THE AUK A QUARTERLY JOURNAL OF ORNITHOLOGY

VOL. 100 OCTOBER1983 No. 4

PARENTAL RECOGNITIONOF OFFSPRING IN THE CLIFFSWALLOW

PHILIP K. STODDARD AND MICHAEL D. BEECHER BehaviorProgram, Department of Psychology, University of Washington, Seattle, Washington98195 USA

ABSTRACT.-We examined variation in the calls and facial patterns of Cliff (Hi- rundo pyrrhonota) chicks to test the prediction that, in in which dependent young intermingle, coloniality necessitates parent-offspring recognition and thus favors the evo- lution of highly variable "signature" traits. The calls of chicks were found to be highly distinctive: interindividual variation was significantly greater than intraindividual variation for five measured parameters. Playback experiments indicated that parents could locate their chicks by these signature calls alone. We found that chick faces were individually distinctive as well. Chick faces could be readily distinguished by human observers, although we did not test whether or not Cliff Swallow parents actually use this information. Studies of several swallow species implicate coloniality as the variable in this family that separates species with distinctive chick signatures and strong parental recognition [Cliff and Bank Swallows (Ripariariparia)] from species in which these traits are weak or absent [North- ern Rough-winged Swallows (Stelgidopteryxserripennis) and Barn Swallows ( rustica)]. Received 9 December 1982, accepted 11 April 1983.

IN most colonially breeding vertebrates with trast, show high interindividual call variability, dependent young, there is a stage at which the and parents can recognize their chicks purely newly mobile offspring intermingle while still by voice. A similar correlation between coloni- receiving direct parental care. In this context, ality and individual distinctiveness of vocaliza- we should expect the evolution of individually tions within a family of has been dem- recognizable characteristics in the young and onstrated in six species of penguins (Jouventin the ability in the adults to distinguish their 1982). young by these characteristics. Moreover, we The Cliff Swallow (Hirundo pyrrhonota), like would predict higher phenotypic variability in the Bank Swallow, is a highly colonial species. offspring and a better-developed ability of par- On typical nesting sites, such as cliff faces, ents to discriminate among offspring in such neighboring nests are often in contact, and nest colonial species than in closely related solitary densities can be as high as 50 nests/M2. Colo- species. These predictions are borne out by the nies vary in size but seldom include fewer than comparative study of the colonial Bank Swal- 25 nests, often more than 50, and occasionally low (Riparia riparia) and the solitary Northern as many as 2,000 (Bent 1942). We therefore pre- Rough-winged Swallow (Stelgidopteryxserripen- dicted extreme phenotypic variability in Cliff nis) (Hoogland and Sherman 1976; Beecher et Swallow chicks and parental discrimination of al. 1981; Beecher 1981, 1982). Rough-winged such variability. On the basis of past results Swallow chicks show little interindividual with the ecologically similar Bank Swallow, we variability in their calls, and parents fail to dis- decided to look for "signature" variation in the criminate between their own chicks and un- calls of chicks. In the first hour of observation related chicks. Bank Swallow chicks, in con- in 1981, however, we saw that chicks possess

795 The Auk 100: 795-799. October 1983 796 STODDARDAND BEECHER [Auk, Vol. 100

individual facial patterns. We therefore exam- the other (control) speaker. As the playback equip- ined facial patterns as well. ment was installed, all remaining chicks were re- moved from the nest to elicit searching behavior by the parents. METHODS To extract the chicks, a small hole was cut in the Two study sites were selected in the high desert of side of the nest. The chicks were flushed out the north-central Washington. The Washburn Island col- mouth of the nest and into a waiting bag by a gently ony consisted of about 50 active nests located on two prodding finger. The hole was then patched with T-shaped concrete support pillars of an elevated set- mud. Detailed instructions for this delicate operation tling tank, 2 m from the bank of the Columbia River. may be obtained by writing to the authors. A second colony under a bridge over Foster Creek A playback trial was begun and at least two ob- also had about 50 active nests. servers recorded approach behavior to the experi- Parents were captured at night earlier in the sea- mental and control speakers. At the termination of a son and were sexed by the extent of their brood 5-min trial, the speaker cords were interchanged at patches. Each was fitted with a unique color-band the tape player to switch the experimental and con- permutation and was breast-dyed with the same col- trol calls between the two speakers. After a silence or pattern. The dual marking greatly facilitated our of about 3 min, or as soon as the parent reappeared, recognition of the adults, both in flight and at the another trial was begun. Four such trials were con- nest, and did not seem to alter their behavior. ducted for each experimental nest. The observers were To record calls, small microphones were mudded uninformed of whether their assigned speaker was into the nest wall, barely protruding into the nest. playing the experimental or control calls on a given Parents showed no reluctance to enter nests with mi- trial. crophones, providing the cords were secured against Facial variation was examined by extracting and the concrete, but they would occasionally peck at a photographing chicks at least 18 days old from nests microphone from inside the nest and twice packed at both colonies. At least two color photographs were mud over the intruding portion. We chose Realistic taken of each chick's face using a macro lens, and a 33-1056A omni-directional, 600 ohm condenser mi- strobe if ambient light was low. The chicks were crophones because of their small size (12 mm diam- banded and replaced in their nests. Unlike Bank and eter X 22 mm long) and flat response curve over the Barn swallows, fledging-aged Cliff Swallows will critical range of 1-8 kHz. Recordings were made on generally stay in the nest when replaced after han- a Uher 4200 or 4400 Report Stereo IC recorder at 9.5 dling. Preliminary observations of color-marked birds cm/s using Scotch 176 Audio recording tape. Tapes at the Washburn Island colony showed that Cliff were scanned on a Unigon 4500 Real Time Spectrum Swallow chicks become mobile between 21 and 24 Analyzer at a tape speed of 2.4 cm/s, and hard copy days of age, when they leave the nests for increas- was produced on a Kay Sonagraph 6061E Spectrum ingly extended periods during which they improve Analyzer equipped with the 6083 Scale Magnifier. their flight capabilities and learn to forage. During Playback experiments were conducted to deter- this phase, which lasts 1-3 days, the chicks are still mine whether parents could identify their own off- fed in their nest by the parents. When they discover spring by voice alone. The playback procedure was their chicks' initial departure, the parent Cliff Swal- based on our observation that parents will search the lows search for them in the air and in other nests in colony for lost chicks (see below). Around the onset the colony, eventually finding them and leading them of chick mobility, we recorded chick signature calls back to the home nest. Parents and chicks call fre- in nests at which we had color-marked at least one quently throughout such sequences. parent. Three calls from two or three chicks in the experimental nest were transferred to one track of a RESULTS 3.5-s tape loop, spaced 1 s apart. Three calls from another nest were placed on the other track of the Chick voices.-Chick vocalizations begin to tape loop in a similar arrangement to serve as a con- acquire an individually unique pattern when trol. When possible, an experimental tape track was chicks are around 15 days of age, although the used as a control in the test. subsequent Grason-Stad- call does not become pure and consistent until ler TDH-49 earphone speakers were mounted above the chicks are between 18 and 21 days of age. the mouths of two nests, one at each end of the hor- Examples of chick signature calls are izontal pillar section, 3 m apart. Cords were secured shown in and run down to the Uher 4200 in our observation Figs. 1 and 2. The call is comprised of two si- blind. During a trial, chick calls from the nest being multaneous whistles. The non-harmonic rela- tested were broadcast from one of the two speakers tionship between the two whistles suggests that (designated the experimental speaker), and calls from they are produced by opposite sides of the 's the control nest were simultaneously played from syrinx. The call is modulated over the frequen- October 1983] Recognition in Cliff Swallows 797

Call 8 1 2

C4 A I ~ U) 0_

0.1 Sec. Fig. 1. Signature call of a Cliff Swallow chick showing the parametersevaluated. F-ratios(see text) are given after each parameterdescription. LAv= fre- quency difference between upper and lower voices (F = 41.5). fL = average frequency of the lower voice (74.0). p = period of frequency modulation (226). ?f4=frequency difference between first modulation c ~~~~/ peak and valley of the lower voice (22.4). n = number of modulation cycles (51.7).

cy range of approximately 1-6.5 kHz with a duration of approximately 100 ms (see Fig. 1). Often there are family resemblances among the signature calls of sibs. We are presently ana- lyzing sibling resemblances and are attempting Fig. 2. Two signature calls each from three un- related Cliff Swallow to disentangle genetic and imitative compo- chicks (A, B, and C). Note the intraindividualconsistency. nents by cross-fostering experiments. To evaluate the individual distinctiveness of these calls, we performed a simple analysis of out and back to the nest several times while variance on each of five parameters. This is the giving a search call. While clinging to the standard method of evaluating whether or not mouth of its nest, the parent would orient to interindividual variability is large relative to the experimental speaker. It would then fly to intraindividual variability (e.g. Cheney and a nest in the vicinity of the speaker. Parental Seyfarth 1980, Beecher et al. 1981). The param- responses to the nest underneath the experi- eters we derived are illustrated in Fig. 1 and mental speaker or the control speaker or an im- are described in its caption. These parameters mediately adjacent nest were regarded as pos- do not exhaust the potential information in itive responses and were categorized from these calls; we are undertaking a more detailed weakest to strongest: aerial speaker check (pass analysis. The present analysis is based on six within 0.3 m of, look at, or hover in front of calls each from nine unrelated chicks (each from speaker) = 1; external contact with speaker nest a different nest). For all five parameters, inter- (touch briefly, perch at nest mouth, peer in- individual variance was significantly greater side) = 2; and enter nest with speaker = 3. The than intraindividual variance; each of the results of the tests are shown in Table 1. For F-ratios was highly significant (P << 0.001; val- all response categories, the seven parents tested ues given in Fig. 1 legend). responded more strongly to the calls of their Playback experiment.-Observations at an ex- own chicks than to control calls (summed score perimental nest began when a marked parent for each parent; sign test, P < 0.01). While it is returned to feed its chicks. Upon discovery of not indicated in Table 1, all birds responded the empty nest, the parent usually flew in loops only to the experimental speaker on the first 798 STODDARDAND BEECHER [Auk, Vol. 100

TABLE 1. Number of speaker responses during play- We presented human subjects with a set of back experiments. Responses are summed across eight color photographs of the faces of 18- to four 5-min trials at each experimental nest. E = ex- 24-day-old chicks. Subjects were then given a perimental call speaker, C = control call speaker. different, randomly chosen photograph of one Ex- of those chicks to match up with a photo from Sex ternal the original eight. People made very few mis- Experi- Con- of ob- Aerial con- takes and scored significantly higher than ran- mental trol served check tact Enter dom on their matches (P < 0.001). Parent Cliff nest nest parent E:C E:C E:C Swallows probably possess discriminatory abil- A20 A4 M 2:0 5:0 ities equal to or better than humans, but this A8 All M 6:1 9:1 All A8 M 40:4 11:1 remains to be demonstrated. Bi B13 F 32:11 B9 Bi M 6:0 1:0 DISCUSSION B13 B9 M 17:6 13:0 5:2 B13 B9 F 1:0 2:0 The present study demonstrates that both the calls and faces of Cliff Swallow chicks are in- dividually distinctive. We have also shown that trial. Responses to the control speaker occurred parents use the individual distinctiveness of the only on later trials. chicks' calls to identify and locate lost chicks. On one occasion, the father from nest B9 A goal for future research will be to determine hovered twice in front of a speaker playing calls how chick facial variation is used by the par- of his chicks as a control for a different exper- ents. imental nest, despite the presence of his chicks Results of studies of parent-offspring recog- in his own nest. The father at nest A20 made nition to date have been consistent with the repeated passes at the observation blind when hypothesis that parent-offspring recognition his sequestered chicks began calling from should be well developed in colonially breed- within their holding bag inside the blind. On ing species in which young intermingle and several occasions we also saw the unmarked absent from or poorly developed in species in second parent fly from the vacant nest to the which offspring mixing rarely occurs before in- experimental speaker. These latter cases are not dependence. In the colonial Bank Swallow and included in our analysis, as we do not have Cliff Swallow, there is extensive variation in positive identifications of the unmarked birds. the signature calls of the chicks, and parents Chickfaces. -The facial patterns of Cliff Swal- can recognize their chicks by their calls alone. low chicks become distinctive around 13 days In the solitary or facultatively colonial Rough- of age, when the feathers on their chins and winged Swallow and (Hirundo foreheads break from their quills. We presume rustica), cross-fostering experiments give no that the distinctive pattern remains constant for evidence of parent-offspring recognition, and each individual beyond the duration of our ob- variation in chick calls and plumage is minimal servation period, because the pattern is made (Hoogland and Sherman 1976, Burtt 1977, up of facial contour feathers, which are re- Beecher et al. 1981, Beecher 1982, Medvin and tained at least until late summer. The quantity Beecher unpubl. obs.). These findings suggest and distribution of white feathers provides the that the large-scale intermingling of chicks that most discernible variation among chicks, but occurs in colonial swallows has favored the background coloration also varies considerably evolution of signature traits in chicks and dis- and includes black, slate, chocolate, rufous, and crimination of these traits by their parents. tan (see Frontispiece). We were surprised by the existence of two As with voices, faces show noticeable family potential modes for chick recognition in Cliff resemblances. Chicks from the same brood Swallows, as the equally colonial Bank Swal- generally have the same background color- lows show no individually distinctive plumage ation and, to a lesser extent, similar distribu- traits. Although we have not yet done the par- tions of white. The three chicks on the right allel experiment on Cliff Swallow face recog- side of the Frontispiece are siblings. The three nition, we were able to recognize different chicks on the left side are from different nests. chicks on this basis ourselves, in the field as October 1983] Recognition in Cliff Swallows 799 well as in the lab test described earlier. Thus, facial patterns. This hypothesis should be dis- we consider it likely that parents use facial pat- tinguished from hypotheses such as the first terns in some way, and we shall briefly discuss two, which propose that visual and acoustic cues the significance of dual modes of recognition. are used under different circumstances. Multiple recognition modes have not yet been demonstrated in birds, though Buckley and ACKNOWLEDGMENTS Buckley (1970, 1972) describe extensive varia- We thank the Colville Confederated Tribes for per- tion in the down coloration of Royal Tern (Ster- mission to conduct research at Washburn Island, na maxima) chicks and believe that chick calls Preston Hardison and Robert Reineke for assistance may also be used for recognition. Two or three in the field, and Jed Burtt, Preston Hardison, John modes are probably common in mammals-ol- Hoogland, and Sara Hiebert for helpful criticism of We have special thanks for Dr. Har- factory, visual, and/or auditory-although only the manuscript. old Stout and Verne Marr. The research was sup- in the case of humans and domestic sheep have ported by National Science Foundation grant BNS80- all three modes been confirmed (e.g. Porter and 23562. Moore 1981, Shallito Walser et al. 1981). We propose three explanations for why the LITERATURE CITED Cliff Swallow might need to recognize its chicks both auditorily and visually, while the ecolog- BEECHER, M. D. 1981. Development of parent-off- ically similar Bank Swallow employs only the spring recognition in birds. Pp. 45-65 in Devel- acoustic mode. opment of perception, vol. 1 (R. Aslin, J. Alberts, 1. A Cliff Swallow parent can find its strayed and M. Petersen, Eds.). New York, Academic chick at another nest by its voice. Once there, Press. . 1982. Signature systems and kin recogni- however, the parent may have difficulty dis- tion. Amer. Zool. 22: 477-490. criminating among five screaming voices in the , I. M. BEECHER, & S. HAHN. 1981. Parent- highly reverberant mud nest. Our recordings offspring recognition in Bank Swallows (Riparia indicate that signature calls degrade severely riparia):II. Development and acoustic basis. Anim. when a parent returns and all chicks are pres- Behav. 29: 95-101. ent and eager to be fed. Faces can be distin- BENT, A. C. 1942. Life histories of North American guished no matter where the chicks are sitting, flycatchers, larks, swallows, and their allies. U.S. thereby providing a distortion-free second ba- Natl. Mus. Bull. 179. sis for discrimination. Bank Swallow burrows BUCKLEY, P. A., & F. G. BUCKLEY. 1970. Color varia- are not nearly so reverberant, so this problem tion in the soft parts and down of Royal Tern chicks. Auk 87: 1-13. is not as critical for Bank Swallow parents. , & . 1972. Individual egg and chick 2. to Related the previous hypothesis, Bank recognition by adult Royal Terns (Sterna maxima Swallow burrows are acoustically isolated by maxima). Anim. Behav. 20: 457-462. the absorptive properties of the sand bank, and BURTT, E. H., JR. 1977. Some factors in the timing Bank Swallow parents are therefore generally of parent-offspring recognition in swallows. exposed only to the loud signature calls of their Anim. Behav. 25: 231-239.. own chicks. Parent Cliff Swallows are exposed CHENEY, D. L., & R. M. SEYFARTH. 1980. Vocal rec- on all sides to the calls of neighboring chicks, ognition in free-ranging Vervet monkeys. Anim. and they may inadvertently learn these calls Behav. 28: 362-367. too. Facial recognition may allow secondary HOOGLAND, J. L., & P. W. SHERMAN. 1976. Advan- and of parental discrimination of offspring from tages disadvantages Bank Swallow (Ri- paria riparia)coloniality. Ecol. Monogr. 46: 33-58. among a larger set of chicks whose calls are JOUVENTIN, P. 1982. Visual and vocal signals in pen- familiar to the parents. guins, their evolution and adaptive characters. 3. Undoubtedly there is a limit to the amount Berlin, Verlag Paul Parey. of signature information that can be carried by PORTER, R. H., & J. D. MOORE. 1981. Human kin a brief 100-ms call. Cliff Swallows may have recognition by olfactory cues. Physiol. Behav. 27: circumvented this problem by exploiting an 493-495. additional recognition mode. If this hypothesis SHALLITO WALSER, E. S., P. MAGUE, & E. WALTERS. is correct, Cliff Swallow parents' recognition of 1981. Vocal recognition of recorded lambs' voices young away from the nest should be partially by ewes of three breeds of sheep. Behaviour 78: impeded by experimental alteration of chick 260-272. FRONTISPIECE. Faces of six fledging-aged Cliff Swallows. The three on the right are from the same nest.