Predicting and Measuring Decision Rules for Social Recognition in a Neotropical Frog.

AbstractMany animals use signals to recognize familiar individuals but risk making mistakes because the signal properties of different individuals often overlap. Furthermore, outcomes of correct and incorrect decisions yield different fitness payoffs, and animals incur these payoffs at different frequencies depending on interaction rates. To understand how signal variation, payoffs, and interaction rates shape recognition decision rules, we studied male golden rocket frogs, which recognize the calls of territory neighbors and are less aggressive to neighbors than to strangers. We first quantified patterns of individual variation in call properties and predicted optimal discrimination thresholds using signal variation. We then measured thresholds for discriminating between neighbors and strangers using a habituation-discrimination field playback experiment. Territorial males discriminated between calls differing by 9%-12% in temporal properties, slightly higher than the predicted thresholds (5%-10%). Finally, we used a signal detection theory model to explore payoff and interaction rate parameters and found that the empirical threshold matched those predicted under ecologically realistic assumptions of infrequent encounters with strangers and relatively costly missed detections of strangers. We demonstrate that receivers group continuous variation in vocalizations into discrete social categories and that signal detection theory can be applied to understand evolved decision rules.

Male song sparrows have elevated testosterone in response to neighbors versus strangers.

Upon hearing a conspecific signal, animals must assess their relationship with the signaller and respond appropriately. Territorial animals usually respond more aggressively to strangers than neighbors in a phenomenon known as the "dear enemy effect". This phenomenon likely evolved because strangers represent a threat to an animal's territory tenure and parentage, whereas neighbors only represent a threat to an animal's parentage because they already possess a territory (providing territory boundaries are established and stable). Although the dear enemy effect has been widely documented using behavioral response variables, little research has been conducted on the physiological responses of animals to neighbors versus strangers. We sought to investigate whether the dear enemy effect is observed physiologically by exposing territorial male song sparrows (Melospiza melodia) to playback simulating a neighbor or a stranger, and then collecting blood samples to measure plasma testosterone levels. We predicted that song sparrows would exhibit increased testosterone levels after exposure to stranger playback compared to neighbor playback, due to the role testosterone plays in regulating aggression. Contrary to our prediction, we found that song sparrows had higher testosterone levels after exposure to neighbor playback compared to stranger playback. We discuss several explanations for our result, notably that corticosterone may regulate the dear enemy effect in male song sparrows and this may inhibit plasma testosterone. Future studies will benefit from examining corticosterone in addition to testosterone, to better understand the hormonal underpinnings of the dear enemy effect.

Age-based discrimination of rival males in western bluebirds.

Adaptive social behavior frequently involves discriminating between classes of individuals such as relatives versus non-relatives, older versus younger individuals, or individuals of different status. In the absence of spatial cues, this discrimination may be based on signals that correlate with fitness-related traits (e.g., older or high-status males may sing higher performance songs) or with identity, for example, when receivers distinguish and classify signalers based on their unique signal structure. Here, we examine vocal age-based discrimination in western bluebirds (Sialia mexicana), a North American songbird in which older males have a significant advantage in obtaining extra-pair fertilizations, and therefore pose a significantly higher threat to paternity than younger males. We asked whether western bluebird males showed a higher response to playback of songs of older males compared to younger males relative to their own age. We prepared song stimuli by removing three potential signals of age that have been identified as important in other species: (1) note consistency (which was achieved by playing a single instance of each note repeatedly), (2) note repertoire size, and (3) singing rate (the latter two were equalized across conditions). Even in the absence of these potential signals of age, young males responded more strongly to playback of older males' songs than to young males' songs, suggesting that they are able to discriminate between age classes relative to the threat they pose. Further research is required to determine whether this discrimination is based on individual recognition or signal features that are correlated with age.

Horneros consider their neighbors as precious foes regardless of territory size and human disturbance.

Research on neighbor-stranger discrimination theory has revealed the significance of social context and biological traits affecting the mechanisms that drive social discrimination, such as the dear enemy or nasty neighbor effects (strangers or neighbors more threatening, respectively). Nevertheless, the effects of territory size and human activity on neighbor-stranger experiments have yet to be explored. By examining behavioral responses to spontaneous duets of neighbors and playbacks of strangers' duets, we tested whether rufous horneros (Furnarius rufus) in smaller territories show heightened aggression, responding more strongly to strangers and less to neighbors than those in larger territories. This could be expected because birds in larger territories might struggle to differentiate competitors due to limited interactions, hindering familiarity with neighbors. Meanwhile, birds in smaller territories are likely to treat neighbors as dear enemies due to the need to minimize territorial costs caused by presumed frequent intrusions or to protect limited resources. Contrary to predictions, rufous horneros responded more strongly to strangers than neighbors, regardless of owner territory sizes. This suggests that the presumed higher intruder frequency in smaller territories does not necessarily lead to adjusted dear enemy relationships. Yet, small territory holders exhibited heightened vocal responses to duets of unfamiliar intruders, indicating a stronger 'dear enemy' effect compared to birds with larger territories. We also tested whether dear enemy relationships would be heightened during weekends. This is linked to the difficulty urban birds might face in distinguishing neighbors from strangers during high human activity days (i.e., on weekdays), due to factors like noise masking intruder acoustic cues and heightened vigilance. Territorial owners exhibited consistent dear enemy behavior towards neighbors, regardless of our proxy for human activity. This underscores their ability in identifying competitor identities within urban settings.

Evidence for acoustic discrimination in lemurs: A playback study on wild indris Indri indri.

Indris Indri indri are group-living lemurs that occupy stable territories over several years and perform remarkable long-distance vocal displays. Vocal exchanges between long-term territory neighbors may contribute to assessing reciprocal resource-holding potentials, thus adaptively reducing the costs of territorial defense by limiting aggressive escalation. Previous work showed that indris' songs show distinctive acoustic features at individual and group level. However, the possibility that indris use such cues for individual or group-level recognition has never been investigated experimentally. We conducted a playback experiment to test whether indris discriminate between familiar and nonfamiliar songs. Our rationale lies in the hypothesis of the dear enemy phenomenon, which predicts that territorial animals will show reduced aggression levels toward familiar neighbors compared with novel rivals. We played back stimulus recordings to wild indris from their territory boundaries and examined their responses in terms of vocal and behavioral indicators of willingness to engage in a fight. In line with our predictions, focal animals responded more rapidly and approached more often the speaker in response to playback stimuli of nonfamiliar individuals than to stimuli of neighboring groups. These results indicate that indris can discriminate between different classes of intruders based on distinctive acoustic features of their song choruses. We suggest that increased aggression directed toward unfamiliar intruders may be explained by higher threat levels associated with dispersal and group formation dynamics. We further discuss the relevance of these findings in a strepsirrhine primate model for comparative studies of vocal communication and sociality.

Modulation of dear enemy effects by male dusky warblers (Phylloscopus fuscatus) at different reproductive stages.

Territorial animals show less aggression during intrusion by neighbours than by strangers, a phenomenon known as the "dear enemy effect". Recent studies have shown that the dear enemy effect is variable in some birds throughout the breeding season. However, there is limited research on changes in dear enemy effects in songbirds during the breeding season. In this study, we monitored dusky warblers (Phylloscopus fuscatus) throughout their breeding stages, conducting playback experiments simulating incursions by neighbours and strangers during their egg-laying and incubation/nestling periods, and recording physical responses and song responses from territory owners. The results showed that male dusky warblers responded similarly to neighbours and strangers during the female egg-laying period, but there was a significantly stronger response to strangers than to neighbours during the incubation/nestling period. This suggests that male dusky warblers adjust the intensity of their defences against neighbours according to the reproductive status of their own mate. This may be because neighbouring males threaten the paternity of territorial males during the egg-laying period, so territorial males demote the 'dear enemy' friendly relationships with their neighbours to defend their mate and paternity. In contrast, during the non-reproductive period of females, when neighbours are less of a threat to the paternity of territorial males, lowering defences against neighbouring males allow them to devote more time and energy to activities that improve their fitness, such as foraging and seeking extra-pair mating.

Identity signaling, identity reception, and the evolution of social recognition in a Neotropical frog.

Animals recognize familiar individuals to perform a variety of important social behaviors. Social recognition is often mediated by communication between signalers who produce signals that contain identity information and receivers who categorize these signals based on previous experience. We tested two hypotheses about adaptations in signalers and receivers that enable the evolution of social recognition using two species of closely related territorial poison frogs. Male golden rocket frogs (Anomaloglossus beebei) recognize the advertisement calls of conspecific territory neighbors and display a "dear enemy effect" by responding less aggressively to neighbors than strangers, whereas male Kai rocket frogs (Anomaloglossus kaiei) do not. Our results did not support the identity signaling hypothesis: both species produced advertisement calls that contain similar amounts of identity information. Our results did support the identity reception hypothesis: both species exhibited habituation of aggression to playbacks simulating the arrival of a new neighbor, but only golden rocket frogs showed renewed aggression when they subsequently heard calls from a different male. These results suggest that an ancestral mechanism of plasticity in aggression common among frogs has been modified through natural selection to be specific to calls of individual males in golden rocket frogs, enabling a social recognition system.

Song sparrows do not discriminate between their own song and stranger song.

Bird song is socially learned. During song learning, the bird's hearing its own vocalization is important for normal development of song. Whether bird's own song is represented and recognized as a special category in adult birds, however, is unclear. If birds respond differently to their own songs when these are played back to them, this would be evidence for auditory self-recognition. To test this possibility, we presented song sparrow males (Melospiza melodia) playbacks of their own songs or stranger songs and measured aggressive responses as well as type matching. We found no evidence of behavioral discrimination of bird's own song relative to the (non-matching) stranger song. These findings cast doubt on an earlier proposal that song sparrows display auditory self-recognition and support the common assumption in playback experiments that bird's own song is perceived as stranger song.

Evolutionarily stable investments in recognition systems explain patterns of discrimination failure and success.

Many animals are able to perform recognition feats that astound us-such as a rodent recognizing kin it has never met. Yet in other contexts, animals appear clueless as when reed warblers rear cuckoo chicks that bear no resemblance to their own species. Failures of recognition when it would seem adaptive have been especially puzzling. Here, we present a simple tug-of-war game theory model examining how individuals should optimally invest in affecting the accuracy of discrimination between desirable and undesirable recipients. In the game, discriminating individuals (operators) and desirable and undesirable recipients (targets and mimics, respectively) can all invest effort into their own preferred outcome. We demonstrate that stable inaccurate recognition will arise when undesirable recipients have large fitness gains from inaccurate recognition relative to the pay-offs that the other two parties receive from accurate recognition. The probability of accurate recognition is often determined by just the relative pay-offs to the desirable and undesirable recipients, rather than to the discriminator. Our results provide a new lens on long-standing puzzles including a lack of nepotism in social insect colonies, tolerance of brood parasites and male birds caring for extra-pair young in their nests, which our model suggests should often lack accurate discrimination. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Are both notes of the common cuckoo's call necessary for familiarity recognition?

Common cuckoos (Cuculus canorus) are best known for their simple two-note calls ("cu-coo"), which are uttered only by males during the breeding season. A previous playback study revealed that territorial males were more tolerant toward playbacks of the calls of familiar, neighbouring individuals than toward unfamiliar, stranger simulated intruders, exhibiting the classical "dear-enemy" phenomenon. Here we experimentally assessed whether the acoustic cues for familiarity recognition are encoded in the first and/or second note of these simple calls. To do so, we played mixed sound files to radio-tagged cuckoos, where the first part of the two-note calls was taken from strangers and the second part from neighbours, or vice versa. As controls, we used behavioural data from two-note neighbour and two-note stranger call playbacks. Cuckoos responded consistently to the two types of mixed sound files. When either the first or second note of the call was taken from a stranger and the other note from a neighbour, they responded to these sound files similarly to two-note playbacks of strangers: they approached the speaker of the playbacks more closely and the calling response-latency to playbacks was longer than to familiar controls. These findings point to the importance of both notes in familiarity recognition. We conclude that familiarity recognition in male common cuckoos needs the complete structure of the two-note cuckoo call, which is characteristic for this species.

Social familiarity affects Diana monkey (Cercopithecus diana diana) alarm call responses in habitat-specific ways.

Male Diana monkeys produce loud and acoustically distinct alarm calls to leopards and eagles that propagate over long distances, much beyond the immediate group. Calling is often contagious, with neighbouring males responding to each other's calls, indicating that harem males communicate both to local group members and distant competitors. Here, we tested whether male Diana monkeys responding to each other's alarm calls discriminated familiar from unfamiliar callers in two populations in Taï Forest (Ivory Coast) and on Tiwai Island (Sierra Leone). At both sites, we found specific acoustic markers in male alarm call responses that discriminated familiar from unfamiliar callers, but response patterns were site-specific. On Tiwai Island, males responded to familiar males' eagle alarms with 'standard' eagle alarm calls, whereas unfamiliar males triggered acoustically atypical eagle alarms. The opposite was found in Taï Forest where males responded to unfamiliar males' eagle alarm calls with 'standard' eagle alarms, and with atypical eagle alarms to familiar males' calls. Moreover, only Taï, but not Tiwai, males also marked familiarity with the caller in their leopard-induced alarms. We concluded that male Diana monkeys encode not only predator type but also signaller familiarity in their alarm calls, although in population-specific ways. We explain these inter-site differences in vocal behaviour in terms of differences in predation pressure and population density. We discuss the adaptive function and implications of this behaviour for the origins of acoustic flexibility in primate communication.