Bird communication

Birds produce a variety sounds to communicate with flock members, mates (or potential mates), neighbors, & family members. These sounds vary from short, simple call notes (and short, simple songs like those of Henslow's Sparrows) . . .

The syrinx is located at the point where the trachea branches into the two primary bronchi. According to one model of syrinx function, sound is generated when:

Characteristics of the sound (e.g., frequency) are influenced by vibrations of the internal tympaniform membrane (ITM). The 'characteristics' of the ITM (e.g., degree to which the membrane protrudes into the air pathway), in turn, are influenced by pressure in the interclavicular air sac (or, as in the diagram above, clavicular air sac) (Gill 1995). Syringeal muscles also influence air flow and the characteristics of sound (Gill 1995):

Each song syllable is accompanied by coordinated movements of the larynx and cornua that maintain an inverse relationship between
the size of the oropharyngeal–esophageal cavity and the song’s fundamental frequency. Left, Lateral view of cardinal showing the dorsoventral
movement (LV) of the larynx from the middle of the second cervical vertebra and its craniocaudal movement (LH) from the dorsal edge of the
beak-skull transition. Right, Ventrodorsal view showing distance between lateral cornua of hyoid apparatus (Cornua).

Different circuits (or impulse pathways) in the brain control song production (posterior descending pathway) and song learning (anterior forebrain pathway). Song production is controlled via a pathway beginning in the brain & travelling to the syrinx:

The 'learning pathway' connects the HVC to RA via areas X, DLM, and LMAN. This forms a recursive loop because the neurons in LMAN also project to area X. Disturbances to this pathway affect song development, but not the production of song in adult males.

Testosterone (and melatonin; see below) appear to play some role in song production. For example:

In songbirds, males and females may have distinctly different brain structures, specifically in those areas involved in the production of song. In many songbirds, males sing while females do not (or sing very little). The ability to sing is controlled by six different clusters of neurons (nuclei) in the avian brain (see diagrams below). Neurons connect each of these regions to one
another. In male songbirds, these nuclei can be several times larger than the corresponding cluster of neurons in females, and in some species (e.g., Zebra Finches), females may lack one of these regions (area X) entirely (Arnold 1980, Konishi and Akutagawa 1985).

Slaty-tailed Trogon calling
(Mayflower Bocawina National Park - Belize)

The functions of bird song may vary among species. Some known & hypothesized functions include:

Birds Reveal their Personality when Singing -- Individual differences in social behavior may have consequences for mate choice and sexual signalling, because partners should develop preferences for personalities that maximize reproductive output. Here we propose that behavioural traits involved in sexual advertisement may serve as good indicators of personality, which is fundamental for sexual selection to operate on temperament. Bird song has a prominent and well-established role in sexual selection, and it displays considerable variation among individuals with a potentially strong personality component.

In a field study of free-living male Collared Flycatchers (Ficedula albicollis), Garamszegi et al. (2008) characterized personality based on the exploration of an altered breeding environment, and based on the risk taken when a potential predator was approaching during a simulated territorial interaction. They found that explorative and risk-taker individuals consistently sang at lower song posts than shy individuals in the presence of a human observer. Moreover, males from lower posts established pair-bonds relatively faster than males from higher posts.

These results may demonstrate that risk taking during singing correlates with risk taking during aggression and with exploration, thus personality may be manifested in different contexts involving sexual advertisement. These findings are in accordance with the hypothesis that the male's balance between investment in reproduction and risk taking is reflected in sexual displays, and it may be important information for choosy females that seek partners with personality traits enhancing breeding success.

Collared Flycatcher

Side, front and back thermal images of a singing canary. The images are colour coded to show temperature
increasing from 15°C (dark blue) through green (22°C), yellow (25°C) and red (30°C) to 32°C (white). The black lines
delineate the head, body, leg and tail sections of the bird (From: Ward and Slater 2005).

Energetic cost of singing - Sexually selected displays, such as male passerine bird song, are predicted to be costly. However, most measurements calculated the rate of oxygen consumption during singing using respirometry have shown that bird song has a low energetic cost. Because birds are reluctant to sing when enclosed inside a respirometry chamber, the energetic cost of singing could differ from that under more normal circumstances. Ward and Slater (2005) used heat transfer modelling, based on thermal images, to estimate the energetic cost of singing by Canaries (Serinus canaria) that were not enclosed in respirometry chambers. Metabolic rate calculated from heat transfer modelling was 14% greater than during standing, suggesting that song production appears to be metabolically cheap for passerine birds and the metabolic cost small enough that it is unlikely represents an important fitness cost under circumstances favorable for energy balance. However, cost will increase as the temperature decreases.

Territory establishment and defense
Motivation and Fitness - Birds may provide information to conspecifics by way of variation in (Becker 1982):

singing rates

may increase during aggressive encounters
may be higher in higher quality males

song duration - may increase or decrease (depending on the species) during conflict situations
song amplitude (or volume) may decrease during aggressive encounters
song frequency - may increase during conflict situations (e.g., Indigo Buntings; Thompson 1972)
song complexity - songs may consist of more or fewer elements during conflict situations (e.g., male Blue Grosbeak utter songs with more syllables during aggressive encounters with other males)

Distraction of potential predators (e.g., Common Yellowthroat flight song)
Coordination of activities
Stimulate females
Attract females for extra-pair copulations
Mate guarding

Song complexity and the avian immune system -- There are three hypotheses to explain how the evolution of parasite virulence could be linked to the evolution of secondary sexual traits, such as bird song. First, female preference for healthy males in heavily parasitized species may result in extravagant trait expression. Second, a reverse causal mechanism may act, if sexual selection affects the coevolutionary dynamics of host-parasite interactions by selecting for increased virulence. Third, the immuno- suppressive effects of ornamentation by testosterone or limited resources may lead to increased susceptibility to parasites in species with elaborate songs. Assuming a coevolutionary relationship between parasite virulence and host investment in immune defense, Garamszegi et al. (2003) used measures of immune function and song complexity to test these hypotheses in passerine birds. Under the first two hypotheses, they predicted avian song complexity to be positively related to immune defense among species, whereas this relationship was expected to be negative if immuno-suppression was at work. They found that adult T-cell mediated immune response and the relative size of the bursa of Fabricius were both positively correlated with song complexity, even when potentially confounding variables were held constant. These results are consistent with the hypotheses that predict a positive relationship between song complexity and immune function, thus indicating a role for parasites in sexual selection.

Regression of short-term song complexity (number of
unique syllables within songs/song length) on T-cell
mediated immune response, after removing allometric
effects by using residuals after controlling for body
mass. Datapoints are phylogenetically independent
linear contrasts (N = 38). The line and equation are from
linear regression forced through the origin.

Song differences of Great Tits at urban and forest sites. (A) Every urban site had a higher minimum frequency than its forest companion site. (B) The minimum frequency (+ SE) varies with note number, and the habitat-dependent spectral divergence remained distinct irrespective of number of notes. Squares = songs from cities; triangles = songs from forest. (C) Minimum frequency correlated between sites of a pair without a strong, larger-scale geographic pattern of isolation by distance. City-forest pairs are labeled by city name. The line of equal values for city-forest pairs in is the top-left corner. (D) Every urban site had a shorter note length than its forest companion site. (E) The duration of the first note varied with note number, but the habitat-dependent temporal divergence remained distinct, especially for the note numbers with substantial sample sizes. Squares = songs from cities; triangles = songs from forest. (F) Duration of the first note did not correlate between sites of a pair, nor was there a larger-scale geographic structure. City-forest pairs are labeled by city name. The line of equal values for city-forest pairs in is the bottom-right corner.

Cities change the songs of birds -- Worldwide urbanization and the ongoing rise of urban noise levels form a major threat to living conditions in and around cities. Urban environments typically homogenize animal communities, and this results, for example, in the same few bird species' being found everywhere. Insight into the behavioral strategies of the urban survivors may explain the sensitivity of other species to urban selection pressures. Slabbekoorn and den Boer-Visser (2006) showed that songs that are important to mate attraction and territory defense have significantly diverged in Great Tits (Parus major), a successful urban species. Urban songs were shorter and sung faster than songs in forests, and were often atypical song types. The authors also found consistently higher minimum frequencies in ten out of ten city-forest comparisons from London to Prague and from Amsterdam to Paris. Anthropogenic noise is most likely a dominant factor driving these dramatic changes. These data provide the most consistent evidence supporting the acoustic-adaptation hypothesis since it was postulated in the early seventies. At the same time, they reveal a behavioral plasticity that may be key to urban success and the lack of which may explain detrimental effects on bird communities that live in noisy urbanized areas or along highways.

In some species, females also sing. This is particularly true in the tropics (see 'duetting' below). Singing by females may be important in:

territory defense (particularly in keeping other females out of a territory)
pair-bonding
mate guarding
reproductive synchronization

When do female birds sing? Hypotheses from experimental studies (Langmore 1998).

(a) The song of a female Superb Fairy-wren. Females use songs to defend their territories against both
males and females. (b) The song of a female Alpine Accentor. Female Alpine Accentors sing to attract males, and
the complexity of their songs increases with age. This song was recorded from a two-year-old female (Langmore 1998).

Singing by female Northern Cardinals -- Yamaguchi (2001) found that female Northern Cardinals learn to sing three times faster than males - the most dramatic example of learning disparities between male & female animals found to date. She collected nestling cardinals & raised them in sound chambers with microphones and speakers that play back the songs of adult cardinals. It takes about a year for a cardinal to learn to sing, and young songbirds learn by imitating adults. During the early sensitive phase, young don’t sing, but listen to singing adults to memorize their songs. Then the practicing begins. “Their initial attempts are pretty miserable,” she says, “but they practice & practice until it matches the memory that was formed earlier during the sensitive phase.”

Source: http://www.flmnh.ufl.edu

Yamaguchi (1998) also analyzed songs and found that females sing with more overtones, creating a slightly nasal sound. Young males also go through a nasal, warbly phase as their testosterone kicks in, but it’s as though the females continue to sing with an adolescent male’s voice. More important, Yamaguchi (2001) discovered that female cardinals memorize adult songs three times faster than males. While both sexes ultimately learned the same number of song types, the females’ sensitive phase was only a third as long as the males’. The different learning rates may reflect an evolutionary adaptation. Like other songbirds, juvenile cardinals disperse from their parents’ territory about 45 days after hatching to establish their own turf before their first breeding season. Away from their natal nest, the young cardinals are suddenly immersed in the new song dialects of other adult cardinals. It appears that females lose the ability to learn new dialects when they disperse, while males are able to learn them and “fit in” with their new neighbors.

“ It might be that males retain the ability to learn songs longer than females so that they can have a better chance of establishing territory in a new area,” Yamaguchi says. “For males, song-matching and fitting into the crowd in a new place are really important, while they’re not for females.” It’s not clear why female cardinals have a shorter window of vocal learning, she says, but then again, “we don’t really know why females sing at all, or how they use their songs.” One hypothesis, she says, is that females sing as a species identification tool, a greeting card to male cardinals that says, “I’m an eligible mate; come court me.” Other researchers have proposed that female cardinals sing to shoo away brightly colored mates from the nest, warning the males not to attract attention to the vulnerable chicks. “I know that female cardinals also use songs in aggressive behavior,” Yamaguchi says. “I’ve seen females battling each other in the field, and they’re singing the whole time as they bang into each other.”

Singing male Northern Cardinal

Early bird: the European Robin starts singing over an hour before some of its neighbors (Photo by S. Crawford)

Early birds have big eyes -- Birds with large eyes begin singing earlier in the morning than their small-eyed neighbors because they can see better in low light. So say British researchers explaining why, on a spring day in Welsh woodland, robins and redstarts pipe up a good hour and a half before chaffinches and blue tits. The keen-sighted early birds probably do get the worms. Big eyes may help the hunt for breakfast, speculates Robert Thomas from the University of Bristol, who led the study (Thomas et al. 2002). Birdsong is an acoustic advertisement. Birds use it to attract mates and defend territory. But singing also alerts predators. So a bird does not sing before it can see well enough to spot approaching danger, speculates Thomas. Yet a bird also does not want to waste time crooning when the sun is high enough to search for food. The earlier it can see to sing, the earlier it can see to start foraging. The link between the dawn chorus and eye size was first mooted in the 1960s, but this is the first time that it has been tested. Previous data was very confusing, says Graham Martin, who works on birds' senses at the University of Birmingham, UK. Thomas's team measured light levels and the times at which 57 different bird species began singing at various sites across Britain and Europe. When they measured the diameter of each bird's exposed eye surface, they realized that big-eyed birds sing earlier than those of the same body size but with smaller eyes. They also found that small birds sing earlier than large birds with the same-sized eyes as them. One explanation for this may be hunger. Small birds cannot store as much food overnight and they use up energy more quickly than large birds. "Only large birds can afford to take it easy," says Thomas Szekely, another member of the research team. "Small birds may sing earlier because they have to get up earlier to search for food." -- Natasha McDowell, Nature Science Update

Song Variation

Locally distinct versions of song (or song 'dialects') have been described in several species. Hypotheses to explain dialects include:

Historical hypothesis - Because vocal dialects are the result of song learning, geographical variation in song may simply reflect recent history. New 'dialects' develop when birds (who sing particular songs or song types) colonize new areas (Gill 1995).
Racial specialization, or ecological, hypothesis - Song dialects reflect the genetics of local populations. Females may make mate choice decisions based on a male's dialects and young males may establish territories in particular areas based on the dialects of resident male. If so, dialect boundaries may represent 'genetic' boundaries, with birds in a particular 'dialect area' genetically 'adapted' to that particular area. This may be the case in certain populations of White-crowned Sparrows in the western United States.
Social adaptation hypothesis - Dialects develop when young males dispersing into an area learn the songs of established males. For example, in Indigo Buntings, young males that sing like their neighbors have greater reproductive success (Payne 1982).

Song Repertoires

In many species of songbirds, including Northern Cardinals, Carolina Wrens, and many others, males possess repertoires of song types. These repertoires typically consist of perhaps 6 - 12 song types, but may range anywhere from 2 to an apparently unlimited number (as in, for example,Northern Mockingbirds). Interestingly, however, males in other species, such as Common Yellowthroats, have just one song. Repertoires of song types may have a variety of functions:

Each song type has a different meaning
Advertise quality (more song types = better quality)
Permit more effective communication with conspecific males (i.e., matching the song types of neighbors)
Prevent 'exhaustion' of nerves & muscles
Prevent habituation

Northern Mockingbird

Relationships between a male song sparrow's song repertoire size and mean kinship (k_m) with the female population. Males with larger song repertoires were less closely related to the female population, including all females in the set of potential mates (open symbols, dashed line) and excluding close female relatives of each focal male (filled symbols, solid line). Regression lines are shown for clarity.

Secondary sexual ornamentation and non-additive genetic benefits of female mate choice -- Ornamental secondary sexual traits are hypothesized to evolve in response to directional mating preferences for more ornamented mates. Such mating preferences may themselves evolve partly because ornamentation indicates an individual's additive genetic quality (good genes). While mate choice can also confer non-additive genetic benefits (compatible genes), the identity of the most 'compatible' mate is assumed to depend on the choosy individual's own genotype. It is therefore unclear how choice for non-additive genetic benefits could contribute to directional mating preferences and consequently the evolution of ornamentation. In free-living Song Sparrows (Melospiza melodia), Reid (2007) found that individual males varied in their kinship with the female population. Furthermore, a male's song repertoire size, a secondary sexual trait, was negatively correlated with kinship such that males with larger repertoires were less closely related to the female population. The smaller repertoires of more closely-related males probably represents direct inbreeding depression in the expression of this secondary sexual trait. After excluding close relatives as potential mates, individual females were on average less closely related to males with larger repertoires. Therefore, female Song Sparrows expressing directional preferences for males with larger repertoires would on average acquire relatively unrelated mates and produce relatively outbred offspring. Such non-additive genetic fitness benefits of directional mating preferences, which may reflect genetic dominance variance expressed in structured populations, should be incorporated into genetic models of sexual selection.

Song sharing (Beecher and Brenowitz 2005) -- Song sharing is common in songbirds and is found in a variety of social contexts, not only in territorial neighbors (the most commonly studied context), but also in lekking species and communal breeders. Song sharing in the neighbor context is best understood in the context of the Dear Enemy hypothesis. According to this hypothesis,

long-term neighbors are preferred to newcomers because newcomers are inherently expansionist, whereas old neighbors generally respect territory boundaries once they have been mutually established. Neither preferring nor cooperating with familiar neighbors requires shared songs, but shared songs are a reliable signal (a ‘badge’) of familiarity or locality because they must be learned in the local neighborhood. Consistent with this hypothesis, Wilson and Vehrencamp (2001) found that neighboring Song Sparrows sharing fewer songs were more aggressive with one another than were neighbors sharing more songs.
A corollary of the Dear Enemy hypothesis for territorial songbirds is that established neighbors should use their songs in place of time- and energy-costly physical interactions to minimize unnecessary territorial conflicts. Playback studies of Song Sparrows and Banded Wrens have supported this prediction. Even when neighbors do not share any song types (with respect to the investigators' criterion), they might still be able to song match using songs in their repertoires that they perceive as being most similar.

Song learning

Avian vocalizations can be inherited, learned, or invented. In some species, like Brown-headed Cowbirds, males develop normal songs even when raised in acoustic isolation. However, for most species of songbirds, at least some aspects of their singing behavior is learned. That learning, though, is guided by inherited (innate) mechanisms.

Stages of song development (birds with fixed repertoires):

1 - Critical learning period

information stored for later use
usually less than a year in duration, & may be much shorter than that (e.g., 2 months for Marsh Wrens)
often extends into the 1st breeding season (giving young males a chance to learn from experienced, neighboring males)

2 - Silent period

song components that have been memorized during learning period are stored in the brain
up to 8 months in duration

3 - Subsong period

period of practice without communication (vocal play?)
birds utter low volume, unstructured notes initially &, in a few weeks, sounds become more like the species-specific song
First attempts to actually sing (plastic song); birds continue to alter song structure (e.g., here's a song of an adult Canyon Wren . . . and singing by a young wren)

4 - Song crystallization

plastic song becomes increasingly less 'plastic' &, finally, the 'adult (or final) version' of song(s) is(are) sung
in 'crystalized song', birds may use only a fraction of the elements they first learned & practiced

Stages (and duration) of song development in White-crowned Sparrows

Timeline for zebra finch song learning. Young birds first memorize the song of an adult 'tutor' during a
critical period for 'sensory' learning of song. Later, during a 'sensorimotor' learning period, they begin to sing and
gradually match their initially immature vocalizations to the memorized song using auditory feedback. After this learning
process, adult song normally remains unchanging, or 'crystallized'. For zebra finches, the periods of
sensory and sensorimotor learning overlap. Many other species, such as the white-crowned sparrow, do not crystallize
song until close to one year of age, and have a much clearer separation between the sensory and sensorimotor
learning periods. Still other species, such as the canary, seem to reiterate the processes of sensory and sensorimotor
learning each season, perhaps under the regulation of seasonal variability in hormone levels (Brainard and Doupe 2000).

Photomicrographs showing HVC of control (A) and parasitized (B) male Canaries and Robust nucleus of the Archopallium (RA) of control (C) and parasitized (D) birds. HVC was smaller in the parasitized birds (B) compared to the control (A) group, whereas RA showed no reduction in size (C vs. D). Scale bar is 100 mm.

Parasites affect song complexity and neural development in a songbird -- There is now considerable evidence that female choice drives the evolution of song complexity in many songbird species. However, the underlying basis for such choice remains controversial. The developmental stress hypothesis suggests that early developmental conditions can mediate adult song complexity by perturbing investment in the underlying brain nuclei during their initial growth. Spencer et al. (2005) found that adult male Canaries (Serinus canaria), infected with malaria (Plasmodium relictum) as juveniles, develop simpler songs as adults compared to uninfected individuals, and exhibited reduced development of the high vocal center (HVC) song nucleus in the brain. Their results show how developmental stress not only affects the expression of a sexually selected male trait, but also the structure of the underlying song control pathway in the brain, providing a direct link between brain and behavior. This novel experimental evidence tests both proximate and ultimate reasons for the evolution of complex songs and supports the Hamilton–Zuk hypothesis of parasite-mediated sexual selection. Together, these results propose how developmental costs may help to explain the evolution of honest advertising in the complex songs of birds.

Singing in their sleep - Researchers have shown that young birds sleeping at night may be reviewing the songs they've learned during the day (Dave and Margoliash 2000). Normally, the brain is desensitized to outside stimuli during sleep, partly because of changing concentrations of a norepinephrine. But the robustus archistratalis (RA), a

region of the Zebra Finch brain involved in singing, exhibits an increase in neurological activity during sleep. It is generally believed that the activity of the sleeping brain helps to consolidate what was learned during the day, but how this occurs has never been directly shown. Dave and Margoliash (2000) recorded electrical impulses from single neurons in the RA of anesthetized, asleep and awake birds as they listened to recordings of their own songs played back on a computer. Without fail, birds that were asleep or anesthetized exhibited reduced regular oscillations but showed occasional bursts of strong activity in their RA neural impulse patterns. When the birds occasionally woke up during the night, the bursting patterns quickly disappeared and were replaced by the steady oscillating pattern seen during the day. "This is surprising because the same neurons that show no response during the day have these strong responses to the bird's own song when they are asleep. It's possible that songs learned during the day affect the bursting patterns of the RA at night, serving to solidify the newly learned songs in the bird's mind," says Margoliash.

What is learned?

1 - Syllables?

innate in Galliforms, Columbiformes, & suboscines
learned in most oscines studied, but some species can derive syllables from call notes (e.g., begging calls)