What's the rumpus? Resident temperate forest birds approach an unfamiliar neotropical alarm call across three continents.

Alarm signals have evolved to communicate pertinent threats to conspecifics, but heterospecifics may also use alarm calls to obtain social information. In birds, mixed-species flocks are often structured around focal sentinel species, which produce reliable alarm calls that inform eavesdropping heterospecifics about predation risk. Prior research has shown that Neotropical species innately recognize the alarm calls of a Nearctic sentinel species, but it remains unclear how generalizable or consistent such innate signal recognition of alarm-calling species is. We tested for the responses to the alarm calls of a Neotropical sentinel forest bird species, the dusky-throated antshrike (Thamnomanes ardesiacus), by naive resident temperate forest birds across three continents during the winter season. At all three sites, we found that approaches to the Neotropical antshrike alarm calls were similarly frequent to the alarm calls of a local parid sentinel species (positive control), while approaches to the antshrike's songs and to non-threatening columbid calls (negative controls) occurred significantly less often. Although we only tested one sentinel species, our findings indicate that temperate forest birds can recognize and adaptively respond globally to a foreign and unfamiliar tropical alarm call, and suggest that some avian alarm calls transcend phylogenetic histories and individual ecological experiences.

Red-winged blackbirds nesting nearer to yellow warbler and conspecific nests experience less brood parasitism.

In functionally referential communication systems, the signaler's message intended for a conspecific receiver may be intercepted and used by a heterospecific eavesdropper for its own benefit. For example, yellow warblers (Setophaga petechia) produce seet calls to warn conspecifics of nearby brood parasitic brown-headed cowbirds (Molothrus ater), and red-winged blackbirds (Agelaius phoeniceus) eavesdrop on and recruit to seet calls to mob the brood parasites. Prior work found that warblers nesting closer to blackbirds were less likely to be parasitized, suggesting that blackbirds may even be the target of warbler's seet calls to assist with antiparasitic defense. Here we discovered for the reverse to apply too: blackbirds nesting closer to yellow warblers also experienced lower probability of brood parasitism. Concurrently, we also found that blackbirds nesting closer to other blackbirds also experience lower parasitism rates. Although these are strictly correlational results, they nonetheless suggest that blackbirds are better able to defend their nest against cowbirds when also listening to nearby warblers' referential alarm calls.

Referential alarm calling elicits future vigilance in a host of an avian brood parasite.

Yellow warblers (Setophaga petechia) use referential 'seet' calls to warn mates of brood parasitic brown-headed cowbirds (Molothrus ater). In response to seet calls during the day, female warblers swiftly move to sit tightly on their nests, which may prevent parasitism by physically blocking female cowbirds from inspecting and laying in the nest. However, cowbirds lay their eggs just prior to sunrise, not during daytime. We experimentally tested whether female warblers, warned by seet calls on one day, extend their anti-parasitic responses into the future by engaging in vigilance at sunrise on the next day, when parasitism may occur. As predicted, daytime seet call playbacks caused female warblers to leave their nests less often on the following morning, relative to playbacks of both their generic anti-predator calls and silent controls. Thus, referential calls do not only convey the identity or the type of threat at present but also elicit vigilance in the future to provide protection from threats during periods of heightened vulnerability.

Heterospecific eavesdropping on an anti-parasitic referential alarm call.

Referential alarm calls occur across taxa to warn of specific predator types. However, referential calls may also denote other types of dangers. Yellow warblers (Setophaga petechia) produce "seet" calls specifically to warn conspecifics of obligate brood parasitic brown-headed cowbirds (Molothrus ater), which lay their eggs in the warblers' and other species' nests. Sympatric hosts of cowbirds that do not have referential alarm calls may eavesdrop on the yellow warbler's seet call as a warning system for brood parasites. Using playback presentations, we found that red-winged blackbirds (Agelaius phoeniceus) eavesdrop on seet calls of yellow warblers, and respond as much to seet calls as to cowbird chatters and predator calls. Red-winged blackbirds appear to eavesdrop on seets as warning system to boost frontline defenses on their territories, although they do not seem to perceive the warblers' seets as a cue for parasitism per se, but rather for general danger to the nest.

Neural mechanisms of auditory species recognition in birds.

Auditory communication in humans and other animals frequently takes place in noisy environments with many co-occurring signallers. Receivers are thus challenged to rapidly recognize salient auditory signals and filter out irrelevant sounds. Most bird species produce a variety of complex vocalizations that function to communicate with other members of their own species and behavioural evidence broadly supports preferences for conspecific over heterospecific sounds (auditory species recognition). However, it remains unclear whether such auditory signals are categorically recognized by the sensory and central nervous system. Here, we review 53 published studies that compare avian neural responses between conspecific versus heterospecific vocalizations. Irrespective of the techniques used to characterize neural activity, distinct nuclei of the auditory forebrain are consistently shown to be repeatedly conspecific selective across taxa, even in response to unfamiliar individuals with distinct acoustic properties. Yet, species-specific neural discrimination is not a stereotyped auditory response, but is modulated according to its salience depending, for example, on ontogenetic exposure to conspecific versus heterospecific stimuli. Neuromodulators, in particular norepinephrine, may mediate species recognition by regulating the accuracy of neuronal coding for salient conspecific stimuli. Our review lends strong support for neural structures that categorically recognize conspecific signals despite the highly variable physical properties of the stimulus. The available data are in support of a 'perceptual filter'-based mechanism to determine the saliency of the signal, in that species identity and social experience combine to influence the neural processing of species-specific auditory stimuli. Finally, we present hypotheses and their testable predictions, to propose next steps in species-recognition research into the emerging model of the neural conceptual construct in avian auditory recognition.

How canaries listen to their song: Species-specific shape of auditory perception.

The melodic, rolling songs of canaries have entertained humans for centuries and have been studied for decades by researchers interested in vocal learning, but relatively little is known about how the birds listen to their songs. Here, it is investigated how discriminable the general acoustic features of conspecific songs are to canaries, and their discrimination abilities are compared with a small parrot species, the budgerigar. Past experiments have shown that female canaries are more sexually responsive to a particular song element-the "special" syllables-and consistent with those observations, it was found that special syllables are perceptually distinctive for canaries. It is also shown that canaries discriminate the subtle differences among syllables and phrases using spectral, envelope, and temporal fine structure cues. Yet, while canaries can hear these fine details of the acoustic structure of their song, the evidence overall suggests that they listen at a more global, phrase by phrase level, rather than an analytic, syllable by syllable level, except when attending to some features of special syllables. These results depict the species-specific shape of auditory perception in canaries and lay the groundwork for future studies examining how song perception changes seasonally and according to hormonal state.

Relative salience of syllable structure and syllable order in zebra finch song.

There is a rich history of behavioral and neurobiological research focused on the 'syntax' of birdsong as a model for human language and complex auditory perception. Zebra finches are one of the most widely studied songbird species in this area of investigation. As they produce song syllables in a fixed sequence, it is reasonable to assume that adult zebra finches are also sensitive to the order of syllables within their song; however, results from electrophysiological and behavioral studies provide somewhat mixed evidence on exactly how sensitive zebra finches are to syllable order as compared, say, to syllable structure. Here, we investigate how well adult zebra finches can discriminate changes in syllable order relative to changes in syllable structure in their natural song motifs. In addition, we identify a possible role for experience in enhancing sensitivity to syllable order. We found that both male and female adult zebra finches are surprisingly poor at discriminating changes to the order of syllables within their species-specific song motifs, but are extraordinarily good at discriminating changes to syllable structure (i.e., reversals) in specific syllables. Direct experience or familiarity with a song, either using the bird's own song (BOS) or the song of a flock mate as the test stimulus, improved both male and female zebra finches' sensitivity to syllable order. However, even with experience, birds remained much more sensitive to structural changes in syllables. These results help to clarify some of the ambiguities from the literature on the discriminability of changes in syllable order in zebra finches, provide potential insight on the ethological significance of zebra finch song features, and suggest new avenues of investigation in using zebra finches as animal models for sequential sound processing.

Acoustic fine structure may encode biologically relevant information for zebra finches.

The ability to discriminate changes in the fine structure of complex sounds is well developed in birds. However, the precise limit of this discrimination ability and how it is used in the context of natural communication remains unclear. Here we describe natural variability in acoustic fine structure of male and female zebra finch calls. Results from psychoacoustic experiments demonstrate that zebra finches are able to discriminate extremely small differences in fine structure, which are on the order of the variation in acoustic fine structure that is present in their vocal signals. Results from signal analysis methods also suggest that acoustic fine structure may carry information that distinguishes between biologically relevant categories including sex, call type and individual identity. Combined, our results are consistent with the hypothesis that zebra finches can encode biologically relevant information within the fine structure of their calls. This study provides a foundation for our understanding of how acoustic fine structure may be involved in animal communication.