Urocitellus parryii ( Richardson, 1825 )

Mclean, Bryan S., 2018, Urocitellus parryii (Rodentia: Sciuridae), Mammalian Species 50 (964), pp. 84-99 : 84-96

Urocitellus parryii ( Richardson, 1825)

Arctic Ground Squirrel

Arctomys parryii Richardson, 1825:316 . No type locality designated, restricted to “Five Hawser Bay, Lyon Inlet, Melville Peninsula, [Hudson Bay, Nunavut,] Canada ” by Preble (1902:46).

Spermophilus parryii: Lesson, 1827:244 . Name combination.

Arctomys parryi var. phaeognatha Richardson, 1829:161 . Type locality “Hudson’s Bay,” Canada. Incorrect subsequent spelling of Arctomys parryii Richardson, 1825 .

Spermophilus leucostictus Brandt, 1844:379 . Type locality “regionibus versus Ochotam et Uth fluvium valde aestimatae.” (= Khabarovsk Region, Okhotsk District, Ohota River), Eastern Siberia, Russia (translated by Pavlinov and Rossolimo 1987).

Spermophilus brunniceps von Kittlitz, 1858:337 . Type locality “ Kamchatka.” Nomen nudum.

A [rctomys]. kennicottii Ross, 1861:434. Type locality “Fort Good Hope, Mackenzie,” Northwest Territories, Canada.

Spermophilus parryi var. parryi: Allen, 1874:292 . Name combination. Incorrect subsequent spelling of Arctomys parryii Richardson, 1825 .

Spermophilus parryi var. kodiacensis Allen, 1874:292 . Type locality originally given as “Island of Kodiac,” Alaska, USA; restricted to “Kodiak Island, Alaska,” USA, based on designation of lectotype by Howell (1938:103). Incorrect subsequent spelling of Arctomys parryii Richardson, 1825 .

Spermophilus empetra: Allen, 1877:839 . Name combination.

[ Spermophilus empetra ] var. empetra: Allen, 1877:839 . Name combination.

[ Spermophilus empetra ] var. kodiacensis: Allen, 1877:839 . Name combination.

Spermophilus osgoodi Merriam, 1900:18 . Type locality “Fort Yukon, Alaska,” USA.

Spermophilus barrowensis Merriam, 1900:19 . Type locality: “Point Barrow, Alaska,” USA.

Spermophilus beringensis Merriam, 1900:20 . Type locality: “Cape Lisbourne (Coal Veins), Alaska,” USA.

Spermophilus empetra plesius Osgood, 1900:29 . Type locality “Bennett City, head of Lake Bennett, British Columbia,” Canada.

Citellus buxtoni Allen, 1903a:139 . Type locality “Gichiga, west coast of Okhotsk sea, [Magadan Oblast,] Siberia,” Russia.

Citellus stejnegeri Allen, 1903a:142 . Type locality “Near Petropaulski, southeastern Kamchatka,” Russia.

Citellus stonei Allen, 1903b:537 . Type locality “Wrangel, Alaska, ” USA; corrected to “ Stevana Flats, near Port Muller, Alaska Peninsula, Alaska,” USA, by Allen (1903b:xvii).

Citellus parryii: Miller and Rehn, 1903:75 . Name combination.

C [itellus]. plesius: Osgood, 1903:25 . Name combination.

Citellus plesius ablusus Osgood, 1903:25 . Type locality “Nushagak, Alaska,” USA.

C [itellus]. barrowensis: Osgood, 1903:25 . Name combination.

C [itellus]. kodiacensis: Osgood, 1903:26. Name combination.

Citellus nebulicola Osgood, 1903:26 . Type locality “Nagai Island, Shumagin Islands, Alaska,” USA.

[ Citellus] osgoodi: Osgood, 1903:27 . Name combination.

[ Citellus parryi ] kadiacensis: Trouessart, 1904:338. Name combination. Incorrect subsequent spelling of Arctomys parryii Richardson, 1825 and Spermophilus parryii var. kodiacensis Allen, 1874 .

[ Citellus parryi] plesius: Trouessart, 1904:338 . Name combination. Incorrect subsequent spelling of Arctomys parryii Richardson, 1825 .

[ Citellus] beringensis: Trouessart, 1904:338 . Name combination.

Citellus (Colobotis) parryi kennicotti: Preble, 1908:162 . Name combination. Incorrect subsequent spelling of Arctomys parryii Richardson, 1825 and A [rctomys]. kennicottii Ross, 1861.

Colobotis buxtoni: Ognev, 1926:93 . Name combination.

Citellus lyratus Hall and Gilmore, 1932:396 . Type locality “Iviktook Lagoon, about 35 miles northwest of Northeast Cape, St. Lawrence Island, Bering Sea, Alaska,” USA.

Citellus eversmanni leucostictus: Chaworth-Musters, 1934:557 . Name combination.

Citellus (Urocitellus) eversmanni stejnegeri: Ognev, 1937:331 . Name combination.

Citellus (Urocitellus) eversmanni janensis Ognev, 1937:332 . Type locality “Mestnost’ Kenûrâh, v verhovâh r. Âny, dolina reki, Verhoânskij okrug.”

Citellus parryii parryii: Howell, 1938:91 . Name combination.

Citellus parryii barrowensis: Howell, 1938:95 . Name combination.

Citellus parryii ablusus: Howell, 1938:98 . Name combination.

Citellus parryii buxtoni: Howell, 1938:100 . Name combination.

Citellus parryii nebulicola: Howell, 1938:100 . Name combination.

Citellus parryii lyratus: Howell, 1938:101 . Name combination.

[ Citellus parryii] osgoodi: Heptner, 1941:25 . Name combination.

[ Citellus parryii] leucostictus: Heptner, 1941:25 . Name combination.

[ Citellus parryii ] steinegeri: Heptner, 1941:26. Name combination. Incorrect subsequent spelling of Citellus stejnegeri Allen, 1903a .

[ Citellus parryii ] janensis: Heptner, 1941:26. Name combination.

Citellus (Urocitellus) undulatus buxtoni: Ognev, 1947:213 . Name combination.

Citellus (Urocitellus) undulatus stejnegeri: Ognev, 1947:214 . Name combination.

Citellus (Urocitellus) undulatus janensis: Ognev, 1947:215 . Name combination.

C [itellus]. undulatus leucostictus: Rausch, 1953:121 . Name combination.

Citellus undulatus parryii: Rausch, 1953:121 . Name combination.

Citellus undulatus barrowensis: Rausch, 1953:122 . Name combination.

Citellus undulatus osgoodi: Rausch, 1953:123 . Name combination.

Citellus undulatus plesius: Rausch, 1953:123 . Name combination.

Citellus undulatus ablusus: Rausch, 1953:123 . Name combination.

Citellus undulatus kodiacensis: Rausch, 1953:124 . Name combination.

Citellus undulatus lyratus: Rausch, 1953:125 . Name combination.

Spermophilus undulatus kennicottii: Bee and Hall, 1956:43 . Name combination.

Spermophilus undulatus parryii: Harper, 1956:17 . Name combination.

Spermophilus undulatus ablusus: Hall and Kelson, 1959:343 . Name combination.

Spermophilus undulatus kodiacensis: Hall and Kelson, 1959:343 . Name combination.

Spermophilus undulatus lyratus: Hall and Kelson, 1959:343 . Name combination.

Spermophilus undulatus nebulicola: Hall and Kelson, 1959:343 . Name combination.

Spermophilus undulatus osgoodi: Hall and Kelson, 1959:343 . Name combination.

Spermophilus undulatus plesius: Hall and Kelson, 1959:343 . Name combination.

Citellus undulatus coriakorum Portenko et al., 1963:96 . Type locality “Kamčatskaâ oblast’, Korâkskij AO, r. Ačajvaâm.” (= Russia, Kamchatka Region, Korâkskij Autonomous District, Ačajvaâm River—translated by Pavlinov and Rossolimo 1987).

Citellus parryi coriacorum: Gromov et al., 1965:187 . Name combination. Incorrect subsequent spelling of Arctomys parryii Richardson, 1825 and Citellus undulatus coriakorum Portenko et al., 1963 .

Citellus parryi tschuktschorum Chernyavsky, 1972:210 . Type locality: “sred. teč. r. Amguèma, Vost. Čukotka.” (= middle reaches of the Amguema River, eastern Chukotka Peninsula, Russia—translated by Baranova and Gromov 2003). Incorrect subsequent spelling of Arctomys parryii Richardson, 1825 .

S [permophilus]. p [arryii]. osgoodi: Nadler et al., 1973:34 . Name combination.

S [permophilus]. p [arryii]. plesius: Nadler et al., 1973:34 . Name combination.

S [permophilus]. p [arryii]. ablusus: Nadler et al., 1973:34. Name combination.

S [permophilus]. p [arryii]. lyratus: Nadler et al., 1973:34 . Name combination.

S [permophilus]. p [arryii]. steinegeri: Nadler et al., 1973:35. Name combination. Incorrect subsequent spelling of Citellus stejnegeri Allen, 1903a .

S [permophilus]. p [arryii]. leucostictus: Nadler et al., 1973:35 . Name combination.

S [permophilus]. p [arryii]. janensis: Nadler et al., 1973:35. Name combination.

Spermophilus parryii kennicotti: Robinson, 1973:1 . Name combination. Incorrect subsequent spelling of A [rctomys]. kennicottii Ross, 1861.

S [permophilus]. p [arryii]. nebulicola: Nadler and Hoffmann, 1977:748 . Name combination.

Urocitellus parryii: Helgen et al., 2009:297 . First use of current name combination.

CONTEXT AND CONTENT. Order Rodentia , suborder Sciuromorpha , family Sciuridae , subfamily Xerinae , tribe Marmotini . The following 10 subspecies and their synonyms are recognized ( Helgen et al. 2009):

U. p. ablusus ( Osgood, 1903:25). See above; stonei (Allen) is a synonym.

U. p. kennicottii ( Ross, 1861:434). See above; barrowensis (Merriam) and beringensis (Merriam) are synonyms.

U. p. kodiacensis ( Allen, 1874:292). See above.

U. p. leucostictus ( Brandt, 1844:379) . See above; buxtoni (Allen) and tschuktschorum (Chernyavsky) are synonyms.

U. p. lyratus (Hall and Gilmore, 1932:396) . See above.

U. p. nebulicola ( Osgood, 1903:26) . See above.

U. p. osgoodi ( Merriam, 1900:18) . See above.

U. p. parryii ( Richardson, 1825:316) . See above; phaeognatha (Richardson) is a synonym.

U. p. plesius ( Osgood, 1900:29) . See above.

U. p. stejnegeri ( Allen, 1903a:142) . See above; brunniceps (von Kittlitz) , coriakorum (Portenko) and janensis (Ognev) are synonyms.

DIAGNOSIS

Urocitellus parryii ( Fig. 1 ) is the northernmost species within the family Sciuridae and the only sciurid with a Holarctic distribution. A quintessential high-latitude mammal and the largest species in the genus Urocitellus , U. parryii is a member of the bigeared species group of Urocitellus , all of which are larger-bodied, more mesic-adapted and have greater latitudinal distributions than their congeners. In pelage, U. parryii is the most intensely and variably colored of its congeners (except possibly U. columbianus, Columbian ground squirrel). The dorsum varies in color from pale buff or grizzled buff to ochre or rich chestnut and is more deeply colored than the unmarked venter, being noticeably flecked with white spots in all color phases. U. parryii has a more colorful head than body, with forehead darker than cheeks; shoulders, forelimbs, and hindlimbs that are unmarked but more colorfully washed than the venter; and a relatively long-haired tail that is grizzled or dark above and buffy, ochre or reddish below.

Urocitellus parryii is easily distinguished from members of the small-eared group of Urocitellus based on its much greater head–body length (> 200mm) and weight (the latter approaching an order of magnitude in some individuals); longer tail (> 60 mm) and hind feet (> 40 mm); and longer, denser, and more colorful pelage. Individuals of most subspecies (except U. p. plesius ) can be distinguished from other Nearctic big-eared Urocitellus (except U. columbianus ) by greater weight (usually> 450 g) and longer head–body length (usually> 340 mm); darker and more colorful pelage with dorsal flecking; and longer, bushier tail. From U. columbianus , it can be distinguished primarily by its more buffy (and less reddish) coloration, but U. parryii also averages slightly larger than U. columbianus in total length (245 versus 233 mm, respectively) and tail length (55 versus 50 mm, respectively). From the Palearctic U. undulatus , long-tailed ground squirrel, with which it was formerly considered conspecific and resembles most closely, U. parryii is distinguished by a more richly colored head, bolder dorsal flecking, and greater color contrast between head and back (Krystufek and Vohralik 2013), as well as a slightly larger average total length (245 mm in U. parryii versus 220 mm in U. undulatus , respectively). U. parryii has a karyotype of 2 n = 34, distinguishing it from all other Urocitellus except for U. elegans (Wyoming ground squirrel) and U. armatus (Uinta ground squirrel). U. parryii is also easily distinguished based on geography, being nowhere sympatric with any congener.

GENERAL CHARACTERS

Urocitellus parryii ( Fig. 1 ) resembles other true ground squirrels in gross external morphology in having a semicylindrical body plan, dorsoventrally compressed cranium, shortened pinnae, relatively short but stout limbs, and relatively elongated manus, pes, and digits with sharp claws. The posture of U. parryii is plantigrade; forelimbs and hindlimbs possess 4 and 5 digits, respectively. Membranous cheek pouches are present. Tail length is typically 35–50% of head–body length. Ranges of external measurements (mm) for mainland subspecies excluding U. p. plesius are as follows: total length, 340–495; tail length, 88–165; hind foot length, 52–68. Ranges of the same measurements (mm) from the more diminutive U. p. plesius are as follows: total length, 300–363; tail length, 85–105; hind foot length, 50–57. Ear length in U. parryii ranges from 10 to 21 mm. Adult weights from 450 to 1,000 g are possible, and average greater in northern than southern populations. Weights exceeding 1 kg have occasionally been reported in U. p. parryii , U. p. kennicottii, U. p. osgoodi , and U. p. leucostictus ( Howell 1938; Batzli and Sobaski 1980; Buck and Barnes 1999a; Krystufek and Vohralik 2013). Sexual dimorphism exists; males average 2–4% greater in cranial dimensions ( Pearson 1981), 4–10% greater in external linear measurements, and occasionally up to 10% greater in body mass than females. However, Mayer (1953) described ear lengths greater in female than in male U. p. kennicottii.

Urocitellus parryii shows significant variation in pelage color across its range, which in several instances is unreflective of phylogeny. Extremes of dorsal hue are the pale buff of U. p. lyratus and some U. p. leucostictus and the dark ochre and rich chestnut of U. p. parryii and U. p. osgoodi , respectively. Amounts of dorsal flecking range from marked to diffuse; variation along this continuum can also be observed within some subspecies. The heels of U. parryii are partially to densely haired. Tail coloration is darkest in U. p. kodiacensis, U. p. parryii , and U. p. osgoodi , being nearly completely black above in some populations of the latter. Howell (1938) and Rausch (1953) gave additional pelage descriptions for most subspecies. Melanism occurs in U. p. osgoodi , U. p. plesius , and U. p. kennicottii (and possibly additional subspecies). Howell (1938) reported that about 20% of U. p. osgoodi specimens examined were melanistic. Guthrie (1967) interpreted this trait as fire melanism and suggested it was maintained by balancing selection due to the high frequency of wildfires in central Alaska.

Howell (1938) detailed the distinguishing craniodental morphological characters of U. parryii . The skull ( Fig. 2 ) is more robust and angular than in other Urocitellus , with a broader and heavier zygomatic arch, heavier postorbital processes, broader nasals, broader and more inflated auditory bullae, and a welldeveloped posterior loph of M3. Greatest length of skull and zygomatic breadth for subspecies (excluding U. p. plesius ) range from 53.2 to 65.8 mm and 33.2 to 44.3 mm, respectively. Ranges of the same measurements in U. p. plesius are 50.7–56.4 mm and 32.3–35.5 mm, respectively. Additional cranial measurements (mm; mean and ranges for 6 males—Howell 1938) for the nominal subspecies U. p. parryii are as follows: cranial breadth (= breadth of braincase), 24.7 (23.5–25.5); palatal length, 31.2 (30.3–32.5); interorbital breadth, 13.4 (12.9–13.8); postorbital breadth, 13.4 (12.7–14.1); length of nasals, 23.6 (21.9–25.1); length of maxillary toothrow, 13.6 (13.2–14.1). Aging can result in cranial modification, including bone thickening, more pronounced postorbital constriction, and increased ossification of incisive foramina ( Pearson 1981).

Robinson and Hoffmann (1975) analyzed cranial morphology of big-eared Urocitellus in a multivariate context; although their study included only 2 subspecies of U. parryii (U. p. kennicottii and U. p. leucostictus ), cluster analyses recovered greater shape differences between those subspecies than among some species pairs of big-eared Urocitellus . Cranial size, pronouncement of temporal ridges, length of nasals, and relative development of the posterior loph of M3 are variable among some subspecies of U. parryii ( Howell 1938) ; a list of other variable mensural characters can be found in Pearson (1981). The skull characters that best distinguish U. p. kennicottii from the Palearctic U. p. leucostictus were given by Robinson (1973). Interspecific variation in cranial morphology of big-eared Urocitellus is strongly allometric and also correlated with latitude (Robinson and Hoffmann 1975). Similarly, intraspecific cranial variation among Nearctic U. parryii is broadly correlated with latitude, as well as with temperature and precipitation ( Pearson 1981); larger forms are found in coolest and driest conditions. No significant cranial variability was found in Siberian U. parryii ( Vorontsov et al. 1984) . Cranial size in male (but not female) U. parryii is negatively correlated with elevation ( Pearson 1981). Cranial size in female (but not male) U. parryii on islands is positively correlated with island area, temperature, and precipitation ( Pearson 1981). U. parryii appears to have experienced rapid rates of evolution in molariform tooth size and shape relative to other marmotine ground squirrels ( Goodwin 2009).

FORM AND FUNCTION

Form. — Urocitellus parryii pelage contains both coarse guard hairs and wooly underhairs. Two annual molts occur, one at spring emergence and another in late summer prior to hibernation. Spring molt is initiated at the nose and forehead, proceeds posteriorly, and evinces definite molt lines; the winter molt proceeds in the opposite direction but without definite molt lines ( Butterworth 1958). The dental formula of U. parryii is i 1/1, c 0/0, p 2/1, m 3/3, total 22. Brain volume has been estimated as 5.23 and 4.15 ml in males and females, respectively; this metric scales with body size but does not appear to be sexually dimorphic ( Iwaniuk 2001).

Like many other hibernating ground squirrels, U. parryii shows circannual rhythms in body mass, lean mass, and fat mass; all parameters increase throughout the active season ( Sheriff et al. 2013). Adult body mass fluctuates up to 35% of maximum mass annually (Morrison and Galster 1975; Batzli and Sobaski 1980; Buck and Barnes 1999a; Sheriff et al. 2013). In males and females, lean mass increases by 16% and 18%, respectively, over the active season ( Sheriff et al. 2013). Percent body fat varies from 22% and 25% at spring emergence to 30% and 41.5% at autumn immergence, respectively (Buck and Barnes 1999a), although some populations display even greater differences ( Sheriff et al. 2013). Rates of mass and fat reserve gain vary significantly with sex and age class (Galster and Morrison 1976; Buck and Barnes 1999a; Sheriff et al. 2013; Wheeler and Hik 2014a) but may be constant across different levels of caloric intake and food macronutrient profiles ( Hatton et al. 2017). U. parryii possesses both white and brown adipose tissue, both of which are increased substantially in preparation for hibernation, via enlargement of individual adipocytes (Boyer and Barnes 1999). Increases in fat mass account for a greater percentage of overall weight gain than do increases in lean mass during this time ( Sheriff et al. 2013).

Mammae of female U. parryii are unhaired during the active season. Testes of males are scrotal during the short breeding season and abdominal the remainder of the year. In U. p. plesius , testes mass fluctuates by up to 90% across the active season, from 4.5-g prebreeding to <0.5 g prior to hibernation ( Boonstra et al. 2011). Sperm production lasts 1–2 weeks and is followed rapidly by involution of testicular elements, then regeneration and preliminary spermatogenesis ( Mitchell 1959). Adrenal glands appear to be the site of androgen production; adrenal mass of U. parryii has been reported as 2 times that of U. columbianus ( Boonstra et al. 2011, 2014). Diameter of the male urethra was reported as 3 mm (Bee and Hall 1956).

Males can undergo dramatic weight loss of up to 21% (12 g /day) during the short breeding period, while other age and reproductive classes exhibit no mass change at this time. Nevertheless, body condition has been documented as worse in females than males during the breeding season, but similar during hibernation (Galster and Morrison 1976). Female overwinter mass loss has been measured as 11–47%, while that of males is minimal (although the latter pattern may be due in part to use of food caches in hibernacula following spring arousal—Buck and Barnes 1999a, 1999b). The rate of mass loss during hibernation appears to be linear (Galster and Morrison 1976); Buck and Barnes (1999b) calculated this rate as 0.7–1.6 g /day in female U. parryii .

Function.— Due to extremes of its life history, Urocitellus parryii displays substantial annual fluctuations in hormonal concentrations, metabolic rate, and other physiological and reproductive parameters. Plasma androgen levels are high in breeding males, being 10–200 times higher than concentrations in some other ground squirrel species ( Boonstra et al. 2011, 2014). Androgen levels are higher in reproductive males versus nonreproductive males and juveniles and higher in males than in females (Buck and Barnes 2003; Boonstra et al. 2011). Androgen concentrations display 2 distinct active season peaks, the first coinciding with female emergence and onset of estrous (concentrations 5–12 ng /ml—Barnes 1996; Boonstra et al. 2001a, 2011; Buck and Barnes 2003) and the second occurring prior to hibernation and being roughly 60% of the spring peak (Buck and Barnes 2003). Boonstra et al. (2011) argued that elevated androgen levels may be required by both sexes to achieve active season muscle growth sufficient for overwinter protein catabolism and glucose production. U. parryii maintains significantly higher androgen levels in muscle than in lymph nodes, which promotes active season muscle development while minimizing negative effects on immune function ( Boonstra et al. 2014).

Free cortisol levels of U. parryii have been reported as 175.9 nM/l, and this parameter, as well as overall cortisol responsiveness, is lower than in some other sciurids (Boonstra and McColl 2000). Breeding U. parryii males have 20% higher free cortisol levels and 3 times lower corticosterone-binding capacity than nonbreeders, juvenile males, and breeding females, presumably due to chronic active season stress ( Boonstra et al. 2001a, 2001b; Hik et al. 2001). Chronic stress is also reflected immunologically; breeding adults have lower hematocrit and lower white blood cell counts relative to nonbreeders ( Boonstra et al. 2001b). Hematocrit has been reported as 39.9%, 46.6%, and 41.8% in breeding, nonbreeding, and juvenile males, respectively ( Boonstra et al. 2001b). White blood cell counts between 0.9 and 1.9 cells per field of view were reported ( Boonstra et al. 2001b). The extreme hormonal and immunological profiles of male U. parryii have been collectively interpreted as reflecting a life history trade-off of long-term survival for reproductive success (Boonstra and McColl 2000; Boonstra et al. 2001b). However, juvenile males also display hormonal signatures of chronic stress, presumably associated with the high stress of dispersal ( Boonstra et al. 2001a, 2001b). U. parryii in lower-quality habitats display relatively lower cortisol levels, corticosteroid binding capacity, hematocrits, and blood glucose levels than those in higher-quality habitats, reflecting the stress of increased predation risk in the former ( Hik et al. 2001).

Body temperatures of U. p. kennicottii during the active season average 38.4–39.3°C ( Chappell 1981; Long et al. 2005), while body temperatures during overwinter bouts of euthermia may be lower than this ( Karpovich et al. 2009). Male active season body temperatures in the wild display diurnal oscillations from 2 to 5°C and are entrained to a 24.0- to 24.2-h periodicity; temperature minima correspond to times spent in burrows on rainy days or at night ( Long et al. 2005; Williams et al. 2012a). At temperatures above 25°C, a captive U. parryii displays thermoregulatory and respiratory distress, and temperatures above 30°C are lethal (Sullivan and Mullen 1954). Mass-specific metabolic rates of both sexes decrease throughout the active season, with averages of 3.68 and 4.74 W /kg reported in male and female U. p. kennicottii, respectively ( Sheriff et al. 2013). However, metabolic rates do not appear to change significantly at ambient temperatures from 5 to 25°C (Sullivan and Mullen 1954). Sheriff et al. (2013) showed that U. parryii is able to increase body mass during the active season without a corresponding decrease in metabolic rate. The average energetic cost of thermoregulation in active U. parryii was estimated at 20 kJ/day ( Chappell 1981).

Urocitellus parryii is the northernmost hibernating terrestrial animal species. During initiation of torpor, maintenance of high body temperatures and circadian rhythms ceases, and these characteristics are absent during hibernation ( Barnes 1989; Williams et al. 2012a, 2012b). However, gradual decreases in body temperature actually begin 45 days prior to initial torpor, a period during which maximum and minimum body temperatures show different patterns of decrease ( Sheriff et al. 2012). Some wild populations may begin multiday torpor without any preliminary torpor bouts ( Sheriff et al. 2012). When in torpor, body temperatures of both sexes descend to steady states that can be maintained at up to 15°C warmer than ambient soil temperatures, depending on geographic location (Buck and Barnes 1999b).

Initiation of hibernation in U. parryii is accompanied by additional physiological adjustments including slowing of heart rate to 3–4 beats/min, reduced blood flow, and increasingly sporadic breathing (Boyer and Barnes 1999). Hibernation consists of sequential 2- to 3-week torpor bouts interrupted by short, spontaneous arousals, the latter of which are not synchronous among individuals within populations. Metabolic rate during hibernation has been reported at as low as 0.01 ml/g/h (Boyer and Barnes 1999; Karpovich et al. 2009), but this rate increases as ambient temperatures become extremely low ( Karpovich et al. 2009). U. parryii is also the largest species of hibernator known to employ supercooling, wherein body fluids cool to subfreezing temperatures without becoming solid. It endures steady state body temperatures during hibernation as low as −2.9°C ( Barnes 1989), and whole-body average temperatures during torpor were reported as −1.7 to −1.9°C ( Barnes 1989; Lee et al. 2016). Rates of rewarming from torpor to 30°C have been reported as 4.9°C/h ( Lee et al. 2016), although the time to euthermia increases as ambient temperatures decrease ( Karpovich et al. 2009). U. parryii exhibits longer torpor bouts and shorter arousal bouts than a sympatric hibernator, the Alaska marmot ( Marmota broweri — Lee et al. 2016).

Both lipids (from adipose) and protein (from muscle) are utilized for energetic demands during hibernation; protein may provide up to one-fifth of necessary carbon (Galster and Morrison 1976). Rates of catabolism vary among different muscle groups (Galster and Morrison 1976). Buck and Barnes (1999b) reported 21% loss in lean mass in hibernating female U. p. kennicottii. However, hibernaculum temperature was uncorrelated with body condition at emergence, suggesting the latter may not be impacted by increased thermogenesis and more frequent arousals due to colder hibernacula (Buck and Barnes 1999a). The amount of polyunsaturated fatty acids in autumn diets is important for overwinter survival and also influences the length of torpor and arousal periods ( Frank et al. 2008). Hatton et al. (2017) characterized the gut microbiomes and metatranscriptomes of captive U. parryii maintained on varying diets.

DISTRIBUTION

Urocitellus parryii is distributed broadly in the northern Holarctic region ( Fig. 3 ; Hall 1981; MacDonald and Cook 2009; Cook et al. 2010; Krystufek and Vohralik 2013). In North America, it occurs from 52° N latitude to as far north as the shores of the Arctic Ocean in Alaska ( USA), Yukon, Northwest Territories, and Nunavut ( Canada). Easternmost and westernmost limits of this range are the shores of Hudson Bay (in Nunavut and northwestern Manitoba) and the Seward Peninsula and some islands of the Aleutian Arc, respectively. It occurs as far south as northern British Columbia and Manitoba. However, its wide Nearctic range is somewhat discontinuous; in Alaska, it is notably absent from large portions of the Klondike region, the lower Yukon River valley (except U. p. osgoodi ), and the Yukon- Kuskokwim Delta. U. parryii in Asia is confined to Russia, where it occupies a nearly identical latitudinal range as in North America and is found discontinuously across northeastern Siberia east of the Lena River (Sakha) to the shores of the Bering Sea. However, the core of this Palearctic range is in Chukotka and Kamchatka east of the Kolyma River ( Ognev 1947; Chernyavsky 1972; Krystufek and Vohralik 2013). Krystufek and Vohralik (2013) cited a 20th-century range expansion along the Indigirka River between Predporožnyj and Tebûlâh. Across its range, U. parryii is found from sea level to about 1,500 m in elevation. Several major mountain ranges are inhabited such as the Brooks and Alaska ranges in North America and the Chersky Range in Russia. U. parryii occurs on numerous islands in the Nearctic; U.p. lyratus is endemic to St. Lawrence Island in the Bering Sea. However, a more complex history of colonization and humanmediated introduction has shaped its occurrence on islands of southwestern Alaska and the Aleutian Arc ( Cook et al. 2010). Numerous records of island introduction by indigenous peoples or Europeans exist, including as prey for furbearers and for use in garment making (see Cook et al. 2010 and West et al. 2017 for additional details). U. p. kodiacensis appears to have been introduced to Kodiak Island ( Howell 1938; Cook et al. 2010). The insular distribution of U. parryii in the Palearctic is limited to Ajon, in northern Chukotka (Krystufek and Vohralik 2013).

FOSSIL RECORD

The earliest fossils potentially assignable to Urocitellus parryii are from the Fish Creek fauna in northernmost Alaska and date to 2.4 million years ago or older ( Repenning et al. 1987). Additional early records are available from the early to middle Pleistocene of Yukon and are dated at 1.5–1.7 million years ago (Fort Selkirk Local fauna—Storer 2003). However, the specific identity of both series of specimens is inconclusive, particularly given that U. undulatus likely arose from Nearctic stock ( McLean et al. 2016) and must therefore have colonized Asia via Beringia. Material more confidently assignable to U. parryii is available from the middle to late Pleistocene of Yukon and Alaska (Sangamon interglacial and Illinoian glaciation—Guthrie and Matthews 1971; Jopling et al. 1981; Harington 2011). A relative abundance of material exists from the middle Wisconsin glaciation through Holocene (80,000 years ago to present—Graham and Lundelius 2010); much of that material comes from fossil ground squirrel middens, which themselves have contributed to understanding of Beringian late Quaternary paleoecology and paleoenvironments ( Zazula et al. 2007). Mummified remains of U. parryii have been documented at sites in both the Palearctic and Nearctic ( Zazula et al. 2007; Harington 2011; Faerman et al. 2017); Faerman et al. (2017) provided a calibrated radiocarbon (14 C) date of 33,075 years on fossil U. parryii from Yakutia, Russia. One extinct subspecies (U. p. glacialis — Vinogradov 1948) is recognized from the late Pleistocene of Russia ( Faerman et al. 2017).

ONTOGENY AND REPRODUCTION

Young Urocitellus parryii are naked, blind, and altricial at birth, develop in nests for 27–28 days, and are weaned within roughly 1 week following emergence from natal burrows ( Carl 1971; Hubbs and Boonstra 1997; Lacey et al. 1997). Juvenile emergence occurs from mid-June to mid-July depending on the exact timing of breeding ( Carl 1971; Kiell and Millar 1978; Batzli and Sobaski 1980; McLean 1982; Hubbs and Boonstra 1997; Byrom and Krebs 1999). Weight at emergence is 20–30% of adult weight (200–300 g—Kiell and Millar 1978; Batzli and Sobaski 1980; Buck and Barnes 1999a), and ontogenetic allometric variation exists such that at emergence, external linear measurements of juveniles are closer to adult proportions than is weight (Kiell and Millar 1978). Juvenile males grow faster than females (Hubbs and Boonstra 1997; Wheeler and Hik 2014a); rates of 7 and 5 g /day have been reported, respectively (Buck and Barnes 1999a). Young typically reach adult weight toward the end of their 2nd season (Buck and Barnes 1999a). Secondyear males and females are capable of breeding despite being less than 12 months old, though not all will do so ( Sheriff et al. 2011). Wheeler and Hik (2014a) suggested that juvenile growth rates are dependent on habitat, being higher in more open habitats due to either decreased predation risk or availability of higherquality forage. In males, however, relative influence of habitat characteristics on weight gain decreases through time (Wheeler and Hik 2014a). Specific growth rates of juvenile U. p. parryii are several times higher than in some other marmotine ground squirrel genera (Kiell and Millar 1978).

Urocitellus parryii breeds just once a year. As in many other Urocitellus , breeding individuals of both sexes are reproductively mature upon spring emergence. In reproductive males, reactivation of the circadian clock in spring leads to an increase in circulating testosterone, resumption of heterothermy, and gonadal development prior to emergence. These testosterone increases prevent reentry into torpor; conversely, females and nonreproductive males may repeat spring torpor bouts if weather conditions remain poor ( Williams et al. 2017). Male U. p. kennicottii are known to maintain active season body temperatures for up to 10 days in hibernacula before their emergence ( Sheriff et al. 2011). Three to 4 days following emergence, breeding females enter estrus for a single afternoon ( Lacey et al. 1997; Buck and Barnes 1999a). Copulation usually occurs underground ( Lacey et al. 1997), gestation lasts 25 days ( Mayer 1953; Lacey et al. 1997; Sheriff et al. 2011), and parturition is completed by late May at low latitudes ( McLean 1982) or the first one-half of June at high latitudes ( Carl 1971; Kiell and Millar 1978). Temporal variation of this same magnitude has been observed among sites in northern Alaska ( Sheriff et al. 2011).

Female U. parryii commonly give birth to up to 9 young. Mean counts of embryos or placental scars have been reported as 4.9 in U. p. plesius (Hubbs and Boonstra 1997) and 6.5–7.6 in U. p. kennicottii ( Richardson 1825; Mayer 1953; Carl 1971). Ognev (1947) reported 7–9 embryos per female in U. p. leucostictus . Embryo resorption has been reported ( Carl 1971). Litter counts based on trapping data are generally lower than embryo counts, from 4.1 in U. p. plesius (range 1–5— Lacey et al. 1997) to 5.5–6.1 in U. p. kennicottii ( Carl 1971). Geist (1933) observed 5 live young in a U. p. lyratus nest. Weight gain by female U. p. plesius due to pregnancy was reported as 61 g (McLean and Towns 1981). Approximately equal juvenile sex ratios are documented (Batzli and Sobaski 1980; McLean 1982).

ECOLOGY

Population characteristics. — Urocitellus parryii is colonial, and aspects of its population biology have been studied in detail. Density of breeding adults varies with latitude and habitat; in northernmost Alaska, densities range from 0.2 to 1.7 adults/ha ( Mayer 1953; Batzli and Sobaski 1980), although 5– 8 adults /ha are typical farther south ( Carl 1971; Donker and Krebs 2011). However, variation of equal or greater magnitude can occur between habitats in U. p. plesius , with <1–3/ ha documented in boreal forest habitats (Hubbs and Boonstra 1997; Byrom and Krebs 1999; Byrom et al. 2000; Hik et al. 2001; Donker and Krebs 2011; Werner et al. 2015) and 3–16/ha documented in meadow or tundra habitats ( Lacey et al. 1997; Hik et al. 2001; Donker and Krebs 2011; Werner et al. 2015). Population densities increase in summer before juvenile dispersal, and local densities can also be higher during hibernation than in the active season ( Carl 1971). Significantly higher densities than those listed above are reported from experimental manipulations (Hubbs and Boonstra 1997; Byrom and Krebs 1999; Byrom et al. 2000).

Colony size is relatively stable in tundra populations of U. p. kennicottii, although turnover of individuals can be high ( Carl 1971; Batzli and Sobaski 1980). Conversely, colony size may fluctuate widely in the subarctic ( Boutin et al. 1995; Hubbs and Boonstra 1997; Lacey and Wieczorek 2001). However, U. parryii is not a cyclic species; extreme population lows are induced by extrinsic phenomena such as crashes in hare ( Lepus ) populations that increase predation pressure on squirrels ( Boutin et al. 1995; Hubbs and Boonstra 1997; Byrom et al. 2000; Werner et al. 2015). During a period of decreased hare numbers in Yukon, Byrom et al. (2000) recorded that 96% of active season mortalities were due to predation. Populations can also be impacted by climatic factors such as anomalously high or low snowpack; the former may limit access to spring forage by delaying snowmelt (Hubbs and Boonstra 1997; Williams et al. 2017) and the latter decreases overwintering success by reducing soil insulation (Karels and Boonstra 2000; also see Carl 1971; Buck and Barnes 1999a). Hubbs and Boonstra (1997) suggested female U. parryii have higher overwinter survival than males, and Carl (1971) suggested pregnancy rates differ between highquality and low-quality habitats.

Based on their study of U. p. kennicottii, Batzli and Sobaski (1980) suggested 3 types of U. parryii colonies exist: those in favorable habitats with high densities, little fluctuation in density, and consistent growth rates; those in acceptable habitats with lower densities that are also more susceptible to density fluctuations; and “refugee” populations ( Carl 1971) that do not breed and inhabit areas only temporarily. Data from U. p. plesius appear to support parts of this model. In Yukon, this subspecies inhabits alpine meadows, lower-elevation meadows, and boreal forests ( McLean 1982; Byrom and Krebs 1999; Donker and Krebs 2011, 2012). Alpine meadows support high population densities with higher recruitment and boreal forests function as sink habitats, supporting smaller populations with lower densities, lower recruitment rates, and occasionally extreme fluctuations (Donker and Krebs 2011, 2012). Nonbreeding (“refugee”) colonies from this region have not been explicitly reported.

Predation and food resources are the major factors influencing population dynamics of U. parryii ( Byrom et al. 2000; Karels and Boonstra 2000). At normal population levels, food is the more important of these and is known to improve female overwinter survival, spring body mass, percent of females lactating, and reproductive success. Juvenile recruitment and growth rates also benefit from increased food availability (Hubbs and Boonstra 1997; Byrom et al. 2000; Karels and Boonstra 2000). Strong density dependence has been inferred in U. parryii ; proportions of females weaning a litter or successfully overwintering are inversely correlated with population density (Karels and Boonstra 2000). However, concordant with the noncyclic nature of U. parryii , active season survival is not density-independent (Karels and Boonstra 2000). Also, when extreme population declines occur, predation may become more important than resource availability in determining U. parryii population growth rates ( Byrom et al. 2000).

Juvenile mortality may be up to 75% in U. parryii . As in many other ground-dwelling sciurids, U. parryii females exhibit high natal philopatry, with juvenile dispersal and mortality being highly male biased. Male dispersal rates appear independent of population density, while those of females are dependent on resource availability (Byrom and Krebs 1999; Karels and Boonstra 2000). Male dispersal distances can be up to 4 times greater than in females, and males may exhibit higher survival than females when dispersal distances are this long (Byrom and Krebs 1999). Males dispersing from high-quality habitats have higher survival than those dispersing from lower-quality habitats (Donker and Krebs 2012).

Space use. —Optimal habitats for Urocitellus parryii are open tundra and meadows, although boreal forests and tundra-forest–meadow-forest ecotones are also used in southern parts of its range. U. parryii is locally common in some anthropogenically modified habitats as well. As a burrower, its primary habitat requirement is well-drained soils. In tundra systems, it occupies well-drained areas on hillsides, hillocks, bluffs, and along creeks and riverbanks ( Quay 1951; Mayer 1953; Carl 1971; Batzli and Sobaski 1980), where it prefers sandy, sandy clay, or loamy soils with permafrost levels deep enough to allow burrows ( Quay 1951; Mayer 1953; Carl 1971). Typically, these habitats are characterized by expanses of evergreen tundra shrubs ( Dryas and various Ericaceae ), deciduous shrubs (e.g., Salix ), and monocots (e.g., Carex, Eriophorum ). In subalpine areas of Alaska and Yukon, U. parryii prefers high- or low-elevation meadows and boulder fields characterized by forbs, grasses, and lichens and interspersed to various degrees with willow ( Salix ), poplar ( Populus ), spruce ( Picea ), birch ( Betula ), or aspen ( Populus — McLean 1982; Lacey et al. 1997; Byrom and Krebs 1999; Donker and Krebs 2012).

Territories of male U. parryii are generally larger than those of females. Areas are 0.31–4.3 ha for males ( Mayer 1953; Carl 1971; Batzli and Sobaski 1980) and 0.15–3.2 ha for females (Batzli and Sobaski 1980; McLean 1982; Byrom and Krebs 1999). Territory sizes of both sexes appear negatively correlated with population density ( Carl 1971; Batzli and Sobaski 1980; Byrom and Krebs 1999). U. parryii is known to forage most often within 30 m of burrows, but usually not directly at burrow entrances (Batzli and Sobaski 1980). The home ranges of males may be significantly larger than, and positively correlated with, sizes of defended territories ( Carl 1971). Female home ranges do not change demonstrably across the active season ( McLean 1982). Extreme movements of up to 1 km /day have been recorded ( Mayer 1953; Batzli and Sobaski 1980), and sightings as far as 4 km out on sea ice have been noted ( Carl 1971).

Urocitellus parryii constructs a variety of burrows. Residence burrows are used perennially as both hibernacula and natal burrows; they may have up to 6 or more entrances and are usually up to 1 m deep ( Ognev 1947; Batzli and Sobaski 1980; Buck and Barnes 1999a). Latrines may also be located in adjacent cavities ( Mayer 1953). Secondary (or “transient”) burrows may have up to 4 entrances and are usually <0.5 m deep; they are used primarily for short-term safety while foraging (or for longer if predators are present). Carl (1971) referred to secondary burrows as “duck holes,” noting they never contain enlarged cavities or nests. Carl (1971) also described additional burrow types, such as boundary pits (shallow diggings <25 cm deep located at edges of male territories). The longest and deepest burrows documented occur in sandy habitats ( Ognev 1947). Burrow complexes of intermediate size and containing 4–11 openings can be constructed within 4 days ( Carl 1971).

Nests of U. parryii are 22–30 cm wide and may be lined with dry grass, leaves, lichens, or fur ( Geist 1933; Mayer 1953; Barnes 1989); nesting materials are rolled into a ball during hibernation ( Barnes 1989). Winter hibernaculum temperatures vary with local snow cover and also with the presence of shrubby vegetation (Buck and Barnes 1999a). Females tend to occupy warmer hibernacula than males, and adults occupy warmer hibernacula than juveniles (Buck and Barnes 1999a). In spring, females may plug entrances to natal burrows with loose dirt prior to juvenile emergence ( Mayer 1953). A daytime burrow is often used as a strategy to maintain optimal body temperatures ( Long et al. 2005).

Diet. — Urocitellus parryii is a generalist herbivore that consumes a broader variety of plant types than most other Arctic rodents, with forbs comprising the largest portion. Feeding preferences do not appear to be in proportion to local plant abundances, but instead are driven by palatability, which is correlated with moisture and nutrient content (Batzli and Sobaski 1980; McLean 1985). The most common dietary components are members of the families Fabaceae , Saxifragaceae , Salicaceae , and Ericaceae ; grasses ( Poaceae ) contribute to a smaller proportion. Roots, shoots, leaves, and flowers are all consumed, although flowers may be the only parts of less palatable plants that are eaten. Lichens, mosses, and fungi may also be taken in lesser quantities. Hobbie et al. (2017) found significant dietary differences between populations of U. p. kennicottii. Seasonal variation in diet also exists; spring diet appears more variable than that of summer and autumn, and seeds may contribute to a larger proportion of the latter (Batzli and Sobaski 1980). McLean (1985) demonstrated that male and female U. p. plesius have comparable diets for most of the season, but these diverge by autumn; however, there was little effect of sex on dietary stable isotope ratios in northern Alaskan populations ( Hobbie et al. 2017). The foraging patterns of U. parryii on legumes may potentially lead to competition with moose ( Alces alces ), porcupine ( Erethrizon dorsatum ), snowshoe hare ( Lepus americanus ), or feral horses ( Equus ferus caballus — McLean 1985).

Although classified here as a herbivore, U. parryii like many other small mammals will regularly consume animal material, including arthropods. It will also consume meat of other vertebrates, including collard lemmings ( Dicrostonyx groenlandicus — Boonstra et al. 1990), voles ( McLean 1985), mice ( Geist 1933), various birds ( Ognev 1947; Cade 1951; Ebbert and Byrd 2002), and dried meats ( Geist 1933; Cade 1951; Mayer 1953) if available. Ten percent of juvenile snowshoe hare mortality in Yukon was attributed to predation by U. p. plesius ( O’Donoghue 1994) . U. parryii will also consume eggs and chicks of seabirds and is thus capable of contributing to local declines in nesting densities of these species (Ebbert and Byrd 2002; West et al. 2017). Cannibalism in U. parryii appears fairly common and has been documented on juveniles and adults killed by aggressive males ( Steiner 1972; Holmes 1977; McLean 1985), individuals in captivity (Osgood etal. 1915; Musacchia 1954) and on hibernating, handicapped, trapped, and roadkill individuals ( Cade 1951; Mayer 1953).

Diseases and parasites. — Urocitellus parryii harbors the siphonapterid fleas Oropsylla alaskensis and O. idahoensis (Nadler and Hoffmann 1977) . The former occurs on high-latitude Asian and North American populations of U. parryii ; the latter is not host specific and parasitizes other Nearctic ground squirrel species ( Haas et al. 1978; Lewis 2002). The sucking louse Linognathoides (= Neohaematopinus ) laeviusculus is known from U. p. kennicottii ( Weber 1950; Carl 1971). The roundworm Ascaris laevis ( Tiner 1951; Carl 1971) and the cestode Paranoplocephala wigginsi ( Rausch 1954) are known from U. parryii ; Carl (1971) further documented the presence of “unidentified” nematodes. Echinococcus has been reported in U. p. lyratus ( Thomas et al. 1954) ; however, Rausch and Schiller (1956) expressed doubt about the true extent of susceptibility to that parasite. Five species of apicomplexans (parasitic protists) have been recorded from U. parryii : Eimeria callospermophili , E. cynomysis , E. lateralis , E. morainensis , and E. yukonensis ( Sampson 1969; Seville et al. 2005).

Interspecific interactions. — Urocitellus parryii has a variety of predators across its geographic range. In tundra systems, mammalian predators include red fox ( Vulpes vulpes ), grizzly bear ( Ursus arctos ), gray wolf ( Canis lupus ), wolverine ( Gulo gulo ), ermine ( Mustela erminea ), and occasionally Arctic fox ( Vulpes lagopus — Ognev 1947; Chesemore 1968; Carl 1971; Reid et al. 1997). U. parryii may also be prey for most high-latitude raptor species such as golden eagle ( Aquila chrysaetos — Reid et al. 1997), peregrine falcon ( Falco peregrinus — Bradley and Oliphant 1991), gyrfalcon ( Falco rusticolus —Poole and Boag 1988), rough-legged hawk ( Buteo lagopus — Reid et al. 1997), and snowy owl ( Bubo scandiacus — Quay 1951; Carl 1971), as well as petrels and gulls ( Ognev 1947). In the subalpine and boreal habitats typical of U. p. plesius , major predators include Canada lynx ( Lynx canadensis ), coyote ( Canis latrans ), weasels (Mustelinae), northern goshawk ( Accipeter gentilis ), red-tailed hawk ( Buteo jamaicensis ), and great-horned owl ( Bubo virginianus —Byrom and Krebs 1999). Carl (1971) implicated red fox as the most significant predator at Ogotoruk Creek (coastal northwest Alaska) and calculated a predation rate of 4.2 squirrels/day for 1 fox at that site. He documented prey switching in autumn in foxes and grizzly bears, with the former feeding on marine mammal carcasses but the latter increasingly able to excavate squirrel burrows as permafrost depths lower ( Carl 1971). Hubbs and Boonstra (1997) reported roughly equal avian and mammalian predation near Kluane Lake, Yukon (45% and 55%, respectively). However, in this same region, Byrom et al. (2000) found 75% of adult mortality by avian predators, while Donker and Krebs (2012) found 100% of predation by avian predators. Poole and Boag (1988) reported gyrfalcon predation on U. parryii in Northwest Territories that was heavily biased toward juveniles.

Burrowing and deposition of waste by U. parryii can have significant impacts on soil geomorphology and local plant communities. As much as 18,000 kg of soil per hectare may be excavated every year by U. p. plesius in Yukon, and this can also accelerate denudation ( Price 1971). Waste deposition can lead to fertilization via increases in available nitrogen and phosphorus around burrow systems, and this in combination with burrowing appears not only to increase the number of grasses and some vascular plant species, but also to decrease overall species richness surrounding burrows (Wheeler and Hik 2013). Bee and Hall (1956) stated that mutualistic habitat and antipredator interactions exist between U. parryii and the Alaska marmot.

HUSBANDRY

Urocitellus parryii can be captured using wire mesh live traps (e.g., Tomahawk [Tomahawk Live Trap, Hazelhurst, Wisconsin]; Havahart [Woodstream Corporation, Lititz, Pennsylvania]) baited with peanut butter, oats, fresh apple, or carrots. Many populations are easily habituated to long-term trapping or observation, and recapture success up to 95% has been reported (Hubbs and Boonstra 1997). Prebaiting for 1–2 days may increase juvenile capture rates (Hubbs and Boonstra 1997). U. parryii is successfully marked using dyes (e.g., Nyanzol) applied to areas where it cannot be removed (i.e., neck and back), as well as with ear tags or by toe clipping.The latter can be used to identify individuals from snow tracks ( Carl 1971). U. parryii can be successfully monitored via radiotelemetry (e.g., Werner et al. 2015) and with the use of passive integrated transponder tags (e.g., Sheriff et al. 2013). Numerous studies describe methods for maintaining U. parryii under laboratory conditions (e.g., Karpovich et al. 2009).

BEHAVIOR

Urocitellus parryii has a tightly constrained phenology, with an active season of 4–5 months and a hibernation period of 7–8 months. Extreme values for adult hibernaculum emergence and immergence across the range are early April and early October, respectively; however, timing of both activities varies with latitude, microclimate, sex, and age. Adult males always emerge prior to females, but male emergence occurs earlier at lower latitudes (early April—McLean and Towns 1981; Lacey et al. 1997) and later at high latitudes (mid to late April—Carl 1971; Sheriff et al. 2011). Females tend to emerge 7–10 days later than males at lower latitudes and 9–14 days later than males at high latitudes ( Carl 1971; Sheriff et al. 2011). Females that do not breed in their 1st year emerge from hibernacula up to 3 weeks later than those that do ( Sheriff et al. 2011). Interestingly, differences in microclimate can lead to variation in emergence dates comparable to that among latitudes, up to 9 and 13 days for males and females at sites in northern Alaska, respectively ( Sheriff et al. 2011). Autumn immergence likewise varies with age, sex, and habitat. Adults enter hibernacula before juveniles ( Carl 1971; McLean 1982; Sheriff et al. 2011), presumably due to the need for 1st-year individuals to acquire sufficient fat reserves. Adult females immerge before males (McLean and Towns 1981; Hubbs and Boonstra 1997; Sheriff et al. 2011). Female hibernation is thus absolutely longer than males, with lengths of 242–246 days and 191–205 days reported in northern Alaska, respectively (Buck and Barnes 1999b; Sheriff et al. 2011). Unlike in adults, 1st-year males and females display similar hibernation durations, but chronologies vary in the sex-specific manner mentioned above (McLean and Towns 1981; Sheriff et al. 2011). U. parryii hibernates singly, in a ball with dorsum uppermost ( Carl 1971).

Urocitellus parryii is polygynous, with breeding males aggressively establishing and maintaining spring territories that contain multiple females ( Carl 1971; Batzli and Sobaski 1980; Lacey and Wieczorek 2001). Male dominance appears related to body mass (Watton and Keenleyside 1974), and detailed descriptions of male territorial disputes can be found in Carl (1971) and Watton and Keenleyside (1974). Lacey and Wieczorek (2001) recorded extremes of 1 and 14 females per male territory in Yukon. Females do not help to defend territories ( Carl 1971). The male:female ratio appears inversely related to habitat quality and is always female biased ( Mayer 1953; Batzli and Sobaski 1980; Hubbs and Boonstra 1997; Byrom et al. 2000). Territories of breeding males are mostly non-overlapping, with absolute sizes that differ based on population density (Lacey and Wieczorek 2001). Neighboring males are not likely to be close relatives (Lacey and Wieczorek 2001), and surviving males can hold the same territory in sequential years ( Carl 1971). In addition to breeders, there is further segregation into floater and refugee males each spring ( Carl 1971). Floater males may reside in colonies between defended territories and can take over territories and females belonging to deceased males ( Carl 1971). An increase in territoriality also occurs in the autumn, presumably related to defense of hibernation burrows or the food caches they contain ( Carl 1971; Buck and Barnes 2003). Scent marking has been observed in U. parryii (Watton and Keenleyside 1974; Buck and Barnes 2003).

Intersexual interactions of U. parryii are minimal for much of the year ( Carl 1971) but become intense surrounding estrus, when male movements are centered on female home ranges (Lacey and Wieczorek 2001). Multiple matings are common in females (average of two according to Lacey et al. 1997), but 1st matings are most often with the male in whose territory a female resides (Lacey and Wieczorek 2001). The order of mating in turn often predicts paternity, suggesting male territoriality is directly related to reproductive success (Lacey and Wieczorek 2001). Unlike males, natal burrows of related females are significantly closer to one another than among nonrelatives ( McLean 1982), and antagonistic interactions have been shown to increase among females as relatedness decreases ( McLean 1982). Following juvenile emergence, females may selectively clump young with related females ( McLean 1982). In late summer, male aggression toward juveniles increases, often resulting in wounding or death ( Steiner 1972; Batzli and Sobaski 1980). Such aggression may act to enforce dispersal, either for population control ( Steiner 1972) or inbreeding avoidance (Batzli and Sobaski 1980; Byrom and Krebs 1999).

Urocitellus parryii maintains a circadian rhythm throughout the active season despite the fact that some high-latitude populations experience 24 h of daylight. Individuals of U. p. kennicottii occurring north of the Arctic Circle were active 14–16 h/ day, largely between 500 and 2,200 h ( Chappell 1981). The percent of time spent above ground is correlated with mean surface temperatures, being higher in June and July and lower in early and late portions of the active season ( Long et al. 2005). The circadian clock is either fully inhibited or significantly desynchronized during hibernation, leading to the cessation of body temperature and clock protein expression oscillations ( Ikeno et al. 2017). Entrainment of the circadian clock to a roughly 24-h periodicity following the final torpor bout requires 10–27 days in males but occurs more rapidly in females ( Williams et al. 2012a, 2012b). It is hypothesized that this clock has retrainment cues other than exposure to daylight ( Williams et al. 2012a).

Foraging strategies of U. parryii during the active season may be adapted to local habitat conditions in an effort to minimize predation risk. In U. p. plesius , giving-up densities (amounts of food left in a food patch when an animal will choose to move to other patches) are greater in lower visibility, shrub-dominated habitats relative to open tundra or meadow habitats, and the time spent in erect vigilance posture is greater in the former (Wheeler and Hik 2014b). As a result, foraging may be less efficient in shrubby habitats where individuals have more difficulty acquiring information about predators (Wheeler and Hik 2014b).

Urocitellus parryii is known to swim ( Mayer 1953) as well as climb in shrubs ( McLean 1985) or lower branches of small trees (observed by BSM). Juveniles exhibit play behavior ( Mayer 1953). U. parryii is capable of a wide variety of vocalizations, including alarm calls, fright calls, and belligerence calls ( Carl 1971). Multiple alarm calls exist, including loud, piercing whistles ( Mayer 1953). Some alarm calls may be courtship specific ( Lacey et al. 1997). Belligerence calls include molar rattling, growling, or hissing ( Carl 1971). U. parryii is generally more vocal near burrows than in open ground ( Mayer 1953). Tail-flicking behavior is common and is often be accompanied by piloerection of tail hairs ( Mayer 1953). Mayer (1953) documented individuals taking dirt baths in loose or excavated soil.

GENETICS

Urocitellus parryii has a diploid (2 n) number of 34 chromosomes, which it shares with 2 other species in the big-eared group ( U. armatus , U. elegans ). The fundamental number of U. parryii is 64 in all populations across its range (Nadler 1966; Nadler et al. 1984). The karyotype contains 20 metacentrics and 12 submetacentrics. X and Y chromosome morphology differs from U. armatus but not demonstrably from U. elegans (Nadler 1966) . Similarity in chromosome Giemsa-banding patterns exists among populations ( Nadler et al. 1984). Nadler et al. (1984) suggested that the 2 n = 34 karyotype of U. parryii may be the ancestral condition in the big-eared clade from which all other known karyotypes (2 n = 30–36) evolved. However, this is unsupported by DNA sequence analyses, which confirm that U. parryii is derived within the big-eared species group ( Harrison et al. 2003; McLean et al. 2016).

Unlike karyotypic data, significant geographic and subspecific-level protein electrophoretic variation has been documented in U. parryii . Serum transferrin is the most widely examined electrophoretic locus in the context of U. parryii systematics and phylogeography. This and other loci (both genotypes and allele frequencies) suggest shallow divergence between Palearctic and North American Arctic populations, but more significant divergence between these populations and those in the North American subarctic (U. p. kodiacensis, U. p. lyratus , U. p. ablusus, U. p. plesius —Nadler and Hughes 1966; Nadler 1968; Nadler and Youngman 1969, 1970; Nadler et al. 1973). However, 2 G6PD alleles that are unique to Palearctic populations have been identified (Nadler and Hoffmann 1977). High levels of polymorphism and significant divergence (F st) in microsatellite loci among insular and mainland populations of southwestern Alaska have also been identified; among the most distinctive insular populations were those on Ushagat, Unalaska, and Kavalaga Islands ( Cook et al. 2010).

Range-wide phylogeographic analyses based on mitochondrial and nuclear sequence data recover 4 major clades within U. parryii (with subspecies inclusive): Arctic (U. p. kennicottii, U. p. parryii ), Northern Beringian (U. p. leucostictus , U. p. lyratus , U. p. osgoodi ), Southern Beringian (U. p. ablusus, U. p. kodiacensis, U. p. nebulicola , U. p. stejnegeri ), and Southeast (U. p. plesius ; Eddingsaas et al. 2004; Galbreath et al. 2011; McLean et al. 2016; Faerman et al. 2017). As suggested by their names, both the Northern and Southern Beringian mitochondrial clades have amphi-Beringian distributions ( McLean et al. 2016). Results of sequence analyses along with karyotypic, electrophoretic, and geographic considerations (e.g., insularity) support the majority of current subspecific arrangements. There is, however, conflict among the evolutionary histories that have been inferred from these datasets.

Morphological, enzymatic, and parasitological data have been summarized and a model of U. parryii migration and evolution outlined (Nadler and Hoffmann 1977). This model consisted of 1) initial divergence of U. parryii from the Palearctic U. undulatus in Siberia, 2) eastward colonization of Beringia by forms ancestral to U. p. lyratus and U. p. ablusus, and 3) further diversification within Nearctic Beringia of Arctic (U. p. parryii , U. p. kennicottii, U. p. osgoodi ) and subarctic (U. p. plesius ) lineages. Nadler and Youngman (1970) and Nadler and Hoffmann (1977) also considered U. p. osgoodi as closely related to U. p. kennicottii and U. p. parryii . Available data disagree with these hypotheses in several respects. First, sequence data support Nearctic populations as ancestral within U. parryii ( Eddingsaas et al. 2004; Galbreath et al. 2011), suggesting westward colonization of the Palearctic during the late Pleistocene ( Galbreath et al. 2011; Faerman et al. 2017). Second, Nearctic subspecies do not appear to be each other’s closest relatives, inconsistent with a narrative of diversification following singular colonization of North America. Instead, multiple mitochondrial clades occupied core Beringia during the late Pleistocene, each of which are now trans-Beringian in distribution ( Galbreath et al. 2011; McLean et al. 2016). Most data accumulated to date support a scenario of in situ Beringian range shifts and diversification within U. parryii in response to late Pleistocene climate change and glaciation (Nadler and Hoffmann 1977; Eddingsaas et al. 2004; Galbreath et al. 2011; McLean et al. 2016; Faerman et al. 2017).

CONSERVATION

Due to a relatively large geographic range and sometimes locally high abundance, Urocitellus parryii is not currently a conservation concern. It is currently classified as “Least Concern” by the International Union for Conservation of Nature and Natural Resources ( Cassola 2016). Overhunting at local to regional scales may be the most significant conservation threat to U. parryii at present ( Cassola 2016). Although once used more intensively as a food source and for pelts by indigenous peoples (e.g., Ross 1861; West et al. 2017), which may have resulted in reductions in local densities and abundance (Bee and Hall 1956), current impacts of hunting on range-wide stability are today likely minimal. However, evidence of this is still needed in areas where the species has been historically understudied and undersampled (e.g., Northwest Territories and Nunavut, Canada).

Direct anthropogenic threats such as land use changes, conflicts with livestock, and pest management may impact some U. parryii populations (e.g., Davidson et al. 2012). The overall magnitude of these threats is probably lower in U. parryii than southern congeners; still, patchy distributions typical of this species render it locally vulnerable to such pressures. U. parryii inhabits boreal forests in some southern parts of its range; these habitats are considered marginal and function as population sinks relative to tundra and meadows (Donker and Krebs 2012; Werner et al. 2015). There is high potential for local extirpation in these populations, and continued assessment of possible negative effects of land use activities (such as forest resource extraction) is therefore necessary in these areas specifically.

Perhaps most importantly, U. parryii faces an evolving variety of threats related to global climate change. High northern latitudes are experiencing rates of warming that are elevated relative to global averages.At landscape scales, this results in increased active season temperatures, reduced snowpack and earlier spring snowmelt, and changing composition of tundra plant communities, including encroachment of shrubs and boreal forest. The latter in particular is known to impact the foraging ecology and population dynamics of U. parryii . Changes in hydrology, soil drainage, and potential phenological mismatches with important plant or arthropod food sources are further local-scale threats. Wheeler and Hik (2013) provide a comprehensive review of these and other climate-related issues. Finally, sea-level rise presents an additional challenge for insular populations of U. parryii . While U. p. lyratus is a true island endemic, conservation prioritization of U. p. kodiacensis, U.p. nebulicola , and other unnamed insular populations is a more complex issue that requires further assessment of their endemicity and evolutionary uniqueness.

REMARKS

The generic name Urocitellus is derived from the Latin uro for tail and citellus for ground squirrel. The specific epithet of Urocitellus parryii honors English Admiral and Arctic explorer Sir William Edward Parry, commander of the expedition on which the type series was collected, in 1821 ( Richardson 1825).

Figures

Fig. 1.—An adult Urocitellus parryii from the north slope of Alaska in 2012. Used with permission of the photographer, Michael J. Sheriff.

Fig. 2.—Dorsal, ventral, and lateral views of skull and lateral view of mandible of an adult female Urocitellus parryii kennicottii (United States National Museum [USNM] 292987) from the mouth of Anaktuvuk River, Alaska, USA.

Fig. 3.—Geographic distribution of Urocitellus parryii. Subspecies are as follows: 1, U. p. ablusus; 2, U. p. kennicottii; 3, U. p. kodiacensis; 4, U. p. leucostictus; 5, U. p. lyratus; 6, U. p. nebulicola; 7, U. p. osgoodi; 8, U. p. parryii; 9, U. p. plesius; 10, U. p. stejnegeri. Approximate subspecific limits modified from Ognev (1947) and Hall (1981).