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Mammalia 2015; aop
*Corresponding author: Boris Kryštufek, Slovenian Museum
ofNatural History, Prešernova 20, SI-1000 Ljubljana, Slovenia,
e-mail: bkrystufek@pms-lj.si
Ahmad Mahmoudi: Faculty of Sciences, Department of Biology,
Ferdowsi University of Mashhad, Mashhad, Iran
Alexey S. Tesakov: Geological Institute of the Russian Academy
ofSciences, Pyzhevsky per. 7, Moscow 119017, Russia
Jan Matějů: Karlovy Vary Museum, Pod Jelením skokem 30,
36001Karlovy Vary, Czech Republic
Rainer Hutterer: Zoologisches Forschungsmuseum Alexander
Koenig, Adenauerallee 160, 53113 Bonn, Germany
Boris Kryštufek*, Ahmad Mahmoudi, Alexey S. Tesakov, Jan Matějů and Rainer Hutterer
A review of bristly ground squirrels Xerini and
ageneric revision in the African genus Xerus
DOI 10.1515/mammalia-2015-0073
Received April 28, 2015; accepted October 13, 2015
Abstract: Bristly ground squirrels Xerini are a small rodent
tribe of six extant species. Despite a dense fossil record the
group was never diverse. Our phylogenetic reconstruction,
based on the analysis of cytochrome b gene and including
all known species of Xerini, confirms a deep divergence
between the African taxa and the Asiatic Spermophilopsis.
Genetic divergences among the African Xerini were of a
comparable magnitude to those among genera of Holarc-
tic ground squirrels in the subtribe Spermophilina. Evi-
dent disparity in criteria applied in delimitation of genera
in Sciuridae induced us to recognize two genera formerly
incorporated into Xerus. The resurrected genera (Euxerus
and Geosciurus) are clearly distinct between each other
and from Xerus in nucleotide sequences and in external,
cranial and dental morphology. They occupy discrete
ranges and show specific environmental adaptations.
Atlantoxerus is more likely a sister to the remaining Afri-
can genera than being nested inside them. We readdress
nomenclatural issues associated with Xerini, list and ref-
erence all names above the species groups, and detail in
words and figures those characters which differentiate the
taxa. We propose Tenotis Rafinesque, 1817 (type species
is Tenotis griseus Rafinesque, 1817), which is occasion-
ally synonymized with Euxerus, as a not identifiable name
(nomen dubium).
Keywords: Atlantoxerus; cytochrome b; Euxerus; Geo-
sciurus; Spermophilopsis.
Introduction
Bristly ground squirrels from the arid regions of Central
Asia and Africa constitute a coherent monophyletic tribe
Xerini sensu Moore (1959). The tribe contains six species
in three genera of which Atlantoxerus and Spermophilop-
sis are monotypic. The genus Xerus in its present scope
(Thorington and Hoffmann 2005), consists of four species
in three subgenera: X. inauris and X. princeps (subgenus
Geosciurus), X. rutilus (subgenus Xerus), and X. eryth-
ropus (subgenus Euxerus). Recent phylogenetic recon-
struction based on molecular markers retrieved Xerus to
be paraphyletic with respect to Atlantoxerus (Fabre etal.
2012), therefore challenging the suitability of the generic
arrangement of the group.
We address in this paper the current taxonomic divi-
sion of Xerini and its concordance with various sources of
evidence. Specifically, we (i) review the taxonomic history
of bristly ground squirrels, (ii) reconstruct phylogenetic
relationships among the extant species using a complete
mitochondrial gene for cytochrome b (cytb), (iii) confront
genetic distances among bristly ground squirrels with
distances between the genera of Holarctic ground squir-
rels, (iv) analyse phenotypical traits of taxa, (v) their
biogeography and fossil history, and (vi) propose a novel
generic taxonomy for the group which consents to the
available body of evidence. We conclude that classifica-
tion of African taxa into four genera, as proposed around
a century ago by Thomas (1909) and Pocock (1923), is
more in accordance with operational criteria which are
currently in use for the delimitation of genera in squirrels
(e.g. Helgen etal. 2009) than is a two-genera system advo-
cated by the majority of recent authors (cf. Thorington and
Hoffmann 2005).
Taxonomic history
The only Asiatic species, “the curious prairie-dog-like
Spermophilopsis leptodactylus” (Moore 1959), is morpho-
logically and geographically so remote from the African
Xerini, that the two were only rarely treated simultane-
ously. Genus Spermophilopsis, coined by Blasius (1884)
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B. Kryštufek etal.: Bristly ground squirrels Xerini
for a species known since 1823 as Arctomys leptodacty-
lus, was ignored by Pocock (1923), and classified together
with Palaearctic ground squirrels (now in Spermophi-
lus and Urocitellus) by Obolenskij (1927). Ognev (1940)
cherished the uniqueness of Spermophilopsis among the
squirrels occupying the Palaearctic Asia by placing it into
a subfamily on its own, emphasizing simultaneously its
close resemblance to the African bristly ground squirrels.
Ellerman (1940) formally grouped Spermophilopsis with
Xerus and Atlantoxerus and his arrangement, not seri-
ously challenged ever since (but see Simpson 1945: 79),
received support from several molecular phylogenetic
reconstructions (Herron etal. 2004, Fabre etal. 2012, Ge
etal. 2014).
Xerus was originally proposed as a subgenus of
Sciurus (Hemprich and Ehrenberg, 1833). Already Water-
house (1839) used Xerus as a full genus, and he was fol-
lowed by the majority of subsequent authors (Temminck
1853, Brandt 1855, Murray 1866, Gray 1867, Alston 1876,
etc.). Two other generic names were introduced for bristly
ground squirrels shortly after the paper by Hemprich
and Ehrenberg (1833), Geosciurus (Smith 1834) and Sper-
mosciurus (Lesson 1836), while Euxerus was coined with
considerable delay (Thomas 1909). The Barbary ground
squirrel, known (as Scyurus [sic!] getulus) already to
Gessner (1551 n.v., and subsequent editions: 1569, 1583),
was recognized as a member of its own subgenus Atlan-
toxerus (within Xerus) only towards the end of the 19
th
century (Forsyth Major 1893). Earlier on this animal was
classified either into Sciurus (Brisson 1762, Erxleben 1777,
Smith 1834, Murray 1866, Jentink 1882, Lataste 1885) or
into Xerus (Temminck 1853, Gray 1867, Flower and Lydek-
ker 1891, Forsyth Major 1893, Trouessart 1897). In the 19
th
century the taxonomic scope of Xerus was understood
very differently than it is now and the genus contained
also squirrels which are currently classified into the
tribes (sensu Thorington and Hoffmann 2005) Sciurini
and Protoxerini (Huet 1880, Trouessart 1880, Forsyth
Major 1893, Palmer 1904). Gray (1867) defined the scope
of Xerus as agreed at present and Jentink (1882) correctly
concluded that the genus contains three species; Geosci-
urus princeps as the fourth species was recognized much
later (Thomas 1929).
The early 20
th
century saw two generic classifica-
tions of fundamental importance for understanding the
taxonomic relationships among African bristly ground
squirrels. Thomas (1909) based his taxonomic system
on dentition, evidently following Forsyth Major (1893)
who claimed that “squirrels should be classified by their
dental and cranial characters just as other rodents are,
and [...] not [...] on such superficial characters as the
presence or absence of stripes or similar external char-
acters”. Pocock (1923), on the other hand, created his
classification on the baculum, a heterotopic bone which
was shown by Thomas (1915) to be in squirrels a supe-
rior taxonomic character relative to skull and dentition.
Importantly, although Thomas (1909) and Pocock (1923)
based their revisions on non-overlapping character sets,
they both recognized four genera, i.e. all listed hereafter
in the account on taxonomy.
Ellerman (1940) concluded that genera of African
bristly ground squirrels are based “on the least or vaguest
excuses” and retained only Xerus (with Geosciurus and
Euxerus as subgenera) and Atlantoxerus. This arrange-
ment was adopted in nearly all subsequent major revi-
sions and taxonomic lists (Simpson 1945, Amtmann
1975, Carleton 1984, Corbet and Hill 1980, 1986, Honacki
et al. 1982, Hoffman et al. 1993, Nowak 1999, Thoring-
ton etal. 2012, Waterman 2013a, Monadjem etal. 2015).
Allen (1954), in his list of African mammals, retained the
system of three genera, but after 1940 such a view was
accepted only by few mammalogists: Hill and Carter
(1941), Schouteden (1947), Roberts (1951), Setzer (1956),
Rosevear (1969), Depierre and Vivien (1992), Kingdon
(1997), Osborn and Osbnornová (1998), and Reiner and
Simões (1998). In his influential taxonomic arrangement
of diurnal squirrels, Moore (1959) accepted Euxerus and
Geosciurus as subgenera of Xerus, but at the same time
commented that a generic position might be more appro-
priate solution.
Materials and methods
Our analysis is based on published evidence and on exam-
ination of archived museum material representing all
extant species of Xerini. For practical reasons we subse-
quently use Xerus in its narrow sense (containing only X.
rutilus), and refer to Euxerus and Geosciurus as to genera.
Molecular phylogeny
Phylogenetic relationships among bristly ground squirrels
were assessed using 25 published sequences for cytb gene
representing Xerus, Euxerus, both species of Geosciurus
and Spermophilopsis (Supplemental Appendix 1). In addi-
tion to data downloaded from GenBank we sequenced
cytb gene for Atlantoxerus getulus. Restriction of our anal-
ysis to a single gene marker ensured a complete taxonomic
sampling of Xerini, which is an advantage with respect to
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3
previous phylogenetic assessments. Because our aim was
to achieve a generic system of Xerini which will be com-
parable to generic divisions in other groups of squirrels
we quantified the cytb intergeneric variation in Holarctic
ground squirrels from the subtribe Spermophilina which
were recently generically revised (Helgen et al. 2009).
Intergeneric metrics in Spermophilina served as stand-
ard for setting genera in Xerini. We therefore downloaded
from GenBank further 138 cytb sequences representing 39
species of Holarctic ground squirrels in nine genera. For
taxonomic scope and accession numbers see Supplemen-
tal Appendix 1.
DNA of Atlantoxerus getulus (voucher PMS 19301; Sup-
plemental Appendix 2) was extracted using a QIAamp
®
DNA Mini kit (Qiagen, Valencia, CA, USA), following the
manufacturer’s conditions. Cytb was amplified using the
trans-mammalian primers L14727-SP and H15497-SP (Irwin
et al. 1991). Amplification was performed using a 20 μl
reaction containing 2.5 m MgCl
2
, 0.5 μ of forward and
reverse primer, 0.2 m of dNTPs and one unit of Fermentas
Taq in the supplied ammonium buffer. Cycling conditions
consisted of an initial stage of 95°C for 5min followed by
40 cycles of denaturation (40s at 94°C), primer annealing
(40s at 48°C) and extension (1min at 72°C). Sequencing
was performed on an ABI PRISM 3130 Genetic Analyzer
using BigDye Terminators chemistry (Applied Biosystems,
Foster City, CA, USA). Sequences were edited manually
using CodonCode aligner software (CodonCodes Inc.,
Ewing etal. 1998).
Phylogenetic relationships among bristly ground
squirrels were assessed using sequences from all extant
species of Xerini and 39 species of Holarctic Spermophil-
ina (Supplemental Appendix 1). An assembled alignment
file consisting of 171 sequences with 1140 bp length was
aligned with Clustal W (Thompson etal. 1997) algorithm
using BioEdit 7.0.5 (Hall 1999). As pseudogenes are known
to represent source of error for mitochondrial phylogeny
(Triant and DeWoody 2009), cytb sequences were checked
for the absence of stop codons and indels.
The most appropriate evolutionary model of
sequences was estimated based on Akaike Informa-
tion Criterion (AIC) using Modeltest software (Posada
and Crandall 1998). The phylogenetic relationships
among haplotypes were reconstructed using two dif-
ferent optimality criteria: Maximum Likelihood (ML)
and Bayesian inference of phylogeny (BI). ML tree was
inferred in RaxML (Silvestro and Michalak 2012) with a
general time-reversible model (GTR)+gamma distribu-
tion (G)+proportion of invariable sites (I) (G=0.8596
and I=0.3815) using rapid hill-climbing algorithm. Node
robustness values were estimated using both rapid
bootstrapping and ML heuristic search options. BI analy-
sis based on the same model was performed with four
Markov chain Monte Carlo (MCMC), as two simultaneous
analyses using MrBayes 3.1.2 (Ronquist and Huelsenbeck
2003), which started from random trees and were run for
4,000,000 iterations. The first 5000 trees were discarded
as burn-in, afterward the trees were sampled every 100
th
generation. The branch supports for BI were assessed
with Bayesian posterior probabilities (BPP). Five species
belonging to the family Gliridae (Graphiurus murinus,
Muscardinus avellanarius, Eliomys quercinus, Dryomys
nitedula, Glis glis and Glirulus japonicus) were used as
outgroups for rooting trees.
The cytb intergeneric variation among nine genera
of Spermophilina and between five genera of Xerini was
quantified assuming Kimura 2 parameter (K2P) substitu-
tion model in MEGA6 (Tamura etal. 2013).
Phenotypical analyses
We studied 181 museum vouchers housed in ten different
collections (Supplemental Appendix 2). Information on
sex, locality, and external dimensions was deduced from
specimen tags. Skull morphology was quantified with tra-
ditional morphometric methods using a set of nine cranial
variables. The following linear measurements were scored
using a Vernier calliper with accuracy to the nearest
0.1mm: condylobasal length, length of rostrum from pre-
maxilla to 3
rd
molar, length of rostrum from premaxilla to
margin of hard palate, length of upper diastema, length
of upper tooth row, breadth across zygomatic arches,
breadth of braincase, occipital height, and length of man-
dible. To minimize the effect of ontogenetic growth, only
adult individuals were used in analyses. Age was assessed
following the criteria in Helgen etal. (2009).
To characterize the morphological variation among
samples and to find patterns in our data of high dimensions
we used principal components analysis (PCA) which was
performed on the correlation matrix of log
10
-transformed
cranial variables. Transformation of data to logarithms
has the advantage of normalizing the distribution of the
measurements, equalizing the variances, and preventing
dominance of the analysis by large values at the expense
of small ones. First few principal components (PC) usually
explain a high proportion of variance in the original data
set which allows a reduction of the dimensionality of a
multivariate dataset and facilitates visualization of the
relations among the studied objects. Statistical tests were
run in Statistica (Version 5.5, StatSoft, Tulso, OK, USA,
1999).
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B. Kryštufek etal.: Bristly ground squirrels Xerini
Results and discussion
Molecular phylogeny
We analyzed simultaneously all the sequences. The 165
samples yielded 144 different cytb haplotypes. For the
1140 bp-long sequence, 644 polymorphic sites (56.5%)
were found with a total of 930 mutations, 574 of which
were parsimony informative. No stop codons, insertions
or deletions were observed in the alignment. As expected
under neutral evolution (Martin and Palumbi 1993), the
majority of polymorphic sites were at third positions (369
variable sites, 57.3% of all variable sites), followed by first
positions (157 variable sites, 24.4% of all variable sites)
and second positions (118 variable sites, 18.3% of all vari-
able sites). The mean transition/transversion ratio was
4.61. The nucleotide composition was characterized by
a deficit of guanines (5.9%), similar to that described in
other mammals (Irwin etal. 1991).
Phylogenetic relationships that were reconstructed by
the two different methods (ML and BI) yielded very similar
results. Both approaches retrieved a basal dichotomy into
two lineages which matched Xerini and Spermophilina,
respectively. Within the latter, a branching pattern yielded
an identical topology to those published by Harrison etal.
(2003) and Herron et al. (2004); consequently, only the
inset of the BI tree with Xerini is shown in Figure1. All
nodes were highly supported in both analyses (BP>95%,
BPP>0.89). The Central-Asiatic Spermophilopsis hold a
basal position in the tree. Chaining hierarchy of African
genera retrieved Atlantoxerus at the basal position and
Geosciurus as the most derived group.
The only published phylogenetic reconstruction of
all recent Xerini is by Fabre etal. (2012) who used four
markers, two mitochondrial (cytb and gene encoding 12S
RNA) and two nuclear markers (Interphotoreceptor retin-
oid-binding protein exon IRBP and Recombination acti-
vating gene 1 RAG-1). The cladogram retrieved the basal
position of Spermophilopsis (Figure 1). Within the African
taxa Euxerus holds the basal position which, however,
benefited low support (BP<70%) while Atlantoxerus is in a
strongly supported (BP≥95%) sister position against Xerus.
Sister relationships between Xerus+Atlantoxerus and Geo-
sciurus benefited moderate support (70%≤BP≤95%).
Evidently, phylogenetic trees failed to provide robust
and conclusive results on the evolutionary relationships
within African Xerini. One of possible reasons for discrep-
ancy between the two trees is in incomplete sampling in
Fabre etal. (2012) since their matrix (6 species×4 genes)
contained high proportion (=42%) of missing values.
Figure 1:Bayesian inference tree (above) reconstructed from
cytochrome b sequences of six species of Xerini. Numbers on the
branches correspond to posterior probability values; bootstrap
supports at all nodes were >95% (not shown). Below is cladogram
depicting the highest-likelihood topology for relationships among
Xerini, with symbols indicating bootstrap supports (from Fabre etal.
2012). Sequences used in tree constructions: Cytb – cytochrome
b, IRBP – Interphotoreceptor retinoid-binding protein exon, 12S –
gene encoding 12S RNA, RAG-1 – Recombination activating gene 1.
Both trees are insets from wider phylogenetic analyses, consider-
ing 45 species of squirrels (six species of Xerini and 39 species of
Spermophilina), and rooted with six species of Gliridae (above), and
1265 species of rodents (below).
As a next step we explored inter- and intrageneric
genetic K2P distances in two lineages of squirrels, the Xerini
and the Spermophilina (Table1). In Xerini, the intergeneric
K2P estimates ranged between 13.8 and 22.5% (n=6) and were
mainly within the margins observed among nine genera of
Spermophilina (range=12.4–20.5%; mean 16.7%±2.43;
n=36). The intergeneric divergences clearly exceeded intra-
generic heterogeneity which ranged between 3.7 and 4.7%
(n=3) in Xerini and from 0.2 to 9.6% (mean=5.5%±3.4;
n=9) in Spermophilina. It is therefore safe to conclude that
metrics of K2P genetic distances provides strong support for
a generic split of the African bristly squirrels.
Table 1:Pairwise K2P genetic distances (in percent; mean±SD)
among genera of Xerini.
. Atlantoxerus –
. Xerus .±. 4.7±0.6
. Euxerus .±. .± 3.7±0.7
. Geosciurus .±. .± .±. 4.5±0.4
. Spermophilopsis .±. .±. .±. .±.
Italicized are average intrageneric distances on diagonal
(not estimated in Atlantoxerus and Spermophilopsis).
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Chromosomes
Chromosomal data are available for Spermophilopsis
(Liapunova and Zholnerovskaya 1969, Nadler etal. 1969)
and for all African bristly ground squirrels: Atlantoxerus
(Petit et al. 1984), Xerus (Nadler and Hoffmann 1974,
Baskevich et al. 1995), Euxerus (Dobigny et al. 2002,
Granjon and Duplantier 2009), and both species of Geo-
sciurus (Robinskon etal., 1986). All species share identi-
cal diploid number (2n) of 38 pairs of chromosomes. With
the exception of one pair of acrocentrics, the remain-
ing chromosomes are metacentric and submetacentric,
resulting in a fundamental number of autosomal arms
(NFa) of 70. The X chromosome is submetacentric in all
species while the small Y chromosomes is acrocentric in
Euxerus and metacentric in Xerus, both species of Geo-
sciurus and Spermophilopsis; the details are not known
for Atlantoxerus. Differences in morphology of the Y
chromosome most probably originate from the pericen-
tric inversion which is the predominant drive of chro-
mosomal change in squirrels (Richard and Dutrillaux
2012). Such differences provide little useful information
for phylogenetic reconstructions of interrelationships in
Sciuridae because of convergent and reverse rearrange-
ments of the karyotype (Romanenko etal. 2011, Richard
and Dutrillaux 2012). Evidently, Xerini have retained
a conservative karyotype which remains similar to the
ancestral condition in squirrels (Li etal. 2006, Beklemi-
sheva etal. 2011).
Phenotypical traits
Morphological evidence is thoroughly documented in
Flower and Lydekker (1891), Forsyth Major (1893), Thomas
(1909), Pocock (1922, 1923), Ellerman (1940), Ognev (1940),
Moore (1959), Rosevear (1969), and Denys etal. (2003).
External morphology
All bristly ground squirrels are externally modified for ter-
restrial life. They are of moderate size according to squir-
rel standards and grade in length of head and body (in
mm; parenthesized are mean±SD) as follows: Atlantoxerus
(175.8±12.42, n=28) <Xerus (222.8±8.80, n=12) <Geo-
sciurus inauris (238.3±11.87, n=12) ≈Spermophilop-
sis (243.5±17.62, n=22) ≈G. princeps ( 2 47. 8 ±12.83, n=6)
≈Euxerus (249.3±15.46, n=26). One-way ANOVA retrieved
highly significant (F>90, p <0.0001) heterogeneity among
species in all external measurements.
Secondary sexual dimorphism in size (SSDS) is not
a major source of intraspecific variation in Xerini. The
SSDS is reportedly not readily apparent in Xerus (O’Shea
1991), Geosciurus (Smithers 1971, Waterman and Herron
2004, Skurski and Waterman 2005) and Euxerus (Water-
man 2013b). Usually, males are slightly larger and heavier
than females. We tested SSDS using two variables (length
of hind foot and condylobasal length of skull) utilized by
Matějů and Kratochvíl (2013) in their assessment of the
phenomenon in Spermophilina. Geosciurus princeps was
excluded due to a small sample of females. ANOVA on the
remaining species failed to retrieve significant difference
in any comparison (F<3.3, p>0.1). Based on these results
we pooled sexed in subsequent statistical tests.
Fur is short, coarse or rush (brittle), with some hairs
flattened and grooved. Xerus has the most pronouncedly
spiny pelage, followed by Euxerus and Geosciurus princeps;
G. inauris has less bristly hair. Ventral side is more sparsely
haired and is even partly bare. Basic color varies from cin-
namon or sandy to dark chocolate-brown but is most fre-
quently red sandy to red brown. Differences in color among
local populations may depend on rainfall (Waterman
2013a,b). Additionally, skins in Xerus and Euxerus are fre-
quently stained from the soil what changes the color of the
feet, tail, and even the entire body ( Hollister 1919). Dorsal
pelage is monochromatic (Xerus and Spermophilopsis) or
striped (the remaining species). The pattern is simple, with
a single flank stripe of all-white hairs in Euxerus and Geo-
sciurus. Atlantoxerus has an indistinct spinal line in addi-
tion to lateral stripes (Figure2).
African Xerini are relatively long-tailed for ground-
dwelling squirrels (Figure 2). Length of tail relative
to length of head and body ranks between species as
follows (in%; parenthesized are mean±SD): Atlantoxerus
(70.42±6.79, n=10) <Euxerus (80.6±8.45, n=26) <Xerus
(84.2±7.95, n=12) <Geosciurus inauris (86.9±7.10, n=12) <G.
princeps (103.2±6.27, n=6). The long clawed ground squir-
rel Spermophilopsis (Figure 3) is decidedly short-tailed
(29.2±4.42, n=21). The tail is dorso-ventrally flattened
(distichous) with long hairs directed sideways rather than
bushing out evenly all around. Long tail hair is mono-
chromatic in Xerus, but has white and black bands in the
remaining genera. In Spermophilopsis the black and white
pattern is restricted to the terminal half of the tail and is
most extensive on its ventral side. The tail in Xerini serves
multiple purposes, i.e. in thermoregulation (in hot days as
a parasol to prevent overheating; Bennett etal. 1984), in
social interactions (Herron and Waterman 2004) and in
antipredatory behavior, either by alarming conspecifics
(Sludskiy etal. 1969) or mobbing and harassing snakes by
sideway flicking (Apps 2000).
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B. Kryštufek etal.: Bristly ground squirrels Xerini
Figure 2:Representatives of genera in African bristly ground squirrels Xerina: 1 – Atlantoxerus getulus (Fuerteventura, Canary Islands;
photo courtesy Alenka Kryštufek); 2 – Geosciurus inauris (Etosha National Park, Namibia; photo courtesy Emmanuel Do Linh San); 3 – Xerus
rutilus (Samburu National Park, Kenya; photo by Jan Matějů); 4 – Euxerus erythropus (captive; photo courtesy Klaus Rudloff).
Figure 3:Long-clawed ground squirrel Spermophilopsis leptodactylus
(Kyzyl Kum, Kazakhstan; photo courtesy Nedko Nedyalkov).
Pocock (1922) stressed that African Xerini are unique
in having “a supplementary superciliary tuft of long vibris-
sae over the posterior angle of the eye” (i.e. superciliary or
supraorbital vibrissae), and Sokolov and Kulikov (1987)
reported a cluster of vibrissae on the outer antebrachium
about halfway between the elbow and the wrist (the ante-
brachial vibrissae; Figure4) as a distinctive trait in Sper-
mophilopsis. As a matter of fact, both types of vibrissae are
present in all species of Xerini.
Feet of Xerini are peculiar among squirrels in being
of perissodactyle type, i.e. having digit III the longest
and digits II and IV of about same length (Figure 4).
Atlantoxerus deviates from other genera in having the
feet more slender and in retaining metatarsal pads. The
remaining African species display stouter feet with small
plantar pads and lack the metatarsal pads; Geosciurus
has the most robust and fossorial feet of all genera. Sper-
mophilopsis differs from African genera in having much
enlarged claws and densely haired paws and soles (Figure
4). There was significant heterogeneity among species in
length of hind foot relative to length of head and body
(One-way ANOVA of log
10
-transformed quotients: F=15.61,
p <0.0001). Xerus (relative length of hind foot: 29.5±0.57,
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B. Kryštufek etal.: Bristly ground squirrels Xerini
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n=12) and both species of Geoscirus (G. inauris: 28.1±0.57,
n=12; G. princeps: 29.3±0.80, n=6) had relatively the
longest foot. Hind foot was the shortest in Spermophil-
opsis (23.9±0.48, n=17); Atlantoxerus (29.5±0.568, n=12)
and Euxerus (25.7±0.41, n=23) were intermediate in this
respect.
The ear conch is usually reduced in ground dwelling
squirrels and this holds also for Xerini. In Atlantoxerus,
Xerus and Euxerus, the ear is relatively large, with its
margin staying away from head. The ear is reduced to a
thick fold of skin in Geosciurus and Spermophilopsis. The
orifice is sheltered by a tragus in Euxerus, Xerus, and
Spermophilopsis, but is exposed in Atlantoxerus (which
still retains the tragus) and Geosciurus (which lacks the
tragus).
Atlantoxerus and Spermophilopsis have four pairs of
nipples: one pectoral, two abdominal and one inguinal
pair, respectively (Figure5). Xerus and Geosciurus have two
pairs (the posterior abdominal and the inguinal). Typical
count in Euxerus is three pairs (both abdominal and the
inguinal), however of 14 lactating females examined, four
Figure 4:Right front paw (ventral view) in (1) Spermophilopsis
leptodactylus (ZFMK 92.478) and (2) Atlantoxerus getulus (NMW
28084). Roman numerals correspond to digits (No. I is the thumb);
a.v. – antebrachial vibrissae. Note that digit III is longer than either
digits II and IV. Also note differences in length of claws (decidedly
longer in Spermophilopsis) and in hairiness of the palm (nude in
Atlantoxerus). Not to scale.
Figure 5:Nipples in (1) Spermophilopsis leptodactylus (ZFMK
92.496) and (2) Euxerus erythropus (ZFMK 76.38): p – pectoral; a1
and a2 – 1
st
and 2
nd
abdominal; i – inguinal. Not to scale.
individuals from Senegal and Uganda lacked the inguinal
pair hence retaining only both abdominal pairs. For Sper-
mophilopsis occupying Afghanistan, Obolenskij (1927)
reports three pairs of nipples, however, we counted four
pairs on each of two female skins from the country (ZFMK
92.478, 92.479; Figure 5). Similarly to our results, Ognev
(1940) identified four pairs in Spermophilopsis.
Glans penis is relatively large with well-developed
baculum. The baculum is terminally situated and con-
sists of a compressed blade which carries a cartilaginous
or partly ossified crest; the crest expands posteriorly and
represents the distal dorsal crest of the glans. In all its
aspects the baculum in Xerini differs profoundly from this
structure in Arctomyinae (Pocock 1923, Ognev 1940).
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Cranial and dental morphology
We assessed the overall cranial similarity by subjecting
nine linear skull measurements to PCA. First principal
component (PC1) explained 72.7% of variation in the origi-
nal data set and had high (>0.76) positive loadings for all
variables. PC2 (9.5% of variance explained) had moder-
ately high loadings for zygomatic width (0.52) and breadth
of braincase (0.44). Projection of specimens’ scores onto
PC1 and PC2 retrieved clear differences among the taxa
(Figure6). Species grouped along PC1 according to size,
from Atlantoxerus (the smallest) on the left hand side to
Geosciurus (the largest) on the right hand size. Evidently,
the majority of Xerini are large, and Xerus is the only
genus of intermediate size. PC2 sorted taxa according to
their relative breadth of skull. Most extreme were Spermo-
philopsis (the broadest skull) and Euxerus (the narrowest
skull). Wide skulls are evidently more common in Xerini
than narrow skulls.
Ellerman (1940) and Moore (1959) stressed the
cranial similarity between Geosciurus and Spermophil-
opsis, which is clearly retrieved also from our results. It
is equally well evident that the similarity is superficial
due to a robustness of our approach. Namely, the nine
parameters we used to quantify each skull missed many
details of cranial shape which are grasped at glance
Figure 6:Bivariate plot of six Xerini species onto the first two prin-
cipal components (PC) derived from ordination of nine cranial meas-
urements (transformed to log
10
). Percentage of variance explained
by individual PC is in parentheses. 95% confidence ellipses show
the dispersion of all specimens within each species and letters indi-
cate group centroids. Skulls (in dorsal view) are depicted to scale:
A– Atlantoxerus getulus (PMS 19301); E – Euxerus erythropus (ZFMK
47.972); Gi – Geosciurus inauris (NMW 32092); Gp – Geosciurus
princeps (NMW 32097); S – Spermophilopsis leptodactylus (NMW
25782); X – Xerus rutilus (ZFMK 81.234).
already on a dorsal profile of the skull (Figure 6). For
example, Spermophilopsis has a longer rostrum tapering
towards its apex and relatively shorter brain case while
the rostrum is short and blunt in Geosciurus, and the
braincase is longer. African genera were widely apart in
the morphospace defined by the first two principal com-
ponents and did not overlap at all. Groups are not defined
in advance in the PCA, therefore morphometric distances
between the objects are not biased, e.g. by minimizing
variance within each group and maximizing variance
among groups as is the case in a discriminant analysis.
Plot in Figure 6 therefore reflects the actual relationships
what allows the conclusion of significant cranial differen-
tiation among the genera of African Xerini.
The upper incisors are thickened and opisthodont
(Figure7), with the antero-posterior diameter exceeding
the transverse diameter. The front surface has shallow
grows in Atlantoxerus but is smooth in the remaining
genera. Among the characteristic features of cheek-teeth
Figure 7:Skull of Atlantoxerus getulus (NMW 43000) in dorsal,
lateral and ventral views (from top to bottom). Arrows point on
traits which are informative for taxonomic ranking of Xerini.
1– lacrimal bone; 2-postorbital process of the frontal bone;
3–anterior extension of the squamosal bone; 4 – parieto-
interparietal suture; 5–interparietal suture; 6 – anteriorly projected
external ridge on the front face of the zygomatic plate; 7 – jugal
bone; 8– opisthodont upper incisor; 9 – masseteric tubercle;
10– buccinator foramen; 11– masticatory foramen; 12 – posterior
margin of hard palate; 13 – external meatus acusticus.
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9
Fossil history
The ranges of extant Xerini are disjunct. The main occupa-
tion in Africa (Atlantoxerus and Xerus sensu lato), and a
smaller one in western Asia (Spermophilopsis) reflect the
much more extensive former distribution (Figure9). The
fossil record is surprisingly dense, particularly during
the Miocene in Eurasia and northern Africa. The group
however was never diverse, being represented at most by
two or three genera at a time.
The earliest true Xerini are known from the Late Oli-
gocene and belong to two closely related fossil genera:
Kherem Minjin, 2004 from Mongolia (Maridet etal. 2014)
and Heteroxerus Stehlin and Schaub, 1951 (Aragoxerus
Cuenca, 1988 is a synonym), from west Europe (Baudelot
and Olivier 1978, Werner 1994). Their widely scattered dis-
tributional records indicate an extensive trans-Palaearctic
distribution of Xerini at the very beginning of their known
history.
Heteroxerus and Atlantoxerus are the best know
genera of Xerini in the Eurasian and North African record
throughout the Miocene. Both had a cuspate bunodont
dental pattern but differed in size. The larger Atlantoxerus,
known since the Early Miocene of Europe (Aguilar 2002)
and China (Qiu etal. 2013), occupied Asia (northern and
north-western China, Mongolia, Pakistan, Thailand,
Kazakhstan, Arabia, Anatolia), south-western Europe
(Italy, France, Spain), and northern Africa. The smaller
Heteroxerus hold a stable range in the western Mediter-
ranean and was also recorded from the Early Miocene
of western Kazakhstan (Kozhamkulova and Bendukidze
2005), from the Middle Miocene of Siwalik, Indostan
(Flynn and Wessels 2013), and from the Middle and Late
Miocene of South Africa (Winkler etal. 2010). The Middle
Miocene marks the maximum range expansion and abun-
dance of Xerini in Eurasia. This peak was followed by
the extinction of Kherem and Heteroxerus in the Middle
(Maridet etal. 2014) and Late Miocene (de Bruijn, 1999),
respectively, and by the emergence of Xerus sensu lato,
which appeared for the first time in the early Late Miocene
of Ethiopia (Geraads 2001). The second earliest record
(tentatively Xerus sensu stricto) comes from late Late
Miocene of Kenya (Manthi 2007).
In the Pliocene and Early Pleistocene the fossil record
of Xerini clearly declined throughout Eurasia, and the
formerly continuous range became increasingly frag-
mented. The genus Atlantoxerus survived until Early Plio-
cene in Spain and persisted into the earliest Pleistocene
in northern China. In northern Africa, where Atlantoxerus
still had an extensive trans-regional distribution during
the Late Miocene, the range contracted to Morocco and
morphology shared by all fossil and recent Xerini are (i)
metaloph disconnected from protocone, and (ii) a pres-
ence of ectolophid and hypoconulid in lower molars. The
morphological trends recorded in the group are limited
to size increase and moderate hypsodonty development
on the basis of the bunodont dental pattern (Denys etal.
2003). Atlantoxerus is the most bunodont and brachyo-
dont, and Spermophilopsis is distinctly hypsodont, likely
an adaptation to a marked herbivorous diet. The man-
dibular tooth-row is more distinctly bunodont than the
maxillary. Low cusps and ridges became obliterated into
wide re-entrant folds fairly early in life. Atlantoxerus,
Spermophilopsis and Euxerus retain the 3
rd
upper premo-
lar (Figure8). This tooth, invariably small and peg-like, is
frequently missing in Euxerus (absent in seven skulls of 39
examined, i.e. 18%) and may be occasionally absent also
in Atlantoxerus and Spermophilopsis.
Cladistic analysis of African Xerini, based on 13
cranial and 9 dental traits (Denys et al. 2003), did not
unambiguously resolve phylogenetic relationships among
species and branching topology depended on a taxo-
nomic sampling. Atlantoxerus, however, emerged as the
most distinct with a putative sister position against the
remaining species.
Figure 8:Left maxillary (above) and right mandibular (below) tooth-
rows in Xerini: 1 – Euxerus erythropus (NHML 69.10.24.18/ZFMK
97.467), 2 – Xerus rutilus (ZFMK 81.234/ZFMK 96.251); 3 – Geosciu-
rus inauris (ZFMK 55.147); 4 – Atlantoxerus getulus (PMS 19301 /
ZFMK 88.195); 5 – Spermophilopsis leptodactylus (ZFMK 92.497/
ZFMK 92.496). Abbreviations for cheek-teeth: P/p – upper/lower
premolar, M/m – upper/lower molar; numbers refer to a position in
the tooth-row. Scale bar=2 mm.
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B. Kryštufek etal.: Bristly ground squirrels Xerini
Figure 9:Distributional ranges of Xerini. Fossil (Late Oligocene to Early Pleistocene) records (top inset) are based on Fortelius (2015)
with corrections and additions from Gromov and Erbajeva (1995), Kozhamkulova and Bendukidze (2005), Winkler etal. (2010), Flynn and
Wessels (2013), and Maridet etal. (2014). Map of recent ranges (inset below) does not show the isolate of Euxerus erythropus in Morocco,
and the population of Atlantoxerus getulus introduced to Fuerteventura, Canary Islands.
Algeria by the Early Pliocene, and to Morocco by the Early
Pleistocene.
The African record of Xerus sensu lato is patchy.
The group is known throughout the Pliocene from East
Africa (Kenya, Tanzania, Ethiopia), during the Early
Pleistocene from Chad, and during the Late Pleistocene
from central South Africa (Winkler etal. 2010). The Early
Pleistocene emergence of Spermophilopsis in deposits
of Badkhyz, southern Turkmenistan (Gromov and Erba-
jeva 1995), marks the presence of the genus within its
modern range. The increase of dryness towards the end
of the Miocene and the opening of savannahs may have
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directed the evolution of Xerini towards adaptations to
arid environments.
The phylogenetic reconstruction of the Xerini is quite
straightforward, due to low taxonomic diversity and good
fossil record. Geologically, the oldest representative is Het-
eroxerus which is the smallest and the most plesiomorphic
in dental morphology. By the Early Miocene Heteroxerus
may have given rise to Atlantoxerus (Jaeger 1977). Xerus
presumably diverged from a primitive Atlantoxerus stock
during the Early to Late Miocene (Denys etal. 2003). Simi-
larly, proto-Spermophilopsis possibly emerged after the
late Middle Miocene from a population fragment of Atlan-
toxerus in south-Central Asia. A palaeoecological analysis
of the chronological distribution of Xerini (Atlantoxerus
and Heteroxerus) during the Neogene of Spain retrieved
a marked positive dependence of taxonomic diversity on
increase in temperature. The group “flourished during the
late Early to Middle Miocene thermal optimum in Spain
and declined during the subsequent Middle Miocene
cooling episode” (Van Dam and Weltje 1999).
Systematics and nomenclature
The two available phylogenetic trees confirm a basal
dichotomy into an African and an Asiatic lineage, but
suggest very different relationships within the African
bristly ground squirrels. For the latter, the most probable
is a basal position of Atlantoxerus, which was retrieved
in our molecular reconstruction and in a cladistic analy-
sis of cranial and dental traits (Denys etal. 2003). Atlan-
toxerus shares with Spermophilopsis several traits (two
upper premolars, high number of nipples, and opened
parieto- interparietal suture) what induced Moore (1959)
to presume close phylogenetic links between the two.
Atlantoxerus is also unique among the African species in
its relatively soft fur, in retaining metatarsal pads and in
the shape of the suture between the jugal and the lacrimal
(see below). At least some of these traits are probably ple-
siomorphic for Xerini.
Although the phylogenetic relationships remain unre-
solved, metrics of genetic distances requires a taxonomic
partition of African Xerini. The genetic disparity is fully
concordant with the ecomorphological discrepancy there-
fore a division of the genus Xerus (sensu Ellerman 1940)
into three genera more properly reflects the taxonomic
relationships among the sub-Saharan bristly ground squir-
rels. Also noteworthy, the generic split of Xerus creates
genera of Xerini which are separated by genetic distances
comparable to those in another lineage of ground dwell-
ing squirrels, the Spermophilina (cf. above).
Subsequently we list and reference all names above
the species group in Xerini. Species group names are com-
piled in Ellerman (1940), Allen (1954), Ognev (1940) and,
Pavlinov and Rossolimo (1987). Type localities and other
relevant passages where quoted as originally published
(shown by quotation marks). For each taxon above the
species group we provide a brief diagnosis, understand-
ing a diagnosis as “A statement in words that purports to
give those characters which differentiate the taxon from
other taxa with which it is likely to be confused” (ICZN
1999).
Subfamily Xerinae Murray
Xeri Murray, 1866, p. 256. Type genus is Xerus (by tau-
tonomy). Emended to Xerini (Kryštufek and Vohralik
2013).
Xerinae Osborn, 1910, p. 535. Type genus is Xerus (by
tautonomy).
Xerini Simpson, 1945, p. 79. Type genus not defined.
Simpson evidently changed the rank from Osborn’s
(1910) subfamily to a tribe, without altering its scope.
In the past, the subfamily Xerinae was usually defined to
include the African genera Xerus and Atlantoxerus, and
the Asiatic Spermophilopsis (Osborn 1910, Pocock 1923).
Steppan etal. (2004) redefined the scope of Xerinae by
including also Arctomyinae Grey, 1821 (Marmotinae
Pocock, 1923 is a synonym; cf. Kryštufek and Vohralik
2013). A phylogenetic reconstruction of Fabre etal. (2012)
retrieved Xerinae to consist of two lineages, which are
appropriately classified as tribes (Kryštufek and Vohra-
lik 2013), the Xerini (cf. below) and the Callosciurini
Simpson, 1945. The scope of Callosciurini is identical to
the content of the subfamily Callosciurinae of Steppan
et al. (2004). Close relationships between Xerini and
Callosciurini are evident from chromosomal data (O’Shea
1991).
Tribe Xerini Murray: Bristly ground squirrels
For synonyms see under Xerinae.
Ground squirrels with coarse, bristly or spiny fur during
at least one season; hair is usually scanty; the feet is elon-
gate and slender, the 3
rd
digit longer than 4
th
(Figure4);
the claws are long and comparatively straight (fossorial);
pinna minute or reduced to a stiffened skin fold, antitra-
gal thickening set near the middle of the posterior edge of
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pinnae; membranous cheek-pouches are missing. Xerini
have supplementary superciliary vibrissae and the ante-
brachial vibrissae (Figure 4). The baculum consists of a
compressed blade which carries a cartilaginous or partly
ossified crest. Number of nipples is two to four pairs
(Figure 5).
Skull (Figure 7) is typically with (i) the bony palate
considerably prolonged beyond the ends of the tooth-row,
(ii) enlarged lacrimal bone, (iii) well developed and anteri-
orly projected external ridge on the front face of the zygo-
matic plate, (iv) the squamosal bone extending up to the
base of postorbital process of the frontal bone, (v) a power-
ful masseteric tubercle, (vi) a short and massive pterygoid
processes, and (vii) the opisthodont upper incisors (Flower
and Lydekker 1891, Pocock 1922, Ellerman 1940, Ognev
1940, Moore 1959). The karyotype is conservative (2n=38).
Xerini occupy dry open habitats in the Palaearctic
region (central Asia and the area of the Atlas Mts.), and of
sub-Saharan Africa (the Sudano-Guinean, Somali-Masai,
and Zambezian savannas; Denys 1999). Genera occupy
exclusive non-overlapping ranges, except for slight
overlap between Xerus and Euxerus in Eritrea, Ethiopia,
Uganda and Kenya (Figure 9). Four genera of total five are
monotypical what induced Moore (1959) to speculate that
Xerini are in the contracting phase of their evolution.
Xerini, as typical ground squirrels, dig underground
burrows and do not climb trees; Atlantoxerus seeks shelter
among rocks and easily climbs on rock slopes. Spermophil-
opsis is a habitat specialist, mainly dependent on moving
sands. All species are diurnal and do not practice torpor.
No common name is in use for the African and the
Asiatic Xerini combined. We propose “bristly ground
squirrels”, a name capturing an evident character in
common to these animals.
The tribe contains two subtribes: Xerina of Africa and
Spermophilopsina of Central Asia.
Subtribe Xerina Murray: African bristly
ground squirrels
For synonyms see under Xerinae.
Subtribe Xerina includes African members of the tribe
Xerini, with long tail and a pelage which is bristly (rough
in Atlantoxerus) at all seasons; a bold light (whitish)
ring is surrounding the eye, and three genera of totally
four have flank stripes (Figure 2). Soles and plants are
nude (Figure4); the pollex bears a tiny nail, claws on the
remaining digits are not enlarged (<10mm in length); two
tufts of supraorbital vibrissae are present; the cerebral
dura mater has no melanocits; the external meatus acus-
ticus lacks a bony tube (except in Geosciurus); buccinator
and masticatory foramina are separate (Figure 7).
Few common names were in use in the past for Xerina:
“spiny (or bristly) squirrels” (Murray 1866, Flower and
Lyddeker 189, Osborn 1910) and “African ground squir-
rels” (Pocock 1922, Simpson 1945, Li etal. 2006). Pocock
(1922) was perhaps the first who used the combination
“bristly ground squirrels”.
Genus Xerus Hemprich and Ehrenberg:
Unstriped ground squirrels
Xerus Hemprich and Ehrenberg, 1832, Plate IX. Type
species is Sciurus (Xerus) brachyotus Hemprich and
Ehrenberg (=Xerus rutilus).
Spermosciurus Lesson, 1842, p. 110. Type species is Sciurus
rutilus Cretzschmar (cf. below). Spermosciurus was
proposed as a subgenus of Sciurus.
Content. – A monotypic genus, containing only X. rutilus.
Xerus rutilus (Cretzschmar): Unstriped
ground squirrel
Sciurus rutilus Cretzschmar, 1828, p. 59, plate 24. Type
locality is “eastern slope of Abysinnia”; probably
Massawa (cf. Thorington and Hoffmann 2005), today
in Eritrea.
Amtmann (1975) recognized eight subspecies but also
noted that subspecific classification is uncertain.
Etymology. – Xerus is Greek for “dry”; “called from the
character of the fur, which is harsh and often spiny”
(Palmer 1904). Species name rutilus is Latin for “red” or
“golden red” in allusion to the colouration of the pelage.
Diagnosis. – Xerus rutilus is a medium-sized member of the
subtribe Xerina and the only one with a plain, unstriped
pelage (Figure 2). The ears are moderately large, with the
tragus present. Metatarsal pads are absent (Pocock 1922).
Females have posterior abdominal and the inguinal pairs
of nipples (four nipples totally). The baculum (length=6
mm) is typified by a wide and spearhead-shaped upper
surface of the blade and a low dorsal median crest (Pocock
1923). Skull is moderately wide (Figure 6) and the 3
rd
upper
premolar is absent (Figure 8); the jugal bone is bluntly
truncated against the lacrimal.
Distribution. – Endemic to a Somali-Masai savannah
(Denys 1999), occupying dry bushland and savannah in
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Somalia, Ethiopia, Eritrea, Kenya, Tanzania and eastern
Uganda (O’Shea 1991) (Figure 9). A century ago reported
for Sinkat (Anderson 1902) in what is today Sudan, but
current presence in Sudan questioned by O’Shea (1991).
Remark. – Xerus rutilus is reviewed in O’Shea (1991) and
Waterman (2013c).
Genus Euxerus Thomas: Striped ground
squirrels
Euxerus Thomas, 1909, p. 473. Type species is Sciurus
erythropus E. Geoffroy.
Tenotis Rafinesque 1817 , p. 362. Type species is Tenotis
griseus Rafinesque. Tenotis griseus is listed in Palmer
(1904: 668) and Kretzoi and Kretzoi (2000: 403) but
ignored in other nomenclatural sources. Rafinesque
proposed T. griseus under “Sciurus erithopus. Geoffr.”
(a misprint for erythopus) and defined Tenotis as
“contain[ing] all the squirrels with pouches [...] who
live under ground”; as such Tenotis does not match
Xerini which lack internal pouches. Locality for T.
griseus is not known and we propose the name Tenotis
as not identifiable (nomen dubium).
Content. – A monotypic genus, containing only
E.erythropus.
Euxerus erythropus (É. Geoffroy Saint-
Hilaire): Striped ground squirrel
Sciurus eyrthoupus (sic) É. Geoffroy Saint-Hilaire, 1803, p.
178. Type locality: “Inconnue” (=unknown). A speci-
men from Senegal, acquired by Florent Prévost in
November 1820 and deposited in Muséum National
d’Histoire Naturelle, Paris (MNHN-ZM-MO-2000-601),
was designated as neotype (Rode 1943). Type locality is
therefore (“probably”) Senegal (Allen 1954). The ICZN
(1971: 224) ruled erythoupus by Geoffroy Saint-Hilaire
to be an incorrect original spelling for erythropus,
placed erythoupus on the Official Index of Rejected
and Invalid Specific Names in Zoology, and validated
the emendation of the specific name erythoupus to
erythroupus. Wilson and Reeder (1993) regarded Geof-
froy Saint-Hilaire (1803) (“a very rare book”; Jentink
1882) as not validly published, what was rebuffed in
Corbet and Hill (1994); with reference to Hill 1980).
Six subspecies were recognized by Amtmann (1975) and
tentatively mapped in Herron and Waterman (2004).
Etymology. – “Eu” is Greek for “typical”+Xerus; i.e. “a
typical bristly ground squirrel”. The species name eryth-
ropus is from “eruthros” (red) and “pous” (a foot, both
Greek), i.e. “a red-footed”, although “there is nothing to
indicate why Geoffroy should have chosen the name... as
it is [red-footed] in fact not one which has any particular
application to any known form [of E. erythropus]” (Rose-
vear 1969: 132); note the above claim by Hollister (1919)
who stated that feet and other parts of body are often
stained with the soil what changes the color.
Diagnosis. – Euxerus erythropus is a large member of the
subtribe Xerina, recognizable by a combination of flank
stripe (Figure 2), narrow skull (Figure 6), and a high inci-
dence of the 3
rd
upper premolar (present in ~80% of indi-
viduals; Figure 8). The ears are moderately large, with
tragus present. Metatarsal pads are absent and plantar
pads are more reduced in size than in any other African
species (Pocock 1922). Females have two (Figure 5) or three
pairs of nipples (mean=2.71±0.469, n=14). The baculum
(length=8–9 mm) consists of a cylindrical proximal part and
distal compressed blade; the dorsal crest ossifies only partly
(Pocock 1923). The Y chromosome is acrocentric (biarmed in
the remaining Xerini). The jugal bone is bluntly truncated
against the lacrimal (i.e. without a short wedge-like exten-
sion between the lacrimal and maxillary; Figure 10).
Distribution. – Endemic to the Sudano-Guinean savannah
(Denys 1999). E. erythropus is a habitat generalist (Rose-
vear 1969) occupying a wide subtropical and tropical belt
between the equator and the transition of the Sahelian zone
and Sahara (Granjon and Duplantier 2009, Monadjem etal.
2015). Range extends from the Atlantic coast in the west to
Eritrea, western Ethiopia and north-western Kenya in the
east (Figure10). There is an isolate in the Souss region in
western Morocco (Blanc and Petter 1959). Remnants of the
Neolithic age from Bir Kiseiba in southern Egypt (Osborn
and Osbnornová 1998) are another evidence of a wider
occurrence in Palaearctic Africa during the Holocene. The
19
th
century records for Egypt (Jansen 1882) and “Nubia”
(Supplemental Appendix 2) however most probably refer to
what is now Sudan (cf. Anderson 1902).
Remarks. – Euxerus erythropus is reviewed in Rosevear
(1969), and (as Xerus erythropus) in Herron and Waterman
(2004) and Waterman (2013b).
Genus Geosciurus Smith: South African
ground squirrels
Geosciurus Smith 1834, p. 128. Type species is “X. capen-
sis” (synonym of Sciurus inauris Zimmermann), sub-
sequently designated by Thomas (1897, p. 933).
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Content. – Geosciurus contains two species which differ
morphologically (de Graaff 1981, Herzig-Straschil et al.
1991) and in nucleotide sequences (Herron etal. 2005).
Geosciurus inauris (Zimmermann): Cape
ground squirrel
Sciurus inauris Zimmermann 1780, p. 344. Type locality
is “Kaffirland, 100 miles north of the Cape of Good
Hope” (Skurski and Waterman 2005).
A monotypical species which however includes three
deeply divergent phylogeographic lineages (Herron etal.
2005).
Geosciurus princeps Thomas: Damara
(Kaokoveld) ground squirrel
Geosciurus princeps Thomas, 1929, p. 106. Type locality is
“Otjitundua, Central Kaokoveld, Namibia, Africa.”
A monotypical species.
Etymology. – The name Geosciurus is derived from “geos”
(Greek for earth)+Sciurus (Greek for a squirrel, from “skia”
for “shade”+“oura” for “tail” (both Greek), i.e. “a shade-
tail” “on account of the way a squirrel holds his bushy
tail over his back” (Gotch 1995); Geosciurus is therefore
“a ground squirrel” (allusion on its habits). The species
name inauris consists of “in” (not, without)+“auris” (ear;
both Latin) in allusion “to the very small ear pinnae of the
species” (de Graaff 1981). The name princeps (Latin for
“first” or “primary”) “may refer to the larger than average
size, brighter coloration and more profusely ringed tail of
this species in contrast to the somewhat smaller, drabber
inauris.” (de Graaff 1981).
Diagnosis. – More fossorial than other African bristly
ground squirrel. Size is large, fur is bristly; flanks with a
stripe (Figure 2); hind foot robust, metatarsal pads absent;
the ear extremely reduced to a rounded thickened rim,
tragus absent; two pairs of nipples (posterior abdominal
and the inguinal). Baculum (length is 8mm in G. inauris)
consists of long proximal cylindrical portion and elon-
gated distal part; the upper surface of the blade is narrow
and strongly constricted; dorsal crest is long (Pocock
1923). Skull is broad and deep, with a short rostrum and
elongate braincase (Figure 6); jugal bone is bluntly trun-
cated against the lacrimal. Cheek-teeth are relatively hyp-
sodont; the 3rd upper premolar is absent (Figure 8).
Distribution. – The genus Geosciurus is endemic to Zam-
bezian savannah (Denys 1999; Figure 9); G. inauris occupy
open savannahs in Botswana, Republic of South Africa,
and Namibia (Herzig-Straschil 1979) but possibly disap-
peared during the last century from Zimbabwe (Skurski
and Waterman 2005). G. princeps is restricted to the western
escarpment in Namibia and very marginally occurs in
Republic of South Africa and Angola. Although ranges of
the two species overlap, they select different habitats and
segregate in behavior (Herzig-Straschil and Herzig 1989).
Remarks. – Both species of Geoscirus are well covered
(as Xerus) in general faunal reviews of the mammals
occupying the southern African subregion (de Graaff
1981, Skinner and Chimimba 2005). For other reviews
Figure 10:Anterior zygomatic arch in three genera of Xerini to show differences in a suture between the lacrimal (lac), the maxillary (max)
and the jugal (ju) bones. 1 – Spermophilopsis leptodactylus (NMW 32092); 2 – Atlantoxerus getulus (NMW 43000); 3 – Euxerus erythropus
(ZFMK 97.472). Arrow points on a wedge-like extension of the jugal between the lacrimal and maxillary in Spermophilopsis and Atlan-
toxerus. A bluntly truncated top of jugal bone at the lacrimal bone which is distinctive of sub-Saharan Xerina, is shown by triangle. Not to
scale.
Unauthenticated
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B. Kryštufek etal.: Bristly ground squirrels Xerini
15
see Skurski and Waterman (2005), Waterman and Herron
(2004) and Waterman (2013d,e).
Genus Atlantoxerus: Barbary ground
squirrels
Atlantoxerus Forsyth Major, 1893, p. 189. Type species is
“X. getulus (Gesn[er])” (=Sciurus getulus Linnaeus).
Atlantoxerus was proposed as a subgenus of Xerus.
Scope. – A monotypic genus, containing only A. getulus.
Atlantoxerus getulus (Linnaeus): Barbary
ground squirrel
Sciurus getulus Linnaeus 1758, p. 64. The type locality
(“Habitat in Africa” = Lives in Africa) was restricted to
“Barbary” (= Mediterranean Africa between Egypt and
the Atlantic coast) by Thomas (1911: 149), and to “Agadir”
(Morocco) by Cabrera (1932: 217). On p. 218 Cabrera justi-
fied this step as follows (our translation from Spanish):
“(1) Imports of animals and other goods from Morocco
in the 17
th
and 19
th
century came mostly from the port
“Santa Cruz de Berberia”, the current name of which is
Agadir. Examples are squirrels figured in the painting
“Arche Noah” by the Dutch artist P. Breughel [actually
Jan Breughel the Elder, 1568–1625], now in the Prado in
Madrid [Prado holds one of the later versions while the
original is in the J. Paul Getty Museum; Kolb 2005], and
in the book by Gessner from 1551. The picture in Gessner
subsequently inspired Ray (1693, Synops. Method.
Anim. Quadrup., p. 216) to discuss this squirrel. (2) Lin-
naeus based his name on the reports of Ray (as above),
and of Edwards 1751 (A natural history of birds, vol. 4,
plate 198), who reported and figured a squirrel from
“Santa Cruz (on the Western Coast of Barbary, border-
ing on the Atlantic Ocean)”. The specimen figured in
Gessner (1551), argues Cabrera, should be regarded as
the type of the species.
No subspecies are recognized.
Etymology. – The name Atlantoxerus was coined from Greek
“Atlas” or “Atlantos” (=the Atlas Mts. in Morocco)+“Xerus”
(dry in Greek) in allusion to the arid habitat. The species
name is derived from Gaetulia (Romanized for a Berber
Getulia), an ancient district in Northern Africa around the
Atlas Mts.
Diagnosis. – The smallest species of Xerini, and the
only one having a light spinal stripe (Figure 2), present
metatarsal pads, a paired interparietal bone (Figure 7),
upper incisor with traces of a groove, and brachiodont
and bunodont cheek-teeth. Among the African Xerina,
Atlantoxerus is unique in having rough, but not bristly
(spiny) fur, four pairs of nipples, exposed orifice which is
not sheltered by a tragus, in retaining the parieto-inter-
parietal suture (Figure 7), and in having a short wedge-
like extension of the jugal bone between the lacrimal and
maxillary (Figure 10). Baculum (length=7 mm) has a long
proximal portion and simple blade which is asymmetrical
in dorsal view and has a medial crest (Pocock 1923). The
3
rd
upper premolar is present (Figure 8).
Distribution. – Endemic to north-western Africa (Figure9)
in Morocco and present very marginally also in western
Algeria (Aulagnier and Thevenot 1986, Kowalski and
Rzebik-Kowalska 1991). In 1966–1970 introduced to
Fuerteventura, the Canary Islands (Bertolino 2009).
Prefers open rocky habitats.
Remarks. – Atlantoxerus getulus is reviewed in Aulagnier
(2013).
Subtribe Spermophilopsina Ognev:
Long-clawed ground squirrels
Spermophilopsinae Ognev 1940, p. 432. Type genus is
Spermophilopsis (by tautonomy).
Genus Spermophilopsis Blasius:
Long-clawed ground squirrels
Spermophilopsis Blasius, 1884, p. 325. Type species: Arcto-
mys leptodactylus Lichtenstein, 1823.
Content. – A monotypic genus.
Spermophilopsis leptodactylus (Lichtenstein):
Long-clawed ground squirrel
Arctomys leptodactylus Lichtenstein, 1823, p. 119. Type
locality is “140 Werst diesseits Buchara”, interpreted
as “vicinity of Kara-Ata, 140 km north-west from
Buchara, Uzbekistan” (Ognev 1940: 452). Thorington
etal. (2012: 202) erroneously fixed the type locality to
“Dagestan, Russia”.
Gromov and Erbajeva (1995) recognized three subspecies
which differ in size and color.
Etymology. – “Spermophilus” (a genus of ground squir-
rels) from “sperma” (seed) and “phylos” (loving; both
Unauthenticated
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16
B. Kryštufek etal.: Bristly ground squirrels Xerini
Greek) in allusion to the animal’s principal food+“opis”
(Greek) “of appearance”; i.e. “of same appearance as
ground squirrel”. The species name is from “leptos”
(slender)+“dactylos” (finger, both Greek), on allusion on
slender fingers bearing excessively long claws.
Diagnosis. – A large and short-tailed bristly ground
squirrel with a seasonally dimorphic pelage (bristly and
sparse in summer, long, dense and silky in winter); dorsal
color is plain, with no stripes (Figure 3). The external ear
is extremely reduced to a rounded thickened rim, the
tragus and the antitragus however are present. Soles and
plants are densely clothed with hair; the pollex is clawed;
claws on the remaining digits are heavily thickened and
enlarged (>10mm in length) (Figure 4); 1 tuft of supraor-
bital vibrissae. Melanocits are present in the cerebral dura
mater (Sokolov 1963). Skull is wide and deep, with short
braincase (Figure 6); external meatus acusticus has a bony
tube; the parieto-interparietal suture is retained in adults;
jugal bone has a short wedge-like extension between the
lacrimal and maxillary (Figure 10); buccinator and mas-
ticatory foramina fused. Cheek-teeth are strongly hyp-
sodont; the 3
rd
upper premolar is present (Figure 8).
Distribution. – The long-clawed ground squirrel is
restricted to sandy deserts (“peski” in Russian) of Central
Asia, from the Caspian Sea in the west to Lake Balkash in
the east, and from the Sea of Aral in the north to northern
Afghanistan in the south (Figure 9). The majority of distri-
butional area is in Turkmenistan, Uzbekistan and south-
ern Kazakhstan.
Remarks. – Abundant information on various biological
issues of Spermophilopsis leptodactylus exists in Russian
(Sludskiy etal. 1969, Komarova 1980, Zubov and Svidenko
2005) which however is unknown to the English speaking
community (cf. Thorington etal. 2012). For general review
in English see Ognev (1966) and for a study of the ecology
(in French) see Ružić (1967).
Conclusions
1. Bristly ground squirrels (tribe Xerini) inhabit arid
regions of Central Asia and Africa. Their disjunctive
range witnesses a much more extensive former distri-
bution. The group is known since the Late Oligocene.
In the Middle Miocene the Xerini peaked in range
expansion and abundance but declined afterwards.
Despite of a dense fossil record, the group was never
diverse taxonomically.
2. Extant Xerini are arranged into six species and three
genera of which Atlantoxerus and Spermophilopsis are
monotypic. The genus Xerus is further split into three
subgenera.
3. Phylogenetic reconstruction based on mitochondrial
gene for cytb retrieved deep divergences in African
Xerini, which are of comparable magnitude to those
among genera of Holarctic ground squirrels in the
subtribe Spermophilina (subfamily Arctomyinae).
Herein we recognize two genera (Euxerus and Geo-
sciurus), formerly incorporated in Xerus, which are
clearly distinct in external, cranial and dental mor-
phology, occupy discrete ranges and show specific
environmental adaptations.
4. A multigenic phylogenetic reconstruction by Fabre
et al. (2012) nested Atlantoxerus within the African
Xerini. This may be an artefact of incomplete genetic
sampling across taxa which left a high proportion of
missing values in the data matrix. Our cytb recon-
struction and morphological analyses, together with
published odontological analyse by Denys et al.
(2003) suggest Atlantoxerus to be in a sister position
against the remaining African taxa. All analyses con-
firm the sister position of the Asiatic Spermophilopsis
against the African Xerina.
5. We propose Tenotis Rafinesque, 1817 (type species is
Tenotis griseus Rafinesque, 1817), which is occasion-
ally synonymized with Euxerus, as a not identifiable
name (nomen dubium).
6. Generic classification for the African Xerina proposed
herein:
Family Sciuridae
Subfamily Xerinae, new content
Tribe Xerini
Subtribe Xerina
Genus Xerus, new content
Genus Euxerus, new rank
Genus Geosciurus, new rank
Genus Atlantoxerus
Subtribe Spermophilopsina
Genus Spermophilopsis
Acknowledgments: Many people helped in this study by
providing information and advice. We thank (abc) Cécile
Callou (Muséum national d’Histoire naturelle, Paris),
Pepijn Kamminga (Naturalis Biodiversity Center, Leiden),
Vladimir Vohralik (Department of Zoology, Charles Uni-
versity, Prague), and Neal Woodman (National Museum
of Natural History, Washington D.C.). For access to col-
lections (cf. Supplemental Appendix 2 for collection acro-
nyms) we thank: Eileen Westwig (AMNH), Paula Jenkins
and Roberto Portela Miguez (NHML), Linda K. Gordon
(NMNH), Barbara Herzig and Frank Zachos (NMW), Katrin
Unauthenticated
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B. Kryštufek etal.: Bristly ground squirrels Xerini
17
Krohmann (SMF), Alexandr Pozdnyakov (SZM), Galina
I. Baranova, Nataliya Abramson and Alexandra Davy-
dova (ZMSP). For providing photographs of animals and
granting permits to reproduce them in this paper we are
grateful to (abc) Alenka Kryštufek (Ljubljana, Slovenia),
Emmanuel Do Linh San (Fort Hare, Republic of South
Africa), Klaus Rudloff (Berlin, Germany), and Nedko
Nedyalkov (Sofia, Bulgaria). Two anonymous referees pro-
vided valuable comments on an earlier draft. Visit of B.K.
to London received support from the SYNTHESYS Project
http://www.synthesys.info/ which is financed by Euro-
pean Community Research Infrastructure Action under
the FP7 Integrating Activities Programme.
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