The Condor 104:387±394 ᭧ The Cooper Ornithological Society 2002

VOCAL DISTINCTIVENESS AND RESPONSE TO CONSPECIFIC PLAYBACK IN THE SPOTTED , A NEOTROPICAL SUBOSCINE

SUSANNE C. BARD1,4,MICHAELA HAU2,MARTIN WIKELSKI2 AND JOHN C. WINGFIELD3 1Department of Psychology, University of Washington, Box 351525, Seattle, WA 98195 2Department of and Evolutionary Biology, Princeton University, Guyot Hall 303, Princeton, NJ 08544 3Department of Zoology, University of Washington, Box 351800, Seattle, WA 98195

Abstract. We studied individual variation in song characteristics of the ( naevioides), a Neotropical suboscine, and tested for song discrimination using playback of male neighbors and strangers. Discriminant analysis of four frequency and temporal characteristics of the songs of 25 male and ®ve female Spotted revealed signi®cant differences among individuals. Each song was assigned correctly to the individual that produced it with over 70% accuracy. However, during ®eld playback, male Spotted Antbirds did not discriminate between neighbor and stranger song. Our results suggest that selection has not favored the of neighbor-stranger discrimination, perhaps because all conspeci®c intruders pose a threat. The temporal characteristics of Spotted Antbird songs differed signi®cantly between the sexes, but frequency characteristics did not. Females re- sponded signi®cantly less strongly to male playback than males, suggesting that each sex plays a distinct role in territorial defense. Key words: Hylophylax naevioides, neighbor-stranger discrimination, playback experi- ment, song, Spotted Antbird, tropical suboscine, vocal distinctiveness.

VariacioÂn Individual del Canto y Respuesta al Playback Coespecõ®co en Hylophylax naevioides, un Suboscino Neotropical Resumen. Estudiamos la variacioÂn individual de las caracterõÂsticas del canto de Hylophy- lax naevioides, un suboscino neotropical y evaluamos si esta especie responde de forma diferente al playback de individuos vecinos o desconocidos. Un anaÂlisis discriminante de cuatro caracterõÂsticas temporales y espectrales del canto de 25 machos y cinco hembras de H. naevioides revelo que existõÂan diferencias signi®cativas entre individuos. Cada canto fue asignado correctamente al individuo que lo produjo en maÂs del 70% de los casos. Sin embargo, en un experimento de playback en el campo los machos no distiguieron entre el canto de inidividuos vecinos y desconocidos. Estos resultados sugieren que la seleccioÂn no ha favorecido la evolucioÂn de la discriminacioÂn entre vecinos y desconocidos porque todos los intrusos coespecõ®cos suponen una amenaza. Las caracterõÂsticas temporales, pero no las espectrales, del canto de los H. naevioides di®rieron signi®cativamente entre ambos sexos. Las hembras respondieron signi®cativamente menos que los machos al playback con cantos de machos, lo que sugiere que cada sexo desempenÄa un papel diferente en la defensa del territorio.

INTRODUCTION inate between neighbors and strangers and be- The ability to distinguish between familiar and tween other conspeci®cs (Lambrechts and unfamiliar conspeci®cs based on vocal cues may Dhondt 1995, Stoddard 1996), this issue has not help maintain bene®cial relationships and mini- been addressed in suboscine . Further- mize costly aggressive interactions between an- more, in Neotropical suboscine species where all imals (Stoddard 1996). While it has been estab- individuals of both sexes sing a similar song, it lished that many oscine passerines can discrim- is unclear how individuals of each sex distin- guish each other and what role each sex plays in territorial interactions. Manuscript received 2 April 2001; accepted 21 Jan- Individual vocal discrimination has been dem- uary 2002. onstrated in a number of vertebrates such as 4 Present address: Science and Natural History Film- making, Montana State University, P.O. Box 174120, group-living mammals and colonial , where Bozeman, MT 59717. E-mail: [email protected] complex social relationships require ®ne percep-

[387] 388 SUSANNE C. BARD ET AL. tual abilities (Rendall et al. 1996, Sayigh et al. In order for vocal recognition or discrimina- 1998, Wanker et al. 1998, Holekamp et al. tion to be possible, song characteristics must 1999). In several social, nonpasserine birds that vary consistently between individuals. In other do not learn their vocalizations, vocal discrimi- words, interindividual variation must be high nation has also been demonstrated (Watanabe compared with intraindividual variation (Falls and Ito 1991, Lengagne et al. 2000). For in- 1982). Selection pressure for discrimination of stance, Speirs and Davis (1991) found that co- conspeci®cs could further increase interindivid- lonial AdeÂlie penguins (Pygoscelis adeliae) re- ual variability and decrease intraindividual var- spond differently to playback of neighbors, iability (Beecher 1982). We compared the songs strangers, and mates. Some territorial nonpas- of male and female Spotted Antbirds to deter- serine birds exhibit neighbor-stranger discrimi- mine if song varies consistently between indi- nation, and the ability to distinguish between fa- viduals. We also assessed what proportion of miliar neighbors and unfamiliar intruders may songs could be classi®ed to the individual that be advantageous in territorial maintenance. Ex- produced them based on a variety of song char- amples are the Blue Grouse (Dendragapus obs- acteristics, and whether the sexes differed in curus; Falls and McNicholl 1979), and the Pu- these characteristics. keko (Porphyrio porphyrio; Clapperton 1987). METHODS Suboscines are widespread in the Neotropics and many maintain stable territories and long- STUDY AREA AND SUBJECTS lasting pair bonds (Greenberg and Gradwohl Our study area was Limbo Plot, a 100-ha site 1986, Morton 1996, Morton and Derrickson along Pipeline Road in Soberania National Park, 1996). Discrimination between neighbors and in a lowland moist tropical forest near Gamboa, strangers based on vocal cues may also be im- (9Њ9ЈN, 79Њ45ЈW). Limbo Plot has a portant to territorial suboscines. marked grid system, which facilitated the accu- The Spotted Antbird (Hylophylax naevioides) rate mapping of Spotted Antbird pairs, their ter- is a strongly territorial Neotropical suboscine. ritories, and territorial boundaries. North to Spotted Antbirds are sexually dimorphic, social- south, Limbo Plot is marked every 25 m, and ly monogamous, and stay in pair bonds for many east to west every 100 m. This ®eld site is de- years (Hau et al. 1999, 2000, Wikelski et al. scribed in detail by Robinson et al. (2000). A 2000). Males and females codefend large terri- map of Spotted Antbird territories on Limbo Plot tories of approximately 4.7 ha. (Willis 1972, was kindly provided by J. J. Nesbitt. Each Spot- Robinson et al. 2000). In large and densely veg- ted Antbird at Limbo Plot was color banded for etated territories, auditory cues may provide identi®cation. more information than visual cues at a distance. RECORDING EQUIPMENT AND PROCEDURES Discrimination of the familiar songs of neigh- To obtain recordings for song analysis, we elic- bors from the unfamiliar songs of strangers ited singing behavior by playing male conspe- could be favored in this species, to decrease ag- ci®c songs on Spotted Antbird territories. Indi- gressive interactions between neighbors and to viduals were recorded in the ®eld using a Senn- aid in territorial defense. heiser MZP 816 directional microphone attached We hypothesized that like many oscines, to a Sony Professional Walkman tape recorder. Spotted Antbirds would respond more aggres- We recorded at a distance of 3±4 m until 5±50 sively to strangers than to neighbors at the reg- songs were collected for each individual. All ular territorial boundary. We tested whether songs were recorded between 18 June and 20 Spotted Antbirds can make these distinctions by August 1997. presenting both sexes with song playback of male neighbors and strangers. We also compared SONG VARIATION ANALYSIS the responses of males and females, to determine Two hundred ®fty-seven song examples from 25 whether the sexes defend their territories equal- male and ®ve female Spotted Antbirds were dig- ly. In species where both sexes sing year round, itized and analyzed using software partitioning of sex roles in territorial defense (Burt 2001). For each song example we mea- may be ef®cient (Willis 1972, Morton and Der- sured center frequency in kHz (the point half- rickson 1996, Levin 1996a). way between the highest and lowest frequency SPOTTED ANTBIRD VOCALIZATIONS 389 of the song), frequency range (difference in kHz Each male served both as a subject for play- between the highest and lowest frequency), du- back trials and as a source of a song for trials ration of the song, and song speed (number of on his neighbor. Stranger songs were recorded song syllables per sec, counting paired short and from Spotted Antbird males holding territories long elements as a single syllable). Song data at least 5 km from the study site. No individual's were recorded directly into a log ®le and con- song was used on more than one subject, to verted to SPSS 8.0 for Windows (SPSS Inc. avoid pseudoreplication (Kroodsma 1989b). 1997) for statistical analysis. We tested whether Playback trials were conducted between 6 Au- among-individual song differences exceeded gust and 12 September 1997, during the Spotted within-individual differences within each sex, Antbird breeding season in Panama (May±Oc- using one-way ANOVAs on each of the four tober, Willis 1972, Wikelski et al. 2000). Play- characteristics. We also compared male and fe- back trials were conducted at the center of each male song characteristics with ANOVAs on in- and at the border of the territory shared dividual means of the four song characteristics. with the neighbor whose song was used as the To determine whether individuals could be stimulus. Responses at both locations were re- correctly classi®ed by their song characteristics corded because some species reach maximum we conducted a discriminant function analysis. response levels when they detect intruders at the We used this analysis because if neighbor- center of their territory (Stoddard et al. 1990). stranger discrimination occurs it is probable that The response to male playback by both the male birds use a combination of song variables (Clap- subject and his mate was recorded. perton and Hayward 1987, McShane et al. Four trials were conducted on each subject's 1995). To test the generality of the classi®cation territory: one each with neighbor and stranger we estimated classi®cation error rates by cross- stimuli, at both the territorial border and the cen- validation, which generates a discriminant func- ter of the territory. Territorial boundaries were tion by withholding one observation at a time, con®rmed by luring each male as far as he and then classi®es that observation. This con- would go to the edge of his territory with con- trols for the classi®cation bias inherent in con- speci®c male song, one week before the play- structing discriminant functions with the same back trials were initiated. observations that they are subsequently used to The playback speaker was mounted on a tri- classify (Johnson and Wichern 1992). To deter- pod 0.7 m from the ground at a distance of 4 m mine which variables were most important in from the observer. Trials were conducted be- distinguishing individuals, we computed a step- tween the hours of 06:30 and 11:30 from 6 Au- wise discriminant analysis. gust 1997 to 12 September 1997. When subjects sang spontaneously before playback, we initiat- PLAYBACK PROCEDURES AND CONDITIONS ed the trial only after it had stopped singing for For the playback experiment, we selected 10 ter- 2 min. We broadcast each playback song at 70 ritories held by Spotted Antbird pairs on Limbo dB (at 5 m) every 12 sec, until the subject ¯ew Plot. We recorded songs from each male on in or vocalized. At this point, the 9-min trial those territories. All Spotted Antbirds sing only began, consisting of 1 min of silence, 1 min of one song type, and stimulus songs were selected playback (4 songs spaced at 12-sec intervals), randomly from a high-quality subset of a male's followed by 3 min of silence, 1 min of playback, total recordings. After recording, the songs were and 3 more min of silence. Neighbor and strang- digitized and band-pass ®ltered to remove insect er treatments were attempted on successive and other ambient noise using Canary 1.2.1 soft- days, weather permitting. If a did not appear ware (Cornell Bioacoustics Laboratory), with a within 15 min of playback, the trial was aborted 44 100 Hz, 16-bit sample rate. Playback tapes for that day and repeated on another day. Trials were prepared using SOUNDMAKER 1.0.3 were also aborted if a male or female from a software (Micromat Computer Systems, Wind- neighboring territory sang or approached the sor, California). Playbacks were presented using speaker. The order of neighbor and stranger a Sony TCM-59V tape recorder attached via 15 stimulus presentation was chosen randomly, and m of speaker cable to a Sony SRS-A31 6-W neighbor and stranger stimuli were encrypted on speaker. the tape box to avoid observer bias. No more 390 SUSANNE C. BARD ET AL.

TABLE 1. Correlation matrix between four Spotted Antbird song variables in a discriminant function anal- ysis.

Center Frequ- Speed frequ- ency (sylla- ency range Duration ble Song characteristic (kHz) (kHz) (sec) secϪ1) Males n ϭ 25 Speed 0.15 0.01 ±0.23 1.00 Duration ±0.09 0.19 1.00 Frequency range ±0.03 1.00 Center frequency 1.00 Females n ϭ 5 Speed ±0.14 ±0.15 ±0.29 1.00 Duration ±0.14 0.34 1.00 Frequency range ±0.19 1.00 Center frequency 1.00

were compared between males in three sets of paired t-tests: (1) neighbor vs. stranger at the territorial border, (2) neighbor vs. stranger at the territory center, and (3) mean neighbor and stranger at the border vs. the center. We compared the response of males to that of their mates for all variables except number of ¯ights. Because male and female responses had unequal variances and were not normally dis- tributed, we used Wilcoxon signed-ranks tests on the mean individual response over all four playback conditions. The proportion of males vs. females responding at all to playback was com- puted using a chi-square test. SPSS 8.0 was used for these analyses.

RESULTS SONG VARIATION FIGURE 1. Examples of the complete songs of two female and two male Spotted Antbirds recorded near For all song characteristics measured, among- Gamboa, Panama. individual song variation exceeded within-indi- vidual variation in males (F24,197 Ͼ 13.6, P Ͻ 0.001 for all four characteristics). The result was than one trial per pair of neighbors was con- similar among females (F4,26 Ͼ 8.3, P Ͻ 0.001). ducted on a given day. The songs of two females and two males illus- Response measures. During each 9-min trial, trate the frequency and temporal differences be- we recorded the following behaviors of male tween individuals and between the sexes (Fig. and female subjects: (1) number of songs, (2) 1). Within each sex, the song variables in the closest approach to speaker (m), (3) number of analysis were not strongly correlated (Table 1). aggressive calls, (4) number of ¯ights, (5) laten- Discriminant function analysis with cross-vali- cy (the time elapsed before ®rst response), and dation revealed that 73% of male Spotted - (6) whether the subject made an audible or vis- bird songs were correctly classi®ed to the indi- ible response to playback. vidual that produced them based on a linear The number of songs, closest approach, num- combination of frequency and temporal charac- 2 ber of aggressive calls, and number of ¯ights teristics (␹ 96 ϭ 1320.3, P Ͻ 0.001). The ®rst SPOTTED ANTBIRD VOCALIZATIONS 391

FIGURE 2. Mean Ϯ SE song characteristics of male and female Spotted Antbirds recorded near Gamboa, Panama. *P Ͻ 0.05, ***P Ͻ 0.001. function accounted for 62% of the variance, the second function 25%, the third function 9%, and the fourth function 4%. Each function was in- dependently signi®cant after the functions al- ready entered in the analysis were accounted for. Discriminant function analysis on females re- vealed that 94% of cross-validated song cases were correctly assigned to the individual that 2 produced them across all functions (␹ 12 ϭ 100.8, P Ͻ 0.001). A stepwise discriminant analysis revealed that the center frequency was the most important variable in differentiating male songs (F24,197 ϭ 84.8, P Ͻ 0.001). After adjusting for center fre- quency, the remaining variables, song speed, fre- quency range, and duration of the song, still con- tributed signi®cantly to individual vocal distinc- tiveness (song speed F48,392 ϭ 67.3, P Ͻ 0.001; frequency range F72,584 ϭ 44.9, P Ͻ 0.001; total duration F96,771 ϭ 32.3, P Ͻ 0.001). The sexes differed signi®cantly in the tem- poral domain of the song (Fig. 2). Females sang FIGURE 3. Response to neighbor and stranger play- shorter songs (F1,28 ϭ 30.1, P Ͻ 0.001) at a fast- back by male Spotted Antbirds at the territorial border and center (left), and a comparison of mean male and er speed than males (F1,28 ϭ 4.7, P Ͻ 0.05). In contrast, for the two frequency characteristics female responses across all treatments (right). Female responses to playback were too weak for us to record (center frequency and frequency range), means the number of ¯ights they made. Means Ϯ SE are for male and female song were not different shown. *P Ͻ 0.05. (center frequency: F1,28 ϭ 0.05, P Ͼ 0.8; fre- quency range F1,28 ϭ 2.0, P Ͼ 0.1). The duration of the song was the characteristic most different between neighbor-stranger playback or location between the sexes. However, one female did treatments on whether a male responded at all consistently sing songs within the range of (visibly or audibly) to playback during a trial 2 males for all characteristics including duration. (␹ 3 ϭ 0.9, P Ͼ 0.8). Comparing response by sex, males responded RESPONSE TO PLAYBACK signi®cantly more vigorously than females on all Male subjects did not respond more strongly to response measures (Fig. 3). Male Spotted Ant- stranger playback than to neighbor playback for birds sang ®ve times more often than females (Z any response measure (Fig. 3; all t36 Ͻ 1.5, all ϭϪ2.5, P Ͻ 0.05), females produced almost no P Ͼ 0.1). Additionally, there were no differences aggressive calls compared with a mean male re- 392 SUSANNE C. BARD ET AL. sponse of 7.2 calls per trial (Z ϭϪ2.5, P Ͻ speci®c discrimination in oscines (Beecher 0.05), and males approached an average of 6 m 1982). While there is some evidence of a posi- closer than females to the playback speaker, a tive relationship between production learning trend that was nearly signi®cant (Z ϭϪ1.9, P and perception in oscines (Pytte and Suthers ϭ 0.06). Because these tests do not take into 1999), it has been hypothesized that contextual account females that did not respond at all dur- learning preceded production learning (Janik ing the trials, they probably underestimate the and Slater 2000) in vertebrates. Janik and Slater difference between male and female response. (1997) de®ned contextual learning as the asso- Because female response to playback was so ciation of a pre-existing signal with a new con- weak, they were too far away for us to record text. Contextual learning allows to use the number of ¯ights they made. vocal cues to distinguish between conspeci®cs Males were also much more likely to make a (Janik and Slater 2000). Spotted Antbirds and visible or audible response to playback than fe- other suboscines should be capable of contextual 2 males across all treatments (␹ 1 ϭ 20.9, P Ͻ learning in a variety of social interactions, in the 0.001). Females were equally likely to respond absence of production learning. to playback at the border as at the center of the Ranging, a perceptual process that allows 2 territory (␹ 1 ϭ 0.004, P Ͼ 0.9). Females took birds to distinguish between signals based on the an average of 4 min longer to respond to play- quality or degradation of the message, may have back than their social mate, when they respond- also preceded production learning (Morton and ed at all (Z ϭϪ2.5, P Ͻ 0.05). Derrickson 1996). The (Cerco- macra tyrannina), another Neotropical subosci- DISCUSSION ne, shows perceptual discrimination on the basis Vocal discrimination is not possible unless song of song quality and environmental attenuation characteristics vary consistently among individ- (Morton and Derrickson 1996). uals (Falls 1982). Our results show that individ- If the potential for discrimination of neighbors ual Spotted Antbirds sing distinct songs. Center and strangers exists in Spotted Antbirds through frequency and speed at which the song is pro- contextual learning or ranging, why has natural duced contribute strongly to these individual dif- selection not favored its evolution? Despite ferences. However, individual differences are some similarities to the territoriality of temper- necessary but not suf®cient for neighbor-strang- ate species, many aspects of Spotted Antbird ter- er discrimination. ritoriality may differ in ways that are not fully When challenged with playback, male Spotted understood, making neighbor-stranger discrimi- Antbirds did not distinguish between neighbors nation less important. Like many tropical spe- and strangers as expected. Subjects were no cies, Spotted Antbirds must defend their terri- more aggressive to stranger playback than they tories constantly against intruders throughout the were to neighbor playback. While distinguishing year (Willis 1972, Wikelski et al. 1999, Hau et between neighbors and strangers could be ad- al. 2000). They also have larger territories to de- vantageous to Spotted Antbirds in territorial in- fend than many temperate species (Willis 1972, teractions, this behavior has not been selected. Robinson et al. 2000). Tropical birds also tend Song learning for production is considered to sing less often on territory than temperate ubiquitous in the oscine passerines (Nottebohm species (Morton 1996). It is possible, then, that 1972, Kroodsma 1982). In contrast, suboscine every singing intruder is seen as a potential passerines probably do not learn their songs threat, whether familiar or unfamiliar, and treat- (Kroodsma 1989a, Brenowitz 1991). Suboscine ed with equal aggression. Eastern Phoebes (Sayornis phoebe) that were The differences in song structure and play- deafened developed normal song in the absence back responses between males and females in of auditory feedback (Kroodsma and Konishi this study have implications for the role each sex 1991). No neural regions similar to the song sys- plays in territorial interactions. Male Spotted tem of oscines have been observed in suboscines Antbird songs are longer and slower than those (Brenowitz 1997). Oscines exhibit more song of females. These differences may facilitate the variation between individuals than suboscines, a recognition of the sex of intruders during terri- likely result of production learning (Kroodsma torial defense and help identify potential mates. 1982). High song variation may facilitate con- Willis (1972) observed that male Spotted Ant- SPOTTED ANTBIRD VOCALIZATIONS 393 birds are more active in general territorial de- for the use of the ®eld site and logistical support. This fense than females. In our study, the lower re- study was funded by an NSF grant to JCW. sponse to male playback by females in compar- LITERATURE CITED ison to males suggests that males are more re- sponsible for defense against other intruding BEECHER, M. D. 1982. Signature systems and kin rec- ognition. American Zoologist 22:477±490. males. It is also possible that females in our BRENOWITZ, E. A. 1991. Evolution of the vocal control study did not respond to male playback at all, system in the avian brain. Seminars in the Neu- but rather followed their mates as they became rosciences 3:399±407. agitated over playback. However, females could BRENOWITZ, E. A. 1997. Comparative approaches to the avian song system. Journal of Neurobiology play an important role in defense against other 33:517±531. intruding females. Recent playback and decoy BURT,J.M.[ONLINE]. 2001. Syrinx-PC, version 2.0., experiments (MH, pers. obs.) suggest that while ͗www.syrinxpc.com͘ (18 February 2001). female Spotted Antbirds respond less strongly to CLAPPERTON, B. K. 1987. Individual recognition by male playback with a live decoy than males do, voice in the Pukeko, Porphyrio porphyrio mela- notus (Aves: Rallidae). New Zealand Journal of females typically respond more aggressively Zoology 14:11±18. than males to female playback with a decoy. CLAPPERTON, B. K., AND T. L. HAYWARD. 1987. Indi- Several empirical studies of other spe- viduality in contact calls of the Pukeko (Aves: Ra- cies show similar sex-role differences in terri- llidae). New Zealand Journal of Zoology 14:19± 28. torial interactions. In Bay (Thryothorus FALLS, J. B. 1982. Individual recognition by sounds in nigricapillus), females respond much more ag- birds, p. 237±278. In D. E. Kroodsma and E. H. gressively to female playback than to male play- Miller [EDS.], Acoustic communication in birds. back, and vice-versa for males, and females use Academic Press, New York. FALLS,J.B.,AND M. K. MCNICHOLL. 1979. Neighbor- their songs to deter other females from intruding stranger discrimination by song in male Blue on their territories (Levin 1996a, 1996b). Win- Grouse. Canadian Journal of Zoology 57:457± tering female Stonechats (Saxicola torquata) are 462. also more aggressive toward other females than GREENBERG, R., AND J. GRADWOHL. 1986. Stable terri- to males (Gwinner et al. 1994). Similarly, in tories and constant densities in tropical forest in- sectivorous birds. Oecologia 69:618±625. Dusky Antbirds, males respond more aggres- GWINNER, E., T. ROEDL, AND H. SCHWABL. 1994. Pair sively to male playback and females respond territoriality of wintering Stonechats: behavior, more aggressively to female playback (Morton function, and hormones. Behavioral Ecology and and Derrickson 1996). Sociobiology 34:321±327. HAU, M., M. WIKELSKI,K.K.SOMA, AND J. C. WING- Additional ®eld and laboratory experiments FIELD. 2000. Testosterone and year-round territo- should be conducted to further test for conspe- rial aggression in a tropical bird. General and ci®c discrimination in Spotted Antbirds and oth- Comparative Endocrinology 117:20±33. er suboscines. In addition to testing for neigh- HAU, M., M. WIKELSKI, AND J. C. WINGFIELD. 1999. Environmental control of reproduction in Neo- bor-stranger discrimination, experiments should tropical birds. 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