Negotiation of territorial boundaries in a songbird.

How do territorial neighbors resolve the location of their boundaries? We addressed this question by testing the predictions of 2 nonexclusive game theoretical models for competitive signaling: the sequential assessment game and the territorial bargaining game. Our study species, the banded wren, is a neotropical nonmigratory songbird living in densely packed territorial neighborhoods. The males possess repertoires of approximately 25 song types that are largely shared between neighbors and sequentially delivered with variable switching rates. Over 3 days, boundary disputes among pairs of neighboring males were synchronously recorded, their perch positions were marked, and their behavioral interactions were noted. For each countersinging interaction between 2 focal males, we quantified approach and retreat order, a variety of song and call patterns, closest approach distance, distance from the territorial center, and female presence. Aggressors produced more rattle-buzz songs during the approaching phase of interactions, whereas defenders overlapped their opponent's songs. During the close phase of the interaction, both males matched frequently, but the key determinant of which one retreated first was song-type diversity-first retreaters sang with a higher diversity. Retreaters also produced more unshared song types during the interaction, and in the retreating phase of the interaction, they overlapped more. A negative correlation between song-type diversity asymmetry and contest duration suggested sequential assessment of motivational asymmetry. The use of this graded signal, which varied with distance from the center and indicated a male's motivation to defend a particular position, supported the bargaining model. The bargaining game could be viewed as a series of sequential assessment contests.

Unfavourable environment limits social conflict in Yuhina brunneiceps.

Identifying the factors that modulate cooperative and competitive behaviours is the key to understanding social evolution. However, how ecological factors affect social conflict and their fitness consequences remain relatively unexplored. Here, using both a game-theoretical model and empirical data, we show that Taiwan yuhinas (Yuhina brunneiceps)--a joint-nesting species in which group members are unrelated--employ more cooperative strategies in unfavourable environmental conditions. Fighting duration was lower, fewer total eggs were laid and incubation was more likely to start after all females completed egg laying (which causes more synchronous egg hatching). Surprisingly, as a consequence, there were more surviving offspring in unfavourable conditions because the cooperative strategies resulted in fewer dead nestlings. To our knowledge, this study is the first theoretical analysis and empirical study demonstrating that an unfavourable environment reduces social conflict and results in better fitness consequences in social vertebrates.

Integrating perspectives on vocal performance and consistency.

Recent experiments in divergent fields of birdsong have revealed that vocal performance is important for reproductive success and under active control by distinct neural circuits. Vocal consistency, the degree to which the spectral properties (e.g. dominant or fundamental frequency) of song elements are produced consistently from rendition to rendition, has been highlighted as a biologically important aspect of vocal performance. Here, we synthesize functional, developmental and mechanistic (neurophysiological) perspectives to generate an integrated understanding of this facet of vocal performance. Behavioral studies in the field and laboratory have found that vocal consistency is affected by social context, season and development, and, moreover, positively correlated with reproductive success. Mechanistic investigations have revealed a contribution of forebrain and basal ganglia circuits and sex steroid hormones to the control of vocal consistency. Across behavioral, developmental and mechanistic studies, a convergent theme regarding the importance of vocal practice in juvenile and adult songbirds emerges, providing a basis for linking these levels of analysis. By understanding vocal consistency at these levels, we gain an appreciation for the various dimensions of song control and plasticity and argue that genes regulating the function of basal ganglia circuits and sex steroid hormones could be sculpted by sexual selection.

Parental care, cost of reproduction and reproductive skew: a general costly young model.

Understanding the mechanisms by which animals resolve conflicts of interest is the key to understanding the basis of cooperation in social species. Conflict over reproductive portioning is the critical type of conflict among cooperative breeders. The costly young model represents an important, but underappreciated, idea about how an individual's intrinsic condition and cost of reproduction should affect the resolution of conflict over the distribution of reproduction within a cooperatively breeding group. However, dominant control in various forms and fixed parental care (offspring fitness dependent solely on total brood size) are assumed in previous versions of costly young models. Here, we develop a general costly young model by relaxing the restrictive assumptions of existing models. Our results show that (1) when the complete-control assumption is relaxed, the costly young model behaves very differently from the original model, and (2) when the fixed parental care assumption is relaxed, the costly young-costly care model displays similar predictions to the tug-of-war model, although the underlying mechanisms causing these similar patterns are different. These results, we believe, help simplify the seemingly divergent predictions of different reproductive skew models and highlight the importance of studying the group members' intrinsic conditions, costs of producing young, and costs of parental care for understanding breeding conflict resolution in cooperatively breeding animals.

Group provisioning limits sharing conflict among nestlings in joint-nesting Taiwan yuhinas.

Offspring often compete over limited available resources. Such sibling competition may be detrimental to parents both because it entails wasted expenditure and because it allows stronger offspring to obtain a disproportionate share of resources. We studied nestling conflict over food and its resolution in a joint-nesting species of bird, the Taiwan yuhina (Yuhina brunneiceps). We show that adult yuhinas coordinate their feeding visits, and that this coordination limits competition among nestlings, leading to a 'fairer' division of resources. Transponder identification and video-recording systems were used to observe adult feeding and nestling begging behaviours. We found that: (i) yuhinas feed nestlings more often in large parties than in small parties; (ii) feeding events occurred non-randomly in bouts of very short intervals; and (iii) food distribution among nestlings was more evenly distributed, and fewer nestlings begged, during large-party feeding bouts compared with small-party feeding bouts. To our knowledge, this is the first study in a cooperative breeding species showing that adults can influence food allocation and competition among nestlings by coordinating their feeding visits. Our results confirm the hypothesis that the monopolizability of food affects the intensity of sibling competition, and highlight the importance of understanding the temporal strategies of food delivery.

Climatic patterns predict the elaboration of song displays in mockingbirds.

Climatic variability and unpredictability affect the distribution and abundance of resources and the timing and duration of breeding opportunities. In vertebrates, climatic variability selects for enhanced cognition when organisms compensate for environmental changes through learning and innovation. This hypothesis is supported by larger brain sizes, higher foraging innovation rates, higher reproductive flexibility, and higher sociality in species living in more variable climates. Male songbirds sing to attract females and repel rivals. Given the reliance of these displays on learning and innovation, we hypothesized that they could also be affected by climatic patterns. Here we show that in the mockingbird family (Aves: Mimidae), species subject to more variable and unpredictable climates have more elaborate song displays. We discuss two potential mechanisms for this result, both of which acknowledge that the complexity of song displays is largely driven by sexual selection. First, stronger selection in more variable and unpredictable climates could lead to the elaboration of signals of quality. Alternatively, selection for enhanced learning and innovation in more variable and unpredictable climates might lead to the evolution of signals of intelligence in the context of mate attraction.

The deterrent effect of bird song in territory defense.

Using the responses of territory owners to playback to infer the territorial function of acoustic signals is common practice. However, difficulties with interpreting the results of such experiments have obscured our understanding of territorial signalling. For instance, a stronger response to playback is often interpreted as more aggressive, but there is no consensus as to whether this should be in response to the least or most threatening simulated intruder. Rather than following a gradual increase or decrease, the relationship between signal intensity and response strength may instead describe a peaked curve. We manipulated banded wren (Thryophilus pleurostictus) songs to simulate low-, median-, and high-performance singers and used these songs as stimuli in playback experiments. Banded wrens were less likely to approach the high-performance stimulus compared with the low- and median-performance stimuli. However, the birds that did approach the high-performance stimulus sang more than those that approached the low-performance stimulus. In addition, birds were more likely to match the songs when exposed to the median- and high-performance stimuli compared with the low-performance stimuli, and song matching predicted approach behavior. These results are in accordance with theoretical models of aggressive encounters in which low-performance opponents are challenged without further assessment. Median- and high-performance opponents, however, may require further assessment, and the latter may be perceived as too intimidating for approach.

Trill consistency is an age-related assessment signal in banded wrens.

Older males tend to have a competitive advantage over younger males in sexual selection. Therefore, it is expected that signals used in sexual selection change with age. Although song repertoire size in songbirds is often mentioned as an age-related trait, many species, including the banded wren (Thryothorus pleurostictus), do not increase their repertoires after the first year. Here, we show that banded wrens reproduce the trill notes in their songs with less variability between them (i.e. more consistently) when they grow older. In a playback experiment, we also show that banded wrens discriminate between younger and older birds based on structural aspects of their song. In a second experiment, banded wrens also respond differentially to natural songs versus songs with artificially enhanced consistency. We argue that consistency in trill note reproduction may be achieved through practice. Sexual selection in the form of male-male competition may therefore operate on a phenotypic trait, the expression of which is enhanced by practice.

Singing in the face of death: male banded wrens sing more to playback in their last breeding season.

Investment in signalling is subject to multiple trade-offs that vary with life-stage, leading to a complex relationship between survival and trait expression. We show a negative relationship between survival and song rate in response to simulated territorial intrusion in male banded wrens (Thryophilus pleurostictus), and test several explanations for this association. (1) Male age failed to explain the association: though age affected song rate in a cross-sectional analysis, longitudinal analysis showed that individuals did not increase their song rate as they got older. Reconciling these results suggests differential selection against young males that respond to intrusion with low song rates. (2) Mortality costs of high song rates did not appear to explain the negative relationship between song rate and survival because, though song rate in response to playback was condition-dependent, high song rates in a different context did not appear to impose mortality costs. (3) High levels of territorial pressure may have increased mortality, but were not associated with high song rates in response to playback. (4) Since song rates did not increase with age, but tended to increase only in the last year of life, we tentatively suggest that the negative relationship between song rate and survival could represent a terminal investment in territorial defence by males in their final breeding season, though further work is needed to confirm this conclusion.

Syllable Type Consistency is Related to Age, Social Status, and Reproductive Success in the Tropical Mockingbird.

Many animals repeat standardized displays multiple times while attracting a mate or deterring a rival. In such contexts it is possible that the ability to perform each display or signal type in a consistent fashion is under direct selection. Studies on sexual selection on song learning in birds have focused on differences in repertoire size with less attention to the potential importance of being able to perform each song/syllable type with high consistency. We present evidence that tropical mockingbirds decrease the variation between renditions of each syllable type as they grow older (i.e., become more consistent) and that more consistent males in this species tend to have higher dominance status and reproductive success. These findings stress the importance of consistency in the performance of sexual displays and suggest that this parameter may be very relevant even in species that are selected for high vocal diversity (i.e., large repertoires). In addition to signalling dominance status and age, we hypothesize that syllable type consistency may also be an indicator of the integrity of brain function in birds analogous to the tests used for neuropsychological assessment in humans.

Context-dependent functions of avian duets revealed by microphone-array recordings and multispeaker playback.

In many tropical animals, male and female breeding partners combine their songs to produce vocal duets [1-5]. Duets are often so highly coordinated that human listeners mistake them for the songs of a single animal [6]. Behavioral ecologists rank duets among the most complex vocal performances in the animal kingdom [7, 8]. Despite much research, the evolutionary significance of duets remains elusive [9], in part because many duetting animals live in tropical habitats where dense vegetation makes behavioral observation difficult or impossible. Here, we evaluate the duetting behavior of rufous-and-white wrens (Thryothorus rufalbus) in the humid forests of Costa Rica. We employ two innovative technical approaches to study duetting behavior: an eight-microphone acoustic location system capable of triangulating animals' positions on the basis of recordings of their vocalizations [10] and dual-speaker playback capable of simulating duets in a spatially realistic manner [11]. Our analyses provide the first detailed spatial information on duetting in both a natural context and during confrontations with rivals. We demonstrate that birds perform duets across highly variable distances, that birds approach their partner after performing duets, and that duets of rivals induce aggressive, sex-specific responses. We conclude that duets serve distinct functions in aggressive and nonaggressive contexts.

Is bird song a reliable signal of aggressive intent?

In this commentary, we discuss recent experiments on the reliability of bird song as a signal of aggressive intent during territorial conflicts. We outline relevant theoretical views on honest signaling, highlighting the vulnerability handicap hypothesis as a possible explanation for soft song's reliability in predicting attack. We also sketch possible methods of testing whether soft song agrees with key predictions of the vulnerability handicap hypothesis. Finally, we suggest possible empirical refinements that may be useful in future studies of signals of intent, both in birds and in animals broadly. In particular, we argue that future studies of intent should strive to incorporate the following elements into their experimental design: (1) multi-modal signal components, (2) interaction dynamics, and (3) minimal time intervals. Simulated exchanges using dynamically-interactive models may provide a powerful means of incorporating all three of these design features simultaneously.

How reliable are the methods for estimating repertoire size?

Quantifying signal repertoire size is a critical first step towards understanding the evolution of signal complexity. However, counting signal types can be so complicated and time consuming when repertoire size is large, that this trait is often estimated rather than measured directly. We studied how three common methods for repertoire size quantification (i.e., simple enumeration, curve-fitting and capture-recapture analysis) are affected by sample size and presentation style using simulated repertoires of known sizes. As expected, estimation error decreased with increasing sample size and varied among presentation styles. More surprisingly, for all but one of the presentation styles studied, curve-fitting and capture-recapture analysis yielded errors of similar or greater magnitude than the errors researchers would make by simply assuming that the number of types in an incomplete sample is the true repertoire size. Our results also indicate that studies based on incomplete samples are likely to yield incorrect ranking of individuals and spurious correlations with other parameters regardless of the technique of choice. Finally, we argue that biological receivers face similar difficulties in quantifying repertoire size than human observers and we explore some of the biological implications of this hypothesis.

Relative threat and recognition ability in the responses of tropical mockingbirds to song playback.

It has been suggested that individual recognition based on song may be constrained by repertoire size in songbirds with very large song repertoires. This hypothesis has been difficult to test because there are few studies on species with very large repertoires and because traditional experiments based on the dear enemy effect do not provide evidence against recognition. The tropical mockingbird, Mimus gilvus, is a cooperative breeder with very large song repertoires and stable territorial neighbourhoods. The social system of this species allowed us to test individual recognition based on song independently from the dear enemy effect by evaluating male response to playback of strangers, neighbours (from shared and unshared boundaries), co-males (i.e. other males in the same social group) and own songs. Although subjects did not show a dear enemy effect, they were less aggressive to co-males than to all other singers. Our results suggest that recognition in tropical mockingbirds (1) does not simply distinguish between familiar and unfamiliar singers, (2) requires a small sample of both songs and song types, (3) does not rely on individual-specific sequences of song types and (4) is not likely to rely on group-specific vocal signatures potentially available in cooperatively breeding groups. We conclude that this is a case of true recognition and suggest that the lack of a dear enemy effect in this and other species with large repertoires may relate to the role of song in mate attraction and the perception of neighbours as a threat to future paternity.

Song matching, overlapping, and switching in the banded wren: the sender's perspective.

Interpreting receiver responses to on-territory playback of aggressive signals is problematic. One solution is to combine such receiver-perspective experiments with a sender-perspective experiment that allows subjects to demonstrate how their choice of singing strategies is associated with their approach behavior. Here we report the results of a sender-perspective study on the banded wren (Thryothorus pleurostictus), and combine information on context and results of previous receiver-perspective experiments to clarify function. Territorial males were presented with a 5-min playback consisting of song types present in their repertoire. We assessed the degree to which the subjects' song matching rate, overlapping rate, and song-type versatility were correlated with their approach latency, closeness of approach, latency to first retreat, and time spent close to the speaker. Male age, breeding stage, and features of the playback stimuli were also considered. Song matching was associated with rapid and close approach, consistent with the receiver-perspective interpretation of type matching as a conventional signal of aggressive motivation. Overlapping was associated with earlier retreat, and together with the aversive receiver response to our previous overlapping playback experiment suggests that overlapping is a defensive withdrawal signal. High versatility was associated with slower first retreat from the speaker and high levels of reciprocal matching between subject and playback. Males with fledglings sang with particularly low versatility and approached the speaker aggressively, whereas males with nestlings overlapped more and retreated quickly. Finally, older males matched more but overlapped less.

RESPONSES OF MALE TROPICAL MOCKINGBIRDS TO VARIATION IN WITHIN-SONG AND BETWEEN-SONG VERSATILITY.

Despite their large vocal repertoires and otherwise highly versatile singing style, male mockingbirds sometimes sing in a highly repetitive fashion. We conducted a playback experiment to determine the possible signal value of different syllable presentation patterns during simulated male intrusions in the Tropical Mockingbird (Mimus gilvus) testing the hypothesis that more repetitive singing represents a stronger threat and generates a stronger aggressive response. Responses were measured in terms of approach and singing behavior and were analyzed using McGregor's (1992) multivariate method. We also introduce the use of survival analysis for analyzing response variables for which subjects do not perform the behavior in question in at least one of the replicates (known as 'right-censored variables' in the statistical literature). As predicted by theory, experimental subjects responded more aggressively to songs composed of a single note than to variable ones. However, versatility at the between-song level had an opposite effect as high song switching rates generated stronger responses than low ones. Given the lack of a statistical interaction between within-song versatility and switching rate, we conclude that these two parameters may serve independent purposes and possibly transmit different information. We discuss the possibility that the signal value of variation in vocal versatility lies in the mediation of territorial conflicts, the attraction of female partners and/or the mediation of conflicts over access to reproductive females.

Vocal performance influences male receiver response in the banded wren.

In a variety of songbirds the production of trilled song elements is constrained by a performance tradeoff between how fast a bird can repeat trill units (trill rate) and the range of frequencies each unit can span (frequency bandwidth). High-performance trills serve as an assessment signal for females, but little is known about the signal value of vocal performance for male receivers. We investigated the relationship between trill rate and frequency bandwidth in banded wren (Thryothorus pleurostictus) songs. Trilled song elements showed the same performance tradeoff found in other passerines and individuals differed in performance of some trill types. We tested the hypothesis that males of this species assess each other based on trill performance with a two-speaker experiment, in which territory owners were presented with alternating renditions of the same song type manipulated to differ in trill rate. Subjects were significantly more likely to approach the faster trill stimulus first. However, subjects that received trill types closer to the performance limit spent less time close to the fast speaker. Our results show that male banded wrens discriminate and respond differently to songs based on their vocal performance. Thus, performance of physically challenging songs may be important in intra- as well as inter-sexual assessment.

Accuracy of an acoustic location system for monitoring the position of duetting songbirds in tropical forest.

A field test was conducted on the accuracy of an eight-microphone acoustic location system designed to triangulate the position of duetting rufous-and-white wrens (Thryothorus rufalbus) in Costa Rica's humid evergreen forest. Eight microphones were set up in the breeding territories of 20 pairs of wrens, with an average intermicrophone distance of 75.2+/-2.6 m. The array of microphones was used to record antiphonal duets broadcast through stereo loudspeakers. The positions of the loudspeakers were then estimated by evaluating the delay with which the eight microphones recorded the broadcast sounds. Position estimates were compared to coordinates surveyed with a global-positioning system (GPS). The acoustic location system estimated the position of loudspeakers with an error of 2.82+/-0.26 m and calculated the distance between the "male" and "female" loudspeakers with an error of 2.12+/-0.42 m. Given the large range of distances between duetting birds, this relatively low level of error demonstrates that the acoustic location system is a useful tool for studying avian duets. Location error was influenced partly by the difficulties inherent in collecting high accuracy GPS coordinates of microphone positions underneath a lush tropical canopy and partly by the complicating influence of irregular topography and thick vegetation on sound transmission.

Overlapping signals in banded wrens: long-term effects of prior experience on males and females.

We tested the signal value of song overlapping in banded wrens (Thryothorus pleurostictus), using interactive playback to either overlap or alternate with their songs. Males shortened song duration and decreased variability in song length when their songs were overlapped by playback, suggesting that they were attempting to avoid being overlapped and perhaps being less aggressive. A novel finding was an effect of long-term prior experience: song lengths remained relatively short in alternating trials that followed two or more days after overlapping trials. Approach responses to the two treatments did not differ overall, but there was a parallel effect of prior experience: males tended to stay further from the speaker during alternating treatments if they had previously been overlapped by playback. Some females paired to the male subjects sang in response to playback and were also influenced by prior experience, singing more during alternating trials that had not been preceded by an overlapping trial. Male overlappers may signal dominance over a rival to other male or female receivers in a communication network, but it is currently unclear whether overlapping indicates motivation to escalate an aggressive interaction, or whether this singing strategy is related to male quality. Banded wrens are long-lived and maintain year-round territories, so modifying responses to rivals based on prior experience is likely to be important for success.

Neighbour recognition by resident males in the banded wren, Thryothorus pleurostictus, a tropical songbird with high song type sharing.

Several studies and reviews have suggested that the ability to discriminate between neighbours and strangers decreases as neighbour song repertoire size and song type sharing increase. We tested the recognition capabilities of territorial male banded wrens by comparing the aggressive approach responses of focal birds to three playback treatments: shared song types sung by an adjacent neighbour (neighbour song), shared song types sung by unfamiliar birds (mimic song), and unshared song types sung by unfamiliar birds (unfamiliar song). All three treatments for each male were broadcast from the same location on the territorial boundary shared with the appropriate neighbour. As expected, focal males responded nonaggressively to the neighbour treatment and aggressively to the unfamiliar song treatment. The approach response to the mimic treatment was statistically indistinguishable from the unfamiliar treatment and significantly higher than the neighbour treatment, suggesting that most males were able to recognize unfamiliar singers even when the song types played were very similar to those of their neighbours. The relative strength of responses to the mimic varied: some males treated the mimic song with low aggression levels typical of responses to neighbour song. Repertoire sizes of focal and neighbour birds, the fraction of song types shared among neighbouring males, and the similarity of neighbour and mimic song types did not explain this variation. Therefore, within the short 3-min period of our playback experiments, some birds may have used repertoire composition as a recognition cue and confused the mimic with the neighbour. Copyright 2001 The Association for the Study of Animal Behaviour.