Journal of Comparative Psychology Copyright 1991 by the American Psychological Association, Inc. 1991, Vol. 105, No. 2, 125-133 0735-7036/91/J3.00 Localization in Small : Absolute Localization in Azimuth

Thomas J. Park and Robert J. Dooling University of Maryland, College Park

Nine small birds of 3 species (Melopsittacus undulatus, Serinus canarius, and guttatd) were trained in an operant procedure to fly to sound sources for food reward. The angle between the 2 sound sources was varied on a session-by-session basis, and threshold (i.e., minimum resolvable angle) was taken as the angle that corresponded to a performance level of 75% correct. In all, thresholds were calculated for pure tones of 5 different frequencies, noise bands of 3 different spectral compositions, and species-specific contact or distance calls recorded from each of the 3 species. Thresholds for both simple and complex stimuli were larger than 25°. There were statistically significant species differences for each set, but these differences were not correlated with species differences in head size. Birds with 1 plugged performed as well as binaural birds in this task. Birds deafened in 1 ear, however, performed at chance.

It is well established that binaural in the barn whose interaural distance is approximately 50 vertebrates depends primarily on time and energy differences mm (Knudsen, 1980; Knudsen & Konishi, 1979; Konishi, between the . Because the available acoustic cues are 1983). Measured with the search coil technique, have constrained by head size, sound localization is an especially been shown to localize noise bursts with errors less than 2° interesting phenomenon in small birds, which have both when the sound source was within 15° of the midline (Knud- closely spaced ears and poor high frequency (Knud- sen, Blasdel, & Konishi, 1979). sen, 1980; Kuhne & Lewis, 1985; Mills, 1972). These facts Unfortunately, barn owls may not be representative of birds seem to preclude good spatial resolving power. Whereas other in general, and they may even be exceptional among preda- vertebrates, such as mammals, clearly rely on binaural inten- tory birds. Calford, Wise, and Pettigrew (1985) suggested that sity and time differences to localize , small birds lack at least three diurnal predators—the brown falcon, the swamp the required separation between the ears to create appreciable harrier, and the brown goshawk—may rely on intensity dif- binaural differences in either intensity or time. One reason ferences created by the interaural pathways to localize sound for examining sound localization in small birds, then, is to in the horizontal plane. Barn owls, by contrast, probably use test the generality of the classical theory of sound localization time differences for horizontal localization. derived from studies of sound localization in mammals (Mills, Other recent studies have examined sound localization 1972). ability in birds not obviously specialized for sound localiza- The study of sound localization in birds is interesting for tion. Jenkins and Masterton (1979) showed that pigeons could yet another reason. Recent evidence suggests that the acoustic use binaural cues to localize a sound source between 2 speak- characteristics of at least some vocal signals may be the result ers positioned 60° to the left and right of the 's midline. of selection for locatability (Brown, 1983; Erulkar, 1972; Interestingly, pigeons were able to localize both low and high Knudsen, 1980; Marler, 1955, 1959). Some species, for ex- frequencies equally well, which suggests that both interaural ample, may have evolved contact or distance calls that are time and interaural intensity cues were being used. Recently, easy for conspecifics to localize and alarm calls that may be Lewald (1987) used a heart-rate conditioning procedure to difficult for predators to localize (Marler, 1955, 1959). measure relative sound localization thresholds in homing Although behavioral studies of sound localization in birds pigeons. The pigeons showed remarkably low spatial thresh- are sparse, there have been several laboratory investigations olds for noise stimuli of only 4° in a relative sound localization of sound localization in birds that are specialized for sound task (a task that requires the to report change in localization. The most extensive research to date has been on location, not absolute location). In earlier studies, bullfinches (Schwartzkopff, 1950) and grosbeaks (Granit, 1941) were able to discriminate between This work is based in part on a dissertation submitted to the speakers separated by 20°-24° with tone stimuli. More re- University of Maryland by Thomas J. Park in partial fulfillment of cently, bobwhite quail (Gatehouse & Shelton, 1978) were the requirements for the degree of Doctor of Philosophy. This research shown to discriminate between speakers separated by 100° was supported by National Institutes of Health Grant NS-25768 and with broadband noise stimuli. But, as far as we know, there National Science Foundation Grant BNS-8405159 to Robert J. Dool- has been only one modern laboratory experiment aimed at a ing. parametric measurement of sound localization ability in a We thank the following persons for suggestions on earlier versions of this article: Steven Brauth, William Hall, William Hodos, Stewart small bird: Klump, Windt, and Curio (1986) trained great tits Hulse, Georg Klump, Arthur Popper, Kazuo Okanoya, John Ro- (Parus major) to fly to one of two perches in order to receive sowski, and two anonymous reviewers. food (an absolute localization task). Minimum audible angles Correspondence concerning this article should be addressed to of about 20° were found for white noise, a 2.0 kHz tone, and Thomas J. Park, who is now at the Department of Zoology, University three types of vocalizations: a scolding call, a mobbing call, of Texas, Austin, Texas 78712. and a song element. The vocalization most difficult to localize

125 126 THOMAS J. PARK AND ROBERT J. DOOLING was the "seeet" call. This is the call that Marler (1955) of 8 g on a perch was sufficient to trigger the switches. (The smallest predicted would be difficult for predators to localize and the bird used, the zebra finch, weighs about 13 grams.) same type of alarm call studied by Shalter (1978) and Brown Each station was elevated 60 cm above the floor of the chamber (1982). Klump et al. concluded that localization thresholds (measured from floor to perch) by a 1 cm in diameter black steel rod for the great tit could be explained in the traditional way by affixed to a black steel base. One station, the observation station, contained an additional observation perch located 5 cm in front of binaural time difference cues with the tits probably resolving the hopper opening. The perching stations were arranged so that the interaural time differences of about 18 jts. observation station faced the other two stations, the response stations, The purpose of our experiment is twofold. First, we wanted positioned 83 cm from the observation station. Each response station to extend the findings of Klump et al. (1986) to three other had a 3-in. diameter speaker mounted above the hopper opening. species of small birds (i.e., budgerigars, canaries, and zebra Figure 1 is a schematic representation of a response station. finches). These species have interear distances in the same Sound stimuli were stored on disk in digital form and output at a range as that of the great tit, and we hypothesized that they sampling rate of 20 kHz through a digital-to-analog converter, a 10 too would show relatively poor sound localization thresholds kHz low-pass filter, and a power amplifier. The two speakers were (i.e., no better than 20°). Second, we wanted to test the matched, alternated frequently over the course of this experiment, prediction that sound localization ability in birds may be and replaced once with no effect on discrimination behavior. Cali- bration was performed by measuring spectra at the observation station correlated with head size, given that larger interaural distances for noise and tones emitted from each speaker in the sound field. can theoretically provide better cues for sound localization Intensity differences among the spectra were less than 2 dB. Energy (R. S. Heffner & Heffner, 1987). at harmonics of pure tone stimuli was not measurable above back- Finally, two basic behavioral methods have been used to ground at test levels when the fundamental was 63 dB (SPL). To measure sound localization in animals, and they give slightly measure the energy at the harmonics, the intensity of the fundamental different results. One method requires the subject to detect a was increased to 90 dB. Energy at the first harmonic (first overtone) change in sound source position (relative localization). The was at least 52 dB lower than the fundamental. All experimental other method, as used in our experiment, requires the subject events were controlled by a microcomputer. to indicate the position of a sound source (absolute localiza- tion).

Method

Subjects

The subjects in this experiment were three budgerigars (Melopsit- tacus undulatus; 2 male and 1 female), two canaries (Serinus canarius; 2 male and 1 female), and three zebra finches (Poephila guttata; 2 male and 1 female). All of the birds were experimentally naive, young adults between 1 and 2 years old. These three species were selected both for the range of interaural distances they represent (i.e., for budgerigars, 15.1 mm; for canaries, 13.5 mm; and for zebra finches, 11.8 mm) and for the fact that audiograms are available for all three species (Dooling, Mulligan, & Miller, 1971; Dooling & Saunders, 1975; Hashino & Okanoya, 1989; Okanoya & Dooling, 1987). All the birds were housed in standard breeding cages with a light/ dark schedule correlated to the season. The birds were reinforced with yellow millet during experimental sessions, and they were deprived according to procedures developed in earlier experiments (e.g., Park & Dooling, 1985; Park, Okanoya, & Dooling, 1985).

Apparatus

Psychophysical testing took place in a 3 x 3 x 3 m, single-walled soundproof chamber, carpeted and lined with sound-absorbing foam. Three perching stations were located inside the chamber. Each station consisted of a standard pigeon grain feeder with light, a response perch made from a wooden dowel, and a 24-volt light to illuminate the perch. The front panel of the grain feeder was 8 cm wide x 16 cm high, and the feeder opening, centered in the front panel, was 4 cm wide x 6 cm high. The perch was attached to the arms of two microswitches that projected 2.5 cm in front of the Figure 1. A schematic representation of the response station show- hopper opening. The arms of the switches projected through the front ing the response perch (a), grain feeder opening (b), speaker (c), panel of the hopper through holes located 0.5 cm to the sides of the station light (d), food magazine (e), microswitch (f), and steel sup- hopper opening at the level of the bottom of the opening. A weight porting rod (g). SOUND LOCALIZATION IN BIRDS 127

Stimuli be functionally similar for the three species in that they occur in roughly the same behavioral context (Dooling, Park, Brown, Oka- The birds were tested with pure tones, noise bands, and bird calls. noya, & Soli, 1987; Price, 1979). All three species' calls have a The stimuli were presented at 63 dB (A SPL, fast) at the birds' head substantial amount of energy in the region of best hearing for each with intensity randomized ±2 dB for each sound presentation. Tone species, and the particular calls used as stimuli in this experiment are and noise stimuli were 200 ms long (5 ms rise/fall times), and call representative of the contact calls of each species in terms of duration, stimuli were approximately 200 ms long, a sufficient duration for spectrum, and frequency and amplitude modulation. All three calls localization even if the subjects depend on making head movements were produced by female birds. (e.g., scanning) during localization (Jenkins & Masterton, 1979; Kon- ishi, 1983). The use of pure tones helps to characterize the nature of sound Procedure localization ability and provides important data for comparison with other species. Thus, all the birds were tested with pure tones of 0.5, Figure 2 shows a schematic representation of the procedure. Before 1.0, 2.0, 4.0, and 6.0 kHz. Complex signals, on the other hand, each session the two response stations were positioned to form a generally contain a range of frequencies that provide more cues for predetermined angular separation in front of the observation station. localization than do pure tones. Noise is one example. AH things At the beginning of a session, the front of the observation station was being equal, thresholds for broadband noise probably provide the illuminated, and a bird was placed on the observation perch. When most valid estimate of the best localization possible for a given species. the bird perched on the observation station response perch, it was Testing with selected narrow bands of noise can also reveal which reinforced. A trial began when a bird perched back on the observation spectral regions provide the best cues for localization. We used three perch (facing the response stations after hopping from the response different spectral noises: a broadband noise, a low-frequency band of perch), triggering the attached microswitches. One second later, a noise low-passed at 2 kHz, and a high-frequency band of noise high- stimulus was produced randomly from one of the two response passed at 4 kHz. stations; then both response stations were illuminated, and the obser- Complex vocal signals also typically cover a range of frequencies vation station was darkened. The trial was canceled if the bird left and provide a wealth of possible cues for localization. It is especially the observation perch before the stimulus presentation was completed interesting to test an on its own species-specific calls to or if the bird did not leave the observation perch within 2 s. examine the possibility that auditory mechanisms for sound localiza- A response was recorded when the bird perched on one of the two tion and the characteristics of complex vocal signals may be closely response perches and triggered the attached microswitches. If the bird linked in some way. The call stimuli consisted of a natural contact landed at the station that produced the sound, the hopper light was or distance call from each of the three species. These calls appear to illuminated, and the food hopper was raised for 2 s. If the bird landed

Perch on Perch on Land at correct station, response observation reinforcement perch, sound perch, from one reinforcement speaker Land at Incorrect station, p=.25 p=.5 time out

Premature flight or no flight for 2 sec

OBSERVATION STATION RESPONSE STATIONS ILLUMINATED ILLUMINATED

Figure 2. A schematic representation of the behavioral test procedure. (A budgerigar is at the observation station [left] and initiates a trial by landing on the observation perch. After a stimulus presentation the bird flies to one of the two response stations [right].) 128 THOMAS J. PARK AND ROBERT J. DOOLING at the other station, all lights were extinguished for 10 s. After positive iiriiiiiirni reinforcement or lights out, the observation station was illuminated, 100 and the response stations were darkened. When the bird flew to the perch at the observation station, the hopper light was illuminated for 2 s, and with a probability of .25, the food hopper was raised for 2 s. O The next trial began after this reinforcement. §80 Each bird required approximately 3-4 weeks of training before K actual testing in this psychophysical procedure. The birds were first exposed to the apparatus with the three perching stations separated 8 70 H by only a few centimeters and with a small amount of seed available in each. The birds quickly learned to eat from the three stations. W 60 O Then sound stimuli were introduced (noise, tones, and calls), and the stations were gradually moved farther apart on subsequent sessions. To eliminate any possible position bias, correction trials were used during the initial training sessions. A correction trial followed an 40 incorrect response, and the same speaker that produced the sound on the previous trial was selected again. In subsequent testing, none of i i i i i i i i i i i i i the birds demonstrated a position bias even with angles below thresh- 30 old. 0 20 40 60 80 100 180 After training, the birds were tested in a pseudorandom order on 3-9 angles between 10° and 180° in azimuth. The number of angles tested was fewer in cases where the percentage of correct responses 1 1 I 1 1 1 1 1 1 1 1 i i remained far above chance at very small angles or far below chance 100 at very large angles. ~ BUDGERIGARS 90 /A^ Data Analysis o 4y — 6 gj 80 The psychometric function for each bird for each stimulus was y /•^ 0- obtained by plotting the percentage of correct responses as a function _ 870 of speaker location for each session. Two sessions of 50 trials were /* / ^^* obtained for each bird with each sound at each angle. Thresholds for E- w 60 - each session were determined by calculating the angle that corre- o sponded to the traditional threshold performance of 75% correct. ~ &T-^% A. 5kHz 50 +A • 1kHz Analysis of variance (ANOVA) tests with the 75% threshold from A - each session were used to compare differences among species and S A 2kHz stimuli, and because several analyses were required, an alpha level of 40 * 4kHz .01 was chosen for significance. O 6kHz Because there are several ways to calculate thresholds from a two- Qr\ i i i i i i i i i i i i i alternative choice procedure (H. E. Heffner & Heffner, 1984; Klump et al., 1986; Penner, 1978), we chose to report here complete psycho- 0 20 40 60 80 100 180 metric functions as well as the thresholds (minimum audible angles) that corresponded to a performance level of 75% correct. Data from an earlier study on great tits, to which our data are compared, defined i i i i i i i i i i i i i threshold as the angle which resulted in a performance level of 65% 100 correct. This criterion corresponds to a performance level that is ~ A. 5kHz ZEBRA FINCHES - significantly different from a chance level of 50% in a binomial • 1kHz O 6kHz distribution with a probability level of p < .01 (Klump et al., 1986). A 2kHz The average psychometric functions shown in the figures were u derived by first calculating an average individual psychometric func- Ku 8o0n _ * 4kHz ^^-4. tion for each bird (average percentage of correct responses at each K angle for the 2 sessions). Then the mean psychometric function for 8 70 each species was calculated by averaging the individual psychometric functions. Hu 60 X/X' K Control Experiments A A _

Several control experiments were conducted to confirm the use of 40 binaural mechanisms and to clarify the strategies and cues used in localization. These included temporary ear plugs, monaural deafen-

Table 1 Speaker Separation (Degrees) at 75% Correct for Pure Tones 100 - Frequency (in kHz) 90 E- 2.0 w Species 0.5 1.0 2.0 4.0 6.0 (plug) K 80 Canary 168.0 69.0 36.0 25.0 35.0 30.0 Budgerigar 90.0 71.0 55.0 49.0 45.0 62.5 8 70 Zebra finch — 180.0 88.0 71.0 — 80.0 Note. Only one animal from each species was tested with a monaural S 60 ear plug; these thresholds reflect the first two sessions after plugging. o K Noise ^ 50 • Broad Band - edges secured with cyanoacrylate ester. As an extra precaution, the A Low Pass outside of the plug and the surrounding area was covered with 1-2 40 * High Pass - mm of rubber cement. The birds with plugs were then tested at two angles with broadband noise and a 2-kHz tone at two intensity levels i i i i i i i i i i i i (i.e., 63 dB [SPL] and 43 dB [SPL]). 0 20 40 60 80 100 180 To demonstrate incontrovertibly that the birds use binaural cues, one bird from each species was monaurally deafened and then tested with broadband noise and the 2-kHz tone. Deafening was accom- plished by applying anesthetic to the canal and then sec- \ i i i i i i i i r I I 100 tioning the eardrum. The birds were held by hand for the deafening BUDGERIGARS procedure, which took approximately 2 min. The ear canal was first exposed by moving the feathers away from the external opening with a damp swab. The canal was then rinsed with lidocaine hydrochloride, o which was applied with a 1-ml syringe and then blotted away. A 24- gao gauge syringe needle with the tip bent into a hook was used to K puncture and then rip the eardrum. The section was then verified visually with an otoscope. In each case, the right eardrum received 8 70 the section. The birds showed no signs of discomfort after the proce- E- § 60 dure, and testing began 48 hr later and continued for a total of 2 Noise days. o Finally, very brief tone pips only 20 ms in duration were also used • Broad Band to assess the role of scanning movements in sound localization. The A Low Pass rationale for this manipulation was that stimulus presentation is over 40 * High Pass before a purposeful movement can be initiated (Jenkins & Masterton, 1979; Konishi, 1983). As a control for scanning movements, we tested I I I I I i i i i i i i all the birds at two angles with 20-ms bursts of broadband noise and 30 a single 20-ms burst of a 2-kHz tone. 0 20 40 60 80 100 180

Results i i i i i i i i i i i i i 100 Absolute Localization of Pure Tones ZEBRA FINCHES f~ 90 - Figure 3 shows psychometric functions at each frequency 0 for each species. The thresholds that corresponded to a per- • formance level of 75% correct are given in Table 1. The most oK 9_---'•' ^^^^* ^ " -^^~^ £ striking feature about these data are the very poor thresholds; £0_ 70 " some in fact never reached the 75% criterion. There are also t iz /^ ^* /^ large differences in thresholds among the three species. Ca- w 60 _ X""^ ^' — u w ^ naries generally have lower thresholds, whereas zebra finches K tend to have the highest thresholds. All three species perform w 50 Noise worst when tested on the 0.5 kHz tone. OH • Broad Band By a two-way ANOVA (3 stimuli; 2 canaries, 3 budgerigars, 40 K A Low Pass and 3 zebra finches; and 2 sessions each), there were signifi- 4 High Pass cant differences among species, F(2, 39) = 52.18, p < .001, fin i i i i > i i i i i > i i as well as among stimuli, F(2, 39) = 15.68, p < .001. There 0 20 40 60 80 100 130 180 was no significant interaction effect, F(4, 39) = 2.72, p = .04. There were significant differences among the stimuli for the ANGLE (DEGREES) canaries and zebra finches but not for the budgerigars. These Figure 4. Psychometric functions for birds tested on broadband and analyses were performed only on the data from the 1.0, 2.0, narrow-band noise stimuli. 130 THOMAS J. PARK AND ROBERT J. DOOLING

Table 2 two-way ANOVA, there were differences among species, F(2, Speaker Separation (Degrees) at 75% Correct for Noises 35) = 263.15, p < .001, and among stimuli, F(2, 35) = 13.41, Noise bandwidth p < .001. There was also a significant interaction effect, F(4, 35) = 11.50, p < .001. (Note that only 2 zebra finches were Broadband tested with the high- and low-pass noise bands.) Canaries and Species Broadband Low-pass High-pass (plug) budgerigars did not show significant differences in thresholds Canary 29 26 26 26 among the three noise bands, which indicates that localization Budgerigar 27 30 40 30 Zebra finch 101 180 70 cues provided by each band were equally effective. Zebra finches, on the other hand, showed lower thresholds for Note. Only one animal from each species was tested with a monaural ear plug; these thresholds reflect the first two sessions after plugging. broadband noise than either low- or high-frequency noise stimuli. Control experiments showed no effect from plugging one and 4.0 kHz tones because zebra finches failed to reach the ear or from tests with short 20-ms bursts of noise, but, as in threshold criterion at 0.5 and 6.0 kHz. the control experiments with pure tones, monaurally deafened In comparing these three species, canaries and budgerigars birds performed at chance levels even with the speakers sep- showed lowest thresholds for high-frequency tones, whereas arated by 180°. These results argue for a binaural mechanism. the zebra finches showed lowest thresholds for midfrequency tones. Canaries and budgerigars showed roughly similar thresholds for 2.0, 4.0, and 6.0 kHz tones. At each frequency Absolute Localization of Species-Specific Contact zebra finches showed higher thresholds than the other two Calls species. Clearly, the most difficult frequencies for the finches to localize are the lowest (0.5 kHz) and the highest (6.0 kHz). Figure 5 shows sonograms of the contact or distance calls None of the birds showed a deficit when tested on brief 20- used as stimuli. The canary call has a wider spectral range ms stimuli. This argues against the possibility that the birds and is characteristically whistlelike to the human ear. The were using a scanning strategy. The sound localization ability budgerigar call has energy concentrated in a relatively narrow of the birds was also not affected by plugging one ear. This frequency range of 2-4 kHz with a substantial amount of suggests that the birds were using binaural intensity cues. frequency and amplitude modulation. The zebra finch call is Finally, monaurally deafened birds performed at chance levels characterized by a distinctive harmonic structure. even at the widest angle of 180°. Taken together, these results Figure 6 shows the psychometric functions for each species indicate that the birds were probably relying on binaural time tested on calls. These data are also given in Table 3. The three cues for localizing sound. species are remarkably consistent in their ability to localize each of these calls. The canary and budgerigar thresholds are Absolute Localization of Noise Bands similar to each other, whereas the zebra finch thresholds are much higher. There are significant differences among species Figure 4 shows the psychometric functions for each species in a two-way ANOVA, F(2, 39) = 26.44, p < .001, but not tested with three noise bands. Thresholds that corresponded among stimuli, F(2,39) = 1.00, p = .37. There is no significant to 75% correct detection are given in Table 2. Budgerigars interaction effect, F(4, 39) = 1.48, p = .23. and canaries show similar thresholds for all three noise stim- The individual thresholds for each subject with each stim- uli. Thresholds for the zebra finches are much higher. By a ulus are given in Table 4.

CANARY BUDGERIGAR ZEBRA FINCH CALL CALL CALL REQUENC Y

)0 ms

Figure 5. Sonograms of contact calls from each species used as test stimuli. SOUND LOCALIZATION IN BIRDS 131

I I i i i i I i i i i i i Table 3 100 CANARIES ^ ___—=,•— Speaker Separation (Degrees) for 75% Correct for Calls Type of contact call (species) E- 9° o /^^ Species Canary Budgerigar Zebra finch W on OS °° / Canary 28 27 28 OH Budgeriar 30 30 32 o Zebra finch 56 82 57 o 70 - 2; W 60 - o Call Type Discussion OS g50 / • Canary MH These experiments measured birds' abilities to indicate the A Budgerigar location of a sound source in azimuth. The results support a 40 4 Finch general body of experimental and anecdotal evidence that or\ i i i i i i i i i i i i i small birds do not localize sound very well. None of the oU thresholds measured were below 25°. The thresholds meas- 0 20 40 60 80 100 180 ured here for the canaries and the budgerigars (adjusted for equivalent threshold criteria) correspond well with the thresh- olds measured for the great tit (Klump et al., 1986). For I 1 I 1 I 1 i i i i i i i broadband noise, for instance, the great tit showed a threshold 100 ~ BUDGERIGARS . of 20°, whereas our canaries and budgerigars showed 65% thresholds of 17° and 24°, respectively. Our zebra finches 90 A ^^^ showed much higher thresholds. These comparisons are o ^* shown in Table 5. 80 « - The hypothesis that localization ability is correlated with o / interaural distance is not supported by our results. Even u 70 /I though zebra finches, with the smallest interaural distance, E- fjj consistently showed the worst thresholds in this experiment, 52 I I w 60 canaries and great tits (with larger interaural distances than u ~ f* Call Type OS zebra finches but smaller than budgerigars) showed the best 50 * • Canary thresholds. We must conclude there is no simple relation £ A Budgerigar between head size and localization ability in these species of 40 •» Finch small birds. Measurements of sound attenuation by the heads of budg- i i i i i i i i i i i erigars, canaries, and zebra finches were made in the test 0 20 40 60 80 100 180 apparatus with calibrated microphones and 2-mm probe tubes mounted at the opening of the auditory meatus. The maxi- mum intensity differences between ipsi- and contralateral ears was less than 2 dB, below 4 kHz. Furthermore, the birds did 1 I 1 1 1 i i i i i i not show a deficit in performance when one ear was plugged 100 " ZEBRA FINCHES (Tables 1 and 2). Such results argue generally against binaural

EH 9° u / ^^^^ Table 4 u Rn K 80 /•^-^4^^^ Species 8 70 x^ A" f EH Budgerigar Canary Zebra finch •Z w 60 V/ Stimulus 1 2 3 1 2 1 2 3 OS * Call Type Tones w 50 OH 1.0 kHz 59.0 57.5 69.0 66.0 70.0 157.0 180.0 180.0 • Canary 2.0 kHz 62.0 20.0 62.0 35.5 37.0 106.5 83.0 142.0 40 A Budgerigar _ 4.0 kHz 44.0 50.0 53.0 26.0 25.5 71.0 73.0 83.0 4 Finch Noise i i i i i i i i i Broadband 27.0 29.0 27.5 25.5 38.5 88.5 75.0 116.0 Low-pass 52.5 19.0 19.0 24.5 30.0 180.0 174.0 0 20 40 60 80 100 130 180 High-pass 52.0 39.0 27.0 23.0 35.5 180.0 129.0 Calls ANGLE (DEGREES) Canary 28.0 30.0 33.0 25.0 38.0 58.0 56.5 58.0 Figure 6. Psychometric functions for birds tested on species-specific Budgerigar 35.5 26.0 22.5 23.0 36.0 83.5 75.0 180.0 contact calls. Zebra finch 30.0 32.0 32.0 25.5 34.0 44.0 79.0 80.0 132 THOMAS J. PARK AND ROBERT J. DOOLING intensity differences as a cue in localizing sound. Still, it may Table 6 be premature to completely rule out binaural intensity cues. Minimum Detectable Time Difference in Microseconds Perhaps under normal conditions, interaural sound transmis- at Minimum Audible Angle sion in conjunction with independent action of the avian Species stapedius muscles may accentuate binaural intensity differ- ences especially for complex sounds (Calford & Piddington, Stimulus Budgerigar Canary Zebra finch Great tit 1988; Coles, Lewis, Hill, Hutchings, & Gower, 1980; Counter 1.0 kHz 62.4 55.1 23.6 & Borg, 1982). 2.0 kHz 54.0 34.7 51.6 18.0 From each species' interaural distance and minimum au- 4.0 kHz 49.8 24.9 48.8 21.9 dible angle, it is also possible to calculate the maximum time Note. Data for the great tit are from Klump, Windt, and Curio (1986). Data for the pigeon and barn own are not included because difference available for localization (Kuhn, 1977). These val- of the differences in psychophysical tasks used to measure thresholds. ues are shown in Table 6 along with data for the great tit. These values are not so small as to preclude the possibility that these species of bird are relying on conventional mecha- nisms of sound localization (Klump et al., 1986). Here again, It must be mentioned that the task involved in this study though, the existence of the avian interaural pathway compli- may be different in important ways from the kind of sound cates this interpretation. Recent evidence from cochlear mi- localization problem faced by small birds in their natural crophonic recordings in a number of avian species indicates environment. It is likely, for instance, that a small bird trying that the interaural pathway can enhance interaural delay to locate a singing neighbor (or even a predator) will have the especially at low frequencies (Calford & Piddington, 1988). advantage of more than a single, brief presentation of the It may be that neural adaptations play a large role in sound neighbor's call or song. A small bird attempting to locate the localization in small birds and may compensate for the effect source of an environmental sound can also change its position of differences in head size. For example, Masterton, Thomp- relative to the sound source—a strategy not possible under son, Bechtold, and Rocards (1975) compared localization the constraints of our testing paradigm. ability and the relative size of the medial superior olive in the Finally, locating a sound source (absolute localization) can cat, hedgehog, rat, and tree shrew. They found a higher be considered a different problem from discriminating move- correlation between medial superior olive size and localization ment or change in sound source location (relative localiza- ability than between interaural distance and localization abil- tion). Both humans (Irvine, 1986) and cats (Martin & Webs- ity. Perhaps localization ability in birds is more highly corre- ter, 1987) show lower thresholds when tested in relative lated with a neural substrate such as the size of the nucleus localization tasks as compared with absolute localization laminaris (the putative avian analogue of the medial superior tasks. To our knowledge no one has yet tested a bird species olive) than with interaural distance. in both types of task. Therefore, whereas we focus this report The fact that small birds present a problem for classical on absolute localization in small birds, relative sound local- theories of sound localization has been recognized for some ization abilities remain unknown. An ecologically complete years (Granit, 1941; Schwartzkopff, 1955). Our results, along account of how well small birds can localize sound in the with those of Klump et al. (1986), provide the first compara- natural environment will probably have to await results from tive data on sound localization ability in small birds that can relative localization tests. Comparing absolute and relative be used to address this issue. The answer is that small birds localization abilities will also be useful in revealing underlying do not localize sounds well, as was predicted from their small mechanisms. interaural distance. The results are mildly surprising with regard to the locatability of vocal signals. The differences both References among and within species in the locatability of complex, vocal signals were quite small. In aggregate these results argue Brown, C. H. (1982). Ventroloquial and locatable vocalizations in against a special relation between the mechanisms of sound birds. Zeitschrift fur Tierpsychologie, 59, 338-350. localization and the acoustic characteristics of complex vocal Brown, C. H. (1983). Primate auditory localization. In R. W. 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