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 altasierrae new species Suggested common name: Greenhorn Mountains Slender Salamander Figure 7 A–C Batrachoseps attenuatus (part) Grinnell and Camp 1917 :137 Batrachoseps attenuatus attenuatus (part) Dunn 1926 :232 Batrachoseps relictus (part) Brame and Murray 1968 :5 Batrachoseps pacificus relictus (part) Yanev 1980 :535 Batrachoseps relictus (part) Jockusch, Wake and Yanev 1998 :13 Holotype . Museum of Vertebrate Zoology ( MVZ ) 59909, an adult male from 1.5 mi [ 2.4 km ] SE Alta Sierra [Greenhorn Mountains], Kern Co., California, USA ( 35.732°N , 118.538°W ), collected on 26 June 1952 by Keith Murray. Paratypes . MVZ 190953 and MVZ 190955 , both from Hwy. 155, 0.85 km N (by road) Greenhorn Summit, Kern Co., California, USA ( 35.744°N , 118.557°W ), collected 28 May 1984 by Robert W. Hansen; MVZ 190961 – 190963 and MVZ 190965 – 190967 , all from Hwy. 155, 1 km ESE (by road) Greenhorn Summit, Kern Co., California, USA ( 35.735°N , 118.554°W ), collected 24 June 1984 by Robert W. Hansen and D. C. Holland ; MVZ 190976 – 190979 from Tiger Flat Rd. (= U.S. Forest Service Rd. 23S16), 0.7 km N (by road) junction Hwy. 155 at Greenhorn Summit, Kern Co., California, USA ( 35.744°N , 118.554°W ), collected 24 June 1984 by Robert W. Hansen and D. C. Holland ; MVZ 190983 – 190985 from Tiger Flat Rd. (= U.S. Forest Service Rd. 23S16), 0.85 km N (by road) junction Hwy. 155 at Greenhorn Summit, Kern Co., California, USA ( 35.745°N , 118.553°W ), collected 24 June 1984 by Robert W. Hansen and D. C. Holland . Referred specimens. Paratypes of Batrachoseps relictus : Los Angeles County Museum ( LACM ) 33082– 33090 and MVZ 184906–184908 from 1.2 mi [ 1.9 km ] S White River Camp Grounds, Tulare Co., California, USA ( 35.840N , 118.649°W ), collected 31 March 1957 by A. H. Brame, Jr. ( MVZ 184906–8 are described as “3 cleared & stained specimens in D. B. Wake collection” by Brame and Murray (1968)) ; LACM 33091–33093 from 1 mi [ 1.6 km ] above O’Quinn Meadow, Tulare Co., California, USA ( 35.863°N , 118.628°W ), collected 31 March 1957 by L. Hughes and A. H. Brame, Jr.; LACM 33080–33081 from White River Camp Grounds (Lower Camp), Tulare Co., California, USA ( 35.845°N , 118.636°W ), collected 31 March 1957 by A. H. Brame, Jr. Additional referred specimens: MVZ 156360–156365 from Quaking Aspen Meadows along Hwy. 190, South Fork of Middle Fork Tule River, Tulare Co., California, USA ( 36.118°N , 118.544°W ); MVZ 156366–156392 from the upper reaches of Spear Creek along U.S. Forest Service Rd. 24S06, 6.9 km SE junction of 23S05 and 3.2 km NE Portuguese Pass, Tulare Co., California, USA ( 35.821°N , 118.583°W ); MVZ 156393–156399 from White River drainage, at Sugarloaf Peak, U.S. Forest Service Rd. 23S05, 0.6 km N junction U.S. Forest Service Rd. 24S06, Tulare Co., California, USA ( 35.843°N , 118.614°W ), all collected 29 July 1975 by Kay P. Yanev and Samuel S. Sweet; MVZ 224835 from road to Sugarloaf Village, 1.0 km SE Sugarloaf Village, Tulare Co., California, USA ( 35.820°N , 118.641°W ), collected 26 March 1994 by Elizabeth L. Jockusch, David B. Wake and others; MVZ 158244 and MVZ 158226– 158228 from 9.5 km E Cherry Hill Road on Sherman Pass Road, Tulare Co., California, USA ( 35.983°N , 118.381°W ), collected 11 July 1980 and 28 July 1979 , respectively, by Robert W. Hansen; MVZ 224810 from Hwy. 155, 9.0 km NW Lake Isabella and ca. 2.2 km SE Alta Sierra, Tulare Co., California, USA ( 35.724°N , 118.527°W ), collected 27 March 1994 by Elizabeth L. Jockusch, David B. Wake and others. Diagnosis. A small, relatively slender species (SL of 8 adult males 38.0 mm ± 2.4 mm ; of 8 adult females 40.1 mm ± 3.5 mm ) distinguished from other species of Batrachoseps in the southern Sierra Nevada and vicinity as follows: from B. relictus by a relatively longer trunk, a relatively narrower head, shorter limbs, and smaller feet, and by females having many fewer maxillary teeth; from B. simatus by its smaller adult body size with a relatively narrower head and chest and fewer trunk vertebrae (mode 18–19 versus 20–21 in B. simatus ); from B. bramei by a relatively shorter and narrower head, longer trunk, shorter limbs, narrower feet and longer tail, and smaller number of maxillary and vomerine teeth; from B. gregarius by its more robust morphology including a relatively longer and broader head, shorter trunk, longer limbs, and larger hands and feet; from B. stebbinsi by its less robust morphology and much smaller size; from B. campi and B. robustus by its less robust morphology, much smaller size, different color pattern and unpaired premaxillary bone. Distinguished from its close relative B. kawia by having fewer maxillary teeth; from B. regius Jockusch, Wake and Yanev 1998 by having a relatively longer trunk and tail, shorter head, shorter limbs, smaller feet and fewer maxillary teeth; and from B. diabolicus Jockusch, Wake and Yanev 1998 by having fewer trunk vertebrae, a relatively narrower head, shorter limbs and smaller feet. Description. Batrachoseps altasierrae is a small (adults less than 50 mm standard length), slender species with a relatively narrow head and short limbs. The facial region is relatively narrow, and the eyes are not generally protuberant enough to be seen in ventral view. Mental hedonic glands are not visible under the chins of males. Grooving patterns of the head, throat, and neck are typical of the genus. Standard length ranges from 8.4–9.5 (mean = 9.0) times head width in males and 8.2–9.9 (mean = 9.3) times head width in females. There are relatively few teeth, especially on the maxilla: 4–5 (mean = 4.8) premaxillary teeth in males, 4–12 (mean = 6.4) in females; 9–27 (mean = 17.4) maxillary teeth in males, 18–28 (mean = 21.9) in females; 6–13 (mean = 10.9) vomerine teeth in males, 9–16 (mean = 11.8) in females. Vomerine teeth are arranged somewhat patchily. Small maxillary teeth are borne in a long row extending about two thirds of the way through the eye in males and to the posterior end of the eye in females. In females, premaxillary teeth are the same size as maxillary teeth; in males, the premaxillary teeth are enlarged. Males and females both have 18–19 trunk vertebrae and 17–18 costal grooves between the limb insertions. The tail is long and fairly cylindrical, tapering at the tip. The tail is 1.3–1.5 (mean = 1.4) times SL in males and 1.1–1.6 (mean = 1.3) times in females in specimens lacking evidence of tail regeneration. There is no basal tail constriction. The postiliac gland is present. The limbs are relatively short in length, and limb interval ranges from 7–9.5 (mean = 8.3) in males and 7.5–9.5 (mean = 8.5) in females. SL ranges from 6.2–7.5 (mean = 6.8) times hind limb length in males and 6.3–7.8 (mean = 7.1) times in females. The hands and feet are relatively narrow; foot width ranges from 1.4–1.7 mm (mean 1.6 mm ) in males and 1.4–2.0 mm (mean 1.7 mm ) in females. The digits are short, well formed and discrete with expanded tips that bear subterminal pads. Webbing is insignificant. Fingers and toes in order of decreasing length are 3-2-4-1. Measurements of the holotype (in millimeters). Maximum head width 4.9; snout to gular fold (head length) 7.4; head depth at posterior angle of jaw 2.7; eyelid length 2.2; eyelid width 1.2; anterior rim of orbit to snout 1.4; horizontal orbital diameter 1.8; interorbital distance 1.9; snout to forelimb 9.3; distance separating external nares 1.6; snout projection beyond mandible 0.5; snout to posterior angle of vent (SL) 42.5; snout to anterior angle of vent 36.9; axilla to groin length 25.6; tail tip broken after 33.5; tail width at base 3.3; tail depth at base 2.7; forelimb length 6.3; hind limb length 6.8; limb interval 9; width of right hand 1.2; width of right foot 1.6; foot length 2.1; length of third toe 0.9; body width behind forelimbs 2.9. There are 4 premaxillary, 27 maxillary, and 13 vomerine teeth; vomerine teeth are arranged somewhat patchily. There are 17 costal grooves between the limb insertions. Coloration of the holotype (in alcohol). The ground color is dark blackish brown dorsally and laterally (and in the limbs), and fades to lighter brown ventrally. A prominent dorsal stripe ranging in color from dark brown to reddish brown is present and is well demarcated on its lateral borders. Habitat and distribution. This species is restricted to higher elevations in the southern Sierra Nevada. The elevational range is from 900–2440 m . Populations extend from the higher elevations on the northern side of the Lower Kern River Canyon to the Tule River drainage and upper elevations of the Little Kern River drainage in Kern and Tulare counties, California, USA ( Fig. 1 ). Two populations, separated by just over 1 km , are known from the western margin of the Kern Plateau, Tulare Co., California, USA . Most populations are found in coniferous forest containing a mixture of pine, fir and incense cedar ( Fig. 7 F). FIGURE 7. B. altasierrae and B. relictus . A. Holotype of B. altasierrae . B. B. altasierrae from the type locality in life (no voucher). C. Digital x-ray of the skull and forelimbs of an adult female B. altasierrae (MVZ 156394, SL = 39.9 mm) from Sugarloaf Peak, Tulare Co., California. D. Adult B. relictus from Breckenridge Mountain, Kern Co., California in life (no voucher). E. Digital x-ray of the skull and forelimbs of an adult (SL = 45.3 mm) female B. relictus from Breckenridge Mountain (MVZ 267114). F. Type locality of B. altasierrae . G. High elevation site on Breckenridge Mountain, Kern Co., California at which specimens referred here to B. relictus were discovered. Nearly all individuals at this locality have been found within the seep shown in the foreground. Habitat photos taken on 28 May 2011. Refer to the web version of this article for color figure. B. altasierrae has not been found in sympatry with any other species of Batrachoseps . It closely approaches B. gregarius at lower elevations on the western edge of its range. B. gregarius is found within 5 km of B. altasierrae along the Middle and North Forks of the Tule River, where B. altasierrae occurs as low as 900 m . In the Greenhorn Mountains, B. gregarius is known from as high as 1460 m (MVZ 266680–266683; 35.745°N , 118.598°W ) and B. altasierrae from as low as 1460 m (California Academy of Sciences (CAS) 224163, identified by morphology; 36.176°N , 118.692°W ) in the vicinity of Cedar Creek; these populations are separated by less than 1.5 km . On the eastern edge of its range, B. altasierrae closely approaches B. bramei , but the two species appear to be separated by elevation, although the highest-elevation samples of B. bramei are from less than 200 m below the lowest-elevation samples of B. altasierrae in the Greenhorn Mountains. The ranges of these species are separated by less than 10 km between Alta Sierra and Wofford Heights. They may also approach each other along the Upper Kern River Canyon. B. altasierrae on Sugarloaf Peak, Tulare Co., California occurs less than 10 km away from B. bramei along Tobias Creek, Tulare Co., California. B. altasierrae is known from Peppermint Creek, Tulare Co., California; this locality is about 2 km from the Kern River. The nearest known B. bramei is about 10 km south; however, the range of B. bramei likely extends north from there along the Kern River. On the Kern Plateau, east of the Kern River, B. altasierrae has been found 1.6 km from the nearest population of B. robustus in habitat typical of both species ( Wake et al. 2002) and less than 10 km from the nearest B. bramei . At higher elevations to the north of the Tule River drainage, B. altasierrae is replaced by its sister species, B. kawia . To date, all robust specimens (that is, not B. gregarius ) from the South Fork of the Kaweah River identified with molecular data belong to B. kawia , whereas robust specimens from the Tule River drainage carry mitochondrial DNA from B. altasierrae . The northernmost specimen of B. altasierrae is from Mountain Home State Forest, Tulare Co., California, USA (CAS 214814; 36.269°N , 118.668°W ), which is 12 km southeast of the southernmost B. kawia from entrance to Soldiers Cave near South Fork entrance Sequoia National Park, Tulare Co., California, USA (MVZ 237285; 36.345°N , 118.7568°W ). Very few specimens are available from the higher elevations separating these drainages. Molecular sequence data show that some populations along the North Fork of the Middle Fork of the Tule River have genes from both B. altasierrae and B. kawia , but the contact zone appears to be narrow (Jockusch et al. unpublished). Etymology. Named for the mountain hamlet of Alta Sierra, located at the summit of the Greenhorn Mountains, an area where this species is particularly common. The species name is formed as a noun in the genitive. Comments. Jockusch et al. (1998) included a rediagnosis of B. relictus based on specimens from both the Lower Kern River Canyon and the Greenhorn Mountains. We use their series from the Greenhorn Mountains as the paratypes for B. altasierrae . All molecular data identified in previous publications as coming from B. pacificus relictus ( Yanev 1978 , 1980 ) or B. relictus ( Jockusch 1996 ; Jockusch et al. 1998 ; Jockusch & Wake 2002 ) are from B. altasierrae or from more northern members of its species group. Thus, the molecular diagnoses provided by Jockusch et al. (1998) to distinguish B. relictus from other species all in fact apply to B. altasierrae rather than to B. relictus . Molecular differentiation within B. altasierrae is limited. Yanev (1978) included six populations of B. altasierrae , ranging from the vicinity of the type locality in the Greenhorn Mountains to Quaking Aspen Meadow, on the South Fork of the Middle Fork of the Tule River near the northern end of the range, in her allozyme study of the genus. These populations were separated by a maximum Nei’s (1972) genetic distance (D) of 0.075. Mitochondrial DNA ( cob ) data also show a low level of variation ( Jockusch & Wake 2002 ). Conservation. By virtue of their previous inclusion in B. relictus , populations of B. altasierrae have been listed as a Species of Special Concern by the State of California and Sensitive Species by the U.S. Forest Service. Our impression is that populations of B. altasierrae are healthy, both in the Greenhorn Mountains and within the Tule River drainage; individuals have been found in large numbers when surface conditions were appropriate. For example, about 60 individuals were seen along a single stream in the vicinity of Sugarloaf Village, Greenhorn Mountains, Tulare Co., California in a few hours of searching in August 1995 . B. altasierrae was also abundant in the Tule River drainage, Tulare Co., California in April 2008 : individuals were found at numerous sites, and at Moorehouse Creek, along Hwy. 190 ( 36.153°N , 118.657°W ), 10 individuals were found in an area of a few square meters of moist pine needle litter in less than 10 min.