The Bulimulidae (Mollusca: Pulmonata) from the Región de Atacama, northern Chile

The bulimulid genus Bostryx Troschel, 1847 is the most species-rich genus of land snails found in Chile, with the majority of its species found only in the northern part of the country, usually in arid coastal zones. This genus has been sparsely studied in Chile and there is little information on their distribution, diversity or ecology. Here, for the first time, a formal analysis of the diversity of bulimulids in the Región de Atacama, northern Chile, is reported. Of the seventeen species recorded for the area, most of them were efectively found in the field collections and one record was based on literature. Five taxa are described as new: Bostryx ancavilorum sp. nov., Bostryx breurei sp. nov., Bostryx calderaensis sp. nov., Bostryx ireneae sp. nov. and Bostryx valdovinosi sp. nov., and the known geographic distribution of seven species is extended. Results reveal that the Región de Atacama is the richest region in terrestrial snails in Chile, after the Juan Fernández Archipelago. All of the terrestrial molluscan species occurring in the area are endemic to Chile, most of them with restricted geographic distributions along the coastal zones, and none of them are currently protected by law. Further sampling in northern Chile will probably reveal more snail species to be discovered and described.

The family Bulimulidae Tryon, 1867 is represented in Chile solely by the genus Bostryx Troschel, 1843, an endemic South American genus distributed from Suriname to Chile (Breure, 1978). In Chile, this genus is found mostly on coastal localities in northern-central Chile, from Arica, Región de Arica y Parinacota (18 • 29 ′ S, 70 • 20 ′ W), to Coquimbo, Región de Coquimbo (29 • 57 ′ S, 71 • 20 ′ W). This work presents a review, with distributions and illustrations, of all the Bostryx species found in the Región de Atacama, northern Chile, including a key to all the taxa under consideration. The aim of this preliminary paper is to contribute to the knowledge of the land snail fauna in Chile, particularly to assess conservation status of all these species, which are particularly endangered in the coastal areas of the country.

MATERIALS AND METHODS
The Región de Atacama is situated in northern Chile (25 • 17 ′ S to 29 • 30 ′ S), it covers approximately 75,176 km 2 and has one of the lowest human population densities in the country, being also one of the most desertic areas of Chile. This Región occupies the southern part of the Atacama Desert and has a cold desert climate (BWk) (Peel, Finlayson & McMahon, 2007), and a high relative humidity (Average 74%) in its coastal areas, product of night fogs and high coastal nubosity; with very scarce precipitation, most of which is associated with the El Niño Southern Oscillation (ENSO) events (Juliá, Montecinos & Maldonado, 2008;Squeo et al., 2006). Detailed descriptions of the surveyed area, particularly of the flora and higher fauna are provided in Squeo, Arancio & Gutiérrez (2008).
Most of the collections were made in the coastal desert areas around the port of Caldera (27 • 04 ′ S; 70 • 50 ′ W) during the summers of 2009 to 2012 and in August-December 2012. Surveys were undertaken in a similar manner as those of Cowie & Robinson (2003) and also by collecting litter for further sorting in the laboratory. A synopsis of the localities is given in Table 1. The studied samples were variably preserved, from live specimens with periostracum and epiphragm to eroded shells. The terminology of shell morphology is based upon Breure (1979)   lip; HT, holotype; LW, height of last whorl, including lip; NW, number of whorls; PT, paratype WA, width of aperture, including lip. All the measurements are given in mm, otherwise indicated. The electronic version of this article in Portable Document Format (PDF) will represent a published work according to the International Commission on Zoological Nomenclature (ICZN), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone. This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix http://zoobank.org/. The LSID for this publication is: urn:lsid:zoobank. org:pub:3F2E9582-A5D0-431D-BC3E-3917DC812323. The online version of this work is archived and available from the following digital repositories: PeerJ, PubMed Central and CLOCKSS.   Description: Shell up to 16.8 mm, 1.95 times as long as wide, elongate-ovate, rimateumbilicate, with slightly convex whorls, fragile. Shell thin, translucent, slightly pinkish, decorated with minute streaks of opaque white. Surface lustrous, with marked axial growth striae, fine spiral striae more marked towards the subsutural area, where it crosses the axial growth lines. Protoconch small, smooth; on magnification it shows a fine microsculpture of axial costulae. Spire acute, slightly concave, with 6.25 slightly convex whorls, a little angulated near the well-impressed sutures. Last whorl very slightly carinated at the perifery, compressed below. Aperture elongate-subovate, 1.77 times as long as wide, 0.55 times the total height. Peristome simple, sharp, very fragile. Columellar margin concave and folded over the shallow umbilicus, well dilated above. Soft parts unknown.

Distribution:
Only known from type locality.

Etymology:
In honour of Abraham Breure (Naturalis Biodiversity Centre, Leiden, The Netherlands), for his contributions to the taxonomy of land Mollusca, especially that of Chile and Perú, and in particular for his extensive work on Bulimulidae.

Remarks:
This new species has a distinctive light and fragile shell, different from all the other Bostryx species found in the area. Bostryx paposensis (Pfeiffer, 1856), described from Paposo (25 • 05 ′ S; 70 • 25 ′ W), in the Región de Antofagasta, has a shell of similar outline, however its protoconch and first whorls are smaller and darker, the whorls are almost flat and the spire is more convex. This is a rare species, from which only two, somewhat worn complete specimens (paratype with a broken external lip; Fig. 3G) were recovered from Diagnosis: A Bostryx species characterized by a somewhat obese-ovate white shell, with a prominent last whorl, a pink to red colored inside of an oval-elongate aperture, with a strong and angulated columella and a deep umbilicus.
Description: Shell small (H up to 25 mm), obese-ovate, solid, opaque white, with 5.5-6.0 convex whorls; earlier whorls fleshy or corneous, smooth, separated by deep sutures. Protoconch large, smooth; in magnification with very fine wrinkles near the sutures. Surface of shell dull or slightly shining, with irregular wrinkles of growth. Spire slightly short, conic, last whorl slightly angulated at the periphery of shell. Aperture oval-elongate, slightly oblique, receding, over half the shell's length, pale pink to red within; lip moderately thick but sharp, slightly expanded, the edge whitish, simple. Columella broadly dilated, folded over the umbilicus; its inner edge straight or slightly concave, sharp; parietal callus a mere glaze. Umbilicus large, broad and deep. Soft parts unknown.

Distribution:
Only known from type locality.

Remarks:
This new species has a distinctive deep umbilicus, which almost reach the protoconch (Fig. 4E), different from almost all of the other Bostryx species found in the area. This species is also slightly variable in morphology, with some specimens having shorter (Fig. 4A) or larger shells (Fig. 4L); the characteristic wide columella is, however, a constant feature in most of the specimens examined. Bostryx erythrostomus (Sowerby I, 1833) is somewhat similar to this new species, differing in the much larger shells, with a darker coloration of the aperture, the generally more convex whorls, a less pronounced umbilicus and in having a larger and shinier shell. Bostryx huascensis (Reeve, 1848) differs from the new species in its smaller shell with a larger spire and a comparatively smaller and pale brown to brownish colored aperture. This species is restricted to sandy areas around and in the city of Caldera and is exposed to urban development and human intervention of its habitat.  Stuardo & Valdovinos, 1985: 56;Stuardo & Vega, 1985: 135. Bostryx (Peronaeus) erythrostomus Valdovinos, 1999: 150. Bostryx erythrostoma Neubert & Janssen, 2004Köhler, 2007: 132, Fig. 26.

Description (After Pilsbry, 1896):
Shell obese-ovate, solid, white, with irregular indistinct fleshy or gray-blue streaks and small scattered dots, the latter translucent by transmitted light, these markings often inconspicuous; earliest whorls fleshy or corneous, smooth. Protoconch smooth, with very fine axial striae near the sutures visible only under magnification. Surface slightly shining, with irregular wrinkles of growth, and seen under the lens to be cut by superficial incised spiral lines into series of long granules, often absent on middle and base of last whorl. Spire short, conic, composed of 5.5-5.75 very convex whorls, separated by deep sutures. Last whorl rotund. Aperture slightly oblique, round-ovate, over half the shell's length, crimson, rose or red-brown within, becoming light brown in the throat; lip moderately thick but sharp, not expanded, the edge light in color. Columella broadly dilated, its inner edge straight or lightly concave; parietal callus thin, colored. Umbilicus large, colored inside.
Distribution: Stuardo & Vega (1985) recorded this species from Caldera and Huasco at the Región de Atacama, and from Coquimbo at the Región de Coquimbo.
Description (After Rehder, 1945): Shell moderately slender, thin, with 11 moderately convex whorls. Protoconch of two smooth whorls, with the last one-half whorl often showing microscopic crowded wavy riblets. Teleoconch generally smooth except for irregular growth wrinkles and occasional spiral impressed lines giving a malleated appearance to the surface. Shell corneous with irregular opaque-white maculations or streaks, though in the specimens with a heavier shell this mottling may be absent. Last whorl flattened between the periphery and the obtuse keel surrounding the moderately broad umbilicus. Aperture narrowly ovate, outer lip narrowly expanded, columellar lip dilated.
Distribution: This species was described by Rehder (1945) from hills near Copiapó, Región de Atacama. Breure (1978) renamed this species and recorded a new locality at the Quebrada de la Chimba, 10 km N of Antofagasta, Región de Antofagasta, in 350 m altitude.
Remarks: Intensive searches in the type locality around the city of Copiapó yielded no specimens of this taxon; further field collections in the Región de Antofagasta may be useful in order to assess the current presence of this species. Diagnosis: A Bostryx species with an acute apex, characterized by a prominent last whorl of about 0.67 H, with a pattern of opaque white and tan lines on a slender, spindleshaped, malleated translucent shell. Small umbilicus.
Distribution: Stuardo & Vega (1985) cite this species from Paposo and Mejillones, both localities at the Región de Antofagasta. This is the southernmost record for the taxon.
Remarks: This species has a small, sturdier whitish shell, with a thick lip (Pilsbry, 1896).

Description (After Pilsbry, 1896):
Shell umbilicated, ovate-conic, rather solid but thin; corneous, flecked and streaked with white, or opaque white flecked and streaked with corneous, the latter predominating on spire, earlier whorls smooth, corneous. Surface smoothish, with wrinkles of growth, and above the periphery cut into spiral series of long granules by spiral lines. Spire conic, the apex obtuse, smooth. Whorls 5 and a half, slightly convex, the sutures more or less crenulated. Aperture half the total length (more or less), slightly oblique, ovate, white within; outer lip unexpanded, arcuate; columellar lip well dilated above. Remarks: This rare species is slightly similar to B. inaquosum, from which it differs in having a larger, more opaque shell with a less slanted and wider aperture. It can also be compared to B. pupiformis, which have a smaller and more elongated aperture, a much more tenuous parietal callus and a comparatively smaller last whorl. Bostryx anachoreta (Pfeiffer, 1856) differs in having a larger and more elongated shell with a convex-turrited spire (almost concave in the new species), and a larger and narrower aperture.

DISCUSSION
Most of the original descriptions of Bostryx species occurring in Chile have been based solely on conchological characters, and only a few of them have been the subject of additional studies including soft parts (Breure, 1978;Valdovinos & Stuardo, 1988 Rehder (1945) who elevated the subgenus Peronaeus to genus level, however this was not followed by subsequent works dealing with Chilean terrestrial land snails (Breure, 1978;Stuardo & Valdovinos, 1985;Stuardo & Vega, 1985;Valdovinos, 1999). In this regard I am here following Breure (1978) and treating all Bostryx species as belonging to Bostryx s. l.
The Region of Atacama has recently been the subject of several works dealing with its invertebrate fauna, which has uncovered new records and new species endemic to the area (Osorio, 2012;Araya, 2013;Araya & Aliaga, 2015b;Reiswig & Araya, 2014;Collado, 2015;Labrín, Guzmán & Sielfeld, 2015). Most of the taxa discussed in this study were also recorded in often narrow distributions (Table 2), or single localities along the coastal desert. This endemism is alike to that of other bulimid species living in higher altitudes in Peru (Breure & Mogollón, 2010;Breure & Neubert, 2008). In particular, it has been documented that Bostryx snails undergo long-term estivation and that their communities are subjected to the El Niño-Southern Oscillations (ENSO) in the Lomas habitat of coastal Peru (Ramírez et al., 1999). It is very possible that the same circumstances affect the Bostryx communities along the hyper arid coastal areas of the Región de Antofagasta and of the Región de Atacama, where the abundance of shells was correlated with the El Niño phenomena with much more fresh specimens, including the only living snails, found in humid years (JF Araya, unpublished obs., 2015). It was noticed also that there is some relationship between the abundance of shells and the presence of lichen communities in some specific areas; this is consistent with the observation that Bostryx species have been found to feed in lichen and algae (Ramírez et al., 1999). It seems that these snails avoid heat stress and desiccation by retreating beneath the ground surface during the day and being active only when the humidity is high and at night. This behaviour was observed in specimens maintained in captivity, according to Gigoux (1932), and was confirmed during this work. This mode of living may answer why many shells are found in areas with no apparent vegetation, where some species may have living communities despite the aridity of the region. The vast predominance of white shells among the Chilean Bostryx species (nine species of a total of 17 species studied herein) may also represent a strategy for reducing solar radiation absorption and thereby reduce heat, as recorded for other desert snails living in similar conditions (Schmidt-Nielsen, Taylor & Shkolnik, 1971).