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Taxonomic Revision of the Genus Hyperaulax Pilsbry, 1897 (Gastropoda, Stylommatophora, Odontostomidae)

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Taxonomic Revision of the Genus Hyperaulax Pilsbry, 1897 (Gastropoda, Stylommatophora, Odontostomidae) Zoosyst. Evol. 95 (2) 2019, 453–463 | DOI 10.3897/zse.95.38259 Taxonomic revision of the genus Hyperaulax Pilsbry, 1897 (Gastropoda, Stylommatophora, Odontostomidae) Rodrigo B. Salvador1, Daniel C. Cavallari2 1 Museum of New Zealand Te Papa Tongarewa. 169 Tory Street, 6011, Wellington, New Zealand 2 Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo. Avenida Bandeirantes 3900, 14040-900, Ribeirão Preto, SP, Brazil http://zoobank.org/EE9B3C6B-D4AE-4508-BF0E-5CCEEB7F12EA Corresponding author: Rodrigo B. Salvador ([email protected]) Academic editor: Frank Köhler ♦ Received 15 July 2019 ♦ Accepted 27 August 2019 ♦ Published 11 September 2019 Abstract The genus Hyperaulax Pilsbry, 1897 comprises two living species endemic to the oceanic Fernando de Noronha Archipelago, off north-eastern Brazil. They are currently allocated in two subgenera, Hyperaulax s. str. and Bonnanius Jousseaume, 1900, belonging to the family Odontostomidae. Herein we present a taxonomic revision of these species, assessing their familiar allocation within Orthalicoidea, offering updated diagnoses and descriptions, figuring the type materials and further relevant specimens, and providing barcoding DNA sequences. We conclude that Bonnanius is a junior synonym of Hyperaulax, which is classified in Odontostomidae. The genus contains two valid species, H. ridleyi and H. ramagei, both endemic to Fernando de Noronha. Key Words Bonnanius, endemic species, Fernando de Noronha, island speciation, Orthalicoidea, Pulmonata Introduction ognized only three valid species: Tocobaga americanus, T. floridanus and T. wakullae Mansfield, 1937 (previously The genus Hyperaulax Pilsbry, 1897 had a unique com- considered a subspecies of T. americanus). position. It comprised two living species endemic to the The two Recent species are also not without prob- oceanic Fernando de Noronha Archipelago off Brazil, H. lems, as two names are currently considered synonymous ridleyi (Smith, 1890) and H. ramagei (Smith, 1890), and with H. ramagei; moreover, this species is included in eight species from Tampa Silex beds (Oligocene) of Flor- the subgenus Bonnanius Jousseaume, 1900, which can ida, USA: H. americanus (Heilprin, 1887), H. ballistae sometimes be recognized as a valid genus (e.g., Simone (Dall, 1915), H. floridanus (Conrad, 1846), H. heilprin- 2006). The peculiar morphological features of Hyper- ianus (Dall, 1890), H. remolinus (Dall, 1915), H. stearnsii aulax also present some challenges, as it is reminiscent (Dall, 1890), H. tampae (Dall, 1915), and H. tortilla (Dall, of several lineages of Orthalicoidea. The genus is usually 1915). Suspecting this could not reflect an actual relation- placed in Odontostomidae, but it also bears resemblance ship, the fossil species previously assigned to Hyperaulax to insular Bulimulidae from the Galapagos; furthermore, were revised by Auffenberg et al. (2015). Those authors Hyperaulax had also been assigned to the extinct fam- concluded that the fossils bore only a superficial similar- ily Grangerellidae by Henderson (1935), although this ity to Hyperaulax and erected the new genus Tocobaga author suggested this based on Oligocene material from Auffenberg et al., 2015 to house the North American fossil Florida (now in Tocobaga), not the Recent Brazilian spe- species, which they classified in the Bulimulidae rather cies (for a full discussion see Auffenberg et al. 2015). than in Odontostomidae. Auffenberg et al. (2015) consid- Therefore, herein we conducted a taxonomic review ered most of the fossil forms to be synonymous and rec- of the two Recent species of Hyperaulax, assessing their Copyright Rodrigo B. Salvador, Daniel C. Cavallari. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 454 Salvador, R.B. & Cavallari, D.C.: Revision of Hyperaulax familiar allocation within Orthalicoidea and the validity 112.7 km² including land and sea; it was designated as an of the subgenus Bonnanius and of the two species syn- environmental protection area by the Brazil in 1989 and onymized with H. ramagei. Furthermore, an updated di- became a World Heritage Site in 2001. Nevertheless, the agnosis and description, alongside images of the type and islands are populated and suffer the negative impacts of additional materials, is provided here for each species. overtourism and pollution (Claudino-Sales 2019). All the type specimens were analyzed and the main mu- seum collections worldwide that could contain material of Methods Hyperaulax were visited or contacted for loans or photo- graphs and information of their specimens. The type ma- Fernando de Noronha is an archipelago located ca 350 km terials are ill1ustrated herein, alongside additional speci- off northeastern Brazil (3°50'–3°52'S, 32°24'–32°28'W) mens to thoroughly show conchological variation. Shell originating from extinct volcanic structures estimated to measurements were taken with a digital caliper. SEM be 1.8–12.4 Ma old. It comprises the main island of Fer- images of the protoconchs were obtained at the Staatli- nando de Noronha (17 km²) and over 20 smaller islands ches Museum für Naturkunde Stuttgart (SMNS; Stuttgart, and rocks (Fig. 1). The local climate is dry tropical with Germany). a mean annual rainfall of 1,300 mm and a mean annual The material studied in the present work is housed temperature of 25.4 °C. It has strong oceanic influence, in the following collections: ANSP, Academy of Natu- with two well-defined seasons: dry from August to Janu- ral Sciences of Drexel University (Philadelphia, USA); ary and rainy from February to July (Fávaro et al. 2006; MNHN, Muséum national d’Histoire naturelle (Paris, Marques et al. 2007). The vegetation on the islands has France); MNZ, Museum of New Zealand Te Papa Ton- close affinities with the Atlantic Rainforest, though only garewa (Wellington, New Zealand); MZSP, Museu de 5% of the original cover remains (Claudino-Sales 2019). Zoologia da Universidade de São Paulo (São Paulo, Bra- Even so, the islands are rich in endemic species of plants zil); NHMUK, Natural History Museum (London, UK); and animals but have a low overall diversity compared USNM, Smithsonian Institution National Museum of to the mainland, which is especially true for terrestrial Natural History (Washington, DC, USA); ZMB, Museum snails, of which there are three known endemic spe- für Naturkunde, Leibniz Institute for Evolution and Bio- cies (Lopes and Alvarenga 1955). The entire area totals Figure 1. Map showing the location of Fernando de Noronha, Brazil. zse.pensoft.net Zoosyst. Evol. 95(2) 2019, 453–463 455 diversity Science (Berlin, Germany); ZSM, Zoologische Systematics Staatssammlung München (Munich, Germany). The following abbreviations are used herein for shell Superfamily Orthalicoidea dimensions: H, shell height (parallel to coiling axis); D, Family Odontostomidae Pilsbry & Vanatta, greatest shell width (perpendicular to H); h, aperture 1898 height (maximum length parallel to aperture plane); d, aperture width (maximum width parallel to aperture Genus Hyperaulax Pilsbry, 1897 plane); W, number of whorls of shell (approximated to closest quarter); w = number of whorls of protoconch (ap- Bulimulus (Hyperaulax) Pilsbry 1897a: 10; Pilsbry 1897b: 82. proximated to closest quarter). Bonnanius Jousseaume 1900: 39; Schileyko 1999: 337. Two adult specimens of H. ridleyi from lot MZSP 89940 Hyperaulax: Pilsbry 1901: 102; Wenz 1923: 729; Thiele 1931: 660; had a fraction of their foot clipped for molecular study. No Henderson 1935: 145; Morretes 1949: 153; Oliveira et al. 1981: 350; specimen of H. ramagei with preserved soft parts is known. Parkinson et al. 1987: 29; Schileyko 1999: 320; Salgado and Coelho Given our suspected systematic affinity ofHyperaulax , we 2003: 165; Simone 2006: 178; Salvador 2019: 87. also sequenced a specimen of Tomigerus corrugatus Iher- Hyperaulax (Bonnanius): Pilsbry 1901: 103; Thiele 1931: 661; Mor- ing, 1905 (lot MZSP 43077). DNA extraction was carried retes 1949: 153; Zilch 1960: 505; Breure 1974: 52; Oliveira et al. out with QIAGEN DNeasy Blood & Tissue Kit, standard 1981: 350. protocol. We targeted the barcoding fragment of the mito- Hyperaulax (Hyperaulax): Thiele 1931: 661; Morretes 1949: 153; Zilch chondrial COI gene (primers LCO and HCO of Folmer et 1960: 505; Breure 1974: 109. al. 1994), with circa 650 bp. The PCR protocol was set as: Tomigerus (Bonnanius): Parodiz 1962: 453. (1) initial denaturation at 96 °C (2 minutes); (2) denatura- Bonnarius [sic]: Simone 2006: 178. tion at 94 °C (30 seconds); (3) annealing at 48 °C (1 min- ute); (4) extension at 72 °C (2 minutes); (5) repeat steps (2) to (4) 34 times, for a total of 35 cycles; (6) final extension Type species. Bulimus (Bulimulus) ridleyi Smith, 1890, at 72 °C (5 minutes). PCR products were quantified via by original designation. agarose gel electrophoresis, cleaned with ExoSAP-IT™ (Affymetrix Inc.), and Sanger sequenced. The sequences Included species. Hyperaulax ridleyi (Smith, 1890) and were assembled and quality-checked in Geneious Prime H. ramagei (Smith, 1890). (version 2019.0.3, Biomatters Ltd), and uploaded to NCBI GenBank under the accession numbers MN175954 and Diagnosis. Shell bulimoid. Protoconch sculptured by MN175955 (H. ridleyi) and MN175956 (T. corrugatus). sinuous axial riblets, which can anastomose
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