1. Lina Mikolajczyk 1
Spermophilus and alarm calling evolution: a novel method for phylogenetic analysis
Recent phylogenetic re-evaluations in the Rodentia order have sparked quite a controversy
amongst the ground-squirrel (Spermophilus) studying researchers. Indeed, Rodentia encompasses
one of the largest groupings of species, and thus rapid speciation and diversification is often seen,
requiring close attention to phylogenetic relationships. In fact, rodents were already highly
diversified in the Paleocene and Early Eocene, and have since experienced an explosive speciation
(Herron, et al., 2004). Rodents are divided into Sciurognathi and Hystriocognathi, based on the
angle of jaw and incisor position (Herron, et al., 2004), and further, into: Anomaluromorpha (scaly-
tailed flying squirrels, springhares), Castoridae (beavers), Ctenohystrica (gundi, porcupines, guinea-
pigs), Geomyoidea (pocket gophers, pocket mice), Gliridae (dormice), Myodonta (rats, mice,
jerboas), and Sciuroidea (mountain beavers, squirrels, woodchucks) (Herron, et al., 2004). The
clade, Spermophilus, in the order Rodentia, suborder Sciurognathi, family Sciuridae, accounts for
all ground-dwelling squirrels, marmots, and prairie dogs. The sciurid family, colloquially known as
squirrels and allies, includes 51 genera and 278 species and is the third most diverse family of the
order Rodentia. Many sciurids are ground dwellers and some are burrowers, but most of them
(including the flying squirrels) are tree dwellers (Blanga-Kanfi, et al., 2009). Mitochondrial DNA
sequencing of cytochrome b has shown that the genus Urocitellus (ground squirrels), formerly
classified under Spermophilus, is paraphyletic to prairie dogs and marmots, and thus the entire
Spermophilus clade has had to be re-defined. Spermophilus has now been split into the following
clades (Figure 1) (Helgen, et al., 2004): Notocitellus, Ammospermophilus, Otospermophilus,
Callospermophilus, Xerospermophilus, Cynomys, Poliocitellus, Ictidomys, Marmota, Urocitellus,
and Spermophilus sensu stricto. The following table compares distinctive cranial characteristics that
have been used to create these new clades:
Table 1: (table created by LM, compiled from descriptions from Helgen, et al., 2004, Jenkins et al., 1984, Eshelman, et
al., 2000, Bryant, et al., 1945, Sloan, et al., 2005, Michaux, et al., 2008, Elliot, et al., 1984, listed in order of most to
least usage)
Notocitellus (tropical
and ring-tailed ground
squirrel)
Rounded braincase,
blunt rostrum with
very short incisive
foramina;
opisthodont,
anteroposteriorly
deep incisors
Weak expansion
in zygomata
Large and broad auditory
bullae, closed supraorbital
foramina
Brachyodont molars,
parastyle ridge on M1
and M2 joins the
protocone, small P4
and an even smaller
P3 without changing
direction
Ammospermophilus:
sister to notocitellus
Short and narrow
nasals
Short angular process
of the dentary, smaller
2. Lina Mikolajczyk 2
(antelope squirrel) teeth than Notocitellus
(especially P3)
Otospermophilus:
(rock and California
squirrels)
skull superficially
resembles
Poliocitellus, but has
less elongate rostrum
and incisive foramina
along with the listed
characteristics
Large, but not
particularly wide
skull, rounded
braincase
Very large auditory
bullae, open supraorbital
foramina
Large molars, small
P3, orthodont and
opisthodont incisors,
long incisive
foramina, brachyodont
molars
Callospermophilus:
sister to
Otospermophilus
(golden-mantled
squirrels)
Moderate rostrum Very large pinna Postorbital processes are
long and very slender
Orthodont/opisthodont
incisors, long and
narrow incisive
foramina, P3 is
moderate, upper
incisors are slender,
not distinctly recurved
Xerospermophilus:
Mohave, round-tailed,
spotted, perote
squirrels
Delicate skulls, blunt
or long rostra, narrow
braincases
Short postorbital
processes, proportionally
large auditory bullae
Opisthodont incisors,
short incisive
foramina, upper
incisors are gracile,
opisthodont
Cynomys: sister to
Xerospermophilus
(prairie dogs)
Large and wide
zygomata
Large and well-defined
auditory bullae
Proportionally
distinctive incisors,
molars, and premolars,
as well as length of
angular process of
dentary compared to
other medium sized
squirrels, large
divergence of
toothrows
Poliocitellus: very
carnivorous, eats
mammals, birds, toads,
insects, and plants,
fruits, seeds
(Franklin’s Ground
Squirrel)
Very narrow
braincase, longest
and most tapering
(not parallel-sided)
rostrum, broad nasals
Narrow zygomata Wide interorbital region,
weak postorbital
processes, less laterally
elongate meatal portion of
auditory bulla
Long incisive
foramina, small
bicuspidate P3, heavy
incisors, low crowned
cheek teeth
Dietary choice: eggs
Ictidomys: thirteen
lined ground squirrel
Distinctly narrowed
skull, elongated and
distinctively
downward sloping
rostrum, dramatically
narrowed braincase
Delicate postorbital
processes, very small and
laterally compressed
auditory bullae
Stout and very
opisthodont upper
incisors, small cheek
teeth, expansive
diastema that
separates cheek teeth
from incisors, abrupt
change in direction in
the protocone that
joins the parastyle
ridge on M1 and M2
Marmota: in a sense,
the outgroup, includes
all marmots
Smallest eyes, a
nearly flat dorsal
profile, have the most
massive rostrum,
which is also short
Quadrate optic
groove
Very narrow postorbital
constriction, very
prominent nuchal crest,
paroccipital processes
project ventrad well
slender, curved, and
stout upper incisors,
with the enameled
surfaces usually
longitudinally grooved
3. Lina Mikolajczyk 3
and broad below the level of the
tympanic bullae, the
basioccipital bone is
concave ventrally and
does not have a sagittal
ridge, and the processes
on the basioccipital
medial to the tympanic
bullae arise from the
middle of the
ventrolateral margins of
the bone
Urocitellus: 12 species,
most widely studied
ground squirrels for
social and prey
behavior
Cranially very small,
long and parallel
sided rostra, broad
braincase, high
domed braincase
Broad zygomata,
mesopterygoid
fossa is not
narrowed,
occipital
condyles are least
expansive
Smallest auditory bullae
proportional to its size
with the meatal portion
being disproportionally
laterally elongated and
forms an elongated tube
very long postorbital
processes (that are also
well-developed),
interorbital space is very
wide, but, proportionally
to the postorbital width, it
is strangely narrow
Gracile incisors, short
incisive foramina,
large and heavy P3
(proportional to its
size)
Spermophilus sensu
stricto
Heavy postorbital
processes (very
distinctive), causing easy
differentiation from
Urocitellus
4. Lina Mikolajczyk 4
However, as
descriptive as these
characterizations may be,
they are all relative to one
another (What is ‘relatively
wide’? What is ‘average’?
What is a ‘medium-sized’
squirrel? ) and are subject
to loose interpretation,
which is part of the reason
why so many phylogenetic
trees have been created and
later disputed. In addition,
the traditional approach to
phylogenetic analysis,
utilizing cytochrome b or
other mitochondrial DNA,
or even simplistic skull
bone comparison does not
seem to fully capture the
differences among species.
For example, in investigations of post-
cranial skeletal components such as the
scapula (Swiderski, et al., 1993), current phylogenies do not accurately reflect the evolution of this
cohesive bone as multiple separate pieces, even though this is the most likely origin of the scapula,
as assessed by Swiderski, et al.
Most evolutionary studies analyzing skeletal components do not exploit the readily
accessible information available about life styles of species. Of course, dietary, foraging, and
environmental changes are considered, but rarely are they considered in terms of cranial
morphology. In a recent study aimed at re-evaluating the species belonging to Marmota, tooth
morphology, chewing direction, and their effects on the mandible were considered. Marmota has an
Figure 1: Herron, et al 2004. A revised phylogeny of Rodentia
5. Lina Mikolajczyk 5
especially elongated mandible, a feature sometimes used to distinguish fossil marmots from ground
squirrels. The results were uniform; diet did not play an important role in determining the
morphological differentiation of the Marmota mandible (Michaux, et al., 2008) The relationships
between lifestyle and clades, lifestyle and diet, and clades and diet were unclear; however, their
investigation was not further pursued. Yet another study (Yom-Tov, et al., 2011) tried to determine
the effects of climatic changes, foraging range, and weather on skull size and differentiation, and
found no conclusive results. A similar study, performed by Caumul, et al., 2005, on marmots found
that body size accounted for only 10% of variation in skulls, 7% in mandibles, and 15% in molars.
The higher percentage of molar differentiation due to body size was explained through dietary
habits. However, the study later found that local vegetation explained only 7% of variation in skulls
(which was questionable with regards to statistical significance), 11% in mandibles, and 12% in
molars. When a dietary analysis was performed, however, higher variations manifested: 25% of
variation in skulls, 11% in mandibles, and an astoundingly low 9% in molars. Cytochrome b
mitochondrial DNA divergence (phylogeny) explained 15% of variation in skulls, 7% in mandibles,
and 5% in molars. The association of diet and skull shape was strong because the majority of its
components are related to mastication, especially teeth position, palatal shape, and location of
palatine and zygomatic origination of masseters (muscles of mastication). Despite the low
percentages of phylogenetic variance due to those factors, trees based on molar and skull shape
recovered most phylogenetic groupings correctly (correctly as compared to previously established
cytochrome b mitochondrial DNA analyses), but mandible shape did not recover trees of similar
phylogenetic groups nearly as accurately. Mandible shape variation was not associated with cranial
or body size, diet, and a large proportion of variance (65%) was left unexplained. Mandibles are the
most likely to be affected by life history and ecophenotypic effects, which are phenotypic variations
due to life style and station. In addition, the dietary contribution to tooth shape was surprisingly low.
Was it the lack of a dietary ecophenotypic component to molar shape? Or is it the out-of-ordinary
occlusion of marmot molars? We must ask, why was the mandible shape so bad at recovering
phylogeny, and skulls and molars, although better, still not as accurate as DNA analyses? These
studies along with many others not discussed here, have concluded that basic skull morphology is
often an unreliable indicator of phylogenetic relationships because of erratic, adaptation-driven
homoplasy (which is the uniform collection of mtDNA in all cells of an individual) and the
exclusion of other lifestyle factors in phylogenetic analysis (Caumul, et al., 2005).
6. Lina Mikolajczyk 6
It is easy to assess skeletal components in a reductionist manner, forgetting the individual
functions of parts. For example, although mandible studies most often concern themselves with
mastication, the jaws of vertebrates have many other functions, playing roles ranging from
vocalizations to social interactions (see kissing in Urocitellus, below). Perhaps a more profound
analysis of the mandible, in conjunction with its alternative functions, such as alarm calling (which
is well studied in ground squirrels and Marmota), could help delineate the genera of Rodentia. Thus,
I propose, through a comparison of commonalities in Urocitellus (See Figure 2 a,c) and the
seemingly standout and evolutionarily distinct Marmota (Figure 2 b,d) (which has been considered
a type of outgroup to Spermophilus by Cardini, et al., 2004, 2005), the exploration and inclusion of
other factors as influences on changing skull morphology. Their inclusion in comparative studies
may facilitate and further clarify phylogenetic relationships within the Rodentia order.
a) b)
c) d)
Figure 2: a) Urocitellus beldingi and
b)Marmota caligata c) Urocitellus
beldingi skull d) Marmota caligata skull
(Barash, et al, 1974, Jenkins, et al.,
1984)
One of the obstacles that
Cardini, et al. and many others
have encountered is the
7. Lina Mikolajczyk 7
commonly held belief that the sciurid skeleton has a propensity towards morphological convergence,
or the fabrication of synapomorphies in polyphyletic clades due to similar environmental pressures,
thus leading to inaccuracies in establishing monophyletic clades. As has been remarked by
previously cited studies, Cardini, et al. were similarly perplexed that even though phylogenies are
usually not constructed based on social behavior, some clustering reflects similarities in social
systems and communication mechanisms, like the joining of M. camtschatica with M. caudate.
Likewise, M. caligata is closer to M. flaviventris in phylogenetic analyses of ventral cranial shape,
even though it is closer in size, social behavior, and number of alarm calls between M. caligata, M.
vancouverensis and M. Olympus. Cardini, et al., 2005 took a different direction, and have proposed
that a high level of sociality evolved at least twice in marmots. They substantiated this social
evolution through a morphological analysis of the marmot’s and a variety of other Spermophilus
members’ (Ammospermophilus, Urocitellus, Cynomys) ventral craniums, and a comparison of their
social lifestyles. Marmots form large colonies, dig expansive burrow systems and feed prevalently
on plants and grasses. They are exceptionally large for the Spermophilus clade, and are the some of
the biggest hibernating members of Rodentia. Shape changes could be due to a long, distinct,
evolutionary history, but geographical isolation and dietary changes may have also contributed to
the shaping of skeletal characteristics. Petromarmota (a subgenera of Marmota) have an enlarged
ascending mandibular ramus, a narrow diastema and a posteriorly displaced mental foramen. An
enlarged zygomatic arch (and an elongated angular process of the mandible) could be
synapomorphic characters present in the ancestor of Petromarmota. The zygomatic arch and angular
process of the mandible are areas involved in mastication, and their modification in Marmota
(without significant dietary changes) points to the persistence of other factors. Cardini, et al
throughout their multiple studies thus propose that changes in social complexity and alarm
communication during marmot evolution might have affected the brain and sense organs (especially
the ear), and indirectly the shape of the cranium, and more specifically, the mandible. This claim
requires further investigation, and I will attempt to explore the relationship between sociality, alarm
calling and cranial modifications below.
In comparing social behavior within Spermophilus, among generalized Poliocitellus,
Urocitellus, and Marmota (Table 2),
Table 2: compiled from Eshelman, et al., 2000, Jenkins, et al., 1984, Pollard, et al., 2012, Bryant, et al., 1945)
Poliocitellus Urocitellus Marmota
Live alone or in pairs Some grouping, intolerant to all but
kin
Most social, grouping especially
between mother and young
(prolonged in comparison to other
8. Lina Mikolajczyk 8
Spermophilus)
Highly secretive, least social, practice
avoidance, exhibit threat displays and
growl when encountering others
Encounters with nonkin are frequent
in few weeks after emergence, but
decrease as season progresses. Most
interactions between mother and
young, and kin females. Kissing takes
place between adults during breeding
season and for juveniles: nose to nose
contact with head tilted and mouth
sometimes open. Oral glands on the
corner of mouth may be utilized.
Young may delay dispersal for one,
two or more years, adult males
participate in group life, and females
may aggregate in harems or
matrilines, but group cohesiveness
varies.
we see that even though general trends can be observed between the clades, even within
these clades, enough variation occurs that sociality as a sole phylogenetic characteristic would not
fare well compared to cranial analysis. Social living goes hand in hand with communication, but the
details of this relationship are not simple. An alarm call is a specific type of vocalization given in
response to a potential predatory threat. Alarm calls, which alert the surrounding animals of danger,
increase vigilance and are a defense mechanism. Sciurids often show predator specificity in alarm
calls and have a specific call type for aerial and terrestrial predators. These calls are typically loud
and perceptually salient, and they can be elicited and easily recorded by researchers. Sciurid studies
have found that social group size predicts alarm call individuality and size of repertoire (Pollard, et
al., 2012). Species vary in the acoustic structure of their calls and the size of their alarm call
repertoires. For species with multiple alarm call types, different call types may be used to
communicate about different types of predators. Species living in more complex social groups may
have greater need to signal alarm in a more complex manner and thus may use larger alarm call
repertoires. Across ground-dwelling sciurids, alarm call repertoire size varies from one to seven
(Pollard, et al., 2012). Urocitellus and Marmota, even though both, to some extent, are quite social,
have very different alarm calling systems.
Before we continue the relation of alarm calling to skull morphology, we must make sure we
consider that a learning component of alarm calling is not preventing an honest analysis. Since
juveniles emerging above ground from natal burrows do not discriminate behaviorally among the
many calls in Urocitellus, Mateo, et al., investigated the Urocitellus Beldingi alarm call learning
mechanisms. Their learning curve and ability to distinguish between different alarm calls depends
most on rearing history, mainly their pre-emergence exposure to other individuals, which, of course,
depends directly on sociality and how many young and other squirrels are in the burrows (Mateo, et
al., 2001, 2003). Returning to the relationship between sociality and anatomy, Van Vuren, et al.,
2012, found that there was a positive correlation between sociality and length of burrow systems,
9. Lina Mikolajczyk 9
and the authors speculate that multiple residents in one burrow performed by more social species
account for this. Thus, the comparison of Urocitellus and Marmota alarm calling is not affected by
their social systems, since they are both social species with many residents residing in burrows and
contributing similarly to learning of alarm calling. Thus, whatever learning component alarm
calling may have will be easily relatable to sociality and size, and may be discounted as a
prohibitive factor of our analysis.
Sound is produced by the larynx (sound source) with air flow that comes from the lungs and
then passes through air cavities of vocal tract, including the pharynx, oral and nasal cavities
(Volodina, et al., 2011). Sound frequency can be modulated by gape opening, length of the vocal
tract, and the vibratory frequency of vocal folds in the larynx. Thus, other conditions being equal,
the larger larynx with larger vibration structures should produce a lower fundamental frequency. It
would hold seem that heavier animals generally should produce calls of lower frequency. (Volodina,
et al., 2011) In addition, in mammals, the vocal tract is anatomically rigidly related to the skull
dimensions and strong correlations between the condylobasale skull length, the vocal tract osseous
structures, and body weight have been reported (Colak, et al., 2007). Colak, et al examined the body
weight, skull length values, and larynges in various Spermophilus genera, and, as expected, found
these values to be significantly smaller in juveniles than in adults (across all species, except for
Marmota). These differences, however, did not correspond to shifts in call frequencies that normally
accompany growth of the larynx and vocal tract with development. Colak, et al proposed that these
species may actively manipulate elements of their vocal apparatus, adjusting the alarm whistle
fundamental frequency (by varying the length of vibrating portion of vocal folds, aperture of gape,
etc.). Such manipulation would allow squirrels to sever the relationship between larynx size and call
frequency; however, they established that further physiological research is necessary to test this
hypothesis.
If body size were considered a true determinant of alarm calling frequency, then Marmots
should have the lowest frequency alarm calls. However, this has not been observed. Marmota
caligata exhibits 7 distinct vocalizations: long calls, descending calls, ascending calls, low-
frequency calls, growls, whining, and tooth chattering (Blumstein, 1999). They are described as
long- and short interval whistle, accelerando whistle, flight whistle, short alert whistle, ‘‘quee-uck’’
whistle, and yelp. Marmots have the largest repertoire of alarm calls in Spermophilus, and the
function of their calls is exactly the same as ground squirrels: calls serve as a warning against a
predator, as a response to growls, and after reaching refuge (Matrosova, et al., 2007). It is
10. Lina Mikolajczyk 10
interesting to note that Marmots generally did not differentiate between aerial and terrestrial
predators in their calls (Blumstein, 1999). More importantly, however, the frequency of Marmot
calls is comparable, and even more highly variable (have a bigger range) than those of ground
squirrels. (Blumstein, 1999)
Comparatively, within Urocitellus, although the repertoire of alarm calls is definitely lesser
in size compared to Marmots, distinction between each alarm call is made by adults (Leger, et al.,
1984, Jenkins, et al., 1984). Urocitellus Beldingi has two basic types of alarm calls: a brief chirp
that usually consists of a single note, and a more extended trill or churr that consists of several notes
in rapid succession. Chirps are associated with aerial predators or close terrestrial predators (more
danger). Although other alarm calls may have been observed within different species of Urocitellus,
their distinction is blurry, and origins may be subject to laboratory settings (Eshelman, et al., 2000).
During analysis of Urocitellus Armatus (the Uinta Ground Squirrel), more than just two alarm calls
were observed, but the novel ones (the ones not observed in other Urocitellus) seemed to be a
consequence of testing and disruption of social surroundings (when squirrels were placed in
enclosures together, they were not accustomed to their neighbors), manifesting in teeth clattering,
squeals, squawks, and growls. The calls that are best preserved throughout the genus are the ones
used for predator differentiation.
Now aware that body size and sociality are not the key characteristics for the larger breadth
of alarm calls in Marmota, we can examine whether Marmota are capable of adjusting their vocal
frequency because of anatomical characteristics. In addition, let’s examine some of the distinctive
cranial characteristics that have come to define these clades, and analyze their role in vocalization.
As previously discussed, one of the distinguishing characteristics of Urocitellus is their small and
thin auditory bullae proportional to its size with the meatal portion being disproportionally laterally
elongated and forming an elongated tube (Sloan, et al., 2005). Auditory bullae cover parts of the
middle and inner ear, which, of course, play a role in the ability to differentiate between different
alarm calls. Could it be possible that Urocitellus has evolved differential alarm calls due to their
relatively thinner and smaller auditory bullae?
The marmots, with their large repertoire of alarm calls, may also have a cranially-based
explanation. According to Bryant, et al., 1945, the maxilla has been one of the most altered bones in
the course of evolution in squirrels, specifically because of variation in the masseter muscle,
especially masseter lateralis (which has evolved due to diversified feeding). In Urocitellus and
Marmota, the external margins usually slant ventrolaterad, the bases are horizontal, and the
11. Lina Mikolajczyk 11
masseteric tubercles form pronounced elevations ventrolateral to the foramina. Since the superficial
part of the masseter takes its origin from the masseteric tubercle, this muscle is stronger in the forms
with larger masseteric tubercles, which are present in Marmots. Differences present in the region of
the infraorbital foramen are largely dependent upon this muscle, and the infraorbital foramina of
Marmots indicate a larger masseter. Zygomatic plate in both Urocitellus and Marmota forms a
around 50 degree angle with the basicranial axis, but the arch is relatively widened in Marmota in
comparison to other Spermophilus. The jugal bone forms the lateral margin of the ventral half of the
zygomatic plate, overlaps the maxilla in the ventrolateral part of the anterior surface of the plate and
forms an integral part of the zygomatic notch (Bryant, et al., 1945). Marmots have a proportionally
larger jugal bone and have expanded the deep masseter forward on to the rostrum underneath the
widened anterior root of the zygomatic arch (Cox, et al., 2012).
Bryant describes further how marmots and ground squirrels have a lesser width of the
interorbital region and a smaller size of the dorsal and lateral parts of the zygomatic plates, causing
them to have a narrow frontal process of the premaxillae. Marmota has a nearly flat dorsal profile,
very narrow postorbital constriction (which is the narrowing of the skull behind the eyes: its
narrowness is increased in species with bigger chewing muscles), strongly developed superior
nuchal crest (which connects to muscles that allow for increased scapular movement and muscles
involved in inspiration), and a very elongated mandibular. In addition, Marmots have a massive
rostrum that is laterally broad, and allows the passage of their heavy incisors without the formation
of large external swellings on the premaxillae (and no need for cheek pouches). The anterior margin
of the alveolar surface passes ventrad to join the diastemal part in a gradual curve, the junction is
almost at a right angle as a result of the greater depth of the body of the mandible in Marmots. The
increased size of Marmot mandibular, in combination with longer and stronger masseters, may
allow a larger width of gape (in comparison to Urocitellus).
In squirrels that possess cheek pouches, a small muscle runs from the anterodorsal part of
each pouch to the part of the premaxilla posterior to the alveolus of the incisor and anterolateral to
the incisive foramen. The place of origin is marked by a depression which is absent or small in the
sciurids that do not possess cheek pouches. The size of this depression varies directly with the size
of the pouch and the size of the animal. Bryant notes that this depression is faintly indicated in
Marmota, indicating that their cheek pouches are rudimentary. In Marmota, the rudimentary cheek
pouch is situated mostly dorsal to angle of mouth, and have only three muscles, which are derived
from buccinators: from the depression between the coronoid process and M3, on the dorsomedial
12. Lina Mikolajczyk 12
margin of diastema of ramus, and fossa posterior to alveolus of upper incisor. The tradeoff between
cheek pouch muscles and the masseter may also add to the Marmot masseter enlargement.
Urocitellus have larger cheek pouches and further specialization of muscles, but less masseter
elongation and stoutness, Bryant has observed. The anterior convergence of the zygomatic arches is
present in all ground squirrels. In marmots the squamosal roots are nearly horizontal, and the arches
are consequently more widely expanded posteriorly than in other Spermophilus. This results in the
widest posterior expansion and the greatest anterior convergence of the zygomatic arches (in
marmots). Although this has been linked to increased visual acuity, it also alters the location of the
masseter medialis pars anterior and pars posterior, which could also affect gape.
Why is the size of gape that important? Allowing gaping would increase the opening to the
larynx and pharynx, and having specialized and elongated masseters would allow for differential
fine tuning of this opening, allowing for differential aperture size, and a larger repertoire of alarm
calls.
Although Marmota have not been found to be able to differentiate between different alarm
calls, the elongation of their angular process may have two different manifestations in function.
There is a correlation between the ecotympnic bone which supports the eardrum and the length of
the angular process. (Sanchez-Villagra, et al., 1997). Some studies propose that the development
and acuity of hearing and the growth of the angular process may be closely related. For example, in
Marsupials, the length of the angular process can help sharpen hearing, allowing perception of a
bigger repertoire of frequencies (Sanchez-Villagra, et al., 1997). A second hypothesis is that an
elongated angular process is correlated with an increased masseter. There seems to be more support
towards the second explanation. The Marmot inability to distinguish between alarm calls may be
better explained by the fact that the postglenoid and subsquamosal foramina are joined, but are
better developed and separated in Urocitellus. These foramina are present immediately in front of
the external acoustic meatus, and play a role in auditory perception (Bryant, et al., 1945).
Further examples of distinctive cranial morphology leading to distinctive function/behavior
are present in other species. In a comparative study of Callospermophilus (specifically Lateralis and
Saturatus) and other Spermophilus (Eiler, et al., 2004) it was found that Callospermophilus at all
sites within this study vocalized at sound frequencies above 22 kHz, in the ultrasonic range. The
highest recorded vocalization of any Spermophilus, was in S. lateralis was 16 kHz at the University
of California’s White Mountain Research Station in eastern California (Eiler, et al., 2004). Eiler has
concluded that the alarm calls of golden-mantled ground squirrels typically extend into the
13. Lina Mikolajczyk 13
ultrasonic range. Callospermophilus is easily identified by their large pinna, small conchal lobe, and
the most inflated conchal cavity of the Spermophilus (Bryant, et al., 1945). The linkage of these
distinctive characteristics should be considered, seeing as they are defining characteristics of the
clade.
But we should not limit ourselves to alarm calling only. The size of the postorbital processes
varies widely depending on the kind of squirrel; but, in general, the processes are long and project
ventrolaterad and slightly posteriad in ground squirrels and prairie dogs, are long and project laterad
in marmots. The differences in interorbital width and in the part of the skull between the zygomatic
plates appear to result from the differences in the size of the anterior cranial fossa, which in turn are
correlated with the size of the olfactory part of the brain (Bryant, et al., 1945). Assuming that an
increase in the size of the olfactory part of the brain gives rise to differential acuity of smell, it
would be worthwhile to consider and compare the acuity of smell within Spermophilus. One way to
do this might be to consider kin recognition based on gland secretions (“kissing”) across various
levels of sociality in Spermophilus.
Now we must ask whether this is a valid conclusion: can we consider function of individual
cranial components as a way to delineate between genera? Scuirids are considered to be notoriously
prone to homeoplasmy of osteological characters, making it difficult to establish phylogenetic
relationships among similarly-sized ground squirrels (Cardini, et al., 2004, Elliott, et al., 1984). To
better define these relationships, the functionality of osteological characters should be considered,
especially those functions which may seem “alternative” to the conventional ones, such as alarm
calling to mastication. Whether the relation of the mandible in Marmots and their alarm calling is
valid cannot and will not be determined through a literature search. Physiological and anatomical
investigations can only confirm this hypothesis. Nonetheless, it is a worthwhile and fruitful attempt
to include individual bone functionality in phylogenetic analyses, not only for well-roundedness in
research, but for surprisingly constructive results.
14. Lina Mikolajczyk 14
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