Otospermophilus beecheyi ( Richardson, 1829 )

Smith, Jennifer E., Long, Douglas J., Russell, Imani D., Newcomb, Kate Lee & Muñoz, Valeska D., 2016, Otospermophilus beecheyi (Rodentia: Sciuridae), Mammalian Species 48 (939), pp. 91-108 : 91-96

Otospermophilus beecheyi ( Richardson, 1829)

California Ground Squirrel

Arctomys (Spermophilus)beecheyi Richardson, 1829:170 , plate XII. Type locality “neighbourhood of San Francisco and Monterey, in California [ USA];” restricted to Monterey, Monterey Co., California, United States by Grinnell (1933:120).

Spermophilus beecheyi: Cuvier, 1831:331 . Name combination.

Spermophilus grammurus atricapillus Bryant, 1889:26 . Type locality “Comondu, lower California [Baja California Sur, México].”

Spermophilus beecheyi fisheri Merriam, 1893:133 . Type locality “Kern Valley, California (25 km above Kernville).”

Citellus nesioticus Elliot, 1904:263 . Type locality “Santa Catalina Island, [near Avalon] California, [ USA].”

Otospermophilus beecheyi: Mearns, 1907:324 . First use of current name combination.

Citellus beecheyi parvulus Howell, 1931:160 . Type locality “Shepherd canyon, Argus Mountains, California [ USA].”

Citellus beecheyi rupinarum Huey, 1931:17 . Type locality: “Cataviña, lower California [ México], lat. 29° 54 ′ north, 114° 57 ′ west.”

Citellus beecheyi nudipes Huey, 1931:18 . Type locality “Laguna Hanson, Sierra Juàrez, lower California [ México], altitude 5,200 feet. Lat. 31° 58 ′ north, long, 115° 53 ′ west.”

Citellus beecheyi sierrae Howell, 1938:153 . Type locality “Emerald Bay, Lake Tahoe, El Dorado Co., California [ USA].”

CONTEXT AND CONTENT. Order Rodentia , suborder Sciuromorpha , family Sciuridae , tribe Marmotini ( Howell 1938; Hall 1981; Helgen et al. 2009). Eight subspecies of Otospermophilus beecheyi were recognized by Howell (1938), Hall (1981), Thorington and Hoffmann (2005), and Helgen et al. (2009). However, recent genetic studies support elevation of O. b. douglasii to a full species as O. douglasii and inclusion of O. atricapillus as a subspecies of O. beecheyi (ÁlvarezCastañeda and Cortés-Calva 2011; Phuong et al. 2014). Thus, the 3 species of Otospermophilus are O. beecheyi ( Richardson, 1829) , O. douglasii ( Richardson, 1829) , and O. variegatus ( Erxleben, 1777) . To reflect this, we have made every effort to exclude information on O. douglasii (formerly O. b. douglasii ) from this account. Our revised distribution for O. beecheyi follows the traditional subspecific distribution of O. beecheyi from previous workers, with the Sacramento River assumed to be the biogeographic barrier between O. beecheyi and O. douglasii ( Grinnell and Dixon 1918; Howell 1938; Hall 1981). However, the taxonomic delineation of Otospermophilus living in southeastern Yolo and Solano counties, along the northwestern margin of Sacramento–San Joaquin Delta, remains undecided ( Phuong et al. 2014). Given that current uncertainty, we have included information about those squirrels but have noted the county of origin of those data. For brevity, we also excluded information about O. b. atricapillus (formerly O. atricapillus ) because information about its distribution has been previously summarized (Álvarez-Castañeda et al. 1996). We follow this revised taxonomy of O. beecheyi and recognize the following subspecies:

O. b. atricapillus ( Bryant, 1889:26) . See above.

O. b. beecheyi ( Richardson, 1829:170) . See above.

O. b. fisheri ( Merriam, 1893:133). See above.

O. b. nesioticus ( Elliot, 1904:263) . See above.

O. b. nudipes ( Huey, 1931:18). See above.

O. b. parvulus ( Howell, 1931:160). See above.

O. b. rupinarum ( Huey, 1931:17). See above.

O. b. sierrae ( Howell, 1938:153). See above.

NOMENCLATURAL NOTES. Formerly placed in Spermophilus , as S. beecheyi, Helgen et al. (2009) reclassified this species as O. beecheyi in the genus Otospermophilus . Taxonomy follows Helgen et al. (2009). The type specimen was collected by Alexander Collie, ship surgeon and naturalist aboard the H.M.S. Blossom, captained by Frederick William Beechey, whom O. beecheyi was named to honor ( Grinnell 1933; Linsdale 1946).

Otospermophilus beecheyi belongs to the genus Otospermophilus , a name derived from Greek and attributed to the animal’s relatively large ears and its dietary preference for eating seeds. Specifically, “ Otos ” means ear, “ spermatos ” means seed, and “ phileo ” means love ( Jaegar 1955). Otospermophilus is a sister lineage of Callospermophilus ( Helgen et al. 2009) . Members of both genera have crescent markers over the shoulders and relatively large ears for their body sizes ( Helgen et al. 2009).

DIAGNOSIS

The pelage of Otospermophilus beecheyi is laterally and dorsally grayish brown speckled with white spots ( Fig. 1 ). Its distinguishing traits include a yellowish white to light brown venter, a bushy tail, and white rings around the eyes. O. beecheyi is distinct from other ground squirrels in California because of its bushy tail edged with white fur ( Eder and Ross 2005).

Multiple characteristics distinguish O. beecheyi from its congeners (reviewed by Thorington et al. 2012). O. beecheyi differs from O. variegatus , the rock squirrel, in that O. variegatus has a dark grayish dorsum mixed with cinnamon buff. The dorsum of O. variegatus may also be light brown to bone brown to dark blackish brown; its head and shoulders are often black. The eye ring of O. variegatus is sometimes white like that of O. beecheyi , but O. variegatus has a buff or tawny dorsum and a grayish white to cinnamon buff venter ( Thorington et al. 2012). O. beecheyi and O. douglasii possess similar color variation, but the medial stripe of O. douglasii is darker ( Allen 1974).

O. b. beecheyi is less pale and has less silver-gray fur on the sides of the neck and shoulders than O. b. fisheri ( Thorington et al. 2012). O. b. beecheyi is less dark and has more yellowish brown on the venter than Otospermophilus b. nesioticus ( von Bloeker 1967) . O. b. beecheyi may be distinguished from O. b. nesioticus , because O. b. beecheyi lacks any black on the top of its head and ears as well as the mixed black and tawny ochraceous patch that is typical between the shoulders of O. b. nesioticus . O. b. beecheyi is generally darker than O. b. rupinarum and lacks the silver-white mantle found in O. b. nudipes. O. b. beecheyi lacks the blackish- to pinkish-buff dorsal and lateral color typical of O. b. atricapillus (Álvarez-Castañeda and Cortés-Calva 2011) . O. b. beecheyi is generally paler overall than O. b. parvulus (Álvarez-Castañeda et al. 1996). O. b. beecheyi closely resembles O. b. sierra in its appearance, but O. b. beecheyi is more buffy, has less gray on sides of the head, and has a darker venter than O. b. sierra ( Grinnell and Dixon 1918; ÁlvarezCastañeda and Cortés-Calva 2011).

GENERAL CHARACTERS

Otospermophilus beecheyi is widely identified in California by a crescent shape of light brown or peppered fur beginning at the back of the neck and draping down over its shoulders ( Eder and Ross 2005). This grayish white collar is usually present on the back, the neck, and the sides. Although mainly brown with whitepeppered fur on its back, albinistic, melanistic, and xanthic forms have been reported ( Grinnell and Dixon 1918; Ryckman and Lindt 1953). The pelage coloration of O. beecheyi varies with season and land-use type across its range ( Jachowski and Hubbart 2012). Specifically, O. beecheyi on unmanaged grasslands has lighter pelage in the autumn and darker pelage in the winter than those on agricultural and pasture lands ( Jachowski and Hubbart 2012). These site-specific differences apparently increase the efficiency in thermoregulation and reduce the predation risk for squirrels.

Otospermophilus beecheyi varies in body size as a function of temporal, spatial, and latitudinal factors (reviewed by Thorington et al. 2012). These patterns are generally consistent with the predictions of Bergmann’s cline, with the smallest animals occurring in the southern part of the range in xeric environments with reduced precipitation and resource availability ( Blois et al. 2008). For example, Blois et al. (2008) found that adult body size of O. beecheyi varies geographically and climatically but was generally largest in wet and cold (northern) regions. Interestingly, measures of skull length and maxillary toothrow length indicate that body sizes of O. beecheyi at low elevations in the Sierra Nevada Mountains were stable over the past century ( Eastman et al. 2012). Specimens collected from 2000 to 2008 were not significantly larger than those collected from 1902 to 1950 ( Eastman et al. 2012).

Mass of adult O. beecheyi typically ranges from 280 to 738 g, height from 145 to 225 mm, body length from 330 to 510 mm, and tail length from 127 to 229 mm ( Eder and Ross 2005). Fat accumulation accounts for one-third of body mass during the growing seasons (summer and autumn), giving rise to the heaviest annual body mass during this period ( Tomich 1962). As such, masses vary seasonally and across ontogeny ( Holekamp and Nunes 1989; for details on mass variation see “Ontogeny” section). Despite size variation across its range, adult males are always larger than adult females in body and cranial morphometrics ( Howell 1938). Specifically, body dimensions (mm) for adult males (n = 10) and females (n = 10), respectively, were: total length 434 (410–460), 401 (370–442); tail length 177 (156–190), 158 (137–180); hind foot length 59 (57–61), 56 (53–59); and ear length from notch 19.9 (18–21), 20.7 (19–22— Howell 1938). Skull morphology of O. beecheyi ( Fig. 2 ) is nearly identical to its congener O. variegatus ( Hall 1926; Oaks et al. 1987). Cranial dimensions (mm) for adult males (n = 20) and females (n = 20), respectively, were: greatest skull length 59.4 (57–62.4), 57.1 (53.9–60.4); palatilar length 28.8 (27–30.5), 27.5 (26–30); zygomatic breadth 38.3 (36.3–40.5), 36 (33.6–38.6); cranial breadth 24.5 (23.4–25.9), 23.6 (22.7–25.2); interorbital breadth 14.7 (13.2–15.8), 13.8 (12.9–15.4); postorbital constriction 15.6 (14.8–16.9), 15.6 (13.7–16.7); length of nasals 22.1 (20–24), 21 (19.7–22.4); maxillary toothrow 12 (11.2–12.9), 11.9 (10.6–12.7— Howell 1938).

DISTRIBUTION

The 8 recognized subspecies of Otospermophilus beecheyi are distributed from north-central California and west-central Nevada ( United States) to Baja California Norte ( México — Hall 1981; modified by Álvarez-Castañeda and Cortés-Calva 2011 and Phuong et al. 2014; Fig. 3 ). In the state of California, O. beecheyi is distributed from the intertidal zone along the coast ( Roest 1993; Carlton and Hodder 2003) and vertically to at least 3,000 –3,200 m elevation in the Sierra Nevada Range (e.g., Mt. Whitney, Little Cottonwood Creek) and in Riverside County at Mt. San Jacinto ( Grinnell and Dixon 1918).

Otospermophilus b. fisheri is distributed throughout the Central Valley of California and into northeastern California and west-central Nevada; O. b. sierra lives throughout the northern Sierra Nevada range; O. b. parvulus extends from the southern Sierra Nevada Range into the Panamint, Argus, San Bernardino, and Peninsular ranges of south-central California; O. b. beecheyi occurs from the coast east to the western edge of the Central Valley, and south along the Coast Ranges into southern California; O. b. nudipes is distributed from southernmost coastal California into the coast ranges of Baja California Norte; O. b. rupinarum occurs in a relatively restricted region of the desert of Baja California Norte desert adjacent to the southern end of the range of O. b. nudipes ( Hall 1946, 1981). O. b. nesioticus is endemic to the Santa Catalina Island, located off of the shore of southern California ( Hall 1946, 1981).

There are no known successful introductions of O. beecheyi outside of its native range; 2 individuals were released in Dunedin, New Zealand in 1906 but their introduction ultimately failed when they did not reproduce and died out 3 years later ( Thomson 1922).

FOSSIL RECORD

Thorington et al. (2012) proposed 2 hypotheses concerning the possible ancestors of Otospermophilus : 1) Miospermophilus (late Oligocene to middle Miocene, about 24–12 million years ago) and 2) Spermophilus (middle Miocene, 16 million years ago in North America). It has been suggested by Black (1963) that O. beecheyi likely arose from this early Miocene Miospermophilus ancestor and Savage and Russell (1983) reported that numerous Otospermophilus occurred as early as the beginning of the Barstovian late Miocene. More precisely, Savage (1949) documented the occurrence of O. bensoni , a close relative of O. beecheyi , from the early Pleistocene (Irvingtonian age) Irvington Quarry located near Mission San Jose, California. Fossil records of O. beecheyi are known from several late Pleistocene (Rancholabrean age) sites throughout California ( Miller 1978; Kurten and Anderson 1980), including the La Brea tar pits where active tar seeps still trap ground squirrels ( Stock 1972). Pajak et al. (1996) documented O. beecheyi fossils in the Elsinore Fault Zone in Riverside County, California from the lower to middle Pleistocene (Irvingtonian age). Fossils of O. beecheyi were cataloged at numerous late Pleistocene (Rancholabrean age) throughout southwestern California ( Jefferson 1991). In most of these localities, early forms of O. beecheyi were historically associated with large grazing mammals, and extant O. beecheyi continues to live in close association with large grazing mammals, including domesticated cattle (e.g., Howard and Bentley 1959; Fehmi et al. 2005).

ONTOGENY AND REPRODUCTION

Ontogeny. — Otospermophilus beecheyi observed above ground may be categorized into 3 ontogenetic stages: newly emerged young (45–60 days of age), juveniles (> 60–364 days), and adults (> 364 days; young adults of ages 365–729 days are referred to as “yearlings”— Hanson and Coss 2001). Over 800 O. beecheyi from Yolo and Solano counties were examined by Tomich (1962) to document the ontogeny of O. beecheyi . Young are altricial, born hairless with their eyes closed; their skin is red at birth and gradually turns pink as they age ( Tomich 1962). Vibrissae are 2 mm long at 3 days; by 3–7 days, young typically only weigh 9.3 g (range: 7.7–12.6 g — Tomich 1962). By day 13, the head has short silky fur. By day 27, young have their full pelage. By 21–28 days, young are usually able to crawl and have fully erupted incisors by 28 days; by around 1 month, the eyelids start to open ( Tomich 1962). The 1st molt provides young with yellow, fluffy fur and the 2nd molt occurs prior to emergence from the natal burrow and changes fur to a shiny brown with white patches on the shoulders ( Grinnell and Dixon 1918).

At around 6–7 weeks, young are weaned and start to emerge from their burrows and spend time above ground, a phenomenon that may occur as early as in late April, but the precise timing strongly depends upon the specific location of the population ( Tomich 1962). For example, intensive study of O. beecheyi in Yolo County, California indicated that most young emerged in May, but that a small proportion of young emerged from burrows as late as June and July ( Owings and Coss 2007). Similarly, young consistently emerged in May for 3 different years during a study on the University of California Santa Cruz campus ( Holekamp et al. 1988). Regardless of the precise timing of independence, the fur pattern and color of newly emerged young resemble that of adults ( Eder and Ross 2005). Juveniles molt at least twice ( Grinnell and Dixon 1918).

Adult members of most described populations of O. beecheyi typically estivate or hibernate at some point in the year; this results in above-ground absences by adults for many months of each year ( Fitch 1948; Tomich 1962; Dobson 1979; Holekamp et al. 1988; Holekamp and Nunes 1989). In contrast, there are no documented accounts of young of the year hibernating or estivating ( Grinnell and Dixon 1918; Holekamp and Nunes 1989). Instead, they spend most of their 1st year foraging, maturing, and building up body fat for the mating season ( Tomich 1962). O. beecheyi is capable of breeding by the end of its 1st year ( Grinnell and Dixon 1918; Tomich 1962). The typical lifespan is up to 4 years in the wild and up to 9 years in captivity ( Tomich 1962; Ranck et al. 2008).

The precise timing of seasonal changes in surface activity by adult O. beecheyi varies with climate. In cold areas, O. beecheyi may hibernate for several months, whereas squirrels living in warm areas often estivate to avoid excessive heat in the summer ( Grinnell and Dixon 1918). When adults hibernate during unfavorably cold weather, they may do so for up to 6 months at high elevations ( Grinnell and Dixon 1918; Hall 1946). For example, in areas where adults hibernate, males are typically dormant by late July to early August (after the breeding season), but adult females remain active until late September, presumably to put on fat stores for reproduction ( Tomich 1962). At warmer elevations, such as the Central Valley or Mojave Desert, ground squirrels tend to stay in their burrows to escape hot temperatures in the late summer and emerge in mid-winter ( Grinnell and Dixon 1918). On the campus of the University of California at Santa Cruz, O. beecheyi adults disappear from the surface for 3–4 months each year; males estivate from May or June to October or November whereas most females estivate from late July to December or January ( Holekamp et al. 1988).

The mass of young at initial emergence is typically 100– 150 g; young gain weight rapidly in the days following emergence ( Holekamp and Nunes 1989). Juveniles typically reach their adult size after 7–8 months ( Grinnell and Dixon 1918), attaining sex-specific masses resembling those of adults emerging from estivation (males: about 600 g in October or November; females: about 450 g in December or January— Holekamp and Nunes 1989). Annual mass maxima of adults peaked around June before estivation (males: about 1,000 g, females: about 700 g — Holekamp and Nunes 1989).

Reproduction. — Otospermophilus beecheyi likely follows a promiscuous mating system ( Fitch 1948; Boellstorff et al. 1994). Periods of behavioral estrus last only an average ± S.D. of 6.7 ± 3 h ( Boellstorff et al. 1994) or 3–5 h each year ( Holekamp et al. 1988). Despite this short duration, females mate with an average of 6– 7 males during this period ( Boellstorff et al. 1994). Preliminary data are consistent with multiple paternity; polyacrylamide gel electrophoresis confirmed that 8 of 9 litters were fathered by multiple sires ( Boellstorff et al. 1994).

The reproductive season is quite variable geographically and is linked to regional differences in climate ( Thorington et al. 2012). In Yolo and Solano counties where squirrels hibernate, reproduction occurs soon after emergence from the burrow, often starting in February, and lasting only a few weeks ( Tomich 1962). In the San Francisco Bay region, the breeding season often lasts from February through April ( Grinnell and Dixon 1918; Evans and Holdenried 1943). For populations located farther south in California, pregnant females were found throughout the year ( Storer 1930). Additionally, adults living at high elevations in relatively cold climates tend to emerge from hibernation and mate later in the year ( Grinnell and Dixon 1918). Although young are often born during June or July at high elevations, they are born around mid-April in many parts of California ( Grinnell and Dixon 1918). Testicles enlarge during autumn and winter months in preparation for mating and regress by about 10% of maximal mass by July long after the breeding season has ceased ( Tomich 1962).

Overall, observations based on field studies indicate that most females initiate their breeding careers as yearlings ( Evans and Holdenried 1943; Fitch 1948; Tomich 1962; Dobson 1979; Holekamp et al. 1988). After mating, gestation is 25–30 days ( Grinnell and Dixon 1918). Levels of circulating hormones vary with reproductive condition of pregnant and lactating females during the spring breeding season ( Holekamp et al. 1988). Plasma progesterone peaks during pregnancy and then again during lactation. Prolactin peaks during lactation between the 2 peaks in progesterone ( Holekamp et al. 1988).

Adrenal glands of mammals mediate an individual’s physiological response to stressors. Study of these glands allows for an understanding of how each sex copes with the demands of reproduction. For O. beecheyi , adrenals are largest for adult females during pregnancy, but adult males typically have larger adrenal glands than do adult females ( Tomich 1962). In fact, adrenal glands of males in Yolo and Solano counties are largest directly after the mating season, suggesting that males experience more stressors during the mating season than do females ( Tomich 1962).

Most adult females are monestrous, producing only a single litter each year of 4–11 young ( Grinnell and Dixon 1918). Although the average litter size is 5 offspring per reproductive bout ( Tomich 1962), litter sizes may vary seasonally for some populations. For one population, peak litter sizes documented in April averaged 8 young per litter ( Grinnell and Dixon 1918). Female O. beecheyi are capable of giving birth to a 2nd litter if the individuals of the 1st litter fail to survive ( Grinnell and Dixon 1918). Because some females have more than 1 reproductive bout per year, each adult female produces, on average, roughly 6.1 young per year, a value that exceeds the average litter size for a single reproductive bout for the species ( Tomich 1962). If a female does produce a 2nd litter, then this 2nd litter is typically born late in the season ( Grinnell and Dixon 1918). For example, in southern Tulare County, California, 20% of reproductively active females bred a 2nd time within a single breeding season ( Simpson and Lamunyon 1980). In this population, excess embryos were sometimes resorbed in utero, lowering the mean litter sizes birthed by females; older adult females were more likely than younger females to produce a 2nd litter within the same breeding season ( Simpson and Lamunyon 1980).

Figures

Fig. 1.—An adult male Otospermophilus beecheyi from Berkeley Marina, Berkeley, Alameda County, California, United States. Photograph by D. J. Long.

Fig. 2.—Dorsal, ventral, and lateral views of the skull and lateral and dorsal views of the mandible from an adult male Otospermophilus beecheyi (California Academy of Sciences Mammalogy Collections 9003) collected by K.Staeger on 11 July 1940, Calaveras Dam,Alameda Co., California, United States; 59.2 mm total skull length. Greatest skull length is 59.2 mm.

Fig. 3.— Geographic distribution of the 8 subspecies of Otospermophilus beecheyi: 1, O.b. atricapillus; 2, O. b. beecheyi; 3, O. b. fisheri; 4, O. b. nesioticus; 5, O. b. nudipes; 6, O. b. parvulus; 7, O. b. rupinarum; 8, O. b. sierrae (modified from Hall 1981 and Álvarez-Castañeda et al. 1996, and Phuong et al. 2014). The dotted line in the northwest edge of the O. beecheyi range represents an imprecise boundary between O. b. beecheyi and O. douglasii due to genetic uncertainty about the specific geographic division between these 2 species (Phuong et al. 2014). This map should therefore serve as a tentative boundary for O. beecheyi until further genetic data confirm a species division in that region.