Individual voice recognition in a territorial frog (Rana catesbeiana)

Some territorial animals display low levels of aggression towards a familiar territorial neighbour in its usual territory, but exhibit high levels of aggression towards neighbours in novel locations and unfamiliar individuals. Here, we report results from a field playback study that investigated whether territorial males of the North American bullfrog (Rana catesbeiana) could discriminate between the acoustic signals of simulated neighbours and strangers in the absence of contextual cues associated with a specific location. Following repeated exposures to synthetic bullfrog calls from a particular location, subjects responded significantly less aggressively to a familiar call, compared with an unfamiliar one, when both calls were broadcast from familiar and novel locations, indicating that bullfrogs could recognize a neighbour's calls independently of the contextual cues provided by the direction of the neighbour's territory. Subjects responded equally aggressively to unfamiliar calls broadcast from either a familiar or a novel location, which indicates that they could perceive unfamiliar calls as those of a stranger, regardless of where the stranger was encountered. Together, these two results provide evidence that a frog possesses a capacity for individual voice recognition.     

Plasticity of aggressive signalling and its evolution in male spring peepers, Pseudacris crucifer

Acoustic communication is important for determining and maintaining intermale spacing in breeding aggregations of anurans and insects. Because the number and proximity of signalling males can show extensive temporal and spatial variation, we should expect to find mechanisms that permit males to modify their signalling behaviour in ways that balance the needs to attract females and defend their calling space. We conducted two field playback experiments to investigate the role of plasticity in male aggressive signalling in intermale spacing of spring peepers (Anura, Hylidae). In the first experiment, we found a positive correlation between the amplitude of the advertisement calls of a male's nearest neighbour and the stimulus amplitude at which the male first produced aggressive calls. In the second experiment, repeated presentations of advertisement calls above a male's aggressive threshold resulted in rapid decreases in aggressive signalling and significant, but temporary, elevations of aggressive thresholds. We suggest that short-term habituation to a neighbour's calls could function as a proximate mechanism for plasticity in aggression that would allow males to accommodate nearby callers while also tracking fluctuations in the local density of calling individuals. In a third experiment, we examined female choice as an ultimate-level explanation for plasticity in male aggression. Females preferred advertisement calls to aggressive calls, but this preference was weak and was abolished by a 6-dB reduction in the amplitude of the advertisement call. We suggest that female preferences probably function as only one possible source of selection on plasticity in male aggressive signalling and propose energetic limitations as an additional source of selection. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Individual Variation in Advertisement Calls of Territorial Male Green Frogs, Rana clamitans: Implications for Individual Discrimination

Individuals of many territorial species discriminate between familiar territorial neighbors and unfamiliar strangers based on individual differences in acoustic signals. Many anuran amphibians are territorial and use primarily acoustic communication during social interactions, but evidence for acoustically mediated individual discrimination is available only for one species. As a first step in research designed to investigate individual discrimination in a second species of territorial frog, we examined patterns of within-male and among-male variability in 198 advertisement calls of 20 male green frogs, Rana clamitans . The aim was to determine which acoustic properties could be used by males to recognize their territorial neighbors and to estimate limits of reliability afforded by these properties for identifying different neighbors. All of the call properties that we examined exhibited significant inter-individual variation. Discriminant function analyses assigned between 52% and 100% of calls to the correct individual, depending on sample size and the call properties included in the model. This suggests that there is sufficient among-male variability to statistically identify individuals by their advertisement calls. The call properties of fundamental frequency and dominant frequency contributed the most towards discrimination among individuals. Based on their natural history and behavior and the results reported here, we suggest that male green frogs likely discriminate between strangers and adjacently territorial neighbors based on individual variation in advertisement calls.     

Territorial male bullfrogs (Rana catesbeiana) do not assess fighting ability based on size-related variation in acoustic signals

Some animals use communication signals to assess their opponent'ssize and fighting ability during aggressive conflicts. Malefrogs assess their opponent's size based on the fundamentalfrequency (pitch) of advertisement calls, which is negativelycorrelated with body size, an important determinant of fightingability in frogs. I conducted a field playback experiment to investigate whether territorial male bullfrogs assess the sizeof opponents based solely on size-related variation in fundamentalfrequency. I repeatedly broadcast synthetic bullfrog advertisementcalls to three groups of males. Playback stimuli simulateda large male (n = 24), a small male (n = 24), or an acousticallysize-matched male (n = 34). Neither the simulated size of theopponent, the subject's own size, nor the degree of size asymmetrybetween the subject and simulated intruder had significanteffects on the magnitude of responses during the playback testor on the rate of habituation that occurred with repeated stimulation.Post-hoc analyses of effect sizes and statistical power indicatedthat the effects in this study were quite small compared toprevious studies in other frogs. More important, power analysesindicated that this study had high power (1 - ß >0.90) to detect the magnitude of effect sizes observed in previous studies. Thus, territorial male bullfrogs do not appear to assessan opponent's fighting ability based solely on the fundamentalfrequency of acoustic signals. These results contrast starklywith theoretical predictions and previous empirical work withfrogs.     

Aggressive Thresholds of Male Pacific Treefrogs for Advertisement Calls Vary with Amplitude of Neighbors' Calls

In breeding choruses, male Pacific treefrogs (H. regilla) produce advertisement and encounter calls. The role of each call type in establishing intermale spacing patterns was investigated by playing back, at various amplitudes, recordings of these vocalizations to resident males. The aggressive threshold of a male for each call type was defined as the lowest amplitude of playback that elicited encounter calls. Pacific treefrogs consistently had lower aggressive thresholds to playbacks of encounter calls than to playbacks of advertisement calls. Aggressive thresholds to playbacks of advertisement calls were positively correlated with the maximum amplitude of the advertisement calls of neighboring males, as measured at the position of the focal male.     

Aggressive habituation and rim circling in the social organization of bluegill sunfish (Lepomis macrochirus)

Synopsis The rim circling (RC), and aggressive habituation of nesting bluegills were studied in natural colonies during the six days of the reproductive period following spawning. To examine the stimulus specificity of aggressive habituation, selected test individuals and four neighbors were observed on four occasions during one day. After the first observation period established baseline data on aggressive interactions, the appearances of three of the neighbors were manipulated and further observations were made. Two more observation periods followed, separated by a sham manipulation to allow for possible disturbance effects. Fish lengths, inter-nest distances, and positions in the colony were also recorded.An analysis of the data demonstrated that aggressive interaction increased for the three manipulated neighbors. There were no significant differences among the data for the fourth (control) neighbors. The enhanced aggressive interactions between the test and manipulated males were initiated by the males at least partially in response to the changed appearance of the neighbor. Further, the level of aggressive interaction returned to normal after about 2 hours, indicating that the test male had habituated to the new appearances of his neighbors. Thus visual appearance plays an important role in the habituation of aggression between neighboring bluegills. It was not possible to determine if the behavior of the neighbor was also an important cue used in aggressive habituation, but this seems likely. Advantages of aggressive habituation are discussed. It is noteworthy that aggression decreased as internest distance increased.Levels of RC varied significantly over the six days, in a time course dissimilar from aggression. The RC rate is dependent on size of male, nest locality, and circling activity of neighbors. Observations on the synchrony of rim circling indicated social facilitation. It is argued that RC probably fulfills an advertisement function important in defending the brood. The motivation for RC is likely complex, and its performance reflects a mixed aggressive and reproductive strategy in the nesting population. Aggressive habituation functions in the social organization of bluegills to facilitate the occurrence of group displays such as RC.     

Two Novel Vocalizations Are Used by Veeries (Catharus fuscescens) during Agonistic Interactions

Avian vocalizations are common examples of the complex signals used by animals to negotiate during agonistic interactions. In this study, we used two playback experiments to identify agonistic signals in a songbird species with several acoustically complex songs and calls, the veery. In the first experiment, we compared veery singing behavior in response to simulated territorial intrusions including playback of three variations of veery song: 1) song alone as a control, 2) songs with added whisper calls, and 3) songs with introductory notes removed. In the second experiment, we used multimodal stimuli including songs, whisper calls and songs with introductory notes removed, along with a robotic veery mount. Focal males readily responded to all of the playback stimuli, approached the speaker and/or robotic mount, and vocalized. Male veeries gave more whisper calls, and sang more songs without the introductory note in response to all types of playback. However, veeries responded similarly to all types of stimuli presented, and they failed to physically attack the robotic mount. These results indicate that rival veeries use two different types of novel vocalizations: whisper calls and songs lacking the introductory note as agonistic signals, but do not allow us to discern the specific functions of these two vocalizations.     

Regulation of vocal amplitude by the blue-throated hummingbird, Lampornis clemenciae

Animals that rely on vocal communication must broadcast sound so that a perceptible signal is transmitted over an appropriate distance. We found that male blue-throated hummingbirds modified the amplitude of their vocalizations in response to both naturally occurring and experimenter-controlled changes in ambient noise levels. This phenomenon is known as the Lombard effect and may increase the efficiency of acoustic signalling. This study demonstrates the effect under natural field conditions and documents the first hummingbird species (Apodiformes: Trochilidae) to show this behaviour. We measured sound pressure levels (SPLs) of Serial Chip territorial advertisement calls across a natural range of ambient noise, primarily due to creeks within male territories. We found a significant correlation between the amplitude of Serial Chips and the amplitude of background noise. To test this relationship, we broadcast recordings of creek noise at high and low amplitudes while target individuals were producing Serial Chip vocalizations. We measured vocal SPLs before and during the playback. Individuals responded to changes in playback creek noise by changing the amplitude of Serial Chip production. We also measured transmission properties of Serial Chip calls through natural habitat to calculate the approximate amplitude of vocalizations at the position of the calling bird. We suggest that amplitude regulation of vocalizations contibutes to signal transmission distance along with the established relationships between singing behaviour, acoustic structure and habitat. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.     

Fighting talk: complex song elicits more aggressive responses in a vocally complex songbird

Song complexity in many songbirds is a trait subject to sexual selection. It is often associated with male territorial defence. Empirical studies testing differential male responses to rival song in vocally complex songbirds have, however, been scarce. We conducted playback experiments of the endemic New Zealand Tui Prosthemadera novaeseelandiae to test the aggressive response of territorial male Tui to rival songs with differing complexity levels. Overall, complex songs evoked significantly stronger responses from territorial males than did simple songs. Following playback of complex songs, focal males approached the playback more closely and rapidly, and responded with songs of higher complexity than they did to playback of simple songs. This suggests males could both distinguish between different levels of complexity within the Tui repertoire, and perceive a more complex song as a greater territorial threat. Our study is one of the first to demonstrate strong aggressive responses to increased levels of song complexity in a songbird species with highly complex vocalizations.     

Patterns of Vocal Interactions in a Bullfrog (Rana catesbeiana) Chorus: Preferential Responding to Far Neighbors

In chorusing species, males seem to be spaced non-randomly, and their vocal interactions may be governed by particular behavioral rules. We monitored patterns of vocal interactions in a natural bullfrog ( Rana catesbeiana ) chorus to determine the probability with which calls of individual frogs would follow each other's in dyadic sequences. Expected probabilities of responses in a dyad were calculated based upon the joint probabilities of calling (relative calling rates) of the individual frogs; observed probabilities of response reflected the actual number of following responses in each dyad. Results of statistical tests comparing observed and expected probabilities of responding revealed that, when dyads were closely spaced, observed probabilities of a following response were significantly less than the expected probabilities. Conversely, when dyads were composed of more distant males, observed probabilities of responding were significantly greater than expected. Observed probabilities of response were correlated with inter-male distances; males called more frequently than expected following calls of far neighbors, and less frequently than expected following calls of near neighbors. These data suggest that males attend to both nearby and distant callers, and adjust the onset of their own vocalizations appropriately. Males may be actively inhibited by calls of their near neighbors, and their calling may be actively elicited by the calls of their far neighbors.     

Male territorial aggression does not drive conformity to local vocal culture in a passerine bird

In many songbird species, young individuals learn songs from neighbors and then settle nearby, thus creating neighborhoods of conformity to local vocal culture. In some species, individuals appear to postpone song learning until after dispersal, possibly to facilitate conformity to local dialects. Despite decades of study, we still lack a consensus regarding the selective pressures driving this delayed song learning. Two common hypothetical benefits to conformity, and thus delayed song learning, are rooted in territorial interactions; individuals preferentially produce local song either to avoid detection as new arrivals (deceptive mimicry) or to be more effectively recognized as conspecific territory holders. The dickcissel (Spiza americana) is an ideal species in which to study these hypotheses. Males of this species appear to delay song learning until they arrive at their first adult territory, each individual sings a single song type, and conformity to the local song culture is high. Using playback, we contradicted both of the territorial hypotheses described above; male dickcissels did not respond differentially to local vs foreign song playback treatment. We are confident in this lack of difference because dickcissels clearly responded less strongly to a third treatment, neighbor song, than to the other two treatments, demonstrating sufficient power in our experimental design (and providing the first evidence of the dear‐enemy effect in dickcissels). Our results raise the question of why dickcissels respond equally aggressively to both local and foreign songs when other bird species often show reduced aggression toward foreign song. If reduced aggression to foreign song is not ubiquitous in species that achieve conformity through delayed learning, then selection from aggressive territorial interaction seems unlikely to be a general explanation for such delayed learning. Reduced aggression in response to foreign songs in other species may be due to reduced exposure to the stimulus of foreign song or to different cost‐benefit trade‐offs when responding to songs that deviate from the local average.     

Conditional strategies in territorial defense: do Carolina wrens play tit-for-tat?

Neighboring territorial animals are viewed primarily as intenserivals, but there are also opportunities for cooperation amongcompetitors. Many animals respond less aggressively towardneighbors than to strangers. This phenomenon, termed the "dearenemy" effect, should be stable only when the reduced aggressionis reciprocal. Territory owners should use conditional strategiesin territorial defense, showing reduced aggression toward neighbors who cooperate by respecting territorial boundaries but increasingaggression toward invading neighbors. In this study I examinedthe response of territory owners to playbacks of neighborsat shared boundaries before and after intrusions by that neighboror by strangers. Results showed that territory owners did notincrease their aggression toward defecting neighbors but did increase their aggression toward neighbors after a simulatedintrusion by a stranger. This surprising result might reflectthe long-term relationship between neighboring Carolina wrensand the threat posed by rare intruding strangers.     

Sex-specific territorial responses in Tawny Owls Strix aluco

A territorial intruder often poses more of a threat to the territory holder of the same sex as itself. As territorial aggression is associated with costs, aggression shown by birds towards territorial intruders of the opposite sex deserves investigation. This behaviour could arise due to the reproductive value of a mate or through mutualism between members of a pair. We investigated these hypotheses by presenting mated pairs of Tawny Owls Strix aluco with playback of male calls, female calls and a male and female duetting, and recording the number and intensity of responses by the male and female territory holders. Females responded significantly more often to female than to male calls. Males responded equally often to male and female playback. Males which had previously bred successfully with their mate were significantly more likely to respond to female playback in the spring, which suggested males were responding to female playback due to the reproductive value of their mate. There was no evidence of mutualism between members of a pair.     

The Effects of Isolation on the Sensitization and Habituation of Aggression in the Threespine Stickleback (Gasterosteus aculeatus)

Our previous research showed that territorial threespine sticklebacks are more aggressive toward a male conspecific placed in their territory if they have been housed adjacent to a gravid female rather than a male or a nongravid female. This study replicated the condition of a territorial male with an adjacently housed male and compared the results with isolated territorial males. This permitted us to contrast explanations for the increased aggression when the neighbor was a gravid female. If the social context determines the level of aggression, then males with no neighbors (isolates) might be less aggressive because there would be no unique reproductive resource to protect nor any neighbor to protect resources from. Alternatively, if aggression is higher in the isolated group it might be because there was no male neighbor to redirect aggression toward. We found that isolated males were more aggressive toward an intruded male stimulus than males with a male neighbor. The study also provided evidence that sensitization produced by the appearance of an intruding male energizes other aggressive behavior, but not those related to feeding, nor does it cause increase in general activation as measured by increased locomotion.     

The Sound of Arousal: The Addition of Novel Non-linearities Increases Responsiveness in Marmot Alarm Calls

Vocal structure should reflect vocal function. While much attention has focused on quantifying attributes of harmonic vocalizations, the vocalizations of many species also may contain non-linear phenomena such as warbles, subharmonics, biphonation, and deterministic chaos or noise. The function of these non-linearities remains enigmatic. In some species, harmonic vocalizations abruptly become 'noisy' when individuals are physiologically aroused and the sudden onset of these non-linearities could signal arousal or fear to receivers. One untested functional hypothesis is that vocalizations containing non-linearities are more variable from one rendition to the next, and thus are harder to habituate to. In some situations, reducing the likelihood of habituation could be important. Signals that are highly evocative are more difficult to habituate to. Thus, we conducted playback experiments to foraging yellow-bellied marmots ( Marmota flaviventris ) to determine whether the addition of white noise (a non-linear acoustic phenomenon) to alarm calls elicited a greater response than control calls without the non-linearity or control calls with silence, rather than noise, added to them. Marmots spent less time foraging after hearing calls that included noise than after normal or control calls. This result is consistent with the unpredictability hypothesis and suggests that the adaptive value of non-linearities is to prevent habituation.     

Dear Enemies Elicit Lower Androgen Responses to Territorial Challenges than Unfamiliar Intruders in a Cichlid Fish

In many territorial species androgen hormones are known to increase in response to territorial intrusions as a way to adjust the expression of androgen-dependent behaviour to social challenges. The dear enemy effect has also been described in territorial species and posits that resident individuals show a more aggressive response to intrusions by strangers than by other territorial neighbours. Therefore, we hypothesized that the dear enemy effect may also modulate the androgen response to a territorial intrusion. Here we tested this hypothesis in male cichlid fish (Mozambique tilapia, Oreochromis mossambicus) using a paradigm of four repeated territorial intrusions, either by the same neighbour or by four different unfamiliar intruders. Neighbour intruders elicited lower aggression and a weaker androgen response than strangers on the first intrusion of the experiment. With repeated intrusions, the agonistic behaviour of the resident males against familiar intruders was similar to that displayed towards strangers. By the fourth intrusion the androgen response was significantly reduced and there was no longer a difference between the responses to the two types of intruders. These results suggest that the dear enemy effect modulates the androgen response to territorial intrusions and that repeated intrusions lead to a habituation of the androgen response.     

Simulated Birdwatchers’ Playback Affects the Behavior of Two Tropical Birds

Although recreational birdwatchers may benefit conservation by generating interest in birds, they may also have negative effects. One such potentially negative impact is the widespread use of recorded vocalizations, or “playback,” to attract birds of interest, including range-restricted and threatened species. Although playback has been widely used to test hypotheses about the evolution of behavior, no peer-reviewed study has examined the impacts of playback in a birdwatching context on avian behavior. We studied the effects of simulated birdwatchers’ playback on the vocal behavior of Plain-tailed Wrens Thryothorus euophrys and Rufous Antpittas Grallaria rufula in Ecuador. Study species’ vocal behavior was monitored for an hour after playing either a single bout of five minutes of song or a control treatment of background noise. We also studied the effects of daily five minute playback on five groups of wrens over 20 days. In single bout experiments, antpittas made more vocalizations of all types, except for trills, after playback compared to controls. Wrens sang more duets after playback, but did not produce more contact calls. In repeated playback experiments, wren responses were strong at first, but hardly detectable by day 12. During the study, one study group built a nest, apparently unperturbed, near a playback site. The playback-induced habituation and changes in vocal behavior we observed suggest that scientists should consider birdwatching activity when selecting research sites so that results are not biased by birdwatchers’ playback. Increased vocalizations after playback could be interpreted as a negative effect of playback if birds expend energy, become stressed, or divert time from other activities. In contrast, the habituation we documented suggests that frequent, regular birdwatchers’ playback may have minor effects on wren behavior.     

Graded Aggressive Calls in the African Painted Reed Frog Hyperolius marmoratus (Hyperoliidae)

The African painted reed frog, Hyperolius marmoratus, has a potentially complex communication system. Advertisement calls and aggressive calls, although distinct from each other, are in fact two ends of a continuum of graded calls. Playback experiments using standard advertisement calls showed that males increased the proportion of aggressive calls as the stimulus intensity was increased. In addition, three characteristics of the aggressive calls changed in response to higher playback levels. Males increased the number of pulses/call, increased call duration, and decreased dominant frequency. Aggressive calling occurred primarily during the early hours of the night, with considerable overlap with times when females were searching for mates in the chorus. Females tested in two-choice arena trials discriminated against aggressive calls in favor of advertisement calls. It is suggested that aggressive calls reduce a male's ability to attract a female and that a graded signalling system may enable males to escalate agonistic encounters with other males without rendering calls completely unattractive to females.     

Vocalizations of Hypsiboas goianus (Lutz, 1968) (Anura: Hylidae) in Central Brazil

Environmental and morphological factors and social context influence the vocalizations of anuran species. Herein, we observed the acoustic behavior of Hypsiboas goianus males from Central Brazil and analyzed the following calls: advertisement, short aggressive and long aggressive. The acoustic parameters of advertisement calls were not correlated with air temperature, mass or snout–vent length; however, the acoustic parameters of short aggressive calls were influenced by these variables. The temporal parameters of advertisement and short aggressive calls were classified as dynamic properties, while the dominant frequency was considered a static property. Dominant frequency is the most important variable to discriminate calls among individuals.     

Song Functions in Nonduetting Gibbons: Evidence from Playback Experiments on Javan Gibbons (<Emphasis Type="Italic">Hylobates moloch</Emphasis>)

Territorial, pair-living primates usually perform long-distance calls as duets in which adult males and females coordinate their calls. Previous studies using playback experiments have shown that gibbon duets convey information about the status of the caller (location, familiarity, sex of the caller, and paired status) and gibbons use this information to respond to achieve several nonmutually exclusive functions, including intragroup contact, territorial defense, and pair-bond advertisement and strengthening. However, not all pair-living gibbons duet, and it is unclear whether the same results should be expected in nonduetting species. We conducted song playback experiments (N = 47 trials) to test hypotheses about song functions in nonduetting gibbons on two groups of wild Javan gibbons (Hylobates moloch) in the Gunung Halimun-Salak National Park, Indonesia. Javan gibbons initiated movement toward the speaker more quickly in response to songs broadcast in the center of the territory, stranger songs, and songs of unpaired individuals than to songs at the border, neighbor songs, and songs from paired individuals. These results suggest that Javan gibbons can localize songs, and that Javan gibbon songs transmit information about the identity and paired status of the caller. Our results imply that Javan gibbon solo songs are likely to function for territorial defense and pair-bond advertisement like duets in other primates.