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Recognition of group membership by voice in Mexican jays, Aphelocoma ultramarina
ANIMAL BEHAVIOUR, 2001, 62, 297–303 doi:10.1006/anbe.2001.1745, available online at http://www.idealibrary.com on
Recognition of group membership by voice in Mexican jays, Aphelocoma ultramarina STEVEN L. HOPP*, PIOTR JABLONSKI† & JERRAM L. BROWN‡
*Department of Ecology and Evolutionary Biology, University of Arizona, and Arizona-Sonora Desert Museum, Tucson †Department of Neurobiology, University of Arizona and Institute of Ecology and Polish Academy of Sciences ‡Department of Biological Sciences, State University of New York, Albany (Received 3 February 2000; initial acceptance 18 May 2000; final acceptance 2 January 2001; MS. number: A8708R)
Mexican jays live in stable social groups of 5–25 individuals. Groups show complex social organization, with dominance hierarchies and defence of territories against nonmembers. We tested whether Mexican jays displayed vocal recognition of group membership in a population of colour-banded birds in southeastern Arizona, U.S.A. We conducted playback trials of primary calls recorded either from an identified member of the target group or from a member of a nearby but noncontiguous group. Calls were played near established feeding stations during regular feeding sessions. The jays responded differently to calls from outsiders and insiders, with more calling, faster approach latency and more entries into a response circle (i.e. within 5 m of the speaker) in response to calls from outsiders. Thus, the primary calls of jays are used to recognize group membership. Mechanisms by which this recognition is mediated are discussed.
(Stoddard 1996). Less work has focused on vocal recognition within complex social groups or assembly flocks. Several lines of study have concentrated on birds’ abilities to recognize individuals of particular relationships within these larger social groups. These include sibling, mate and parent–offspring recognition (Beecher & Beecher 1983; reviews in Beecher 1991; Jouventin et al. 1999; Palestis & Burger 1999). Fewer studies have assessed the generalized abilities of members in free-ranging social groups to distinguish among individuals within the group, or to distinguish group members from outsiders. Several highly social species show a structural convergence of vocal signals within a group, including both songs and calls: blackcapped chickadees, Poecile atricapilla (Mammen & Nowicki 1981), American crows, Corvus brachyrhynchos and Australian magpies, Gymnorhina tibicen (Brown et al. 1985; Brown 1985; Farabaugh et al. 1988; Brown & Farabaugh 1992), yellow-rumped cacique, Cacicus cela (Feekes 1982), bobwhite quail, Colinus virginianus (Bailey & Baker 1982) and yellow-naped Amazons, Amazona auropalliata (Wright 1996). Such vocal convergence probably serves to convey flock or group membership, and could facilitate group assembly, affiliation or recognition. Structural variation among calls of pinyon jays, Gymnorhinus cyanocephalus, suggests that their acoustic signals could be used for recognition of individuals within
Animals living in stable social groups often possess a varied repertoire of acoustic signals. As these acoustic systems are more carefully studied, a growing sense of the sophistication of vocal recognition abilities emerges. One of these abilities, the recognition of group membership, has been demonstrated in a variety of species, including bats (Boughman & Wilkinson 1998; Wilkinson & Boughman 1998), marine mammals (Strager 1995; Weilgart & Whitehead 1997), birds (Nowicki 1983; Price 1999) and primates (Marler & Mitani 1988; Houser 1996). Group membership coupled with other categories of recognition, such as individuals, mates, relatives, age categories and dominance status, could allow social groups to facilitate behavioural interactions both within and between groups. Among birds, research on avian vocal communication has resulted in a growing understanding of their vocal recognition abilities. Many studies of songbirds in a territorial context have elucidated the range and extent of vocal recognition of neighbours and non-neighbours Correspondence: S. L. Hopp, Department of Ecology and Evolutionary Biology, Biosciences West, University of Arizona, Tucson, AZ 85721, U.S.A. (email: [email protected]). P. Jablonski is at the Department of Neurobiology, University of Arizona, Tucson, AZ 85721, U.S.A. J. L. Brown is at the Department of Biological Sciences, State University of New York, Albany, NY 12222, U.S.A. 0003–3472/01/080297+07 $35.00/0
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groups (Berger & Ligon 1977). Laboratory studies on calls of budgerigars (Melopsittacus undulatus) have shown structural similarities at both the individual and group level, suggesting that these birds could use their calls for recognition of both individual birds and group membership (Brown et al. 1988). Although suggestive, few studies have definitively demonstrated that individuals use these differences in vocal signals to discriminate between group members and individuals from outside the group. Two lines of research, however, have convincingly shown vocal recognition of group membership by vocal signals. Price (1999) has shown that stripe-backed wrens, Campylorhynchus nuchalis, use stereotyped calls to distinguish members of a particular patriline. These calls are learned from older male relatives, and are often, but not exclusively, shared by members within a social and family group. These birds failed to show discrimination when a member of another group shared the same patrilineal calls as their own. In an exemplary series of studies, Nowicki and his colleagues have demonstrated that black-capped chickadees use their calls to recognize group membership. The chickadees have both individual- and flock-specific components of their calls (Mammen & Nowicki 1981). In playback trials, these calls were shown to provide a basis for recognition of group membership (Nowicki 1983). The acoustic similarities within groups result from an apparent convergence of structural components of individual calls over a relatively short period (Nowicki 1989). This gives chickadees a hierarchical system for reacting appropriately and differentially to conspecific calls, depending on social circumstances (Nowicki 1989). Taken together, these studies contribute to an emerging sense that birds in complex social groups possess vocal characteristics allowing subtle distinctions among various recognition categories. One such socially living species is the Mexican jay, which is widely distributed in the middle elevations of central to northern Mexico, and into the mountainous regions of Arizona, New Mexico and Texas, U.S.A. (Brown 1994). These birds live in groups up to 25 individuals, comprised of related and unrelated members of varied ages. Members within these groups commonly coexist for several years. They show dominance hierarchies within a group, engage in nest helping, inhabit stable territories and staunchly defend territory boundaries from individuals of outside groups. These jays also easily learn the relationship between particular auditory stimuli and feeding events, and retain this information over many months (Brown 1997). Their complex system would probably only function efficiently with concomitant complexity of recognition abilities, either by visual or auditory cues. As an initial attempt to examine the range and extent of vocal recognition in this species, we studied whether members of Mexican jay groups were able to distinguish group members from nonmembers. To test this, we conducted playback trials of primary calls produced either by a member of the group or by a nongroup member from a noncontiguous but local group.
METHODS
Study Area The study was conducted in the area in and around the Southwestern Research Station of the American Museum of Natural History, located in the Chiricahua Mountains in the southeastern corner of Arizona. The habitat around the research station is mostly relatively open mixed woodlands of pine (Pinus), live oak (Quercus) and junipers (Juniperus), and more deciduous communities of Arizona sycamore, Platanus wrighti, and Freemont cottonwood, Populus fremontii, along the riparian corridors. The Mexican jays in the vicinity of the research station have been under constant study as a colour-banded population since 1969. Group composition is monitored frequently, and newcomers are banded.
Subjects For our study in 1999, the population consisted of 70 individual Mexican jays in 11 groups, with group size ranging from five to 12 individuals. Of these, all but five individuals were uniquely colour banded. Details of this study population can be found in Brown & Brown (1990) and Brown (1994). On one trial our equipment malfunctioned, giving an irregular stimulus presentation on that trial, so we discarded the data from that group for both conditions, giving an effective sample of 10 groups. To facilitate monitoring of the jay population near the field station, Brown (1997) initiated a procedure wherein the jays were provisioned within their territories, accompanied by an auditory stimulus that attracted them to established feeding/trapping stations. This procedure has the effect of summoning a group to a particular location within the territory on demand, and greatly expedites the monitoring of group composition, checking individuals’ bands, and occasionally capturing unbanded group members (Brown 1997). In provisioning sessions, food items (peanuts or bread) are placed in permanently present open wire-mesh cages at established locations within a territory; these are used for capture when necessary. The assembly stimulus (police whistle) is then used to alert the group to the presence of food. Generally, the group quickly approaches to within a few metres in the area around the feeding station. Individuals then take turns visiting the station, usually taking food items for consumption or caching within the vicinity. We took advantage of these group provisioning assemblies and the birds’ habituation to observers both to tape-record individuals for use as stimuli, and to position groups for playback trials. All feeding stations are located well within the territory boundaries of each group; provisioning signals or playbacks in the present study never elicited responses from neighbouring groups.
Sound Stimuli During provisioning sessions we recorded primary calls from each group. Primary calls are probably the most frequently used, and they can be given in a variety of
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Time (s) Figure 1. Spectrograms (bottom) and corresponding amplitude contours (waveforms; top) of five primary calls given by Mexican jays, showing variation across individuals. The first two are from individuals within the same social group, while the following three were taken from three other groups. The timing between calls is artificial; the signals were edited in sequence for this figure.
contexts (Brown 1994). Figure 1 shows amplitude waveforms (top) and spectrograms (bottom) of five primary calls from five different individuals. The first two calls are from individuals within the same group; the following three were taken from separate groups. Primary calls are relatively brief, somewhat harsh sounding, and typically of ascending frequency sweeps. These calls are often produced in response to disruption to the setting, such as a conspecific intruder, predators, or even humans. These calls are effective in eliciting a territorial response by the jays, and playbacks of the calls have been used to induce approach for the purpose of monitoring groups (Brown & Brown 1985; Brown & Horvath 1989). Members of the group often exchange bouts of primary calls in a conversational manner during group movements. A careful analysis of primary calls in Mexican jays has not been done, and the extent of similarity within or between groups is not known. Typically, during the feeding sessions the jays engage in calling at initially high levels, then taper off to more sporadic bursts while feeding. Primary calls as labelled in this paper are equivalent to those termed ‘loud call notes’ by Brown (1997). In recording sessions, calls were recorded by one individual, while two observers kept track of individual
identity. We used a Sony TCM5000 cassette recorder, and a Sennheiser microphone (ME20/K3U or ME62/K6) held in a 36 cm parabolic reflector (Sony PBR330). Calls were recorded opportunistically, and notes on individual identities were narrated onto the tape immediately following what were judged to be potentially usable bouts of calling. We later digitized the stimuli using Signal software (Beeman 1996) with a sampling rate of 32 kHz, then filtered some to remove extraneous noise. We selected one naturally occurring bout of three to five primary calls given by one identified individual from each group on the basis of recording clarity, without regard for age, sex, or dominance status of the calling individual. We then recorded these call bursts onto playback tapes (one tape for each group), with one natural call sequence presented during an 8-s stimulus interval (repeat cycles from onset to onset). Each trial lasted 120 s, or 15 stimulus cycles.
Trial Procedure For each of the groups we preselected an appropriate location for the playback speaker in a response circle consisting of a relatively isolated natural copse of vegetation. For all groups we were able to find naturally
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isolated vegetation clusters, eliminating the need to tag response circle boundaries. These locations were about 10 m in diameter and approximately 25 m away from the feeding station, separated by a relatively open area. For each trial, we positioned the playback speaker, a wireless amplified speaker custom-made by Mineroff Electronics, about 2 m off the ground near the centre of the response circle, facing the feeding station. We then situated ourselves such that we could easily observe the feeding area and designated response circle. Once positioned, we summoned the group to the feeding station with the police whistle. We waited until the group was actively feeding and had settled from their approach to the station. We then initiated playback of the appropriate stimulus tape, either the within-group call or a prechosen betweengroup stimulus, and two observers independently recorded behavioural indices. Observational measures included the latency for the first entry into the response circle by any individual, and the total number of entries into the response circle during each 8-s stimulus interval. We also tape-recorded each session and later digitized these recordings. From these we counted the total number of antiphonal calls given during the first 16 s (two stimulus intervals) of each trial. Each tape was used in two trials, once as the appropriate within-group (own) playback, and once as a between-group stimulus, preselected such that the between-group tape was from a nonadjacent group, and with no reciprocal pairings of groups. Thus, the stimulus set used for the playbacks was identical for the withinand between-group trials, assuring that other potential factors such as sex, age or dominance of the calling animal were the same for the two conditions. We conducted playbacks over 2 days beginning in early morning, with the ordering of groups the same both days. We also predetermined the presentation condition for each group such that roughly equal numbers of between-group and within-group trials were conducted each day. We conducted the study outside the breeding season in mid-February 1999 to avoid potential influences of nesting activities. As groups were paired to themselves, in analyses we used within-group comparisons for appropriate statistical tests. Because the trials mimicked the vocal component of a territorial intrusion (Brown & Brown 1985; Brown & Horvath 1989), we predicted greater calling, more response circle entries, and more rapid initial entry into the response circle for the between-group trials. However, to allow for the possibility that responses might occur in the opposite direction as predicted, we employed directed tests, which use asymmetrical rejection regions favouring the predicted response direction (Rice & Gaines 1994). If the variables were non-normally distributed we used a nonparametric test (latency measure). We adjusted the significance levels for each test taking into account the three comparisons being made (sequential Bonferroni method: Rice 1989; Zar 1999). In addition, we calculated an overall probability for the unadjusted P values using a Fisher’s combined test, which gives a probability of obtaining the three probabilities as a set (Wolf 1986).
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Stimulus condition Figure 2. Latency for the first group member to enter the response circle. Box plots show the second and third quartile, with the median designated by the horizontal line within each box. The extended bars designate the 10–90% range, and the outlying filled circles show the fifth and 95th percentile points.
RESULTS The median latency to enter the response circle by a group member was much shorter (faster approach) in response to the between-group stimulus than to the within-group stimulus (Wilcoxon matched-pairs signed-ranks test: T=2.24, N=10 pairs, Pcalculated =0.016, Padjusted =0.031) (Fig. 2). Note that the fastest response was actually seen for a within-group playback trial, for which the variability of response was large. The average number of entries into the response circle during the entire 2-min playback trial was greater for the between-group trials (paired t test: t9 =2.72, Pcalculated =0.015, Padjusted =0.044), during which the jays made nearly four times as many entries as during the within-group trials (Fig. 3). Figure 4 shows the average number of antiphonal primary calls given in response to the playback stimulus during the first two 8-s stimulus intervals combined. The average number of calls given was significantly greater in response to the between-group stimulus (paired t test: t9 =2.52, Pcalculated =0.021, Padjusted =0.021). The Fisher’s combined test was significant (26 =25.50, P<0.001), indicating the probability of obtaining these three results as a set by chance. DISCUSSION By all three measures used, Mexican jay groups responded more strongly to playbacks of primary calls from outside their group than to calls from within their group. This response differential was seen in both approach measures and in the immediate antiphonal calling by the groups. Since the stimuli used in the two conditions were
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identical, differential effects due to age, sex, dominance or other subject characteristics of the caller can be eliminated as possible sources of the observed response differences. Instead, the response pattern must be due to some component of group membership. Presumably, this response results from the first step in a territorial encounter, with the approach component perhaps reflecting the beginning of an attempt to dislocate the intruder. In playbacks given to groups, an interpretation of the results must be made carefully, as responses may be influenced by different elements of group dynamics (Hopp & Morton 1998). Because members respond to one another as well as to the playback stimulus, attributing
response differences to particular members or categories of members is not possible. Factors including social facilitation and inhibition, and audience or recruitment effects, may play a role in mediating the differences observed using this type of design. Despite such caveats, we nevertheless have definitively shown that the response seen by the group as a whole is greater to an outsider than to an insider. How this response is mediated in Mexican jays, and whether the observed response results from internal social dynamics or a summation of individual responses cannot be definitively ascertained. Several possible mechanisms may facilitate this difference in group responsivity, either by themselves or in combination. First, it may be that individuals within a group develop some common characteristics in the acoustics of their calls, as has been seen in several other species (see examples in Farabaugh & Dooling 1996, and those given in the Introduction). Such vocal convergence would give the primary calls a group-signature function with common acoustic features serving to directly encode group recognition. Members would then respond more strongly to calls not carrying these shared features. This explanation would predict a greater acoustic similarity for calls recorded within a given group than a comparable set of calls from between groups. A second possibility is that the jays simply recognize each individual member of their own group. Presentation of an outside call would result in the observed response differential because each individual of the group independently recognizes the call as an unfamiliar individual. This explanation would predict a measurable degree of intra-individual similarity of calls, and a concomitant ability to distinguish statistically among individuals on the basis of measurable call features. Third, it may be that within a group each bird simply becomes familiar with the calls given by other group members as a result of stimulus habituation, with categories of familiar (within-group) and unfamiliar (outside-group) calls, but without a distinction made between individuals on the basis of their calls. Calls presented from an outside member would then invoke a greater response as an unfamiliar call, rather than as an exemplar of some particular social category. Fourth, it is possible that responses to outsiders result from a behavioural ‘division of labour’, wherein one or a small number of individuals within the group monitor intrusions, and the alerting reactions of these individuals then trigger a mob response by the group. However, under this scenario we are still left with the question of how the monitors recognize an intruder by vocal characteristics, and we return to the above three explanations. The character of the group responses to playback can be used to examine the viability of each of these explanatory hypotheses. If our observed group response results exclusively from either individual recognition or from familiarity/habituation, we would expect that on the within-group trials, the individual whose call we used for the trial would be the only individual responding to the playback stimulus. Under both explanations, this bird would presumably be the only member of the group
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to consider the playback stimulus to be an outside individual, or an unfamiliar signal, respectively. Although on a few trials we observed only one member to enter the response circle, this occurred during both within- and between-group trials. For most trials more than one individual entered the response circle, even on within-group trials. Because of the difficulty of tracking individuals during trials we cannot address whether the first bird to enter the response circle during within-group trials was more likely to be the individual from which we recorded the playback stimulus. However, the behavioural patterns observed suggest that the response is not based on individual recognition alone. The fourth explanation, the group-monitor hypothesis, would predict that the first individual to enter the response circle would be consistent across the two conditions. For trials where we were able to record this information, this was not the case. Under this explanation we would also expect a typical response scenario to consist of a leader–follower format, where one individual appeared to initiate the response, followed by recruitment of other group members. This pattern was also not what we observed. Rather, we usually observed small subsets of the group react almost simultaneously. The overall pattern of response seen was not uniform enough to favour conclusively any of these explanations. Instead, the response seen may result from a combination of these, perhaps even with differing response tendencies influencing different members of the group. For example, it is possible that while the actual recognition abilities are uniform across individuals, other social mechanisms, such as dominance status, influence an individual’s willingness to respond. Our study demonstrates that Mexican jays are able to recognize group members from nonmembers. How this ability is mediated is unclear, and appears not to be simple. Further studies with this species should focus on the characteristics of the signals, particularly to determine whether reliable differences between groups might occur, and on responses to playbacks by individual members of a group.
Acknowledgments We thank Wade and Emily Sherbrooke for hosting us at the American Museum of Natural History Southwestern Research Station. John McCormack helped during recording sessions. We acknowledge financial support from the Maria Sklodowska Joint Fund II (grant PAN/EPA-96-241) and the Kosciuszko Foundation, from the Center for Polish Culture in New York, U.S.A. We are grateful to the National Science Foundation and National Institute of Mental Health for financial support of the ongoing studies of Mexican jays from 1969 to 1999. Computer equipment bought from funds in the grant KBN-6 PO4F 030 08 was used in preparation of the manuscript. All procedures complied with federal and local laws and Guidelines for the Use of Animals in Research. The research presented here was evaluated and approved by the Animal Behavior Society’s Animal Care Committee on 2 January 2001.
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Recognition of group membership by voice in Mexican jays, Aphelocoma ultramarina STEVEN L. HOPP*, PIOTR JABLONSKI† & JERRAM L. BROWN‡
*Department of Ecology and Evolutionary Biology, University of Arizona, and Arizona-Sonora Desert Museum, Tucson †Department of Neurobiology, University of Arizona and Institute of Ecology and Polish Academy of Sciences ‡Department of Biological Sciences, State University of New York, Albany (Received 3 February 2000; initial acceptance 18 May 2000; final acceptance 2 January 2001; MS. number: A8708R)
Mexican jays live in stable social groups of 5–25 individuals. Groups show complex social organization, with dominance hierarchies and defence of territories against nonmembers. We tested whether Mexican jays displayed vocal recognition of group membership in a population of colour-banded birds in southeastern Arizona, U.S.A. We conducted playback trials of primary calls recorded either from an identified member of the target group or from a member of a nearby but noncontiguous group. Calls were played near established feeding stations during regular feeding sessions. The jays responded differently to calls from outsiders and insiders, with more calling, faster approach latency and more entries into a response circle (i.e. within 5 m of the speaker) in response to calls from outsiders. Thus, the primary calls of jays are used to recognize group membership. Mechanisms by which this recognition is mediated are discussed.
(Stoddard 1996). Less work has focused on vocal recognition within complex social groups or assembly flocks. Several lines of study have concentrated on birds’ abilities to recognize individuals of particular relationships within these larger social groups. These include sibling, mate and parent–offspring recognition (Beecher & Beecher 1983; reviews in Beecher 1991; Jouventin et al. 1999; Palestis & Burger 1999). Fewer studies have assessed the generalized abilities of members in free-ranging social groups to distinguish among individuals within the group, or to distinguish group members from outsiders. Several highly social species show a structural convergence of vocal signals within a group, including both songs and calls: blackcapped chickadees, Poecile atricapilla (Mammen & Nowicki 1981), American crows, Corvus brachyrhynchos and Australian magpies, Gymnorhina tibicen (Brown et al. 1985; Brown 1985; Farabaugh et al. 1988; Brown & Farabaugh 1992), yellow-rumped cacique, Cacicus cela (Feekes 1982), bobwhite quail, Colinus virginianus (Bailey & Baker 1982) and yellow-naped Amazons, Amazona auropalliata (Wright 1996). Such vocal convergence probably serves to convey flock or group membership, and could facilitate group assembly, affiliation or recognition. Structural variation among calls of pinyon jays, Gymnorhinus cyanocephalus, suggests that their acoustic signals could be used for recognition of individuals within
Animals living in stable social groups often possess a varied repertoire of acoustic signals. As these acoustic systems are more carefully studied, a growing sense of the sophistication of vocal recognition abilities emerges. One of these abilities, the recognition of group membership, has been demonstrated in a variety of species, including bats (Boughman & Wilkinson 1998; Wilkinson & Boughman 1998), marine mammals (Strager 1995; Weilgart & Whitehead 1997), birds (Nowicki 1983; Price 1999) and primates (Marler & Mitani 1988; Houser 1996). Group membership coupled with other categories of recognition, such as individuals, mates, relatives, age categories and dominance status, could allow social groups to facilitate behavioural interactions both within and between groups. Among birds, research on avian vocal communication has resulted in a growing understanding of their vocal recognition abilities. Many studies of songbirds in a territorial context have elucidated the range and extent of vocal recognition of neighbours and non-neighbours Correspondence: S. L. Hopp, Department of Ecology and Evolutionary Biology, Biosciences West, University of Arizona, Tucson, AZ 85721, U.S.A. (email: [email protected]). P. Jablonski is at the Department of Neurobiology, University of Arizona, Tucson, AZ 85721, U.S.A. J. L. Brown is at the Department of Biological Sciences, State University of New York, Albany, NY 12222, U.S.A. 0003–3472/01/080297+07 $35.00/0
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groups (Berger & Ligon 1977). Laboratory studies on calls of budgerigars (Melopsittacus undulatus) have shown structural similarities at both the individual and group level, suggesting that these birds could use their calls for recognition of both individual birds and group membership (Brown et al. 1988). Although suggestive, few studies have definitively demonstrated that individuals use these differences in vocal signals to discriminate between group members and individuals from outside the group. Two lines of research, however, have convincingly shown vocal recognition of group membership by vocal signals. Price (1999) has shown that stripe-backed wrens, Campylorhynchus nuchalis, use stereotyped calls to distinguish members of a particular patriline. These calls are learned from older male relatives, and are often, but not exclusively, shared by members within a social and family group. These birds failed to show discrimination when a member of another group shared the same patrilineal calls as their own. In an exemplary series of studies, Nowicki and his colleagues have demonstrated that black-capped chickadees use their calls to recognize group membership. The chickadees have both individual- and flock-specific components of their calls (Mammen & Nowicki 1981). In playback trials, these calls were shown to provide a basis for recognition of group membership (Nowicki 1983). The acoustic similarities within groups result from an apparent convergence of structural components of individual calls over a relatively short period (Nowicki 1989). This gives chickadees a hierarchical system for reacting appropriately and differentially to conspecific calls, depending on social circumstances (Nowicki 1989). Taken together, these studies contribute to an emerging sense that birds in complex social groups possess vocal characteristics allowing subtle distinctions among various recognition categories. One such socially living species is the Mexican jay, which is widely distributed in the middle elevations of central to northern Mexico, and into the mountainous regions of Arizona, New Mexico and Texas, U.S.A. (Brown 1994). These birds live in groups up to 25 individuals, comprised of related and unrelated members of varied ages. Members within these groups commonly coexist for several years. They show dominance hierarchies within a group, engage in nest helping, inhabit stable territories and staunchly defend territory boundaries from individuals of outside groups. These jays also easily learn the relationship between particular auditory stimuli and feeding events, and retain this information over many months (Brown 1997). Their complex system would probably only function efficiently with concomitant complexity of recognition abilities, either by visual or auditory cues. As an initial attempt to examine the range and extent of vocal recognition in this species, we studied whether members of Mexican jay groups were able to distinguish group members from nonmembers. To test this, we conducted playback trials of primary calls produced either by a member of the group or by a nongroup member from a noncontiguous but local group.
METHODS
Study Area The study was conducted in the area in and around the Southwestern Research Station of the American Museum of Natural History, located in the Chiricahua Mountains in the southeastern corner of Arizona. The habitat around the research station is mostly relatively open mixed woodlands of pine (Pinus), live oak (Quercus) and junipers (Juniperus), and more deciduous communities of Arizona sycamore, Platanus wrighti, and Freemont cottonwood, Populus fremontii, along the riparian corridors. The Mexican jays in the vicinity of the research station have been under constant study as a colour-banded population since 1969. Group composition is monitored frequently, and newcomers are banded.
Subjects For our study in 1999, the population consisted of 70 individual Mexican jays in 11 groups, with group size ranging from five to 12 individuals. Of these, all but five individuals were uniquely colour banded. Details of this study population can be found in Brown & Brown (1990) and Brown (1994). On one trial our equipment malfunctioned, giving an irregular stimulus presentation on that trial, so we discarded the data from that group for both conditions, giving an effective sample of 10 groups. To facilitate monitoring of the jay population near the field station, Brown (1997) initiated a procedure wherein the jays were provisioned within their territories, accompanied by an auditory stimulus that attracted them to established feeding/trapping stations. This procedure has the effect of summoning a group to a particular location within the territory on demand, and greatly expedites the monitoring of group composition, checking individuals’ bands, and occasionally capturing unbanded group members (Brown 1997). In provisioning sessions, food items (peanuts or bread) are placed in permanently present open wire-mesh cages at established locations within a territory; these are used for capture when necessary. The assembly stimulus (police whistle) is then used to alert the group to the presence of food. Generally, the group quickly approaches to within a few metres in the area around the feeding station. Individuals then take turns visiting the station, usually taking food items for consumption or caching within the vicinity. We took advantage of these group provisioning assemblies and the birds’ habituation to observers both to tape-record individuals for use as stimuli, and to position groups for playback trials. All feeding stations are located well within the territory boundaries of each group; provisioning signals or playbacks in the present study never elicited responses from neighbouring groups.
Sound Stimuli During provisioning sessions we recorded primary calls from each group. Primary calls are probably the most frequently used, and they can be given in a variety of
Amplitude
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Time (s) Figure 1. Spectrograms (bottom) and corresponding amplitude contours (waveforms; top) of five primary calls given by Mexican jays, showing variation across individuals. The first two are from individuals within the same social group, while the following three were taken from three other groups. The timing between calls is artificial; the signals were edited in sequence for this figure.
contexts (Brown 1994). Figure 1 shows amplitude waveforms (top) and spectrograms (bottom) of five primary calls from five different individuals. The first two calls are from individuals within the same group; the following three were taken from separate groups. Primary calls are relatively brief, somewhat harsh sounding, and typically of ascending frequency sweeps. These calls are often produced in response to disruption to the setting, such as a conspecific intruder, predators, or even humans. These calls are effective in eliciting a territorial response by the jays, and playbacks of the calls have been used to induce approach for the purpose of monitoring groups (Brown & Brown 1985; Brown & Horvath 1989). Members of the group often exchange bouts of primary calls in a conversational manner during group movements. A careful analysis of primary calls in Mexican jays has not been done, and the extent of similarity within or between groups is not known. Typically, during the feeding sessions the jays engage in calling at initially high levels, then taper off to more sporadic bursts while feeding. Primary calls as labelled in this paper are equivalent to those termed ‘loud call notes’ by Brown (1997). In recording sessions, calls were recorded by one individual, while two observers kept track of individual
identity. We used a Sony TCM5000 cassette recorder, and a Sennheiser microphone (ME20/K3U or ME62/K6) held in a 36 cm parabolic reflector (Sony PBR330). Calls were recorded opportunistically, and notes on individual identities were narrated onto the tape immediately following what were judged to be potentially usable bouts of calling. We later digitized the stimuli using Signal software (Beeman 1996) with a sampling rate of 32 kHz, then filtered some to remove extraneous noise. We selected one naturally occurring bout of three to five primary calls given by one identified individual from each group on the basis of recording clarity, without regard for age, sex, or dominance status of the calling individual. We then recorded these call bursts onto playback tapes (one tape for each group), with one natural call sequence presented during an 8-s stimulus interval (repeat cycles from onset to onset). Each trial lasted 120 s, or 15 stimulus cycles.
Trial Procedure For each of the groups we preselected an appropriate location for the playback speaker in a response circle consisting of a relatively isolated natural copse of vegetation. For all groups we were able to find naturally
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isolated vegetation clusters, eliminating the need to tag response circle boundaries. These locations were about 10 m in diameter and approximately 25 m away from the feeding station, separated by a relatively open area. For each trial, we positioned the playback speaker, a wireless amplified speaker custom-made by Mineroff Electronics, about 2 m off the ground near the centre of the response circle, facing the feeding station. We then situated ourselves such that we could easily observe the feeding area and designated response circle. Once positioned, we summoned the group to the feeding station with the police whistle. We waited until the group was actively feeding and had settled from their approach to the station. We then initiated playback of the appropriate stimulus tape, either the within-group call or a prechosen betweengroup stimulus, and two observers independently recorded behavioural indices. Observational measures included the latency for the first entry into the response circle by any individual, and the total number of entries into the response circle during each 8-s stimulus interval. We also tape-recorded each session and later digitized these recordings. From these we counted the total number of antiphonal calls given during the first 16 s (two stimulus intervals) of each trial. Each tape was used in two trials, once as the appropriate within-group (own) playback, and once as a between-group stimulus, preselected such that the between-group tape was from a nonadjacent group, and with no reciprocal pairings of groups. Thus, the stimulus set used for the playbacks was identical for the withinand between-group trials, assuring that other potential factors such as sex, age or dominance of the calling animal were the same for the two conditions. We conducted playbacks over 2 days beginning in early morning, with the ordering of groups the same both days. We also predetermined the presentation condition for each group such that roughly equal numbers of between-group and within-group trials were conducted each day. We conducted the study outside the breeding season in mid-February 1999 to avoid potential influences of nesting activities. As groups were paired to themselves, in analyses we used within-group comparisons for appropriate statistical tests. Because the trials mimicked the vocal component of a territorial intrusion (Brown & Brown 1985; Brown & Horvath 1989), we predicted greater calling, more response circle entries, and more rapid initial entry into the response circle for the between-group trials. However, to allow for the possibility that responses might occur in the opposite direction as predicted, we employed directed tests, which use asymmetrical rejection regions favouring the predicted response direction (Rice & Gaines 1994). If the variables were non-normally distributed we used a nonparametric test (latency measure). We adjusted the significance levels for each test taking into account the three comparisons being made (sequential Bonferroni method: Rice 1989; Zar 1999). In addition, we calculated an overall probability for the unadjusted P values using a Fisher’s combined test, which gives a probability of obtaining the three probabilities as a set (Wolf 1986).
140 120 Latency to enter circle (s)
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Stimulus condition Figure 2. Latency for the first group member to enter the response circle. Box plots show the second and third quartile, with the median designated by the horizontal line within each box. The extended bars designate the 10–90% range, and the outlying filled circles show the fifth and 95th percentile points.
RESULTS The median latency to enter the response circle by a group member was much shorter (faster approach) in response to the between-group stimulus than to the within-group stimulus (Wilcoxon matched-pairs signed-ranks test: T=2.24, N=10 pairs, Pcalculated =0.016, Padjusted =0.031) (Fig. 2). Note that the fastest response was actually seen for a within-group playback trial, for which the variability of response was large. The average number of entries into the response circle during the entire 2-min playback trial was greater for the between-group trials (paired t test: t9 =2.72, Pcalculated =0.015, Padjusted =0.044), during which the jays made nearly four times as many entries as during the within-group trials (Fig. 3). Figure 4 shows the average number of antiphonal primary calls given in response to the playback stimulus during the first two 8-s stimulus intervals combined. The average number of calls given was significantly greater in response to the between-group stimulus (paired t test: t9 =2.52, Pcalculated =0.021, Padjusted =0.021). The Fisher’s combined test was significant (26 =25.50, P<0.001), indicating the probability of obtaining these three results as a set by chance. DISCUSSION By all three measures used, Mexican jay groups responded more strongly to playbacks of primary calls from outside their group than to calls from within their group. This response differential was seen in both approach measures and in the immediate antiphonal calling by the groups. Since the stimuli used in the two conditions were
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Stimulus condition Figure 3. Average±SE number of entries into the response circle during the entire 2-min playback interval.
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Stimulus condition Figure 4. Average±SE number of primary calls given by the groups in response to the first two playback stimuli presented.
identical, differential effects due to age, sex, dominance or other subject characteristics of the caller can be eliminated as possible sources of the observed response differences. Instead, the response pattern must be due to some component of group membership. Presumably, this response results from the first step in a territorial encounter, with the approach component perhaps reflecting the beginning of an attempt to dislocate the intruder. In playbacks given to groups, an interpretation of the results must be made carefully, as responses may be influenced by different elements of group dynamics (Hopp & Morton 1998). Because members respond to one another as well as to the playback stimulus, attributing
response differences to particular members or categories of members is not possible. Factors including social facilitation and inhibition, and audience or recruitment effects, may play a role in mediating the differences observed using this type of design. Despite such caveats, we nevertheless have definitively shown that the response seen by the group as a whole is greater to an outsider than to an insider. How this response is mediated in Mexican jays, and whether the observed response results from internal social dynamics or a summation of individual responses cannot be definitively ascertained. Several possible mechanisms may facilitate this difference in group responsivity, either by themselves or in combination. First, it may be that individuals within a group develop some common characteristics in the acoustics of their calls, as has been seen in several other species (see examples in Farabaugh & Dooling 1996, and those given in the Introduction). Such vocal convergence would give the primary calls a group-signature function with common acoustic features serving to directly encode group recognition. Members would then respond more strongly to calls not carrying these shared features. This explanation would predict a greater acoustic similarity for calls recorded within a given group than a comparable set of calls from between groups. A second possibility is that the jays simply recognize each individual member of their own group. Presentation of an outside call would result in the observed response differential because each individual of the group independently recognizes the call as an unfamiliar individual. This explanation would predict a measurable degree of intra-individual similarity of calls, and a concomitant ability to distinguish statistically among individuals on the basis of measurable call features. Third, it may be that within a group each bird simply becomes familiar with the calls given by other group members as a result of stimulus habituation, with categories of familiar (within-group) and unfamiliar (outside-group) calls, but without a distinction made between individuals on the basis of their calls. Calls presented from an outside member would then invoke a greater response as an unfamiliar call, rather than as an exemplar of some particular social category. Fourth, it is possible that responses to outsiders result from a behavioural ‘division of labour’, wherein one or a small number of individuals within the group monitor intrusions, and the alerting reactions of these individuals then trigger a mob response by the group. However, under this scenario we are still left with the question of how the monitors recognize an intruder by vocal characteristics, and we return to the above three explanations. The character of the group responses to playback can be used to examine the viability of each of these explanatory hypotheses. If our observed group response results exclusively from either individual recognition or from familiarity/habituation, we would expect that on the within-group trials, the individual whose call we used for the trial would be the only individual responding to the playback stimulus. Under both explanations, this bird would presumably be the only member of the group
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to consider the playback stimulus to be an outside individual, or an unfamiliar signal, respectively. Although on a few trials we observed only one member to enter the response circle, this occurred during both within- and between-group trials. For most trials more than one individual entered the response circle, even on within-group trials. Because of the difficulty of tracking individuals during trials we cannot address whether the first bird to enter the response circle during within-group trials was more likely to be the individual from which we recorded the playback stimulus. However, the behavioural patterns observed suggest that the response is not based on individual recognition alone. The fourth explanation, the group-monitor hypothesis, would predict that the first individual to enter the response circle would be consistent across the two conditions. For trials where we were able to record this information, this was not the case. Under this explanation we would also expect a typical response scenario to consist of a leader–follower format, where one individual appeared to initiate the response, followed by recruitment of other group members. This pattern was also not what we observed. Rather, we usually observed small subsets of the group react almost simultaneously. The overall pattern of response seen was not uniform enough to favour conclusively any of these explanations. Instead, the response seen may result from a combination of these, perhaps even with differing response tendencies influencing different members of the group. For example, it is possible that while the actual recognition abilities are uniform across individuals, other social mechanisms, such as dominance status, influence an individual’s willingness to respond. Our study demonstrates that Mexican jays are able to recognize group members from nonmembers. How this ability is mediated is unclear, and appears not to be simple. Further studies with this species should focus on the characteristics of the signals, particularly to determine whether reliable differences between groups might occur, and on responses to playbacks by individual members of a group.
Acknowledgments We thank Wade and Emily Sherbrooke for hosting us at the American Museum of Natural History Southwestern Research Station. John McCormack helped during recording sessions. We acknowledge financial support from the Maria Sklodowska Joint Fund II (grant PAN/EPA-96-241) and the Kosciuszko Foundation, from the Center for Polish Culture in New York, U.S.A. We are grateful to the National Science Foundation and National Institute of Mental Health for financial support of the ongoing studies of Mexican jays from 1969 to 1999. Computer equipment bought from funds in the grant KBN-6 PO4F 030 08 was used in preparation of the manuscript. All procedures complied with federal and local laws and Guidelines for the Use of Animals in Research. The research presented here was evaluated and approved by the Animal Behavior Society’s Animal Care Committee on 2 January 2001.
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