elongated cells, straight; harp with four diagonals vein forming five uniform fields in width, there are not secondary veins (Fig. 2D I); lateral field with two longitudinal veins, not touching the mirror (Fig. 2D IV); anal field with close cells (Fig. 2D III); pars stridents with 72 teeth. Male metanotum with two median (Med. P.) and two lateral projections (Lat. P.), apparently vestigial glandular structure (Fig. 2G).Legs I and II yellowish; TI: two ventral apical spurs, auditory tympana present; TII: four spurs, two internals (1 ventral, 1 dorsal) and two externals, the two dorsal are the smallest. Legs III yellowish, darker in distal portion; TIII yellowish, pubescent; TIII apical spurs: the median is the longest on the inner face and the dorsal is the longest on the outer face. Abdomen: tergites yellowish, the last one darker. Sternites

304 · Zootaxa 4032 (3) © 2015 Magnolia Press BOLFARINI & BICHUETTE pale yellow. Supra anal plate short, light brown, the distal margin arched with dense bristles (Fig. 1K). Subgenital plate with a translucent aspect, pubescent, flatted in the center, the posterior border lightly convex in the center (Fig. 1L). Cerci long (larger than body size), yellowish, with distal portion lighter, ratio (CCer/CC = 1, 23) 14.5/ 11.7 mm. Phallic complex: pseudepiphallic arms thin and flattened, curved to the parameres; pseudepiphallic parameres short, distant from one another, presence in the middle of a membranous region connecting the proximal and apical parts; pseudepiphallic sclerite thin, sub straight; ectophallic apodeme sclerotized, short; rami thin and straight, triangular in lateral view; ectophallic arc curved; endophallic sclerite well developed (Fig. 3D, E, F). Female: relatively similar to male, but larger, less pigmented and apterous; tympanum present in inner face of TI; supra-anal and subgenital plate light yellow, translucent, ovipositor slightly flattened laterally and very sclerotized. Distribution. Known only for Olhos d’Água (Itacarambi municipality) and Lapa do Cipó (Januaria municipality) caves (Figure 5).

Endecous (Endecous) aguassay Mews, 2008 (Figures 1 A–F; 2 A, B, E, H; 3 A–C; 4G) http://lsid.speciesfile.org/urn:lsid:Orthoptera.speciesfile.org:TaxonName:465728

Specimen examined. 1 male, Brazil, Minas Gerais state, Itacarambi, Olhos d’Água caves surroundings, epigean environment (23S 589246.803 mE; 8328939.507 mN). Bolfarini, M.P. & do Monte, B. G. O. leg. Distribution. This species has a wide distribution, covering the Bambui Geomorphological Unit and Quadrilátero Ferrífero region (Figure 5).

Discussion

Endecous peruassuensis sp. n. differs from other Endecous species mainly by the set of characters presented in the diagnosis. We noted that the genus has a variation in the shape and proportion of the FW in relation to the body and in the characters of the male phallic complex. Other characters, such as mouth parts, palp, width and shape of the pronotum, leg size, presence/absence of tympanum (except E. apterus) and number and position of the leg III spurs, can be considered conservative characters. Souza-Dias et al. (2014) defined E. apterus as a troglobitic cricket based on the absence of populations living in the epigean environment and reinforced by the apterous condition. Hence, he imprinted a troglobiomorphism to the genus. Instead, E. peruassuensis n. sp. does not have this condition or any wing variation or reduction. The troglobiomorphisms are character-states that might suggest the relationship of the species with a hypogean environment, and they can be morphological, physiological or behavioral. They differentiate the hypogean from the epigean species, but they do not define the relationship of these species with the underground environment (Juberthie & Decu, 1994). Therefore, the occurrence of a living population (that reproduce) inside the caves and the absence of populations established outside is a better strategy to define a troglobitic species without using a cladistic analysis; however, according Desutter-Grandcolas (1997), the phylogenetic context is still the more precise procedure to define troblobites. E. cavernicolus was referred to as troglobitic by Desutter-Grandcolas (1995), and Mews & Sperber (2008) maintained this classification based on the first author. Souza-Dias et al. (2014) mentioned that Zefa (2000, unpublished data) observed individuals of this species stridulating out of a cave and characterized them as cavicolous with a troglophilic population (Table 2). This species and E. peruassuensis n. sp. do not present the morphological troglobiomorphism known for the genus; however, certain characters must be better compared with epigean-hypogean species of the genus, such as the cerci and antennae sizes as well as the number of teeth in the stridulatory veins. E. peruassuensis sp. n. has a well-established population inside the Olhos d’Água cave, where we observed several individuals in different stages of development, eating and during the mating process. This fact was also observed by Souza-Dias et al. (2014), where several individuals were registered during foraging and reproductive activities. These data corroborate other assumptions that feature the troglobitic style defined by Desutter (1997) because they live and reproduce within the caves. Certain observed morphological and physiological

ENDECOUS PERUASSUENSIS N. SP. Zootaxa 4032 (3) © 2015 Magnolia Press · 305 characteristics might be present in troglobiomorphic species, such as a smaller size for the genus and a reduced escape behavior. This reaction was easily observed as individuals moved slowly when touched. In the Lapa do Cipó cave, we did not observe these facts because the individuals were fewer and more dispersed. E. aguassay, a cavicolous/straminicolous species, have a wide distribution in the Quadrilátero Ferrifero and Bambui karst regions and present an overlap of occurrence areas with these other two species (Fig. 5). According to the ecological-evolutive classification proposed by Trajano (2012), the absence of a source population established outside the cave reinforces the condition of E. cavernicolus as a troglobite. This species lives in parapatry with the cavicolous/straminicolous species E. aguassay, which occupies the epigean environment in the cave surroundings. This epigean-hypogean relationship of geographic occupation between the two species occur also with E. aguassay and E. peruassuensis n. sp., where the latter was recorded only at the Lapa do Cipó and Olhos d’Água caves. Relationships such as those mentioned above were proposed by Howarth (1981, 1983, 1987), Juberthie (1984) and Peck & Finston (1993), who suggest two possible hypotheses about the colonization and speciation in the hypogean environments, i.e., the Climatic Relict Hypothesis (CHR) and the Local Habit Shift Hypothesis (LHSH),which resulted in different speciation processes. Desutter (1996) discussed these two hypotheses in a phylogenetic context and proposed eight other possible combinations based on the geographic distribution, speciation mode and ancestral condition of the environment. Yet, the author questioned the fact that the data come from current distributions of troglobites (directly observed) and that the speciation mode and environmental conditions are not related to past events. Thus, the currently restricted distribution of Endecous species from the Peruaçu region living in sympatry is related to parapatric events, historical factors or even ecological factors. The Olhos D’água cave has, until now, four troglobites species described and is the type locality for the catfish Trichomycterus itacarambiensis Trajano & Pinna, 1996; the pseudoscorpion Pseudochthonius biseriatus Mahnert, 2001 (Pseudoscorpiones); the opilionid Iandumoema uai Pinto-da-Rocha, 1996 (Opiliones); and the amblypygid Charinus eleonorae Baptista & Giupponi, 2003 (Amglypygi). However, five other troglobites species are known. I. uai and C. eleonorae have a known distribution in only two caves (Olhos D’ Água and Lapa do Cipó caves— B.G.O. do Monte, J. E. Gallão, D. M. von Schimonsky and M.E. Bichuette, pers. com.), the same locations where E. peruassuensis n. sp. was found, which suggests that these species have the same distribution and dispersion patterns through the spaces in the limestone rock. We want to emphasize the importance of the Peruaçu Cave National Park region and, more specifically, the Olhos D’água cave and its surroundings, as a priority area for conservation purposes. Moreover, we indicate the urgency in monitoring these troglobitic populations to detect population patterns to be discussed based on the IUCN criteria.

Acknowledgments

We are grateful for the financial support received from the Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq, which partially provided grants to MEB (fellowship 303715/2011-1); to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, MCT/CNPq/MMA/MEC/CAPES/FNDCT-Ação Transversal/FAPs No. 47/2010: “Biota de Orthoptera do Brasil”) for financial support to MPB; to Angélica Maria Penteado Martins Dias, coordinator of Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitoides da Região Sudeste Brasileira (INCT Hympar Sudeste—Processes FAPESP 2008/57949-4 and CNPq 573802/2008- 4)for the use of a stereomicroscope Leica DFC 295; to Luciana Bueno dos Reis Fernandes, biologist at the DEBE/ UFSCar, for taking the stereomicroscope images; to Bruno Gabriel Oliveira do Monte and Vandeir “Branco” Batista de Jesus for their field support; to Diego Monteiro von Schimonsky and Jonas Eduardo Gallão for the previously collected material; to Pedro G. B. Souza-Dias for his helpful comments and suggestions. We also thank the environment governmental agency Instituto Chico Mendes de Conservação da Biodiversidade (ICMBIO) for the collecting permits (license 20165-1). The English was revised by experts from American Journal Experts (AJE).

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