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, 1977
ii 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 in valuable help he gave me throughout my stay at C.S.U.N. I wish to thank him for his enlightening suggestions, ideas, in spiring 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 re ceiver; 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. I am especially indebted to ¥~. 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. And
iii 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 appre ciation is boundless.
iv TABLE OF CONTENTS
ABSTRACT viii INTRODUCTION 1 MA.TERLA.LS AND METHODS 7 Study Area 7 Field Observation Procedure 8 Study of Captive Animals 10 Sound Analysis 11 RESULTS 12 Spectrum of Vocalization 12 1. Chatters 12 2. Squeals 13 3. Whistles 13 4. Grunts 14 5. Screams 14 6, Tooth chatters 14 Ultrasonic Sound 26 FUnctions .of Vocalization 26 a. Response to predators and potential predators 26 Response to aerial predators 27 Response to ground predators 28 Response to conspecifics 29 Vocalizers 30 b. Vocalization used in intraspecific encounters 30 1. Threat 31 2. Blocking 31 3. Supplanting 32 4. Chase 32 5. Fight 33 6. Sand kicking 34 7. Territorial disputes 34 8. Courtship behavior 34 Nature of Sound Used in Agonistic Behavior 35 DISCUSSION 39 LITERATURE CITED 60
v ' '
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 5. Catalog of the vocalizations of the California ground squirrel. 57
vi FIGURES
Figure Page 1. Typical chatters of the California ground squirrel. Adult chatters (A,B,C), a chatter emitted by a young animal (D). 20
2. 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 by a male while chasing a female which he shared his burrows with (A), a grunt emitted during male-male fight (B), a section taken at the point of the arrow of the above grunt. 38
vii 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 commu nication 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 be havior of the animals; feeding boxes were used for intensifying interactions among individuals, Supplementary data were collected from captive squirrels. The recordings were analyzed with a sonagraph.
On the basis of their physical properties, vocalizations fell into six distinct groups: chatters, squeals, grunts, whistles, screams and tooth chatter. 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. Two types of alarm calls were given in response to predators: 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 de- gree of social integration within a species and the complexity of the communication system of that species (Fisler, 1970; Barash, 1977) . The emission of sounds is but one possible means of cornmu- nication, 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 ter ritoriality (Pope, 1946; Evans, 1961). Bird vocalizations include complex songs, thought to accomplish functions asso ciated with courtship, territorial and aggressive behavior, and simple call notes serving for alarm, distress, bond main tenance, 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 rep ertory 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 au- ditory communication system composed of seven calls used to indi- cate 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 ten-
dencies 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. However, such a study could
have other value as well. 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 el
evation 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 herba ceous 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 home- made 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 7.5 inches (11.3 em) per second. 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 bound aries 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. Sounds
were elicited by startling the animals. 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.
1>.. second type of analysis, a section, permits the individual am
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 2.5 to obtain the best contrast. 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. The chatters vary markedly in their structure. 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). Most of the squeals consist of from one to three ha1~onics. 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
of a whistle are summarized in table 3. 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. To the ear it is significantly
different from a grunt. Two screams were recorded. One was
0.07 sec long and the other 0.13 sec, The sharp fre~uency bands
in each are at 4 and 8 KHz. 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. The pulses are repeated at intervals of 0.01 to 0.05 sec. The duration of the pulses varies between 0.013 to 0.023 sec, and the sound usually includes a main fre~uency band that ranges from 0.5 to 5.0 KHz. The sonagram of a typical tooth chatter is shown in 15
figure 3A. The characteristics are summarized in table 4.
i Table 1 Characteristics of the "chatters" of the California ground squirrel
Physical properties of Call n range mean SD
No. of syllables/call 42 2 - 8 . 3.7 1.75 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 Fundamental frequency of first syllable 42 3.2 - .5.0 4.36 o.63 %decrease 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
0'-"""" Table 2 Characteristics of the "squeal" of the California ground squirrel ------·------Physical properties of call n range mean SD
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 0.03- 0.24 0.09 0.0.5
...._.,!-"" 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 Bottom of downsweep (KHz) .4 5.0 - 5.2 5.05 0.070
..... (),) 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 c ~0 ....0 -:s::.
D l 12 ---- ,...___ ~ 8 C= ~ ·• 4 4dilttllt - JU4&1iS!!L.....,.._, -:~
0 0.1 0.2 0.3 0.4 TIME/SEC 21
Fi~re 2~ Squeals (A,B) and whistles (c) of the California ground
squirrel. 22
16 A -- - 12 - -
B -
16 c 12 8 4 0
\ oL------~----~------~------~- 0.1 0.2 0.3 0.4
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 A 12 8
16 B 12 8 N4 1-0 ------· 1% :::w 9 ~~ c '12 z:~ 8 go~ 41 0: II. 16 D 12 8 4 0· I
Lo~--n,--~~--~----~-0.1 0.2 0.3 OA-
TIME 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 ap
proach or appearance of predators, or potential predators, in
cluding 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 re
sponse 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. Twice coyotes were observed in the study area. 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 pop ulation 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. It apparently v-ras not. hunting. 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 dis turbance 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 sub orninate 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. Two times females were feeding while the long call was heard. 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. Three females vocalized more frequently than others. 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 44% by females. 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 ag- gressive 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 in-
t:ruder by staring and vocalizing. I have termed this behavior
a "threat." 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. The intruding animal usually left the area. Fourteen times a male was the individual who was feeding when a sound was heard, while the intruder was a fe- male; 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 ter- ritory 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 du- ration (about 0.04 sec) and single pulsed in 21 out of 30 ob servations (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 male male fight (B) and a section, taken at the point of the arrow of the above grunt (c). 38
.~ '
0.1 0.2 0.3 0.4 TIME I SEC
16 c 12 ~ ~ 8 ~ 4 0
AMPLITUDE 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 air-
borne 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 repre-
sented 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, 3 - 10 KHz according to Wallace and. I'1ahan (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. This hypothesis is supported by Turner (1973) in which a1arm calls given by females ceased only after all the young animals had returned to the vi cinity of the burrow. Also, Balph & Balph (1966) reported that chirps, used by ~. 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 de- pending 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 pes- sible 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 pred ators 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. Only when the bird flew, was a single squeal sounded. Fitch (1946) also saw hawks perched in trees at a verJ close range which did not elicit vocal response in the ~. beecheyi he was studying until they flew. 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 s~uirrels before they chirp than can larger hawks. 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 in- volving vigorous physical contact. The sounds produced during these encounters appear to be closely associated with the hier- archical 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 di- minishing the number of potentially destn1ctive interactions.
b1 the California ground squirrel two vocalizations, the gn1nt and the chatter, appear to indicate dominance. They were co~~only 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 sub- ordinate (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 aggressive- ness. 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 s~uirrel in which this type of graded signal has been reported, ~. tridecemlineatus, does not, however, follow this generalization. The growls it uses as agonistic sounds are shortest in the most intense inter- actions, 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~ueal of the California ground s~uirrel for the same purpose. The s~ueal of ~· armatus is highly variable in structure, fre~uency and length; it includes several bands of fre~uency and consists of several syllables, unlike the single fre~uency squeal of ~· beecheyi which is always a single syllable call. 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 com mon 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 situ ations (Harris, 1966). The Uinta ground squirrel (~. armatus), for instance, has been reported to emit tooth chatter in asso ciation with close aggressive encounters (Balph & Balph, 1966) while the thirteen lined ground squirrel, Spermophilus tri decemlineatus, 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 fre quency 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 enclos~d in cages or traps; Uinta ground squirrels (£. armatus) have been re- ported to do so also (Balph & Balph, 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 pat- tern 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 en- counters 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 dis
tinctive 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 dis
plays 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 situ
ations. ~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 spectro graphically 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 cir cumstances, 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 alert
ness, 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 ele
ments (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 ~· spilosoma and~· mexicanus (Matocha, 1975; Balph & Balph, 1966), 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. All three calls have quite similar fundamental frequencies (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 ~· beldingi, reported by
~~mer (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 imme diate (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 ad vantage of understanding each other's alarm signals.
As mentioned previously, vocalizations of the California ground squirrel have been described by Owings et al. (1977), Fitch (1949) and Linsdale (1946). Only Owings et al., who were mainly concerned with sounds emitted during alarm situations, presented sonagrams. Fitch and Linsdale did not use sound spectrograms. 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 sug gests 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. But I hope the table may serve as an aid in future work. Table .5
Catalog of the vocalization of the California ground SQuirrel
Name used Functions described Previous name Function described in this paper in this paper and source previously
SQUEAL Immediate alarm, A loud chirp Alarm call in re signaling submission described as sponse to low-flying "cheesk" (Fitch) large birds
Very sharp chirp Alarm note (Linsdale)
Whistle (Owings Alarm in response to et al.) low-flying raptors
CHATTER Given in the be A rolling sound Alarm in response to ginning of a long which fades gradually snakes call, or for threat towards its end and signaling dominance (Fitch)
LONG CALL General alarm Chatters followed by Alarm in response to a series of chats a ground predator (Owings et al.)
Long series of barks No function mentioned given more rapidly than one per second (Linsdale)
\.n -.J Table 5-continued
Name used Function described Previous name· Function described in this paper in this paper and source previously
LONG CALL General alarm "Chuee-chu-chu-chuk" Alarm in response to followed by a series a dog, a coyote or of less sharp chirps humans (Fitch)
GRUNT Intimidating a more Growl (Fitch) Given during en submissive animal, counters, usually or given during when forced to take fights refuge in the burrow cf another animal, or while fighting
Grunt or growl To frighten other (Linsdale) squirrels from a burrow
TOOTH CHATTER Used mainly during Tooth chatter Heard during an territorial disputes (Owings et al.) encounter between two animals involving a lateral approach and flank push
l...r\co Table 5-continued
Name used in Functions described Previous name Function described this paper in this paper and source previously
WHISTLE Used during sexual chases
SCREAM Used during territorial encounters, as an announcement of a fight
V\ '..0 60
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