Antrorbis tennesseensis Perez, Shoobs, Gladstone, & Niemiller

Gladstone, Nicholas S., Perez, Kathryn E., Pieper, Evelyn B., Carter, Evin T., Dooley, Katherine E., Shoobs, Nathaniel F., Engel, Annette S. & Niemiller, Matthew L., 2019, A new species of stygobitic snail in the genus Antrorbis Hershler & Thompson, 1990 (Gastropoda, Cochliopidae) from the Appalachian Valley and Ridge of eastern Tennessee, USA, ZooKeys 898, pp. 103-120 : 103

Antrorbis tennesseensis Perez, Shoobs, Gladstone, & Niemiller sp. nov. Figs 1 A–F , 2 A–J

Holotype.

ANSP 476793 (one dry shell in vial, radula, and operculum on SEM stub), stream in Cave Creek Cave (TCS no. TRN5), Roane County, Tennessee, U.S.A.

Paratypes.

ANSP A477042 (same lot as holotype, two whole wet specimens, two dissected wet specimens, one operculum on SEM stub). Three specimens (one dry shell on SEM stub, two whole wet specimens) from Eblen Cave (TCS no. TRN6), Roane County, Tennessee, U.S.A. Specimens are currently housed at the University of Alabama in Huntsville.

Other examined material.

ANSP A476794 (three whole wet specimens), stream in Pedigo Cave (TCS no. TKN103), Knox County, Tennessee, U.S.A. Tentatively classified as Antrorbis cf. tennesseensis .

Morphological diagnosis.

A minute, planispiral Antrorbis , which can be readily distinguished from its sole known congener by the absence of raised tubercles on its finely spirally striate protoconch and its unique radular formula.

Molecular diagnosis.

Average uncorrected pairwise genetic distance at the mitochondrial CO1 locus between A. tennesseensis and A. breweri is 11.7%, with 74.5 ± 2.14 mutations separating the two species. Additionally, average uncorrected pairwise genetic distance at CO1 between the holotype A. tennesseensis and the Pedigo Cave population ( Antrorbis cf. tennesseensis ) is 9.8%.

Description.

Shell ( Figs 2 A–F ; 3 A–C ) planispiral, 1.0-1.75 mm in diameter; 0.58-0.78 mm in height, with 2.75 to 3.25 rounded and variably descending whorls marked by deeply impressed sutures. Aperture nearly circular, almost as wide as high (0.55 × 0.56 mm in the holotype), with an internally thickened and slightly reflected peristome. Umbilicus wide, rapidly expanding. Color pale translucent yellow, with a thick, mottled yellow-orange periostracum. Protoconch ( Fig. 3C ) 1.8 whorls, finely spirally striate, with the innermost striae occasionally and variably punctuated or subtuberculate. Spiral striae continuing into the teleoconch weakly, intersecting with similarly weak axial growth lines.

Operculum ( Fig. 3D, E ) paucispiral with 4.5 whorls, ovate, thin, round, externally concave and sub-conical in profile, with a fragile, tapered periphery. Inner side smooth, with retractor muscle scar variably and roughly thickened but with no peg. Outer side covered with a noticeably thick periostracum.

Radula ( Fig. 3 F–J ) as in its congener A. breweri , but differing slightly in the number of cusps on each tooth: central teeth with 11-13 cusps (5-6+1+5-6) and two basal cusps, laterals with 6-8 cusps on the outer side and 5-6 on the inner side, inner marginals with 26-30 cusps, outer marginals with 19-21 cusps. Data from ANSP 476793, the holotype.

Animal soft body is absent of pigment except for scattered clumps of black granules on stomach and digestive gland; intestine with orange, oval fecal pellets extends from terminal end of animal through body whorl. Digestive system anatomy similar to that described for A. breweri , including intestinal coil in anterior pallial roof exhibiting “reversed-S-shape.” Digestive gland extends for ~1 whorl. Penis simple, strap-like, tapers to a blunt distal end, not as sharply tapered as in A. breweri . Neither terminal papillae nor specialized penial glands observed. Testis one mass with no lobes. Seminal vesicle short and uncoiled, attaching at end of testis. Ovary an orangish mass, filling ~less than 25% of one whorl, capsule gland and albumen gland approximately equal in size, both underly and posterior to the intestine, bursa copulatrix pear shaped. Shells of individuals from Cave Creek Cave are somewhat thicker than those from Pedigo Cave and the fecal pellets are larger and more ovate in shape.

Etymology.

The specific epithet tennesseensis is in reference to this species being from the state of Tennessee. It is also a reference to the University of Tennessee in Knoxville, where several of the authors received degrees (MLN, NSG, and ETC) or are faculty (ASE). Suggested common name is Tennessee Cavesnail.

Distribution.

Antrorbis tennesseensis is known only from two caves developed within karst valleys near the confluence of the Clinch and Tennessee rivers and in upper Cambrian to lower Ordovician carbonate rocks of the Knox Group of the AVR of eastern Tennessee ( Fig. 1 ). Cave Creek Cave and Eblen Cave are only 6 km apart from each other on opposite sides of a surface watershed divide, but cave passages could be hydrologically connected. In contrast, Pedigo Cave ( Antrorbis cf. tennesseensis ) is located to the northeast in northern Knox County. There could be additional caves with A. tennesseensis within the immediate karst area, but the potential for a significantly wider distribution for A. tennesseensis throughout eastern Tennessee is low due to the generally restrictive nature of folded and faulted nature of the karstified strata.

Ecology.

Snails are largely found amongst cobble in shallow cave streams in the dark zone. At Cave Creek Cave, several snails could be observed on a single cobble, and Caecidotea spp. and Crangonyx spp. amphipods were found on the same rocks as snails. From Pedigo Cave ( Antrorbis cf. tennesseensis ), a single small crayfish ( Cambarus bartonii ) was observed, but no other aquatic species were seen in the cave stream. Several snails were also found in close proximity on the same rock, with up to seven individuals on a single rock. No other fauna was found in Eblen Cave, and no egg masses or other aspects of the reproductive biology of A. tennesseensis have been observed from any of the caves. Although annual physicochemical measurements were not acquired in this study, the parameters measured once from each system (Table 3 ) were similar and within the expected conditions for water flowing through carbonate rocks.

Habitat.

Antrorbis tennesseensis has been observed on the sides and undersurface of larger cobble and flat rocks in shallow water (<12 cm water depth) of the stream in Cave Creek Cave and more than one meter of water depth in Pedigo Cave ( Antrorbis cf. tennesseensis ). At Cave Creek Cave, A. tennesseensis has been found only from a small (55 m2) area ca. 40 m from the entrance ( Fig. 4A ). Snails had higher abundances among small cobble substrate and larger rocks in the cave stream near the stream bank (i.e., within 0.6 m), with an average flow rate of 0.34 m/s and depth below 8 cm. At Pedigo Cave, Antrorbis cf. tennesseensis were found throughout the cave stream, and specifically in a riffle with several flat rocks and cobbles ca. 30 m from the entrance. They were also found in deeper pools under larger rocks ( Fig. 4B ). At Eblen Cave, only three snails were found within the primary stream passage accessible in the right fork ca. 100 m from the cave entrance. All snails were found on larger rocks semi-submerged in silt-bottom substrate, which was the primary substrate at the beginning of the stream.

Phylogenetic relationships.

The resulting CO1 gene topology of the ML phylogeny is shown in Fig. 5 . The genus Antrorbis clusters with the stygobitic Cochliopidae along with the recently reassigned Phreatodrobia ( Clark 2019a) and the genus Holsingeria . The holotype population of A. tennesseensis forms a clade with A. breweri . population, but forms a paraphyletic group with the morphologically similar Pedigo Cave population ( Antrorbis cf. tennesseensis ) in the maximum likelihood phylogeny. However, results of the KH and SH tests fail to reject the a priori topology of monophyly (P> 0.05 for both tests).

Conservation assessment.

This species is currently only known from two caves that are within geologically and hydrologically restricted strata. However, the third cave population for Antrorbis cf. tennesseensis was incorporated in these analyses. The NatureServe rank calculated for Antrorbis tennesseensis is Critically Imperiled (G1). For the IUCN Red List assessment, A. tennesseensis was assessed as Endangered (EN) B1a, as the species is known from fewer than five sites and has an EOO <5,000 km2. The AOO was calculated as 12.0 km2 and EOO was 73.3 km2. A maximum of 23 (on 3 June 2018), 54 (on 15 December 2018), and 3 individuals (on 24 March 2019) were observed at Cave Creek, Pedigo, and Eblen Caves, respectively. Mean number of snails observed at Cave Creek Cave and Pedigo Cave (for which multiple surveys were conducted) was 18.4 ± 4.3 and 36 ± 7.8, respectively. Overall, threat impact for this species was calculated as Very High, with the two most outstanding categories of the threat assessment being Human Intrusion and Disturbance and Pollution.

Figures

Figure 1. Distribution of Antrorbis spp. in relation to USGS hydrologic units: regions (HU 2, shaded areas), basins (HU 6, solid black lines), and subbasins (HU 8, solid grey lines; unlabeled in map). Antrorbis breweri occurs within the Upper Coosa subbasin of the South Atlantic-Gulf region, whereas A. tennesseensis and Antrorbis cf. tennesseensis occurs in the Watts Bar Lake and Lower Clinch subbasins within the Upper Tennessee basin (Tennessee region), respectively.

Figure 2. Paratype specimens of Antrorbis tennesseensis sp. nov. A, B Paratypes ANSP A 477042 C-E Antrorbis cf. tennesseensis; ANSP A 476794 F live specimens of Antrorbis cf. tennesseensis from Pedigo Cave. Scale bar: 1 mm. Photograph credits: A-E NFS; F MLN.

Figure 3. Shell, opercula, and radula of Antrorbis tennesseensis sp. nov. A, B Holotype, ANSP 476793 C protoconch of Antrorbis cf. tennesseensis, ANSP 476793 D operculum, outer side, ANSP A 477042 E operculum, inner side, ANSP 476793 F radula of ANSP 476793 G central teeth, ANSP 476793 H lateral teeth, ANSP 476793 I inner marginal teeth, ANSP 476793 J outer marginal teeth, ANSP 476793 Scale bars: 0.5 mm (A, B); 200 μm (C); 200 μm (D, E); 20 μm (F); 5 μm (G); 5 μm (H); 10 μm (I, J). Photograph credits: NFS.

Figure 4. A Cave Creek Cave. Bottom B Pedigo Cave C Eblen Cave (NSG and ETC). Photograph credits: A, B NSG C EBP.

Figure 5. Maximum-likelihood phylogeny of four families within the Cochliopidae. Phylogeny is inferred by W-IQ-TREE based on mitochondrial CO 1 sequences (658 bp aligned). Ultrafast bootstrap support values shown at nodes.