Avian Vocalizations

• Function of vocalizations – calls versus songs – vocabulary • Anatomy/neurology • Song Building • Spectrographic Examples

Songs versus Calls

• Songs are more musical- • Calls are rather brief, complex, loud, relatively simple in structure, and long quieter – Identification of sexual – Warning calls identity in monomorphic species – Feeding calls – Attract mates – Predator mobbing – Establish territory – Migratory communication – Synchronize courtship – Social behavior – Injury – Individual identification – Others??? – Teaching song to young – Others??? Vocabulary of Calls

• Mobbing Calls – Robin, Tufted Titmouse, Black-capped Chickadee; Blue Jay, House Wren, Tufted Titmouse • Flight Calls—American Goldfinch • Migratory Calls, Nocturnal Veery, Swainson’s Thrush, Bobolink

Superb Lyrebird Signals and Songs Minute 45:30 2.5 min. Neurology of Song

• Controlled by left hemisphere of brain • Neural pathways are stimulated by exposure to song – Hormonal control (testosterone) • Song is somewhat fixed in most species; improvisation does occur • Size of neural center is proportional to complexity of song

Evolution of Song

Order Passeriformes—Perching Birds Suborder Tyranni--Sub-Oscines—Tyrant Flycatchers Eastern Phoebe, Eastern Kingbird, Cotingas, Antbirds, Manakins

Suborder Passeri--Oscines—Songbirds Parvorder Corvida (Crows) Jays, Ravens, Lyrebirds, most Australian Bird lineages Parvorder Songbirds Thrushes, Warblers, Sparrows, Orioles, Cardinals, Finches, Chickadees, Nuthatches, etc.

New World Parvorder Parvorder Flycatchers Corvida Passerida

Crows, Jays, Magpies

Songbirds—thrushes, warblers, Flycatchers, Peewee, vireos, chickadees, nuthatches, Kingbirds & Phoebe, orioles, blackbirds, finches . .

Order Passeriformes New World Parvorder Parvorder Flycatchers Corvida Passerida

Song is learned Considerable geographic variation Complex syrinx Order Passeriformes

Ancestral Condition of Song Song is innate Limited geographic variation Simple syrinx Anatomy of Song

• Humans • Birds – LARYNX, hardened – SYRINX, elastic membranes cartilaginous region located located within the chest high in the trachea cavity at the junction of trachea and primary bronchia – In song birds, the syrinx is associated with many pairs of muscles Slow Motion Song and Brown-headed Cowbird Minute 31:40 of Signals and Songs-2.5 min. Anatomy of Song

TRACHEA

SYRINX (double-fluted)

PRIMARY BRONCHI Structure of SYRINX

Syringeal muscles

Semilunar Membrane

Internal and External Labia Internal and External Tympaniform Membranes

Interclavicular Air Sac Sound Production

Rushing air vibrates tympaniform membranes like a drum. Muscles surrounding the syrinx can change its shape. Constriction of labia and semilunar membrane alter air flow. Pressure in interclavicular air sac is necessary to produce sound.

Two halves of syrinx operate independently; creates complex simultaneous notes Development of Avian Song

• Critical Learning Period—early life of bird up to 1 year, bird is exposed to correct song and information is stored in neural center of brain

• Silent Period—syllables of song remain stored without practice or rehearsal Development of Avian Song

• Subsong Period—vocal play; unstructured song is practiced notes at a time. Practicing bird matches notes with those stored in memory.

• Song Crystallization—bird practices and perfects notes; organizes notes into the correct pattern and timing. – Improvisation, imitation, and invention occurs – Neural pathways are completed; auditory feedback is not necessary Haesler et al. 2007. Incomplete and Inaccurate Vocal Imitation after Knockdown of FoxP2 in Songbird Basal Ganglia Nucleus Area X. PLoS Biology 5:1-13.

• Forkhead Box Transcription Factor (FOXP2) – Mutations in humans cause developmental verbal dyspraxia; abnormal speech patterning and comprehension of grammar – Manifested through structural and functional abnormalities of basal ganglia Knockdown of FOXP2 in Zebra Finch Area X

• Area X of brain is where song learning occurs • Virus mediated RNA Interference – Complementary mRNA binds to FOXP2 transcript – FOXP2 protein is not translated • Injected control and experimental virus on 23 days after hatching • GFP shows virus infected cells Knockdown of FOXP2 in Zebra Finch Area X

• RNA interference reduced expression of FOXP2 in experimental subjects

Knockdown of FOXP2 in Zebra Finch Area X

• Experimental birds (shFOXP2) copied songs of tutor with less precision and context than control birds.

• FOXP2 is a developmental gene involved in vocal acquisition; This gene and its function is similar in both birds and mammals Spectrographic Analysis of Bird Songs

Shows pitch of vocalization 10.0 Complexity---harmonics, number of notes Identifications—species, individuals

5.0 Frequency (khz) Frequency

0.0 0 0.5 1.0 1.5 2.0 Time (sec) Spectrograph of Red-eyed Vireo (Vireo olivaceus) White-throated Sparrow Winter Wren Northern Mockingbird Wood Thrush Spectrograph of Bobolink (Dolichonyx orzivorous) Field Sparrow (Spizella pusilla)

Song Sparrow (Melospiza melodia)

Savannah Sparrow (Passerculus sandwichensis) Individual Song Variation in Savannah Sparrows from Cortland County

Savannah sparrow1 Savannah sparrow5 Savannah sparrow6 Non-vocal Bird Sounds

Ruffed Grouse (Bonasa umbellus)---wing drumming Non-vocal Bird Sounds

American Woodcock (Scolopax minor) Courtship Flight

Winnowing of Wilson’s Snipe Track 15 Non-vocal Bird Sounds

Yellow-bellied Sapsucker (Sphyrapicus varius) Drumming Rose et al. 2004. Species-typical songs in white-crowned sparrows tutored with only phrase pairs. Nature 432:753-758.

• Hypothesis: song is constructed by exposure to combination specific and ordered phrase pairs, rather than exposure to entire song, during the critical learning period.

White-crowned Sparrow Song & Tutor Phrases Used

WCS song has five distinct phrases and plenty of variation between individuals. Tutor Phrases

10-14 day old nestlings were exposed to either forward ordered phrase pairs or reverse-ordered phrase pairs.

All phrases were temporally isolated by 10 minute intervals.

What do nestlings exposed to single isolated phrases sing as adults? • Exposure phrases – E, D, C, B, A

• Birds were unable to develop species typical complete song Paired Phrase Tutoring Forward Order Presentation • DE, CD, BC, AB phrase tutoring

• Birds crystallized a full species typical song in proper order Paired Phrase Tutoring Reverse Order Presentation • BA, CB, DC, ED phrase tutoring

• Birds crystallized a full reverse-ordered song Significance

• Phrase pairs represent the minimum sequence information for developing a complete song • Reverse order presentation during critical learning can overcome innate tendency to sing forward order song • Illustrates interaction between exposure and playback (crystallization) phases of song development – Interaction between song-system neurons and song centers in forebrain Yamaguchi, A. 2001. Sex differences in vocal learning in birds. Nature 411: 257-258.

• Northern Cardinal (Carduelis carduelis) is one of a few species where both sexes sing • 40-44 tutored songs played over 1 year period according to a schedule • Identify sensitive period

Sex differences in vocal learning.

• Mean sensitive period (yellow bars) is significantly lower for female cardinals • AH—female cardinals learn songs faster than male cardinals—no surprise here Sex Differences in Vocal Learning Other Differences • Male cardinals learn more songs • Isolated males will improvise near-normal cardinal songs • Isolated females will not develop song— must learn songs Flight Calls Methods of Examining Nocturnal Migration

• Nocturnal migrants routinely call during flight • Flight calls, generally high frequency and short (< 100 ms) • Species specific Nocturnal Flight Call Examples