GENERIC REVISION IN THE HOLARCTIC GROUND
SQUIRREL GENUS SPERMOPHILUS
KRISTOFER M. HELGEN,* F. RUSSELL COLE, LAUREN E. HELGEN, AND DON E. WILSON*
Division of Mammals, National Museum of Natural History, Smithsonian Institution,
P.O. Box 37012, Washington, DC 20013-7012, USA (KMH, DEW)
Department of Biology, Colby College, Waterville, ME 04901, USA (FRC)
Department of Entomology, National Museum of Natural History, Smithsonian Institution,
P.O. Box 37012, Washington, DC 20013-7012, USA (LEH)
The substantial body of research on Holarctic ground squirrels amassed over the past century documents
considerable variability in morphological, cytogenetic, ecological, and behavioral attributes in the genus
Spermophilus F. Cuvier, 1825. Recent molecular phylogenetic studies suggest that the traditionally recognized
genera Marmota Blumenbach, 1779 (marmots), Cynomys Rafinesque, 1817 (prairie dogs), and Ammospermo-
philus Merriam, 1892 (antelope ground squirrels) render Spermophilus paraphyletic, potentially suggesting that
multiple generic-level lineages should be credited within Spermophilus. Herein, we recognize 8 genera formerly
subsumed in Spermophilus, each of which is morphologically diagnosable, craniometrically distinctive, and
recovered as a monophyletic clade in phylogenetic analyses utilizing the mitochondrial gene cytochrome b.
Generic-level names are available for each of these ground squirrel assemblages, most of which are exclusively
or predominantly North American in distribution (Notocitellus A. H. Howell, 1938; Otospermophilus Brandt,
1844; Callospermophilus Merriam, 1897; Ictidomys J. A. Allen, 1877; Poliocitellus A. H. Howell, 1938;
Xerospermophilus Merriam, 1892; and Urocitellus Obolenskij, 1927). Only Spermophilus sensu stricto is
restricted to Eurasia. Generic subdivision of Spermophilus more aptly illuminates the taxonomic relationships,
ecomorphological disparity, and biogeographic history of Holarctic ground squirrels.
Key words: biogeography, cytochrome b, genus, ground squirrels, morphology, morphometrics, phylogeny, Spermophilus,
systematics, taxonomy
Investigation has shown the necessity of subdividing older
groups, as the older generic limits were too broad to permit
grouping forms with sufficient precision. (Palmer 1904:7)
Historically, the classification of organisms was long reliant
on comparisons involving anatomy only, often with consider-
able disagreement between experts over the relationships of
particular phyla and taxa. Today?s systematists, drawing
especially from molecular comparisons and cladistic method-
ology, are able to evaluate taxonomic and phylogenetic
hypotheses with higher expectations for accurate reconstruction
of evolutionary histories. Modern reassessments usually require
reconcilation of phylogenetic interpretations based on molec-
ular evidence with previous frameworks based on more
traditional character sets. Congruence is rarely perfect in such
cases, and a common outcome is the recognition of more taxa
than before, or the elevation of taxa to higher ranks than before,
or both. In essence, molecular studies often provide finer tuning
to established taxonomies, and ideally this new evidence
meshes sufficiently with morphological information to yield
a classification that more appropriately accommodates the
evolutionary relationships of the group in question. Generic
boundaries should effectively indicate evolutionary relation-
ships not only for taxonomic consistency, but also because the
genus is commonly employed as the level of analysis in
phylogenetic, paleontological, macroevolutionary, and other
comparisons. This is especially true for rodents, the most
species-rich order of mammals (e.g., Amori and Gippoliti
2001; Grelle 2002; Helgen 2003; Jansa and Weksler 2004;
McKenna and Bell 1997; Mercer and Roth 2005). The sciurid
genus Spermophilus F. Cuvier, 1825, is an excellent example
of a well-studied genus that is in need of modern, integrative
revision, and this paper is an attempt to provide such an
overview for this varied group of ground squirrels.
As currently recognized, the sciurid genus Spermophilus is
Holarctic in distribution, occurring throughout temperate and
* Correspondents: helgenk@si.edu and wilsond@si.edu
 2009 American Society of Mammalogists
www.mammalogy.org
Journal of Mammalogy, 90(2):270?305, 2009
270
arctic Eurasia from central Europe to China, Mongolia, and
Siberia, and throughout western North America, from Alaska to
Mexico, extending as far east as Ohio (Ellerman and Morrison-
Scott 1966; Hall 1981; McKenna and Bell 1997; Thorington
and Hoffmann 2005; Wilson and Ruff 1999). Species classified
in Spermophilus inhabit a wide range of habitats, including
tropical, subtropical, and temperate forests; hot and cold
deserts; prairies and steppes; open woodlands; and tundra
(Howell 1938; Ognev 1947; Wilson and Ruff 1999). As
currently recognized (Thorington and Hoffmann 2005),
Spermophilus is composed of 41 species allocated into 6
subgenera: Callospermophilus Merriam, 1897 (3 species),
Ictidomys J. A. Allen, 1877 (4 species), Otospermophilus
Brandt, 1844 (5 species), Poliocitellus A. H. Howell, 1938 (1
species), Spermophilus (26 species), and Xerospermophilus
Merriam, 1892 (2 species). All 6 subgenera occur in North
America, but only the subgenus Spermophilus is represented in
Eurasia.
The most comprehensive taxonomic revision of Holarctic
ground squirrels to date was the influential overview by Howell
(1938). He united most larger ground squirrels of North
America and Eurasia (with the exception of prairie dogs and
marmots) under the single genus Citellus Oken, 1816, and
recognized several distinctive subgenera (including Ammo-
spermophilus Merriam, 1892, Notocitellus A. H. Howell, 1938,
Otospermophilus, Callospermophilus, Poliocitellus, Ictidomys,
and Xerospermophilus). Oken proposed the name Citellus for
this group in 1816, and although much of the earlier literature
uses this name, it was subsequently ruled unavailable
(Hershkovitz 1949; International Commission on Zoological
Nomenclature 1956). The basis of the ruling was that Oken?s
names were non-Linnaean, which renders them unavailable in
scientific nomenclature. Before Howell?s (1938) review, it also
was common for many authors to regard some of these
subgenera, especially Otospermophilus and Callospermophi-
lus, as distinctive genera (e.g., Linsdale 1938; Miller 1924), but
essentially all subsequent authors have followed Howell in
including these groupings within Spermophilus (e.g., Black
1963; Miller and Kellogg 1955; Moore 1959, 1961). The most
influential change to Howell?s scheme was made by Bryant
(1945), who raised one of Howell?s subgenera, Ammospermo-
philus, to full generic rank; this has been followed in most
subsequent taxonomic compendia and checklists (e.g., Hall
1981; Hall and Kelson 1959; Hoffmann et al. 1993; Thorington
and Hoffmann 2005). Nevertheless, the species of Ammosper-
mophilus are not more distinctive morphologically relative to
the type species of Spermophilus than are the species of several
of Howell?s other subgenera, especially Notocitellus, Otosper-
mophilus, and Callospermophilus, as we will show in this
revision.
In Russia, various workers studied the Eurasian forms,
recognizing the diversity in the group. Ognev (1947) further
divided Howell?s (1938) nominate subgenus Citellus into 3
component subgenera (Colobotis Brandt, 1844; Urocitellus
Obolenskij, 1927; and Citellus) and Gromov et al. (1965)
elevated several subgenera to generic rank, but these arrange-
ments have not been widely followed, especially among North
American workers.
In the latter part of the 20th century, chromosomal studies
became increasingly influential in estimations of taxonomic
relationships among ground squirrels (e.g., Nadler 1966a,
1966b; Nadler et al. 1973), but these had little impact on the
definition of the genus Spermophilus overall. Most recently,
molecular studies have been used to refine understanding of
the phylogenetic relationships of ground squirrel species,
subgenera, and genera (Harrison et al. 2003; Herron et al.
2004).
Apart from Ammospermophilus, 2 additional genera of
ground squirrels?prairie dogs (Cynomys Rafinesque, 1817,
western North America, 5 recognized species) and marmots
(Marmota Blumenbach, 1779, North America and Eurasia, 14
recognized species)?are considered very closely related to
Spermophilus, as indicated by their classification alongside
Spermophilus and Ammospermophilus in the sciurid tribe
Marmotini (Mercer and Roth 2005; Thorington and Hoffmann
2005). The chipmunks (Tamias Illiger, 1811, Eutamias
Trouessart, 1880, and Neotamias A. H. Howell, 1929) and
Asian rock-squirrels (Sciurotamias Miller, 1901) together are
thought to constitute the sister lineage to Spermophilus,
Ammospermophilus, Cynomys, and Marmota (Giboulet et al.
1997; Steppan et al. 2004). Although commonly classified in
the tribe Marmotini (Thorington and Hoffmann 2005),
chipmunks and Asian rock-squirrels are sometimes segregated
into a distinct tribe, Tamiini (Black 1963; Giboulet et al. 1997).
For convenience throughout this paper we use the tribal
designator Marmotini to refer to Spermophilus (sensu lato),
Ammospermophilus, Cynomys, and Marmota but not to
tamiinin genera. The tribe Marmotini is 1 (along with Xerini
and Protoxerini) of 3 tribes (4 if Tamiini is recognized) in the
subfamily Xerinae (Thorington and Hoffmann 2005).
Recently, molecular analyses based on the mitochondrial
gene cytochrome b (Harrison et al. 2003; Herron et al. 2004)
have suggested that Cynomys is phylogenetically nested within
the taxonomic bounds of the genus Spermophilus as currently
recognized. Marmots, the largest of the ground squirrels, were
traditionally considered to be an early phylogenetic offshoot in
the tribe, but evidence from molecular studies also nested them
within the phylogenetic scope of Spermophilus (Giboulet et al.
1997; Harrison et al. 2003; Herron et al. 2004; Steppan et al.
1999; Thomas and Martin 1993). As with Cynomys and
Marmota, analyses of molecular data indicate that Ammosper-
mophilus also is subsumed phylogenetically within the intra-
generic radiation comprised by the current taxonomic bounds
of Spermophilus (Harrison et al. 2003; Herron et al. 2004).
Both Harrison et al. (2003) and Herron et al. (2004) declined
to tackle the question of appropriate generic boundaries and
nomenclature in Marmotini in light of the paraphyly of
Spermophilus. Delineation of revised generic boundaries in
this case ideally requires not only a well-resolved phylogeny,
but also an overview of available generic names and their type
species, critical considerations of generic definitions and
content, and revised morphological diagnoses of recognized
genera. Herein, we provide this background in order to present
April 2009 271HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
a fresh generic-level classification of squirrels in the tribe
Marmotini.
MATERIALS AND METHODS
Our study draws upon the unparalleled collections of North
American ground squirrels in the United States Biological
Surveys collection, stored at the United States National
Museum of Natural History (USNM) at the Smithsonian
Institution in Washington, D.C. We collected data on standard
external dimensions from original specimen labels, and
calculated selected external proportions based on these data.
These external measurements are abbreviated here as total
length (TL), head and body length (HBL), tail length (TV), and
hind-foot length (HFL). Ear (pinna) length (EL) was not
available for all specimens.
Craniodental variables were measured by the authors with
handheld calipers to the nearest 0.01 mm while viewing the
skull under a stereoscopic microscope as necessary. Single-
tooth measurements are measured across dental crowns. All
measurements of length are reported in millimeters.
For our craniometric comparisons, we measured 33
craniodental variables on 2 intact adult female skulls for every
species of Spermophilus (sensu lato), Ammospermophilus, and
Cynomys (i.e., following the taxonomy of Thorington and
Hoffmann [2005]) available at USNM. All North American
species in these genera are represented in our analyses, along
with 6 of the 14 currently recognized Eurasian species. We
chose fully adult females (with basioccipital?basisphenoid
suture fused and teeth fully erupted and lightly but not
excessively worn) to render comparisons consistent with
respect to age and sex, and because females were better
represented in the USNM collections for several rarer taxa. For
widespread species we generally chose specimens of the
nominate subspecies for inclusion (Appendix I). We measured
the following craniodental variables (as defined and illustrated
in Fig. 1): condylobasal length (CBL); zygomatic breadth (ZB);
breadth of braincase (BBC); height of braincase, measured
from the basioccipital plane to the crown of the braincase
(HBC); rostral breadth (RB); length of nasals (LN); width of
nasals (WN); interorbital breadth (IOB); postorbital breadth
(POB); length of diastema (LD); length of incisive foramina
FIG. 1.?Limits of craniodental measurements employed in our study. Skull drawing of Marmota monax modified from Bezuidenhout and
Evans (2005).
272 JOURNAL OF MAMMALOGY Vol. 90, No. 2
(? anterior palatal foramina; LIF): width of incisive foramina
(WIF); width across infraorbital foramen (WAIF); length of
auditory bulla (LAB); width of auditory bulla (WAB); width of
auditory bullae across external auditory meati (WAAM); width
of palate at P3 (WPP3); width of palate at M1 (WPM1); width
of palate at M3 (WPM3); length of bony palate (LBP);
extension of bony palate (LEBP); postpalatal length (PPL);
length of maxillary toothrow (LMTR); length of angular
process (LAP); and length of condyloid process (LCP). Dental
variables measured (all upper teeth) included width of incisors
(WI), length of incisors (LI), depth of incisors (DI), width of P3
(WP3), length of P4 (LP4), width of 2nd molar (WM2), width
of 3rd molar (WM3), and length of 3rd molar (LM3). USNM
catalog numbers and localities for examined specimens are
provided in Appendix I.
Qualitative comparisons of external and craniodental
anatomy and variation within and among species and genera
were made via direct comparisons of specimens and series at
USNM (the whole collection was utilized). Our comparisons of
Eurasian taxa were bolstered by additional information on
external measurements, cranial measurements, and qualitative
morphology extracted from literature. To clarify and bolster the
generic boundaries we advocate here, our morphological and
morphometric comparisons emphasize differences between
genera, as well as similarities among species classified together
in each genus. To this end, we test and explore craniometric
distinctions between generic clades elucidated by molecular
analyses of the cytochrome-b gene (Fig. 2) primarily with
discriminant function analysis. These and all other statistical
analyses were performed with the software package Statistica
6.0 (Statsoft Inc., Tulsa, Oklahoma).
RESULTS
Molecular Analyses
Analyses by Herron et al. (2004) and Harrison et al. (2003),
both based on the cytochrome-b gene, recovered 11 clades
that we recognize here as genera based on our clarifying
morphological and taxonomic investigations. We discuss and
label them here by number and name (in no special order) with
explicit reference to the results of Herron et al. (2004), whose
analyses included more species and were published more
recently than those of Harrison et al. (2003). Our numbering of
these recovered clades is not linked to the numbering scheme
used by Herron et al. (2004). We have refigured the phylo-
genetic topologies recovered in their paper (Fig. 2) both from
maximum-parsimony analyses and Bayesian analyses. To
indicate the robustness of resolution, we abbreviate maximum-
parsimony bootstrap percentages as MP and Bayesian posterior
probabilities as BPP (e.g., 100 MP, 100 BPP). Our purpose in
reviewing these clades recovered by Herron et al. (2004) is to
link generic names to each of these assemblages by identifying
the type species of available generic-level names and the
phylogenetic affiliations of those species. For convenience,
species are referenced in the section immediately below only by
specific epithet.
Clade 1 (Notocitellus).? In both trees (Fig. 2), a well-
supported clade (99 MP, 100 BPP) consisting of annulatus (the
type species of Notocitellus A. H. Howell, 1938) and adocetus
was recovered as the sister group to Ammospermophilus (albeit
with weak support). These 2 genera are highly divergent from
all other genera in the tribe Marmotini. This clade corresponds
to Howell?s (1938) original taxonomic definition and concept
of Notocitellus, except that Howell recognized this grouping at
the subgeneric level.
Clade 2 (Ammospermophilus).? In both trees (Fig. 2),
species traditionally classified in the genus Ammospermophi-
lus, along with Notocitellus, were recovered as the most
divergent lineage among ground squirrels formerly classified in
Spermophilus (Howell 1938). The 4 sampled species, including
leucurus, the type species of Ammospermophilus, were
recovered as a monophyletic clade in both trees, albeit with
weaker support than for any other genus that we recognize in
this paper (85 MP, 90 BPP).
Clade 3 (Otospermophilus).? In both trees (Fig. 2), the
species variegatus (the type species of Otospermophilus
Brandt, 1844), beecheyi, and atricapillus form a well-supported
monophyletic group (100 MP). These species are traditionally
(and most often exclusively?as done by Howell 1938)
classified together in the subgenus (or genus) Otospermophilus.
A few authors have lumped the species of Notocitellus and
Otospermophilus together under a single genus or subgenus
(Bryant 1945; Hall 1981; Miller 1924)?an arrangement not
supported by the cytochrome-b data.
Clade 4 (Callospermophilus).? In both trees (Fig. 2), the
species lateralis (the type species of Callospermophilus
Merriam, 1897), saturatus, and madrensis form a well-
supported monophyletic group (100 MP). These species are
traditionally and exclusively classified together in the subgenus
(or genus) Callospermophilus. In both trees, this clade is
recovered as the sister lineage to clade 3 (Otospermophilus)
with relatively high support (88 MP, 100 BPP).
Clade 5 (Xerospermophilus).? In both trees (Fig. 2), the
species mohavensis (the type species of Xerospermophilus
Merriam, 1892), tereticaudus, spilosoma, and perotensis form
a well-supported monophyletic group (87 MP, 100 BPP). Two
of these species (mohavensis and tereticaudus) have been
traditionally and exclusively classified together in the subgenus
(or genus) Xerospermophilus; the 2 others (spilosoma and
perotensis) are usually associated with the subgenus (or genus)
Ictidomys, the type species of which falls in clade 8. In
addition, spilosoma is paraphyletic in relation to perotensis. In
both trees, Cynomys is recovered as the sister group to clade 5
(Xerospermophilus).
Clade 6 (Cynomys).? In both trees (Fig. 2), the 5 species
of Cynomys Rafinesque, 1817, including ludovicianus (Ord,
1815), the type species of Cynomys, are recovered as a mono-
phyletic group with high support (100 MP, 100 BPP). These
species are traditionally and exclusively classified together in
the genus Cynomys. As noted, in both trees Cynomys is
recovered as sister group to clade 5 (Xerospermophilus).
Clade 7 (Poliocitellus).? In both trees (Fig. 2), the species
franklinii (type species of Poliocitellus A. H. Howell, 1938) is
April 2009 273HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
recovered in an isolated position. It is weakly supported (,50
MP, 93 BPP) as sister to a group that includes clades 5 and 6
(Xerospermophilus and Cynomys). This species is traditionally
classified exclusively in the subgenus Poliocitellus.
Clade 8 (Ictidomys).? In both trees (Fig. 2), the species
tridecemlineatus (the type species of Ictidomys J. A. Allen,
1877), mexicanus (the type species of the later name
Ictidomoides Mearns, 1907), and parvidens (see generic
account of Ictidomys, below) form a well-supported mono-
phyletic group (100 MP, 100 BPP). These species are
traditionally classified together in the subgenus (or genus)
Ictidomys. In both trees, this clade is recovered as the sister
lineage to a group that consists of clades 5?7, albeit with
variable support (54 MP, 98 BPP). However, Ictidomys also
has included Xerospermophilus spilosoma and X. perotensis,
which appear in clade 5.
FIG. 2.?Phylogeny of Marmotini proposed by Herron et al. (2004) based on analyses of complete sequences of the cytochrome-b gene.
Harrison et al. (2003) presented very similar results. Multiple terminal branches representing the same taxon have been collapsed for simplification
in some cases, and some identifications have since been modified. The shaded taxa represent the 3 genera that have not been traditionally
recognized in Spermophilus. A) Maximum parsimony: ??Strict consensus of all 208 equally optimal trees based on unweighted maximum
parsimony search?? (Herron et al. 2004:1022). Bootstrap percentages for nodes of taxonomic interest (generic and supergeneric) are shown
following Herron et al. (2004). B) Bayesian analysis: ??Majority rule consensus phylogram (with branch lengths averaged over all trees) resulting
from Bayesian phylogenetic analysis using a GTR ? G ? I model of evolution?? (Herron et al. 2004:1024). Posterior probabilities ??estimated from
a total of 4 million post-burn-in generations (from four independent runs)?? are provided for nodes of taxonomic interest (generic and supergeneric)
following Herron et al. (2004:1024).
274 JOURNAL OF MAMMALOGY Vol. 90, No. 2
Clade 9 (Marmota).? In both trees (Fig. 2), the 14 sampled
species of Marmota, including marmota (Linnaeus, 1758), the
type species of Marmota Blumenbach, 1779, are recovered as
a monophyletic group with high support (100 MP, 100 BPP).
These species are traditionally and exclusively classified
together in the genus Marmota. The phylogenetic position of
this clade differs markedly between the 2 trees, but in both trees
it is nested within the taxonomic boundaries of Spermophilus
as currently defined (Thorington and Hoffmann 2005).
Clade 10 (Urocitellus).? In both trees (Fig. 2), a group of
12 species including undulatus (the type species of Urocitellus
Obolenskij, 1927), armatus, beldingi, brunneus, canus,
columbianus, elegans, mollis (including the subspecies idaho-
ensis [see Herron et al. 2004]), parryii, richardsonii, town-
sendii, and washingtoni are recovered as a monophyletic group
with high support (90 MP, 99 BPP). These species are
traditionally classified in the nominate subgenus Spermophilus
along with a diverse group of Eurasian ground squirrels (but
the type species of Spermophilus is citellus, which falls in clade
11). The phylogenetic position of this clade differs markedly
between the 2 trees.
Clade 11 (Spermophilus sensu stricto).?In both trees (Fig. 2),
a group of 11 sampled Eurasian species including citellus
(the type species of Spermophilus F. Cuvier, 1825, and the
unavailable generic name Citellus Oken, 1816), fulvus (the type
species of the later name Colobotis Brandt, 1844), dauricus,
erythrogenys, major, pallidicauda, pygmaeus (including musi-
cus), relictus (and ralli [see Harrison et al. 2003]), suslicus, and
xanthoprymnus are recovered as a monophyletic group with
high support (92 MP, 100 BPP). These species are traditionally
classified in the nominate subgenus Spermophilus along with
a diverse group of primarily North American ground squirrels
associated with clade 10, but these groupings are not recovered
as each others? closest relatives. The phylogenetic position of
Spermophilus (clade 11) differs markedly between the 2 trees.
Craniometric Analyses
In a preliminary discriminant function analysis comparing all
small to medium-sized members of the tribe Marmotini (as
delineated above), Cynomys, Ammospermophilus, and Notoci-
tellus clearly diverge from remaining clades in combination
along the 1st and 2nd canonical variates (CV1 and CV2),
reflecting consistent differences amongst these groupings in
craniodental shape, expressed especially in incisor, cheekteeth,
FIG. 3.?Discriminant function analysis illustrating craniometric
differentiation in the smaller-bodied genera of the tribe Marmotini
(i.e., excluding Marmota, markedly larger than all other lineages),
including Cynomys (Cy) and Ammospermophilus (A), phenetically
distinctive lineages traditionally separated generically from other
North American ground squirrels, and generic lineages previously
included within Spermophilus sensu lato?Spermophilus (S), Uroci-
tellus (U), Poliocitellus (P), Ictidomys (I), Callospermophilus (C),
Xerospermophilus (X), Otospermophilus (O), and Notocitellus (N)
(Table 1). Cynomys, Ammospermophilus, and Notocitellus (denoted
by circled clusters) separate widely from other lineages in concert
along the 1st and 2nd roots, whereas the other lineages form a more-
or-less linear continuum along the 1st axis (see Fig. 5).
TABLE 1.?Underlying statistics (variable coefficients and correla-
tions, eigenvalues, and cumulative varance of canonical variates) of
a discriminant function analysis (see Fig. 3) illustrating craniometric
differentiation among genera within the tribe Marmotini (excluding
Marmota). See ??Materials and Methods?? for variable names.
Standardized coefficients Correlations
Variable CV1 CV2 CV3 CV1 CV2 CV3
CBL 0.694 1.420 4.634 0.049 0.222 0.021
ZB 1.086 1.914 1.102 0.097 0.286 0.027
BBC 0.242 2.151 2.013 0.016 0.201 0.018
HBC 0.742 0.544 0.352 0.043 0.222 0.044
RB 1.446 0.001 0.508 0.047 0.171 0.066
LN 1.409 0.609 0.273 0.101 0.188 0.005
WN 1.144 0.053 0.120 0.106 0.140 0.032
IOB 0.020 0.102 0.642 0.031 0.201 0.016
POB 1.171 0.500 0.008 0.055 0.116 0.022
LD 1.612 1.374 0.834 0.028 0.125 0.082
LIF 0.250 0.341 0.524 0.059 0.163 0.044
WIF 0.324 0.136 0.447 0.029 0.138 0.098
WAIF 0.787 0.385 0.185 0.146 0.231 0.023
LAB 0.632 0.315 0.459 0.027 0.247 0.048
WAB 0.289 0.340 0.350 0.074 0.256 0.158
WAAM 1.290 0.220 2.886 0.088 0.273 0.116
WPP3 0.607 0.097 0.897 0.057 0.227 0.050
WPM1 1.316 0.147 0.862 0.043 0.081 0.006
WPM3 0.003 0.133 0.275 0.005 0.003 0.062
LBP 0.499 0.155 2.119 0.054 0.196 0.055
LEBP 0.336 0.128 0.096 0.015 0.116 0.010
PPL 0.505 0.520 1.498 0.046 0.227 0.002
LMTR 0.387 0.138 1.264 0.119 0.271 0.013
WI 1.720 0.943 0.455 0.091 0.179 0.044
LI 0.348 0.404 0.252 0.019 0.341 0.085
DI 1.964 1.692 0.005 0.040 0.362 0.055
WP3 1.342 0.119 0.691 0.255 0.320 0.097
LP4 0.437 0.432 0.130 0.111 0.236 0.010
WM2 0.681 0.905 0.248 0.122 0.386 0.000
WM3 0.846 0.574 1.054 0.154 0.343 0.011
LM3 0.692 0.020 2.039 0.169 0.303 0.098
LAP 0.578 0.114 0.307 0.131 0.310 0.062
LCP 0.210 1.127 2.000 0.067 0.256 0.086
Eigenvalue 49.953 15.615 5.901
Cumulative
variance 0.610 0.800 0.872
April 2009 275HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
bullae, nasal, zygomatic, and mandibular dimensions (Fig. 3;
Table 1). We elected to exclude the species of Marmota?
already very well known for their very large and diagnostically
distinctive skulls and teeth?from our craniometric contrasts.
Cynomys possesses the most distinctive skull features of the
medium-sized ground squirrels and diverges from all other
groupings along CV2 based especially on proportions of the
incisors, premolars, molars, and auditory bullae; zygomatic
width and the length of the angular process of the dentary; and
relative divergence of the toothrows (Figs. 3 and 4; Table 1; cf.
Howell 1938). Ammospermophilus and Notocitellus, which
may be sister genera (Fig. 2), cluster together separately from
other genera previously associated within Spermophilus along
CV1 due in part to their proportionally small teeth (especially
P3), shorter and narrower nasals, and shorter angular process of
the dentary.
FIG. 4.?Skull of Cynomys ludovicianus, the type species of
Cynomys (USNM 191444, adult female, Boulder County, Colorado,
United States). From top to bottom: dorsal view of cranium, ventral
view of cranium, lateral view of cranium, lateral view of mandible,
and dorsal view of mandible. Scale bar ? 10 mm.
FIG. 5.?Discriminant function analysis highlighting craniometric
distinctions between generic lineages within Marmotini, excluding the
genera Marmota, Cynomys, Ammospermophilus, and Notocitellus (see
Fig. 3). All lineages achieve discrimination along the first 2 canonical
variate roots (CV1 is shown along the horizontal axis in both plots),
reflecting consistent differences in craniodental shape, with the
exception of Callospermophilus and Ictidomys, ecomorphologically
similar but phylogenetically unrelated genera (Fig. 2) that segregate
along the 3rd canonical variate primarily on the basis of slight
differences in size and comparative robustness (Table 2).
276 JOURNAL OF MAMMALOGY Vol. 90, No. 2
In continuing comparisons excluding Cynomys, Ammosper-
mophilus, and Notocitellus, most of the remaining clades
recovered in the molecular analyses are clearly discriminated
from one another in combination along CV1 and CV2,
reflecting consistent and diagnostic distinctions in cranial
shape (e.g., Fig. 5; Table 2).
Although Otospermophilus and Callospermophilus are
apparently closely related (Fig. 2; Harrison et al. 2003; Herron
et al. 2004), these lineages are highly divergent morphologi-
cally. Our analyses of both qualitative morphology and
craniometrics (Fig. 5) indicate that these taxa form discrete
groupings that should be regarded as distinct at the genus level.
Our craniometric results credit indications by Herron et al.
(2004) that 2 species traditionally classified in the subgenus
Ictidomys (spilosoma and perotensis) bear consistent cranio-
dental resemblance to species traditionally classified in
Xerospermophilus (mohavensis and tereticaudus). The pre-
vious classification of perotensis and spilosoma within
Ictidomys represents convergent achievement of an external
striping pattern rather than a close evolutionary relationship
(see generic account of Ictidomys, below).
In our analyses, Callospermophilus and Ictidomys are
recovered as strikingly similar in craniometrics. Although
rather deeply distinct lineages phylogenetically (Fig. 2), they
do not segregate along CV1 and CV2, but instead segregate
only along the 3rd canonical variate (CV3) on the basis of
minor but consistent differences in overall size and robustness
(Fig. 5; Table 2). The remarkable craniometric similarity of
these unrelated lineages of ground squirrels has gone pre-
viously unremarked in the literature but may betray similarities
in ecomorphology and lifestyle.
Consistent craniometric distinctions documented between
these clades of Marmotini complement differences in body
size, external proportions, pelage coloration and ornamenta-
tion, and qualitative cranial distinctions that also diagnose these
distinctive lineages (see generic accounts, below).
SYSTEMATICS
We propose that ground squirrels currently allocated to the
genus Spermophilus (sensu Thorington and Hoffmann 2005)
can be classified in 8 genera, as defined, diagnosed, and
discussed in the following generic accounts. For completeness
of reference, we provide the full citations for each of the
original descriptions of these 8 generic-level names in the
Literature Cited (Allen 1877; Brandt 1844; Cuvier 1825;
Howell 1938; Merriam 1892, 1897; Obolenskij 1927).
Genus Notocitellus A. H. Howell
Tropical Ground Squirrels (Figs. 6 and 7)
Notocitellus A. H. Howell, 1938, N. Am. Fauna, 56:44. Type
species Spermophilus annulatus Audubon and Bachman,
1842.
Content.?Two species of Notocitellus are recognized: N.
adocetus Merriam, 1903, and N. annulatus Audubon and
Bachman, 1842.
Notocitellus adocetus (Merriam, 1903). Proc. Biol. Soc. Wash.,
16:79.
N. a. adocetus (Merriam, 1903:79). Type locality: La Salada,
40 miles [64 km] south of Uruapan, Michoacan, Mexico.
[arceliae (Villa-R., 1942) is a synonym.]
N. a. infernatus (Alvarez and Ram??rez-P., 1968:183). Type
locality: 14 km al norte de El Infiernillo, Michoacan
[Mexico].
Notocitellus annulatus (Audubon and Bachman, 1842). J.
Acad. Nat. Sci. Phila., 8:319.
N. a. annulatus (Audubon and Bachman, 1842:319). Type
locality: western prairies. Restricted by A. H. Howell
(1938:163) to Manzanillo, Colima, Mexico.
TABLE 2.?Underlying statistics (variable coefficients and correla-
tions, eigenvalues, and cumulative varance of canonical variates) of
a discriminant function analysis (see Fig. 5) illustrating craniometric
differentiation among genera within the tribe Marmotini (excluding
Marmota, Cynomys, Ammospermophilus, and Notocitellus). See
??Materials and Methods?? for variable names.
Standardized coefficients Correlations
Variable CV1 CV2 CV3 CV1 CV2 CV3
CBL 0.982 4.832 3.750 0.031 0.022 0.293
ZB 2.641 2.605 1.685 0.004 0.019 0.297
BBC 2.002 2.969 0.256 0.045 0.026 0.283
HBC 1.550 0.628 2.036 0.044 0.048 0.227
RB 2.120 0.352 0.360 0.005 0.049 0.194
LN 0.359 0.091 1.496 0.009 0.023 0.311
WN 1.332 0.325 0.303 0.015 0.026 0.233
IOB 0.703 0.589 0.380 0.088 0.019 0.290
POB 0.811 0.215 0.446 0.070 0.022 0.009
LD 0.441 2.577 1.258 0.022 0.077 0.314
LIF 1.114 0.598 0.206 0.045 0.003 0.312
WIF 0.770 0.393 0.192 0.031 0.087 0.198
WAIF 1.586 0.163 0.306 0.052 0.027 0.288
LAB 0.726 0.375 1.244 0.087 0.032 0.063
WAB 0.458 0.815 0.575 0.016 0.144 0.188
WAAM 2.932 2.056 1.194 0.000 0.095 0.323
WPP3 0.049 1.649 1.328 0.020 0.047 0.212
WPM1 1.437 0.907 1.525 0.027 0.021 0.289
WPM3 0.067 0.148 0.283 0.060 0.075 0.340
LBP 0.831 2.389 1.264 0.005 0.037 0.236
LEBP 0.549 0.200 0.993 0.004 0.037 0.051
PPL 0.927 1.072 0.251 0.036 0.005 0.290
LMTR 0.531 1.486 1.210 0.012 0.009 0.234
WI 1.802 0.607 0.677 0.005 0.051 0.300
LI 0.525 0.536 0.107 0.085 0.084 0.258
DI 2.041 0.188 0.392 0.139 0.063 0.215
WP3 1.777 0.571 0.789 0.127 0.102 0.224
LP4 0.092 0.047 0.190 0.020 0.004 0.226
WM2 0.613 0.487 0.323 0.009 0.007 0.274
WM3 0.694 1.127 1.279 0.026 0.012 0.315
LM3 0.127 2.278 0.931 0.056 0.093 0.261
LAP 0.244 0.321 0.009 0.016 0.054 0.223
LCP 0.609 1.490 0.314 0.008 0.055 0.290
Eigenvalue 29.953 9.550 4.649
Cumulative
variance 0.598 0.789 0.882
April 2009 277HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
N. a. goldmani (Merriam, 1902:69). Type locality: Santiago,
Tepic, Mexico.
Etymology.?The name Notocitellus is derived from the
Greek noto meaning the back and the Latin citellus for ground
squirrel (Jaeger 1955).
Diagnosis.?The species of Notocitellus differ conspicuously
from all other ground squirrels both in external appearance
and craniodental conformation. There are only 3 pairs of teats
(1 axillary and 2 inguinal pairs, verified here for both species),
a trait unique among the tribe Marmotini (Table 3)?all other
genera have 4?6 pairs, usually 5 (Moore 1961). Both species of
Notocitellus have a grizzled black and tan dorsum, borne of
dark?pale banding in the hairs of the dorsal pelage (Fig. 6). The
dorsal fur is coarse, rather than soft as in most other members
of the tribe Marmotini. Externally, the species of Notocitellus
FIG. 6.?Representative skins (all adult females) of the species of Notocitellus (1, 2) and Ammospermophilus (3?7): 1) N. annulatus, USNM
32662, Manzanillo, Colima, Mexico; 2) N. adocetus, USNM 126123, La Salada, Michoacan, Mexico; 3) A. interpres, USNM 119910, San
Andreas Mountains, New Mexico, United States; 4) A. insularis, USNM 146782, Espiritu Santo Island, Baja California Sur, Mexico; 5)
A. leucurus, USNM 61157, San Diego County, California, United States; 6) A. harrisii, USNM 59861, Quitovaquito, Arizona, United States; 7)
A. nelsoni, USNM 54655, Tipton, California, United States. We note that subsequent to our preparation of figures and analyses, Alvarez-
Castan?eda (2007) argued convincingly that insularis should be recognized as a subspecies of A. leucurus.
278 JOURNAL OF MAMMALOGY Vol. 90, No. 2
FIG. 7.?Representative skulls of the respective type species of Ammospermophilus (1) and Notocitellus (2): 1) A. leucurus, USNM 60834,
adult female, San Diego County, California, United States; 2) N. annulatus, USNM 44596, adult female, Manzanillo, Colima, Mexico. From top
to bottom: dorsal view of cranium, ventral view of cranium, lateral view of cranium, lateral view of mandible, and dorsal view of mandible. Scale
bar ? 10 mm.
April 2009 279HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
T
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280 JOURNAL OF MAMMALOGY Vol. 90, No. 2
are distinctive in having relatively long tails, measuring .75%
of head?body length (78?113%, usually about 90%), which are
distichous (as in tree squirrels) rather than being either bushy or
thinly clad (as in other Marmotini); slender bodies; long and
narrow feet; and ears that are large but distinctively short and
broadly rounded (proportionally larger than, but resembling
in shape, the pinnae of Ammospermophilus). Apart from its
distinctively rounded ears, this apomorphous character suite
(in the context of xerine ecomorphology) is convergent on the
body plan of arboreal tree squirrels (i.e., the tribes Nannosciur-
ini, Tamiasciurini, and Sciurini) and we suggest that it reflects
the semiarboreal lifestyle of Notocitellus, unique among the
tribe Marmotini (see below). The cranium of Notocitellus
features a blunt rostrum with very short incisive foramina;
opisthodont, anteroposteriorly deep incisors (usually with very
deep-red enamel faces); weakly expanded, relatively gracile
zygomata; large and broad auditory bullae; a rounded brain-
case; closed supraorbital foramina; and a relatively small P4
and a simple and smaller P3 (less than one-fourth of the size of
P4), which is a unique combination of traits within the tribe
Marmotini (Fig. 7). The molars are relatively brachyodont,
with the parastyle ridge on M1 and M2 rising to join the
protocone without abrupt change in direction (Howell 1938).
Of the ground squirrel genera previously classified within
Spermophilus (sensu lato), only Notocitellus and Otospermo-
philus have relatively long tails (Table 3), and previous authors
have hypothesized a phylogenetic alliance between these 2
lineages based on morphology (cf. Harrison et al. 2003; Howell
1938; Miller 1924), but this is not supported by molecular
phylogenetic analyses (Fig. 2). The skulls of the 2 genera are
superficially similar, but skulls of Notocitellus can be easily
discerned from those of Otospermophilus in having a blunter
rostrum, proportionally much wider interorbital region, much
bigger bullae, proportionally smaller molars, very small P3,
short incisive foramina, and heavier incisors. These and other
distinctions are reflected in their multivariate morphometric
separation in our discriminant function analysis (Fig. 3).
Distribution.?The genus Notocitellus is endemic to west-
central Mexico (Fig. 8), where it is represented by 2 species
that differ conspicuously in body size and have parapatric or
marginally overlapping geographic distributions (Howell
1938). The distribution of N. adocetus extends from eastern
Jalisco and Michoacan to northern Guerrero, including both
humid lowland habitats and more arid areas on the Mexican
Plateau, up to 3,000 m (Best 1995a). N. annulatus is restricted
to lowlands (sea level to approximately 1,200 m) from southern
Nayarit to northwestern Guerrero (Best 1995b). The distribu-
tions of these 2 species may overlap in northern Guerrero
(Howell 1938).
Cytogenetics.?The karyotype of N. adocetus consists of
32 chromosomes, with a fundamental number (number of
autosomal arms) of 60 (Birney and Genoways 1973). The
karyotype of N. annulatus has not been studied (Best 1995b).
Ecology.?Notocitellus is endemic to Mexico, and both
species occupy unique habitats relative to other species of
Marmotini. N. adocetus lives in upland desert shrub communities
such as mesquite woodlands with columnar cactus. It also
occupies low tropical deciduous forest in some areas. Much of
this habitat has recently been converted to low-level agriculture,
and N. adocetus has become adapted to many of these habitats as
well. This species is common in rocky areas along canyon sides,
and also can be found along stone walls in agricultural areas (Best
1995a). N. annulatus occurs along the Pacific coast in tropical
deciduous forest that is seasonally quite arid (Best 1995b). N.
annulatus is equally at home in areas converted to a variety of
agricultural uses. Both species are omnivorous, but feed mainly
on a variety of fruits, seeds, and green vegetation. In some areas,
they are considered a pest on crops. Both species are apparently
more arboreal than other Marmotini, climbing in low trees and
shrubs in search of food. They are diurnal, with most activity in
the morning hours (Valde?z Alarco?n and Te?llez-Giro?n 2005).
FIG. 8.?Geographic distributions of the tropical ground squirrels
(Notocitellus), rock squirrels (Otospermophilus), and golden-mantled
ground squirrels (Callospermophilus) (after Hall 1981).
April 2009 281HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
Comments.?Phylogenetic analyses of cytochrome-b ally
Notocitellus as the sister lineage to Ammospermophilus (Fig. 2;
Harrison et al. 2003; Herron et al. 2004)?an alliance
complemented by shape-related morphometric similarity
(Figs. 3 and 7) and similarities in the shape of the ears, despite
the otherwise extremely different external appearance of the
2 genera (Fig. 6). However, the craniometric resemblance
between Notocitellus and Ammospermophilus might be
credited largely to characteristics possibly primitive for the
tribe Marmotini, including a narrow infraorbital foramen,
inflated bullae, stout incisors, and a small P3.
Genus Otospermophilus Brandt
Rock Squirrels (Figs. 9 and 10)
Otospermophilus Brandt, 1844, Bull. Cl. Phys.-Math. Acad.
Imp. Sci. St. Pe?tersbourg, 2:379. Type species: Sciurus
grammurus Say, 1823 [? S. variegatus Erxleben, 1777].
FIG. 9.?Representative skins (all adult females) of the species of Otospermophilus (1?3) and Callospermophilus (4?6): 1) O. variegatus,
USNM 91718, Santa Rosa, Guanajuato, Mexico; 2) O. atricapillus, USNM 146185, Comondu, Baja California Sur, Mexico; 3) O. beecheyi, USNM
63960, Half Moon Bay, California, United States; 4) C. madrensis, USNM 95348, Sierra Madre, Chihuahua, Mexico; 5) C. saturatus,
USNM 89001, Trout Lake, Washington, United States; 6) C. lateralis, USNM 158507, Beaver Mountains, Utah, United States.
282 JOURNAL OF MAMMALOGY Vol. 90, No. 2
FIG. 10.?Representative skulls of the respective type species of Otospermophilus (left) and Callospermophilus (right): left) O. variegatus,
USNM 46434, adult female, Atemajac, Jalisco, Mexico; right) C. lateralis, USNM 497843, adult female, Gunnison County, Colorado, United
States. From top to bottom: dorsal view of cranium, ventral view of cranium, lateral view of cranium, lateral view of mandible, and dorsal view of
mandible. Scale bar ? 10 mm.
April 2009 283HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
Content.?Three allopatric species are recognized, with
synonyms as delineated by Thorington and Hoffmann (2005):
O. atricapillus (W. Bryant, 1889), O. beecheyi (Richardson,
1929), and O. variegatus (Erxleben, 1777). Type localities as
given below are cited largely based on the authority of
Thorington and Hoffmann (2005) and Howell (1938).
Distinctions between O. beecheyi and O. atricapillus, which
are morphologically very similar, deserve renewed study.
Otospermophilus atricapillus (W. Bryant, 1889). Proc. Calif.
Acad. Sci., Ser. 2, 2:26. Type locality: Comondu, Lower
California [Baja California Sur, Mexico].
Otospermophilus beecheyi (Richardson, 1829). Fauna Boreali-
Amer.,1:170.
O. b. beecheyi (Richardson, 1829:170). Type locality: ??neighbor-
hood of San Francisco and Monterey, in California.??
Restricted by Grinnell (1933) to Monterey, Monterey Co.,
California, USA.
O. b. douglasii (Richardson, 1829:170). Type locality: bank of
the Columbia River, Oregon.
O. b. fisheri (Merriam, 1893:133). Type locality: S. Fork Kern
River, 3 mi. above Onyx, California.
O. b. nesioticus (Elliot, 1904:263). Type locality: Santa
Catalina Island, California.
O. b. nudipes (Huey, 1931:18). Type locality: Hanson Laguna,
Sierra Juarez, 5,200 ft., Baja California, Mexico.
O. b. parvulus (A. H. Howell, 1931:160). Type locality:
Shepherd Canyon, Argus Mts., California.
O. b. rupinarum (Huey, 1931:17). Type locality: Catavina,
Baja California, Mexico.
O. b. sierrae (A. H. Howell, 1938:153). Type locality: Emerald
Bay, Lake Tahoe, El Dorado Co., California.
Otospermophilus variegatus (Erxleben, 1777). Syst. Regn.
Anim., 1:421.
O. v. buckleyi (Slack, 1861:314). Type locality: Packsaddle
Mountain, Llano Co., Texas.
O. v. couchii (Baird, 1855:332). Type locality: Santa Catarina,
few mi. W Monterey, Nuevo Leo?n, Mexico.
O. v. grammurus (Say, 1823:72). Type locality: Purgatory
River, near the mouth of Chacuaco Creek, Las Animas Co.,
Colorado. [juglans (V. Bailey, 1913) and tiburonensis
(Jones and Manning, 1989) are synonyms.]
O. v. robustus (Durrant and Hansen, 1954:264). Type locality:
Pass Creek, Deep Creek Mountains, 8,000 ft., Juab Co.,
Utah.
O. v. rupestris (J. A. Allen, 1903:595). Type locality: R??o
Sest??n, northwestern Durango.
O. v. tularosae (Benson, 1932:336). Type locality: French?s
Ranch, 5,400 ft., 12 mi. NW Carrizozo, Lincoln Co., New
Mexico.
O. v. utah (Merriam, 1903:77). Type locality: foot of the
Wasatch Mts., near Ogden, Weber Co., Utah.
O. v. variegatus (Erxleben, 1777:421). Type locality: not
designated; restricted by Nelson (1898:898) to ??Valley of
Mexico near the City of Mexico?? [Distrito Federal,
Mexico]. [buccatus (Lichtenstein, 1830) and macrourus
(Bennett, 1833) are synonyms.]
Etymology.?The name Otospermophilus is derived from the
Greek otos meaning ear, spermatos for seed, and phileo for
love (Jaeger 1955).
Diagnosis.?The species of Otospermophilus are easily
recognized; they are relatively large squirrels, with long and
bushy tails, pale crescent markings on the sides of the neck and
shoulders, and relatively very large ears (Fig. 9). The fur is
short and sleek, with the dorsal hairs banded dark brown and
buff, generating an impression of grizzling or flecking in the
pelage. There is usually middorsal darkening in the pelage,
extending from the nose or crown to the midback. There are 5
or 6 pairs of mammae. The skull is relatively large but not
particularly wide, and features relatively large molars, a small
P3, orthodont or slightly opisthodont incisors, long incisive
foramina, very large auditory bullae, a rounded braincase, and
open supraorbital foramina?a combination of traits distinctive
among the tribe Marmotini (Fig. 10). The molars are relatively
brachyodont, with the parastyle ridge on M1 and M2 rising to
join the protocone without an abrupt change in direction (cf.
Howell 1938). As in Notocitellus, P3 is simple and very small,
generally less than 25% the size of P4. The skull superficially
resembles that of N. annulatus and Poliocitellus (to which
Otospermophilus bears little external resemblance), but differs
from the latter in its less elongate rostrum and incisive
foramina, more expansive braincase, smaller P3, heavier
molars, and proportionally larger auditory bullae.
Distribution.?The 3 species of Otospermophilus are
disjunctly distributed across the western United States and
Mexico (Fig. 8). O. atricapillus is endemic to the Baja
California Peninsula. O. beecheyi occurs in the far western
United States, from south-central Washington and western
Oregon in the north, throughout much of California and
southwestern Nevada, to northwestern Baja California in the
south. O. variegatus is found in Idaho, Utah, southern Nevada,
and western Texas, extending south to central Mexico (Botello
et al. 2007; Groves et al. 1988; Howell 1938).
Cytogenetics.?The karyotypes of O. variegatus and O.
beecheyi have a diploid number of 38 and a fundamental
number of 72 (Nadler 1966b; Oaks et al. 1987). The karyotype
of O. atricapillus has not been studied (Alvarez-Castan?eda
et al. 1996).
Ecology.?Otospermophilus is a genus of southwestern arid
habitats, extending up into mountainous regions as high as 3,000 m.
The 3 species are large ground squirrels that form colonies in
suitable habitats. O. atricapillus, the Baja California rock
squirrel, occupies montane oases in soils of volcanic origin
(Alvarez-Castan?eda et al. 1996; Castro Arellano and Ceballos
2005). The California ground squirrel, O. beecheyi, also uses
rocky habitats, but also has adapted to agricultural habitats in the
rich soils of the coastal mountain valleys (Cole and North 1999;
Linsdale 1946; Losa Salas 2005). Rock squirrels, O. variegatus,
are the most widespread, and use rocky habitats over a wide
range of general habitat types from the lower slopes of the Rocky
Mountains down through much of central Mexico (Valde?z
284 JOURNAL OF MAMMALOGY Vol. 90, No. 2
Alarco?n and Ceballos 2005b; Schmidt 1999). Although typically
terrestrial, Otospermophilus will occasional climb trees and
shrubs in search of food. All are colonial?perhaps a natural
adaptation to their spotty local distributions dictated by
surrounding terrain. All have benefited from anthropogenic
modifications to their habitats that involve raising crops, which
can augment their natural food supplies of fruit and seeds.
Comments.?Phylogenetic analyses of cytochrome-b conclu-
sively ally Otospermophilus and Callospermophilus as sister
lineages (Harrison et al. 2003; Herron et al. 2004), a result that
echoes some previous hypotheses based on morphological and
chromosomal comparisons (cf. Black 1963; Bryant 1945;
Gerber and Birney 1968; Gromov et al. 1965; Nadler 1966a).
Although these lineages are clearly very closely related, their
respective monophyly (Harrison et al. 2003; Herron et al. 2004)
and profound morphological divergence (Figs. 9 and 10) argue
for their recognition as separate genera, rather than congeneric
subgenera (Gromov et al. 1965; Harrison et al. 2003; Herron
et al. 2004). Externally, both Otospermophilus and Callospermo-
philus share proportionally very large ears and paired crescent
markings over the shoulders (Fig. 9), which we regard as likely
synapomorphic in light of the molecular evidence for their
close relationship. Qualitative cranial features are similar in the
2 genera (Howell 1938), but the skulls show little immediate
resemblance in overall shape, at least as compared to other
Marmotini (Figs. 3, 5, and 10). Skulls of Otospermophilus are
much larger than those of Callospermophilus, and feature
proportionally longer rostra, larger bullae, and heavier teeth,
among other distinctions (Howell 1938).
Genus Callospermophilus Merriam
Golden-Mantled Ground Squirrels (Figs. 9 and 10)
Callospermophilus Merriam, 1897, Proc. Biol. Soc. Wash.,
11:189. Type species: Sciurus lateralis Say, 1823.
Content.?Three species are recognized, with synonyms as
delineated by Thorington and Hoffmann (2005): C. lateralis
(Say, 1823), C. madrensis (Merriam, 1901), and C. saturatus
(Rhoads, 1895). Type localities as given below are cited largely
based on the authority of Thorington and Hoffmann (2005) and
Howell (1938).
Callospermophilus lateralis (Say, 1823). In Long, Account
Exped. Pittsburgh to Rocky Mtns., 2:46.
C. l. arizonensis (V. Bailey, 1913:130). Type locality: Little
Spring, 8,250 ft., San Francisco Mtn., Arizona.
C. l. bernardinus (Merriam, 1898:134). Type locality:
San Bernardino Peak, San Bernardino Co., California.
[brevicauda (Merriam, 1893; not Brandt, 1843) is a
synonym.]
C. l. castanurus (Merriam, 1890:19). Type locality: Park City,
Wasatch Mts., Summit Co., Utah. [caryi (A. H. Howell,
1917) is a synonym.]
C. l. certus (Goldman, 1921:232). Type locality: north base of
Charleston Peak, Clark Co., Nevada.
C. l. chrysodeirus (Merriam, 1890:19). Type locality: Fort
Klamath, Klamath Co., Oregon.
C. l. cinerascens (Merriam, 1890:20). Type locality: Helena,
4,500 ft., Lewis and Clark Co., Montana.
C. l. connectens (A. H. Howell, 1931:161). Type locality:
Homestead, Oregon.
C. l. lateralis (Say, 1823:46). Type locality: near Can?on City.
Restricted by Merriam (1905:163) to Arkansas River, about
26 mi. [42 km] below Canyon City, Fremont Co., Colorado
(USA).
C. l. mitratus (A. H. Howell, 1931:161). Type locality: South
Yolla Bolly Mtn., California.
C. l. tescorum (Hollister, 1911:2). Type locality: head of
Moose Pass, branch Smoky River, 7,000 ft., Alberta
[Canada].
C. l. trepidus (Taylor, 1910:283). Type locality: head Big
Creek, 8,000 ft., Pine Forest Mts., Humboldt Co., Nevada.
C. l. trinitatus (Merriam, 1901:126). Type locality: E. of Hoopa
Valley, 5,700 ft., Trinity Mts., California.
C. l. wortmani (J. A. Allen, 1895:335). Type locality: Kinney
Ranch, Bitter Creek, Sweetwater Co., Wyoming.
Callospermophilus madrensis (Merriam, 1901). Proc. Wash.
Acad. Sci., 3:563. Type locality: Sierra Madre, near Guadalupe
y Calvo, Chihuahua, Mexico (7,000 feet [2,134 m] altitude).
Callospermophilus saturatus (Rhoads, 1895). Proc. Acad. Nat.
Sci. Phila., 47:43. Type locality: Lake Kichelos [? Keechelus],
Kittitas Co., Wash[ingto]n, (elevation 8,000 feet [2,438 m]).
Etymology.?Callospermophilus is derived from the Greek
kallos for beauty, spermatos for seed, and phileo for love
(Jaeger 1955).
Diagnosis.?The species of Callospermophilus are extremely
distinctive externally relative to other Marmotini, a fact
captured in part in their common name?the golden-mantled
ground squirrels. Overall dorsal coloration is pale brown to
reddish brown, and in all 3 species, 2 paired, cream-colored
longitudinal lines extend along the back from the base of each
ear to the rump. These lines are highlighted on either side
throughout their length by thinner lines of dark brown or
blackish fur, creating a striking pattern that contrasts with the
duller brown fur-tipping of the middorsum and the buff to gray
coloration of the sides of the body (Fig. 9). The head and
forequarters are usually set apart from the rest of the body
by their bolder orange-brown or golden-brown hue. Overall
coloration and patterning of Callospermophilus resemble those
of Ammospermophilus (Fig. 6), but differ in that blackish lines
fringe the pale longitudinal lines (lacking in Ammospermophi-
lus), the pale longitudinal lines extend anteriorly to the base
of the ear (extending anteriorly to base of shoulders in
Ammospermophilus), and the head and forequarters are
markedly redder than the rest of the body (generally not so
in Ammospermophilus). Externally, these genera also are easily
discriminated by body size (larger in Callospermophilus) and
in the size of the pinna (comparatively much larger in
Callospermophilus). Species of Callospermophilus are small
to medium-sized (Howell 1938; Table 3), and have a somewhat
hefty or plump, rather than slender, appearance, and longer
and less glossy pelage than most other Marmotini. The tail
April 2009 285HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
is usually quite short, averaging less than half the head?body
length, and the ears are proportionally large (Table 3). Females
have 4 or 5 pairs of mammae (Moore 1961). The rather
generalized skull features orthodont to slightly opisthodont
incisors; relatively long and narrow incisive foramina; a rostrum
of moderate length; and incisors, cheek teeth, and auditory
bullae of moderate size, as reflected in part by the intermediate
position of Callospermophilus along both CV1 and CV2 (Fig.
5) in discriminant function comparisons of the genera of
Marmotini contrasted in this paper (Fig. 5). P3 is relatively
small. Compared to other Marmotini, the postorbital processes
are relatively long and comparatively very slender. The molars
are relatively brachyodont with no abrupt change of direction
in the parastyle ridge on M1 and M2, and the upper incisors are
relatively slender, but comparatively broad, and not distinctly
recurved (cf. Howell 1938).
Distribution.?The 3 species of Callospermophilus are
distributed allopatrically in western North America, from
southern Canada to northern Mexico (Fig. 8). C. madrensis is
restricted to the states of Chihuahua and Durango in
northwestern Mexico (Best and Thomas 1991; Servin et al.
1996). C. saturatus occurs in the Cascade Mountains of
western Washington in the United States and southwestern
British Columbia in Canada (Leung and Cheng 1997). C.
lateralis is widely distributed in montane regions of western
North America from central British Columbia to southern New
Mexico and the Columbia River south to southern California
and Nevada (Howell 1938).
Cytogenetics.?Callospermophilus lateralis has a diploid
number of 42 and a fundamental number of 78 (Nadler 1966b).
The karyotypes of C. madrensis and C. saturatus have not been
determined.
Ecology.?Callospermophilus comprises 3 closely related
allopatric species that occupy mountain meadows and
surrounding habitats in western North America. They are all
inhabitants of midelevation habitats from about 1,000 m to
4,000 m. C. lateralis occupies sagebrush, open woodlands,
scrubby forest edge habitats, disturbed areas such as logged or
burned sites, mountain meadows, and rocky slopes in the
mountainous parts of its range, which includes much of the
Rocky Mountains and Sierra Nevada (Armstrong 1999; Bartels
and Thompson 1993). C. saturatus inhabits krumholtz and
talus in alpine habitats, forests, meadows, and sagebrush
habitats within its range (Trombulak 1988, 1999). C. madrensis
is found in pine forests at elevations above 3,000 m, on slopes
with vegetative cover consisting of Juniperus, Populus,
Pseudotsuga, and Pinus (Valde?z Alarco?n 2005; Best and
Thomas 1991). Callospermophilus species are omnivorous,
feeding on seeds, fruits, leaves, fungi, flowers, stems, insects
(including eggs, larvae, pupae, and adults), small mammals,
carrion, eggs, and nestling birds. They tend to be solitary, but
will aggregate at food sources. They hibernate during the
winter months, and are active throughout the daylight hours in
the summer.
Comments.?The close phylogenetic relationship between
the morphologically divergent genera Callospermophilus and
Otospermophilus (Fig. 2) was illustrated by the molecular
phylogenetic studies of Harrison et al. (2003) and Herron et al.
(2004). The discriminant function analyses ally Ictidomys and
Callospermophilus as craniometrically similar (Figs. 3 and 5),
although they are not closely related among Marmotini. This
result suggests an overall ecomorphological similarity in these
2 boldly patterned genera of Marmotini, which are parapatri-
cally distributed across their geographic ranges (Figs. 8 and
11). The parapatric distributions of these genera are no doubt
influenced by their distinct (but abutting) habitat associations.
Despite their association in our craniometric analyses,
Ictidomys and Callospermophilus can be immediately discrim-
inated on the basis of qualitative craniodental characters
(Bryant 1945; Howell 1938) and external traits, including
pelage patterning, pinna size, and tail length (Table 3).
Genus Spermophilus F. Cuvier
Old World Ground Squirrels (Fig. 12)
Citellus Oken, 1816:842. Unavailable name; see International
Commission on Zoological Nomenclature 1956.
Spermophilus F. Cuvier, 1825. Dents des Mammiferes, p. 255.
Type species: Mus citellus Linnaeus, 1766:80.
FIG. 11.?Geographic distributions of pygmy ground squirrels
(Xerospermophilus), lined ground squirrels (Ictidomys), and Frank-
lin?s ground squirrel (Poliocitellus?after Hall 1981).
286 JOURNAL OF MAMMALOGY Vol. 90, No. 2
Citillus Lichtenstein, 1830:plate 31. Incorrect subsequent
spelling of Citellus Oken, 1816.
Spermatophilus Wagler, 1830:22. Incorrect subsequent spell-
ing of Spermophilus F. Cuvier, 1825.
Colobotis Brandt, 1844:366. Bull. Cl. Phys.-Math. Acad. Imp.
Sci. St. Pe?tersbourg, 2. Type species: Arctomys fulvus
Lichtenstein, 1823:119.
Otocolobus Brandt, 1844:382. Apparent lapsus for Colobotis
Brandt, 1844. Not Otocolobus Brandt, 1842 (a felid).
Colobates Milne-Edwards, 1874:157. Incorrect subsequent
spelling of Colobotis Brandt, 1844.
Mamspermophilus Herrera, 1899:5. Unavailable name because
it is based on zoological formulae (Palmer 1904).
Content.?The delineation of this genus embraces the
Eurasian members of the genus Spermophilus as traditionally
recognized (e.g., Corbet 1978; Ellerman and Morrison-Scott
1966; Gromov et al. 1965; Hoffmann et al. 1993; Ognev 1947;
Thorington and Hoffmann 2005), with the exception of 2
species here classified in Urocitellus?Urocitellus undulatus,
a species endemic to eastern Eurasia, and U. parryii, a mostly
North American species that extends westward from Alaska
into Siberia (the genus Urocitellus is otherwise restricted to
North America). We follow Thorington and Hoffmann (2005),
as supported and updated by Gu?ndu?z et al (2007a, 2007b),
Ozkurt et al. (2007), Tsvirka et al. (2006b), Ermakov et al.
(2006), and Nikol?skii et al. (2007), in recognizing 14 species
FIG. 12.?Representative skulls of the type species of Spermophilus (1), a North American species of Urocitellus (2), and the type species of
Poliocitellus (3): 1) S. citellus, USNM 327292, adult female, Kagithane Dere, Istanbul, Turkey; 2) U. columbianus, USNM 66668, adult female,
Nelson, British Columbia, Canada; 3) P. franklinii, USNM 192733, adult female, Brown?s Valley, Minnesota, United States. From top to bottom:
dorsal view of cranium, ventral view of cranium, lateral view of cranium, lateral view of mandible, and dorsal view of mandible. Scale bar? 10 mm.
April 2009 287HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
of Spermophilus: S. alashanicus Bu?chner, 1888; S. brevicauda
Brandt, 1843; S. citellus (Linnaeus, 1766); S. dauricus Brandt,
1843; S. erythrogenys Brandt, 1841; S. fulvus (Lichtenstein,
1823); S. major (Pallas, 1778); S. pallidicauda (Satunin, 1903);
S. pygmaeus (Pallas, 1778) (now including S. musicus
Me?ne?tries, 1832, as a subspecies [see Ermakov et al. 2006;
Nikol?skii et al. 2007]); S. ralli (Kuznetsov, 1948); S. relictus
(Kashkarov, 1923); S. suslicus (Gu?ldenstaedt, 1770); S.
taurensis Gu?ndu?z, Jaarola, Tez, Yeniyurt, Polly, and Searle,
2007 (cf. Ozkurt et al. 2007; Gu?ndu?z et al. 2007b); and S.
xanthoprymnus (Bennett, 1835). Thorington and Hoffmann
(2005) provided lists of subspecies and synonyms, which we
largely follow here. Type localities are cited largely based on
the authority of Thorington and Hoffmann (2005), Ellerman
and Morrison-Scott (1966), and Ognev (1947). Interspecific
cytogenetic variability (see ??Cytogenetics,?? below), apparent
species-level paraphyly (e.g., Fig. 2), and the capacity for
interspecific hybridization recorded across several species
(Denisov 1961; Denisov and Smirnova 1976; Spiridonova
et al. 2005; Tsvirka et al. 2006a) all indicate the need for
continuing studies of alpha-level taxonomy in the genus.
Spermophilus alashanicus Bu?chner, 1888. Wiss. Res. Prze-
walski Cent. Asien Zool. I:(Sa?ugeth.):11. Type locality:
southern Ala Shan [China]. [dilutus (Formozov, 1929);
obscurus Bu?chner, 1888; and siccus (G. M. Allen, 1925) are
synonyms.]
Spermophilus brevicauda Brandt, 1843. Bull. Acad. Sci., St.
Pe?tersbourg, p. 364. Type locality: habitat, ut videtur, in
provincis Altaicis australiorbis versus lacum Balchasch [Zaisan
Basin, Kazakhstan; see Ellerman and Morrison-Scott (1966)].
[carruthersi (Thomas, 1912); intermedius (Brandt, 1844);
ilensis (Belyaev, 1945); saryarka (Selevin, 1937); and selevini
(Argyropolu, 1941) are synonyms.]
Spermophilus citellus (Linnaeus, 1766). Syst. Nat., 12th ed.,
1:80.
S. c. citellus (Linnaeus, 1766:80). Type locality: Austria;
restricted by Martino and Martino (1940) to Wagram,
Niederosterreich. [citillus (Pallas, 1779) is an incorrect
subsequent spelling.]
S. c. gradojevici (Martino, 1929:76). Type locality: Djerdjelija
[? Djevdjelija], Macedonia. [karamani (Martino, 1940) and
macedonicus Fraguedakis-Tsolis and Ondrias, 1977, are
synonyms.]
S. c. istricus (Calinescu, 1934:106). Type locality: Munteni,
eastern Romania. [laskarevi (Martino, 1940) is a synonym.]
S. c. martinoi (Peshchev, 1955:290), Type locality: Rhodopen
Mts., Bulgaria. [balcanicus (Markov, 1957) and thracius
(Mursaloglu, 1964) are synonyms.]
Spermophilus dauricus Brandt, 1843:379. Type locality: circa
Torei lacum exiccatum Dauuriae et ad Onon Bursa rivum
(Torei-Nor (Lake), Chitinsk. Obl., Russia). [mongolicus (Milne-
Edwards, 1867); ramosus (Thomas, 1909); umbratus (Thomas,
1908); and yamashinae (Kuroda, 1939) are synonyms.]
Spermophilus erythrogenys Brandt, 1841:43. Type locality:
vicinity of Barnaul (Altaisk Krai, Russia). [brunnescens (Belyaev,
1943); heptneri (Vasil?eva, 1964); and ungae (Martino, 1923)
are synonyms.]
Spermophilus fulvus (Lichtenstein, 1823). Naturh. Abh. Evers-
mann?s Reise, p. 119.
S. f. fulvus (Lichtenstein, 1823:119). Type locality: near the
Kuvandzhur River, east of Mugodzhary Mountains, north of
Aral Sea [Kazakhstan]. [concolor (Fischer, 1829); concolor
I. Geoffroy, 1831; giganteus (Fischer, 1829); maximus
(Pallas, 1778); and nanus (Fischer, 1829) are synonyms.]
S. f. hypoleucos (Satunin, 1909:1). Type locality: Kutschan,
northern Persia [Iran]. [parthianus (Thomas, 1915) is
a synonym.]
S. f. oxianus (Thomas, 1915:422). Type locality: 50 mi. SW
Bokhara, Russian Turkestan [Turkmenistan?Uzbekistan
border]. [nigrimontanus (Antipin, 1942) is a synonym.]
Spermophilus major (Pallas, 1778:125). Type locality:
steppe near Samara (Kuibyshev, Kuibyshevsk. Obl., Russia).
[argyropuloi (Bazhanov, 1947); rufescens (Keyserling and
Blasius, 1840); and selevini (Argyropulo, 1941) are synonyms.]
Spermophilus pallidicauda (Satunin, 1903). Ezheg. Zool.
Muz., Akad. Nauk, St. Petersburg, 7:5?6. Type locality:
vicinity of Lake Khulu-Nur, Ullyn Bulyk, Baidarak river,
Mongolian Atlai [Mongolia, Gobi-Altai].
Spermophilus pygmaeus (Pallas, 1778). Nova Spec. Quad. Glir.
Ord., p. 122.
S. p. brauneri (Martino, 1917:3). Type locality: Igren District,
Ecaterinoslav Govt., Crimea [Ukraine]. [kalabuchovi (Ognev,
1937) is a synonym.]
S. p. herbicolus (Martino, 1916:278). Type locality: Aktya-
binsk [? Aktyubinsk] steppes, northern Kirghizia, Russian
Asia [Kazakhstan]. [atricapilla (Orlov, 1927) [not W.
Bryant, 1889]; herbidus (Martino, 1915) [nomen nudum];
and septentrionalis (Obolenskij, 1927) are synonyms.]
S. p. mugosaricus (Lichtenstein, 1823:119). Type locality:
Mugodshary Mountains [Kazakhstan]. [kazakstanicus
(Goodwin, 1935) and nikolskii (Heptner, 1934) are
synonyms.]
S. p. musicus Me?ne?tries, 1832:21. Type locality: il habite le
Caucase sur les montagnes le plus e?leve?es et pas loin des
nieges e?ternalles. Restricted to Ush-Kulan [Georgia] (see
Ognev 1947). [boehmii (Krassovskii, 1932); magisteri
(Heptner, 1948); saturatus (Ognev, 1947) [not Rhoads,
1895]; and typicus (Satunin, 1908) are synonyms.]
S. p. pygmaeus (Pallas, 1778:122). Type locality: ??Maximos et
paene dixerim monstrosos Citillo?s passim ad inferiorum
laikum in campis squalidis.?? Restricted by Ognev (1947) to
??lower reaches of the Ural River,?? Indersk [Kazakhstan].
[arenicola (Rall, 1935) [infrasubspecific, unavailable; not
arenicola (A. H. Howell, 1938)]; binominatus (Ellerman,
1940); ellermani (Harris, 1944); flavescens (Pallas, 1779);
orlovi (Ellerman, 1940); pallidus (Orlov and Fenyuk, 1927)
[not J. A. Allen, 1874]; planicola (Satunin, 1909); ralli
288 JOURNAL OF MAMMALOGY Vol. 90, No. 2
(Heptner, 1948) [replacement name for arenicola Rall, but
apparently preoccupied by ralli Kuznetsov, 1948 (see
discussion by Thorington and Hoffmann [2005])]; satunini
(Sveridenko, 1922); and saturatus (Ognev, 1947) [not
Rhoads, 1895] are synonyms.]
Spermophilus ralli (Kuznetsov, 1948). Zveri Kirgizii [Animals
of Kirgiziya, Moscow Soc. of Naturalists], p. 39. Type locality:
Tip iz kotlovinny Oz. Issyk-Kul? [basin of Lake Issyk-Kul,
Kyrgyzstan]. The correct name for this species is in some doubt
(Thorington and Hoffmann 2005:810).
Spermophilus relictus (Kashkarov, 1923). Trans. Turk. Sci.
Soc., 1:185. Type locality: Kara-Bura Gorge and Kumysh-
Tagh Gorge in the Talus Ala Tau [Talassk. Obl., Kyrgyzstan].
Spermophilus suslicus (Gu?ldenstaedt, 1770). Nova Comm.
Acad. Sci. Petropoli, 14:389.
S. s. boristhenicus (Pusanov, 1958:206). Type locality:
between the rivers Dnestr and Bug, Ukraine.
S. s. guttatus (Pallas, 1770:566). Type locality: rivers Pyana
and Sura, Russia. [guttulatus Schinz, 1845, and leucopictus
(Dondorff, 1792) are synonyms.]
S. s. suslicus (Gu?ldenstaedt, 1770:389). Type locality: in
campis vastissimus tanaicensibus precipue urbes et Tambov
[Voronezh area, Voronezhsk. Obl., Russia]. [averini
(Migulin, 1927); meridioccidentalis (Migulin, 1927); odes-
sana Nordmann, 1842; ognevi (Reshetnik, 1946); and
volhynensis (Reshetnik, 1946) are synonyms.]
Spermophilus taurensis Gu?ndu?z, Jaarola, Tez, Yeniyurt, Polly,
and Searle, 2007. Mol. Phylogenet. Evol., 43:929. Type
locality: Akseki, Yarpuz (378089N, 318539E), 111 km E of
the city of Antalya, Turkey. [torosensis Ozkurt et al., 2007, is
a synonym.]
Spermophilus xanthoprymnus (Bennett, 1835). Proc. Zool. Soc.
Lond., 1835:90. Type locality: Erzurum (Turkey). [schmidti
(Satunin, 1908) is a synonym.]
Etymology.?Spermophilus is derived from the Greek sper-
matos for seed, and phileo for love (Jaeger 1955).
Diagnosis.?Species of Spermophilus lack the diagnostic
pelage patterning or immediately discernible head?body to tail
proportions that characterize members of the genera Ammo-
spermophilus, Notocitellus, Callospermophilus, Otospermo-
philus, and Ictidomys, and differ from each of these genera in
other ways described in our revision. Species of Spermophilus
are cranially smaller than species of Cynomys and Marmota,
and differ consistently from those phenetically distinctive
genera in cranial shape and fur color patterning (Howell 1938).
The pelage is usually longer and less sleek than in most other
Marmotini. Most species of Spermophilus are larger than the
species of Xerospermophilus, and have proportionally smaller
bullae, longer and more parallel-sided rostra, and longer
postorbital processes compared to members of that genus.
Species of Spermophilus can be distinguished from Polio-
citellus in having a proportionally wider braincase and
zygomata, narrower interorbital region, heavier postorbital
processes, shorter and narrower incisive foramina, less reduced
P3, shorter and more parallel-sided rostra, more gracile and less
opisthodont incisors, and a more elongate meatal portion of the
auditory bulla (Fig. 12). Species of Spermophilus (sensu
stricto) are morphologically most similar to species of
Urocitellus, which they resemble especially in external
morphology?a resemblance attested by their traditional
classification together in the subgenus Spermophilus (sensu
lato) (e.g., Hall 1981; Howell 1938; Thorington and Hoffmann
2005). Nevertheless, species of the subgenus Spermophilus
(sensu stricto) can be firmly diagnosed against species of
Urocitellus by a suite of consistent craniometric and qualitative
cranial distinctions. In Spermophilus, the interorbital region is
narrowed relative to the postorbital width, the braincase is
somewhat higher-domed, the palate is proportionally wider
between M1 and M1 but narrower between M3 and M3, the
incisive foramina are wider, the maxillary diastema is propor-
tionally longer, the mesopterygoid fossa is distinctively
narrowed, the occipital condyles are less laterally expansive,
the larger cheek teeth (molars and P4) are proportionally more
massive but P3 is proportionally slightly smaller, the inflated
portion of the auditory bulla is proportionally larger but the
meatal portion is distinctly smaller, the mesopterygoid fossa is
distinctively narrowed, and the upper incisor enamel is whitish
to very pale yellow (more distinctly orange in Urocitellus).
Many of these key differences are reflected in the clear
multivariate discrimination between Spermophilus and Uroci-
tellus in our craniometric analysis (Fig. 5; Table 2).
Distribution.?The geographic scope of the genus Spermo-
philus, as newly delineated here, is restricted to Eurasia. The
distributional range of the genus (Fig. 13) is based on Ognev
(1947), Thorington and Hoffmann (2005), Hoffmann and
Smith (2008), and Zhang et al. (1997). S. alashanicus is
endemic to north-central China (Ningxia, Gansu, Qinghai, and
Nei Mongol). S. brevicauda occupies appropriate habitat south
and westward along the Tien Shan Mountains to the vicinity of
Almaty on both sides of the Kazakhstan?Chinese (Xinjiang)
border. S. pallidicauda occurs in Mongolia and the adjacent
Nei Mongol Autonomous Region and Xinjiang in China. S.
dauricus ranges over Russian Transbaikalia, Mongolia, and
northeastern China. S. ralli occupies the eastern Tien Shan
Mountains and adjacent valleys of Xinjiang (China), Kyrgyzstan,
and Kazakhstan, from the Terskii-Alatau in the southeast to the
Ketmen in the northeast. S. relictus is found in the western Tien
Shan Mountains of Kyrgyzstan and southeastern Kazakhstan.
S. erythrogenys occurs in eastern Kazakhstan and southwestern
Siberia. S. fulvus is broadly distributed from northern
Kazakhstan south through Uzbekistan, western Tajikistan,
and Turkmenistan to northern Iran, west to northern Afghani-
stan, and east into western Xinjiang in China (according to
Thorington and Hoffmann [2005], although Hoffmann and
Smith [2008] did not include fulvus in the Chinese fauna).
S. major occurs in steppe habitats between the Volga and Irtysh
rivers in Russia and northern Kazakhstan. S. citellus ranges
from southeastern Germany, the Czech Republic, and south-
western Poland through southeastern Europe to European
Turkey, Moldova, and western Ukraine. S. pygmaeus occurs
from southwestern Ukraine to Georgia, northwestern Uzbeki-
April 2009 289HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
stan, and Kazakhstan. S. suslicus ranges over the steppes of
eastern and southern Europe, including Poland, eastern
Romania, and the Ukraine north to the Oka River and east to
the Volga River in Russia. S. xanthoprymnus occupies
appropriate habitats in Transcaucasia, Turkey, Syria, and
Israel. A newly described species, S. taurensis, occurs in the
Taurus Mountains in southwestern Anatolia (Gu?ndu?z et al.
2007a; the newly described S. torosensis Ozkurt et al., 2007, is
a synonym [Gu?ndu?z et al. 2007b]).
Cytogenetics.?Karyotypes for most species are recorded
in the literature: S. pallidicauda (diploid number [2N] ? 34),
S. suslicus (2N ? 34?36; fundamental number [FN] ? 64?68),
S. brevicauda (2N ? 36; FN ? 68), S. dauricus (2N ? 36;
FN ? 68), S. erythrogenys (2N ? 36; FN ? 68), S. fulvus (2N ?
36; FN ? 68), S. pygmaeus (2N ? 36; FN ? 68), S. ralli (2N ?
36; FN ? 68), S. relictus (2N ? 36; FN ? 68), S. alashanicus
(2N ? 38; FN ? 60), S. citellus (2N ? 40; FN ? 66?74), S.
xanthoprymnus (2N ? 40?42; FN ? 64?78), and S. taurensis
(2N ? 40?Arslan 2005; Gu?ndu?z et al. 2007a; Liapunova and
Vorontsov 1970; Robinson and Hoffmann 1975; Tsvirka et al.
2006a). Sporadic hybridization may occur where S. major
occurs sympatrically with S. fulvus, S. pygmaeus, S. eryth-
rogenys, or S. brevicauda, or where S. pygmaeus overlaps with
S. erythrogenys or S. suslicus (Denisov 1961; Denisov and
Smirnova 1976; Spiridonova et al. 2005; Thorington and
Hoffmann 2005). A stable zone of hybridization apparently
exists between S. major and S. erythrogenys in the Tobol?Ishim
interfluvial area in Russia (Spiridonova et al. 2005). Tsvirka et al.
(2006a) reported hybridization between S. pallidicauda and
S. alashanicus at several localities in Mongolia.
Ecology.?The species of Spermophilus are primarily
restricted to open plains, steppes, and tundra regions of the
Palearctic. In forested regions, they are restricted to edge
habitats. In the southern parts of the range, some species
inhabit semidesert regions. Many of the species are strongly
colonial, occupying suitable habitat over large areas (Hoffmann
and Smith 2008; Ognev 1947). All are diurnal, and most are
active in the morning once the sun warms the area slightly, then
retreat to underground dens during the heat of the day, to
reemerge late in the day for another feeding bout. Preferred
food items include seeds, shoots, stems, leaves, tubers, and
fruits of a wide variety of plains and grassland species
(Hoffmann and Smith 2008; Ognev 1947). All of the northern
species are hibernators, and in some areas the active season
may be relatively short. In some areas they cause some
depredation to agricultural crops. Several species of Spermo-
philus also are reservoirs for bubonic plague (Ognev 1947).
Comments.?The name Citellus Oken, 1816, was often used
for this genus in the past. Hershkovitz (1949) argued
successfully that Citellus Oken is not an available generic
name and that Spermophilus F. Cuvier, 1825, is the appropriate
name for the genus (International Commission on Zoological
Nomenclature 1956). Gromov et al. (1965) retained Colobotis
as a distinct Eurasian subgenus, containing S. brevicauda, S.
erythrogenys, S. fulvus, and S. major. This subgeneric
classification is not supported by phylogenetic analyses of
cytochrome-b sequence data (Fig. 2; Harrison et al. 2003;
Herron et al. 2004) and in the absence of more detailed studies,
we do not advocate recognition of subgenera within Spermo-
philus (sensu stricto).
Genus Ictidomys J. A. Allen
Lined Ground Squirrels (Figs. 14 and 15)
Ictidomys J. A. Allen, 1877, in Coues and Allen, Monogr. N.
Am. Rodentia, p. 821. Type species: Sciurus tridecemli-
neatus Mitchill, 1821.
Ictidomoides Mearns, 1907, Bull. U. S. Nat. Mus., 56:328.
Type species: Sciurus mexicanus Erxleben, 1777.
Content.?We recognize 3 species in Ictidomys: I. tride-
cemlineatus (Mitchill, 1821), I. parvidens (Mearns, 1896), and
I. mexicanus (Erxleben, 1777). Two other ground squirrel
species, Xerospermophilus spilosoma (Bennett, 1833) and
Xerospermophilus perotensis (Merriam, 1893), have tradition-
ally been allied with tridecemlineatus and mexicanus in the
subgenus Ictidomys (e.g., Cothran et al. 1977; Hall 1981;
Howell 1938), but are not immediately related to those species
(Harrison et al. 2003; Herron et al. 2004), and are here
classified in Xerospermophilus. We suggest that the taxon
FIG. 13.?Geographic distributions of the Old World ground squirrels (Spermophilus) and Holarctic ground squirrels (Urocitellus?after Hall
1981; Hoffmann and Smith 2008; Ognev 1947).
290 JOURNAL OF MAMMALOGY Vol. 90, No. 2
I. parvidens (Mearns, 1896), usually recognized as a subspecies
of I. mexicanus (but markedly smaller than and disjunctly
distributed relative to that taxon), deserves species-level recog-
nition within Ictidomys (and see Fig. 2; Harrison et al. 2003;
Herron et al. 2004). Subspecies and synonyms are as delineated
by Thorington and Hoffmann (2005); and type localities, as
given below, are cited largely based on the authority of
Thorington and Hoffmann (2005) and Howell (1938).
Ictidomys mexicanus (Erxleben, 1777). Syst. Regn. Anim.,
1:428. Type locality: ??In nova Hispania??? Restricted by
Mearns (1896:443) to Toluca, Mexico.
Ictidomys parvidens (Mearns, 1896). Proc. U. S. Nat. Mus.,
XVIII:443. Type locality: Fort Clark, Kinney Co., Texas.
Ictidomys tridecemlineatus (Mitchill, 1821). Med. Repos.
(N.Y.), (n.s.), 6(21):248.
I. t. alleni (Merriam, 1898:71). Type locality: near head of
Canyon Creek, 8000 ft., west slope Bighorn Mts., Wyoming.
I. t. arenicola (A. H. Howell, 1928:213). Type locality:
Pendennis, Kansas.
I. t. blanca (Armstrong, 1971:533). Type locality: 5 mi. W
Antonito, Conejos Co., Colorado.
I. t. hollisteri (V. Bailey, 1913:131). Type locality: Elk Valley,
8,000 ft., Mescalero Indian Reservation, Sacramento Mts.,
New Mexico.
I. t. monticola (A. H. Howell, 1928:214). Type locality: Marsh
Lake, 9,000 ft., White Mts., Arizona.
FIG. 14.?Representative skins (all adult females) of the species of Xerospermophilus (1?4) and Ictidomys (5, 6): 1) X. perotensis, USNM
54273, Perote, Veracruz, Mexico; 2) X. mohavensis, USNM 28743, Salt Wells Valley, California, United States; 3) X. tereticaudus, USNM
117343, Needles, California, United States; 4) X. spilosoma, USNM 78998, Chicalote, Aguascalientes, Mexico; 5) I. mexicanus, USNM 79019,
Silas, Guanajuato, Mexico; 6) I. tridecemlineatus, USNM 250129, White County, Indiana, United States.
April 2009 291HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
FIG. 15.?Representative skulls of the respective type species of Xerospermophilus (1) and Ictidomys (2): 1) X. mohavensis, USNM 40849,
adult female, Salt Wells Valley, California, United States; 2) I. tridecemlineatus, USNM 228976, adult female, Rib Hill, Wisconsin, United States.
From top to bottom: dorsal view of cranium, ventral view of cranium, lateral view of cranium, lateral view of mandible, and dorsal view of
mandible. Scale bar ? 10 mm.
292 JOURNAL OF MAMMALOGY Vol. 90, No. 2
I. t. olivaceus (J. A. Allen, 1895:337). Type locality: Custer,
Custer Co., Black Hills, South Dakota [misspelled as
olivaceous by Hoffmann et al. (1993) and Thorington and
Hoffmann (2005)].
I. t. pallidus (J. A. Allen, 1874:291). Type locality: plains of
lower Yellowstone River, Montana.
I. t. parvus (J. A. Allen, 1895:337). Type locality: Uncom-
pahgre Indian Reservation, 20 mi. northeast of Ouray,
Uintah Co., Utah.
I. t. texensis (Merriam, 1898:71). Type locality: Gaines-
ville, Cooke Co., Texas. [badius (Bangs, 1899) is a
synonym.]
I. t. tridecemlineatus (Mitchill, 1821:248). Type locality:
??region bordering the sources of the river Mississippi??;
restricted to ??Central Minnesota?? by Allen (1895:338).
[hoodii (Sabine, 1822) is a synonym.]
Etymology.?The name Ictidomys is derived from the
Greek words for weasel and mouse, referring to the slender,
musteline body-form of these species.
Diagnosis.?Species of Ictidomys are easily identified on the
basis of their dorsal pelage patterning. Dorsal spotting is more
pronounced in the species of Ictidomys than in any other genus
of Marmotini, such that well-defined linear rows of spots or
stripes or both run anteroposteriorly along the length of the
body, from the crown of the head to the proximal base of the
tail. This pattern is fundamentally different from patterning in
other Marmotini, including the golden-mantled ground squir-
rels (Callospermophilus), the other boldly marked genus
formerly lumped within Spermophilus, and some populations
of X. perotensis and X. spilosoma, in which pale dorsal spotting
is much less pronounced and not clearly arranged in linear rows
(Fig. 14). In I. tridecemlineatus, this patterning is boldly
marked and the rows include continuous lines as well as rows
of spots, whereas in I. mexicanus and I. parvidens, the dorsal
spots are less distinct and form broken lines. The pelage is
usually short and sleek. The external ears are relatively small
and the tail is fringed terminally with pale hairs. The tail is
more than half as long as the head?body (usually shorter in
other smaller-bodied genera of Marmotini; Table 3; Fig. 14).
The skull is distinctively narrowed and features stout and
markedly opisthodont upper incisors, an elongate and distinc-
tively downward-sloping rostrum, small cheek teeth separated
from the incisors by a proportionally expansive diastema,
delicate postorbital processes, a strikingly narrowed braincase,
and relatively small and laterally compressed auditory bullae
(Fig. 15). The metaloph of P4 is not continuous. The small
molars are less hypsodont than in Spermophilus and Uroci-
tellus, and the parastyle ridge on M1 and M2 joins the
protocone with an abrupt change in direction (cf. Howell
1938). The species of Ictidomys also share similarities in
bacular morphology (Bryant 1945).
Distribution.?Ictidomys occurs throughout the prairies,
grasslands, and arid country of central North America (Fig.
11). I. tridecemlineatus is widely distributed across the Great
Plains from central Texas and eastern New Mexico north to
northeastern Utah, south-central Canada, and central Ohio. I.
parvidens is found in the southern Great Plains from southeastern
New Mexico through western Texas south into northeastern
Mexico. I. mexicanus occurs in central Mexico (Hall 1981;
Howell 1938; Streubel and Fitzgerald 1978b; Thorington and
Hoffmann 2005; Young and Jones 1982). Zimmerman and
Cothran (1976) used chromosomal and electrophoretic analyses
to show that natural hybrids occur between I. parvidens and I.
tridecemlineatus in areas where their ranges overlap in western
Texas and southeastern New Mexico, although Cothran (1983)
indicated that hybridization is localized and infrequent.
Cytogenetics.?Nadler (1962) reported cytogenetic charac-
teristics of I. tridecemlineatus and I. parvidens and found both
species to have the same diploid number (2N ? 34).
The fundamental number is 64 for I. parvidens and 62?64
for I. tridecemlineatus (Cothran and Honeycutt 1984).
Ecology.?Ictidomys comprises 3 ecologically similar spe-
cies that are basically separated into northern and southern
species. I. mexicanus and I. parvidens occur in grassland or
arid habitats often in association with shrub species (Valde?s
Alarco?n [sic] 2005), and prefer sandy or gravelly soils at
elevations between 200 and 3,000 m (Young and Jones 1982).
They are omnivorous, feeding on larval and adult insects, green
plants, forbs, and grasses (Zimmerman 1999). The original
habitat for I. tridecemlineatus was likely shortgrass prairie,
especially open, sandy areas with patches of low grass
(Whitaker 1999). However, all 3 species have adapted to live
in disturbed habitats and can be found along roadsides,
cemeteries, lawns, and golf courses throughout their range. In
fact, Ictidomys has possibly extended its range with land
clearance for agriculture (Streubel and Fitzgerald 1978b).
Comments.?As noted above, X. perotensis and X. spilo-
soma were previously included by most authors in Ictidomys,
as influentially arranged by Howell (1938). Harrison et al.
(2003) and Herron et al. (2004) demonstrated that these species
are not closely related to the type species of Ictidomys, I.
tridecemlineatus (and its close relatives mexicanus and
parvidens) and instead demonstrated their close phylogenetic
relationship with X. mohavensis, the type species of Xeno-
spermophilus, and its immediate relative, X. tereticaudus.
We suggest that this phylogenetic alliance is reflected also in
craniometric and other morphological distinctions indicat-
ing an alliance between perotensis/spilosoma and Xerosper-
mophilus, rather than Ictidomys (Figs. 5, 14, and 15). Some
earlier studies also explored and queried the immediate
association between spilosoma/perotensis and tridecemlinea-
tus/mexicanus/parvidens, and their classification within a
single subgenus (e.g., Bryant 1945; Nadler 1962; Nadler and
Hughes 1966).
Genus Poliocitellus A. H. Howell
Franklin?s Ground Squirrel (Fig. 12)
Poliocitellus A. H. Howell, 1938, N. Am. Fauna, 56:42. Type
species: Arctomys franklinii Sabine, 1822:587.
Content.?Poliocitellus is monotypic, comprising only
P. franklinii (Sabine, 1822).
April 2009 293HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
Poliocitellus franklinii (Sabine, 1822). Trans. Linn. Soc. Lond.,
13:587. Type locality: none specified. Restricted by Preble
(1908:165) to Carlton House, Saskatchewan, Canada.
Etymology.?The name Poliocitellus is derived from the
Greek polios, meaning hoary or gray, and the Latin genus name
for ground squirrels, citellus (Jaeger 1955).
Diagnosis.?Poliocitellus franklinii is a medium-sized
member of the tribe Marmotini, larger than the species of
Xerospermophilus, Callospermophilus, Ictidomys, and most
Spermophilus, matching in size many species of Urocitellus as
well as Notocitellus annulatus, but smaller than the species of
Otospermophilus, Cynomys, and Marmota. The tail is bushy
and subequal in length to the head?body, and the ears are short
and rounded (Table 3). The dorsum is conspicuously infused
with orange-brown tones, contrasting with the paler gray-buff
head, rump, tail, and underside, and black banding throughout
the dorsal pelages generates a grizzled overall appearance.
Females have 5 or 6 pairs of teats (Moore 1961). The pelage
is short and sleek. The skull of Poliocitellus differs from that
of Urocitellus and Spermophilus in having a proportionally
narrower braincase and zygomata, wider interorbital region,
weaker postorbital processes, longer incisive foramina,
a smaller P3, a longer and more tapering (rather than
parallel-sided) rostrum, heavier and more opisthodont incisors,
and a less laterally elongate meatal portion of the auditory bulla
(Fig. 12). It differs further from Spermophilus in having more
richly pigmented orange incisor enamel (much paler in
Spermophilus). The skull of Poliocitellus closely resembles
that of Otospermophilus in size and some qualitative features
(Howell 1938), but differs especially from that genus in having
broader nasals, longer incisive foramina, proportionally smaller
bullae, and a larger, bicuspidate P3. The molars are relatively
brachyodont, with the parastyle ridge on M1 and M2 rising
to join the protocone without abrupt change in direction
(cf. Howell 1938).
Distribution.?Poliocitellus franklinii is distributed widely
over the northern Great Plains, extending from Alberta,
Saskatchewan, and Manitoba in Canada south to Kansas and
east to Illinois and Indiana in the United States (Hall 1981;
Ostroff and Finck 2003; Thorington and Hoffmann 2005;
Fig. 11).
Cytogenetics.?Poliocitellus franklinii has a diploid chro-
mosome number of 42 and a fundamental number of 66
(Ostroff and Finck 2003).
Ecology.?Poliocitellus inhabits tall grasslands and tends to
avoid shorter grass habitats. P. franklinii is often found along
forest?grassland borders, marsh edges, and unmowed grass
areas along highways and railroad tracks (Ostroff and Finck
2003). It also occurs in a narrow band of aspen parkland from
the Canadian tallgrass prairie to central Alberta. This species
tends to form small colonies that are occasionally larger in
suitable habitat adjacent to wetter areas such as marshland.
These ground squirrels hibernate for 7?8 months of the year,
emerging around the 1st of May. This species is among the
most carnivorous of the ground squirrels. These ground
squirrels eat small mammals and birds, toads, and a variety
of insects in addition to the more usual green plants, fruits, and
seeds (Murie 1999).
Comments.?Poliocitellus franklinii was included in the
subgenus Ictidomys by Allen (1877), and later isolated in
a monotypic subgenus, Poliocitellus, erected by Howell (1938).
Bryant (1945) considered Poliocitellus to be most closely
related to Callospermophilus and Otospermophilus, but
mitochondrial DNA (mtDNA) comparisons indicate that
Poliocitellus is instead probably a member of a suprageneric
clade that also includes Ictidomys, Cynomys, and Xerospermo-
philus (Harrison et al. 2003; Herron et al. 2004).
Genus Xerospermophilus Merriam
Pygmy Ground Squirrels (Figs. 14 and 15)
Xerospermophilus Merriam, 1892, Proc. Biol. Soc. Wash.,
7:27. Type species: Spermophilus mohavensis Merriam,
1889:15.
Content.?Our definition of Xerospermophilus incorporates
the 2 species previously classified in the subgenus Xerosper-
mophilus (tereticaudus and mohavensis) as well as 2 species
previously classified under the subgenus Ictidomys (spilosoma
and perotensis). Four species of Xerospermophilus are thus
recognized: X. mohavensis Merriam, 1889, X. perotensis
Merriam, 1893, X. spilosoma Bennett, 1833, and X. tereticau-
dus Baird, 1858, with synonyms as delineated by Thorington
and Hoffmann (2005). Type localities, as provided below, are
cited largely based on the authority of Thorington and
Hoffmann (2005) and Howell (1938). It is well established
that X. mohavensis and X. tereticaudus form a species pair, as
do X. spilosoma and X. perotensis (Ernest and Mares 1987;
Hafner and Yates 1983; Herron et al. 2004; Howell 1938).
Further research into species-level boundaries within the
spilosoma?perotensis complex is warranted; X. perotensis
may prove to be best classified as the southernmost sub-
population of X. spilosoma (Harrison et al. 2003; Herron et al.
2004; Howell 1938).
Xerospermophilus mohavensis (Merriam, 1889). N. Am.
Fauna, 2:15. Type locality: Mohave River, California [USA].
Restricted by Grinnell and Dixon (1918) to near Rabbit
Springs, about 15 mi. (24 km) E Hesperia, San Bernardino Co.
Xerospermophilus perotensis (Merriam, 1893). Proc. Biol. Soc.
Wash., 8:131. Type locality: Perote, Veracruz, Mexico.
Xerospermophilus spilosoma (Bennett, 1833). Proc. Zool. Soc.
Lond., 1833:40.
X. s. altiplanensis (Anderson, 1972:275). Type locality: 3 mi.
ESE La Junta, Chihuahua, 6900 ft. [Mexico].
X. s. ammophilus (Hoffmeister, 1959:37). Type locality: 5?
mi. N Samalayuca, Chihuahua [Mexico].
X. s. annectens (Merriam, 1893:132). Type locality: The Tanks,
12 miles from Point Isabel, Padre Island, Texas.
X. s. bavicorensis (Anderson, 1972:276). Type locality: 2 mi.
SW S. J. Bab??cora, Chihuahua, 7450 ft. [Mexico].
294 JOURNAL OF MAMMALOGY Vol. 90, No. 2
X. s. cabrerai (Dalquest, 1951:106). Type locality: 10 km
NNW Nun?ez, San Luis Potos??, Mexico.
X. s. canescens (Merriam, 1890:38). Type locality: Willcox,
Cochise Co., Arizona. [arens (V. Bailey, 1902); macro-
spilotus (Merriam, 1890); and microspilotus (Elliot, 1901)
are synonyms.]
X. s. cryptospilotus (Merriam, 1890:57). Type locality:
Tenebito [? Dinnebito] Wash, Painted Desert, Coconino
Co, Arizona.
X. s. marginatus (V. Bailey, 1902:118). Type locality: Alpine,
Texas. [major (Merriam, 1890) (preoccupied, not Pallas,
1778) is a synonym.]
X. s. obsoletus (Kennicott, 1863:157). Type locality: 50 miles
west of Fort Kearney, Nebraska.
X. s. oricolus (Alvarez, 1962:123). Type locality: 1 mi. E La
Pesca, Tamaulipas [Mexico].
X. s. pallescens (A. H. Howell, 1928:212). Type locality: La
Ventura, Coahuila [Mexico].
X. s. pratensis (Merriam, 1890:55). Type locality: pine plateau
at N foot San Francisco Mtn., Coconino Co., Arizona.
[obsidianus (Merriam, 1890) is a synonym.]
X. s. spilosoma (Bennett, 1833:40). Type locality: Durango,
Me?xico.
Xerospermophilus tereticaudus (Baird, 1858). Mammalia, in
Repts. U. S. Expl. Surv., 8(1):315.
X. t. apricus (Huey, 1927:85). Type locality: Valle de la
Trinidad, Baja California, Mexico (lat. 318209 north; long.
1158409 west).
X. t. chlorus (Elliot, 1904:242). Type locality: Palm Springs,
Riverside Co., California.
X. t. neglectus (Merriam, 1889:17). Type locality: Dolan
Spring, 12 miles northwest of Chloride, Mohave Co.,
Arizona. [arizonae (Grinnell, 1918) and sonoriensis (Ward,
1891) are synonyms.]
X. t. tereticaudus (Baird, 1858:315). Type locality: [Old] Fort
Yuma [Imperial Co., California]. [eremonomus (Elliot,
1904) and vociferans (Huey, 1926) are synonyms.]
Etymology.?Xerospermophilus is derived from the Greek
xeros, meaning dry, spermatos for seed, and phileo for love
(Jaeger 1955).
Diagnosis.?As a group, the species of Xerospermophilus
are all relatively small-bodied (Fig. 14) and pale in coloration
(buff to tan as the predominating color of the body). The pelage
of 2 species (X. mohavensis and X. tereticaudus) is unmarked,
but in some geographic populations of the other 2 species (X.
spilosoma and X. perotensis) the dorsum is marked with
distinctive pale flecking or spotting. It is primarily for this
reason that these latter 2 species have in the past been allied
subgenerically with the lined ground squirrels (Ictidomys?
e.g., Howell 1938). However, unlike the species of Ictidomys,
in X. spilosoma and X. perotensis the flecks or spots do not
form clear anteroposteriorly directed linear rows or coalesce
into stripes. The pelage is short and sleek, and the ears and tail
are relatively short. Skulls of Xerospermophilus are rather
delicately built, with opisthodont incisors, short incisive
foramina, blunt or moderately long rostra, relatively narrow
braincases, short postorbital processes, and proportionally large
auditory bullae (Fig. 15). All species of Xerospermophilus
depart from Ictidomys in having less precipitously downward-
sloping rostra (when viewed in lateral profile), proportionally
much larger bullae, relatively shorter tails, and hairier hind-foot
soles (Figs. 14 and 15). The upper incisors are more gracile
overall, and usually less markedly opisthodont in orientation,
when compared to Ictidomys (Fig. 15). The molars are
relatively brachyodont, with the parastyle ridge on M1 and
M2 rising to join the protocone without an abrupt change in
direction (cf. Howell 1938).
Distribution.?The distribution of Xerospermophilus em-
braces the deserts and grasslands of southern California and the
southwestern United States, extending southward to northern
and central Mexico (Hafner and Yates 1983; Howell 1938;
Thorington and Hoffmann 2005; Fig. 11). X. mohavensis
occupies a limited geographic range in the northwestern
Mojave Desert of California. X. tereticaudus is found in
deserts from southern Nevada through southeastern California
and western Arizona, to northeastern Baja California and
Sonora, Mexico (Ernest and Mares 1987). Hybridization
between X. mohavensis and X. tereticaudus has been detected
along the Mojave River, but the hybrid zone is apparently
narrow and stable (Hafner 1992). X. perotensis occurs in
Veracruz and Puebla in east-central Mexico (Best and Ceballos
1995; Valde?z and Ceballos 1997). X. spilosoma occurs in
desert scrubland and grasslands from central Mexico north
to southern and western Texas, throughout New Mexico to
eastern and northwestern Arizona, and north from Texas to
southwestern South Dakota (Streubel and Fitzgerald 1978a).
Cytogenetics.?All species in the genus have been karyo-
typed: X. perotensis and X. spilosoma (2N ? 32; FN ? 58); X.
tereticaudus (2N ? 36; FN ? 68); and X. mohavensis (2N ?
38; FN ? 70) (Best and Ceballos 1995; Hafner and Yates 1983;
Uribe-Alcocer et al. 1979).
Ecology.?Xerospermophilus, as the name implies, occupies
arid, desert, or semidesert habitats. X. mohavensis (the Mohave
ground squirrel) has a patchy distribution throughout its range
in the Mojave Desert, where it occurs within a wide variety of
arid habitats (Hafner 1999). Although omnivorous, Mohave
ground squirrels tend to be short-term specialists on whatever
appropriate food type is in abundance, be it seeds, leaves, or
insect larvae (Best 1995c). X. tereticaudus (the round-tailed
ground squirrel) lives in the Sonoran and Mojave deserts of
the southwestern United States and typically occupies sandy,
flat desert, sand dunes, and wash edges, but avoids rocky hills
(Ernest 1999). Round-tailed ground squirrels feed primarily on
green vegetation, augmented by seeds and insects seasonally
(Ernest and Mares 1987). They occupy habitats that experience
extremes of temperature from below freezing on winter nights
to exceptionally hot summer days (Castillo 2005). X. spilosoma
(the spotted ground squirrel) ranges throughout much of the
arid and semiarid regions of the southwestern United States and
Mexico (Young 1999). Spotted ground squirrels favor habitats
with deep, sandy soils and scattered desert scrub vegetation
(Streubel and Fitzgerald 1978a). They feed extensively on
April 2009 295HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
green vegetation, seeds, and a variety of insects, including
ants (Arago?n 2005). X. perotensis occupies sandy, semidesert
habitat in the states of Veracruz and Puebla, Mexico (Valde?z
Alarco?n and Ceballos 2005a). This species also is found
associated with agricultural areas within its range (Best and
Ceballos 1995).
Comments.?Merriam (1892) established Xerospermophilus
as a subgenus of Spermophilus with X. mohavensis as the type
species. In his revision of the genus, Howell (1938) also
included X. tereticaudus in this subgenus. Building on the
molecular phylogenetic framework developed by Harrison
et al. (2003) and Herron et al. (2004), here we transfer X.
spilosoma and X. perotensis to Xerospermophilus for the 1st
time, on the basis of their phylogenetic alliance with X.
mohavensis and X. tereticaudus. This is an arrangement that
appears to us to be solid on morphological grounds, because all
species that we recognize in Xerospermophilus share similar-
ities in body size, coloration, and qualitative and craniometric
skull features to the exclusion of other Marmotini.
Molecular phylogenetic comparisons based on mtDNA
(Harrison et al. 2003; Herron et al. 2004) identify Xerosper-
mophilus as the sister genus to the prairie dogs (Cynomys),
albeit with poor support. Species of Xerospermophilus depart
from Cynomys markedly in body size and cranial anatomy, but
resemble prairie dogs in their simple tan and buff coloration
patterns. At least 1 species (X. tereticaudus) is semicolonial,
maintaining individual burrows but also sharing others (Ernest
and Mares 1987).
FIG. 16.?Representative skins (all adult females) of the species of Urocitellus, including the ??big-eared ground squirrels?? (1?7) and the
??small-eared ground squirrels?? (8?12): 1) U. parryii, USNM 128620, Yukon River, Alaska, United States; 2) U. columbianus, USNM 236182,
Gifford, Washington, United States; 3) U. undulatus, USNM 175312, Altai Mountains, Siberia, Russia; 4) U. elegans, USNM 179821, Evanston,
Wyoming, United States; 5) U. richardsonii, USNM 225873, Livingston, Montana, United States; 6) U. armatus, USNM 18830, Fort Bridger,
Wyoming, United States; 7) U. beldingi, USNM 88285, McKinney, California, United States; 8) U. washingtoni, USNM 78578, Pendleton,
Oregon, United States; 9) U. townsendii, USNM 235742, Ellensburg, Washington, United States; 10) U. mollis, USNM 201605, Payette, Idaho,
United States; 11) U. brunneus, USNM 202410, Van Wyck, Idaho, United States; 12) U. canus, USNM 204835, Bend, Oregon, United States.
296 JOURNAL OF MAMMALOGY Vol. 90, No. 2
Genus Urocitellus Obolenskij
Holarctic Ground Squirrels (Figs. 12 and 16)
Anisonyx Rafinesque, 1817, Am. Month. Mag., 2:45. Type
species: Anisonyx brachiura Rafinesque [? Arctomys
columbianus Ord] (preoccupied by a generic-level name in
the insect order Coleoptera [Anisonyx Latreille, 1807]).
Urocitellus Obolenskij, 1927, C. R. Acad. Leningrad:188.
Type species: Spermophilus eversmanni Brandt, 1841 [?
Urocitellus undulatus (Pallas, 1778)].
Content.?The delineation of this genus corresponds to the
North American and northeastern Eurasian members of the
subgenus Spermophilus as traditionally recognized (e.g., Hall
1981; Howell 1938; Thorington and Hoffmann 2005). We
recognize 12 species within Urocitellus: U. armatus Kennicott,
1863; U. beldingi, Merriam, 1888; U. brunneus (A. H. Howell,
1928); U. canus Merriam, 1898; U. columbianus (Ord, 1815);
U. elegans Kennicott, 1863; U. mollis Kennicott, 1863; U.
parryii (Richardson, 1825); U. richardsonii (Sabine, 1822); U.
townsendii Bachman, 1839; U. undulatus (Pallas, 1778); and
U. washingtoni (A. H. Howell, 1938), with synonyms and
subspecies as delineated by Thorington and Hoffmann (2005).
Type localities, as given below, are cited largely based on the
authority of Thorington and Hoffmann (2005), Hall (1981),
Ognev (1947), and Howell (1938).
Urocitellus armatus (Kennicott, 1863). Proc. Acad. Nat. Sci.
Phila., 15:158. Type locality: in the foothills of the Uinta
Mountains, near Fort Bridger, [Uinta Co.] Wyo[ming].
Urocitellus beldingi (Merriam, 1888). Ann. N. Y. Acad. Sci.,
4:317.
U. b. beldingi (Merriam, 1888:317). Type locality: Donner,
Placer Co., California.
U. b. creber (Hall, 1940:59). Type locality: Reese River
Valley, 7 mi. N Austin, Lander Co., Nevada.
U. b. oregonus (Merriam, 1898:69). Type locality: Swan Lake
Valley, Klamath Basin, Oregon.
Urocitellus brunneus (A. H. Howell, 1928). Proc. Biol. Soc.
Wash., 41:211.
U. b. brunneus (A. H. Howell, 1928:211). Type locality: New
Meadows, Adams Co., Idaho.
U. b. endemicus (Yensen, 1991:596). Type locality: Sand
Hollow, 1 km E (up canyon from) OX Ranch headquarters;
T9N, R4W, Sec. 7, NE ?; 5.6 km N, 5.0 km E Payette,
elev. 750 m, Payette Co., Idaho.
Urocitellus canus (Merriam, 1898). Proc. Biol. Soc. Wash.,
12:70. Type locality: Antelope, Wasco County, Oregon. [vigilis
(Merriam, 1913) is a synonym.]
Urocitellus columbianus (Ord, 1815). In Guthrie, New Geogr.,
Hist., Coml. Grammar, Phila., 2nd ed., 2:292.
U. c. columbianus (Ord, 1815:292). Type locality: between the
forks of the Clearwater and Kooskooskie rivers (Idaho Co.,
Idaho, USA). [albertae (J. A. Allen, 1903); brachiura
(Rafinesque, 1817); and erythrogluteia (Richardson, 1829)
are synonyms.]
U. c. ruficaudus (A. H. Howell, 1928:212). Type locality:
Wallowa Lake, Wallowa Co., Oregon.
Urocitellus elegans (Kennicott, 1863). Proc. Acad. Nat. Sci.
Phila., 15:158.
U. e. aureus (Davis, 1939:177). Type locality: Double Springs,
16 mi. NE Dickey, Custer Co, Idaho.
U. e. elegans (Kennicott, 1863:158). Type locality: Fort
Bridger, [Uinta Co., Wyoming, USA].
U. e. nevadensis (A. H. Howell, 1928:211). Type locality:
Paradise, Humboldt Co., Nevada.
Urocitellus mollis (Kennicott, 1863). Proc. Acad. Nat. Sci.
Phila., 15:157.
U. m. artemesiae (Merriam, 1913:137). Type locality: Birch
Creek, about 10 mi. S Nicholia, Idaho. [pessimus (Merriam,
1913) is a synonym.]
U. m. idahoensis (Merriam, 1913:135). Type locality: Payette,
Idaho.
U. m. mollis (Kennicott, 1863:157). Type locality: Camp Floyd
[? Fairfield], Utah Co., Utah. [leurodon (Merriam, 1913);
stephensi (Merriam, 1898); and washoensis (Merriam,
1913) are synonyms.]
Urocitellus parryii (Richardson, 1825). In Parry, Voy.
Discovery Northwest Passage, Vol. 6, app. second voy., p. 316.
U. p. ablusus (Osgood, 1903:25). Type locality: Nushagak,
Alaska. [stonei (J. A. Allen, 1903) is a synonym.]
U. p. kennicottii (Ross, 1861:434). Type locality; Fort
Good Hope, Mackenzie [Northwest Territories, Canada].
[barrowensis (Merriam, 1900) and beringensis (Merriam,
1900) are synonyms.]
U. p. kodiacensis (J. A. Allen, 1874:292). Type locality:
Kodiak Island, Alaska.
U. p. leucostictus (Brandt, 1844:379). Type locality: Okhotsk
River, northeastern Siberia [Russia]. [buxtoni (J. A. Allen,
1903) and tschuktschorum (Chernyavskii, 1972) are synonyms.]
U. p. lyratus (Hall and Gilmore, 1932:396). Type locality:
Iviktook Lagoon, about 35 mi. NW Northeast Cape (Howell
1938:101), St. Lawrence Island, Bering Sea, Alaska.
U. p. nebulicola (Osgood, 1903:26). Type locality: Nagai
Island, Shumagin Islands, Alaska.
U. p. osgoodi (Merriam, 1900:18). Type locality; Fort Yukon,
Alaska.
U. p. parryi (Richardson, 1825:316). Type locality: Five
Hawser Bay, Lyon Inlet, Melville Peninsula [Hudson
Bay, Nunavut Territories], Canada. [phaeognatha (Richard-
son, 1829) is a synonym.]
U. p. plesius (Osgood, 1900:29). Type locality: Bennett City,
head of Lake Bennett, British Columbia [Canada].
U. p. stejnegeri (J. A. Allen, 1903:142). Type locality: near
Petropavlovsk, Kamchatka [Russia]. [brunniceps (Kittlitz,
1858) [nomen nudum]; coriakorum (Portenko, 1963); and
janensis (Ognev, 1937) are synonyms.]
Urocitellus richardsonii (Sabine, 1822). Trans. Linn. Soc.
Lond., 13:589. Type locality: Carlton-House [Saskatchewan,
Canada].
April 2009 297HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
Urocitellus townsendii (Bachman, 1839). J. Acad. Nat. Sci.
Phila., 8:61.
U. t. nancyae (Nadler, 1968). Type locality: 5 mi. N Richland,
Benton Co., Washington.
U. t. townsendii (Bachman, 1839:61). Type locality: On the
Columbia River, about 300 miles [483 km] above its mouth.
Restricted by A. H. Howell (1938:60, 62) to west bank of
Walla Walla River near confluence with Columbia River
[near Wallula, Walla Walla Co., Washington, USA].
[yakimensis (Merriam, 1898) is a synonym.]
Urocitellus undulatus (Pallas, 1778). Nova Spec. Quad. Glir.
Ord., p. 122.
U. u. eversmanni (Brandt, 1841). Type locality: ??In montibus
Altaicus?? [Altai Mountains, Russia?Kazakhstan?China?
Mongolia border region]. [altaicus (Eversmann, 1841) is
a synonym.]
U. u. jacutensis (Brandt, 1844). Type locality: Yakutsk District,
eastern Siberia [Russia].
U. u. menzbieri (Ognev, 1937). Type locality: twenty-three
kilometers from Blagoveschensk (near Ignatijevka), Upper
Amur, eastern Siberia [Russia].
U. u. stramineus (Obolenskij, 1927). Type locality: Near
Leman Gegen, northwestern Mongolia.
U. u. transbaikalicus (Obolenskij, 1927). Type locality: Lake
Ivan, Transbaikalia [Russia]. [intercedens (Ognev, 1937) is
a synonym.]
U. u. undulatus (Pallas, 1778:122). Type locality: Selenga
River valley (Buryat ASSR, Russia). [undulatum (Pallas,
1779) is a synonym.]
Urocitellus washingtoni (A. H. Howell, 1938). N. Am. Fauna,
56:69. Type locality: Touchet, Walla Walla Co., Wash[ington].
(USA). [loringi (A. H. Howell, 1938) is a synonym.]
Etymology.?The name Urocitellus is derived from the Latin
uro for tail and citellus for ground squirrel (Jaeger 1955).
Diagnosis.?Species of Urocitellus lack the diagnostic
pelage patterning or immediately discernible head?body to tail
proportions that characterize members of the genera Ammo-
spermophilus, Notocitellus, Callospermophilus, Otospermo-
philus, and Ictidomys, and differ from each of these genera
in other ways described above. Species of Urocitellus are
cranially smaller than species of Cynomys and Marmota, and
differ consistently from those distinctive genera in cranial
shape and color patterning (Howell 1938). The pelage is
usually longer and less sleek than in most other ground
squirrels. Most species of Urocitellus are much larger than
species of Xerospermophilus, and have proportionally much
smaller auditory bullae, longer and more parallel-sided rostra,
longer postorbital processes, and more gracile incisors
compared to members of that genus (Figs. 12 and 15). Species
of Urocitellus can be distinguished from species of Polio-
citellus in having a proportionally broader braincase and
zygomata, better-developed postorbital processes, shorter in-
cisive foramina, a less reduced P3, shorter and more parallel-
sided rostra, more gracile incisors, and a more laterally
elongate meatal portion of the auditory bulla (Fig. 12). Species
of Urocitellus are morphologically most similar to species of
Spermophilus (sensu stricto), which they resemble especially in
external morphology?a resemblance attested by their tradi-
tional classification within the same subgenus (e.g., Hall 1981;
Howell 1938; Thorington and Hoffmann 2005). Nevertheless,
species of Urocitellus can be reliably diagnosed against species
of Spermophilus by a suite of craniometric and qualitative
cranial distinctions: in Urocitellus (compared to Spermophilus),
the interorbital width is proportionally wider, the larger cheek
teeth (i.e., molars and P4) are proportionally less massive but
P3 is proportionally heavier, the inflated portion of the auditory
bulla is proportionally smaller but the meatal portion is more
expansive laterally (i.e., forming a more elongate tube), the
mesopterygoid fossa is not distinctively narrowed, and the
upper incisor enamel is more distinctly orange (whitish to very
pale yellow in Spermophilus; Fig. 12), among other distinctions
(see ??Diagnosis?? of Spermophilus, above; Fig. 12). Many of
these key differences are reflected in the clear multivariate
discrimination between Urocitellus and Spermophilus in our
craniometric analyses (Fig. 5).
Distribution.?Urocitellus is disjunctly distributed in central
and northeastern Asia, in far northern North America, and in
southern Canada and the western contiguous United States
(Fig. 13).
The distribution of the ??columbianus species-group?? (see
below) encompasses much of western North America west of
the Mississippi and north of Mexico, as well as Canada, Alaska,
and eastern Eurasia at higher latitudes (Fig. 13). U. undulatus
is the only member of this genus that is exclusively Eurasian
in distribution, ranging through eastern Kazakhstan, southern
Siberia, Transbaikalia (Russia), and northern Mongolia to the
provinces of Heilungjiang and Xinjiang in China. U. parryii is
Holarctic in distribution, extending from northeastern Russia
through northwestern Alaska to northwestern Canada. The
distribution of U. columbianus extends from southeastern British
Columbia and western Alberta in Canada south to northeastern
Oregon, central Idaho, and central Montana in the United States.
U. richardsonii occurs in the northern Great Plains in southern
Alberta, Saskatchewan, and Manitoba in Canada south into
Montana, North Dakota, northeastern South Dakota, western
Minnesota, and northwestern Iowa in the United States. U.
elegans extends from southeastern Oregon, southern Idaho,
southwestern Montana, and northeastern Nevada, south to
central Colorado and western Nebraska. U. armatus ranges from
south-central Utah to southern Montana and southeastern Idaho
to western Wyoming. U. beldingi occurs from eastern Oregon
and southwestern Idaho south to northeastern California, and
east to northern Nevada and northwestern Utah.
The distribution of the ??townsendii species-group?? (see
below) is centered in the intermountain west, including the
Great Basin, Snake River Plain, and the Columbia Plateau and
Basin. It encompasses primarily the states of Washington,
Oregon, Idaho, Nevada, and Utah, extending marginally into
eastern California (Hall 1981; Thorington and Hoffmann 2005;
Yensen 1991). U. townsendii occurs in southeastern Wash-
ington. U. washingtoni is found in southeastern Washington
and northeastern Oregon. U. mollis occurs in in southeastern
298 JOURNAL OF MAMMALOGY Vol. 90, No. 2
Oregon and western Idaho, extending southward through most
of Nevada, east-central California, and western Utah. U. canus
ranges from central Oregon to extreme west-central Idaho and
northwestern Nevada. U. brunneus has the smallest range of
any ground squirrel, comprising multiple populations isolated
by habitat fragmentation in west-central Idaho.
Cytogenetics.?Karyotypes have been reported for all
species in the genus (Liapunova and Vorontsov 1970; Nadler
1966a; Nadler et al. 1973, 1984; Yensen and Sherman 1997):
U. beldingi (2N ? 30; FN ? 56), U. columbianus (2N ? 32;
FN ? 60), U. elegans (2N ? 34; FN ? 64), U. armatus (2N ?
34; FN ? 64), U. undulatus (2N ? 34; FN ? 64), U. parryii
(2N ? 34; FN ? 68), U. richardsonii (2N ? 36; FN ? 64),
U. washingtoni (2N ? 36; FN ? 66), U. townsendii (2N ? 36;
FN ? 68), U. brunneus (2N ? 38; FN ? 66), U. mollis (2N ?
38; FN ? 66), and U. canus (2N ? 46; FN ? 66).
Ecology.?Urocitellus occupies a variety of montane and
steppe habitats in northern North America, with 1 Holarctic
species (U. parryii) and 1 restricted to Eurasia (U. undulatus).
U. undulatus occurs in thinly wooded savannahs and grassy
steppes bordering the Gobi Desert, and northward from there it
occupies bushy terrain among oak and beech groves, alpine
meadows, and riparian areas (Ognev 1947). U. parryii inhabits
arctic montane and tundra habitats farther north than any other
ground squirrel (Iwen 1999). U. beldingi is a colonial species
and is generally considered to be a high-elevation species
common in the central Sierra Mountains (Bachman 1999;
Jenkins and Eshelman 1984). U. columbianus also is colonial
and lives in a variety of habitats including alpine meadows,
mountain slopes, and agricultural lands (Elliott and Flinders
1991). Colonies inhabit alpine meadows and can be observed
along roadsides and cultivated land where soil conditions are
appropriate (Elliott 1999). U. brunneus is patchily distributed
in mountain meadows and habitats dominated by sagebrush
and bunch grasses (Yensen and Sherman 1997, 1999). U.
richardsonii inhabits shortgrass prairies in south-central
Canada and the adjacent north-central United States (Durrant
and Hansen 1954; Michener 1999; Michener and Koeppl
1985). U. elegans is a colonial species limited by U. armatus to
sagebrush and grass-covered valleys and foothills where the
ranges of these 2 species overlap in Montana and Idaho (Zegers
1984). U. elegans is also found living in brushy and grass-
covered areas of northern Nevada (Smith 1999). U. armatus
inhabits sagebrush and grassy mountain meadows in Montana,
Wyoming, Utah, and Idaho (Davis 1939; Eshelman and
Sonnemann 2000; Yensen 1999b). U. washingtoni lives in
perennial grassland habitats at low elevation in the Columbia
River basin in southeastern Washington and northeastern
Oregon (Rickart and Yensen 1991; Yensen 1999a). U.
townsendii is typically found in sagebrush and agricultural
habitats within its range (Rickart 1987, 1999c). U. canus
occurs in sagebrush, juniper, and greasewood habitats, in
grasslands and pastures, and in agricultural lands (Rickart
1999a). U. mollis is widely distributed throughout the Great
Basin and along the Snake River in Idaho in desert and
sagebrush habitats (Rickart 1999b).
Comments.?Morphological considerations (Bryant 1945;
Davis 1939; Howell 1938), chromosomal complements
(Liapunova and Vorontsov 1970; Nadler 1966a; Yensen and
Sherman 1997), and some molecular analyses (Fig. 2; Harrison
et al. 2003; Herron et al. 2004) suggest that there are 2
TABLE 4.?Recognized species within the 8 genera of ground
squirrels previously included within the genus Spermophilus (sensu
lato).
Scientific name Common name
Genus Notocitellus Tropical ground squirrels
N. adocetus Tropical ground squirrel
N. annulatus Ring-tailed ground squirrel
Genus Otospermophilus Rock squirrels
O. atricapillus Baja California rock squirrel
O. beecheyi California ground squirrel
O. variegatus Rock squirrel
Genus Callospermophilus Golden-mantled ground squirrels
C. lateralis Golden-mantled ground squirrel
C. madrensis Sierra Madre ground squirrel
C. saturatus Cascade golden-mantled ground squirrel
Genus Spermophilus Old World ground squirrels
S. alashanicus Alashan ground squirrel
S. brevicauda Brandt?s ground squirrel
S. citellus European ground squirrel
S. dauricus Daurian ground squirrel
S. erythrogenys Red-cheeked ground squirrel
S. fulvus Yellow ground squirrel
S. major Russet ground squirrel
S. pallidicauda Pallid ground squirrel
S. pygmaeus Little ground squirrel
S. ralli Tien Shan ground squirrel
S. relictus Relict ground squirrel
S. suslicus Speckled ground squirrel
S. taurensis Taurus ground squirrel
S. xanthoprymnus Asia Minor ground squirrel
Genus Ictidomys Lined ground squirrels
I. mexicanus Mexican ground squirrel
I. parvidens Rio Grande ground squirrel
I. tridemcemlineatus Thirteen-lined ground squirrel
Genus Poliocitellus Franklin?s ground squirrels
P. franklinii Franklin?s ground squirrel
Genus Xerospermophilus Pygmy ground squirrels
X. mohavensis Mohave ground squirrel
X. perotensis Perote ground squirrel
X. spilosoma Spotted ground squirrel
X. tereticaudus Round-tailed ground squirrel
Genus Urocitellus Holarctic ground squirrels
U. armatus Uinta ground squirrel
U. beldingi Belding?s ground squirrel
U. brunneus Idaho ground squirrel
U. canus Merriam?s ground squirrel
U. columbianus Columbian ground squirrel
U. elegans Wyoming ground squirrel
U. mollis Piute ground squirrel
U. parryii Arctic ground squirrel
U. richardsonii Richardson?s ground squirrel
U. townsendii Townsend?s ground squirre
U. undulatus Long-tailed ground squirrel
U. washingtoni Washington ground squirrel
April 2009 299HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS
distinctive species-groups within Urocitellus: the larger (HBL ?
217?495 mm), long-footed (HF ? 40?68 mm), proportionally
longer-tailed species (32?46% of HBL) of the ??columbianus
species-group?? (2N ? 30?36), including U. parryii, U.
columbianus, U. undulatus, U. elegans, U. richardsonii, U.
armatus, and U. beldingi (Fig. 16: 1?7); and the smaller
(HBL ? 167?271 mm), short-footed (HF ? 27?39 mm),
proportionally shorter-tailed (23?32% of HBL) members of the
??townsendii species-group?? (2N ? 36?46), incorporating U.
washingtoni, U. townsendii, U. mollis, U. brunneus, and U.
canus (Fig. 16: 8?12). These groups are sometimes referred to
as the ??big-eared ground squirrels?? and ??small-eared ground
squirrels,?? respectively (Davis 1939; Nadler 1966a; Robinson
and Hoffmann 1975). Should additional molecular comparisons
confirm their trenchant divergence and respective monophyly,
in the future it may be worthwhile to classify these species-
groups in distinct subgenera (there is currently no available
generic-level name for the ??townsendii species-group??).
DISCUSSION
The revision of generic boundaries for Holarctic ground
squirrels (Table 4) better illustrates evolutionary relationships
above the species level, and should set the scene for new
avenues of research in ground squirrel comparative biology.
The various North American and Eurasian ground squirrel
genera differ in their geographic distributions, habitat associ-
ations, and in salient morphological aspects such as body size,
skull conformation, limb and tail proportions, and mammary
number, all of which pose standing questions about their
differential biology. This new classificatory framework
encourages fresh reviews to portray ground squirrel compar-
ative biology in the light of these revised boundaries, including
aspects of fossil history and nomenclature, and dating of
divergence events (Black 1963, 1972; Goodwin and Hayes
1994; Harrison et al. 2003); anatomy and physiology (Bryant
1945, Hudson and Deavers 1973, 1976; Iwaniuk 2001; Miller
et al. 1989; Russell et al. 2001); reproductive biology (Hayssen
2008a, 2008b; Mandier and Gouat 1996; Millesi et al. 1998,
1999; Moore 1961); behavioral and evolutionary ecology
(Armitage 1981; Blumstein and Armitage 1998; Hare and
Murie 2007; Livoreil and Baudoin 1996; Murie and Michener
1984; Yahyaoui et al. 1995); and conservation biology and
management (Van Horne 2007)?tasks well beyond the scope
of our cursory overview.
Our efforts in this paper have been focused on delineating
a generic-level taxonomy of ground squirrels in the tribe
Marmotini consistent with the evolutionary history of the group
and establishing an appropriate nomenclature applicable to
generic-level clades. We note that a great deal of systematic
revisionary work on the tribe Marmotini is still needed. Higher-
level relationships among genera remain to be conclusively
established with solid resolution (Fig. 2), a goal probably best
approached with studies of nuclear DNA sequence data.
Species boundaries in some genera (especially Spermophilus
and Urocitellus) require further detailed consideration, ideally
combining morphological, cytogenetic, and mitochondrial and
nuclear sequence data to demonstrate or reject reproductive
isolation between nominal taxa that are closely related or
difficult to distinguish.
Finally, renewed attention should be focused on the
applicability of ground squirrel subspecies categorizations.
Although subspecies are commonly and formally employed to
characterize geographic variation in most genera (e.g., Eller-
man and Morrison-Scott 1966; Hall 1981; Howell 1938; Ognev
1947; Thorington and Hoffmann 2005), detailed morphological
and genetic studies are needed to evaluate whether currently
recognized trinomial distinctions profitably characterize salient
and consistent patterns of geographic variation among ground
squirrels. We hope that our revision will set the stage for
tackling these and other problems with renewed vigor.
ACKNOWLEDGMENTS
This paper is dedicated to our friend and colleague Robert S.
Hoffmann. We gratefully acknowledge the logistical support, collec-
tion access, and advice provided by staff and researchers in the
Division of Mammals at USNM, including R. Hoffmann, R.
Thorington, S. Peurach, R. Fisher, L. Gordon, C. Ludwig, H. Kafka,
J. Whatton, J. Jacobs, D. Schmidt, A. Gardner, M. Carleton, L.
Emmons, J. Mead, and C. Potter. We also thank M. Herron and an
anonymous reviewer for helpful reviews of our manuscript, J. Matson
for helpful discussion, and B. Gunnell, E. Robinson, M. Wells, and J.
van Veldhuizen for assistance in recurating the USNM ground squirrel
collection. This project was supported by a Postdoctoral Fellowship
from the Smithsonian Institution to KMH and funding from Colby
College and the Oak Foundation provided to FRC during a sabbatical
leave.
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Submitted 24 September 2007. Accepted 22 July 2008.
Associate Editor was Burton K. Lim.
APPENDIX I
Specimens measured for craniometric analyses (all adult females)
are listed by scientific name, specimen (skull) number, and locality.
All specimens are at USNM.
Ammospermophilus.?193304, A. harrisii, United States, Arizona:
Dolan?s Spring; 193305, A. harrisii, United States, Arizona: Dolan?s
Spring; 146786, A. insularis, Mexico, Baja California Sur: Isla
Espiritu Santo; 120449, A. interpres, United States, New Mexico: San
Andreas Mts. opposite Bear Canyon; 131835, A. interpres, United
States, New Mexico: Manzano Mts.; 135831, A. leucurus, United
States, California: Mojave; 135839, A. leucurus, United States,
California: Mojave; 140310, A. nelsoni, United States, California:
Coalinga; 137939, A. nelsoni, United States, California: Coalinga.
(NB: Subsequent to the completion of our analyses, Alvarez-
Castan?eda [2007] has argued convincingly that insularis should be
recognized as a subspecies of A. leucurus.)
Notocitellus.?126139, N. adocetus, Mexico, Michoaca?n: La
Salada; 126114, N. adocetus, Mexico, Michoaca?n: La Salada;
44585, N. annulatus, Mexico, Colima: Manzanillo; 44582, N.
annulatus, Mexico, Colima: Manzanillo.
Otospermophilus.?139748, O. atricapillus, Mexico, Baja California
Sur: San Ignacio; 139744, O. atricapillus, Mexico, Baja California
Sur: San Ignacio; 57567, O. beecheyi, United States, California:
Wilson?s Peak; 57566, O. beecheyi, United States, California:
Wilson?s Peak; 45577, O. variegatus, Mexico, Jalisco: Zapotlan;
45575, O. variegatus, Mexico, Jalisco: Zapotlan.
Callospermophilus.?159752, C. lateralis, United States, Wyo-
ming: Laramie Mountains; 25604, C. lateralis, United States,
Wyoming: Bridger Pass; 95348, C. madrensis, Mexico, Chihuahua:
Sierra Madre Mountains, 7,000 feet; 95368, C. madrensis, Mexico,
Chihuahua: Sierra Madre Mountains, 7,000 feet; 233148, C. saturatus,
United States, Washington: Mt. Rainier; 233147, C. saturatus, United
States, Washington: Mt. Rainier.
Spermophilus.?248096, S. citellus, Hungary: Szegedin; 248103, S.
citellus, Hungary: Szegedin; 155202, S. dauricus, China: ??Kansu??;
155201, S. dauricus, China: ??Kansu??; 251638, S. erythrogenys,
Russia: Siberian Federal District, Altai Krai, Zmeinogorski, Noven-
koie; 254949, S. erythrogenys, Russia: Siberian Federal District,
Tomsk, Kuznetsk, Kuznetsk Steppe; 251637, S. pygmaeus, Ukraine:
Ekaterinoslav (? Dnipropetrovsk), Tgren; 251636, S. pygmaeus,
Ukraine: Ekaterinoslav (? Dnipropetrovsk), Tgren; 251634, S.
suslicus, Belarus: Minsk; 251635, S. suslicus, Belarus: Minsk;
327282, S. xanthoprymnus, Turkey: Talas, Kayseri; 327281, S.
xanthoprymnus, Turkey: Talas, Kayseri.
Ictidomys.?46200, I. mexicanus, Mexico, Jalisco: Atemajac; 46199,
I. mexicanus, Mexico, Jalisco: Atemajac; 30816, I. parvidens, United
States, Texas: Altuda; 40345, I. parvidens, United States, Texas:
Carrizo; 314658, I. tridecemlineatus, United States, Indiana: Amboy;
314657, I. tridecemlineatus, United States, Indiana: Middletown.
Poliocitellus.?192733, P. franklinii, United States, Minnesota:
Brown?s Valley; 192734, P. franklinii, United States, Minnesota:
Brown?s Valley.
Cynomys.?47205, C. gunnisoni, United States, Colorado: Fort
Garland; 47204, C. gunnisoni, United States, Colorado: Fort Garland;
54118, C. leucurus, United States, Colorado: Grand Junction; 54107,
C. leucurus, United States, Colorado: Grand Junction; 246659, C.
ludovicianus, United States, Colorado: Conifer, 7,300 feet; 191444,
C. ludovicianus, United States, Colorado: Boulder County; 433834, C.
mexicanus, Mexico, Coahuila, La Ventura, 5,600 feet; 433837,
C. mexicanus, Mexico, Coahuila, La Ventura, 5,600 feet; 158060,
C. parvidens, United States, Utah: Buckskin Valley; 158986, C.
parvidens, United States, Utah: Buckskin Valley.
Xerospermophilus.?192756, X. mohavensis, United States, Cal-
ifornia: Mojave River; 192754, X. mohavensis, United States,
California: Mojave River; 54272, X. perotensis, Mexico, Veracruz:
Perote; 54273, X. perotensis, Mexico, Veracruz: Perote; 79006, X.
spilosoma, Mexico, Aguascalientes: Chicalote; 79005, X. spilosoma,
Mexico, Aguascalientes: Chicalote; 117343, X. tereticaudus, United
States, California: Needles, 500 feet; 117344, X. tereticaudus, United
States, California: Needles, 500 feet.
Urocitellus.?25565, U. armatus, United States, Wyoming: Fort
Bridger; 25583, U. armatus, United States, Wyoming: Fort Bridger;
192683, U. beldingi, United States, California: Donner; 192688, U.
beldingi, United States, California: Donner; 202410, U. brunneus,
United States, Idaho: Van Wyck; 265912, U. brunneus, United States,
Idaho: Round Valley; 227286, U. canus, United States, Oregon:
Narrows; 227287, U. canus, United States, Oregon: Narrows; 66674,
U. columbianus, Canada, British Columbia: Nelson; 66668, U.
columbianus, Canada, British Columbia: Nelson; 179379, U. elegans,
United States, Idaho: Dickey; 179378, U. elegans, United States,
Idaho: Dickey; 181159, U. mollis, United States, Idaho: Nampa;
181160, U. mollis, United States, Idaho: Nampa; 180895, U. parryii,
Canada, Northwest Territories: Mackenzie District, Artillery Lake;
180893, U. parryii, Canada, Northwest Territories: Mackenzie
District, Kasba Lake; 398315, U. richardsonii, United States,
Minnesota: 5 miles south and 6 miles east of Louisburg; 398240, U.
richardsonii, United States, Minnesota: 5 miles south and 6 miles east
of Louisburg; 235736, U. townsendii, United States, Washington:
Yakima; 235737, U. townsendii, United States, Washington: Yakima;
175272, U. undulatus, Russia, Altai: Tchegan?Burgazi Pass; 175284,
U. undulatus, Russia, Altai: Tchegan?Burgazi Pass; 398330, U.
washingtoni, United States, Washington: 0.5 miles south and 0.5 miles
east of Lind; 398318, U. washingtoni, United States, Washington: 0.5
miles south and 0.5 miles east of Lind.
April 2009 305HELGEN ET AL.?GENERIC REVISION OF SPERMOPHILUS