Analysis of the vocal repertoire of adult pikas: ecological and evolutionary perspectives

Anita. Behav., 1985, 33, 124-134

Analysis of the vocal repertoire of adult pikas: ecological and evolutionary perspectives D O U G L A S A. C O N N E R

Department of Environmental, Population and Organismic Biology, University of Colorado, Boulder, Colorado 80309, U.S.A. Abstract. Analyses of vocalizations and behaviour of field and captive populations of pikas (Ochotona princeps) indicate that adults use at least nine structurally distinct acoustic signals in a variety of contexts.

The pika acoustic repertoire more closely resembles in size and form the repertoires of many rodent species rather than those of other lagomorphs. The evolution of an elaborate acoustic repertoire has been influenced both by the pikas' atypical social organization and the visually disruptive environment in which they live.

Pikas (Ochotonaprinceps) are small, diurnal, nonhibernating lagomorphs that inhabit rock piles (talus) in the mountains of North America, Through most of the year, individuals defend territories encompassing talus with adjoining patches of vegetation (Smith 1981). In the breeding season, a male enlarges its territory to include one or more female territories. Juveniles are forced out of the mother's territory after weaning, and must establish their own territory on the talus or disperse. Males do not contribute to the care of their offspring. There are apparently two litters per season (Smith 1981; Smith & Ivins 1983). Following the breeding season, males and females gather vegetation, which is stored in hay piles within their territories to serve as a food source over the winter (Conner 1983a). There have been several descriptive studies of pika vocalizations as part of more extensive studies of ecology and behaviour (Severaid 1956; Broadbooks 1965; Krear 1965; Barash 1973; Sharp 1973; Tapper 1973; Whitworth 1984). Most investigators mention only the short and the long calls. However, Severaid (1956) listed eight calls, Sharp (1973) recognized four, and Wbitworth (1984) provided sonagrams of the eight calls which had been reported by Severaid (1956). Somers (1973) and Conner (1982, 1983b) studied geographic differences in pika short calls and related this variation to the isolated nature of pika populations. Some temporal measurements of the long call were provided by West (1980). He found significant inter-individual differences, which could potentially be used by pikas for individual recognition.

The most basic questions concerning vocal signals used by pikas in social communication are unanswered. They are probably the most habitatspecific of any small mammal species (Smith 1981). Because the talus they live in is discrete and patchy, it is possible to define reliably their areas of activity. Pikas are diurnal, conspicuous, and habituate quickly to observers. Finally, they are certainly the most vocal of the lagomorphs. The apparent diversity of their vocalizations and the rate at which they use these calls makes them an ideal animal to use in a study of acoustic communication. The present field and laboratory study was designed to answer a number of questions regarding the pikas' vocal communication. (1) How many structurally and functionally distinct vocalizations do adult pikas employ? (2) Who gives these signals and in what contexts? (3) What possible functions do vocalizations serve for the individual?

MATERIALS AND METHODS

I observed and recorded pikas in three populations on the north side of Niwot Ridge, Boulder County, Colorado, about 62 km west of the city of Boulder. Elevations at the sites ranged from 323t to 3281 m. Animals were live-trapped, weighed, sexed, and marked individually with plastic coloured ear-tags. Observations and recordings were made from May 1981 to October 1982. Vocalizations and behavioural data were also obtained from a captive population of pikas maintained in the Department of Environmental, Popu-

124

Conner: Pika vocal repertoire

125

Table I. Description of measurements used in the analysis

of pika short calls and other vocalizations in this study*

.r

I Ii

i kHz

4

O f----.,_._

0

!

!

0.4

0.8

sec

Figure 1. Narrow-band (45-Hz) sonagram of a short call

and the measurements that were used in analysing short calls. An explanation of these measurements can be found in Table I.

lation and Organismic Biology at the University of Colorado, Boulder. Pikas were kept individually in metal cattle troughs lined with alfalfa (Medicago sativa). Vocalizations were recorded from individually housed animals, during male-female pairings arranged for breeding purposes, and from wild-caught pregnant females and their offspring born in the laboratory. Recordings in the field were obtained using an Electro-Voice omnidirectional microphone mounted in a Sony PBS-800 parabolic reflector or an Electro-Voice Soundspot unidirectional microphone and a U h e r 4000 Report IC tape recorder (flat response from 500 to 18 000 H z at 19-05 cm/s). Sound recordings in the laboratory were made with an Electro-Voice omnidirectional microphone mounted in a Sony PBS-800 parabolic reflector and a Sony tape recorder (model TC-800B) (flat response from 500 to 18 000 Hz at 19.05 cm/s). Sound recordings were analysed with a Kay Elemetrics Sona-Graph 6061B, using both narrow- (45-Hz) and wide-band (300-Hz) settings, and a Tektronix model 5223 digitizing oscilloscope. Short calls were measured for 12 structural parameters (Fig. 1, Table I). Different variables were used for the other call types; these are described in the Results. Measurements were made with the aid of a plastic overlay on which a frequency and time scale were marked. Short calls were recorded in territorial and alarm

1. Initial Fundamental Frequency (IF): frequency of the initial portion of the fundamental tone of vocalization (a) 2. Initial Frequency of the Fourth Harmonic (I4F): frequency of the fourth harmonic, which corresponds to third multiple of the fundamental tone (b) 3. Middle Frequency of the Fourth Harmonic (M4F): frequency of the fourth harmonic at a point mid-way through the call (e) 4. Terminal Frequency of Fourth Harmonic (T4F): frequency of the fourth harmonic at termination of the call (g) 5. Note Duration (DNOT): duration of call note. For short calls, this is equivalent to the duration of the call ( d - c ) 6. Number of Changes in Frequency (NFC): number of times a change in direction of frequency occurs within a note. Figure 1 has a single change in direction of frequency from an increase to a decrease in frequency 7. Bandwidth (BAN): the difference in frequency between the highest and lowest frequency of the fourth harmonic ( f - g) 8. Bandwidth Divided by Duration (DBAN): bandwidth divided by the duration of the call note multiplied by a factor of 100 9. Amount of Frequency Change (AMT): the sum of the differences between the highest and lowest frequency for each change in frequency of the fourth harmonic [(i-j) + ( f - g)] 10. Amount of Frequency Change Divided by Duration (AMD): AMT divided by note duration, multiplied by a factor of 100 11. Mean Frequency (MBAN): midpoint of the frequency bandwidth [(f+ g)/2] 12. Peak Amplitude (PEK): measured from an oscilloscope trace of a call: the time in seconds to the peak (greatest) amplitude (signal strength) of a note divided by the note duration * Abbreviations for a particular measurement are in parentheses following the name of the measurement. Lower case letters following the description refer to the illustration of the short call in Fig. 1.

contexts. These were analysed for significant structural differences using stepwise discriminant function analysis (Nie et al. 1975), with context as the group variable. Analyses were performed on the calls of four individuals grouped together and on the calls of each individual separately. A playback series was also performed on the two field populations (eight individuals), using calls recorded in territorial and alarm contexts. Each

Animal Behaviour, 33, 1

126

Table II. Behavioural response scale used to measure

responses to natural and playback short calls Behavioural category Orientation

Rank 0~Does not look at playback 1--Looks toward playback source 2--Turns body to face playback

Calling (within 5 s) 0~No vocalization in response 1--Single call 2--Short call series 3--Long call series Movement

0~Does not move from perch 1--Lifts ventral surface from substrate 2--Moves less than half the distance toward playback 3--Moves greater than half the distance toward playback 4--Retreats into rocks or away from playback

call was separated by 5 min of silence, and the order in which the two calls were presented was changed randomly after each series. Each series of three to five calls of each type was presented through a 12.7-cm Radio Shack speaker and the Sony tape recorder, and was separated by at least 30 min of silence. No individual was tested with more than two series in any 24-h period. Before a series began, an individual had to be stationary (perched on a rock) and facing at least 45 ~away from the speaker. Responses to the two calls were scored according to the type of response and a subjective measure of the response intensity (Emlen 1971). The latency to respond and the response duration were also measured (see Conner 1983b). The behavioural response scale is shown in Table II. Wilcoxon signed-rank tests for matched pairs were used to test for significant differences in the intensity, latency and duration of responses to the two calls (Conover 1980). Statistical significance was accepted at the 0.05 level.

RESULTS

Short Calls

Short calls from the three populations consisted of a harmonically complex single-note structure

with harmonics extending up to 14-16 kHz. Calls had an average initial fundamental frequency of 1187 Hz, with a duration of 0-17 s. Some pronounced frequency modulation was characteristic of all calls analysed, with the number of changes in frequency within a note having the greatest amount of variation (Coefficient of Variation (CV)= SD/~ X 100 = 46"4%). Analysis of call structure and playback experiments suggest that pikas are able to and do distinguish between familiar and unfamiliar individuals by their short calls (Conner, in press). The pika short call was recorded in two contexts. Throughout this study, pikas gave short calls (Fig. 2B, Table III) in an alarm context to both potential terrestrial and avian predators, as well as to any stimulus that appeared suddenly near or on the talus. Pikas also gave short calls (Fig. 2A, Table III) in what may best be described as a territorial context. Individuals would call periodically when perched on a rock within their territories, when sighting an intruding pika, or before and after leaving their territory to gather vegetaton from the adjacent alpine meadows. (Territorial short calls appear to function in maintaining the integrity of a resident's territory: Conner 1983c.) The rates with which the alarm and territorial short calls were given differed according to the time of the year (Fig. 3). Except for a rise in August, the frequency of alarm calls did not vary appreciably during the summer and early fall. Short calls given in territorial context rose abruptly in July from a rate comparable to the rate of alarm calls in June. They reached a peak in August and declined slowly through October. At this time, they were still heard at a much greater rate than alarm short calls. As can be seen from the figure, the pattern of total short call production more closely resembles that of territorial short calls. A stepwise discriminant function analysis was performed on 77 short calls given by four individuals in alarm (37 calls) and territorial contexts (40 calls). Twelve call measurements (Table I) were used as independent variables (after log transformation to satisfy conditions of normality and equality of variances) to determine whether differences in context (group variable) could be separated by the interaction of any of the independent variables. A discriminant function with six variables was obtained (Table IV). The initial frequency of the fourth harmonic and the note duration had the greatest loadings on the discriminant function (Table IV). Of the 77 short calls

Conner." Pika vocal repertoire

127

8 6 4 2 8 6 4

N

2

- t | | i ~

"1-

8 -

~ ---

F

6 4 2 G

8 6 4

0.4

0.8

1.2

1.6

2.0

2.4

2 8

sec Figure 2. Narrow-band (45-Hz) sonagrams of seven acoustic displays in the adult pika repertoire. (A) Short call in a territorial cont&xt. (B) Short call in an alarm context. (C) Panic call. (D) Tooth chatter. (E) Male trill. (F) Female wail given in response to an infant call. (G) Submissive wail.

analysed, 57 (74-03~o) were correctly classified according to context. A second d i s c r i m i n a n t function analysis was performed o n the a l a r m a n d territorial s h o r t calls of each o f four individuals (Table V). W h e n the short calls were analysed by individual, a n even greater p r o p o r t i o n of territorial a n d a l a r m calls

were correctly classified. T h e classification results for three individuals were 100~. T h e s h o r t calls o f the f o u r t h p i k a were correctly classified 9 5 ~ o f the time. While some call characteristics were c o m m o n to all four individuals, n o c o m b i n a t i o n was shared a m o n g two or m o r e animals. This indicates t h a t each individual m a y use a unique c o m b i n a t i o n o f

Animal Behaviour, 33, 1

128

Table III. Call characteristics ()~_+SD) from four individuals for short calls given in alarm and territorial

contexts* IF (Hz)

Context

I4F (Hz)

M4F (Hz)

T4F (Hz)

DNOT (s) NFC

BAN (Hz) DBAN AMT AMD

PEK

MBAN (Hz)

Terrkorial

1241 4624 4855 3703 0- I6 _+163 _+328 _+306 _+375 +0.02

1-4 1603 _+0-6 _+368

97 -+20

2184 136 _+532 -+36

0-28 4468 _+0.09 _+327

Alarm

1128 4547 4638 3572 0.17 _+ 128 _+496 _+273 -+339 -+0.02

1.2 1570 _+0.6 -+263

94 -+24

2170 128 0.27 4357 _+348 _+21 _+0.09 _+289

* For explanation of call measures, see Table I. Table IV. Summary statistics of discriminant func-

tion analysis of 77 short calls given in alarm and territorial contexts ~16

~

~

T~ (Air) T(,rt~lOtiaCl aLsl(T)

g

June (97)

July (406)

Aug (606) Month

Sept (307)

Oct (179)

Figure 3. Changes in short call rate from June to October for territorial, alarm, and total short calls. The number of calls heard is shown in parentheses for each month.

call characteristics to encode differences between the two types of short calls. The results of the playback series using short calls recorded in territorial and alarm contexts (Table VI) show that there were no significant differences in either the intensity, latency or duration of a pika's response to playbacks of alarm and territorial short calls. Apparently, pikas do not respond differently to short calls in different contexts.

Panic Call

This vocalization (Fig. 2C) is heard in several different stressful situations. Panic calls are given when an individual is caught in a live trap, chased by another pika, when startled (infrequently), or preceding an adult wail (see below). In most situations, the call consists of only a single note and is not repeated. This vocalization has been described previously as a higher-pitched and shorter version of the short call. It has a higher fundamental frequency and a

Variable

Function 1

Initial frequency of fundamental Initial frequency of 4th harmonic Middle frequency of 4th harmonic Note duration Number of frequency changes Bandwidth Eigenvalue Canonical correlation Variance explained Wilk's lambda X2 Degrees of freedom Significance

0'59919 1.04649 0-68830 0.90296 0.68432 0.32382 0.42674 0.54690 100 0.70090 25.588 6 0.0003

shorter note duration, but it also differs in other structural parameters. A stepwise discriminant function analysis of the 12 log-transformed call measurements on short ( N = 3 0 ) and panic calls (N = 16) resulted in a single significant discriminant function. O f the seven variables remaining after the analysis, those loading highest were the amount of frequency modulation and amount of fi'equency modulation divided by call duration. Call frequency and duration, while significant, were less important. The discriminant function classified 91.3~ (42) of the 46 calls in the correct group (short or panic calls).

Long Calls The long call (Fig. 4), which is a series of single, double or triple call notes strung together into a vocalization lasting 5-35 s, is given by both males and females, although there are differences between

Conner: Pika vocal repertoire

129

Table V. Discriminant analysis summary statistics for short calls of four pikas in alarm and territorial contexts* Individual:

WW Variables

YY

Function 1 Variables

OO

GO

Function 1 Variables Function 1 Variables

IF M4F T4F DNOT

0.60368 0.63156 -0.84647 0.99068

IF 1.16065 I4F -0.92900 DNOT 1.37092 NFC -0.36764

Eigenvalue Canonical correlation ~o Variance explained Wilk's lambda )~2 Degrees of freedom Significance ~o Calls correctly classified

4.65628 0.90731 100 0.17679 24.259 6 0.0005

9.41427 0.95078 100 0.09602 33.976 5 0.0000t

100

100

M4F T4F NFC AMT

0.79979 1.78724 0.97776 1.50354 1-52065 0.77671 100 0.39672 14.792 6 0.0219 95.24

IF I4F BAN DBAN

Function 1 0-68253 1.30095 0.75069 - 1.26991 24.25385 0-98000 100 0.03960 45.206 4 0.0000t 100

* See Table I for variable abbreviations. ] The low level of probability exceeds the limits of the program.

Table Vl. Mean response intensity, latency and duration to playbacks of short calls in territorial and alarm contexts

Context Territory Alarm

Vo Latency Duration Responded Intensity* (s) (s) to 1.3 1.4

0.71 1-11

8.1 8.6

73 86

* The intensity of a response is the sum of the ranks for the three behavioural categories in Table II. the sexes in its structure. The first few notes at the beginning of a long call are structurally distinct from the remaining notes of the call. Neither the initial notes, nor the notes making up the major portion of an individual's long call, are identical to an individual's short call (compare Fig. 4 to Fig. 2A or B; vocalizations are from the same individual). In the laboratory, males gave long calls while in pursuit of females with w h o m they had been paired during breeding attempts. This was in early summer, a time when captive males would also longcall spontaneously or in response to short calls or other long calls (by pikas in the laboratory). In the field, male pikas gave long calls predominantly during the breeding season (April to June 1982). Males and females gave long calls to a lesser extent during September and October 1982. During the

breeding season, male long calls were most frequently (47.4~) given in response to the short calls of other males and females on the talus. Another 21-1~o were preceded by long calls of other males, and the remainder (31.5~) occurred spontaneously. Long calls given early in the summer, both in the field and in the laboratory, were preceded by a low-amplitude trill (Fig. 2E). O f the early-summer long calls recorded in the laboratory (21) and field (37), only 18~ were not preceded by a detectable trill vocalization. During early fall, none of the long calls heard had a detectable trill preceding it. Fall long calls were heard most often during territorial disputes, especially when one animal was actively attempting to move onto another's territory and the two were in close proximity to one another. Long calls of females given during the breeding season were of two types but neither was recorded in this study. Females in the laboratory infrequently gave long calls similar in form to the male long series early in the summer (Whitworth, personal communication). This occurred most often after agonistic interactions during breeding attempts by males. In the field, I did not hear any females give this long call in the breeding season during this study. The second call given by females consisted of 4-9 ()~= 5"6_+ 3" 1) evenly-spaced call notes, each about as long as the female's short call and with a shorter inter-note interval than that

Animal Behaviour, 33, 1

130 8 6

kHz 4

o18

o'.4

112

1'.6

2'.0

2'.4

21~

312

16.4

16.8

17.2

17.6

26.8

2"7.2

2i.6

28'.0

sec 1"

!t

6

kHz 4

14.8

15.2

15.6

16.0

sec 8 84 6 84

kHz 4

2'

25.2

25.6

26.0

26.4 sec

8

.if~;. 6

kHz

e2-4-

4 2

a4.a

a2'.2

a~.6

3a'.o

a~.4

ad.a

a~.2

3~.6

sec

Figure 4. Narrow-band (45-Hz) sonagrams of selected portions of a male long call given during the breeding season.

found in territorial or alarm short call series. This call was also heard most frequently when male and female territories overlapped early in the summer. Males and females whose territories overlapped at this time would, at times, call in turn. Usually, the male would give a long call on the surface preceded by a trill. Often, as the long call progressed, the male would slowly turn 360~ on the rock on which

he was perched. The female, if not on the surface, would often emerge from the rocks and give a single short call or a long-call series.

Tooth Chatter The tooth chatter (Fig. 2D) consists of a series of closely spaced brief sound pulses ()~ note

Conner. Pika vocal repertoire duration = 0-02 s) with a mean inter-note interval of 0.14 s and a mean frequency of 4346 Hz. The number of notes per call ranged from 5 to 15 (N= 16). The tooth chatter is used in an aggressive context, most frequently by males. It is not a vocal sound: rather, it is produced by an anterior-posterior nlovement of the upper and lower incisors against each other. This sound-was heard at times during male-female pairings in the laboratory, and was produced in the field by territorial residents when in close proximity to intruders. It is a very low-amplitude sound and could be heard only when I was close to the pika that produced it.

131

turally very different from the submissive wail and is given in an entirely different context. The frequency range is similar, but the note duration is much longer (J~=0-42 s). There is also less frequency modulation in the notes and fewer notes per call (range 3 4). The second wail is given by pregnant or lactating females to the harsh nursing chirps of infant pikas. At the same time the calling animal moves around, apparently attempting to find the source of the infant vocalization. This call could also be stimulated by a human observer imitating the nursing chirp call of the young.

Cough Trill The trill (Fig. 2E) is a low-amplitude vocalization which slightly resembles the tooth chatter on sonagrams. It consists of a series of closely spaced notes, 0.02 s in duration and spaced 0.05 s apart. The fundamental frequency of the initial note averaged 946 Hz, and there was usually an increase or decrease in the fundamental frequency of the following notes. Two to three harmonics were usually present. An average call consisted of six notes (range: 2-22) and lasted 0-25 s. Unlike the tooth chatter, the pika trill is a vocal sound and has a more noticeable tonal quality to it. It is given by adult males during the breeding season when following and attempting to mount and copulate with females. This is the trill that often imnlediately precedes the male long call. Females in this study were not heard giving this vocalization, although Severaid (1956) has reported it in females.

'Coughing' or 'huffing' is produced by a violent, brief, forced exhalation through the open mouth. This was the only pika sound not heard in the field. In the laboratory, it occurred during an aggressive interaction between two females, one of whom had been placed in the other's holding bin. It was given by the resident animal as she chased the introduced female.

DISCUSSION The acoustic repertoire of adult pikas consists of at least nine displays, seven vocal and two non-vocal (not produced by vibration of the vocal cords). The trill, tooth chatter and cough are relatively lowamplitude signals, whereas the short calls, panic call, wails and long calls are very loud vocalizations.

Adult Wails

Pika Short Calls

Adult pikas give two types of distress vocalizations, each in a specific context. The first is a submissive wail (Fig. 2G), which is given during aggressive interactions by the subordinate (retreating) animal and during mating attempts by unreceptive females. Structurally, it consists of two types of notes. There is usually a single initial or introductory harmonically complex frequencymodulated note 0.14 s in duration, which increases in frequency. The initial fourth harmonic frequency averages 4079 Hz, with a mean terminal frequency of 5338 Hz. The remaining 3-8 notes are also harmonically complex and frequency-modulated, with a duration of 0-16 s. The second wail vocalization (Fig. 2F) is struc-

Territorial and alarm short calls produced by the same individual are easily separated by call structure, but there is no single call characteristic or set of characteristics that varies together among all individuals. Each individual may use a unique set of characteristics to encode alarm or territorial messages. For receivers, this requires that they are able to perceive the individual encoding rules of each neighbouring pika if they are to make full use of the information a short call contains. Whether they make this perceptual distinction is difficult to determine, because the results of alarm and territorial playback experiments are inconclusive in this regard. Individuals in this study did not respond differ-

132

Animal Behaviour, 33, 1

entially to playbacks of alarm and territorial short calls, although they did respond to them significantly more than to neutral, non-pika calls. A lack of response to a playback or even to naturally occurring calls may be the result of one of three possible causes: (1) the animal may not be able to detect and process physical differences between the two calls, (2) the animal may perceive the differences but may attach no significance to them, or (3) the animal may perceive the differences, but the adaptive responses to the two messages may be the same, or the differences are not detectable by response measures available to the observer. The last explanation is probably the most likely, for several reasons. Individual structural differences exist between the two calls. In addition, a discriminant function analysis of alarm calls given to terrestrial and avian pedators has shown differences in sets of call characteristics which may be used to encode information about different classes (terrestrial and avian) of predators (Conner 1983c). There are also differences in calling behaviour associated with territorial and alarm short calls, such as in the rate of vocalizing (Ivins & Smith 1984), number of calls in a series (Ivins & Smith 1984; this study), and interval between calls (Conner 1983c), all of which suggest that it is adaptive for a pika to be able to determine whether a short call is a territorial or alarm display. Finally, for an animal that is cryptically coloured to match its talus habitat (Conner 1982), and for one that is on its own territory, the most adaptive reaction to either display is probably to do very little either in response to a territorial call (because of energy considerations) or to an alarm call (in order not to make oneself obvious). Once the situation has been evaluated, a response appropriate to the specific situation can be made.

Long Calls Male pikas during the breeding season are faced with two distinct problems. They must attract, court and breed with a female and they must also defend their territories from neighbouring males. Female pikas, on the other hand, are concerned primarily with maintaining the integrity of their territory, which has to support both them and their young until the young are independent. The long call, like the territorial short call, serves an advertisement function related to the caller's territory. Although West (1980) does not mention the trill

preceding male long calls, the trill could be a significant aspect of sexual advertisement. The trill, being a low-amplitude display, is probably directed towards females (which can approach males at this time) while the long call, a loud vocal and somewhat obvious visual display (males often turn 360 ~ as they call), is directed primarily at the males. The female long call appears to serve a territorial function by advertising to other pikas that the talus area occupied by the female is taken. Because females require a territory of their own during the year to raise young, as a defence against predation, and for hay-pile storage, it seems likely that such a vocal display advertising territory ownership would be valuable, It is interesting to note that long calls given outside the breeding season lack the trill and are directed at territorial intruders of both sexes. Long calls were given to intruders by residents which rarely chased the intruder for any distance. Short calls, on the other hand, were given prior to and during active chases which usually extended beyond the resident's territorial border. While both long and short calls serve a territorial function at this time, the long call also suggests that the caller is less likely to interact and/or more likely to remain where it is. On the basis of a univariate analysis of male long calls during the breeding season, West (1980) suggested that the temporal patterning of calls seems to be the principal method of distinguishing individuals, while constancy in note structure, duration and call patterns maintains species-specificity. Another part of my study (Conner 1983c) has shown that both note structure (frequency modulation) and note duration vary significantly among individuals and probably do not play a significant role in species-specificity. Given the large amount of variation between individuals in both short and long calls, species recognition (or, more probably, population recognition: Conner 1983b) is probably a complicated interaction of a suite of call characteristics which has not been determined.

Agonistic Acoustic Displays The agonistic vocal displays of pikas clearly resemble those of other small mammals. The tooth chatter, one of the pikas' non-vocal acoustic displays, is a common vocal agonistic display in many rodent species. It is given primarily by aggressive individuals, and is related to threat and often

Conner: Pika vocal repertoire

precedes attack (Balph & Balph 1966; Zelley 1971; Brooks & Banks 1973; Smith et al. 1977; Gould 1983). The cough, the other non-vocal acoustic display, was given by a resident female to a female intruder but was not heard during male-male or male-female agonistic interactions. The submissive wail and panic call are the two submissive vocal displays associated with agonistic interactions. The submissive wail predominates in aggressive interactions and apparently functions as a display which allows escape. During the late summer, when competition is intense and territorial intrusions frequent, the submissive wail given by sighted and chased intruders often results in the resident allowing the intruder to escape unharmed. Submissive wails are also common during the breeding season and are given by unreceptive females in response to male trills, male pursuits, and attempted mountings. In this context, the wail does not necessarily inhibit the other pika's advances as it does during territorial intrusion. The panic call is an escape-related vocal display heard often in situations in which other conspecitics are not directly involved. Panic calls are given by trapped animals, by pikas that unexpectedly meet other species while moving along the talus or meadows, when being chased or seached for by a predator, or when startled by another pika.

Wail in Response to Infant Vocal Displays The wail given in response to infant distress calls was given only by lactating or pregnant females in response to the calls of related or non-related infants. Females increased their motor activity while calling and this activity was usually, but not always, directed toward the source of the infant calls. That it could be stimulated by the observer imitating an infant call suggests that the stimulus configuration necessary to elicit the call is not very specific and the response threshold of the female is low. Possible explanations are that the call may attract young to the mother when they are capable of leaving the nest, or that it may stimulate continued calling in the young which serves as a homing cue for the female.

133

ground-dwelling sciurids (Waring 1966; Betts 1976; Smith et al. 1977; Smith 1978; Koeppl et al. 1978) and other rodents. Pikas are singly territorial and defend individual territories most of the year (Smith 1981). This type of social organization does not always require an elaborate communication system. For the pika it does, however, because individuals that are aggressive for most of the year must, during the breeding season, come together for mating. Contact signals may be necessary for establishing and maintaining pair bonds and for actual breeding behaviour. Also, though individuals are territorial because of their restriction to talus, they must come in contact, simply because of their close proximity to one another. Competition for space, food resources and breeding opportunities is therefore high. An efficient mechanism for dealing with inter-individual competition which avoids the maladaptive consequences of physical combat and time-consuming chases is an elaborate communication system. As a result, a repertoire of diverse vocal and probably olfactory displays (Meaney 1983) has developed. The pika's habitat may also have influenced the physical structure of the pika's vocal repertoire in order to maximize localization of calls, minimize the degrading effects of background noise (wind), and scattering due to the physical structure of the environment (Wiley & Richards 1978). All of the adult calls involved in long-distance communication (short calls, panic calls, long calls and wails) are characterized by a broad frequency range, repetitive temporal structure frequency modulation and abrupt onset and termination (Conner 1982; this study). These syntactic characteristics allow for binaural comparisons of phase, intensity and time differences which aid in signal source localization (Marler 1967). The acoustic modatity has evolved as an important communication channel because pikas live in a visually disruptive environment and signals need to travel over appreciable distances. Auditory signals are not stopped by the rocky habitat, can be varied structurally in diverse ways to carry many kinds of information, and do not require close contact between signaller and receiver.

Ecological and Evolutionary Perspectives Pikas, unlike other lagomorphs (Peters 1980; Eisenberg 1981), have evolved an extensive vocal repertoire which is much more similar in size and function to some of the more vocal tree- and

ACKNOWLEDGMENTS This study was supported in part by grants from the National Academy of Sciences, Sigma Xi, the

Animal Behaviour, 33, 1

134

Alexander F u n d , N S F G r a n t BNS-79-23463 to M. Bekoff, a n d two University o f C o l o r a d o G r a d u a t e Fellowships. Charles Southwick a n d Molly W h i t w o r t h generously provided access to the captive pika population. M a r c Bekoff, Sherry Conner, V. J. D e G h e t t a n d a n a n o n y m o u s reviewer provided c o m m e n t s on the manuscript. Sherry C o n n e r was an invaluable assistant in the field. C o m p u t e r time was provided by the D e p a r t m e n t o f E n v i r o n mental, P o p u l a t i o n a n d Organismic Biology, U n iversity o f Colorado.

REFERENCES Balph, D. M. & Balph, D. F. 1966. Sound communication of Uinta ground squirrels. J. Mammal., 47, 440 450. Barash, D. P. 1973. Territorial and foraging behavior of pika (Oehotona princeps) in Montana. Am. Midl. Nat., 89, 202-207. Betts, B. J. 1976. Behaviour in a population of Columbian ground squirrels, Spermophilus eolumbianus columbianus. Anim. Behav., 24, 652 680. Broadbooks, H. E. 1965. Ecology and distribution of the pikas of Washington and Alaska. Am. Midl. Nat., 73, 29%335. Brooks, R. J. & Banks, E. M. 1973. Behavioural biology of the collared lemming (Dierostonyx groenlandicus Traill): an analysis of acoustic communication. Anim. Behav. Monogr., 6, 1-83. Conner, D. A. 1983a. Seasonal changes in activity patterns and adaptive value of haying in pikas (Ochotona prhweps). Can. J. Zool., 61, 411-416. Conner, D. A. 1983b. Response of pikas to playback of geographic variations of the short call. J. Mammal., 64, 33(~337. Conner, D. A. 1983c. Acoustic communication in pikas (Oehotonaprineeps). Ph.D. thesis, University of Colorado, Boulder. Conner, D. A. In press. The role of the pika short call in individual recognition. Z. Tierpsychol. Conover, W. J. 1980. Practical Nonparametric Statis'tics. New York: John Wiley. Eisenberg, J. F. 1981. The Mammalian Radiations: An Analysis of Trends in Evolution, Adaptation, and Behaviour. Chicago: University of Chicago Press. Emlen, S. T. 1971. The role of song in individual recognition in the indigo bunting. Z. Tierpsychol., 28, 241-246. Gould, E. 1983. Mechanisms of mammalian auditory communication. In: Advances in the Study of Mammalian Behavior (Ed. by J. F. Eisenberg & D. G. Kleiman), pp. 265-342. Special publication no. 7 of the American Society of Mammalogists. Ivins, B. L. & Smith, A. T. 1984. Responses of pikas to naturally occurring terrestrial predators. Behav. Ecol. Sociobiol., 13, 277~86. Koeppl, J. W., Hoffmann, R. S. & Nadler, C. F. 1978.

Pattern analysis of acoustical behavior in four species of ground squirrels. J. Mammal., 59, 677-696. Krear, H. R. 1965. An ecological and ethological study of the pika (Ochotonaprinceps Bangs) in the Front Range of Colorado. Ph.D. thesis, University of Colorado, Boulder. Marler, P. 1967. Animal communication signals. Science, N. Y., 157, 769-774. Meaney, C. A. 1983. Olfactory communication in pikas (Oehotona princeps). Ph.D. thesis, University of Colorado, Boulder. Nie, N. H., Hull, C. H., Jenkins, J. G., Steinbrenner, K. & Bent, D. H. 1975. Statistical Package Jot the Social Sciences. New York: McGraw-Hill. Peters, R. 1980. Mammalian Communication. A Behavioural Analysis of Meaning. Monterey, California: Brooks/Cole. Severaid, J. H. 1956. The natural history of the pika (mammalian genus Oehotona). Ph.D. thesis, University of California, Berkeley. Sharp, P. L. 1973. Behaviour of the pika (Ochotona princeps) in the Kananaskis region of Alberta. M.Sc. thesis, University of Alberta, Edmonton. Smith, A. T. 1981. Territoriality and social behavior of Ochotona princeps. In: Proceedings of the Worm Lagomorph Conference (Ed. by K. Meyers & C. D. McInnes), pp. 310-323. Ontario: Guelph University Press. Smith, A. T. & Ivins, B. L. 1983. Reproductive tactics of pikas: why have two litters? Can. J. Zool. 61, t551-1559. Smith, C. C. 1978. The structure and function of the vocalizations of tree squirrels (Tamiasciurus). J. Mammal., 59, 793-808. Smith, W. J., Smith, S. L., Oppenheimer, E. C. & Devilla, J. G. 1977. Vocalizations of the black-tailed prairie dog, Cynomys ludovieianus. Anim. Behav., 25, 152-164. Somers, P. 1973. Dialects in Southern Rocky Mountain pikas, Ochotona princeps (Lagomorpha). Anita. Behav., 21, 124-137. Tapper, S. C. 1973. The spatial organization of pikas (Ochotona), and its effect on population recruitment. Ph.D. thesis, University of Alberta, Edmonton. Waring, G. H. 1966. Sounds and communications of the yellow-bellied marmot (Marmota flaviventris). Anim. Behav., 14, 177-183. West, E. W. 1980. Adaptive patterns in behavior of the Sierran pika, Ochotonaprinceps. Ph.D. thesis, University of California, Davis. Whitworth, M. R. 1984. Maternal care and behaviourat development in pikas, Ochotona princeps. Anita. Behav., 32, 743-752. Wiley, R. H. & Richards, D. G. 1978. Physical constraints on acoustic communication in the atmosphere: implication for the evolution of animal vocalizations. Behav. Ecol. Sociobiol., 3, 69-94. Zelley, R. A. 1971. The sounds of the fox squirrel, Sciurus niger rufiventer. J. Mammal., 52, 597 603.

(Received 30 September 1983," revised 23 February 1984; MS. number." .44169)