Morphological and molecular diversification of slender salamanders (Caudata: Plethodontidae: Batrachoseps) in the southern Sierra Nevada of California with descriptions of two new species Author Jockusch, Elizabeth L. Author Martínez-Solano, Iñigo Author Hansen, Robert W. Author Wake, David B. text Zootaxa 2012 3190 1 30 journal article 45455 10.5281/zenodo.215268 faaebecf-4cd9-4f87-88c4-402339b99d3b 1175-5326 215268 Batrachoseps bramei new species Suggested common name: Fairview Slender Salamander Figures 4–5 B. simatus (part) Brame and Murray 1968 :16 Holotype . Museum of Vertebrate Zoology ( MVZ ) 217944, an adult female from Packsaddle Canyon, adjacent to Kern River, 1137 m elevation, Tulare Co., California, USA ( 35.945°N , 118.476°W ), collected 9 March 1991 by Robert W. Hansen. Paratypes . MVZ 168749–168755, same locality as holotype , collected 10 March 1979 by Robert W. Hansen; MVZ 217945, same data as holotype ; MVZ 168756–168763 and MVZ 168950 from Brin Canyon at junction Kern River, Tulare Co., California, USA ( 35.952°N , 118.471°W ), collected 11 March 1979 by Robert W. Hansen; MVZ 168737–168738 and MVZ 168740 from Fairview, Tulare Co., California, USA ( 35.927°N , 118.494°W ), collected 10 March 1979 by Robert W. Hansen. Referred specimens. MVZ 107168–107169 from 3.6 km S Fairview, E side of Kern River, Tulare Co., California, USA ( 35.892°N , 118.464°W ), collected 18 February 1973 by Samuel Sweet and Marjorie Reaka; MVZ 107170 (collected 18 February 1973 by Samuel Sweet), MVZ 168739, MVZ 168741–168748 (collected 10 March 1979 by Robert W. Hansen) all from Fairview, E side of Kern River, Tulare Co., California, USA ( 35.927°N , 118.494°W ); MVZ 217946–217954 from Cannell Creek, S side, W of Aqueduct, E of Kern River, Kern and Tulare counties, California, USA ( 35.794°N , 118.434°W ), collected 10 March 1991 by Robert W. Hansen; MVZ 224858– 224859 from Upper Kern River Canyon at Mountain Highway 99 bridge over Kern River at confluence with South Falls Creek, E side of Kern River, Tulare Co., California, USA ( 35.968°N , 118.486°W ), collected 27 March 1994 by Elizabeth L. Jockusch, David B. Wake and others; MVZ 267129–267137 from trail along W side of Kern River, ca. 0.8–1.0 km N Mountain Highway 99 bridge over Kern River at confluence with South Falls Creek, Tulare Co., California, USA ( 35.973°N , 118.488°W to 35.977°N , 118.487°W ), collected 28 January 2010 by Elizabeth L. Jockusch, Elizabeth K. Timpe and Chris Evelyn; MVZ 267140–267142 from Tobias Creek drainage, along trail in vicinity of its crossing of Tobias Creek, Tulare Co., California, USA ( 35.902°N , 118.516°W ), collected 22 March 2007 by Elizabeth L. Jockusch and Iñigo Martínez-Solano; MVZ 267154 from Whiskey Flat Trail, ca. 1 km N of Bull Run Creek, W side of Kern River, Tulare Co., California, USA ( 35.793°N , 118.452°W ), collected 20 March 2008 by Iñigo Martínez-Solano and Elizabeth L. Jockusch; MVZ 267118–267122 from Plater Rd., just N junction Burlando Rd., Kern Co., California, USA ( 35.736°N , 118.428°W ), collected 21 March 2008 by Elizabeth L. Jockusch and Iñigo Martínez-Solano; MVZ 251741–251749 from WNW of Wofford Heights, Tillie Creek drainage, Kern Co., California, USA ( 35.714°N , 118.476°W ), collected 27 March 2005 by Brad Alexander. Diagnosis. A small, slender species (standard length, SL, of ten adult males 34.3 mm ± 2.4 mm ; of eleven adult females 35.5 mm ± 3.8 mm ) distinguished from other species of the B. nigriventris group as follows: from B. simatus by smaller adult size, somewhat more robust appearance (including a longer, broader head, longer limbs and larger feet) and fewer trunk vertebrae (mode 18–19 versus 20–21 in B. simatus ); from B. relictus by its longer legs and wider feet; from B. gregarius and B. nigriventris by its substantially more robust appearance including a longer and broader head, longer limbs, and larger hands and feet; from B. stebbinsi Brame and Murray 1968 by its much smaller size and less robust morphology. Distinguished from other species of Batrachoseps in the southern Sierra Nevada as follows: from B. campi Marlow, Brode and Wake 1979 and B. robustus , both members of subgenus Plethopsis , by its unpaired premaxillary bones and smaller, less robust habitus and from B. kawia by its more robust, longer-limbed morphology. FIGURE 4. Holotype of B. bramei (MVZ 217944). A. Digital x-ray of skull and forelimbs. Digital x-rays were processed using the levels and curves functions in Adobe Photoshop. B. Photo of holotype in life. Description. Batrachoseps bramei is a small (adults generally less than 45 mm standard length), slender species with a relatively broad, dorsoventrally flattened head and long limbs. The facial region (from the eyes to the snout) is relatively large and almost as broad as the posterior portion of the head; the eyes are moderately protuberant and visible projecting beyond the jaw line in ventral view. The nostrils are small and the nasolabial protuberances are slight to moderate. There is no evidence of a mental hedonic gland under the chins of males. Grooving patterns of the head, throat, and neck are typical of the genus. Standard length ranges from 7.2–8.1 (mean = 7.7) times head width in males and 7.5–9.9 (mean = 8.0) times head width in females. Teeth are relatively numerous: 6– 11 (mean = 7.4) premaxillary teeth in males, 8–18 (mean = 13.7) in females; 31–49 (mean = 40.0) maxillary teeth in males, 32–68 (mean = 47.2) in females; 12–17 (mean = 14.8) vomerine teeth in males, 10–25 (mean = 17.9) in females. The vomerine teeth are arranged patchily to semi-patchily. Small maxillary teeth are borne in a long row extending about to the posterior end of the eyes in females. The premaxillary teeth are the same size as maxillary teeth in females; in males the premaxillary teeth are substantially enlarged. Both males and females have 17–18 costal grooves between the limb insertions. The tail is tapering and relatively short, exceeding body length only in the largest animals. The tail is 1.0–1.1 (mean = 1.0) times SL in males, and 0.9–1.1 (mean = 1.0) times in females in specimens lacking evidence of tail regeneration. There is no basal tail constriction. The postiliac gland is visible as an obscure pale spot. The limbs are relatively long; limb interval ranges from 4.5–6 (mean = 5.2) in males and 5–8 (mean = 5.9) in females. SL ranges from 4.5–6.0 (mean = 5.1) times hind limb length in males and 4.6–5.7 (mean = 5.0) times in females. The hands and feet are relatively large; foot width ranges from 1.7–2.2 mm (mean 2.0 mm) in both males and females. The digits are well formed and discrete with expanded tips that bear subterminal pads. Webbing occurs between the fingers and toes of some individuals, and extends to approximately the second phalanx. Fingers and toes in order of decreasing length are 3-2,4-1. Digit 1 is very reduced. FIGURE 5. Color pattern variation in B. bramei . A. Specimen from the type locality; note the rust colored patches over the shoulders. The presence of these patches is typical of B. bramei . B. MVZ 267142, from Tobias Creek, Tulare Co., California. C–F. Four specimens from Cannell Creek, Kern and Tulare counties, California, showing range of coloration found in this population. The bold red coloring is not known from other populations. Refer to the web version of this article for color figure. Measurements of the holotype (in millimeters). Maximum head width 4.1; snout to gular fold (head length) 8.3; head depth at posterior angle of jaw 1.9; eyelid length 2.5; eyelid width 1.2; anterior rim of orbit to snout 1.3; horizontal orbital diameter 1.7; interorbital distance 1.4; snout to forelimb 10.7; distance separating external nares 1.7; snout projection beyond mandible 0.5; snout to posterior angle of vent (SL) 40.7; snout to anterior angle of vent 37.3; axilla to groin length 23.4; tail length 33.5; tail width at base 1.9; tail depth at base 1.8; forelimb length 6.7; hind limb length 7.2; limb interval 8; width of right hand 1.7; width of right foot 2.2; foot length 2.9; length of third toe 0.8; body width behind forelimbs 2.2. There are 15 premaxillary, 46 maxillary, and 20 vomerine teeth; the row of maxillary teeth on the right appears short, ending at the posterior border of the internal naris. There are 18 costal grooves between the limb insertions. Coloration of the holotype (in life). Uniformly flat black ventrally with delicate sprinkling of punctate guanophores; ventral guanophores are tiny and rarely connect; most numerous on gular region and at lowest density on tail; guanophores abundant on lateral surfaces, where they become expanded and form irregular patches. On lateral surfaces, guanophores cover more area than ground color. Dorsum metallic silver as a result of numerous expanded guanophores that are especially concentrated dorsolaterally; silvery coloration has metallic brassy-gold highlights; from a distance the silver on black background appears bluish-gray. Guanophores on head more disconnected and less concentrated, but the whole head, including eyelids and snout, is heavily spotted. Pigment most concentrated on nape of neck and front of limbs. Limbs heavily pigmented, especially proximally, but even fingers and toes have extensive spotting. Dark gray iris also has some dorsal guanophores. Only face region has light spotting. Ground color of dorsum slate black to brownish black. Under high magnification, it is clear that the lateral guanophores are more white and superficial, while the dorsal ones are deeper and more metallic. They co-occur on the dorsum, with the superficial cells rare. On the tail, the metallic color becomes gold or brassy and very concentrated. Morphological variation. Males sampled from the northern end of the range have relatively small adult body size compared to populations from the southern end of the range (mean of 8 males from southern Wofford Heights 42.1 ± 3.6 mm vs. 33.8 ± 3.7 mm for 28 males from northern Packsaddle/Brin/Fairview). No significant differences in female body size across populations were detected; however, sample sizes were <10 for three of four populations from which series were measured. Comparisons between animals from Cannell Creek and the vicinity of the type locality show that chest width is slightly narrower in populations from near the type locality, which accounts for the significant differences in PC2 and PC3, described above. Wofford Heights individuals have insignificant webbing compared to the type series. Coloration is highly variable both within and between populations ( Fig. 5 ). Many specimens have distinct patches of color over the shoulders; these are usually coppery to gold in color, and do not fully fuse into the dorsolateral stripes. More northern individuals generally exhibit fairly subdued dorsal coloration, but individuals from Cannell Creek can be boldly marked and have reddish as well as metallic coloration. Habitat and distribution. Batrachoseps bramei is known only from the Upper Kern River Canyon, and along the west side of the current Lake Isabella; the southern limit of its distribution is near the original junction of the main and South forks of the Kern River ( Fig. 1 ). The southernmost samples are from Wofford Heights on the west side of the river and ca. 2 km S of the Cannell Creek drainage on the east side of the river. The range extends north at least as far as 1 km N of the confluence of South Falls Creek with the Kern River. Thus, known populations range for about 30 km from south to north. Areas farther north, which are accessible only by trail, have not been thoroughly surveyed; it is likely that the range extends farther north in the Upper Kern River Canyon. B. bramei occurs within an elevational range of 860–1280 m , one of the most restricted among all species of Batrachoseps . B. bramei has not been found in sympatry with any other species of Batrachoseps . It closely approaches B. simatus in the Lower Kern River Canyon ( 13 km between Wofford Heights B. bramei and Erskine Creek B. simatus ; 20 km between Cannell Trail B. bramei and Erskine Creek B. simatus ); however, these two species are separated by a major drainage (either the main or South Fork Kern River) as well as by xeric, inhospitable terrain around the confluence of the South Fork and Upper Kern River at Lake Isabella. B. bramei also closely approaches B. robustus , which has been collected within 7 km of the river, but at much higher elevation ( 2214 m ), and B. altasierrae sp. nov. (see below). The range of B. bramei on the east side of the Kern River lies entirely within a prominent uplifted ridge of metamorphic rocks paralleling the river. Local populations of salamanders are associated with north-facing slopes and talus. A chaparral plant community consisting of species of the genera Ceanothus, Arctostaphylos, Ribes and Chrysothamnus , as well as Pinus sabiniana and occasionally Quercus chrysolepis , characterizes this area. Most individuals have been found beneath rocks, often on or at the base of talus slopes ( Fig. 6 ). However, specimens have been found in a variety of other habitats and under a variety of cover objects, including under a log in an open sandy flood plain, under logs and rocks in grasslands, in gravel on the river bank, and in leaf litter in protected groves ( Fig. 6 ). Individuals have been observed active at night during winter and early spring and have been collected from beneath surface cover objects under snow. Salamanders have been found under surface cover at body temperatures (inferred from substrate temperatures) of 2.2–16.4°C (mean = 8.4°C, N = 101). Etymology. Named in honor of Arden H. Brame, Jr., who, along with Keith Murray, was the first to recognize the distinctiveness of Batrachoseps in the Kern River Canyon. The species name is formed as a noun in the genitive. FIGURE 6. Habitats occupied by B. bramei in the Kern River Canyon. A. Type locality, Packsaddle Canyon, 1135 m elev., Tulare Co., California (photo taken 5 March 2011). On the east side of the Kern River, salamanders are often associated with metamorphic rock in seepage areas as shown here. B–D. On the west side of the Kern River, B. bramei has been found in a diversity of habitats including the following: B. under isolated cover objects in oak grassland S of Kernville, Kern Co., California (photo taken 21 March 2008); C. in pine litter along Tobias Creek, Tulare Co., California (photo taken 22 March 2007) and D. under rocks and in leaf litter N of South Falls Creek, Tulare Co., California (photo taken 28 January 2010; numerous individuals were found on this date). Refer to the web version of this article for color figure. Comments. In their classic work on Batrachoseps , Brame and Murray (1968) referred animals from the Upper Kern River Canyon to B. simatus , but noted that they were morphologically different. Stebbins (1985 , 2003 ) followed this taxonomy. Jockusch and Wake (2002) treated populations from the Upper Kern River Canyon, all included here in B. bramei , as undescribed lineages based on a phylogeny inferred from mitochondrial DNA sequence data, but the high genetic diversity within the region led them to raise questions about whether more than one species might be present. Jennings (2004) treated populations from the Upper Kern River Canyon as an undescribed species and provided a vernacular name “Fairview slender salamander.” Bartlett and Bartlett (2009) refer to the species as awaiting formal description but provide a short species account, a distribution map, and a color photograph and refer to it as the “Fairview Slender Salamander.” Until 2004, it was believed that Batrachoseps from the canyon proper occurred only on the eastern and southern sides of the river. After specimens were found in the Tillie Creek drainage on the northwest side of the river, exploration intensified on that side, and specimens have now been found at almost all sites north of Tillie Creek that we have sampled with moderate effort (>4 person-hours of searching under good conditions). Conservation. The range of B. bramei lies entirely within plant communities that naturally experience periodic fire. The use of heavy equipment for fire suppression has the potential to negatively impact salamander habitat. Road maintenance of Mountain Highway 99 (Kernville–Johnsondale) should take into account the intimate proximity of some populations to road-edge habitat. Most known populations occur on public lands administered by Sequoia National Forest. Although B. simatus has become difficult to find and is listed as a Threatened Species by the State of California, B. bramei appears to be more abundant and can be found consistently throughout its range.