Bird Vocalizations 1

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Bird Vocalizations 1
http//ibc.hbw.com/ibc/phtml/votacio.phtml?idVideo
725tipus1 boreal owl
Pygmy Owl (Glaucidium passerinum) hooting
http//people.eku.edu/ritchisong/birdcommunicatio
n.html top of page or about 20 down

• JodyLee Estrada Duek, Ph.D.
• With assistance from Dr. Gary Ritchison
• http//people.eku.edu/ritchisong/parentalcare.html
  

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Birds produce a variety of 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) . . . http//people.eku.edu/ritchisong/b
  irdcommunication.html top(with an occasional
  'buzzy' song of a Grasshopper Sparrow in the
  background)
• . . . to surprisingly long, complex songs (e.g.,
  the Superb Lyrebird with David Attenborough).
• Sometimes birds generate sounds by using
  substrates (like woodpeckers) or special feathers
  (like American Woodcock) or special wings (like
  manakins).
• Red-capped Manakin (Pipra mentalis) using its
  wings to generate sound. http//www.youtube.com/wa
  tch?vT2Bsu4z9Y3k
• Male Anna's Hummingbirds use their tail feathers
  to generate sound.  http//www.youtube.com/watch?v
  K_2JFK-tnnE
• Most sounds, however, are produced by the avian
  vocal organ, the syrinx.
• Common loon http//www.youtube.com/watch?vHw1It3A
  lXmQ

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Syrinx  

• 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
• contraction of muscles (thoracic abdominal)
  force air from air sacs through the bronchi
  syrinx
• the air molecules vibrate as they pass through
  the narrow passageways between the external labia
  the internal tympaniform membranes (or, as in
  the diagram above, tympanic membrane.
• With two separate passageways (and membranes),
  some birds are able to generate two different
  sounds at the same time
• hear a 'self-duet' by a Clay-colored Robin
  http//animaldiversity.ummz.umich.edu/site/resourc
  es/naturesongs/ccro12.wav/view.html(Source Doug
  Von Gausig's webpage at http//www.naturesongs.com
  /costa.html)

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The sound of the song

• Characteristics of the sound (e.g., frequency)
  are influenced by vibrations of the internal
  tympaniform membrane (ITM).
• Superfast syringeal muscles -- Elemans et al.
  (2004) have found that Ring Doves (Streptopelia
  risoria) use "superfast" muscles to make their
  distinctive call. The dove's familiar cooing
  sound includes a trill, which is caused by an
  airflow that makes membranes in the syrinx
  vibrate.
• The quality of sound can be further influenced by
  tracheal length, by constricting the larynx, by
  muscles in the throat, or by the structure and/or
  movements of the bill (e.g., here are some
  complex 'Bird Songs in Slow Motion').
• Although the above model has been generally
  accepted, Goller and Larsen (1997a, 1997b, 1999)
  provide evidence that other structures (not the
  ITM) are the source of sound in both songbirds
  (oscines) and non-songbirds because birds can
  still vocalize when the medium (or internal)
  tympaniform membrane is experimentally kept from
  vibrating.  
• Birdsong sounds sweeter because throats filter
  out messy overtones songbirds adjust the size and
  shape of their vocal tract to 'fit' the changing
  frequency

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Control of the song

• Central motor control 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
• Testosterone (and melatonin) appear to play a
  role in song production
• Autoradiographic studies have shown that the
  neurons of the song-controlling nuclei
  incorporate radioactive testosterone, whereas
  other regions of the brain do not (Arnold et al.
  1976).
• Male Zebra Finches - correlation between the
  amount of song the concentration of serum
  testosterone (Pröve 1978)
• Seasonal changes in testosterone levels
  correlated with seasonal singing patterns
• When testosterone levels are low, decrease in
  song a decrease in size of male-specific brain
  nuclei (Nottebohm 1981).
• In adult Chaffinches, castration eliminates song,
  but injection of testosterone induces such birds
  to sing even in November, when they are normally
  silent (Thorpe 1958).
• Females in some species can be induced to sing by
  injecting them with testosterone (Nottebohm
  1980).

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Spectrograms of hoots from three different male
Scops owls showing the variation in frequency.
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Male quality and owl hoots 1

• The evolution of communication through
  intrasexual selection is expected to lead
  signalers to transmit honest information on their
  fighting ability.
• Hardouin et al. (2007) studied information
  encoded in acoustic structure of territorial
  calls of a nocturnal raptor.
• During territorial contests, male Scops Owls
  (Otus scops) give hoots composed of a downward
  frequency shift followed by a stable plateau.
• Hardouin et al. (2007) found that the frequency
  of the hoot was negatively correlated with the
  body weight of the vocalizer.
• They shifted the frequency of natural hoots to
  create resynthesized calls corresponding to
  individuals of varying body weight and used these
  stimuli in playback experiments simulating an
  intrusion into the territory of established
  breeders.
• Territory owners responded less intensely when
  they heard hoots simulating heavier intruders,
  and males with heavier apparent weight tended to
  give hoots with a lower frequency in response to
  playbacks simulating heavier intruders.

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Male quality and owl hoots 2

• Although the current lack of understanding of the
  mechanisms of voice production in owls limits our
  ability to discuss the bases of this
  relationship, one possibility is that it may
  result from physiological constraints that
  operate during sound production.
• For example, lower-pitch hoots may be more costly
  to produce and/or reflect superior muscular or
  respiratory abilities.
• The relationship between pitch and body weight
  may reflect the fact that heavier,
  better-condition males are also characterized by
  higher testosterone levels, which in turn affect
  the frequency of their vocalizations.
• Indeed, male condition and testosterone levels
  have been shown to positively correlate, and
  higher testosterone levels are typically
  associated with more intense sexual displays.
• Moreover, experimental studies have demonstrated
  that injections of testosterone lower the
  frequency of male calls in birds, e.g., Gray
  Partridges (Perdrix perdrix) and Zebra Finches
  (Taeniopygia guttata).

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Melatonin Shapes Brain Structure In Songbirds

• Springtime's lengthening days spark the growth of
  gonads and a rush of sex hormones that drive
  songbirds to melodic song.
• Bentley et al. (1999) also identified melatonin
  as a critical ingredient that regulates singing
  and fine-tunes the effects of testosterone on the
  brain

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Sexual differentiation of the avian brain

• 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).

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Classification of Bird Sounds 1

• Songs
• primarily under the influence of sex hormones
• generally important in reproduction (e.g.,
  defending territories attracting mates)
• Calls
• generally concerned with coordination of the
  behavior of a pair, family group, or flock (e.g.,
  several vocalizations of Carolina Chickadees)
• not primarily sexual, but important in
  'maintenance' activities, such as foraging,
  flocking, responding to threats of predation
• usually are acoustically simple (e.g., contact
  notes of Northern Cardinals)
• may serve a variety of functions
• location/contact/individual recognition
  Montezuma Oropendola contact calls
• Slaty-tailed Trogon calling http//www.youtube.com
  /watch?vsgBfb9eDx-g (Mayflower Bocawina
  National Park - Belize.. (more))

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Classification of Bird Sounds 2

1. nocturnal flight calls. These calls help birds
   form and maintain in-flight associations, and
   also provide locational information that helps
   flying birds avoid collisions.

Nocturnal flight call of a Black-and-White
Warbler RealAudio AIFF WAV (at 1/6 speed
RealAudio AIFF WAV) Video of Black-and-white
Warbler at Mayflower Bocawina National Park,
Belize ... http//www.youtube.com/watch?vKsvo29-
Sw08
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Classification of Bird Sounds 3

• Sonograms of distress calls from six species.
• Sooty- capped Bush-Tanager,
• (b) Black-capped Flycatcher, 
• (c) Green Violet-ear (pictured below),
• (d) Gray-breasted Wood- Wren,
• (e) Streak-breasted Treehunter, and 
• (f) Yellowish Flycatcher.
• Each sonogram represents  1 sec of distress
  calling. 

1. distress (Listen to a Downy Woodpecker distress
   call)

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Distress Calls of Birds in a Neotropical Cloud
Forest 1

• Neudorf and Sealy 2002 -- Distress calls are
  loud, harsh calls given by some species of birds
  when they are captured by a predator or handled
  by humans.
• recorded the frequency of distress calls in 40
  species of birds captured in mist nets during the
  dry season in a Costa Rica cloud forest.
• They tested the following hypotheses proposed to
  explain the function of distress calls
• calling for help from kin or reciprocal
  altruists
• (2) warning kin
• (3) eliciting mobbing behavior
• (4) startling the predator
• (5) distracting the predator through attraction
  of additional predators.

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Distress Calls of Birds in a Neotropical Cloud
Forest 2

• results did not support calling-for-help, warning
  kin, or mobbing hypotheses.
• genera that regularly occurred with kin or in
  flocks were not more likely to call than
  non-flocking genera.
• no relationship between calling frequency and
  struggling behavior as predicted by the predator
  startle hypothesis.
• Larger birds tended to call more than smaller
  birds, providing some support for both the
  predator distraction and predator startle
  hypotheses.
• Calls of higher amplitude may be more effective
  in startling the predator.
• Distress calls of larger birds may also travel
  greater distances than those of smaller birds,
  supporting the predator manipulation /
  distraction hypothesis.
• The adaptive significance of distress calls
  remains unclear as past studies have generated
  conflicting results.
• While more playback experiments are necessary to
  determine if calls indeed attract other
  individuals or predators, these results suggest
  that distress calls do not function to attract
  helpers or mobbers but are more likely directed
  toward predators.

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Classification of Bird Sounds 4

• feeding
• aggression
• courtship
• copulation or post-copulatory (e.g., see 'Calls'
  section of this account of Broad-winged Hawks and
  this description of copulation in Burrowing Owls)
  
• begging (e.g., young Downy Woodpeckers while
  being fed)
• Kookaburra nest http//www.youtube.com/watch?vwRu
  hApDLzrE
• alarm (aerial predator vs. ground predator)  for
  an example of crow alarm calls check
  http//www.crows.net/analysis.html also listen
  to the alarm call of a Masked Antpitta, Hylopezus
  auricularis

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Alarm calls

• Domestic Chicken - aerial predator alarm call
• Domestic Chicken - ground predator alarm call

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Alarm calls

• White-breasted wood wren http//www.youtube.com/wa
  tch?vnyDZRvn_U0A

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Chickadee language 1

• Black-capped Chickadees (Poecile atricapilla)
  have a complex language for warning flock-mates
  about predators.
• It was already known that chickadees utter a
  high-pitched "seet" when a predator was overhead,
  and used their "chick-a-dee" call to, among other
  things, alert flock-mates to mob a threatening
  bird that was perched.
• However, Templeton et al. (2005) put flocks of
  six chickadees in an enclosure and recorded their
  responses.
• In the presence of a harmless quail, chickadees
  gave no alarm.
• But when a tethered raptor (hawk or owl) entered
  the cage, the alarms began.
• Alarms were more frequent when Saw-whet and Pygmy
  owls were present.
• But the alarms also had a different sound.
• In the presence of small predators, the
  chickadees tacked an average of four "dees" to
  their call "chick-a-dee-dee-dee-dee."
• When the larger, but less dangerous, Great Horned
  Owl was present, they used two dees
  "chick-a-dee-dee."
• Smaller predators are more dangerous because of
  their greater agility

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Chickadee language 2

•  To prove that the "language" was conveying
  information, Templeton et al. (2005) played back
  the recordings to chickadees.
• Recordings made in response to more dangerous
  raptors elicited more mobbing behavior,
  confirming that the chickadees understood the
  meaning of the calls.
• While this may be the most sophisticated bird
  "vocabulary" found to date, Templeton suspects
  others are out there.
• This is the most detailed communication we have
  found, but it is also the finest scale that
  anyone has looked.
• All these signaling systems are a lot more
  complicated than we really expect, until we spend
  a lot of time and energy looking at them

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Predator wingspan compared to the number of "dee"
tones  on the end of the chickadees calls. The
smaller (and more  agile) the predator, the more
"dees" get added, suggesting  that chickadees
recognize the danger of smaller predators.
Hear a chickadee response to a Pygmy Owl - click
here.  Hear a chickadee response to a Great
Horned Owl - click here. Black-capped chickadee
video
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Nuthatches eavesdrop on chickadees

• Many animals recognize the alarm calls produced
  by other species, but the amount of information
  they glean from these eavesdropped signals is
  unknown.
• Black-capped Chickadees (Poecile atricapillus)
  have a sophisticated alarm call system in which
  they encode complex information about the size
  and risk of potential predators in variations of
  a single type of mobbing alarm call.
• Templeton and Greene (2007) showed experimentally
  that Red-breasted Nuthatches (Sitta canadensis)
  respond appropriately to variation in
  heterospecific "chick-a-dee" alarm calls (i.e.,
  stronger mobbing behavior to playback of
  small-predator alarm calls), indicating that they
  gain important information about potential
  predators in their environment.
• These results demonstrate a previously
  unsuspected level of discrimination in intertaxon
  eavesdropping.

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• Siberian Jay (Photo by John van der Woude)

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Calls 'describe' predator's behavior

• Predation may cause natural selection, driving
  evolution of antipredator calls.
• calls can communicate predator category and/or
  predator distance
• risk posed by predators depends also on predator
  behavior, and ability of prey to communicate
  predator behavior to conspecifics would be a
  selective advantage reducing predation risk.
• Griesser (2008) tested with Siberian Jays
  (Perisoreus infaustus), a group-living bird
• Predation by hawks, and owls, is substantial and
  sole cause of mortality in adults
• Field data and predator-exposure experiments
  revealed jays use antipredator calls depending on
  predator behavior.
• playback experiment demonstrated that
  prey-to-prey calls are specific to hawk behavior
  (perch, search, or attack) and elicit distinct,
  situation-specific responses.
• first study to demonstrate that prey signals
  convey information about predator behavior to
  conspecifics.
• Given that antipredator calls by jays serve to
  protect kin group members, lowering mortality,
  kin-selected benefits could be an important
  factor for the evolution of predator-behavior-spec
  ific antipredator calls in such systems.

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Low frequency calls of cassowaries 1
Photo by D. DeMello, Wildlife Conservation
Society
http//www.valleyanatomical.com/

• some birds can detect wavelengths in the
  infrasound range, there has been litle evidence
  that birds produce very low frequencies.
• Mack and Jones (2003) made 9 recordings of a
  captive Dwarf Cassowary (Casuarius benneti) and
  one recording of a wild Southern Cassowary (C.
  casuarius) in Papua New Guinea.
• Both species produced sounds near the floor of
  the human hearing range in their pulsed booming
  notes down to 32 Hz for C. casuarius and 23 Hz
  in C. benneti. 

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Low frequency calls of cassowaries 2

• Natural selection should favor evolution of
  vocalizations that reach targets with minimal
  degradation, and low frequencies propagate over
  long distances with minimal attenuation by
  vegetation.
• New Guinea forests often have a fairly thick
  understory of wet leafy vegetation that could
  quickly attenuate higher frequencies.
• very low frequency calls of cassowaries probably
  ideal for communication among widely dispersed,
  solitary cassowaries in dense rainforest.
• How cassowaries produce such low vocalizations is
  currently unknown.   
• All three cassowary species have keratinous
  casques rising from the upper mandible over the
  top of the skull up to 17 cm in height.
• Hypotheses concerning the function of the casque
  include
• a secondary sexual character,
• (2) a weapon in dominance disputes,
• (3) a tool for scraping the leaf-litter, or
• (4) a crash helmet for birds as they bash through
  the undergrowth.
• The later three seem unlikely based on field
  observations.
• Future research should include the possibility
  that casque might play some role in sound
  reception or acoustic communication.

http//www.valleyanatomical.com/
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Energetic cost of singing

• Sexually selected displays, such as male
  passerine bird song, predicted to be costly.
• measurements calculating 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
  in a respirometry chamber, energetic cost of
  singing could differ under more normal
  circumstances.
• Ward and Slater (2005) used heat transfer
  modeling, based on thermal images, to estimate
  the energetic cost of singing by Canaries
  (Serinus canaria) not enclosed in respirometry
  chambers.
• Metabolic rate calculated from heat transfer
  modeling was 14 greater than during standing,
  suggesting song production is metabolically cheap
  for passerines and the metabolic cost small
  enough that it is unlikely to represent important
  fitness cost
• However, cost will increase as the temperature
  decreases.

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The functions of bird song 1

• may vary among species some known hypothesized
  functions include
• Identification
• Songs have characteristics that permit other
  birds to identify the species, sex (if both males
  and females sing), and individual identity of a
  singer.
• Characteristics important in permitting specific,
  sexual, individual recognition vary among
  species but may include (Becker 1982)
• song duration
• interval between song elements (also called notes
  or syllables, e.g., see sonagrams of Mangrove
  Warbler songs)
• frequency
• syntax - the order of elements within a song
  (e.g., Tropical Mockingbird)
• structure of elements, e.g., duration and
  frequency
• Mate attraction
• Territory establishment and defense

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The functions of bird song 2

• Motivation and Fitness - Birds may provide
  information to conspecifics by 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 conflicts
• 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

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Song complexity and the avian immune system 1

• There are three hypotheses to explain how
  evolution of parasite virulence could be linked
  to evolution of secondary sexual traits, such as
  bird song.
• female preference for healthy males in heavily
  parasitized species may result in extravagant
  trait expression.
• a reverse causal mechanism may act, if sexual
  selection affects coevolutionary dynamics of
  host-parasite interactions by selecting for
  increased virulence.
• 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
  passerine birds.

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Song complexity and the avian immune system 2

• 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. 

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• 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.

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Cities change the songs of birds

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

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In some species, females also sing.

• This is particularly true in the tropics (see
  'duetting'). Singing by females may be important
  in
• territory defense (particularly in keeping other
  females out of a territory)
• mate guarding
• pair-bonding / attraction
• reproductive synchronization

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When do female birds sing? Hypotheses from
experimental studies (Langmore 1998).
36

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

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Singing by female Northern Cardinals

• Yamaguchi (2001) found 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 dont
  sing, but listen to singing adults to memorize
  their songs.
• Then the practicing begins.
• initial attempts are pretty miserable
• they practice until it matches the memory that
  was formed earlier during the sensitive phase

Source http//www.flmnh.ufl.edu
38
Singing by female Northern Cardinals 2

• Yamaguchi (1998) also analyzed songs and found
  females sing with more overtones, a slightly
  nasal sound.
• Young males also go through a nasal, warbly phase
  as their testosterone levels rise, but its as
  though females continue to sing with an
  adolescent males voice.
• Yamaguchi (2001) discovered female cardinals
  memorize adult songs three times faster than
  males.
• While both sexes ultimately learned same number
  of song types, 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.

39
Singing by female Northern Cardinals 3

• Away from their nest, young cardinals are
  suddenly immersed in 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.
•  Perhaps 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
• For males, song-matching and fitting into the
  crowd in a new place are really important, while
  theyre not for females
• Its not clear why female cardinals have a
  shorter window of vocal learning, but we dont
  really know why females sing at all, or how they
  use their songs
• One hypothesis is that females sing as a species
  identification tool, a greeting to male cardinals
  that says, Im an eligible mate come court me.
  
• Others have proposed female cardinals sing to
  shoo away brightly colored mates from the nest,
  warning the males not to attract attention to the
  vulnerable chicks.
• female cardinals also use songs in aggressive
  behavior
• Yamaguchi says Ive seen females battling each
  other in the field, and theyre singing the whole
  time as they bang into each other.

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Male northern cardinal

• http//www.youtube.com/watch?vNrI8t6nhlgg

Tucson, Arizona