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Audition and Hemispheric Specialization in Songbirds and New Evidence from Australian Magpies

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The neural processes of bird song and song development have become a model for research relevant to human acquisition of language, but in fact, very few avian species have been tested for lateralization of the way in which their audio-vocal system is engaged in perception, motor output and cognition. Moreover, the models that have been developed have been premised on birds with strong vocal dimorphism, with a tendency to species with complex social and/or monomorphic song systems. The Australian magpie (Gymnorhina tibicen) is an excellent model for the study of communication and vocal plasticity with a sophisticated behavioural repertoire, and some of its expression depends on functional asymmetry. This paper summarizes research on vocal mechanisms and presents field-work results of behavior in the Australian magpie. For the first time, evidence is presented and discussed about lateralized behaviour in one of the foremost songbirds in response to specific and specialized auditory and visual experiences under natural conditions. It presents the first example of auditory lateralization evident in the birds' natural environment by describing an extractive foraging event that has not been described previously in any avian species. It also discusses the first example of auditory behavioral asymmetry in a songbird tested under natural conditions.
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symmetry
S
S
Article
Audition and Hemispheric Specialization in
Songbirds and New Evidence from
Australian Magpies
Gisela Kaplan
School of Science and Technology, University of New England, Armidale, NSW 2351, Australia;
gkaplan@une.edu.au
Academic Editor: Sergei D. Odintsov
Received: 20 June 2017; Accepted: 21 June 2017; Published: 28 June 2017
Abstract:
The neural processes of bird song and song development have become a model for research
relevant to human acquisition of language, but in fact, very few avian species have been tested for
lateralization of the way in which their audio-vocal system is engaged in perception, motor output
and cognition. Moreover, the models that have been developed have been premised on birds with
strong vocal dimorphism, with a tendency to species with complex social and/or monomorphic
song systems. The Australian magpie (Gymnorhina tibicen) is an excellent model for the study of
communication and vocal plasticity with a sophisticated behavioural repertoire, and some of its
expression depends on functional asymmetry. This paper summarizes research on vocal mechanisms
and presents field-work results of behavior in the Australian magpie. For the first time, evidence is
presented and discussed about lateralized behaviour in one of the foremost songbirds in response to
specific and specialized auditory and visual experiences under natural conditions. It presents the
first example of auditory lateralization evident in the birds’ natural environment by describing an
extractive foraging event that has not been described previously in any avian species. It also discusses
the first example of auditory behavioral asymmetry in a songbird tested under natural conditions.
Keywords:
auditory perception; auditory lateralization; song production; extractive foraging; visual
laterality; memory; Australian magpie
1. Introduction
Field studies of behavioural laterality in birds are still relatively rare, but the few undertaken
so far have shown that laterality may play a role in vigilance behaviour [
1
,
2
], in predation and
sexual behaviour [
3
,
4
] and even in tool manufacture, as shown in the New Caledonian crow,
Corvus moneduloides [
5
]. In fact, in the special case of tool use and manufacture by crows, the activity
appears to be strongly lateralized because birds were seen to use their right eye even when this posed
some difficulties [6].
Asymmetries in avian species have been found in visual processing from sensory input to motor
output, admittedly largely in domestic chickens [
7
,
8
] and pigeons [
9
]. Lateralized foot use has
been shown in pigeons [
10
,
11
], the New Zealand k
¯
ak
¯
a [
12
], some songbirds (sittellas and crested
shrike-tits [
13
]), Japanese jungle crow [
14
] and also in cockatoos and some parrots [
7
,
15
17
]. This paper
will explore whether such lateralities, as shown in the visual behavior of many vertebrate species [
18
],
may also be present in auditory abilities and their behavioral expressions in birds.
Without a doubt, vision and audition are the most well-developed sensory abilities both in birds
and in humans, and they are often used in conjunction: for example, there is plenty of evidence that
learning is particularly effective and often more powerful when vision and audition are coupled [
19
,
20
].
In many oscine birds, song learning occurs in a visual context, suggesting that both auditory and
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Symmetry 2017,9, 99 2 of 27
visual perceptual systems could be involved in the acquisition process. Hultsch et al. [
21
] examined, in
male juvenile nightingales, whether song performance improved after coupling visual with auditory
stimuli. It did and did so convincingly [
21
]. In a study on chickens, Van Kampen and Bolhuis [
22
]
demonstrated that learning is improved through compound training with simultaneous exposure
to visual and auditory stimuli, showing that either modality has some facilitating effects on the
memorization of features from the other modality. Such coupling has also worked in the combination
of visual with aversive olfactory stimuli [
23
]. Additionally, there is evidence from research on zebra
finches that visual stimuli activate auditory brain areas, e.g., the HVC, formerly called high vocal
centre, now called HVC and used as a proper noun (see Figure 1below) [
24
]. Given this interaction
between auditory and visual processing and, since visual lateralization is widespread in avian species,
it could be that auditory processing is also lateralized.
The importance of asymmetry in song production was identified early by Nottebohm [
25
]. He
found that when the HVC in the left hemisphere was lesioned, male canaries could not produce song.
When the HVC in the right hemisphere was lesioned, it had no effect on song production [
25
]. However,
such lateralization does not apply to song production in all species, since it has been shown in zebra
finches that some perceived manifestations of lateralization in the HVC during song production proved
to be rapid switches between hemispheres and that the overall contributions of both sides were actually
equal [26].
In research on memory formation, hemispheric dominance has been found in zebra finch males.
Gobes and Bolhuis [
27
] showed that tutored-song memory and a motor program for the bird’s
own song have separate neural representations in the songbird brain. Lesions to the caudomedial
nidopallium (NCM) of adult male zebra finches impaired tutor-song recognition, but did not affect the
males’ song production or their ability to discriminate calls. Lesions were bilateral, so any potential
lateralization could not be measured. Moorman and colleagues [
28
] recently measured neuronal
activation during sleep in juvenile zebra finch males that were still learning their songs from a
tutor. They found that during sleep, there was learning-dependent lateralization of spontaneous
neuronal activation in the NCM. Birds that imitated their tutors well were left dominant, whereas
poor imitators were right dominant, similar to language proficiency-related lateralization in humans.
Indeed, interest in comparative work in song production and perception and human speech [
29
] has
increased substantially in the last decade, finding important similarities in the role of specific auditory
nuclei between humans and birds [30,31].
Limitations: Species Investigated
The species most often chosen for detailed neurobehavioral research on auditory perception/song
performance is the zebra finch. The choice makes sense on a number of levels: the song of this species
is relatively simple and has a defined learning period, the birds are easy to keep in a laboratory setting
(opportunistic breeders as they are, they reproduce easily in captivity and over short periods of time).
However, research of song in zebra finches has some limitations. The zebra finch is a sexually
dimorphic bird in which only the male sings. This is not the case in all avian species. In fact, the zebra
finch has model character only for songbirds with credentials similar to itself [
32
,
33
]; these include, for
instance, migratory songbirds of high latitudes that need to fit a complete reproductive time-table into
the shortest possible time frame: find a mate in spring, breed, raise offspring and migrate in autumn.
Under such circumstances, offspring have to become independent rapidly. Juvenile males have to be
taught how to be able to compete and win a female, relying on recall and a perfect memory of the song
that an adult male tutor may have taught them in the previous year [34,35].
Having chosen such a model for research on bird song may have implied a questionable
underlying assumption that song in all songbirds is purely a male activity (be this for courtship
or territorial display) and may be exclusive to the breeding season. The zebra finch model also implies
that song is mostly or always crystallized early in development with limited or non-existent ability for
any ongoing learning/brain plasticity. However, as has always been known, there is a considerable
Symmetry 2017,9, 99 3 of 27
number of songbirds with vast and flexible repertoires [
36
], and some of these live in complex social
groups. Burish et al. [
37
] argued that telencephalic volume is strongly correlated with social complexity.
This correlation, so they show, accounts for almost half of the observed variation in telencephalic size,
more than any other behavioral specialization examined, including the ability to learn song. Moreover,
female song is widespread and ancestral in birds [
38
41
]. In other words, as was recognized some time
ago, relying on the zebra finch model in terms of broader questions of behavior could lead to ignoring
the importance of social learning in non-reproductive contexts [
42
,
43
], the significance of variability
in avian communication outside the breeding context and the possibility of different underlying
mechanisms of brain activity [
44
46
] for hearing and vocal production, of which lateralization may be
an important manifestation.
Since the discovery of mirror neurons in birds by Prather and colleagues [
47
], we also know that
birds can learn song without being actively supervised and instructed by an adult. Tchernichovski
and Wallman [48] explain that, on input, the motor signal is delayed, and this implies that the mirror
neurons are providing a ‘corollary discharge’ signal: that is, a neural representation of the song being
heard is available to the bird on first hearing it, and the bird can now check the encoded version against
the song it later sings; or expressed differently, the bird has the same neuron activation whether it sings
or just listens and gets a copy of the song in its memory against which it can judge its own output
(performance) of the song.
Importantly, the mirror neurons identified by Prather et al. [
47
] belong to a population of neurons
that is not replaced, as other neurons in the song system are [
49
], but is stable across song development.
It is this stability that enables the juvenile to improve its song as the memory trace of the correct
version remains present and can be accessed. It was established decades ago that amongst the network
of nuclei involved in song perception and production, some are essential and some are not essential
for song production [50], as discussed below.
2. Song Control System, the Auditory System and Lateralization
Song development and song production entail a set of complex interactions between neurological,
physiological and behavioral events, and it has taken more than thirty years of research to begin to
understand the nature, type and dynamics of these interactions.
Songbirds possess a network of interconnected nuclei in the fore-, mid- and hind-brain used in
the perception and production of vocalizations (see Figure 1) [
51
]. Furthermore, feedback loops are
essential for vocal learning, and these are found only in passerines and parrots (and two species of
humming birds), cetaceans and humans. In the former group are the HVC, the robust nucleus of the
arcopallium (RA) and the tracheosyringeal component of the hypoglossal nucleus (nXIIts), which are
necessary for the acquisition and expression of learned song [
50
], whilst the latter include Area X
and the lateral magnocellular nucleus of the anterior nidopallium (LMAN) [
52
54
]. All of these main
nuclei and some important auxiliary nuclei (Figure 1), represented on both sides of the brain, have
been tested for lateralized expression. The budgerigar, a psittacine species, capable of vocal learning,
but not classed as a songbird, has multiple forebrain areas for vocal production, but some of these, it
appears, are not homologous to those of songbirds [55].
A link has been made sometimes between size of song nuclei and song complexity. It is said
that song nuclei tend to be larger in those species that have more complex songs, and the HVC is
larger in individuals with larger repertoires [
56
]. However, the relationship between presence and
size of nuclei and actual song performance is not always matched. Gahr et al. [
57
] found that the
male and the female of the African duetting bush shrike, Laniarius funebris, produce songs of similar
complexity, but the HVC is, nevertheless, sexually dimorphic (larger in the male than in the female).
The Australian magpie, Gymnorhina tibicen, also duets, and these findings are therefore relevant here.
Gahr et al. [
57
] argued that their results show how misleading it can be to assume a causal relation
between sex difference in vocal behaviour and in the size of brain areas involved in song production
and learning.
Symmetry 2017,9, 99 4 of 27
Symmetry 2017, 9, 99 4 of 26
Figure 1. Song control system and auditory pathways. (A) The song control system. (B) Auditory
pathways; simplified-arrows indicate flow of activations; right lateral view. (A) Song output via the
main nuclei, the HVC of the nidopallium; RA, robust nucleus of the arcopallium; LMAN, lateral
magnocellular nucleus of the anterior nidopallium; Area X of the striatum; DLM, medial subdivision
of the dorsolateral nucleus of the anterior thalamus; DM, dorsomedial subdivision of nucleus
intercollicularis of the mesencephalon; Uva, nucleus uvaeformis; nXIIts, tracheosyringeal portion of
the nucleus hypoglossus (nucleus XII); rVRG, rostral ventral respiratory group. (B) Auditory input
HVC of the nidopallium with HVC shelf (lightly shaded); CLM, caudolateral mesopallium; CMM,
caudomedial mesopallium; Field L, large area (light grey) subdivided into L1, L2 and L3; NCM,
caudomedial nidopallium; RA, robust nucleus of the arcopallium; Ov, nucleus ovoidalis; MLd,
nucleus mesencephalicus lateralis, pars dorsalis; LL, lateral lemniscus subdivided into: LLD, dorsal
nucleus; LLI, intermediate nucleus; LLV, ventral nucleus; CN, cochlear nucleus;
SO, superior olive (adapted from [58]).
However, our own investigations of the song control system in magpies do not confirm those of
Gahr and colleagues [57], as is summarized below. Moreover, unlike model species such as zebra
finches, Taeniopygia guttata, Australian magpies do not use song as part of a reproductive strategy.
Both males and females sing [59], and song in both males and females declines, not increases, during
the breeding season and does not appear to play any known role in mate choice [60].
Exciting research in recent years has focused on specific areas of the brain and found intensity
invariant neurons in Field L, important for distant conspecific recognition (temporal resolution of
30 ms) and noise invariant neurons for individuals at closer distance with a temporal resolution of
just 10 ms [61]. While these areas (NCM and CM) were once just considered secondary auditory areas,
they have now been recognized as important loci for conspecific song discrimination and individual
song recognition and, as such, have behavioural significance [62–67]. Indeed, Woolley and
colleagues [68] identified all nine functional areas in the forebrain and midbrain of the zebra finch
(four in the midbrain alone), each of which was shown to play a specific role in extracting distinct
complex sound features [68]. With the importance of these areas now identified, it should also be
possible to ask whether any of these specific sound inputs activate neurons differentially in the left
or the right hemisphere.
Indeed, a study by Poirier et al. [69] using functional magnetic resonance imaging (fMRI)
discovered that, in zebra finches, the mid-brain shows neural activation in song recognition of both
individual (own) and conspecific song, which is a crucial auditory and cognitive ability. These nuclei,
called MLd (dorsal part of the lateral nucleus of the mesencephalon), are located in the midbrain, a
subcortical region that, not so long ago, had been considered non-plastic and even ‘primitive’ [69].
They showed that there was a distinct right-side bias in the MLd, confirming a complex topography
across the forebrain regions [70]. In other words, in perception of song, as distinct from song
production, robust evidence is now emerging of lateralization of the mechanisms involved. In
starling research, behaviourally-relevant song stimuli were used to test whether the NCM might be
Figure 1.
Song control system and auditory pathways. (
A
) The song control system. (
B
) Auditory
pathways; simplified-arrows indicate flow of activations; right lateral view. (
A
) Song output via
the main nuclei, the HVC of the nidopallium; RA, robust nucleus of the arcopallium; LMAN,
lateral magnocellular nucleus of the anterior nidopallium; Area X of the striatum; DLM, medial
subdivision of the dorsolateral nucleus of the anterior thalamus; DM, dorsomedial subdivision of
nucleus intercollicularis of the mesencephalon; Uva, nucleus uvaeformis; nXIIts, tracheosyringeal
portion of the nucleus hypoglossus (nucleus XII); rVRG, rostral ventral respiratory group. (
B
) Auditory
input HVC of the nidopallium with HVC shelf (lightly shaded); CLM, caudolateral mesopallium;
CMM, caudomedial mesopallium; Field L, large area (light grey) subdivided into L1, L2 and L3; NCM,
caudomedial nidopallium; RA, robust nucleus of the arcopallium; Ov, nucleus ovoidalis; MLd, nucleus
mesencephalicus lateralis, pars dorsalis; LL, lateral lemniscus subdivided into: LLD, dorsal nucleus;
LLI, intermediate nucleus; LLV, ventral nucleus; CN, cochlear nucleus; SO, superior olive (adapted
from [58]).
However, our own investigations of the song control system in magpies do not confirm those
of Gahr and colleagues [
57
], as is summarized below. Moreover, unlike model species such as zebra
finches, Taeniopygia guttata, Australian magpies do not use song as part of a reproductive strategy. Both
males and females sing [
59
], and song in both males and females declines, not increases, during the
breeding season and does not appear to play any known role in mate choice [60].
Exciting research in recent years has focused on specific areas of the brain and found intensity
invariant neurons in Field L, important for distant conspecific recognition (temporal resolution of
30 ms) and noise invariant neurons for individuals at closer distance with a temporal resolution of
just 10 ms [
61
]. While these areas (NCM and CM) were once just considered secondary auditory
areas, they have now been recognized as important loci for conspecific song discrimination and
individual song recognition and, as such, have behavioural significance [
62
67
]. Indeed, Woolley and
colleagues [
68
] identified all nine functional areas in the forebrain and midbrain of the zebra finch
(four in the midbrain alone), each of which was shown to play a specific role in extracting distinct
complex sound features [
68
]. With the importance of these areas now identified, it should also be
possible to ask whether any of these specific sound inputs activate neurons differentially in the left or
the right hemisphere.
Indeed, a study by Poirier et al. [
69
] using functional magnetic resonance imaging (fMRI)
discovered that, in zebra finches, the mid-brain shows neural activation in song recognition of both
individual (own) and conspecific song, which is a crucial auditory and cognitive ability. These
nuclei, called MLd (dorsal part of the lateral nucleus of the mesencephalon), are located in the
midbrain, a subcortical region that, not so long ago, had been considered non-plastic and even
‘primitive’ [
69
]. They showed that there was a distinct right-side bias in the MLd, confirming a complex
topography across the forebrain regions [
70
]. In other words, in perception of song, as distinct from
Symmetry 2017,9, 99 5 of 27
song production, robust evidence is now emerging of lateralization of the mechanisms involved.
In starling research, behaviourally-relevant song stimuli were used to test whether the NCM might be
a site for categorizing complex communication signals, and it was indeed confirmed, largely on the
right side of the brain [71,72].
There is no need here to catalogue all the various nuclei with lateralized functions in avian
auditory perception and song output; in their review on memory-related brain lateralization [
73
],
Moorman and Nicol (2015) published a very useful table listing nuclei concerned, together with
the species and lateralized functions. Suffice it to say that avian species that are lateralized do not
necessarily have the same side bias: chaffinches, song sparrows and canaries were found to be left
lateralized for control of song, whereas the zebra finch is largely right lateralized [
51
]. The point is
rather that the number of species tested is relatively limited and, except for the starling, they belong to
a group of birds that are sexually dimorphic, may be short-lived, limited in repertoire and of varying
brain plasticity. Each may have its own specific architecture with respect to how and what is lateralized.
It is a contention of this paper that lateralization may well be different, probably stronger and
show more functional separation, the more complex a repertoire is and the greater the ability to learn.
It is further a contention that in cases of functional changes of song, one might also expect changes in
brain activation and different adaptations, particularly in species that, more like humans, show the
same vocal capacities in male and female and are life-long learners. Although this hypothesis cannot
be fully tested or confirmed in one paper, it would seem an important and necessary task to establish
research on such a species, especially for comparative purposes with human vocal development.
Australian magpies satisfy these criteria.
3. A Life-Long Learner as a Model Species
This paper reports new data and summarizes previous research obtained both in the laboratory
and in the field concerned with auditory and visual hemispheric specialization in the Australian
magpie, a species native to Australia. The magpie is one of Australia’s foremost songbirds apart from
the lyrebird. It is territorial, and residents consist of pairs with long-term bonds, their immediate
offspring of one year and sometimes those of previous years.
The main reasons why magpies make a very useful model for perceptual research and memory
formation is that in both males and females, song does not crystallize. With a lifespan of 25 or
more years, they readily add new elements and sequences to their song, and they are also excellent
mimics [
74
,
75
]. In these qualities, there are substantial overlaps with parrots and specifically with
Australian cockatoos, as well as with ravens and crows. We know that they are amongst the most
cognitively complex and long-lived birds (sulphur-crested cockatoos: 100 years; galahs: 80 years) [
76
].
These attributes are not odd anomalies in avian species, as may once have been believed, but may be
significant in that these specific characteristics appeared early in avian evolution.
Some researchers concerned with hemispheric specialization have especially raised the question
of evolution [
77
79
], but so far, little has been made of the geographic origin of modern birds. It has
been known since the 1980s, but generally scientifically accepted since 2004, that a number of bird
lineages and all modern songbirds in the world today arose in East Gondwana, now Australia [
80
82
],
seemingly the only location where lineages survived the mass extinction events of 65 mya, including
galliformes and anseriformes [
83
], to name a few among the precocial birds, although taxonomists
still argue about dates [
84
], and all (altricial) songbirds. Songbirds radiated out from Gondwana
to the rest of the world, a process that took tens of millions of years [
85
,
86
]. For reasons of similar
climate and vegetation, those species that only went as far as the subtropical and tropical islands to the
north of the supercontinent and to the tropical regions of northern hemispheric mainlands (the Indian
subcontinent was once part of Gondwana) could presumably keep some of the traits they had acquired
in Gondwana. Cockatoos probably arose in the Cretaceous [
87
,
88
], i.e., belong to the most ancient
lineages of altricial land birds, and their highly lateralized footedness and its connection with complex
cognition, a link that has been made only recently [
16
], gains significance given its very ancient origin.
Symmetry 2017,9, 99 6 of 27
As to songbirds, Sibley’s and Ahlquist’s broad taxonomical subdivision into Corvida and
Passerida [
89
], although not necessarily used by taxonomists now, is still very useful to explain
certain broad commonalities and traits. Corvida contain overwhelmingly birds with complex cognitive
abilities (from problem solving, tool use, to measurably larger brain to body ratios) than the Passerida.
Zebra finches (a native Australian species) belong to the Passerida, smaller songbirds that were the
ones identified as among the main, probably first, ‘escapees’ from the Gondwanan continent. Magpies
and crows belong to the Corvida, the group consisting of many species, in which we find most
extant examples of complex vocal behaviour, learning and problem-solving abilities, qualities that
significantly and overwhelmingly are present in species forming long-term bonds and/or engaging in
cooperative breeding [
76
,
90
]. Most of these lineages, including magpies and lyrebirds [
74
,
91
,
92
], are
capable of substantial and accurate mimicry. In summary, brain plasticity, large repertoires and often
sophisticated vocal communication may require special architectural features in the brain. One could
speculate that avian brains of songbirds of ancient lineages, and even of non-songbirds as cockatoos,
might also be highly lateralized and be so for other functions [68].
3.1. Song Production in Australian Magpies
Magpies have an extraordinarily large repertoire. Strangely, ‘repertoire size’ in the literature, with
a few exceptions [65], tends to mean the number of syllables in a song or total number of identifiably
different songs a bird might sing, and is measured as such rather than as the sum total of vocalizations,
not only song. To establish the true range of brain asymmetry or the lack thereof, it would seem
important to consider the entire range of a bird’s utterances (see Figure 2), since these are likely to
represent different contexts and functions and may be under different neural control. In addition, there
is the question of where and how the brain gets engaged when vocalizations are a matter of affect or
are learned and/or intentional, such as in referential signalling [
93
]. To my knowledge, there is little to
no research that has been done on any of these aspects, including any lateralization of their perception
or production.
My own fieldwork on magpie vocal behavior identified as many as 27 different alarm calls [
94
],
falling roughly into six distinct types, recognizable in sonograms as highly specific in profile. Field
studies playing back alarm calls established that at least one of these calls is a referential alarm call,
signalling the presence of an eagle [95]. We then also established the stability of such referentiality in
different magpie subspecies and very different locations [96].
It would seem important to learn whether several categories of vocalizations have greater left or
right hemisphere activation and what this might tell us. We already know from studies of song learning
in zebra finches that new songs learned are memorized in the right hemisphere while the original song
(long-term memory) is retrieved from and shows neural activity in the left hemisphere [
27
]. However,
according to the results reported by Olsen et al. [
97
], direction and strength of laterality depend on
how well each song is learned and by whom: The greater the retention of song from their first tutor,
the more right-dominant the birds were when exposed to that song; but the more birds learned from
their second tutor, the more left-dominant they were when exposed to the first song [
97
]. Lateralized
memory strengthens the performance of well-learned song and presumably enables the bird to be
competitive for females in the coming season. Since magpies are improvisers and have no tutors [
75
],
it is likely that the quality of learning and recall determines whether the sounds are stored in long-term
memory (left hemisphere) [98].
Symmetry 2017,9, 99 7 of 27
Symmetry 2017, 9, 99 7 of 26
Figure 2. Range of vocalizations expressed by Australian magpies. Range of vocalizations in the
Australian magpie. These categories can roughly be subdivided as those that are a matter of affect,
such as distress, fear and anger, but alarm calls, while also short, may involve forebrain regions (as in
referential calls) or even in mobbing calls. Learned vocalizations in song, while not tutored, may have
elements that are territorial or regional markers, and all mimicry is of course learned. Intentional
vocalizations can be long or short, but they must have stereotyped characteristics, be uttered only in
the presence of conspecifics and would usually lead to a change of behaviour in others (see [93,95]).
3.2. Song Control System in Magpies
When we sectioned magpie brains, albeit in a small sample (N = 9), we found that the female
and male song nuclei of the magpie are about equal in volume and well developed and also
well-developed in juvenile magpies (2–3 months post fledging), which is consistent with the vocal
competence of juvenile magpies [99]. We also found the same song control nuclei and in the same
topographical position in the forebrain of the Australian magpie, as present in canaries and
zebra finches [50,52,99,100].
Our results indicate that, from juvenile to adult age, the volume of RA increases (10%), and the
volume of the Area X decreases (19%). No such age-dependent change occurred in the HVC or LMAN
(see Figure1). The volume of mMAN (the medial magnocellular nucleus located adjacent to LMAN)
was 40% smaller in juvenile females compared to a juvenile male and an adult female, but the volume
of RA in the juvenile male was some 36% smaller than that of the juvenile females, suggesting that
there may be both sex- and age-dependent differences in these nuclei. Interestingly, juvenile female
magpies showed a fully-developed RA nucleus 2–3 months after fledging, whereas some RA was
developmentally delayed in the juvenile males, and the reverse applied to the nucleus mMAN [99].
Since all of the measurements were made on coronal sections and only one side of the brain was
measured, no data examining lateralization were collected.
The Syrinx
The primary sound-producing organ in a bird is the syrinx, and the secondary system aiding
sound production consists of the larynx, mouth, tongue and laryngeal muscles. Opening and closing
of the beak may also affect the song produced [101–103].
The musculature controlling the syrinx is considered such a crucial anatomical feature that
songbirds have been classified as such according to the absence or presence of these muscles [104];
or rather, the definition of a true songbird is based on the identification of the number of muscles
present in the syrinx. Some avian species do not have a syrinx and produce sounds via clavicular
sacs, and suboscines may have a syrinx with just one or two pairs of syringeal muscles. Certain
Figure 2.
Range of vocalizations expressed by Australian magpies. Range of vocalizations in the
Australian magpie. These categories can roughly be subdivided as those that are a matter of affect,
such as distress, fear and anger, but alarm calls, while also short, may involve forebrain regions (as
in referential calls) or even in mobbing calls. Learned vocalizations in song, while not tutored, may
have elements that are territorial or regional markers, and all mimicry is of course learned. Intentional
vocalizations can be long or short, but they must have stereotyped characteristics, be uttered only in
the presence of conspecifics and would usually lead to a change of behaviour in others (see [93,95]).
3.2. Song Control System in Magpies
When we sectioned magpie brains, albeit in a small sample (N= 9), we found that the female
and male song nuclei of the magpie are about equal in volume and well developed and also
well-developed in juvenile magpies (2–3 months post fledging), which is consistent with the vocal
competence of juvenile magpies [
99
]. We also found the same song control nuclei and in the same
topographical position in the forebrain of the Australian magpie, as present in canaries and zebra
finches [50,52,99,100].
Our results indicate that, from juvenile to adult age, the volume of RA increases (10%), and the
volume of the Area X decreases (19%). No such age-dependent change occurred in the HVC or LMAN
(see Figure 1). The volume of mMAN (the medial magnocellular nucleus located adjacent to LMAN)
was 40% smaller in juvenile females compared to a juvenile male and an adult female, but the volume
of RA in the juvenile male was some 36% smaller than that of the juvenile females, suggesting that
there may be both sex- and age-dependent differences in these nuclei. Interestingly, juvenile female
magpies showed a fully-developed RA nucleus 2–3 months after fledging, whereas some RA was
developmentally delayed in the juvenile males, and the reverse applied to the nucleus mMAN [
99
].
Since all of the measurements were made on coronal sections and only one side of the brain was
measured, no data examining lateralization were collected.
The Syrinx
The primary sound-producing organ in a bird is the syrinx, and the secondary system aiding
sound production consists of the larynx, mouth, tongue and laryngeal muscles. Opening and closing
of the beak may also affect the song produced [101103].
The musculature controlling the syrinx is considered such a crucial anatomical feature that
songbirds have been classified as such according to the absence or presence of these muscles [
104
]; or
rather, the definition of a true songbird is based on the identification of the number of muscles present
Symmetry 2017,9, 99 8 of 27
in the syrinx. Some avian species do not have a syrinx and produce sounds via clavicular sacs, and
suboscines may have a syrinx with just one or two pairs of syringeal muscles. Certain suboscines,
e.g., Tyranni, such as pittas, have a mesomyodian syrinx with either no or just one pair of syringeal
muscles [105].
In the true oscines, as are magpies, the syrinx is equipped with four or more pairs of syringeal
muscles, typically five pairs, important in the production of song. More recent research suggests that
the syringeal muscles have mainly a modulatory function [
106
]. Furthermore, as some writers about
psittacine vocalization have pointed out, the complexity of sound and a rich vocal repertoire may belie
the simplicity of the sound-producing apparatus [107].
In early 19th century studies of the function of the syrinx, it was assumed that both sides of
the syrinx always act together to produce one sound; but since the development of spectrographs, it
could be shown that this was not the case, and birds could produce harmonically unrelated sounds
simultaneously on both sides of the syrinx, giving rise to the ‘two-voice’ theory of song. Nottebohm [
25
]
lesioned the hypoglossal nerve leading to the left side of the syrinx of male canaries, the consequence
of which was that the bird’s song was severely affected, losing the majority of its syllables, but
sectioning the right side alone had relatively little effect on the postoperative song, a finding that was
confirmed by testing other small songbirds, such as several species of sparrow and chaffinch [
50
,
108
].
The experiments have shown that the neural control of the syrinx is lateralized, with the left side being
dominant. However, to assume that neural control and physiological adaptations come only in a fixed
model for all songbirds would be incorrect.
Birds vocalize by expelling air over the elastic membranes of the syrinx housed within the
inter-clavicular sac, an air sac in the pleural cavity. In songbirds, the syrinx consists of two parts, one
in each bronchus, and each is innervated separately [
50
]. For a long time, sound was seen as being
produced by the actions of lateral and medial labia, as well as the medial tympaniform membranes in
the syrinx (see Figure 3). The actual sound-generating mechanism, however, appears to be located
in the lateral tympaniform membranes (LTM) and not, as believed in classic theories, the medial
tympaniform membranes (MTM). Goller and Larsen [
106
] showed in his sample of songbirds (a female
crow, Corvus brachyrhynchus, wild-caught male Northern cardinals, Cardinalis cardinalis, and brown
thrashers, Toxostoma rufum) that even the removal of the MTM did little to alter song performance.
Instead, they concluded on experimental evidence that, since sound production is always accompanied
by vibratory motions of both labia, the vibrations of the labia had to be the actual sound source.
The onset and termination of vocalization (called phonation) is usually controlled by the syringeal
muscles that open or close the lumen on each side of the syrinx. The elasticity and complexity of
the membranes may determine the quality of sounds. The air pressure, the muscles and the internal
membranes can interact to produce near pure tones (single frequency and similar to human whistles).
Symmetry 2017,9, 99 9 of 27
Symmetry 2017, 9, 99 9 of 26
Figure 3. Syrinx anatomy. The syrinx of Gymnorhina tibicen (A,D). (A) The first panel shows the
exposed syrinx deep in the chest of the Australian magpie (requiring sectioning the sternum),
autopsied and photographed by the author. The two lips (musculature) at the bottom of the image
are at the point of dividing into the two bronchial branches. The syrinx is connected to the trachea
and the bronchial tubes below, but at the most vibratory section, just above the thick muscle belt,
there are sinews and ligaments. (B) shows the syringeal cartilage, dorsal view (as (A), of the European
black-billed magpie, Pica pica, a relative in name only of the Australian magpie, which was named
after the European magpie. However, both are songbirds and of about equal size. In Pica pica, the four
tracheosyringeal cartilages are fused to form the tympanum. The photograph of the Australian
magpie syrinx in (A) shows the trachea, the tympanum and the tracheosyringeal cartilage. Where the
cartilage splits into its bronchosyringeal arms, this is covered in the photograph by a layer of muscle
flaps (inversely heart-shaped). (C) presents a diagram of a syrinx (horizontal plane) of a male
European blackbird, Turdus merula, one of the most common European songbirds, diverse and
musical in its song. (D) is a histologically-prepared horizontal cross-section of a syrinx of an adult
male Australian magpie prepared by the author. Note the similarities of details of (C) with (D). The
syrinx of the blackbird and the Australian magpie is arranged very similarly, particularly in the
medial and lateral labia, the lateral and the medial tympaniform membranes and the asymmetrical
arrangement of the syringeal muscles [75,108,109].
The production of sounds depends on a number of additional physiological features, called the
peripheral auditory system. The length of the trachea is important since formant frequencies are
inversely proportional to the length of the vocal tract; i.e., if this were halved, the formant frequencies
would be doubled [110]. Nowicki’s paper of 1987 [111] showed that not just the syrinx, but the vocal
tract contributed to the sound quality, at least in filtering sound [112], although, as a singular tube, it
would not contribute to our understanding of lateralization, but can explain certain auditory
characteristics [113,114]. Indeed, Hoese and colleagues [101] provided evidence experimentally of an
important coordination between beak and sound output (Figure 4), showing that restricting beak
movement or closed beak vocalizations [115] changed the tonal quality of song and caused
frequency-dependent changes in amplitude that may alter the message and, thus, require some
instructional cues from the forebrain, and these may indeed be lateralized.
Figure 3.
Syrinx anatomy. The syrinx of Gymnorhina tibicen (
A
,
D
). (
A
) The first panel shows the exposed
syrinx deep in the chest of the Australian magpie (requiring sectioning the sternum), autopsied and
photographed by the author. The two lips (musculature) at the bottom of the image are at the point
of dividing into the two bronchial branches. The syrinx is connected to the trachea and the bronchial
tubes below, but at the most vibratory section, just above the thick muscle belt, there are sinews and
ligaments. (
B
) shows the syringeal cartilage, dorsal view (as (
A
), of the European black-billed magpie,
Pica pica, a relative in name only of the Australian magpie, which was named after the European
magpie. However, both are songbirds and of about equal size. In Pica pica, the four tracheosyringeal
cartilages are fused to form the tympanum. The photograph of the Australian magpie syrinx in (
A
)
shows the trachea, the tympanum and the tracheosyringeal cartilage. Where the cartilage splits into
its bronchosyringeal arms, this is covered in the photograph by a layer of muscle flaps (inversely
heart-shaped). (
C
) presents a diagram of a syrinx (horizontal plane) of a male European blackbird,
Turdus merula, one of the most common European songbirds, diverse and musical in its song. (
D
) is
a histologically-prepared horizontal cross-section of a syrinx of an adult male Australian magpie
prepared by the author. Note the similarities of details of (
C
) with (
D
). The syrinx of the blackbird
and the Australian magpie is arranged very similarly, particularly in the medial and lateral labia, the
lateral and the medial tympaniform membranes and the asymmetrical arrangement of the syringeal
muscles [75,108,109].
The production of sounds depends on a number of additional physiological features, called the
peripheral auditory system. The length of the trachea is important since formant frequencies are
inversely proportional to the length of the vocal tract; i.e., if this were halved, the formant frequencies
would be doubled [
110
]. Nowicki’s paper of 1987 [
111
] showed that not just the syrinx, but the
vocal tract contributed to the sound quality, at least in filtering sound [
112
], although, as a singular
tube, it would not contribute to our understanding of lateralization, but can explain certain auditory
characteristics [
113
,
114
]. Indeed, Hoese and colleagues [
101
] provided evidence experimentally of
an important coordination between beak and sound output (Figure 4), showing that restricting
beak movement or closed beak vocalizations [
115
] changed the tonal quality of song and caused
frequency-dependent changes in amplitude that may alter the message and, thus, require some
instructional cues from the forebrain, and these may indeed be lateralized.
Symmetry 2017,9, 99 10 of 27
Figure 4.
Body postures for specific phonations/song types in Australian magpies. The bird (
A
)
is producing a low-level alarm call; posture erect and vigilant, and head raised slightly, beak open.
(
B
) The same bird quietly singing. Note the bird is erect, but relaxed, and the beak is closed. The arrow
points to the laryngeal area, and movement of feathers is clearly visible while the bird sings. (
C
) A pair
carolling (i.e., using the territorial call). The birds arch their backs, extend their necks and throw their
heads back, opening the beak widely to produce this loud and specialized call; chest and belly feathers
tend to be ruffled as if major muscle groups are also involved in sustaining the call. Body posture and
beak movement thus substantially differ from postures adopted in alarm calls or song.
3.3. Sound Production in the Magpie
Having identified the anatomy of the magpie’s syrinx, our laboratory then proceeded to test
phonation in wild magpies [
116
]. As in other songbirds, magpies have a tracheobronchial syrinx in
which the cranial end of each primary bronchus contains a pair of vibratory structures, the medial
and lateral labia, which vibrate in response to aerodynamic forces and produce sound when adducted
into the expiratory airstream of the bronchial lumen (Figure 3above). The muscles on each side of the
syrinx are innervated by the ipsilateral tracheosyringeal branch of the hypoglossal nerve so that each
side of the syrinx is under independent motor control by ipsilateral motor neurons that are in turn
controlled by the central song system predominantly on the same side [116].
Lateralization of song production at the level of the syrinx (i.e., the contribution of the left and
the right side of the syrinx) is relatively easy to ascertain either by syringeal nerve section or by
measuring airflow on the left and right sides. If there is no airflow through one side of the syrinx, this
indicates that the labial valve on the ipsilateral side of the syrinx is closed and silent. Vocalizations
must therefore be generated by airflow through the contralateral side of the syrinx, and this was true
of some magpie vocalizations, as described below [116].
Symmetry 2017,9, 99 11 of 27
We discovered during our investigation (see the details of the method in [
116
]) that in magpies,
the left and right sides of the syrinx can simultaneously generate different, harmonically unrelated
frequencies during some of these bilaterally-produced vocalizations. At first glance, this result fit into
the ‘two-voice’ theory. However, in magpies, it was not a matter of syllables being produced on one
side and some others on the other, but the distribution of activation was according to the frequency of
sound. The higher frequency was consistently produced on the left side. The left/right distribution of
frequencies explains why magpies can drop three or even four octaves of sound from one note to the
next. Moreover, this lateralization of frequency range is in the opposite direction from other songbirds
with very complex song or large repertoires studied previously, in which the right side of the syrinx
produces the highest fundamental [116].
Another finding was that magpies sometimes sang syllables unilaterally while maintaining
bilateral airflow through the syrinx. This motor pattern is rare in other songbirds so far studied,
which nearly always silence the contralateral side of their syrinx during unilateral phonation [
117
].
The results also showed a number of nonlinear phenomena (such as biphonation, deterministic chaos,
etc.) in which the two acoustic sources of the syrinx interact. Nowicki and Capranica [
118
] had found
these in the black-capped chickadees, Parus atricapillus, and identified them as heterodyne frequencies
(not harmonics), resulting from cross-modulation between the two syringeal sides. In magpies, we
found such nonlinear phenomena in begging calls, and here, they were a prominent feature. Still, the
workings of the syrinx in its detailed functions suggests that further investigation in species differences
of lateralization may be important. Brenowitz [
119
] argued that revision may even be necessary
especially for large songbirds or when songbirds with substantially larger song repertoires are being
examined and concern the role hemispheric specialization may play.
Indeed, lateral specialization for different frequency ranges may, in fact, increase the range of
frequencies that the bird can sing. There is some evidence of the advantages of lateralized control
in so far as the magpies’ patterns of syringeal lateralization are more similar to those in the brown
thrasher, Toxostoma rufum, the grey catbird, Dumetella carolinensis, and the northern mockingbird,
Mimus polyglottos, all of the family Mimidae, than to the motor patterns of other species that have
been studied. In the northern mockingbird, two-voiced singing is achieved from a single side of the
syrinx unlike the magpie’s dual use of different frequency ranges on each side of the syrinx [
120
].
The comparison with the Mimidae species is useful because they are amongst the most prolific singers
and thus invite comparison with the Australian magpie. We know of none of these prolific singers,
including our own study, as to whether they are lateralized consistently in one direction or whether
lateralization changes over time since the method permits only seven days of testing of awake and
relatively confined birds. The thermistors that had been implanted were removed after a week and the
birds released [116]. Perhaps even more important is the possibility that, if the syringeal activation is
lateralized consistently in the same direction, one might surmise that this could contribute to versatility
and complexity in song repertoire.
4. Testing Sound Perception and Laterality in Field and Laboratory Studies
So far, some of the areas of interest in lateralization in song/vocal production have been raised.
The last section of this paper will now be devoted to auditory perception in magpies as gleaned
from scores in field observations and some specific elements of foraging behaviour, pertinent to
lateralization, discussed.
We have a good and representative sample of hearing ranges of non-songbirds, raptors and
songbirds [
121
], and one can infer from the magpie’s own vocalizations that their auditory range is
likely to fit in well into the average range of hearing in songbirds so far tested (see Figure 5).
It is important to know this hearing range well because without this biological evidence, it would
be difficult to argue for auditory perception and lateralization at extreme upper and lower ends of
hearing capabilities, unless there is some evidence, as one of the following field observations will show.
Symmetry 2017,9, 99 12 of 27
Audible sounds perceived by magpies may range from 0.5 kHz to 7 kHz, requiring higher sound
pressure levels (SPL) for the very low frequencies (below 1 kHz), as well as for sounds above 5 kHz,
at least judging by the range of sounds they can produce. At the low frequency end is a call that
magpie females make. It is a particularly low frequency call emitted near or in the nest and typically
directed at offspring (see Figure 5C). Its function seems to be both affiliative, as well as mildly punitive.
The latter has been recorded in contexts when the offspring were still begging for food in the nest after
the mother had fed them; a reassuring ‘growl’ (sometimes referred to as purrs) immediately stopped
all begging (personal observation).
Symmetry 2017, 9, 99 12 of 26
at least judging by the range of sounds they can produce. At the low frequency end is a call that
magpie females make. It is a particularly low frequency call emitted near or in the nest and typically
directed at offspring (see Figure 5C). Its function seems to be both affiliative, as well as mildly
punitive. The latter has been recorded in contexts when the offspring were still begging for food in
the nest after the mother had fed them; a reassuring ‘growl’ (sometimes referred to as purrs)
immediately stopped all begging (personal observation).
Figure 5. Magpie range of vocalizations. The figure shows the wide range of frequencies produced in
magpie vocalizations, not included here is an actual song/warble sequence typically in the range of
1.5–2.2 kHz. y axis: frequencies in kilohertz (kHz); x axis: time in seconds. (A) is a complex single
alarm call (type that is often a precursor to the eagle alarm call); (B) a sharp high amplitude alarm
call; (C) a ‘purr’, discussed below; (D) is a mobbing call, containing a good deal of noise (grey); note
that the mobbing call, stretched here for better visibility, has a characteristic midsection, which clearly
distinguishes this category of call from alarm calls; that midsection being of less than 1 ms can at best
be identified by a human ear as a faint ‘click’ sound, but with better temporal resolution of hearing in
birds, it is likely to be unmistakable for conspecifics. Note that (A,B,D) are very high amplitude
sounds, and (A,B) have frequency ranges (audible harmonics with considerable energy, darker
horizontal lines/regular intervals) from 2 to 6 kHz and in some special calls, as (B), even maintaining
some energy at 7–8 kHz. (C) By contrast, a very low amplitude ‘purr’ vocalization, is even lower (400–
500 Hz) than the fundamentals of alarm calls and below the magpie’s typical song and is usually
delivered at 35–40 dB. Every example presents just one sound, but the darker harmonics indicate that
the call has some energy at that frequency level, well above the first formant (A) at
6 kHz; (B,D) at approximately 5–6 kHz), and accordingly, one may assume that magpies can also hear
most of the sounds they produce, even if the very upper limit harmonics (at 7 kHz and beyond) may
become inaudible to magpies).
Anatomical differences between mammalian and avian audition have often been called upon to
possibly explain differences in perception. Cohen [122] suggested that the hearing threshold of
humans is generally about 18 dB lower than that of passerines, and the lesser hearing capacity in
songbirds has been attributed to some main factors, although they have been questioned. King and
McLelland [103] had shown that the basilar membrane of the cochlea of birds is restricted in size by
head size. In pigeons, for example, this membrane is a mere 3 mm long, less than a tenth of that in
the human ear. However, while this membrane carries the neuro-epithelial receptor cells, cells are far
more densely packed in avian than in human ears, and so, King and McLelland [103] point out that
the ‘crista basilaris’, in its cross-section, has about ten-times more receptor cells than the mammalian
organ of Corti. A counter-argument made by Henry and Lucas [123] is that the avian middle ear has
just a single ossicle, the columella, that transfers acoustic energy to the cochlea, while mammals
possess three middle ear ossicles, and these ossicles improve high-frequency efficiency. Several
studies of columellar middle ear systems indicate that efficiency is greatest from 2 to 3 kHz and
declines sharply above 3–4 kHz (reviewed in [124]).
Figure 5.
Magpie range of vocalizations. The figure shows the wide range of frequencies produced
in magpie vocalizations, not included here is an actual song/warble sequence typically in the range
of 1.5–2.2 kHz. y axis: frequencies in kilohertz (kHz); x axis: time in seconds. (
A
) is a complex single
alarm call (type that is often a precursor to the eagle alarm call); (
B
) a sharp high amplitude alarm
call; (
C
) a ‘purr’, discussed below; (
D
) is a mobbing call, containing a good deal of noise (grey); note
that the mobbing call, stretched here for better visibility, has a characteristic midsection, which clearly
distinguishes this category of call from alarm calls; that midsection being of less than 1 ms can at best
be identified by a human ear as a faint ‘click’ sound, but with better temporal resolution of hearing in
birds, it is likely to be unmistakable for conspecifics. Note that (
A
,
B
,
D
) are very high amplitude sounds,
and (
A
,
B
) have frequency ranges (audible harmonics with considerable energy, darker horizontal
lines/regular intervals) from 2 to 6 kHz and in some special calls, as (
B
), even maintaining some energy
at 7–8 kHz. (
C
) By contrast, a very low amplitude ‘purr’ vocalization, is even lower (400–500 Hz)
than the fundamentals of alarm calls and below the magpie’s typical song and is usually delivered at
35–40 dB. Every example presents just one sound, but the darker harmonics indicate that the call has
some energy at that frequency level, well above the first formant (
A
) at 6 kHz; (
B
,
D
) at approximately
5–6 kHz), and accordingly, one may assume that magpies can also hear most of the sounds they produce,
even if the very upper limit harmonics (at 7 kHz and beyond) may become inaudible to magpies).
Anatomical differences between mammalian and avian audition have often been called upon
to possibly explain differences in perception. Cohen [
122
] suggested that the hearing threshold of
humans is generally about 18 dB lower than that of passerines, and the lesser hearing capacity in
songbirds has been attributed to some main factors, although they have been questioned. King and
McLelland [
103
] had shown that the basilar membrane of the cochlea of birds is restricted in size by
head size. In pigeons, for example, this membrane is a mere 3 mm long, less than a tenth of that in
the human ear. However, while this membrane carries the neuro-epithelial receptor cells, cells are far
more densely packed in avian than in human ears, and so, King and McLelland [
103
] point out that the
‘crista basilaris’, in its cross-section, has about ten-times more receptor cells than the mammalian organ
of Corti. A counter-argument made by Henry and Lucas [
123
] is that the avian middle ear has just
a single ossicle, the columella, that transfers acoustic energy to the cochlea, while mammals possess
three middle ear ossicles, and these ossicles improve high-frequency efficiency. Several studies of
Symmetry 2017,9, 99 13 of 27
columellar middle ear systems indicate that efficiency is greatest from 2 to 3 kHz and declines sharply
above 3–4 kHz (reviewed in [124]).
However, there is apparently another level at which avian audition is different and, in this case,
arguably better than the human ear, and this is in the temporal resolution of sounds, which, according
to King and McLelland [
103
], was alleged to be 10-times faster in songbirds than in human ears, but
if true, would provide a substantial auditory advantage and possible specialized ability to focus on
specific sounds. By 2002, a study by Dooling and colleagues [
125
] tackled this question of temporal
resolution. They found that birds were capable of discriminations between two sounds that differed
in fine structure over time intervals as small as 1 ms, much faster than any estimate of the monaural
temporal resolution capacity of humans. The researchers were thus able to demonstrate that the
temporal resolution in the processing of acoustic communication signals in birds was well beyond
the limits typically reported for humans; with the correction of King and McLelland’s [
103
] claims,
however, that a bird’s discrimination of the temporal fine structure of complex sounds is two- to
three-times, not ten-times, better than the limits shown for humans [
125
]. Henry and Lucas [
123
]
speculated that taxa with lower temporal resolution may compensate for this with greater frequency
resolution. They base this on theoretical models of cochlear tuning that predicts a trade-off between
temporal resolution and frequency resolution [126].
Whether or not any of these very specific aspects of audition in birds are lateralized remains
largely unchartered territory. Studies in temporal resolution have been undertaken mostly on aquatic
mammals [
127
]. Interest had also been particularly consistent with respect to localizing sound by
establishing interaural time differences (ITDs) and interaural level differences (ILDs). The puzzle
is how birds with small heads can identify the direction of sounds [
128
130
]. A more recent study
suggests that budgerigars may be able to localize pure tones as high as 4 kHz based solely on ITD
information and that small birds generally may be able to enhance directional hearing by using the
acoustic coupling of the middle ear cavities and so perform well above expectations [
131
]. In larger
birds, one suspects that head turning, studied in the context of visual perception, may be useful to
identify sounds, and these could reveal side biases.
Indeed, several such studies of auditory laterality have been undertaken by placing the sound
sources behind the test birds, some purely for establishing threshold levels [
122
]. The playback
method, placing specific auditory stimuli to the side or behind an animal, is a technique that is
usually used in larger animals as, for instance, a study on dogs that tested hemispheric specializations
for processing auditory stimuli [
132
]. Dogs turned their head to the right side (left hemisphere) in
response to conspecific vocalizations, but to the left side (right hemisphere) in response to the sound
of a thunderstorm. In birds, because of their small heads, it usually becomes a little more difficult
although not insurmountable to test auditory responses. One study, for instance, tested experienced
and young, inexperienced harpy eagles and exposed them to sounds of pure tones, of a bird (tinamous)
and of a potential prey item (howler monkey calls) and of a conspecific from a speaker placed behind
the bird. Both young and adult harpy eagles turned their head to the left when exposed to irrelevant
sounds, such as pure tones or peeps of the tinamous, and both turned right on hearing the calls
of another harpy eagle. On hearing the calls of the howler monkey, however, the captive young
harpy eagle without hunting experience oriented to the left, whereas the eagle experienced in hunting
oriented significantly to the right, clearly an example of purely auditory orienting asymmetry [
133
].
This suggests that socially-relevant information and potential food items are identified by sound alone
and processed by the left hemisphere.
In humans, a behavioral method used to establish hemispheric dominance in auditory perception
is dichotic listening in which subjects have earphones in both ears and similar sounding consonants
(such as Da/Ta) are delivered to each ear separately and simultaneously, and the subjects then tell the
experimenter which consonant/syllable they mostly heard. Research in those cases have shown a clear
right ear/left hemisphere dominance [134,135].
Symmetry 2017,9, 99 14 of 27
The same method (in principle) has been successfully employed in studying the ability of
budgerigars to identify cues of interaural time differences (ITDs) and interaural level differences (ILDs)
by implanting headphones [
131
], a technique also used to test left-right identification of sounds [
136
].
Interestingly, in humans, ITD performance drops off markedly for frequencies above 1.5 kHz, but
budgerigars maintained sensitivity up to 4 kHz. The method could be used to also establish ear
preference. Possible methods of auditory lateralization testing for lateralized brain functions have
recently (2017) been discussed by Rogers and invite further study [137].
5. Field Studies Concerning Audition in Australian Magpies
5.1. Introduction
Very few field studies have shown lateralization of auditory processing in birds. There has been
one study that meticulously established that some prey search by magpies is based purely on audition.
Floyd and Woodland [
138
] hypothesized that magpies can forage for scarab larvae purely by listening
to the chewing sounds they make in the soil. These sounds are so faint that the experimenters were
unable to hear what the magpies heard under the same field conditions.
Magpies feed regularly on scarab larvae, and they are a prized food owing to their size (2–3 cm)
and the high protein content and fluids they provide. Some studies confirmed that, in some cases, grubs
retrieved from below the surface could be found by visual means. In heavily infested areas in England,
rooks, Corvus frugilegus, and starlings, Sturnus vulgaris, feeding on scarab larvae, Phyllopertha horticola,
were able to do so because of visual cues, for instance when turf had died off, i.e., had changed colour,
or the soil surface was loose and could be lifted and pulled aside [
139
]. The American robin, Turdus
migratorius, was also shown to use visual surface cues (worm casts) for locating earthworms [
140
].
Similarly, it was known that in Australia the currawong, Strepera graculina, closely related to the
Australian magpie, both belonging to the family of Artamidae, used a similar visual guidance system
in years of severe infestation of scarab beetles of the species Seriesthis pruinosa [141].
However, not all scarab larva species leave identifying marks on the surface. Floyd and
Woodland [
136
] wanted to know how magpies could find larvae that leave no visual cues. First,
they established that there were no visual or other cues by which the magpies could identify where
the larvae were, and they then conducted a series of auditory tests, finally pre-recording the chewing
sounds the larvae made while feeding underground and playing back these sounds to magpies through
micro-speakers. Under well-controlled experimental conditions, they could then test whether the
magpies found the sound source. They did.
The speakers they used for playback in the field had a frequency response of 50–12,000 Hz [
138
].
Most of the sounds played backed to the magpies were at frequencies between 50 and 800 Hz, but
there was a small high frequency component in the 1700–3000-Hz range. The scarabs produced sounds
at an intensity of 30–38 dB. As tape hiss intensity was 30 dB, the subjects were offered a choice of
playback of scarab noises or tape hiss alone (at 30 dB); the former resulted in immediate and successful
responses; the latter did not elicit responses. Playback intensities were measured at 2 cm above ground
level [138].
5.2. Foraging for Scarab Beetles by Magpies Is Lateralized
My own field observations on foraging behaviour in magpies (specifically for scarab larvae) are
based on recordings made over a three-year period using several of our well-established research field
sites on the Northern Tableland, near the city of Armidale, New South Wales (30
32
0
S, 148
29
0
E). All
sites were permanent magpie territories of 3–7 residents, consisting of one breeding pair, juveniles and
also some young adults (daughters from the previous year). Each territory was at least 2.5 hectares
in size, flat grassland dotted with the occasional mature gum trees, some pine trees and shrubs, an
environment in which scarab larvae flourish. Two of the territories were adjacent to each other while
the visits to two others were separated from each other by at least 2 km and 5 km, respectively.
Symmetry 2017,9, 99 15 of 27
On this Northern Tableland, largely sheep-grazing country, at altitudes of about 1000 m, three
species of scarab beetles were strongly represented [
142
]. The larvae may pupate and emerge as beetles
any time between November and March, i.e., larvae reach their full size at exactly the time when
magpie offspring fledge (around September, sometimes earlier-depending on weather conditions) and
make the greatest protein and food demands on the parent birds.
Magpies feed exclusively on the ground, and they walk, putting one foot before another, while
foraging, sometimes referred to as ‘walk-foraging’ [
143
]. Their ground feeding habits make them
easy to watch and follow their foraging in open fields especially. Moreover, magpies forage very
systematically and according to a time-plan. They will reliably be at one specific transect of their
territory at a certain time of day and will generally walk diagonally and in half a meter to meter
distance from one another (Figure 6). No matter how large the territory, once their habits and time
frame were known, observations could be made at set times in the morning and in the afternoon
(changing the hour of day weekly to cover the times of their most vigorous foraging in the morning
and the later afternoon).
Symmetry 2017, 9, 99 15 of 26
Magpies feed exclusively on the ground, and they walk, putting one foot before another, while
foraging, sometimes referred to as ‘walk-foraging’ [143]. Their ground feeding habits make them easy
to watch and follow their foraging in open fields especially. Moreover, magpies forage very
systematically and according to a time-plan. They will reliably be at one specific transect of their
territory at a certain time of day and will generally walk diagonally and in half a meter to meter
distance from one another (Figure 6). No matter how large the territory, once their habits and time
frame were known, observations could be made at set times in the morning and in the afternoon
(changing the hour of day weekly to cover the times of their most vigorous foraging in the morning
and the later afternoon).
Figure 6. Directionality and spacing in magpie foraging. Magpies tend to walk slowly and steadily in
a direct line and in parallel to each other, taking transect after transect in a methodical way.
Each territory was visited daily for five days a week between September and March for three
consecutive seasons, and all observable incidents of extractive foraging were recorded. Individual
magpies could not be identified.
In the first weeks of watching foraging behavior closely, it became clear that the steps in all
successful extractive foraging events were the same; the foraging bird was: (1) scanning the ground
walking slowly; (2) then stopping and seemingly looking closely at the ground binocularly;
(3) holding absolutely still; (4) in the last moment, turning the head so that the left side of the head/ear
was close to the ground; (5) straightening up, the bird then executed a powerful jab into the ground;
(6) then retrieving a large scarab larva from the grassy surface; and (7) expertly removing the hard
head and the biting mandibles before swallowing it or feeding it to an offspring. Steps 3–7 typically
lasted less than 30 s.
5.3. Results: Extractive Foraging
The sheer consistency of the foraging sequence and the changed posture of the bird observed
made it possible to recognize the special extractive foraging strategy and made it clear, especially in
some years with greater abundance of scarab larvae, that this was not an unusual and rare event, but
a seasonal and integral part of the foraging behaviour of the territorial magpies, at least in a region
where scarab larvae were often abundant.
A total number of observations accounted for 446 attempts at extractive foraging, but only 135
observations were ultimately included. One reason for the exclusion of a substantial number of
seemingly successful extractions was the consequence of the behaviour of juveniles. Young juveniles
(a month old or less post fledging) walked with the parent bird, but had the tendency to intervene in
Figure 6.
Directionality and spacing in magpie foraging. Magpies tend to walk slowly and steadily in
a direct line and in parallel to each other, taking transect after transect in a methodical way.
Each territory was visited daily for five days a week between September and March for three
consecutive seasons, and all observable incidents of extractive foraging were recorded. Individual
magpies could not be identified.
In the first weeks of watching foraging behavior closely, it became clear that the steps in all
successful extractive foraging events were the same; the foraging bird was: (1) scanning the ground
walking slowly; (2) then stopping and seemingly looking closely at the ground binocularly; (3) holding
absolutely still; (4) in the last moment, turning the head so that the left side of the head/ear was close
to the ground; (5) straightening up, the bird then executed a powerful jab into the ground; (6) then
retrieving a large scarab larva from the grassy surface; and (7) expertly removing the hard head and
the biting mandibles before swallowing it or feeding it to an offspring. Steps 3–7 typically lasted less
than 30 s.
5.3. Results: Extractive Foraging
The sheer consistency of the foraging sequence and the changed posture of the bird observed
made it possible to recognize the special extractive foraging strategy and made it clear, especially in
Symmetry 2017,9, 99 16 of 27
some years with greater abundance of scarab larvae, that this was not an unusual and rare event, but
a seasonal and integral part of the foraging behaviour of the territorial magpies, at least in a region
where scarab larvae were often abundant.
A total number of observations accounted for 446 attempts at extractive foraging, but only 135
observations were ultimately included. One reason for the exclusion of a substantial number of
seemingly successful extractions was the consequence of the behaviour of juveniles. Young juveniles
(a month old or less post fledging) walked with the parent bird, but had the tendency to intervene
in the process of foraging, by posting themselves in front of the adult to block the path, just so as to
ensure that the morsel was fed to them as shown in Figure 7.
Symmetry 2017, 9, 99 16 of 26
the process of foraging, by posting themselves in front of the adult to block the path, just so as to
ensure that the morsel was fed to them as shown in Figure 7.
Figure 7. Parent feeding scarab larvae to magpie juvenile. Female magpie feeding a larva to a young
fledgling. Such an example was not included in the analysis, and this method of feeding, the juvenile
right in front of the parent bird, was limited in time and dependent on the juvenile’s development.
Blocking the way and front of feeding was observed only in juveniles one month post-fledging. By
two months post-fledging, most juveniles walked next to the adult (usually on the right side) and
actively started observing the processes of the adult’s food acquisition.
The most common reason for exclusion, however, concerned problems for the observer
regarding distance or terrain. The most obvious problem occurred when the magpies foraged with
their backs turned towards the observer and often at some distance, and in such cases, it made it
difficult to be certain of the direction of head movements prior to extraction. Hence, such sequences
were excluded even when the actual retrieval of larvae was seen.
The instances included were based on the foraging data obtained from four different territories.
In an area of over 18 hectares traversed daily, the total number of resident magpies observed seems
small (N = 16), and hence, it is very possible that, in some cases, the same magpies were scored
repeatedly if they happened to be the successful ones in extracting the larvae, and this may partially
account for the consistency of the findings. Relatedness is unlikely to be an issue in these results since
juveniles forced out by the parents tend to roam in bachelor groups for at least four years and feed in
non-dedicated, usually inferior, sites before some of them succeed in finding a suitable territory and
a partner. There is no evidence that a daughter or son might secure a neighbouring territory.
Equally, the number of juveniles observed, at least in the first month of the season (September),
typically made no contribution to extractive foraging, but were keen consumers: they often did not
commence making successful extractions of larvae on their own until nearly the middle of the
observation period. Hence, although some magpies may have contributed several scores of
extractions of larvae over the observation period of three months, this does not invalidate the
observations because each event was a new event and an individual magpie could have approached
the excavation site differently on each occasion.
Most incidents of successful extractive foraging were observed in October and November, the
observed incidents sharply declining after mid-December when the ground became very dry and
compacted and most scarab beetles might have emerged (see Figure 8).
Figure 7.
Parent feeding scarab larvae to magpie juvenile. Female magpie feeding a larva to a young
fledgling. Such an example was not included in the analysis, and this method of feeding, the juvenile
right in front of the parent bird, was limited in time and dependent on the juvenile’s development.
Blocking the way and front of feeding was observed only in juveniles one month post-fledging. By two
months post-fledging, most juveniles walked next to the adult (usually on the right side) and actively
started observing the processes of the adult’s food acquisition.
The most common reason for exclusion, however, concerned problems for the observer regarding
distance or terrain. The most obvious problem occurred when the magpies foraged with their backs
turned towards the observer and often at some distance, and in such cases, it made it difficult to be
certain of the direction of head movements prior to extraction. Hence, such sequences were excluded
even when the actual retrieval of larvae was seen.
The instances included were based on the foraging data obtained from four different territories.
In an area of over 18 hectares traversed daily, the total number of resident magpies observed seems
small (N= 16), and hence, it is very possible that, in some cases, the same magpies were scored
repeatedly if they happened to be the successful ones in extracting the larvae, and this may partially
account for the consistency of the findings. Relatedness is unlikely to be an issue in these results since
juveniles forced out by the parents tend to roam in bachelor groups for at least four years and feed in
non-dedicated, usually inferior, sites before some of them succeed in finding a suitable territory and a
partner. There is no evidence that a daughter or son might secure a neighbouring territory.
Equally, the number of juveniles observed, at least in the first month of the season (September),
typically made no contribution to extractive foraging, but were keen consumers: they often did
not commence making successful extractions of larvae on their own until nearly the middle of the
observation period. Hence, although some magpies may have contributed several scores of extractions
of larvae over the observation period of three months, this does not invalidate the observations because
Symmetry 2017,9, 99 17 of 27
each event was a new event and an individual magpie could have approached the excavation site
differently on each occasion.
Most incidents of successful extractive foraging were observed in October and November, the
observed incidents sharply declining after mid-December when the ground became very dry and
compacted and most scarab beetles might have emerged (see Figure 8).
Symmetry 2017, 9, 99 17 of 26
Figure 8. Walk-foraging and successful extractive foraging events. The majority of scarab larvae were
retrieved in October, decreasing substantially by December and found only scarcely thereafter and
not at all by February (percentage figures refer to successful retrievals counted). The large
light-shaded semi-circle shows the months and hours when juveniles started searching for scarab
larvae on their own, mostly with relatively little success.
All 135 recorded sequences showed the same left ear preference: the bird being observed tilted
the head so that the left ear was held closer to the ground before straightening up and delivering the
successful jab of its beak into the soil (Figure 9). This tilting of the head to a left position was clearly
visible in each of the incidents. One would expect to find that not all scores of extractive foraging
used the left ear (i.e., at least some magpies might have tilted the head in the other direction), but this
was not so. Even though some of the scores were likely repeats for the same individual, the total
absence of right ear use means that the bias is significant at the population level.
Figure 9. Lateralized auditory detection of prey item. The image of the magpie shows Step 4 in the
extractive foraging sequence, moving the head from a 90° angle, binocular viewing, to a 45° angle,
moving the beak to the right and up so that the left ear is closer to the ground.
5.4. Discussion
To my knowledge, this is the first example of auditory lateralization in the field describing an
extractive foraging event that has not been described in any avian species. It is also the first example
of auditory behavioural asymmetry under natural conditions.
The point made here is that the foraging strategy was not based on visual scanning, but crucially
on auditory examination of a potential prey item and that it was consistently performed by the left
ear. In the image shown above (Figure 9), the bird is walking leftwards, and the right ear would have
Figure 8.
Walk-foraging and successful extractive foraging events. The majority of scarab larvae were
retrieved in October, decreasing substantially by December and found only scarcely thereafter and not
at all by February (percentage figures refer to successful retrievals counted). The large light-shaded
semi-circle shows the months and hours when juveniles started searching for scarab larvae on their
own, mostly with relatively little success.
All 135 recorded sequences showed the same left ear preference: the bird being observed tilted
the head so that the left ear was held closer to the ground before straightening up and delivering the
successful jab of its beak into the soil (Figure 9). This tilting of the head to a left position was clearly
visible in each of the incidents. One would expect to find that not all scores of extractive foraging used
the left ear (i.e., at least some magpies might have tilted the head in the other direction), but this was
not so. Even though some of the scores were likely repeats for the same individual, the total absence of
right ear use means that the bias is significant at the population level.
Symmetry 2017, 9, 99 17 of 26
Figure 8. Walk-foraging and successful extractive foraging events. The majority of scarab larvae were
retrieved in October, decreasing substantially by December and found only scarcely thereafter and
not at all by February (percentage figures refer to successful retrievals counted). The large
light-shaded semi-circle shows the months and hours when juveniles started searching for scarab
larvae on their own, mostly with relatively little success.
All 135 recorded sequences showed the same left ear preference: the bird being observed tilted
the head so that the left ear was held closer to the ground before straightening up and delivering the
successful jab of its beak into the soil (Figure 9). This tilting of the head to a left position was clearly
visible in each of the incidents. One would expect to find that not all scores of extractive foraging
used the left ear (i.e., at least some magpies might have tilted the head in the other direction), but this
was not so. Even though some of the scores were likely repeats for the same individual, the total
absence of right ear use means that the bias is significant at the population level.
Figure 9. Lateralized auditory detection of prey item. The image of the magpie shows Step 4 in the
extractive foraging sequence, moving the head from a 90° angle, binocular viewing, to a 45° angle,
moving the beak to the right and up so that the left ear is closer to the ground.
5.4. Discussion
To my knowledge, this is the first example of auditory lateralization in the field describing an
extractive foraging event that has not been described in any avian species. It is also the first example
of auditory behavioural asymmetry under natural conditions.
The point made here is that the foraging strategy was not based on visual scanning, but crucially
on auditory examination of a potential prey item and that it was consistently performed by the left
ear. In the image shown above (Figure 9), the bird is walking leftwards, and the right ear would have
Figure 9.
Lateralized auditory detection of prey item. The image of the magpie shows Step 4 in the
extractive foraging sequence, moving the head from a 90
angle, binocular viewing, to a 45
angle,
moving the beak to the right and up so that the left ear is closer to the ground.
Symmetry 2017,9, 99 18 of 27
5.4. Discussion
To my knowledge, this is the first example of auditory lateralization in the field describing an
extractive foraging event that has not been described in any avian species. It is also the first example
of auditory behavioural asymmetry under natural conditions.
The point made here is that the foraging strategy was not based on visual scanning, but crucially
on auditory examination of a potential prey item and that it was consistently performed by the left
ear. In the image shown above (Figure 9), the bird is walking leftwards, and the right ear would have
been nearer for auditory inspection than the left, but the bird turned the head right around in order to
listen to the underground larva with its left ear. In all cases included in the sample, the birds turned to
position their left ear close to the ground.
It seems highly unlikely that this head tilt related to improving visual scanning. The visual field
of magpies in the binocular field at close range is about 28–34
[
4
], and any fixation of a potential
prey item is therefore most accurate when the beak points at about 90
to the ground (for binocular
viewing). Since scarab larvae create no visual surface cues, as Floyd and Woodland (1981) had so
convincingly shown [
138
], the only way magpies are able to identify the location of the underground
prey item is by auditory means. Hence, regarding the head tilt prior to grasping the grub, we are left
with only one explanation, namely that the bird obtained confirmation of the presence of a scarab larva
exclusively by aural means.
In retrospect, watching magpie groups combing through their territories in such an orderly
fashion (Figure 6above) and doing so grid-by-grid every day may well be a result of having acquired
the skill of extractive foraging. Clearly, the sounds that larvae make are so faint that they would be
easily missed unless a group spaces out in such a way that every part of the ground can actually be
scanned by listening to sounds at very close proximity.
5.5. Additional Field Results in Magpie Foraging
The results of foraging raise the question why this auditory behaviour is left-biased (right
hemisphere) and significant at the population level and how this may fit the results in other and
related studies we had conducted.
The extractive foraging results of lateralized listening follow from the results obtained on
lateralized foraging behaviour in magpies in a series of additional field studies conducted by members
of our laboratory [
4
,
144
]. One tested head turning during foraging (visual scanning); another scored
eye preferences for tracking moving prey (for both, see [
4
], called Study 2 in the summarizing table
below); and a third scored the side of begging behaviour of juveniles walk-foraging with a parent
bird [144] (see the results summarized in Table 1below).
Head turning during visual foraging (pecking food from the ground) was found to favour the
right eye/left hemisphere. There was a slight, but significant bias at the population level for the bird to
turn its head so that the right eye monocular field was directed towards the ground.
In a third study (eye preference for moving prey [
4
]), we supplied the magpies with food by
purposely throwing mince-meat pieces in their direction and then scoring which eye they last used
before taking and consuming it. Of 155 scores, 97 percent were left-eye dominant, meaning they
involved left-eye viewing the moving target before food retrieval.
Later that year (also published in [
4
]), we had the opportunity to observe magpies dealing with
moving prey items and watching the magpies trying to capture them. There was a locust plague, and
locust were either jumping or flying up from the grass. Under natural conditions, we received the
same results as in the food-supplementation experiment, finding a strong left-eye/right hemisphere
preference. The results are consistent with use of the right hemisphere processing spatial information
as known from studies in chicks [145].
In another field study (called Study 4 here; see also Table below [
144
]), it was recorded on which
side juveniles approached the parent birds and begged for food while walk-foraging, and a significant
group-level bias for begging on the right side of the parent was found. Juveniles were 2.46-times
Symmetry 2017,9, 99 19 of 27
more likely to beg on the right side than on the left [
144
]. By begging on the right side of a parent, a
juvenile uses its left eye to view the adult and is in the parent’s right visual field. Hoffman et al. [
144
]
pointed out that visual inputs from the right visual field are processed by the left hemisphere, which
is known to inhibit conspecific aggression, as found in chickens [
146
]. By approaching in the right
hemifield, a juvenile magpie may also avoid being scolded by the parent bird [
144
]. Alternatively, and
more likely, as a recent comparison across species indicates [
147
], the infant is positioning itself so that
it can monitor the parent’s behavior using its left visual field and right hemisphere, specialized for
processing social behaviour.
Table 1. Hemispheric specializations in five field studies on foraging and vigilance in magpies.
Study No. (Subjects)
No. Scores
(Behavioral)
Total/Bracket:
Majority of
Responses
Left Eye or
Ear/Right
Hemisphere
Right Eye or
Ear/Left
Hemisphere
Authors
(1) Extractive foraging 16 135 (135) Left ear dominant Kaplan, this
paper,
(2) Head-turning
during foraging 20 266 (116) Right eye dominant Rogers and
Kaplan 2006 [4]
(3) Tracking moving
prey 12 159 (155) Left eye dominant Rogers and
Kaplan 2006 [4]
(4) Begging position
of juveniles during
foraging
6 parent-juvenile
pairs 16/64 scores Left eye dominant
(begging juveniles)
Right eye dominant
(feeding adult)
Hoffman et al.
and Rogers 2006
[144]
(5) Inspecting
predator 55
270 (compound
score/various
behaviors)
Left eye dominant
Koboroff, Kaplan
and Rogers 2008
[148]
Brackets give the number of subjects/behavior showing eye/ear bias.
A fifth field study, not on foraging, but on eye preference in magpies when viewing a predator,
scored eye use when presented with taxidermic models of a potential predator, a lace monitor [
148
].
We established by scoring monocular fixations from video footage that magpies used their left eye
in the majority of instances while inspecting the potential predator, such as jumping (73%), prior to
circling (65%), as well as during circling (58%) and for high alert inspection of the predator (72%), and
we concluded that mobbing and perhaps circling are likely agonistic responses controlled by the left
eye/right hemisphere [148].
The results of the second field study are consistent with preferred use of the left hemisphere and
right eye in control of feeding responses as has also been shown in other species, including the zebra
finch [
149
]. In the third field study, magpies show a right eye/left hemisphere preference reflecting
a specialization for spatial information using global cues and also for rapid responding. It is thus
noteworthy that of the three foraging tasks, two were controlled by the right hemisphere or expressed
differently; it would appear odd that two foraging tasks looking for prey on the ground and looking for
prey under the ground are managed by different hemispheres. The reason for this becomes clear in this
context: one is consistent with feeding responses generally, while the other method (extractive foraging
using the left ear) is based on spatial information and auditory cues. Hence, these two foraging
methods do not just require different strategies, but are under the control of different hemispheres.
While three of the findings for four field studies relate to visual lateralization in magpies (see Table 1),
there may also be an auditory element to them.
My field study of foraging for scarab larvae showed a very strong bias towards the left ear to
pinpoint the larvae’s presence under the ground, leaving the right ear free to respond to the begging or
other calls of an offspring. This may allow the magpie to attend to two tasks at once. Rogers et al. [
148
]
showed in chicks that the performance of two tasks simultaneously, such as foraging and attending to
a predator overhead, is undertaken effectively in strongly-lateralized chicks in which visual search is
processed by the left hemisphere and predator detection by the right hemisphere [150].
Symmetry 2017,9, 99 20 of 27
Furthermore, agonistic responses are processed by the right hemisphere, consistent with research
results in chicks [
146
] and other species [
151
]. Chicks also use the left eye to examine novel objects and
the details of a stimulus detecting small changes in familiar stimuli, whereas the right eye detects large
changes that represent categories rather than details [
152
]. It is conceivable and even probable that the
same hemispheric specializations that apply to eye use apply also to ear use.
6. Conclusions
This paper has presented evidence of lateralized behaviour in phonation and listening in one
songbird species. Motor output and the way magpies produce song were shown to involve an entire
range of techniques that enable an individual magpie not only to maintain singing for hours, but
allow for a range of extraordinary modulations at a wide range of frequencies by using unusual
techniques of lateralized frequency use (higher on left, lower on right side of syrinx). Paradoxically,
so far, specific functions for their varied song have not been discovered. It is clear that their song can
identify individuals one from another [
75
], but such individual recognition is conceivably achieved
by just listening to their territorial call, referred to as carolling. There appears to be no territorial
advantage for having a larger or smaller repertoire. It is possible, given that magpies form auditory
maps of other species in their territory (they mimic only heterospecific sounds pertaining to their
territory [
74
,
76
]), that the auditory memory, in this case of heterospecific sounds, is lateralized on the
left side, as in other songbirds, but this has not been studied. It is also possible that such auditory
‘maps’ may be linked to other brain regions.
The substantial and innovative neuroscientific research in avian vocal production and vocal
perception over the last decades notwithstanding, it pertains largely to a few small songbird species.
Ocklenburg and Güntürkün in their paper [
153
] published a telling ‘cladogram’ showing that we
have no information at all on lateralization in vocal production (central and peripheral) and vocal
perception on any of the 28 clades of extant non-songbirds. Although Passeriformes are just one clade
in this cladogram [
153
], Passeriformes, i.e., the true songbirds, actually make up the majority of all
extant birds (over 5000 species). Additionally, while we know plenty about the zebra finch and a few
other songbird species in this regard, there is little to no information available on almost all other
extant songbirds either. It would help to understand whether large repertoires and flexible/plastic
brains have developed other or additional neural mechanisms for song production and perception
and whether this is achieved via specific hemispheric specializations. The magpie is certainly a
representative of this kind of songbird. With an evolutionary history of likely more than 20 million
years and in an evolutionary context of substantial speciation pre- and post the mass extinction of
65 mya, the emergence of a major songbird at that time may be as fascinating genetically as it is in its
current performance.
Here, results of several field studies were presented. The results of lateralization in the field have
been telling us that there are behaviours that are clearly highly lateralized in magpies. Extractive
foraging has a particular place in ethological-cognitive research and, in primates, has been identified
as one of the very complex cognitive behaviours and, when reported, relies usually on vision or on
experience, but not purely on audition (the very specialized adaptations of the aye-aye being one of
the few known exceptions).
This is the first paper that reports this auditory behaviour in a songbird and, furthermore, shows
that the success of it may depend on a highly lateralized neuronal aspect in the auditory system.
The results of the other field studies on foraging behaviour make a powerful point that the bird has
to handle very different experiences and tackle potential dangers while foraging or encountering
predators. Here, it has been shown that these key functions are lateralized, which may have substantial
advantages for survival.
Acknowledgments:
The research on magpies was largely funded by the Australian Research Council and also by
an annual personal bequest to Kaplan (The Cardigan Fund) made to our Research Centre of Neuroscience and
Animal Behaviour and these funding sources are gratefully acknowledged.
Symmetry 2017,9, 99 21 of 27
Author Contributions:
This is the original contribution by the author and any reference to previously published
materials, be this by the author or other researchers, is fully acknowledged.
Conflicts of Interest: There is no conflict of interest.
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Chapter
This chapter covers methods of measuring preferences to use one eye or ear to attend to a stimulus, which reflects lateralized processing of sensory information. It begins with monocular occlusion as a way of measuring differences in strength or nature of response elicited by particular visual stimuli. Depending on the type of stimulus presented a preference for responding using the left or right eye can be found (e.g. chicks show a right-eye preference when searching for food grains and a left-eye preference when attacking a conspecific or responding to a predator). Especially in species with their eyes positioned on the sides of their head, this reflects differences in processing by the left and right sides of the brain. In these species it is also possible to test responses to stimuli presented in the left versus right monocular visual fields without having to apply eye patches. A method of determining the extents of the monocular and binocular visual fields is explained. Then a modification of the monocular testing method involving rotation of the stimulus around the animal being tested is discussed: as shown in frogs and toads, response to prey moved in this manner differs between clockwise and anticlockwise rotation. Eye preferences can also be determined using binocular presentation of stimuli that cause the test animal to turn its head to permit monocular fixation of the stimulus before a specific response is made (e.g. before attacking a conspecific, as scored in chicks and horses). Angles adopted by fish when viewing their image in a mirror have been used to measure lateralization of attending to a conspecific. Another approach is simultaneous introduction of identical stimuli into the monocular field of each eye and assessment of side biases in responding (as in toads striking at insect prey). Visual pathways are discussed briefly to help explain how eye preferences reveal brain lateralization. Next, several methods of measuring lateralization of processing and responding to auditory stimuli are covered and finally some points are made about future directions of research along these lines. The suitability of these methods for testing different species is considered in all sections of the chapter.
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In monolingual humans, language-related brain activation shows a distinct lateralized pattern, in which the left hemisphere is often dominant. Studies are not as conclusive regarding the localization of the underlying neural substrate for language in sequential language learners. Lateralization of the neural substrate for first and second language depends on a number of factors including proficiency and early experience with each language. Similar to humans learning speech, songbirds learn their vocalizations from a conspecific tutor early in development. Here, we show mirrored patterns of lateralization in the avian analog of the mammalian auditory cortex (the caudomedial nidopallium [NCM]) in sequentially tutored zebra finches, in response to their first tutor song, learned early in development, and to their second tutor song, learned later in development. The greater the retention of song from their first tutor, the more right-dominant the birds were when exposed to that song; the more birds learned from their second tutor, the more left-dominant they were when exposed to that song. Thus, the avian auditory cortex may preserve lateralized neuronal traces of old and new tutor song memories, which are dependent on proficiency of song learning. There is striking resemblance in humans: early-formed language representations are maintained in the brain even if exposure to that language is discontinued. The switching of hemispheric dominance related to the acquisition of early auditory memories and subsequent encoding of more recent memories may be an evolutionary adaptation in vocal learners necessary for the behavioral flexibility to acquire novel vocalizations, such as a second language.