Research Article |
Corresponding author: Rodrigo Brincalepe Salvador ( salvador.rodrigo.b@gmail.com ) Academic editor: Frank Köhler
© 2019 Rodrigo Brincalepe 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.
Citation:
Brincalepe Salvador R, Cavallari DC (2019) Taxonomic revision of the genus Hyperaulax Pilsbry, 1897 (Gastropoda, Stylommatophora, Odontostomidae). Zoosystematics and Evolution 95(2): 453-463. https://doi.org/10.3897/zse.95.38259
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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.
Bonnanius, endemic species, Fernando de Noronha, island speciation, Orthalicoidea, Pulmonata
The genus Hyperaulax Pilsbry, 1897 had a unique composition. It comprised two living species endemic to the oceanic Fernando de Noronha Archipelago off Brazil, H. ridleyi (Smith, 1890) and H. ramagei (Smith, 1890), and eight species from Tampa Silex beds (Oligocene) of Florida, USA: H. americanus (Heilprin, 1887), H. ballistae (Dall, 1915), H. floridanus (Conrad, 1846), H. heilprinianus (Dall, 1890), H. remolinus (Dall, 1915), H. stearnsii (Dall, 1890), H. tampae (Dall, 1915), and H. tortilla (Dall, 1915). Suspecting this could not reflect an actual relationship, the fossil species previously assigned to Hyperaulax were revised by
The two Recent species are also not without problems, as two names are currently considered synonymous with H. ramagei; moreover, this species is included in the subgenus Bonnanius Jousseaume, 1900, which can sometimes be recognized as a valid genus (e.g.,
Therefore, herein we conducted a taxonomic review of the two Recent species of Hyperaulax, assessing their familiar allocation within Orthalicoidea and the validity of the subgenus Bonnanius and of the two species synonymized with H. ramagei. Furthermore, an updated diagnosis and description, alongside images of the type and additional materials, is provided here for each species.
Fernando de Noronha is an archipelago located ca 350 km off northeastern Brazil (3°50'–3°52'S, 32°24'–32°28'W) originating from extinct volcanic structures estimated to be 1.8–12.4 Ma old. It comprises the main island of Fernando de Noronha (17 km²) and over 20 smaller islands and rocks (Fig.
All the type specimens were analyzed and the main museum collections worldwide that could contain material of Hyperaulax were visited or contacted for loans or photographs and information of their specimens. The type materials are illustrated herein, alongside additional specimens to thoroughly show conchological variation. Shell measurements were taken with a digital caliper. SEM images of the protoconchs were obtained at the Staatliches Museum für Naturkunde Stuttgart (
The material studied in the present work is housed in the following collections:
The following abbreviations are used herein for shell dimensions: H, shell height (parallel to coiling axis); D, greatest shell width (perpendicular to H); h, aperture height (maximum length parallel to aperture plane); d, aperture width (maximum width parallel to aperture plane); W, number of whorls of shell (approximated to closest quarter); w = number of whorls of protoconch (approximated to closest quarter).
Two adult specimens of H. ridleyi from lot
Additional orthalicoid COI sequences were obtained from GenBank, originating from the work of
All sequences were aligned in Geneious Prime with the MUSCLE plugin (Edgar 2004; default settings, accuracy-optimized) and further proofed manually. A tree was built in Geneious Prime by Bayesian Inference (MrBayes plugin;
Bulimulus (Hyperaulax)
Bonnanius
Hyperaulax:
Hyperaulax (Bonnanius):
Hyperaulax (Hyperaulax):
Tomigerus (Bonnanius):
Bonnarius
[sic]:
Bulimus (Bulimulus) ridleyi Smith, 1890, by original designation.
Hyperaulax ridleyi (Smith, 1890) and H. ramagei (Smith, 1890).
Shell bulimoid. Protoconch sculptured by sinuous axial riblets, which can anastomose and fade on abapical region. Umbilicus surrounded by a periumbilical spiral angulation.
Shell small to medium-sized, bulimoid, with ca 4–5 convex whorls; ground color cream, ochre or brown, with 1–4 lighter-colored spiral bands on lateral portion of whorls; periumbilical region completely or marginally discolored, whitish; apex (especially protoconch) usually of lighter color. Suture well-marked. Protoconch sculptured by numerous fine sinuous axial riblets, transition unclear. Teleoconch overall smooth except for axial growth lines. Aperture ovoid; peristome white, reflected, thickened, and continuous, with 0–4 apertural teeth. Umbilicus perforate, well marked.
After
Hyperaulax ridleyi. A–E. Lectotype,
The genus Bonnanius is considered here synonymous with Hyperaulax as there are no diagnostic characters allowing its clear separation other than its larger shell size. The presence of teeth in the aperture of H. ramagei (previously classified in Bonnanius) could be used as a diagnostic genus-level character; however, it is well known that odontostomid genera show great inter- and intraspecific variation in the presence and strength of apertural teeth. Moreover, some specimens of H. ridleyi do show a palatal tooth (Fig.
The protoconch sculpture has always been deemed a good character to define genera in Orthalicoidea and has more recently received large support from molecular studies (
Other conchological characters are very similar in both H. ridleyi and H. ramagei: the roughly pentagonal shape of the aperture and its positioning in relation to the body whorl, the long palatal tooth (absent in most H. ridleyi specimens), the shape of the umbilicus and the periumbilical spiral angulation, the unsculptured teleoconch (except for growth striations), and the periostracum color (brown with at least one white spiral band).
The classification of Hyperaulax in Odontostomidae has been well supported in the literature, with just a few different classification schemes. For instance,
In any event, there are other conchological characters favoring an allocation within Odontostomidae, such as the elevated embryonic whorls (
Our analysis of interspecific affinities using the barcoding region of the COI marker has grouped Hyperaulax (H. ridleyi only) with Tomigerus, as expected by our morphological analysis, with a posterior probability of 0.997. However, these two species were grouped with Simpulopsis Beck, 1837 (family Simpulopsidae) in our Bayesian tree, instead of being grouped with other odontostomids. This is likely due to the fact that COI alone is not sufficient to solve family-level relationships among stylommatophoran snails (
It is curious that another orthalicoid lineage, from the other side of South America, evolved an uncannily similar shell shape to Hyperaulax: Naesiotus wolfi (Reibisch, 1892), from the Galapagos (lectotype
Bulimus (Bulimulus) Ridleyi
E.A.
Bulimulus (Hyperaulax) ridleyi:
Buliminus ridleyi:
Hyperaulax ridleyi:
Hyperaulax (Hyperaulax) ridleyi:
Hyperaulax (s. str.) ridleyi:
Bulimus (Bulimulus) ridleyi:
Fernando de Noronha Archipelago, Fernando de Noronha Island and Rata Island. Original (
Known only from Fernando de Noronha Archipelago.
Lectotype
Types. BRAZIL: Fernando de Noronha:
The shell is smaller overall and has a more elongated and slender profile. The protoconch has a more raised ridge and its sculpture consists largely of more anastomosed riblets. Typically, there is no apertural dentition.
Shell small, bulimoid, slender; spire tall; W ~ 4¾–5. Shell color ochre to brown; body whorl sometimes darker than rest; fine white spiral band on middle portion of whorl; periumbilical spiral angulation discolored, whitish; peristome white. Protoconch (w ~1¾) rounded, with raised ridge that becomes a faint subsutural ridge on teleoconch; sculptured by fine sinuous axial riblets, which sometimes anastomose (especially on abapical area of whorl); transition to teleoconch unclear. Teleoconch smooth (except for growth lines). Suture well marked, but not deep. Aperture ovoid, elongated. Peristome reflected and slightly thickened; presence of small channel-like structure on division between parietal and palatal regions of aperture; parietal callus might be present in older specimens. Apertural teeth usually absent, but faint elongated tooth on middle portion of palatal region may be present (Fig.
Lectotype: H = 11.4 mm, D = 5.9 mm, h = 4.8 mm, d = 3.0, W = 5¼, w = 1¾. Paralectotype #1: H = 9.5 mm, D = 5.3 mm, h = 4.4 mm, d = 3.0 mm, W = 4½, w = 1½. Paralectotype #2: H = 9.1 mm, D = 5.3 mm, h = 4.3 mm, d = 2.9 mm, W = 4½, w = 1¾. Paralectotype #3: H = 8.9 mm, D = 5.2 mm, h = 4.3 mm, d = 2.9 mm, W = 4½, w = 1¾. Paralectotype #4: H = 8.9 mm, D = 5.2 mm, h = 4.2 mm, d = 2.8 mm, W = 4½, w = 1¾. Average (n = 63, except for w, where n = 10): H = 10.2 ± 1.00 mm (min = 7.8 mm, max = 12.7 mm), D = 5.7 ± 0.51 mm, h = 4.9 ± 0.45 mm, d = 3.5 ± 0.34 mm, W = 4¾ to 5 (min = 4¼, max = 5½), w = 1¾ (occasionally 1½).
Other than showing a reasonable variation in shell size, the species displays little conchological variation (Fig.
Unfortunately, not much can be found in the literature about this species’ habitat or habits, but the museum labels point to a variety of collection locales, albeit more usually referring to dead shells only. In any event, this species has been reported alive from forested areas, mangrove, beaches, dunes, and gardens.
“Turbine, in cui la prima voluta è (…)”
Bulimus (Tomigerus) Ramagei
E.A.
Bulimus
(Tomigerus?) Ramagei:
Bonnanius bouvieri
Bonnanius bonnanius
Hyperaulax (Bonnanius) ramagei:
Tomigerus (Bonnanius) ramagei:
Bulimus (Tomigerus) ramagei:
Bonnanius ramagei:
Hyperaulax ramagei:
Bonnarius
[sic] ramagei:
Fernando de Noronha Archipelago, Fernando de Noronha Island, Ponta do Tabaco. Original (
Known only from Fernando de Noronha Archipelago.
Lectotype
Types. BRAZIL: Fernando de Noronha:
The shell is larger overall and has a broader profile. The riblets on the second part of the protoconch are more defined. The peristome is strongly thickened and displays marked apertural teeth.
Shell medium-sized, bulimoid, rounded; W ~ 4½. Shell color chestnut brown; spire apex light brown to cream-colored; up to four equidistant white spiral bands might be present on lateral portion of whorls (but entirely brown morphs also occur); periumbilical region usually discolored, whitish; peristome and apertural teeth white. Protoconch (w ~1¾) rounded; first ½ whorl presenting undefined anastomosing sculpture; remainder sculptured by fine sinuous axial usually well-defined riblets (but sometimes anastomosed in some areas) that become less pronounced towards teleoconch; transition to teleoconch unclear (but sometimes with thickening of the last riblet). Teleoconch smooth (except for growth lines, which become more marked towards aperture). Suture well-marked, but not deep. Aperture roughly ovoid, but angulate. Peristome reflected and strongly thickened; some older specimens show continuous thickening of the peristome; parietal callus might be present in older specimens. Apertural teeth present: two knob-like parietal teeth positioned slightly towards the interior of shell (not always present); long palatal tooth in the middle portion of palatal region (its surface goes from smooth to serrated, with up to three distinct points); columellar tooth elongated, with smooth surface. Both columellar and palatal tooth produce a marked depression on outer wall of shell. Umbilicus slit-like.
Lectotype: H = 17.3 mm, D = 12.3 mm, h = 8.8 mm, d = 6.6, W = 4, w = 2. Paralectotype #1: H = 22.3, D = 15.6 mm, h = 10.9 mm, d = 7.7 mm, W = 4¾. Paralectotype #2: H = 23.5 mm, D = 16.0 mm, h = 11.2 mm, d = 8.7 mm, W = 5. Paralectotype #3: H = 19.5 mm, D = 14.6 mm, h = 10 mm, d = 7.2 mm, W = 4½, w = 1¾. Paralectotype #4: H = 19.6 mm, D = 13.7 mm, h = 8.8 mm, d = 6.7 mm, W = 4½. Paralectotype #5: H = 20.3 mm, D = 13.2 mm, h = 9.8 mm, d = 7.4 mm, W = 4¾, w = 1¾. Syntype of Bonnanius bouvieri: H = 22.5 mm, D = 15.4 mm (Breure, 1975). Average (n = 34, except for w, where n = 10): H = 17.9 ± 1.56 mm (min = 16.1 mm, max = 22.0 mm), D = 12.9 ± 0.96 mm, h = 9.7 ± 0.71 mm, d = 7.6 ± 0.63 mm, W = 4½ (min = 4¼, max = 5), w = 1¾ (occasionally 2).
The names H. bouvieri and H. bonnanius were synonymized with H. ramagei by
The shell features of H. ramagei display some morphological variation: (1) shell size, from some rather small specimens to very large ones (Hmin = 16 mm and Hmax = 22 mm); (2) shell color can go from entirely brown to marked with four white spiral bands; (3) aperture size, relative to remainder of the shell; (4) shell shape, with some specimens having a much shorter spire (Fig.
Some of the specimens available (including some paralectotypes) appear to be of a sub-fossil state, as already noted by
Hyperaulax is here classified in the Odontostomidae and presently contains two species, H. ridleyi and H. ramagei, both endemic to Fernando de Noronha Archipelago. This genus seems to be more closely related to Tomigerus than to other odontostomids.
According to recent collection events on Fernando de Noronha, H. ramagei cannot be found alive in spite of meaningful search efforts (L.R.L. Simone personal communication). In fact, museum specimens of H. ramagei still bearing the periostracum typically date back to the first half of the 20th century. It is a troubling possibility that presently this species has a much-reduced range or is altogether extinct. Future collection efforts should focus on this species to properly define its status according to current guidelines for conservation (
Finally, another curious aspect of the fauna of Fernando de Noronha deserving further study is Amphisbaena ridleyi Boulenger, 1890, an amphisbaenid (worm lizard) endemic to the archipelago that possesses adaptations for a durophagous diet including a large proportion of land snails (
We are very grateful to Luiz R.L. Simone (
Below are listed the COI sequences of other Orthalicoidea species, obtained from the work of
The sequence of the outgroup taxon was obtained from GenBank: Planorbis planorbis EF012175 (Planorbidae).