CALIFORNIA STATE UNIVERSITY, NORTHRIDGE
SOUND COMMUNICATION IN THE
••
CALIFORNIA GROUND SQUIRREL
A thesis submitted in partial satisfaction
of the requirements for the degree of Master of Science in
Biology
by
Nurit !!_evy
August, 1977
The thesis of Nurit Levy is approved:
California State University, Northridge
August,
ii
1977
ACKNOWLEIX;MENTS
I wish to thank all the people who have helped and encouraged
me with this study.
Most of all I would like to express my
deepest thanks and appreciation to Dr. Jim Dole for the invaluable help he gave me throughout my stay at C.S.U.N.
I
wish to thank him for his enlightening suggestions, ideas, inspiring guidance, and for the kindness, patience and innumerable
hours he spent in thoughtfully reading the preliminary drafts
leading to this manuscript.
I also wish to thank him for his
most exciting and stimulating lectures which motivated me to do
this research and become involved with animal behavior.
I am also most grateful to Drs. George Fisler and Charles
Weston for their helpful suggestions.
Many thanks are extended
to Dr. Andrew Starret for providing me with his ultrasonic receiver; to Mr. Tom Haley who taught me how to use the sonagraph;
and to Mr. Tom Nayler who took very special care of it.
Sincere
thanks to Professor Pedro Durant who was a great help in the early
stages of the study, to Mr. Paul Abravaya for designing new
traps and to Mr. Jeff Werber for building them.
indebted to
¥~.
I am especially
George Boyle and Mr. Edward Boyle for permitting
the use of their ranch for this study and to Mr. Roger Beam for
his kindness and cooperation in providing access to the study
area whenever needed.
My most sincere thanks to Marilyn, for
her efficiency and enthusiasm in typing this manuscript.
iii
And
finally, I wish to thank all my fellow graduate students that
were of great help and encouragement throughout the study ,
particularly Betty Rose and Steve Lenchner, for whom my appreciation is boundless.
iv
TABLE OF CONTENTS
ABSTRACT
INTRODUCTION
MA.TERLA.LS AND METHODS
Study Area
Field Observation Procedure
Study of Captive Animals
Sound Analysis
RESULTS
Spectrum of Vocalization
1. Chatters
2. Squeals
3. Whistles
4. Grunts
5. Screams
6, Tooth chatters
Ultrasonic Sound
FUnctions .of Vocalization
a. Response to predators and potential
predators
Response to aerial predators
Response to ground predators
Response to conspecifics
Vocalizers
b. Vocalization used in intraspecific
encounters
1. Threat
2. Blocking
3. Supplanting
4. Chase
5. Fight
6. Sand kicking
7. Territorial disputes
8. Courtship behavior
Nature of Sound Used in Agonistic Behavior
DISCUSSION
LITERATURE CITED
v
viii
1
7
7
8
10
11
12
12
12
13
13
14
14
14
26
26
26
27
28
29
30
30
31
31
32
32
33
34
34
34
35
39
60
'
TABLES
Table
Page
1.
Characteristics of the "chatters" of the California
ground squirrel.
16
2.
Characteristics of the "squeal" of the California
ground squirrel.
17
3.
Characteristics of the "whistles" of the California
ground squirrel.
18
4.
Characteristics of "tooth chatter" of the California
ground squirrel.
23
Catalog of the vocalizations of the California
ground squirrel.
57
5.
vi
'
FIGURES
Page
Figure
1.
2.
Typical chatters of the California ground squirrel.
Adult chatters (A,B,C), a chatter emitted by a young
animal (D).
20
Squeals (A,B) and whistles (C) of the California
ground squirrel.
22
J.
Tooth chatter (A), pulsed grunt (B), two continuous
grunts (C), and scream (D) of the California ground
squirrel.
4.
A grunt emitted
which he shared
emitted during
at the point of
by a male while chasing a female
his burrows with (A), a grunt
male-male fight (B), a section taken
the arrow of the above grunt.
vii
38
ABSTRACT
SOUND COMMUNICATION IN THE CALIFORNIA GROUND SQUIRREL
by
Nurit Levy
Master of Science in Biology
August, 1977
The purpose of this study was to examine the vocal communication system of the California ground squirrel, Spermophilus
beecheyi.
Tape recordings of the sounds of marked squirrels were
made in the field, while concurrent notes were taken on the behavior of the animals; feeding boxes were used for intensifying
interactions among individuals,
from captive squirrels.
Supplementary data were collected
The recordings were analyzed with a
sonagraph.
On the basis of their physical properties, vocalizations fell
into six distinct groups:
screams and tooth chatter.
chatters, squeals, grunts, whistles,
By combination and repetition of
these sounds, the use of the same sounds in different contexts,
and the use of graded signals, the number of messages used for
viii
communication was increased.
in response to predators:
Two types of alarm calls were given
squeal indicated an immediate alarm;
a long call (chatters followed by repeated signals) served as an
alerting signal for less immediate danger.
Females were found to
be more alert than males and gave most of the long alarm calls.
A whistle was emitted during sexual chases.
During agonistic
encounters, grunts and chatters were used in association with
domina...'1.ce and a tendency to attack, while a squeal was used to
indicate subordination and a tendency to flee.
Some sounds
(grunts, screams and tooth chatter) were found to be associated
with territorial defense.
ix
INTRODUCTION
Communication has been defined as "an action on the part of
one organism that alters the probability pattern of behavior in
another organism in a fashion adaptive to either one or both of
the participants (Wilson,
1975). Its advantage to any species
lies in the potential for transmission of adaptive information
among the groupmembers.
Indeed, communication is an essential
part of social organization, for the ability of group members to
communicate makes social bonds possible.
As might be expected,
among vertebrates, a correlation tends to exist between the degree of social integration within a species and the complexity
of the communication system of that species (Fisler,
Barash,
1970;
1977) .
The emission of sounds is but one possible means of cornmunication, but the rapidity of sound transmission over great
distances and through objects and vegetation makes it well adapted
for information transfer in many circumstances.
Its importance
is readily documented by its widespread occurrence among the
vertebrates, for the use of sound signals is well known in all
groups except the reptiles.
For instance, many species of fish
use sounds for attraction between sexes, defense against other
species, threat and schooling (Moulton,
1963). Amphibian calls
are well known to serve in mating, maintaining territories, for
warning and for signaling release from clasping in copulation
1
2
(Blair, 1968).
Sound emission in reptiles, although minimal,
is associated in some groups with reproductive activity and territoriality (Pope, 1946; Evans, 1961).
Bird vocalizations
include complex songs, thought to accomplish functions associated with courtship, territorial and aggressive behavior,
and simple call notes serving for alarm, distress, bond maintenance, flocking, nesting, and attracting other individuals
to food sources (Stokes and Williams, 1972).
Mammals typically
have a well-developed vocal organ and many species have highly
developed sound communication systems. ·Primates have been
studied extensively in this regard.
In one species, the vervet
monkey (Cercopithecus aethiops), 21 different situations have
been found to cause distinct sounds, including several different
agonistic calls, distinct alarm calls for different predators
in different proximities, and different infant sounds (Struhsaker,
1970).
Vocalizations in rodents are also widespread and in some
species extend into the ultrasonic range.
Peromyscus nasutus,
for instance, vocalizes up to 100KHz (Sebeok, 1968).
A very
elaborate vocal display known is the "song" of the humpback
whale (Megaptera novaegliae) analyzed by Payne and McVay (1962),
which is thought to serve in identifying individuals and keeping
groups together during migrations.
As among vertebrates in general, in some groups of land
mamrnals it has been demonstrated that the extent of vocal repertory correlates with the degree of sociality.
Among Canids,
for instance, foxes (Vulpes vulpes), characterized by relatively
3
solitary and asocial behavior patterns, show a more limited
vocal communicatory repertory than do wolves (Canis lupus)
whose social organization is much more complex (Fox, 19?0).
Similarly among primates, chimpanzees (Pan troglodytes), the
socially most advanced of the nonhuman primates, well-known for
their extraordinary cooperation, possess a rich repertory of
sounds composed of 25 signals (Busnel, 1963), whereas the less
social gorilla (Gorilla gorilla beringei) employs only 16-17
vocal displays.
In rodents, a study by Fisler (1970) also shows
that the number and complexity of acoustical signals varies
from the more socially organized guinea pig (Cavia
porcellus)~
to the less social mouse (Reithrodonto~ys megalotis), whereas
the least number of sounds is used by the unorganized jird
(Meriones unguiculatus).
A similar relation occurs among squirrels.
The black
tailed prairie dog (Cynomys ludovicianus), which lives in a very
highly organized social system, employs an exceptionally rich
repertory of auditory signals.
It emits nine different sounds
for different intensities of alarm, intra- and interspecies
threat, contact, distress, apprehension and pleasure (King, 1955;
Waring, 1967).
The Olympic marmots (Marmota olympus merriam),
which live in distinct, well-integrated colonies, have an auditory communication system composed of seven calls used to indicate alarm, distress, departure of a predator, yearling fights
and more vigorous adult fights (Barash, 1973).
The colonial
yellow bellied marmot (Marmota flaviventris) is also knoWn to
4
possess a vocal repertory of seven distinct vocalizations
aroused by different stimulus situations (Waring, 1966).
As
reported by Brand (1976), the chipmunk (Eutamias townsendii), a
relatively social squirrel, also uses seven calls for communication.
Several are used as alarm calls and the rest in agonistic and
courtship situations.
On the other extreme of the social scale,
fox squirrels (Sciurus niger) live thinly scattered and appear
to be rather solitary.
A study of
~.
!!.• shermani revealed only
two kinds of barking noises (Moore; 1957); ~· !!.• rufiventer is
said to possess a repertory of several different calls, most of
them given during chase ( Zelley, 1971) •
No other sounds are used
in social contexts.
The social ground squirrels fall somewhere between the
prairie dogs and the solitary squirrels in their degree of social
organization and accordingly might be expected to have a sound
system of intermediate complexity.
Matocha (1975), working with
Spermophilus tridecemlineatus, found the animals to have a vocal
repertory of six distinct call types used to signal alarm, to
call young, and for threat.
In the arctic ground squirrel
(Spe:rrnophilus undulatus), the sound communication system is also
based on six distinctly different sounds which in combinations
or through repetition provide additional signals.
Several of
these signals serve as distinctive alarm calls for ground and
aerial predators (Melchior, 1971).
Other detailed descriptions of sounds of social ground
squirrels have not yet been reported.
Indeed, the most common
5
ground-dwelling squirrel in California, the Ca)..ifornia ground
squirrel (Spermophilus beecheyi) has not yet been well studied
in this regard, although the general behavior and ecology of
this animal have been studied by Linsdale (1946), Fitch (1948),
Evans (1949) and Owings (1977).
Communicative signals of the
California ground squirrel involve both vocal and mechanical
sound.s, the latter produced by the tail and coat of hair, scent
produced by the anal and dorsal skin glands, and tactile signals
(Linsdale, :!.949).
The vocalizations used in alarm situations
were subjectively described by both Linsdale and Fitch, without
the use of e1ectrospectrographic techniques.
Linsdale described
four different sounds made by trapped animals and three types of
vocalizations heard in the field.
Fitch mentions five sounds
that are modifications of the same basic.type of call and another
two different types of vocalizations.
Owings has presented
sonagrams of two different calls used in alarm situations, that
he suggests are relative.ly predator - specific with respect to
avian and mammalian predators.
None of the previous studies
have dealt with sounds emitted by the animals during any kind
of social interaction other than those used for warning.
A
strong tendency has been found in some groups of mammals, living
in open environments to social integration.
As reviewed by
Wilson (1975), this tendency has been demonstrated among ungulates,
most primates, and among severa.l species of rodents.
Examples of
rodents include the black-tailed prairee dog (Cynomys ludovicianus)
and the vole (microtus brandti) in open grasslands, the Arctic
6
ground squirrel (Spermophilus parryi) on the open tundra, and
marmots (Marmota) in Alpine meadows.
This correlation can also
be shown in the Columbian ground squirrel (Spermophilus columbianus),
"a creature of the open country" (Manville, 1959).
While living
in an exposed habitat, social life and a communal alarm system
might substitute for the cover of rocks and vegetation, as had
been suggested by Wilson (1975).
The California ground squirrel is .largely restricted to
open grasslands supporting short herbaceous growth (Evans, 1949).
Therefore, it seems reasonable, because of the apparent tendencies of mammals which live in open areas to have elaborate
social systems, and because of the relationship between the degree
of socialization of mammals and the degree of utilization of a
vocal communication systems, that the California ground squirrel,
~~own
to emit sounds, would employ a sound signal system.
It
was the goal of this research to investigate the vocalizations
of this animal using audiographic techniques, with an emphasis
on the sound signals used in social contexts.
As indicated above, the primary importance in studying the
California ground squirrel vocalizations lies in increasing our
knowledge of social communication.
have other value as well.
However, such a study could
Since the California ground squirrel
is the chief rodent pest of California, destroying crops and
serving as a reservoir for diseases, notably plague and tularemia
(~;vans,
1949), a better knowledge of its communication systems
. might be of value in developing a system for controlling the
7
species, as has been attempted for repelling starlings and crows
by broadcasting to them their recorded distress call (Frings,
1963).
:rt!ATERIALS AND METHODS
Study Area.
The main part of the study was based on field
observations conducted on Oat Mountain in the Santa Susana Range
north of the San Fernando Valley, in southern California The
hills of this range rise to 1143 m above sea level.
My study
area was located on slightly undulating topography at an elevation of
732 m.
It was on a cattle ranch which was fenced and
patrolled so that it was very rarely visited by human beings
other than the investigators.
The hills in the region are mostly of open grassland, with
a fair growth of herbs and grasses that dry up in summer, and
which are heavily grazed by cattle.
Valley oaks (Quercus lobata)
and coast live oaks (Quercus agrifolia) grow in the canyons and
as occasional scattered individuals.
In some areas, California
sagebrush (Artemisia californica) is common.
The most abundant
shrub is white sage (Salvia apiana) and.the more common herbaceous species which typically dominate the plant community are
Brassica nigra, Erodium cicutarium, Cryptantha micrantha,
Gnapt.ha1inm sp. and Avena sp.
Throughout the grassy area of
these hills, California ground squirrels are abundant.
Other
mammals that are known to use the area are mule deer (Odocoileus
8
hemionus), coyote (Canis latrans), bobcat (Lynx rufus), and
pocket gopher (Thomomys bottae).
The most frequently encountered
predatory birds were the red tailed hawk (Buteo jamaicensis)
and golden eagle (Aquila ch:cysaetos).
The natural predators
of the California ground squirrel observed, in order of their
frequency of appearance during this study, were red tailed hawks,
golden eagles, coyotes and bobcats.
The weather in the region of the study site is mild through
.
most of the year. Temperatures, on the average, .during summer
0
reach 27-32 C and occasionally go up as high as 43°C,
In winter,
average midday temperatures reach 16°C but at night may drop to
-7°C.
Precipitation falls mainly in winter, occasionally as
snow.
Very often during winter and spring, strong winds with
velocities exceeding 64 kph blow.
In such times the activity of
the squirrels is markedly diminished and only a few individuals
come out of their burrows and spend any time above ground.
Field Observation Procedure.
The field study began in
October, 1975 and continued until June, _1977.
Observations
were made through all seasons of the year, twice a week on the
average, during daylight hours.
The squirrels were typically
active from late morning to early afternoon during October March, and through the early morning and late evening hours
during the hotter monts, April - September.
Squirrels were trapped in Tomahawk livetraps or in homemade traps,
50
x
50
em, made of soft aviary wire.
Since re-
9
capturing of each individual every three months on the average
was necessary, the two different kinds of traps were used; squirrels
which had learned to avoid one kind, often readily entered the
other.
As bait, freshly cut pieces of apple dipped in peanut
butter were used,
When first captured, the squirrels were toe clipped for
per~anent
identification, weighed, sexed and color marked using
Rodol A fur dye applied as spots in various positions on the
body.
Numbers were assigned to the positions of the marks.
By
combining several spots any number up to 100 could be designated.
The reproductive condition of the animal, the position of the
testis in males, and the appearance of the vagina and the nipples
in females, was recorded.
On subsequent captures, the squirrels
were re-weighed, their fur was remarked if necessary because
of the loss of a mark due to molting, and notes were again taken
on reproductive condition.
The behavior of the animals was observed from a vehicle
parked inside the colony, using
7 x 35 binoculars. The squirrels
habituated very quickly to the presence of the car and ignored it.
During observations notes were taken on vocalizations, postures
and general behavior of individuals.
Specific attention was
paid to behavior patterns connected with conflict between two
or more squirrels.
Vocalizations were recorded on magnetic tape using a
UHER 4oOO Report-1 portable tape recorder set at
(11.3 em) per second.
7.5
inches
A Sony Electret Condenser Microphone -
50, was used with an AD -
38
windscreen, a tightly woven thin
cloth that excludes direct blasts of the wind when in use in the
field.
The microphone was placed close to a feeding box, 10-25 rn
from the car.
It was connected by a cable to the recorder in
the car, which was turned on and off as needed,
For the purpose of intensifying interactions among individuals,
feeding boxes filled with wild bird mix (a combination of d.roso
millet, red. millet, wheat, rape, corn and milo) i'l"ere used.
Each
box was built in a way that enabled only one animal to feed at
a time.
Typically at my arrival several boxes were set at
different locations in the colony.
After the squirrels had de-
tected the presence of the boxes and had begun visiting them,
some boxes were removed, leaving fewer out in order to induce
more interactions.
In the breeding season, when territorial
behavior was observed, the boxes were set at territorial boundaries where interactions were most likely to occur.
ililtside the
breeding season, the boxes were usually placed in a region where
there was a concentration of burrow entrances.
Study of Captive Animals.
In order to corroborate
~ield
data, captured animals were also studied from October, 1976 to
June, 1977,
The squirrels used were caught near the location of
the field study area.
Each was marked with fur dye nnd kept in
a 2.4 x 2.4 x 2.4 m cage made of hardware cloth,
They were
given a constant supply of water and were fed wild bird mix.
Feeding boxes were used as nests.
11
The voca:.Liza.tions of the captive squirrels were recorded at
irregular intervals using the equipment described above.
were elicited by startling the animals.
Sounds
An attempt to detect
sounds in the ultrasonic frequency range was also made, using an
ultrasonic receiver Model M 114 B (Massa laboratories Inc.)
that converts ultrasonic sounds to audible sounds.
Sound Analysis.
Recordings were analysed in the laboratory
with a Kay Sona-Graph 7029-A which produces a visual representation
of the sound, the sonagram.
In this study, two different picto-
rial representations of the sounds were used.
The first display
gives an overall, three dimensional picture of the signal being
analy<::ed., including frequency, amplitude and time.
The frequency
of the sound is represented along the vertical asis, time along
the horizontal axis and amplitude by the darkness of the graph.
second type of analysis, a section, permits the individual am-
1>..
plitude of each frequency component to be displayed along the
horizontal plane at any preselected point in time; frequency is
indicated along the vertical plane.
Sections were taken at
different points in time of calls that were relatively long
in duration, for the purpose of detecting changes in amplitude
as
a,
fmwtion of time.
In all analyses, a frequency range of 5 - 16000 Hz, linear
scale, and large drum were used.
A calibration tone generator
provided frequency markers every 1000 Hz along the frequency
scale of the pattern.
-·---·--·-·----··---.
·-·----------------------
Sonagrams of each sound were made using
~-----~------
----------~----------
-~
-------
~
~-----
-------------
12
both the narrow band and the wide band filters.
The narrow
band filter emphasizes frequency resolution while the wide
band filter emphasizes time resolution.
In most analyses, the
gain control, used to manipulate the dynamic range of' the
pattern was set at 0, and the mark level, which controls the
darkness of the pattern, was set at
contrast.
2.5
to obtain the best
Frequency and time interval measurements were made
from each sonagram to the nearest 100Hz and 1 msec respectively.
;.
i
I
When harmonics (integral multiples of the fundamental frequency)
were present, the fundamental (lowest) frequency was measured.
RESULTS
Spectrum of Vocalizations
Sounds were grouped and named on the basis of both the
way they sounded to the ear of the observer and their physical
characteristics drawn from their graphic representation.
The
calls show a considerable degree of variation within and
among individuals.
All calls fell into the following six
distinct types.
1.
Chatters
A chatter is defined as any signal composed of a series
of two to eight short syllables, units of sound represented
by a continuous tracing along the horizontal and/or vertical
axis of a sonagram, emitted in a rapid sequence.
vary markedly in their structure.
The chatters
The fundamental of the first
13
syllable is always of equal or higher frequency than that of
the following ones.
The simplest chatters are those emitted by
young animals (fig. 1D) and consist only of straight frequency
bands, lacking the up and down sweeps that were present in the
more complex adult chatters.
Mean length of all chatters is
0.26 sec while the syllables of the chatter range from 0.01 to
0.09 sec long, separated by intervals of from 0.01 to 0.06 sec.
Typical chatters are
sho~~
in figure 1, the characteristics of
these sounds are listed in table 1.
2.
Sg_ueals
A squeal is defined as any single, structurally simple
tonal vocalization, that is, the sound is characterized by one
or more relatively narrow frequency bands.
The frequency
bands are either horizontal (fig. 2A) or with an ascending
tendency (fig. 2B).
three
ha1~onics.
Most of the squeals consist of from one to
The fundamental frequency varies between J.O
to 4.8 KHz and the duration, which is significantly different
when given under different conditions, varies from O,OJ to
0.24 sec,
~e
characteristics of squeals are summarized in
table 2.
3.
l-;lflistles
The whistle is a short, tonal vocalization consisting of
an upsweep followed by a downsweep in frequency.
The signal
length of all whistles is surprisingly consistent, ranging
from 0.33 to 0.34 sec.
A typical call begins at 5.2 to 6.0 KHz,
rises to above 7,0 KHz and then drops again to slightly below the
14
starting
fre~uency.
There are no harmonics above the fundamental.
Two whistles are represented in figure 2C and the characteristics
3.
of a whistle are summarized in table
4.
Grunts
The term grunt is given to all atonal low intensity sounds
that cover a wide
fre~uency
range.
Grunts are given in syllables
of 0.02 sec, separated by intervals of 0.01 sec or more, or as
continuous signals of up to 0.53 sec.
The mean duration of a
grunt is 0,21 sec, the standard deviation being 0.14 (n=61).
Samples of grunts are shown in figure 3B, C.
5.
Scream
A scream is similar to a grunt in that it is atonal,
covering a wide
fre~uency
range.
It differs, however, in in-
eluding frequency components which are definitely stronger,
sharper and more intense.
different from a grunt.
To the ear it is significantly
Two screams were recorded.
0.07 sec long and the other 0.13 sec,
in each are at 4 and 8 KHz.
The sharp
One was
fre~uency
bands
One of the screams is depicted in
figure 3D.
6.
Tooth chatter
Voiceless low intensity sounds made by rapid.iy moving the
teeth against each other, are termed tooth chatter.
are repeated at intervals of 0.01 to
0.05
sec.
The pulses
The duration
of the pulses varies between 0.013 to 0.023 sec, and the sound
usually includes a main
5.0
KHz.
fre~uency
band that ranges from
0.5
to
The sonagram of a typical tooth chatter is shown in
15
figure 3A.
i
The characteristics are summarized in table 4.
Table 1
Characteristics of the "chatters" of the California ground squirrel
Physical properties of Call
n
range
mean
. 3.7
SD
No. of syllables/call
42
2 - 8
Duration of signal (sec)
42
0.08 - 0.55
0.26
0.17
Length of a single syllable (sec)
160
0.01 - 0.09
0.06
o.o6
Intersyllables interval (sec)
105
0.01 - 0,06
0.03
0.02
42
3.2 - .5.0
4.36
o.63
in the fundamental
frequency through the call
17
9 - 80
31.57
23.23
Maximum frequency recorded (KHz)
42
13 - 16
14.62
0.96
Fundamental frequency of
first syllable
%decrease
1.75
0'""""
Table 2
Characteristics of the "squeal" of the California ground squirrel
---------------------------------------------------------------------------------·---------------------Physical properties of call
n
Fundamental frequency (KHz)
.56
J.O - 4.8
3.77
0.47
Second harmonic (KHz)
49
6.0 - 13 •.5
7.90
1.60
Third harmonic (KHz)
4.5
10.0 - 14.0
11.4.5
1.21
Fourth harmonic (KHz)
33
14.0 - 16.0
14.68
0.95
lliration (sec)
.56
0.09
0.0.5
range
0.03- 0.24
mean
SD
!-""
...._.,
Table 3
Characteristic of whistles of the California ground squirrel
Physical properties
n
range
mean
SD
Call duration (sec)
4
0.033 - 0.034
0.034
0.001
Bottom of upsweep (KHz)
4
5.2
:- 6.0
5.60
0.570
Top of upsweep (KHz)
4
7.0
- 7.5
7.25
0.350
.4
5.0
- 5.2
5.05
0.070
Bottom of downsweep (KHz)
.....
(),)
19
Figure 1
Typical chatters of the California ground squirrel.
Adult chatters (A,B,C), a chatter emitted by a young
animal
(D).
20
A
1
12
8
4
0
B
16
12
---
N8
r
~4
~0
c
....0
-:s::.
l
12
8
4
0
D
,...___~
----
4dilttllt
-
C = ~ ·•
JU4&1iS!!L.....,.._,
-:~
0.1
0.2
0.3
TIME/SEC
0.4
21
Fi~re 2~
Squeals (A,B) and whistles (c) of the California ground
squirrel.
22
16
--
A
-
-
12
B
-
-
c
16
12
8
4
0
\
0.4
0.3
0.2
0.1
oL------~----~------~------~TIME I SEC
Table 4
Characteristics of tooth chatters of the California ground squirrel
Physical properties
n
range
mean
SD
Pulse duration
6
0.013 - 0.023
0.017
0.005
Inter-pulse duration
6
0.010 - 0.051
0.028
0.013
I~
24
Figure }
Tooth chatter (A), pulsed grunt (B), 2 contiL~ous grunts
(C), and scream (D) of the California ground squirrel.
25
i
16
12
8
A
16
B
12
8
N4
--------·
1-0
1%
w
:::
9
~~
c
'12
~ 8
z:
~ 41
go
0:
II.
16
D
12
8
4
0·
I
Lo~--n,--~~--~----~0.1
0.2
0.3
OATIME I SEC
26
Ul tl•asonic Sounds
The repertoire of the squirrels, except for screams, was
repeated at various times by the caged animals.
U::;.ing the ultra-
sonic receiver at the cage, the five different call types were
monitored.
No ultrasonic sound components up to a frequency of
150 KHz were detected in any of them.
Funct.ions of Vocalizations
a.
Response to predators and -potential predators
In the study area, known predators were observed near the
squirrels 45 times.
Vocal responses were hear·d 39 times (87%).
Two distinctive calls were found to be associated with the approach or appearance of predators, or potential predators, including humans.
The simplest call was a single squeal.
The
second type, termed a "long call," was more complex and consisted
of a series of one of two chatters followed by repetitive squeals
with intervals of 0.6 - 0.7 sec between them throughout most of
the call.
The duration of the entire series of calls ranged
from 1 • .5 :mi.'J.utes to 4o minutes.
At the beginning of a series
of squeals, the amplitude of each squeal was higher towards
its end, while at the end of the series, the amplitude was
highest at the beginning.
Also, towards the end of each series,
the squeals became shorter in duration and the intervals longer
(1.0 - 112 sec).
vfuile emitting the long call the vocalizer usually sat up
on its :rump, head and. bocly held erect, looking in the direction
L______ ,
27
of the
int~~der.
The tail commonly was flicked with each sound
unit.
An animal emitting a single squeal in response to a pred-
ator or potential predator, was either fleeing or called and then
ran directly to a nearby burrow.
The vocalizer did not assume
any particular posture while giving the signal.
Response to aerial predators.
Twenty-seven times aerial
predators (24 red tailed hawks and three golden eagles) were
seen flying in the vicinity of the co.lony but not directly over
it, or if over it, at a high elevation.
On
21 of these occasions
a long call was given by one of the squirrels.
Six red tailed
hawk appearances failed to elicit a vccal response.
In sixteen instances aerial predators (12 red tailed hawks
and 4 golden eagles) were seen to approach the study area flying
low to the ground.
In every case, a vocal response of the
first type (a single squeal) was given.
Once, a red tailed hawk was seen sitting on a cable only
10 m a·way from three animals and emitting calls.
The squirrels
appeared to ignore the hawk, continuing to feed in the grass.
l~en
the bird took off, however, a single squeal was emitted by
one of ths animals, which ran to a burrow.
Airplanes on nine occasions elicited long call response.
However, ma,ny times, while passing over the area, no vocal response nas heard.
There were no obvious di.fferences in the ele-
vation or the shapes of airplanes that did or did not elicit a
response •
..
-
-
--~
----
----·-- --------- ------··-·--·-
------ -· ··-
"
------- ----· ---------·
···- ------------------ ______ .,_
·---~
·----------·.
..
--------
-----~----
------
28
Response to ground predators.
the study area.
Twice coyotes were observed in
Both times the coyotes were apparently seen by a
squirrel while still at a distance of more than 2.5 m from the
colony but approaching very slmdy and staring, as if hunting.
On both occasions one of the squirrels responded with the long
call.
Such an approach, eliciting the same vocal response,
was also ncted by another investigator studying the same population of squirrels (Jeff Werber, personal communication).
Once, a bobcat sauntered through the study area at a
leisurely gait, passing about 20 m from three squirrels.
apparently v-ras not. hunting.
It
Upon seeing it, the squirrels
assumed alert postures, sitting on their rumps, still, while
Hatching it walk by.
No vocal response was heard.
In my study area, snakes were never seen.
However, to
test the response of the squirrels to snakes a bull snake
(Pituophis melanoleucus) and a king snake (Lam-proueltis getulus)
were introduced into a cage of captured animals.
They responded
by tail flagging and sand kicking, as described by Owings et al.
( 1977) , -t.o both snakes without making any vocal response.
The squirrels at the study area rare.ly ca.lled in response
to the presence of humans moving about the area.
However, in
another popu.lation of squirrels located about 16 km north of
the study station and 1-Thich was se.ldom disturbed by humans, twice
one animal began a long cal.l when I approached it from a distance.
The squirrels kept in the cage emitted a single squeal 32 out
of 41 times that I entered their cage.
29
Cattle moving casually while eating Here a very common disturbance at the study area.
In the hundreds of times I have seen
cattle enter the area, I have never heard a ground squirrel give
any vocal response, although when the cattle passed close
qy,
some squirrels ran to burrows.
ResEQnse of conspecifics.
In response to hearing a single
squeal usually all animals in the vicinity ran directly to
nearby burrows.
Some stayed in the entrances and looked in the
direction from which the call came.
Once, upon hearing the
signal, a dominant male feeding at a box failed to run to a
burrow; instead it only assumed an alert posture, sitting on its
rump, and looked at the red tailed hawk that vras already heading
away from the study area,
In all other cases animals feeding at
a box at the time the signal was given responded as described
above; these observations included five dominant males, two suborninate females and three unmarked individuals of unknown sex.
Upon first hearing long calls some animals usually ran to a
burrow and others sat upright on their rumps, still, oriented
towards the sound source.
About one minute after a call had begun,
the animals usually went back to their previous activities.
In
1.3 cases a dominant male was feeding at a feeding box when the
first~a:l
in the series was heard; on two occasions the animal
fled to a burrow, but the other 11 times the male merely assumed
an alert, upright posture and did not leave the feeding box.
times females were feeding while the long call was heard.
Two
On one
30
of the occasions the female ran to a nearby burrow and on the
other it stayed out, responding by assuming an alert, upright
posture.
A subordinate male was seen once at a feeding box
when the call was heard, and upon hearing it, the animal ran to a
burrow.
A long call was recorded and played back to the squirrels
both at a normal rate and with shorter intervals (approximately
0.3 sec instead of the usual 0.6 - 0.7) between squeals, but
without cha.""l.ging the nature of the squeals.
The. response to
both did not differ from the usual response to a long call;
some squirrels ran to nearby burrows while some stayed out.
Vocalizers.
Of the 40 long calls heard, 34 were given by
females, five by males (two dominant and three subordinants)
and one -by a young, unmarked animal of unknown sex.
females vocalized more frequently than others.
Three
Once, over a
period of three weeks, one female gave the long call nine times.
She was the only animal heard by me to give this call during
this period.
There was not any difference notable in response,
depending on who was giving the call.
The other type of alarm, a
single squeal, was emitted 56% of the times by males and
females.
44%
by
No difference in responses was noted.
b.
Vocalizations used in intraspecific encounters
In the California ground squirrel, several types of agonistic
behavior occur ranging from threat to chase and to the more aggressive types of interaction, such as various forms of fighting.
31
. Although many interactions were observed in the area, only those
which occurred near the microphone, which was always set close to
a feeding box, where accompanying sounds could reasonably be
expected to be heard, were noted.
Certain sounds were found to
be closely correlated with specific social interaction.
The
interactions that occurred by the feeding box, and the sounds
associated with them were as follows:
1.
Threat
Sometimes one individual upon seeing
anot..~er
individual ap-
preaching at a distance apparently caused the retreat of the int:ruder by staring and vocalizing.
a "threat."
I have termed this behavior
Chatters were the usual sound emitted while threat-
ening, eight times by males threatening females, two times by
males threatening males and two times by females threatening
males.
I have never noted a female threatening another female.
No apparent differences were notable between the chatters of
males and females.
Commonly the animal threatened vocalized also, although
they did not invariably do so.
Five times, females threatened
by males emitted a squeal while fleeing, and two times a squeal
was emitted by males that were threatened by females.
Once, a tooth chatter was produced by a male after he
threatened a female, and she ran away without emitting a
squeal.
2.
Blocking
When an individual feeding at a feeding box was closely ap-- --··
~
----------- _.,_ -------------------
--·-··
----
- ---· ------
---~--------
---------·----
--- -·- ---- ------------------
------~--
--
-~-
-------- -----·
32
preached and disturbed by another individual who tried to eat too,
the animal feeding sometimes was heard to emit a grunt, with no
other obvious change in behavior.
left the area.
The intruding animal usually
Fourteen times a male was the individual who
was feeding when a sound was heard, while the intruder was a female; in one instance a female blocked an
intr~ding
male.
In
another four instances an adult male blocked a young unmarked
animal of unknown sex.
In two of these latter occasions the in-
truding young animal emitted a squeal while running away.
3.
Supplanting
When an individual was feeding and another individual appeared,
the feeding animal sometimes moved away and was replaced by the
"intruder."
Owings et al. (1977) calls this supplanting.
On
most such occasions the intruding animal emitted a grunt while
arriving at the feeding box.
Supplantings that involved sounds
occurred 17 times when a female was feeding and a male supplanted
her, eight times between two females and two times when a male
supplanted an unmarked young animal of unknown sex.
On one
occasion when a dominant male supplanted a female with whom he
shared burrm-1s, she failed to move quickly away and instead stayed
beside him after his initial grunt.
The male produced tooth
chatter for a few seconds, then emitted another grunt, after
which she left.
4.
Chase
As referred to by Owings et al. (1977), chasing is described
as one individual running after another individual.
Chase in-
3.3
valved two types of vocaliza-tions, chatters and grunts that
were heard on different occasions.
Grunts were emitted five
times by males chasing females and three times by males chasing
males, interactions that took place outside the breeding season
when the males did not show any obvious territorial behavior.
Another three times, grunts were emitted by young,
unmark~d
animals of unknown sex who were chasing other young unmarked
individuals (sex unknown),
Chatters were emitted four times
by males chasing females'and one time by a male chasing a male
(outside the breeding season).
No apparent differences, either
seasonal, territorial or sexual were found in the circumstances
that were involved with the interactions in which either grunts
or chatters were emitted.
5. Fight
Vocalizations were associated with some forms of fight,
interactions in which the two animals are biting and clawing
each other while running in a circle, (circle fight), rolling
over and over on the ground, (roll fight), or boxing fight in
which two squirrels hit at each other with their front feet
while standing upright (Fisler, 1976),
~1ale
- male fights
of all kinds, as also reported by Owings et al. (1977), were
seen much more frequently than female - female fights.
Grunts
were recorded nine times during male - male fights and three
times during female - female fights.
A. tooth chatter was emitted
during each of the only two male - female roll fights, which
took place near the microphone.
34
Once, two screams preceded a flank slam (Owings et al.
1977)
which was followed immediately by a roll fight between two
males, interacting at a feeding box placed the first time at
their territorial boundary during the breeding season.
I was
not able to tell whether the sounds were emitted by the winner,
the loser, or both.
6.
Sand ktcking
Sand kicking, pushing sand toward the opponent with the
fore feet, was observed four times between two males.
The
kicking action was always performed by the animal in whose territory the interaction was induced, and each kicking action was
always accompanied by a grunt, emitted by the defending animal.
7. Territorial disputes
Interactions between two males, induced pn their territorial
boundaries commonly elicited a variety of behavior patterns.
Among them are cheek-back rubbing, an apparent scent marking
behavior (Owings et al,
1977), an apparent displacement activity
that involved going rapidly through the motions of washing,
lateral approaches that involved displaying with the bodies
parallel, the backs arched and tail hairs erect and the tail
oriented towards the opponent (Owings et al.
1977). lliring en-
counters between males at their territorial boundaries, in which
all three types of activity were observed, tooth chatter was
heard continuously, with
or~y
short p&uses, and was stopped
when one of the animals broke off the encounter.
8,
Courtshiu behavior
35
During sexual chases, part of courtship behavior (Owings et al.
1977), males were seen repeateclly chasing females .for short
distances.
D~ring
these chases the female would stop, allowing
the male to sniff the genital area and then both would run
again.
During each of four such sexual chases which occurred
near a microphone, whistles were emitted by the male involved.
The Nature of Sounds Used in Agonistic Behavior
Grunts emitted during chases, blackings and supplantings
show differences in duration and structure, depending more on
the participants than on the type of contest.
When the interaction
was between a male and a young individual or between a male and
a female who shared his burrows, the grunts were short in duration (about 0.04 sec) and single pulsed in 21 out of 30 observations (fig. 4A).
While interacting with females that were
not seen to share burrows with the males involved, the grunt was
either highly pulsed (two observations) or consisted of a single
pulse of an intermediate duration, about 0.2 sec (fig. 3B, C).
Grunts were longest in duration (up to 0.53 sec) when emitted
during fights and the energy was most concentrated at 0 - 5 KHz
at these times (fig. 4B).
The chatters involved in agonistic interactions tend to be
composed of more syllables than those used for alarm.
The mean
number of syllables of chatters used for alarm is 2.25, while in
agonistic interactions it is 4.64.
Sq_ueals emitted by animals that were being chased, blocked,
supplanted or threatened were significantly shorter (a mean
value of 0.065 sec) in duration than the squeals used for alarm
(a mean value of 0.138 sec).
37
Figure 4
A grunt emitted by a male, while chasing a female which he
shared his burrow with (A) a grunt emitted during malemale fight (B) and a section, taken at the point of the
arrow of the above grunt
(c).
38
.~
0.1
0.2
TIME I SEC
16
12
8
4
0
c
~
~
~
AMPLITUDE
0.3
0.4
'
r·---------------·--- ____ ,__ ·- ---------· ---------- ----··------ -. --- - ---·--·-----·--- -·----- --·-----·-··· --- -------------- -- --·-- --·---- --- ·-- --·- -·-- ---DISCUSSION
The squirrels usedtwo distinctive vocalizations when
alarmed.
Sometimes they emitted a loud, single squeal; other
times they produced a more elaborate call composed of chatters
followed by repeated squeals, the long call.
Owings et al.
(1977) reported the long ca.ll in this species to be given in
response only to aerial predators.
However, I have heard the
long call many times emitted in an apparent response to airborne predators, such as red tailed hawks and golden eagles,
flying at a distance, and have heard the squeal given when I
approe.ched the squirrels closely.
Mo observations show a grea:ter
consistency between the type of call produced and the immediacy
of the threat, than with the type of predator involved.
The
squeal was produced only when there was a sudden alarm caused
by the close approach of either an aerial and potential ground
predator, hence presumably an immediate danger.
The long call,
on the other hand, was given when an animal was alerted but
apparently not greatly alarmed; it was heard in response 'to both
kinds of predators, but only when they were seen at a distance
and therefore not an immediate threat.
The postures and actions taken by the animals giving the
two different calls further suggest that they actually indicate
two different levels of alarm.
When emitting a squeal the animal
does not assume a specific posture; rather it emits the call in
39
!------------ ---- ---
~--------
-- --------- ---·-·· -- --
·--------~--
------· -
whatever attitude it is in at the time the predator is first
seen, and immediately runs to shelter.
In contrast, while
emitting the long call, the vocalizer sits upright on its rump,
a behavior pattern that ·presumably enables the emitter to watch
the predator, at the expense of making himself more conspicuous
to it; presumably the risk is not great while the predator is
far away,
A similar posture is described for the Columbian
ground sq_uirrel (~ columbianus) while emitting repetitive alarm
calls (Ma~~ille,
1959).
Likewise, the responses of the other animals when hearing
the two alarm calls suggests that they indicate different degrees
of alarm.
For instance, when the sq_ueal is given all animals in
the vicinity run immediately to shelter, as does the caller.
On
the other hand., in response to hearing the long call some of the
animals typically assume an alert posture, apparently watching
the apparent cause of alarm.
Such an attitude would presumably'
permit them to rely on their own visual perception to determine
the intensity of the danger.
The indication of the immediacy of danger by distinctive
alarm calls is not unique
in~.
beecheyi,
Among members'of
the genus Spermouhilus that have been studied in this regard,
§_. trid.ecem.lineatus has also been reported to give two different
vocal alarm responses depending on the intensity of the danger.
The animals of this species use a trill as a generalized warning
while a long purr is produced when an immediate threat is
present (Matocha,
1975).
~.
beldingi has also been reported to
'-- ---- ·---·--·-··---··· -------------------- ----·· -----~------ ... _____________________________ -··--- ···---------· ·-----· __________________ !
41
~---------~-~--
--------··- -----------------··----. ---·-·------·--·---------·----- '"". ---·---··--·-·
·----
--·--
----~--·----
i
have an alarm call associated with an extreme danger, as represented by a hawk or a close ground predator (Turner,
1973).
Other members of the genus Spermophilus, however, have been
reported to give different alarm calls depending on the nature
of the predator involved, rather than the immediacy of danger,
as Owings et al.
(1977) have suggested is the case in the
population of S. beecheyi they studied.
S. armatus, for instance,
is said to chirp in response to an airborne predator and to give
a churr call in response to a ground predator (Balph & Balph,
1966). Also,
~·
undulatus is reported to use a single whistle
in response to an aerial predator and a chatter in response to
predators approaching on the ground (Melchior,
1971).
The reasons for the differences between my work and that
of Owings et al.
(1977) in regard to the apparent "meaning" of
the two alarm calls is not yet clear.
It might be that there are
environmental factors within the tiw populations that modify the
way they respond, as has also been suggested by Balph & Balph
(1966) foy £. armatus. Whatever the explanation, however, a
vocal response indicating the severity and intensity of alarm,
would seem to include more adaptive information than one·indicating
the nature of predator perceived.
Transmitting information about
the immediacy for the need to respond, rather than about the cause
of the alarm, would seem to increase the probability of surviving.
It vmuld appear to be of lesser import, for instance, to know if
the predator were a coyote or hawk, than to know if the predator,
whatever its nature, were upon you or merely approaching at a
42
distance.
Marler
(1967) suggested that the more adaptive kinds of
sounds used in alarm calling would be those that provide the
fewest cues to a potential predator about the location of the
caller.
For a call to be localized by birds and mammals, which
rely upon binaural detection of differences in the various
properties of the sound, the sound should be broken, vary in
pitch and consist of a wide range of frequencies.
The squeal,
used by the California ground squirrel in both types of alarm
calls, does not fit this pattern, hence is presumably an ideal
alarm signal.
It is a pure tone, with no transients or dis-
continuities and, therefore, does not facilitate the localization
of the caller.
On the other hand, it is loud and audible at
great distances.
Besides having the advantage of being hard to localize and
reaching many conspecifics, the squeal is presumably heard by
the predators.
The frequency of the squeal (about 4KHz) is
vrell within the hearing capacity,
Wallace and. I'1ahan
3 - 10 KHz according to
(1975), of the most frequently seen predator
of the California ground squirrel in my study area, the red
tailed hawk.
Since the method of hunting employed by hawks de-
pends upon surprise, and as suggested by Brown
(1975), surprise
is often prevented by hearing alarm signals, the utilization of
an alarm call might bear the additional advantage of causing the
hawks to hunt elsewhere.
That might also explain why the squirrels,
while emitting the long call, sometimes continue calling after the
43
:predator is no longer visible,· although it may still perceive the
sounds.
Most of the time, the long calls of the California ground
squirrel in my study area were emitted by females; males seldom
gave the call.
Presumably the threshold of females for any alarm-
ing stimulus is lower, in general, than that of males.
This may
be because the females are usually more submissive (as observed
in most of the encounters) and therefore less relaxed and more
alert to any threat to them.
This, however, seems unlikely to be
the whole explanation, since of the five times ma.les were heard
to call, two were dominant anima1s; unfortunately the sample of _
males is too small to be indicative.
A lower threshold of re-
sponse in the females might also have evolved as one of the
mechanisms to protect their own offspring.
That is, because they
have more direct responsibilities to the young, they may have been
selected for greater alertness than males.
supported by Turner
This hypothesis is
(1973) in which a1arm calls given by females
ceased only after all the young animals had returned to the vicinity of the burrow.
chirps, used by
~.
Also, Balph & Balph
(1966) reported that
armatus to indicate the presence of predators
and also during intraspecific interactions, were given mostly at
the period before the young
offsprin~
appeared above ground and
at this time mostly by females.
The response of the animals to the call also differed depending on their social rank.
Typi~ally
the most dominant
animals are less likely than subordinate ones to flee in response
r·· -··- -···-··- ·-····---·---·-
to hearing the long call.
The reason for the difference in re-
sponse is not clear, but it may be because dominant animals
generally are under less stress than are subordinates.
Perhaps,
being under more stress, the subordinates are more attuned to
respond to any danger, predator or a dominant conspecific; hence,
presumably their fleeing tendencies are higher.
The long calls of the Cq,lifornia ground squirrel are often
combined with a visual display, flicking of the tail, which might
bear more information regarding the predator, as also suggested
by Linsdale (1949).
The Columbian ground squirrel (Spermophilus
columbianus) also flicks its tail when emitting alarm calls
(Manville, 1959), as does the black tailed prairie dog (Cynomys
ludovicianus) (Waring, 1966).
This display might help conspecifics
in locating the caller, since alarm calls are typically difficult
to locate, and thereby facilitate determining the location of the
predator, helped by the orientation of the signaler made more
obvious while its tail is flicking.
Rattlesnakes were found by Fitch (1946) to be the main source
of predation upon the California ground squirrels in his study
area.
Both he and Linsdale (1949) reported that the appearance
of individuals of any of several species of snakes evoked vocal
responses by the squirrels.
Although snakes were never seen in
our study area, they did not elicit vocal response when placed in
a cage with squirrels that were brought from that area.
Owings
et al. (1977) also did not observe any vocal response to snakes,
neither in the field nor when released into a cage with squirrels
45
taken from an area in which many rattlesnakes had been seen.
The reason for these differences are not clear, but it is pessible that there are populational differences, either genetic or
learned, regarding vocal response to snakes.
Balph & Balph
(1966) observed encounters between S. armatus and snakes both
in the field and in an arena.
They also have never heard a
vocal response during the encounters.
The response of the California ground squirrel to predators appears to be triggered by cues relative to the predators'
actions, hence its presumed intentions, rather than merely the
sight of it.
Hawks not in flight, for instance, even when
calling at a very close range, seem not to elicit any vocal
or behavioral response in the squirrels, at least in the one
instance seen.
sounded.
Only when the bird flew, was a single squeal
Fitch (1946) also saw hawks perched in trees at a verJ
close range which did not elicit vocal response in the
he was studying until they flew.
~.
beecheyi
Perhaps the shape of a bird
while flying, and possibly its size and velocity, too, are
responsrble for the response of the squirrels to lt as Schleidt
(1961) reported to be the case in the response of birds to
pred.ator models.
This assumption is also supported by the fact
that the squirrels sometimes gave vocal responses to airplanes
which in the proper attitude and at sufficient altitude may have
a similar shape and apparent size.
Size of an airborne object
appears to be critical-in eliciting a response inS. armatus,
as well, for Balph & Balph (1966) have reported that smaller
46
hawks can get closer to the
larger hawks.
s~uirrels
before they chirp than can
The actions of ground predators also appear crit-
ical, since vocal response of the California ground squirrel to
ground predators or potential predators was elicited only if they
were showing an apparent intention to hunt.
Others (one bobcat
and many cattle) that were seen just passing by, did not elicit
any vocal response.
Most animals living in organized groups have evolved signals
indicative of motivation of an individual and its status within
the social group.
These usually can be observed best during
agonistic encounters.
In the California ground squirrel the
forms of aggression involving vocalizations vary widely, from
relatively mild threat and intimidation to actual fights involving vigorous physical contact.
The sounds produced during
these encounters appear to be closely associated with the hierarchical status of the emitter, his motivational readiness and
his propensity to attack or flee.
This close coincidence of
specific sounds with specific actions implies that the sounds
have
cow~unicative
properties, thus making it possible for the
receiver to predict the behavior of the signaller, thereby diminishing the number of potentially destn1ctive interactions.
b1 the California ground squirrel two vocalizations, the
gn1nt and the chatter, appear to indicate dominance.
co~~only
They were
given by the dominant animal in encounters and seemed to
serve as a warning to the subordinate animal.
Often such signals
permitted priority of access without actual fighting.
When
47
distances between animals were relatively great (more than about
two meters) as in threat, the chatter was common.
In closer
encounters such as blocking, chasing and supplanting, the more
dominant animal commonly was heard to emit grunts.
Grunts were
also heard during fights, but in no case could the signaller be
identified.
Other species of ground squirrels that have been studied also
use signals for dominance.
Both -S. tridecemlineatus and -S. armatus
use growls for the purpose of threat and intimidation (Harris,
1966; Balph & Balph, 1966). The growls of .e_. tridecemlineatus,
according to their oscillographic representation, seem to be
similar to the grunts emitted by the California ground squirrel;
those emitted by
.e_.
armatus may also be similar, but no sonagrams
are available for comparison.
Dominant African unstriped ground
squirrels (Xerus rutilus), of either sex, have been reported to
make a rough scolding chatter upon the close approach of a subordinate (O'Shea, 1976).
This chatter resembles in its description
that of the California ground squirrel.
Grunts appear to form a graded sound system which includes
a range of forms correlated with situations of varying aggressiveness.
In general, the more aggressive the squirrel, the longer
the grunt.
Such a gradation presumably permits the transmittal
of information as to the level or degree of aggression.
Similar
graded signals are common in many animals and are particularly
well-developed in aggressive displays; as suggested by Wilson
(1975), the greater the motivation of an animal or the more intense
48
the action about to be performed, the more intense and prolonged
is the signal given.
The only other ground
type of graded signal has been reported,
~.
s~uirrel
in which this
tridecemlineatus,
does not, however, follow this generalization.
The growls it
uses as agonistic sounds are shortest in the most intense interactions, taking the form of a single short phrase when animals are
fighting; on the other hand, a continuous growl is given when an
animal is mildly disturbed (Harris, 1966).
The short, soft s~ueal, commonly given by the less aggressive
of the two animals in agonistic encounters, seems to act as a
signal of submission,
Presumably the sound indicates the inten-
tion of a subordinate to flee or surrender the food box, thereby
avoiding an attack,
Subordinates of S. armatus have been reported
to emit a squeal (Balph & Balph, 1966), and X. rutilus fre~uently
issue a low, gentle churring sound (O'Shea, 1976) when attacked
by a dominant animal.
However, these sounds, presumably signals
of submission, differ from the
s~uirrel
for the same purpose.
variable in structure,
bands of
single
fre~uency
fre~uency
syllable call.
(!.
s~ueal
The
fre~uency
of the California ground
s~ueal
of
~·
armatus is highly
and length; it includes several
and consists of several syllables, unlike the
squeal of
~·
beecheyi which is always a single
The churr of the unstriped African ground
s~uirrel,
rutilus), cannot be directly compared since no sonagrams are
available, but the verbal description given does not suggest a
s~ueal-like
sound,
Male California ground
s~uirrels
show organization of indi-
viduals into territories during the breeding season and, in common with many land mammals, employ auditory signals to claim and
maintain territorial boundaries.
Three types of sounds were
found to be typically associated with territorial behavior in
~·
beecheyi:
grunts, issued while sand kicking; screams, emitted
preceding roll fights; and tooth chatter, emitted during several
kinds of interactions including lateral approaches, marking and
grooming which were induced at a territorial boundary.
Pre-
sumably, such sounds, coupled with other types of signals, s.erve
as an efficient way of territorial defense.
Once boundaries are
established, they can be maintained without repeatedly fighting.
Tooth chatter, although used
by~·
beecheyi mainly durine;
territorial disputes, was also heard a few times when animals
were engaged in agonistic encounters such as threat, supplantation
and fight.
Tooth chatter is also known in many rodents, and
nearly all Sciuridae, and is generally agreed to be associated
with conflict situations.
It has been suggested that it serves
as an outlet for aggression between two males (Arvolva, 1974).
It seems to take place mainly during mildly disturbing situations (Harris, 1966).
The Uinta ground squirrel (~. armatus),
for instance, has been reported to emit tooth chatter in association with close aggressive encounters (Balph & Balph, 1966)
while the thirteen lined ground squirrel, Spermophilus tridecemlineatus, produces tooth chatter in close-quarter threat
situations (Matocha, 1975).
The signals used by the California ground squirrel during
50
agonistic interactions all structurally fit a pattern of sounds
which are easily localized.
Tooth chatter, chatters, as well as
some of the grunts are broken sounds; tooth chatter and grunts
cover a wide frequency range while the chatter consists of frequency transients.
These sounds probably have been favored by
natural selection to serve functions such as threat, intimidation
or claiming a territory because it is important that conspecifics
know the exact location of the signaller.
Sounds that are used intraspecifically at close range .
need not carry over long distances.
Probably, therefore, grunts
and tooth chatter, both low intensity sounds not likely to be
heard by predators, have been selected.
On the other hand,
chatters, which are also used intraspecifically, were audible
to the human observer at distances of several meters; but in
most cases when used intraspecifically chatters were involved in
signalling at distances of more than two meters.
It seems as
though, at the expense of assuring the reception of the sound
by a conspecific, the signaller is exposing itself to detection
by predators.
The chatter, although highly complex in adults, shows a
very simple structure (fig. 1D) when emitted by young animals, a
situation which parallels that of many mammals and birds (Evans,
1968).
This may imply that the more complex attributes of the
adult call develop through learning and
experience~
it is equally
probable, however, that the change is the result of maturation of
the vocal apparatus or associated nervous system.
Harris (1966),
in his study of the development of the voice of three different
species of ground squirrels of the genus Spermophilus (subgenus
Ictidomys), found that the vocalizations of the young squirrels
of the three species are more alike than those of adults.
He
reported that the juvenile sound is gradually developed into an
adult sound, but does not provide evidence for the mechanism
involved.
In this study captive California ground squirrels gave their
entire repertoire, except screams, at some time while
cages or traps; Uinta ground squirrels
ported to do so also (Balph & Balph,
(£.
enclos~d
in
armatus) have been re-
1966). These observations
might indicate that the vocalizations are not given with any
awareness regarding the presence of other animals, but are only
vocal reflexes, symptomatic of emotional states such as anger,
fear and sexual arousal, as has been suggested by Andrew
(1972).
Presumably selection for those sounds that also serve to change
the behavior pattern of conspecifics has led to the development
of the vocal communication system which now exists.
If true,
the basic cause of vocalizations may be changed in the internal
state, both in the normal social context when the sound emitted
could be expected to lead to an alteration in the behavior pattern of a social companion, and in the absence of a conspecific.
This appears to be true in other animals, for Andrew
(1962) has
described the same vocalizations in primates during social encounters and in situations where no social partner is present.
Andrevr
(1972) further discusses the assumption that all
52
animals displays, and presumably vocal displays as well, are
caused by conflicts between aggression, fear and sex.
The
performance of different displays may be the result of distinctive combinations of intensities of these three drives.
He suggests that aggression is activated when an animal is
frustrated, and therefore frustration can be a cause for displays occurring outside a natural context.
Such a hypothesis
might account for the fact that my animals, presumably frustrated
while held in a cage, unable to flee, and afraid of attacking a
human observer, emitted signals which, under normal conditions,
are used for threat and sexual chases.
The effect of frustration
on unrelated behavior patterns also has been shown by Pearson
(1970) who reported that isolated male guinea pigs show a wide
range of courtship and threat displays on finding empty a food
dish from which they have been trained to feed.
Ca~ifornia
ground squirrels use the same sounds, although
sometimes with slight differences in intensity and duration,
under different circumstances.
Thus, it appears that certain
sounds have different "meanings" when given in different
contexts,
Squeals, for instance, were used during both alarm
and agonistic situations; chatters also occurred in both situations.
~ullen
(1972) has pointed out that in many animals some
signals are emitted in more than one set of circumstances and
that the meaning of a call varies with the nature, state or status
of the caller, the attendant circumstances, and the status and
state of the recipient.
Smith (1969) has suggested that, because
53
the number of ways of producing signals is limited and therefore
there are only few kinds of signals possible in any given species,
messages that can be used in more than one context have been
favored by natural selection.
~.
armatus also use the same
signals under different circumstances, to serve di£ferent
functions; chirps given when hawks fly near are the same spectrographically as those used in intraspecific threat, and the churr
calls, given in response to ground predators, are the same as
those used intraspecifically (Balph & Balph, 1966).
When a certain sound is being used by the California ground
squirrel under different circumstances there is always a common
factor in the state of the animal giving the signal, even though
its presumptive meaning is different.
The squeal, £or .instance,
is always emitted while the caller flees, either £rom another
squirrel or from a predator.
In trQs example, the common factor
is fear, which presumably causes the animal to
flee~
An animal
giving a chatter call has always been disturbed, either by a
predator or by a conspecific, but is not likely to £lee.
This
rr.ight provide further evidence that sounds used in communication
may be
o~~y
a sign of a change in a central state.
In addition to using discrete signals under a.if£erent circumstances, the California ground squirrel has increased the
number of messages in its communication system by the use of
graded signals and by combining distinct sounds into a more
complex call.
The use of grunts of differing duration, pre-
sumably to indicate different aggressive tendencies, is an ex-
54
ample of the former.
The combination of chatters and squeals
to make up the long call, which seems to indicate general alertness, exemplifies the latter.
The Arctic ground squirrel,
~·
andulatus, is also known to increase the number of its available
messages by combinations or repetition of single acoustic elements (Melchior, 1971).
It may be significant that only six structurally different
sounds have been found to be used in the vocal communication
system of the California ground squirrel, the same number of
sounds reported to be produced by the Arctic ground squirrel
(Spermophilus undulatus), the Uinta ground squirrel (~. armatus)
and the thirteen lined ground squirrel (S. tridecemlineatus),
the only other representatives of the genus Spermophilus whose
vocalizations have been thoroughly studied (Melchior, 1971;
Balph & Balph, 1966; :Hatocha, 1975).
The similarity in number
may indicate that vocal communication systems in each have evolved
from a fixed set of basic sounds present in all members of the
genus.
The fact that structurally some of the sounds in the
different species appear to be similar in nature, although
differing in details, supports this view.
Tooth chatter and
grunt-like sounds, for instance, are consistently used by
ground squirrels.
The chatter of the California ground squirrel
is similar to that of the Arctic ground squirrel,
~.
undulatus;
both may be more primitive forms of the trill vocalization used
by §.. tridecemlineatus and §.. armatus as well as by
and~· mexicanus (Matocha,
~·
1975; Balph & Balph, 1966),
spilosoma
all of
55
which belong to a group of ground squirrels evolutionarily more
advanced than~. beecheyi (Black,
1963). The trill vocalization
consists of a series of about 20 bursts of energy with short
intervals, given in a rapid sequence.
Both the chatter and the
trill are typically given when an animal is disturbed, indicating
a similar function in all species.
Some of the calls used for alarm also appear to be strikingly
similar throughout the genus Spermophilus.
The squeal of the
California ground squirrel, used for sudden alarm, appears to be
very similar structurally to the whistle of the Arctic ground
squirrel (Melchior,
1971) and to the chirp of the Uinta ground
squirrel (Balph & Balph,
1966), both of which are given in re-
sponse to airborne predators.
fundamental frequencies
All three calls have quite similar
(4.0 - 4.5
KHz).
In addition, the bird-
like alarm calls of the Columbian ground squirrel (~. columbianus),
described by Manville
(1959) as clear, sharp chirps, and a call
given in immediate alarm situations by
~~mer
~·
beldingi, reported by
(1973) to be a high pitched, high intensity call, may
also correspond in structure to the squeal used by the California
ground squirrel; unfortunately, sonagrams of these sounds have
not been published.
The single squeal used for immediate alarm in the California
ground squirrel is remarkably similar to the calls of many small
birds given in response to hawks or owls when the threat is immediate (Thorpe,
1972). Although I saw no unequivocal response of
squirrels to bird calls, Arctic ground squirrels,
~.
undulatus,
56
have been reported to respond to a call emitted by a yellow
wagtail in the same manner as to their own alarm call (Melchior,
1971). Clark & Denniston (1970) noted
that~· richardsoni re-
sponds to warning calls of the prairie dog (Cynomys levcurus),
which are also similar in nature to the squeal.
The striking
similarity in critical alarm calls throughout the genus
Spermophilus and among many prey birds and other mammals, may
be the result of selection for sounds with properties that make
them very difficult for predators to localize.
In addition, the
use of similar sounds for the same function presumably provides
the different species of prey birds and mammals with the advantage of understanding each other's alarm signals.
As mentioned previously, vocalizations of the California
ground squirrel have been described by Owings et al.
Fitch
(1977),
(1949) and Linsdale (1946). Only Owings et al., who were
mainly concerned with sounds emitted during alarm situations,
presented sonagrams.
spectrograms.
Fitch and Linsdale did not use sound
In table
5
I have listed all the sounds which
have been identified and described by the above authors, together
with their suggested functions, and have attempted to equate
each with the sounds I recorded and the role my evidence suggests each plays in
cow~unication
in the population I studied.
The comparison may not be accurate because I did not have any
objective basis for making them.
as an aid in future work.
But I hope the table may serve
Table .5
Catalog of the vocalization of the California ground SQuirrel
Name used
in this paper
Functions described
in this paper
Previous name
and source
Function described
previously
SQUEAL
Immediate alarm,
signaling submission
A loud chirp
described as
"cheesk" (Fitch)
Alarm call in response to low-flying
large birds
Very sharp chirp
(Linsdale)
Alarm note
Whistle (Owings
et al.)
Alarm in response to
low-flying raptors
CHATTER
Given in the beginning of a long
call, or for threat
and signaling dominance
A rolling sound
which fades gradually
towards its end
(Fitch)
Alarm in response to
snakes
LONG CALL
General alarm
Chatters followed by
a series of chats
(Owings et al.)
Alarm in response to
a ground predator
Long series of barks
given more rapidly
than one per second
(Linsdale)
No function mentioned
\.n
-.J
Table 5-continued
Name used
in this paper
Function described
in this paper
Previous name·
and source
Function described
previously
LONG CALL
General alarm
"Chuee-chu-chu-chuk"
followed by a series
of less sharp chirps
(Fitch)
Alarm in response to
a dog, a coyote or
humans
GRUNT
Intimidating a more
submissive animal,
or given during
fights
Growl (Fitch)
Given during encounters, usually
when forced to take
refuge in the burrow
cf another animal, or
while fighting
Grunt or growl
(Linsdale)
To frighten other
squirrels from a
burrow
Tooth chatter
(Owings et al.)
Heard during an
encounter between two
animals involving a
lateral approach and
flank push
TOOTH CHATTER
Used mainly during
territorial disputes
l...r\
co
Table 5-continued
Name used in
this paper
Functions described
in this paper
WHISTLE
Used during sexual
chases
SCREAM
Used during territorial
encounters, as an
announcement of a fight
Previous name
and source
Function described
previously
V\
'..0
60
LITERATURE CITED
Andrew, R.J. 1962. The situations that evoke vocalization in
primates, Ann. N.Y. Acad, Sci., 102:296-315.
- - - - - · 1972. The information potentially available in mammal
displays, In R.A. Hinde (ed.), Non-verbal communication,
Cambridge Univ, Press, Cambridge, p. 177-404.
Arvolva, A. 1974. Vocalization in the guinea-pig, Cavia porcellus,
Ann. Zool, Fennici, 11:1-96.
Balph, D.M., and D.F. Balph. 1966. Sound communication of Uinta
ground squirrels. J, Mamm,, 47:440-450.
Barash, D.P. 1973, The social biology of the Olympic marmot.
Anim, Behav. Monographs, 6:182-184,
• 1977. Sociobiology and behavior.
Holland Inc., New York,
--=-~-
Elsevier North-
Black, C.C. 1963. A review of North American tertiary Sciuridae.
Bull. Mus. Camp. Zoo],, 130:109-248.
Blair, W.F. 1968. Amphibians and reptiles, In T.A. Sebeok (ed.),
Animal communication, Indiana Univ, Press, Bloomington,
P• 289-310.
Br:md, R. 1976. The vocal repertoire of chipm:mks (Genus Eu tamias)
in California. Anim, Behav., 24:319-335.
Busnel, R.G. (ed,) 1963. Acoustic behavior of animals.
Publ., New York, 933 pp.
Elsevier
Clark, T.1~., and R.H. Denniston. 1970. On the descriptive ethology
of Richardson's ground squirrel. Southwest, Nat., 15:193-200.
Cullen, F.M. 1972. Some principles of animal communication. In
R.A. Hinde (ed,), Non-verbal communication, Cambridge Univ.
PresE, Cambridge, p. 101-122.
Evans, F.C., and R. Holdenried, 1949. A population study of the
beecheyi ground squirrel in central California, J. Mamm.,
24:231-260.
Evans, L.T. 1961 Structure as related to behavior in the organization of populations in reptiles, In W,F, Blair (ed,),
61
Vertebrate speciation, Austin Univ. Press, Texas.
Fisler, G.F. 1970. Communication systems and organizational
systems in three species of rodents. Bull. So. Calif.
Acad, Sci., 69:43-51.
------~-·
1976. Agonistic signals and hierarchy changes of
antelope squirrels. J. Mamm., 57:94-102.
Fitch, H.S. 1948. Ecology of the California ground squirrel on
grazing lands. The Am. Midl. Nat., 39:513-596.
Fox, M.W. 1970. A comparative study of the development of facial
expressions in canids: wolf, coyote and foxes. Behav.,
36:49-73.
Frings, H., and M. Frings. 1963. Pest control with sound,
Sound, its uses and control 2(1).
Harris, J.P. 1966. Voice and associated behavior in ground
squirrels. Ph.D. Thesis, Univ. of Michigan.
King, J.A. 1955. Social behavior, social organization, and
population dynamics in a black tailed prairie dog town in
the Black Hills of South Dakota. Contrib, Lab. Vert, Biol.,
Univ. Michigan, 67:1-123.
Linsdale, J.M. 1946. The California ground squirrel.
California Press, Berkeley and Los Angeles.
Univ. of
Manville, R.H. 1959. The Columbian ground squirrel in northwestern
Montana. J. Ma~~., 40:24-44.
Marler, P. 1967. Animal communication signals.
769-?71+.
Science, 157:
Matocha, K.J. 1975. Vocal communication in ground squirrels,
Genus Spermophilus. Ph.D. Thesis, Texas Tech. Univ. ·
Melchior, H.R. 1971. Characteristics of Arctic ground squirrels
alarm calls. Oecologia, 7:184-190.
Moore, J. 1957. The natural history of the fox squirrel, Scuirus
niger shermani. Bull. Mus. Nat. Hist. , 113:39-40.
Moulton, J.M. 1963. Acoustic behavior of fishes. In R.G. Busnell
(ed.), Acoustic behavior in animals, Elsevier Publ., New York,
p. 655-693.
O'Shea, T. 1976. Home range, social behavior and dominance
relationships in the African unstriped ground squirrel,
62
Xerus rutilus,
J, Mamm.,
57:451-460,
Owings, D.H., M. Borchert, and R. Virginia, 1977. The behavior of
California ground squirrels. Anim, Behav., 25:221-230.
Payne, R.S., and S, McVay. 1971. Songs of humpback whales,
Science, 173:585-597.
Pearson, M. 1970. Causation and development of behavior in the
guinea pig. Ph.D. Thesis, University of Sussex,
Pope, C.H. 1946. Turtles of the United States and Canada,
~Dopf, New York.
A.A.
Schleidt, V.W.M. 1961. Reaktionen von truthuhnern auf fliegende
raubvogel und versuche zur analyse ihrer AAM's, Aeit,
Tierpsychol, 18:534-560.
Sebeok, T.A. (ed.) 1968, Animal communication,
Press, Bloomington, Indiana and London.
Indiana Univ.
Smith, J. v-r. 1969, Messages of vertebrate communication.
Science,
165:145-150.
Stokes, A.W., and H.W. Williams, 1972 Courtship feeding calls in
gallinaceous birds. Auk, 89:177-180.
Strousaker, T.T. 1970. Auditory communication among vervet
monkeys (Cercopith~cus aethiops), In S.A. Altmann (ed.),
Social communication among primates.
Thorpe, W.H. 1972. Vocal communication in birds. In R.A, Hinde
(ed.), Non-verbal coF~unication, Cambridge Univ, Press,
Cambridge, p. 153-175.
Turner, L.W. 1973. Vocal and escape responses of Spermophilus
beld.ingi to predators. J. Mamm., 54:990-993.
Wallace, G.J., and H.D. Mahan. 1975. An introduction to Ornithology.
:P1acmillan fubl. Co. Inc., New York, p. 168-186.
Waring, G.H. 1966. Sounds and communications of the yellow-bellied
marmot (Marmota :Haviventri§.). Anim. Behav., 14:177-183.
Waring, G.H. 1967. Sounds of black tailed, white tailed and
Gunnison's prairie dogs. Ph.D. Thesis, Colorado State Univ.
Wilson, E.O. 1975. Sociobiology the new synthesis.
Press, Cambridge, 697 pp.
Harvard Univ.
Zelley, R.A. 1971. The sounds of the fox squirrel, Sciurus niger
rufiventer,
J. Mamm., 52:597-603.