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1 Zootaxa 4425 (2): Copyright 2018 Magnolia Press Article ISSN (print edition) ZOOTAXA ISSN (online edition) A remarkable new species of cavernicolous Collartidini from Madagascar (Hemiptera: Heteroptera: Reduviidae) DOMINIK CHŁOND 1, ERIC GUILBERT 2, ARNAUD FAILLE 2,3, PETR BAŇAŘ 4 & LEONIDAS-ROMANOS DAVRANOGLOU 5 1 University of Silesia, Faculty of Biology and Environmental Protection, Department of Zoology, ul. Bankowa 9, Katowice, Poland. dominik.chlond@us.edu.pl 2 Muséum National d'histoire Naturelle, Département de Systématique et Evolution, UMR 7205 CNRS, CP50-45 rue Buffon, Paris, France. guilbert@mnhn.fr 3 Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Passeig Maritim de la Barceloneta 37, Barcelona, Spain. arnaud1140@yahoo.fr 4 Department of Zoology, Fisheries, Hydrobiology and Apiculture, Faculty of AgriSciences, Mendel University, Zemědělská 1, Brno, CZ , Czech Republic. petrbanar@seznam.cz 5 Oxford Flight Group, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, United Kingdom. leonidas-romanos.davranoglou@queens.ox.ac.uk Abstract Mangabea troglodytes sp. nov. (Hemiptera: Heteroptera: Reduviidae: Emesinae) is described based on four specimens collected in a cave of the Namoroka Karstic System, Madagascar, and deposited in the Collection of the Muséum National d Histoire Naturelle, Paris. The dorsal habitus as well as diagnostic characters of male and female genitalia are extensively illustrated and imaged. A key to species of the genus Mangabea Villiers, 1970 is provided and the degree of cave specialization of the new species is discussed. Key words: Heteroptera, Reduviidae, Emesinae, Mangabea, Madagascar, new species, cave, taxonomy Introduction Reduviidae is the second largest family of true bugs (Hemiptera: Heteroptera), which comprises of approximately 6,500 described species (Putshkov & Putshkov , Maldonado Capriles 1990). Given that Madagascar is considered one of the world s richest biodiversity hotspots, the fauna of Madagascan Reduviidae is particularly rich, comprising of 342 described species (Maldonado Capriles 1990 Labina & Kerzhner 2001, Villiers 1979). In recent years there has been a surge in studies describing new reduviid taxa from Madagascar (e.g. Chłond 2010a, 2010b, 2010c, 2011a, 2011b, 2014; Chłond & Junkiert 2010, 2011; Hwang & Weirauch 2010; Zhang & Weirauch 2011; Chłond & Guilbert 2012; Chłond & Baňař 2013; Chłond 2016; Chłond et al. 2016; Baňař et al. 2016; Forthman et al. 2016; Weirauch 2008), indicating that our knowledge on the island s reduviid fauna still remains far from complete. The Collartidini are a tribe of Emesinae of particular phylogenetic significance, as they have traditionally been considered as the sister-group to all other Emesinae (Wygodzinsky 1966). In addition, the biogeography of this tribe is interesting due to its strongly disjunct distribution, with species ranging from the Canary Islands, the Afrotropics, the Middle East, Sri Lanka and Taiwan (Rédei & Tsai, 2010; Wygodzinsky 1966). Concerning the Madagascan Collartidini, only one genus is known, among 28 genera and 99 species of Madagascan Emesinae (Villiers 1979). Mangabea was first described as a monotypic genus by Villiers (1970), initially including M. orientalis Villiers, 1970, until the description of a second species, M. barbiger Weirauch, 2008, almost 40 years later. The genus was erected by Villiers based on the distinctly elongated head with the anteocular part longer than the first visible labial segment and large eyes almost connected (holoptic) dorsally. These morphological characters differentiate Mangabea from other representatives of the tribe Collartidini. 372 Accepted by D. Redei: 10 Apr. 2018; published: 30 May 2018
2 Examination of unidentified specimens of Emesinae collected by Arnaud Faille during the 2016 expedition of the Muséum National d Histoire Naturelle (MNHN) in the Tsingy de Namoroka National Park, Madagascar, deposited in the MNHN, Paris revealed a remarkable undescribed species of Mangabea living in the caves of Namoroka. The type material is represented by three males and one female, while additional specimens comprise of two larvae. In this study, we describe the new species and also provide an identification key for the species of Mangabea. Material and methods The type material and the additional specimens are deposited in MNHN. External structures were examined using a stereoscopic microscope Nikon SMZ25 with a DS-Ri2 digital camera. All drawings were made using a camera lucida. Genitalia of the holotype male and paratype female were macerated in 10% KOH for 16 hours in 38 C or boiled for 10 minutes in 10% KOH, then rinsed in distilled water, and subsequently dissected under the stereoscopic microscope. Male genitalia were imaged at the Oxford University Museum of Natural History using a Leica M165c microscope with a Leica DFC490 camera, while stacked images were combined using Helicon Focus. Measurements are given in millimeters. All specimens were originally preserved in 70% ethanol, but were subsequently dried and pinned. The holotype male was observed and imaged by an environmental Phenom XL scanning electron microscope (SEM) (Phenom-World B.V., The Netherlands), which did not require destructive coating of the specimen. SEM imaging took place in low vacuum conditions at 10, 15 and 20 accelerating voltage with a secondary electron detector. Key to the species of Mangabea 1 Micropterous; anterior pronotal lobe distinctly enlarged (Fig. 2); posterior pronotal lobe reduced, not covering mesonotum; eyes reduced; 4 or more pairs of setae on ventral surface of head; legs extremely slender and long (Fig. 16) M. troglodytes sp. nov. - Macropterous; anterior pronotal lobe relatively short; posterior pronotal lobe covering mesonotum; eyes almost connected dorsally (holoptic); 3 or 2 pairs of setae on ventral surface of head Fascicle of stout setae on gena; anterior pronotal lobe not swollen, slightly smaller than posterior lobe; 3 pairs of setae on ventral surface of head M. barbiger Weirauch, Gena armed with 2 pairs of single setae; anterior pronotal lobe swollen, slightly longer than posterior lobe; 2 pairs of setae on ventral surface of head M. orientalis Villiers, 1970 Taxonomy Mangabea Villiers, 1970 Type species: Mangabea orientalis Villiers, 1970, by original designation. Revised diagnosis: Mangabea is recognized among the extant genera of Collartidini by moderate body size ( mm), elongate head, first visible labial segment not reaching anterior margin of eye, ventral surface of all visible labial segments or only second and third visible labial segments with dense vestiture, fore coxa with five or less spine-like setae. In macropterous forms basal cell pentagonal; discal cell long, more than three fourths of length between rm and tip of wing; crossvein proximal to rm vein present. Mangabea troglodytes Chłond, Guilbert, Baňař & Davranoglou sp. nov. (Figs. 1 26) Type material: Holotype : Madagascar Namoroka 29.X.2016 / Grotte Canyon S ' E ' alt. 161 m, A. Faille leg.; Paratypes 2 and 1 : Madagascar Namoroka 29.X.2016 / Grotte Canyon S ' E ' alt. 161 m, A. Faille leg. (MNHN). A NEW SPECIES OF COLLARTIDINI FROM MADAGASCAR Zootaxa 4425 (2) 2018 Magnolia Press 373
3 Other material examined: Larva instar IV: Madagascar Namoroka 29.X.2016 / Grotte Canyon S E alt. 161 m, A. Faille leg.; Larva instar II: Madagascar Namoroka 29.X.2016 / Grotte Canyon S E alt. 161 m, A. Faille leg.; instar stage was tentatively assigned based on overall body size, given that wing pads were not present. Diagnosis: The species is easily recognized within the genus Mangabea by the following combination of characters: body large sized and elongate, anterior pronotal lobe distinctly longer than posterior lobe (Fig. 2), extremely long and slender antennae and legs (Fig. 1), reduced eyes (Figs. 2, 16), 4 pairs of large spines on ventral surface of head, hemelytra micropterous (Fig. 1). FIGURE 1. Mangabea troglodytes sp. nov.: dorsal habitus. Description: Long and relatively robust body with distinctly elongated head and prothorax. Eyes reduced, legs slender and very long. Distinct spines on head and fore legs (Figs. 2, 16 23). Body generally dull. Color: Body light brown-yellowish with paler legs (Figs. 24, 25). Eyes black. Ventral margins of antennifers and basal margin of scape black. Head covered by short, pale setae inserted in darkly pigmented pits (pits are pigmented mostly on dorsal and ventral part) and brown spines. Thorax, legs and abdomen covered by pale and brown setae (some inserted in darker pits). Fore leg with brown spines. Apical third of fore tibia dark to light brown. 374 Zootaxa 4425 (2) 2018 Magnolia Press CHŁOND ET AL.
4 FIGURE 2. Mangabea troglodytes sp. nov.: head and prothorax, lateral view. Structure: Head: Strongly elongate, dorsally and ventrally covered by medium-sized and short, semi-erect setae, placed in distinct pits, with apices directed anteriad (Figs. 2, 16 17, 20 21). Anteocular (males) and 2.57 (female) times longer than postocular part. Interocular furrow deeply impressed, postocular globular. Eyes reduced, with few, relatively large ommatidia, vertically elongated, not reaching dorsal or ventral surface outlines of head in lateral view (Fig. 16). Head ventrally curved in lateral view, armed ventrolaterally with four large pairs of spines, two smaller pairs and a small fascicle of spines, arranged in the following order (starting from base of head moving towards apex): first pair of large spines situated on postocular, immediately before eye (Figs. 2, 16); second pair on anteocular, immediately after eye, at level of interocular furrow (Figs. 2, 16 17); third and fourth pairs immediately before and at level of antennifer respectively (Figs. 2, 20); two pairs of smaller spines placed on gena (Figs ), immediately before a small fascicle of spines (Figs. 2, 20 21). Antenna extremely long; scape longest, attaining first half of abdominal segment II, slightly curved at base. Pedicel thinner than scape. Basi- and distiflagellomere thinnest (Figs. 1, 24, 25). First visible labial segment gradually broadened distally, with two lateroventral rows of 11 spine-like setae; fourth spine largest (Figs. 2, 20, 21). Second visible labial segment distinctly enlarged in basal half and thinner in apical half (Figs. 2, 22). Second and third visible labial segments A NEW SPECIES OF COLLARTIDINI FROM MADAGASCAR Zootaxa 4425 (2) 2018 Magnolia Press 375
5 with two lateroventral rows of spine-like setae (spines smaller than on first segment). Labium at rest attaining posterior margin of coxal cleft (Figs. 2, 23 25). Thorax: Prothorax densely covered by anteriad-facing, mediumsized setae (Figs. 2, 24, 25). Anterior pronotal lobe ovoid and shiny, and 2.61 longer than posterior pronotal lobe in males and females respectively, with a deep median longitudinal sulcus extending in its entire length. Anterolateral margins of pronotal collar large and robust, with apices facing fronto-laterally. Posterior pronotal lobe greatly reduced, not covering mesonotum. FIGURES 3 5. Mangabea troglodytes sp. nov. 3, pygophore, dorsal view; 4, styloids, outer view; 5, valvifer VIII, outer view. Scutellum subtriangular with raised and distinctly depressed median area (Fig. 1). Apex of scutellum rounded. Raised median area of scutellum diamond-like, covered by relatively long setae. Proepisternum separated from proepimeron, basally both elements connected by distinct pleural suture, apically proepisternum partially covering proepimeron. Mesepisternum and metepisternum enlarged, covered by medium-sized setae placed in distinct pits. Prosternum with prosternal process not elevated. Fore coxa with two rows of spine-like setae (Fig. 2), frontal row with 4 5 large spine-like setae and ventral row with over 30 relatively small spine-like setae. Fore trochanter with 2 6 variably sized spine-like setae. Fore femur with 4 5 groups of 2 6 spines, with first spine in each group smallest, remaining spines gradually longer, with final spine longest (Figs. 2, 18 19); distal third of fore femur with 4 long spines (Fig. 2). First tarsomere very short, second and third of equal length. Claws unmodified. Reduced hemelytra not reaching posterior margin of metathorax, covered by dense, relatively short setae placed mostly on costal margin. Abdomen: Distinctly elongate, ovoid and dull, densely covered by medium-sized, thin setae, both dorsally and ventrally (Fig. 1). Connexival margin smooth. Spiracles of second abdominal segment placed on dorsolateral surface of tergite I, on long and thin tubercles; subsequent spiracles of similar structure, located at the median part of each mediosternite, beneath the connexival suture. Genitalia: Male - Pygophore subquadrangular with a triangular, elongated process with rounded apex, and with a distinct central, rounded elevation covered by variably sized (mostly long) setae (Fig. 3). Parameres slightly curved in lateral view (Figs 8 11). Crown with long setae dorsally and a sharp, slit-like apical process (Figs. 6 7, 9 10). Aedeagus subrectangular (Figs. 10, 13), articulatory apparatus with slender basal plates which fuse medially (Fig. 12, aa), and a short but horizontaly broad ponticulus basilaris (Fig. 12). Pedicel broad in ventral view (Fig. 13, pd). Phallotheca distinctly bent at base (Figs. 13, 15, ph), with a Y-shaped dorsal phallothecal sclerite (Fig. 15, dps) Uninflated endosoma with a pair of outer lobes, each provided with 4 raised lines on their surface (Fig.12, el). Partially inflated endosomal surface covered with granulose denticles (Fig. 14, dnt). Female: Valvifer VIII covered with variably sized setae, with rounded margins and a broad triangular process (Fig. 5). Styloids club-shaped, with relatively long setae apically (Fig. 4). Measurements (in mm, female in parentheses): Body length: (10.64); maximum width of abdomen: (1.51); head length: (1.73); head width: (0.67); length of anteocular part: Zootaxa 4425 (2) 2018 Magnolia Press CHŁOND ET AL.
6 (1.26); length of postocular part: (0.49); greatest width of head across eyes: (0.3); length of antennal segments I:II:III:IV: (6.17): (3.56): (2.85): (2.97); length of visible labial segments I:II:III: (1.06): (0.83): (0.52); length of anterior pronotal lobe along midline: (1.41); length of posterior pronotal lobe along midline: (0.54); maximum width of anterior pronotal lobe: (1.14); maximum width of posterior pronotal lobe: (1.15); length of scutellum: (0.46); length of hemelytra: (1.03). Etymology: The species name of this cave-inhabiting species is the Greek noun τρωγλοδύτης (latinised as troglodytes), meaning one who inhabits caves. FIGURES Mangabea troglodytes sp. nov. 6 8, right paramere, three different aspects; 9 11, left paramere, three different aspects. A NEW SPECIES OF COLLARTIDINI FROM MADAGASCAR Zootaxa 4425 (2) 2018 Magnolia Press 377
7 FIGURES Phallus of Mangabea troglodytes sp. nov. 12, phallus, dorsal view; 13, phallus, ventral view; 14, phallus, lateral view; 15, schematic of dorsal phallothecal sclerite and outline of phallotheca, dorsal view; aa= articulatory apparatus; dnt= denticles on endosoma; dps= dorsal phallothecal sclerite; el= endosomal lines; pd= pedicel; ph= phallotheca. Distribution and ecology: West Madagascar: Namoroka Canyon (Fig. 26). The type locality is located in a remote area of Tsingy de Namoroka National Park. Grotte Canyon is a large cave with various galleries, most of them dry during the time of the year when the specimens were collected. Individuals of the new species were found in the deepest part of the cave, on a vertical surface of the cave wall covered by a prominent network of roots, together with the cave-inhabiting Cixiidae Typhlobrixia namorokensis Synave, 1953, a potential prey organism of this species. The fauna of this cave consists of a rich assemblage of troglobitic species, e.g. spiders, Opiliones, Blattodea (Nocticolidae) as well as two new species of Coleoptera (Staphylinidae) including the first cave beetle known from Madagascar (Löbl & Faille 2017, Faille & Lecoq in press). 378 Zootaxa 4425 (2) 2018 Magnolia Press CHŁOND ET AL.
8 FIGURES SEM images of Mangabea troglodytes sp. nov. 16, eye; 17, spine-like setae on ventral surface of head; 18, spine-like setae on coxa; 19, spine-like setae on femur. Discussion Troglobitic adaptations in Emesinae. Although many species of Emesinae frequently inhabit caves, most are trogloxenic or troglophilic and have not evolved conspicuous adaptations for a strictly cave-inhabiting life style (e.g. e.g. reduction or loss of eyes) other than becoming paler than their free-living relatives (Pope 2013, Wygodzinsky 1966). The elongate body of most emesines is considered by some authors as a preadaptation (exaptation) for the cave niche, which might explain the repeated colonisation of caves by many emesine genera (reviewed by Wygodzinsky 1966 and Pope 2013). There are only three troglobitic emesine species, two pertaining to the Collartidini (Collartida anophthalma Espanol & Ribes, 1983 and C. tanausu Ribes, Oromi & Ribes, 1998) and one to the Ploiarolini (Nesidiolestes ana Gagné & Howarth, 1974) (Gagné & Howarth 1974, Ribes et al. 1998). Several traits of M. troglodytes sp.nov. may represent adaptations for a fully troglobitic life style and are shared with the other two troglobitic Collartidini: eyes reduced, pale cuticle, body and appendages much longer than freeliving congeners. The micropterous condition may not necessarily be a troglobitic adaptation, although many cave specialists (e.g. C. anophthalma, C. tanausu, many nocticolid cockroaches and dolichopodid crickets) are also characterized by the reduction or absence of wings. The enlarged anterior pronotal lobe, and the strip-like posterior pronotal lobe are correlated to microptery and the reduction of the flight apparatus, following a similar pattern to other heteropteran taxa with reduced wings (e.g. Davranoglou 2014). Additional ecological observations may shed light on the degree of cave-specialisation of the newly described species. A NEW SPECIES OF COLLARTIDINI FROM MADAGASCAR Zootaxa 4425 (2) 2018 Magnolia Press 379
9 Relationships. The highly specialized morphology of M. troglodytes sp. nov. makes it difficult to elucidate its relationships to its free-living congeners, coupled with the fact that internal genitalia are known only from M. barbiger. However, the two species share raised lines on the endosoma (Fig. 12, el; Weirauch 2008), which may indicate a close relationship. However, if this trait is found in M. orientalis and other undescribed congeners (P. Baňař, unpublished) as well, it may suggest that this could represent an apomorphy for the genus, as the endosoma of other Collartidini is of very different form (e.g. Rédei & Tsai 2010, Wygodzinsky 1966). FIGURES SEM images of Mangabea troglodytes sp. nov. 20, anteocular part of head with spine-like setae; 21, first visible labial segment; 22, second visible labial segment; 23, third visible labial segment. 380 Zootaxa 4425 (2) 2018 Magnolia Press CHŁOND ET AL.
10 FIGURES Mangabea troglodytes sp. nov. 24, adult in its natural habitat; 25, IV instar larva in its natural habitat. A NEW SPECIES OF COLLARTIDINI FROM MADAGASCAR Zootaxa 4425 (2) 2018 Magnolia Press 381
11 FIGURE 26. Distribution of Mangabea troglodytes sp. nov. Acknowledgements The authors would like to thank the Malagasy authorities, the staff of MNP (Madagascar National Parks), Marc Gansuana and the staff of EWE Madagascar and the residents of the Namoroka area for their invaluable help during the expedition. Gernot Kunz for providing the in-situ photos of imaginal and nymphal stages of Mangabea troglodytes sp. nov. and Mariusz Kanturski for providing the SEM images. The authors would like to thank to Łukasz Junkiert for preparing the drawings 1-5. We are also thankful to Darren Mann, Head of Life Collections, Oxford University Museum of Natural History, for allowing us to use the microscopes and cameras at their facility. Petr Baňař was supported by grant MENDELU AF-IGA-2018-tym004. Leonidas-Romanos Davranoglou was funded by The Alexander S. Onassis Public Benefit Foundation Scholarships for Hellenes for conducting this research. 382 Zootaxa 4425 (2) 2018 Magnolia Press CHŁOND ET AL.
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