Aves Trnasfer

Avian visual perception:
Interocular and intraocular transfer

and
head-bobbing behaviour in birds
A Dissertation submitted for

the Degree of Philosphiae doctoris (PhD) in Neuroscience
at the
International Graduate School of Neuroscience (IGSN)
of the
RUHR-UNIVERSITY BOCHUM
by
Laura Jimnez Ortega
October 2005
Printed with permission of the International Graduate School of Neuroscience of the

RUHR-UNIVERSITY BOCHUM
First Referee: Prof. Dr. Nikolaus F. Troje
Second Referee: Prof. Dr. Onur Gntrkn
Third Referee: Prof. Dr. L. Huber (Wien)
Date of the oral examination: 30-11-2005
Table of contents
1. GENERAL INTRODUCTION ....................................................................................1
1.2 Intraocular and interocular transfer in pigeons ............................................................................................... 2
1.2.1 Intraocular transfer of information ......................................................................................................... 3
1.2.2 Interocular transfer of information.......................................................................................................... 5
1.2.3 Interim summary ....................................................................................................................................... 9
1.3 Visual asymmetries in birds.............................................................................................................................. 10
1.3.1 Right eye/left hemisphere dominances................................................................................................... 11
1.3.2 Left eye/right hemisphere dominances .................................................................................................. 12
1.3.3 Asymmetric interhemispheric transfer.................................................................................................. 14
1.3.4 Interim summary ..................................................................................................................................... 16
1.4 Head-bobbing in birds ...................................................................................................................................... 16
1.4.1 Biomechanical function ........................................................................................................................... 17
1.4.2 Image stabilization................................................................................................................................... 18
1.4.3 Motion parallax........................................................................................................................................ 19
1.4.4 Head-bobbing birds ................................................................................................................................. 20
1.4.5 Interim summary ..................................................................................................................................... 22
1.5 Anatomical substrate ........................................................................................................................................ 22
1.5.1 The avian eye............................................................................................................................................ 22
1.5.2 Visual pathways in the avian brain ........................................................................................................ 26
1.5.3 Interim summary ..................................................................................................................................... 30
1.6 Goals of this work ............................................................................................................................................. 31
2. GENERAL METHODS ...........................................................................................32

2.1 Experimental arena .......................................................................................................................................... 32
2.2 Motion capture system...................................................................................................................................... 33
2.3 Subjects ............................................................................................................................................................. 34
2.4 Training Procedure .......................................................................................................................................... 34
3. EXPERIMENT 1, 2 AND 3: INTRAOCULAR AND INTEROCULAR TRANSFER IN

PIGEONS. ..................................................................................................................38
3.1 Experiment 1: Limits of intraocular transfer in pigeons I: frontal to lateral direction. ................................ 38
3.1.1 Methods .................................................................................................................................................... 39
3.1.2 Results....................................................................................................................................................... 41
3.1.3 Discussion ................................................................................................................................................. 46
3.2 Are pigeons capable of interocular transfer between the two yellow fields? .................................................. 49
3.2.1 Methods .................................................................................................................................................... 50
ii
3.2.2 Results....................................................................................................................................................... 51
3.2.3 Discussion ................................................................................................................................................. 53
3.3 Limits of intraocular transfer in pigeons II: lateral to frontal direction. ....................................................... 56
3.3.1 Methods .................................................................................................................................................... 56
3.3.2 Results....................................................................................................................................................... 57
3.3.3 Discussion ................................................................................................................................................. 59
3.4 Interim summary............................................................................................................................................. 62
4. EXPERIMENT 4: PATTERN RECOGNITION DURING HEAD-BOBBING: ARE

PIGEONS CAPABLE OF PATTERN RECOGNITION DURING THE THRUST
PHASE? .....................................................................................................................63
4.1 Methods............................................................................................................................................................. 63
4.2 Results ............................................................................................................................................................... 67
4.2.1 Percentage of correct responses.............................................................................................................. 67
4.2.2 Head-bobbing motion .............................................................................................................................. 69
4.3.3 Interim summary ..................................................................................................................................... 81
5. EXPERIMENT 5: WHY DO BIRDS BOB THEIR HEADS? ....................................82

5.1 Methods............................................................................................................................................................. 83
5.1.1 List of head-bobbing and non head-bobbing birds............................................................................... 83
5.1.2 Taxonomic tree of head-bobbing and non head-bobbing birds ........................................................... 85
5.1.3 Analysis of behavioural and ecological factors under head-bobbing .................................................. 87
5.2 Results ............................................................................................................................................................... 89
5.2.1 Head-bobbing and non head-bobbing birds list.................................................................................... 89
5.3 Discussion ....................................................................................................................................................... 100
5.3.1 List of head-bobbing and non-bobbing birds: exceptions within a family........................................ 101
5.3.2 Rare or occasional head-bobbing behaviour ....................................................................................... 103
5.3.3 Are body-bobbing birds head-bobbing birds? .................................................................................... 106
5.3.4 Are other-head-movements functions similar to head-bobbing functions? ...................................... 106
5.3.5 Head-bobbing evolution ........................................................................................................................ 107
5.3.6 Ecological and behavioural factors under head-bobbing, body-bobbing and non-bobbing ........... 114
5.3.7 Interim Summary .................................................................................................................................. 115
6. GENERAL DISCUSSION .....................................................................................117

6.1 Intraocular and interocular transfer of information.................................................................................... 117
6.1.1 Intraocular transfer of information ..................................................................................................... 118
6.1.2 Interocular transfer of information...................................................................................................... 120
6.2 Pattern recognition during head-bobbing...................................................................................................... 122
6.3 Why do birds bob their heads? ....................................................................................................................... 124
6.4 Summary ......................................................................................................................................................... 126
iii
APPENDIX................................................................................................................128
A. Intraocular and interocular transfer ............................................................................................................ 128
B. Pattern recognition during head-bobbing ................................................................................................... 132
C. Why birds bob their heads?........................................................................................................................... 134
REFERENCES .........................................................................................................157
iv
ABSTRACT
Two aspects of the avian visual perception were investigated: inter- and intraocular transfer of
information in walking pigeons as well as head-bobbing behaviour in birds. The retina of the
pigeon has two areas of enhanced vision: the red field pointing into the frontal binocular field
and the yellow field projecting into the lateral monocular field. The entire retina projects to the
tectofugal pathway, whereas the monocular area projects to the thalamofugal pathway. The
first part of this study examines how information received in different retinal areas is
generalised in the pigeon brain. The pigeons task was to discriminate between two shapes by
pecking on one of the two keys located at one end of an experimental alley, while walking
between two feeders. In the first study intraocular transfer between the red and the yellow field
was tested, by moving the stimulus presentation from the frontal to the lateral visual field in
consecutive steps. When the stimuli were located at 45 in the experimental arena, we observed
a drastic decrease of performance that may be due to a switch between the tectofugal and the
thalamofugal pathway. Intraocular transfer of information was also tested from lateral to
frontal direction. The transfer of information was poor or inexistent. Interocular transfer of
information between the yellow fields of the eyes was also tested. A lack of interocular transfer
was found in eight out of nine birds. Pigeons showed more difficulties to learn the task in the
monocular right visual field than in the monocular left visual field.
It is widely accepted that head-bobbing (HB) may act as an optokinetic behaviour, stabilizing
the retinal image and allowing pattern recognition during the hold phase. Pattern discrimination
during HB was tested by presenting two shapes during the hold phase, the thrust phase, or
randomly. The pigeons discriminated the shapes during the entire HB cycle: no differences
between the phases were observed. Finally, a list of 322 species of head-bobbing and nonbobbing birds is offered. The development of HB in evolution and its behavioural and
ecological characteristics were also investigated. Half of the birds of the world may be headbobbing birds; the rest may be equally divided between body-bobbing (hopping) and nonbobbing birds. HB may have appeared for the first time in a common ancestor of all living
birds. However, evidence for suppressions and several independent evolutions of HB were
observed. Head-bobbing may be a mechanism developed early in evolution to solve visual
demands, like pattern recognition and to monitor predators, in birds with lateralised eyes.
General Introduction 1
1. GENERAL INTRODUCTION
Birds are the most visually dependent class of vertebrates (Gntrkn, 2002), as they are
highly specialised in visual perception. They live in a wide variety of habitats from desert to
rain forest and feed on a wide range of food: seeds, insects, small mammals, carcass, etc. Some
birds suffer a strong predator pressure, while others are predators themselves. Birds may need
to afford different visual demands that lead to different visual specialisations. The flying ability
is probably one of the greatest challenges for the avian visual system. For these reasons avian
models have often been used to investigate different aspects of the visual system.
The optic nerves in birds are almost completely decussated (Weidner, Reperant, Miceli, Haby,
& Rio, 1985), furthermore the birds brain has a limited amount of interhemispheric
commissures (Bischof & Watanabe, 1997; Ehrlich & Saleh, 1982; Saleh & Ehrlich, 1984) and
a lack of corpus callosum. Due to these unique characteristics, cerebral asymmetries, using the
avian visual model, have been broadly investigated. These asymmetries represent an important
neural principle in many vertebrates brains, including humans (Rogers & Andrew, 2002).
There is much evidence indicating that interhemispheric interactions may be an important
component for understanding visual asymmetries (Gntrkn & Bohringer, 1987; Keysers,
Diekamp, & Gntrkn, 2000; Parsons & Rogers, 1993). In this context, the study of
interocular transfer and intraocular transfer of information in the avian brain may also
contribute to a better understanding of visual asymmetries in vertebrates.
Many studies about asymmetries have been done in chickens and pigeons (Gntrkn, 1997a).
As a result, we have a better understanding of the visual system of those animals (Zeigler &
Bischof, 1993), although there are still many unresolved questions. One open question is the
role of head-bobbing in visual perception. Pigeons and chickens are head-bobbing birds, that
is, they move the head backward and forward while walking and landing (Dagg, 1977b;
Dunlap & Mowrer, 1930).
Head-bobbing is present in at least 40% of the birds, furthermore it has been demonstrated that
head-bobbing is controlled visually (Friedman, 1975b).The head-bobbing function is not yet
well understood, however the contribution of head-bobbing in visual perception is widely
accepted (Davies & Green, 1988; Friedman, 1975; Green, Davies, & Thorpe, 1992; Green,
Davies, & Thorpe, 1994; Troje & Frost, 1999, 2000).
Very often in inter- and intraocular transfer studies, the possible role of optic flow and headbobbing in visual perception was not considered. In most cases, the experimental conditions of
the studies prevent the birds to show head-bobbing (examples can be found in: Mallin &
Delius, 1983 ; Nye, 1973; Remy & Emmerton, 1991b; Roberts, Phelps, Macuda, Brodbeck, &
Russ, 1996). In addition, there are few experiments investigating interocular transfer between
the yellow visual fields. This is probably due to the difficulties in training pigeons to solve
visual tasks in the lateral visual field (Remy & Watanabe, 1993).
The main aim of this work is to combine these two aspects of the visuals system in birds: on
the one hand to contribute to a better understanding of information transfer and its
asymmetries, and on the other hand to investigate the functional significance of head-bobbing
in birds.
1.2 Intraocular and interocular transfer in pigeons

Pigeons and many other birds have lateralised eyes. The Pigeons eye is specialised to acute
near binocular vision at short distances during pecking and to panoramic vision at long
distances (Bloch & Martinoya, 1982a; Goodale, 1983). These two different visual functions are
mediated by two separate visual fields that project into two retinal areas: a binocular dorsotemporal red field and a monocular yellow field. The red field is pointing into the lower visual
field, while the yellow field is pointing into the upper frontal and lateral visual fields.
In a natural situation a bird might perceive stimuli with both eyes, and also with different areas
of the retina. The main goal of inter- and intraocular transfer experiments is to clarify the way
in which information retrieved from both eyes and different retinal areas is integrated in birds
brains (Remy & Watanabe, 1993).
1.2.1 Intraocular transfer of information

Intraocular transfer experiments in birds are infrequent and difficult to interpret (Remy &
Watanabe, 1993). Two main limiting factors are responsible for that: first it is difficult to
establish the retinal area in which the stimuli are presented in freely moving subjects; second
training birds in the lateral visual field has been proved to be an arduous task.
The first attempt to train birds in the lateral visual field was done by Nye (1973). He trained six
pigeons in 4 different tasks: rectangular bar detection task, rotating disk of bars detection
task, colour (red and green) and brightness (high and low) discrimination tasks. Birds learned
the task successfully when the stimuli were presented behind the pecking keys in the frontal
visual field. In contrast, when the stimuli were presented laterally in screens located 90 to each
side of the axis of the beak, the response of the birds dropped to chance level. Further attempts
to train the birds with stimuli presented in the lateral screens did not succeed. The pigeons
performed at chance level after weeks of training in the bar and rotating disk detection
tasks. For colour and brightness discrimination the author trained the pigeons initially in the
frontal visual field and moved the screens in 18 azimuth steps to the lateral sides. A
progressive drop of percentage of correct responses to chance level occurred when approaching
90. Nye concluded that pigeons do not possess the neural capability required to learn to use
information contained in laterally located stimuli to directly control pecking behaviour.
In a previous experiment, Levine (1952) found a drop in the discrimination performance when
the stimuli were shifted from a subrostral to an anterorostral position. He interpreted these data
as a lack of intraocular transfer in pigeons between two separate functionally independent
retinal areas.
Mallin and Delius (1983) conducted an intraocular transfer experiment in head fixed pigeons.
The birds were trained to discriminate two coloured lights using jaw movements
(mandibulando) as an operant response. They found a weak transfer of light colour
discrimination from one locus to another within the visual field of the same eye. Interestingly,
they also found a poor intraocular discrimination transfer of coloured lights when the stimuli
were shifted from frontal to lateral position and vice versa. However, the transfer from lateral
to frontal position was slightly better (around 10%) than the reverse performance. These
observations were confirmed by Remy and Emmerton (1991b) in head-fixed pigeons, who
described the existence of information transfer from the lateral to frontal visual field and
observed a lack of information transfer from the frontal to the lateral visual field in a light
discrimination task.
Most recently, Roberts et al. (1996) trained eight unrestrained pigeons in an experimental
chamber to perform a symbolic delayed matching to sample task. The results confirm previous
findings obtained in head-fixed pigeons (Mallin & Delius, 1983; Remy & Emmerton, 1991b),
that is, there is intraocular transfer of information from the lateral to the frontal visual field, but
not vice versa. They also demonstrated that pigeons are capable of discriminating stimuli in the
lateral visual field, in contradiction to Nyes hypothesis (1973).
Two main suggestions have been proposed to explain intraocular transfer asymmetries. First,
Nye (1973) argued that pigeons were incapable of learning a discrimination task that requires a
pecking response when the stimuli are presented in the lateral visual field. However, it has
been demonstrated that pigeons are capable of stimulus discrimination in the lateral visual field
(Bloch & Martinoya, 1982b; Goodale & Graves, 1982; Mallin & Delius, 1983; Remy &
Emmerton, 1991b; Roberts et al., 1996). Second, it has been proposed that intraocular transfer
of information from the lateral to the frontal visual field may be an ecological advance. On the
one hand, birds should be able to switch from lateral to frontal vision when perceiving food
and approaching to peck (Friedman, 1975; Remy & Emmerton, 1991b; Roberts et al., 1996). In
addition, intraocular transfer from lateral to frontal visual field may be required to monitor the
environment for approaching predators while the frontal vision is occupied in feeding (Remy &
Emmerton, 1991b; Roberts et al., 1996). On the other hand, there is no need for information
transfer from the frontal to the lateral field. Usually objects processed by the lateral visual field
are not seen in the frontal field first (Roberts et al., 1996). Field observations suggest that if an
object is processed by the lateral visual field, it is often shifted to the frontal visual field but
rarely vive versa.
1.2.2 Interocular transfer of information

Interocular transfer has been traditionally studied by covering one eye during the process of
learning a visual task. Once the bird reaches a certain criterion of performance, the naive eye
is tested in the same task (Goodale & Graves, 1982).
According to Levine (1945a), the earliest interocular transfer experiment was done in 1917 by
Khler. He observed that chickens showed interocular transfer in discriminating two sheets of
grey paper differing in brightness, which were located horizontally at ground level. In contrast
to Khlers findings, a lack of interocular transfer was found in pigeons trained monocularly in
a go/no-go colour discrimination task. In this experiment the stimuli were displayed on a
vertical screen above ground level (Beritov & Chichinadse, 1935).
Levine conducted a set of experiments using a jumping stand in which birds were placed in a
rotating perch that forced them to jump onto one of two platform according to different stimuli
(colours and shapes discrimination) (Levine, 1945a, 1945b, 1952). If the bird chose the
incorrect platform according to the presented stimuli, it collapsed and the animals dropped into
a net. If the correct platform was chosen, the birds were allowed to stay there for 15 seconds.
He observed that information transfer between the two eyes in pigeons depends on the location
of the stimuli in the visual field with reference to the position of the birds head. If the stimuli
were presented horizontally in a plane below the pigeons head (subrostral), interocular transfer
was present. In contrast, if the stimuli were presented vertically in front of the pigeons head
(anterostral) there was an absence of transfer (Levine, 1945a, 1945b, 1952). Two hypotheses
were proposed to explain these results: the sensorimotor integration hypothesis ( Watanabe,
1986) and the retinal locus hypothesis (Goodale & Graves, 1982; Levine, 1945b; Mallin &
Delius, 1983).
The sensorimotor integration hypothesis proposes that pigeons may transfer information
depending on whether the response (manipulandum) and the stimuli (stimulandum) have
the same or different spatial locations. When manipulandum and stimulandum share the same
spatial locations, for example the stimulus is presented on the surface of the pecking key,
interocular transfer of information is expected. If they are located in different spatial location a
lack of interocular transfer is predicted (Remy & Watanabe, 1993).
To test the sensorimotor integration hypothesis, pigeons were trained in three conditional
spatial tasks employing two pecking keys arranged either vertically or horizontally (Watanabe,
1986). No matter whether the keys were arranged horizontally or vertically, if manipulandum
(response of the pigeon) and stimulandum were located in the same pecking key, there was a
perfect interocular transfer of information. However, if manipulandum and stimulandum were
located in different keys (for example: the stimulus was presented in the lower key and the
pigeons had to peck in the upper key) the pigeons were incapable of interocular transfer.
The retinal locus hypothesis proposes that interocular transfer occurs when the stimuli are
presented in the dorso-temporal part of the retina (red field), but not when the stimuli are
presented in the other parts of the retina (yellow field) (Goodale & Graves, 1982). The first
author supporting this hypothesis was Levine (1952). He proposed that in the pigeons eyes
there are at least two independent visual areas: a retinal locus corresponding to the subrostral
position in the visual field (below the head) and a retinal locus pointing into the anterostral
position (in front of the head) of the visual field. He argued that only the subrostral retinal
locus has the required neural connections which mediate interhemispheric transfer of
information. Furthermore, anterostral-subrostral transfer did not occur within a single eye.
Catania (1965) challenged this hypothesis by training pigeons to peck on a key located in front
of the pigeon head, in brightness, colour and pattern discrimination tasks. The stimuli were
projected either on the frontal key or on one of two lateral screens. Pigeons showed interocular
transfer of information in both conditions. Catania offered two explanations for the lack of
interocular transfer in Levines experiments. Pigeons are laterally far-sighted and anteriorly
near sighted. In the jumping stand, the pigeons have to cock their head to one side in order to
observe the stimuli with the lateral visual field. The direction in which the head has to be
cocked depends on the covered-eye, and therefore this change of posture may affect interocular
transfer of information. Moreover, the amount of training may influence interocular transfer: In
Catanias studies the pigeons might have been over-trained in comparison to the pigeons in
Levines experiments (Catania, 1965).
A set of experiments replicating Levines jumping stand were designed to investigate Catanias
postural hypothesis (Goodale & Graves, 1982). Furthermore, the authors conducted several
key-pecking (FR1) discrimination tasks to test training amount and task difficulty as possible
factors in interocular transfer. They claimed that the lack of interocular transfer was a genuine
phenomenon which did not depend on postural habit, amount of training and task complexity.
Furthermore, birds trained binocularly in the jumping stand often showed evidence of learning
with only one eye when tested monocularly. They concluded that: the lack of interocular
transfer found in situations such as the jumping stand is a consequence of the discriminative
stimuli falling within the monocular field. Therefore, Goodale and Graves (1982) proposed
that interocular transfer occurs when the stimuli were projected into the red field, but not when
they were presented to the yellow field
Mallim and Delius (1983) conducted an experiment with head fixed pigeons using jaw
movements (mandibulando) as an operant in a colour discrimination task. They presented two
coloured lights in different locations of the retina. The advantage of this experimental design is
that the spatial localization of the stimuli is separated from the response and the presentation of
the stimuli in a certain retinal locus is controlled. Birds showed interocular transfer of
information when the discrimination task was monocularly presented inside the red field and a
lack of interocular transfer when the stimulus was presented within the yellow field. These
results support the retinal locus hypothesis, although Remy and Watanabe (1993) pointed out
that, in this task, pigeons did not need to direct their response spatially. Furthermore, the
pigeons beak was oriented towards the position of the stimuli in the frontal position, whereas
during the lateral stimulation the beak is oriented in a different direction.
The retinal locus and sensorimotor integration hypotheses may not be contradictory.
Retinal locus may be crucial when a task does not require sensorimotor integration. However,
if a task requires sensorimotor integration, interocular transfer will not occur even when the
stimuli falls into the binocular field (Remy & Watanabe, 1993).
In addition, some experimental findings suggest that other characteristics of a task, such as
biological relevance, may influence interocular transfer. A lack of interocular transfer was
found in avoidance of the visual cliff (Zeier, 1970). Transfer of information was absent in heat
reinforcement but it was present in a similar task using food reinforcement (Gaston, 1984).
Interocular transfer was also observed in taste aversion in chicks (Bell & Gibbs, 1979; Gaston,
1984), as well as in cardiac conditioning in pigeons (Mihara & Watanabe, 1982) and in
conditioned withdrawal in pigeons, chickens and gulls (Stevens & Klopfer, 1977).
Furthermore, interocular transfer in pigeons colour discrimination but not in motor response
training has been found (Stevens & Kirsch, 1980). Pigeons eyes were occluded during initial
acquisition of the pecking response and subsequently during learning colour discrimination.
When the animals were tested with the occluded eye they were unable to respond. Once the
pigeons were trained to peck a blank response key, transfer of the colour discrimination task
was observed. This is an interesting result, because most of the pigeons discrimination
experiments involve training of the motor response under binocular condition prior to
monocular training on the experimental task. Additional studies of interocular transfer of the
motor response would be useful to explain this phenomenon (Remy & Watanabe, 1993).
In a recent publication, interhemispheric transfer of memories was tested in pigeons
(Nottelmann, Wohlschlager, & Gntrkn, 2002). Pigeons task was to peck on one of two
vertical keys according to a pattern displayed on both keys. Six pairs of patterns were used, for
half of these pairs the animals had to peck the upper pattern, for the other half the lower one.
Transfer of information from the left eye/right hemisphere to the right eye/left hemisphere, but
not vice versa was observed. In this experiment, stimuli are presented within the red field and
sensorimotor integration occurs, however a lack of interocular transfer is found when the
stimuli are presented in the right hemisphere. Therefore, asymmetries in bird brain should be
considered as an important factor for interocular transfer. Most probably, asymmetries and
interocular transfer of information are interrelated phenomena in birds. In fact, Skiba et al
(2000) found asymmetries in interocular transfer of information. A faster shift of learned
colour cues from the dominant right to the left eye than vice versa was reported.
Finally, it should be noted that none of the hypotheses is capable of explaining all experimental
results in interocular transfer. The retinal locus hypothesis together with the current
knowledge of the anatomic aspects and asymmetries will lead to a better understanding of the
interocular transfer phenomenon.
1.2.3 Interim summary

The main goal of inter- and intraocular transfer experiments is to clarify the way in which
information retrieved from both eyes and different retinal areas is integrated in birds brains.
Interocular transfer experiments test the transfer of information between the two eyes (i.e.,
between the two hemispheres), whereas intraocular transfer experiments test the transfer of
information between different retinal areas of the same eye.
Birds have two distinctive retinal areas: a lateral monocular yellow field and a frontal binocular
field, often called the red field. Intraocular transfer has been investigated training the animals
to solve a visual task presented in one of these two visual fields and testing in the other.
Investigations in non walking pigeons have demonstrated that there is information transfer
from the lateral to the frontal visual field. However, a lack of transfer was found from the
frontal to the lateral visual field.
In birds, interocular transfer has been traditionally studied by covering one eye during the
process of learning a visual task. Once the animal reaches a certain criterion of performance,
the naive eye is tested in the same task. Interocular transfer depends on the experimental
conditions and the task. Two main hypotheses have been proposed to explain the presence or
absence of interocular transfer: the sensorimotor integration hypothesis and the retinal
locus hypothesis.
The sensorimotor integration hypothesis proposes that pigeons may transfer information if
the response and the stimuli share the same spatial locations. In contrast, if they do not share
the same spatial location, a lack of interocular transfer will be observed. The retinal locus
hypothesis proposes that interocular transfer occurs when the stimuli are presented within the
red field, but not when the stimuli are presented in the yellow field.
1.3 Visual asymmetries in birds

Birds are highly visual animals, their visual capabilities are the most specialised among
vertebrates (Gntrkn, 2003). The optic nerves in birds are almost completely decussated
(Weidner et al., 1985). In addition, the amount of thalamic and mesencephalic commissures in
birds is very limited (Bischof & Watanabe, 1997; Ehrlich & Saleh, 1982; Saleh & Ehrlich,
1984). Consequently, hemispheric asymmetries can be easily investigated by directing the
visual information to one hemisphere by the simple mechanism of temporarily covering one
eye.
These characteristics make the avian visual system a very valuable model for the study of
visual asymmetries. Many studies in visual asymmetries have been done by using a variety of
birds species, like marsh tits (Clayton & Krebs, 1994a), domestic chicks (Andrew, 1988;
Andrew & Dharmaretnam, 1993; McKenzie, Andrew, & Jones, 1998; Rogers & Andrew,
2002, Parsons, 1993 #3354), zebra finches (Alonso, 1998; Voss & Bischof, 2003), European
starlings (Hart, Partridge, & Cuthill, 2000), quails (Valenti, Sovrano, Zucca, & Vallortigara,
2003) and pigeons (Gntrkn & Bohringer, 1987; Gntrkn et al., 2000; Gntrkn &
Hahmann, 1994; Prior & Gntrkn, 2001; Prior et al., 2004; Skiba et al., 2000).
1.3.1 Right eye/left hemisphere dominances

Monocular occlusion studies revealed a right eye/left hemisphere dominance in discriminating
two-dimensional artificial patterns in pigeons (Gntrkn, 1985) and three dimensional natural
objects by means of a grain-grit task in pigeons (Gntrkn & Kesch, 1987), zebra finches
(Alonso, 1998) and chickens in a pebble-floor task (Mench & Andrew, 1986). Right eye
system dominance is also found in pattern discrimination (Gntrkn, 1997a). A higher degree
of illusion is observed for the right eye, when the birds were stimulated with geometrical optic
illusions (Gntrkn, 2003).
Some complex studies in pigeons have shown that memories of visual engrams and pattern
information are stored unilaterally in the left hemisphere (Gntrkn, 1997a; Nottelmann et al.,
2002; von Fersen & Gntrkn, 1990). This asymmetry, in memorizing visual stimuli, most
probably results in a right eye/left hemisphere advantage in homing (Ulrich et al., 1999),
although when pigeons are tested in circumstances in which they cannot rely on visual cues,
like landmarks, the left hemisphere advantage vanishes (Prior, Lingenauber, Nitschke, &
Gntrkn, 2002). A right eye dominance is also found in large-scale homing as a consequence
of a strong lateralisation of the avian magnetic compass and optic flow processing in favour of
the left hemisphere (Prior et al., 2004).
There is evidence for left hemisphere asymmetries in cognitive processes such as learning-tolearn. In a colour discrimination reversal learning task birds learned faster with their right
eye/left hemisphere than with the left eye/right hemisphere (Diekamp, Prior, & Gntrkn,
1999)
Although, it has been demonstrated that the European starling shows an asymmetric
distribution of photoreceptors in the retina, the majority of the asymmetries described are
attributed to genuine central processes. They are not due to peripheral factors such as visual
acuity (Gntrkn & Hahmann, 1994), wavelength discrimination (Remy & Emmerton,
1991a), or depth resolution (Martinoya, Rivaud, & Bloch, 1983).
Due to the amount of evidences in favour of the left hemisphere superiority, accumulated early
in the literature, it has been postulated as the dominant hemisphere. At the moment, it is
believed that none of the avian hemispheres dominates completely the visual analysis
(Gntrkn, 2003). In fact, there is also evidence for right hemisphere superiority in a variety
of tasks.
1.3.2 Left eye/right hemisphere dominances

Left eye/right hemisphere dominance has been observed in geometric or spatial information in
marsh tits (Clayton & Krebs, 1994b) and chicks (Tommasi & Vallortigara, 2001; Vallortigara,
2000). A right hemisphere dominance is also found for social recognition, like aggressive and
sexual responding, in chicks (Rogers & Andrew, 2002; Vallortigara, 1992). Wild living
Kookaburras (Dacelo gigas) search for food on the ground using preferably their left eye
(Rogers, 2002). In pigeons, a left eye/right hemisphere advance was found in choice reaction
times to a patter discrimination task (Di Stefano, Kusmic, & Musumeci, 1987). Most recently,
left eye/right hemisphere dominances was observed in the spatial distribution of attention
related to food detection for pigeons and chickens (Diekamp, Regolin, Gntrkn, &
Vallortigara, 2005).
The opposite left-right specialisation hypothesis for the lateral and frontal visual fields propose
that the left eye/right hemisphere may be dominant in the lateral visual field which is mainly
focused at long distances, whereas the right eye/left hemisphere may be dominant in binocular
vision which is specialised on short distance visual processes (Evans & Evans, 1999; Evans,
Evans, & Marier, 1993; Rogers, 2000; Vallortigara, Cozzutti, Tommasi, & Rogers, 2001).
In fact, in the majority of the experiments in visual asymmetries, the stimuli were shown in the
frontal binocular visual field, which is mainly analysed by the tectofugal pathway (Gntrkn
& Hahmann, 1999; Skiba et al., 2000). However, some evidences of lateral visual field
processing have arisen recently. Chickens fixated approaching predators by turning the head
abruptly to one side preferably using the left eye (Evans et al., 1993) and showed shorter
reaction times using the left eye to detect a novel moving stimuli (a model raptor) (Rogers,
2000). In contrast, hens responded to a food call by fixating downward with the frontal visual
field. This pattern was not observed when alarm calls and contact calls were presented (Evans
& Evans, 1999). Furthermore, Social recognition experiments showed that chickens use either
the lateral field of its left eye, or the frontal field of the right eye, before pecking at a stranger,
but not at cagemates (Vallortigara et al., 2001).
Having a lateralised brain may allow dual attention to short distance tasks like feeding (using
the right eye/left hemisphere system) and long distance tasks like vigilance for predators (left
eye/right hemisphere system) (Rogers, 2000).
A recent study with pigeons found a left hemisphere dominance of the thalamofugal visual
pathway in a pattern discrimination task in an open arena (Budzynski & Bingman, 2004). The
thalamofugal pathway receives information from the lateral visual field, and therefore it is
assumed that it may be specialised in far field information processing. Therefore, the left
hemisphere dominance in the open arena may contradict the opposite left-right specialisation
hypothesis for the lateral and frontal visual fields in chicks. Moreover, the main asymmetry
was observed in the visual wulst, a structure that belongs to the thalamofugal pathway but also
contributes to the tectofugal pathway (Bagnoli, Grassi, & Magni, 1980; Engelage & Bischof,
1994; Folta, Diekamp, & Gntrkn, 2004; Miceli, Reperant, Villalobos, & Dionne, 1987).
However, it should be taken into consideration that the retinal projection of the stimuli was not
controlled.
Two more alternatives for explaining hemispheric specialisation have been discussed in the
literature. The right eye/ left hemisphere in chicks may be involved in the analysis of novelty
and in the spatial configuration of the environment (R.J. Andrew & Dharmaretnam, 1993).
This proposal is not in contradiction with the opposite left-right specialisation hypothesis for
the lateral and frontal visual fields, indeed a novel stimulus may be perceived first with the
lateral visual field.
In addition, asymmetries in the birds visual system may increase the computational speed of
certain processes by concentrating them into one hemisphere. A good example is that visual
lateralisation improves grain-grit discrimination success in pigeons (Gntrkn et al., 2000).
Furthermore in a double task, like finding food and being vigilant for predators, not-lateralised
chicks perform worse than lateralised ones (Rogers, Zucca, & Vallortigara, 2004).
Consequently to the ecological advantages of being capable to attend to both predators and
feeding source, the computational advantages of processing information in one hemisphere
should be added. Most probably the asymmetric avian brain is a consequence of the interaction
between the ecological and computational advantages mediated by the anatomical substrate.
1.3.3 Asymmetric interhemispheric transfer

Various studies have investigated asymmetries of transfer between the two hemispheres. Such
investigations can give valuable cues to understand interhemispheric transfer, visual
asymmetries, and their interactions.
In chickens, a poorer interocular transfer of information from the left eye system to the right
eye system than in the opposite direction was described. A passive avoidance task was used, in
which birds learned to avoid a bead covered with a bitter substance. Binocular and right lesions
in the intermediate hyperstriatum ventrale (IMHV) resulted in amnesia (in monocularly trained
birds) when the chicks were tested with the left eye open. On the other hand, left IMHV lesions
did not impair performance regardless of the eye used (Sandi, Patterson, & Rose, 1993).
Furthermore, lesions in the left IMHV right after training induced amnesia in binocularly
trained birds, whereas bilateral ablations of IMHV lesions made one and six hours posttraining did not result in amnesia (Patterson, Gilbert, & Rose, 1990). Sandi et al (1993)
explained those results as a consequence of a relationship between lateralisation of IMHV
function and the visual asymmetries which occur at the behavioural and structural level. They
proposed a model in which the memory trace is not fixed into the left IMHV, but it is
transferred within one hour to the right IMHV.
Another IMHV asymmetry has been found in chicks imprinted with an artificial object. Lesion
studies showed that within the first hours after imprinting there is information transfer from left
IMHV to the right IMHV which may be responsible for storing the visual characteristics of the
imprinted object (Horn, 1991; Nicol, Brown, & Horn, 1995).
An asymmetrical transfer of information has been found in marsh tits for memory storage.
Monocular occlusion was used to investigate lateralisation and memory transfer in a food
storing and in a one-trial associative learning task. In both cases it was found that both eyes are
involved in short-term storage, whereas only the right eye system is responsible for long-term
storage. The results indicated that memories are transferred from the right to the left eye
system between 3 and 24h after the memory formation. Seven hours after the memory
formation, the engram is no longer accessible to the left eye system but has not yet reached the
right eye system (Clayton, 1992; Clayton & Krebs, 1994).
In pigeons, it has been demonstrated that each hemisphere shifts colour information to the
contralateral side, but the efficiency of the transfer is time and side dependent. There is a faster
shift of learned colour cues from the right to the left eye than vice versa within the first 50
minutes after acquisition. For intervals longer than 3 hours, no differences have been found
(Skiba et al., 2000). The authors of this experiment concluded that inter-ocular transfer from
the right to the left eye should be facilitated due to a higher bilateral representation of the leftsided tectofugal pathway.
The interhemispheric asymmetries in food storing, colour discrimination and passive avoidance
are not in the same directions. Those differences may arise by the diverse types of cognitive
processes required for each task (Skiba et al., 2000). For example, a storing food task demands
the utilization of spatial cues which are mainly processed in the right hemisphere, whereas
visual cues needed for a pattern discrimination task are processed mainly in the left
hemisphere. For giving a coherent explanation of interhemispheric asymmetry patterns, three
factors should be considered, functional asymmetries, time course, and physiological
characteristics.
In birds, right eye/left hemisphere dominance is observed in pattern discrimination, stimulus
categorization and memory of visual stimuli. In contrast, left eye/right hemisphere superiority
has been found in processing geometric information, social recognition like aggressive and
sexual responding. It has been recently proposed that the right eye/left hemisphere may be
dominant for short distance tasks like feeding, whereas the left eye/right hemisphere may be
specialised in long distance tasks like vigilance. In addition having an asymmetric brain may
increase computational speed and allow dual attention to short and long distances.
Asymmetries in the information transfer between the two hemispheres have also been
described. In a passive avoidance task a poorer interocular transfer of information from the left
eye system to the right eye system than in the opposite direction was found. In Marsh tits,
memories are transferred from the right to the left eye system between 3 and 24h after the
memory formation. In pigeons, it has been demonstrated that there is a faster shift of learned
colour cues from the right to the left eye than vice versa, within the first 50 minutes after
acquisition.
1.4 Head-bobbing in birds

Pigeons, chickens, moorhens, partridges, storks, crows, ibises, and many other birds show a
characteristic head movement while walking (Dagg, 1977b; Davies & Green, 1988; Dunlap &
Mowrer, 1930; Friedman, 1975; Friedman, 1975; Frost, 1978). In pigeons, the head moves
backward and forward with respect to the body with a frequency that ranges from about 2 to 10
Hz (Troje & Frost, 2000). Head-bobbing is characterized by a hold phase and a thrust phase
(Fig. 2). During the hold phase the head of the bird remains stable in space (Frost, 1978; Troje
& Frost, 2000), whereas during the thrust phase the head is moved forward (Fig. 1 and Fig. 2).
In pigeons, heead-bobbing movement has been observed during walking, landing flight
(Davies & Green, 1991), prior to pecking (Goodale, 1983), and in other behaviours. Even a
stationary bird actively observing its environment, shows head-bobbing behaviour.
Head-bobbing was first described in 1930 by Dunlap and Mowrer. Since then, three main
functions have been proposed, a biomechanical function and two visual functions: image
stabilization and depth perception through motion parallax.
Horizontal displacement (pixels)
Head movement of a walking moorhen

1400
1200
1000
800
600
400
200
0
0.2
0.4
0.6
0.8
1.2
1.4
Time (s)
Figure 1: Head position of a walking moorhen (Gallinula chloropus) in freedom. The head position in space was
obtained by frame by frame analysis of walking moorhen video recordings. The horizontal coordinate of the head
position, given by pixels, was plotted against the time.
1.4.1 Biomechanical function

In walking birds, head-bobbing is synchronized with the motion of the feet (Dagg, 1977a;
Dunlap & Mowrer, 1930). For this reason, the first attributed function to head-bobbing was a
biomechanical function (Dagg, 1977b). However, later it was shown that head-bobbing is
controlled visually and can be elicited independently of active locomotion (Friedman, 1975;
Friedman, 1975; Frost, 1978). Although this finding points clearly to a visual function, headbobbing may also have a biomechanical correlation. Body movements are synchronized with
head movements in various behaviours and the stride length of a walking bird is correlated
with the relative magnitude of head-bobbing (Fujita, 2004). Troje and Frost (1999) proposed a
central pattern generator involved in coordinating complex motion patterns. Eye stabilization
may play a role in enhancing equilibrium during walking (Fujita, 2002).
1.4.2 Image stabilization

Some remarkable evidences supporting the visual function of head-bobbing were found in
Ring Doves (Friedman, 1975). A single bird was trained to walk inside a cylindrical cage; at
least two of the six experimental conditions demonstrated an unequivocal dissociation between
walking and head-bobbing. In one condition, the bird walked on a mobile false floor while the
cage and the visual surrounding were static. Head-bobbing was not observed in this case. In
another experimental condition, the bird remained static on the floor but the cage was moved
smoothly in a rostral-to-caudal direction, provoking optic flow. A clear head-bobbing
behaviour was observed in this situation. These findings were corroborated in pigeons: headbobbing was abolished when the animals walking on a treadmill matched the belt velocity,
confirming that head-bobbing is visually elicited (Frost, 1978).
Taking in account those results, it was suggested that the hold phase could be similar to other
optokinetic behaviours stabilizing the retinal image (Frost, 1978). During the hold phase the
head is not completely stabilized, but it slips slightly providing the necessary error signal that
drives the compensation mechanism to stabilize the head (Frost, 1978; Troje & Frost, 2000).
Stabilizing the retinal image allows object recognition and allows the visual system to
distinguish between self motion and outside world motion (Davies & Green, 1988; Frost, 1978;
Troje & Frost, 1999). Whooping cranes, during foraging, walk at speeds that permit them to
keep their heads immobilized with respect to the visual surroundings while covering large
search areas (Cronin, Kinloch, & Olsen, 2005). In spite of the fact that image stabilization is
widely accepted as a head-bobbing function, it has been found that in running and landing
pigeons the hold phase is replaced with a flexion phase which maintains alternation between
two different head velocities. However, in these cases the retraction of the head does not
compensate the fast forward movement of the body and the head is not stabilized (Green, 1998;
Green et al., 1994). These observations suggest that head-bobbing may have several functions
depending on the situations and environmental demands.
1.4.3 Motion parallax

During the thrust phase, pigeons and other birds may use motion parallax computation to
derive distances. Pigeons and many other birds like ibises, storks, partridges, chickens,
woodcocks etc. have laterally placed eyes with very small binocular fields. Stereo vision as a
cue for depth perception can play a role only in a very restricted area. It is therefore assumed
that birds use motion parallax to monocularly derive depth information (Green et al., 1994).
Figure 2: Stroboscopic image from a walking pigeon
that illustrates the typical head-bobbing which consists
of a period in which the head remains fixed in space
(hold phase) and a period in which it is quickly moved
forward (thrust phase). From: (Frost, 1978).
Several animal species discriminate depth through motion parallax: locust (Collett, 1978;
Wallace, 1959), praying mantis (Kral, 1998, 2003; Poteser & Kral, 1995; Poteser, Pabst, &
Kral, 1998), barn owl (van der Willigen, Frost, & Wagner, 2002) and gerbils (Goodale, Ellard,
& Booth, 1990). Those animals perform head movements called peering in order to generate
the necessary optic flow for motion parallax computation. Bees are also capable of calculating
depth through motion parallax taking advantage of the ambient optic flow generated during
flying (Lehrer, Srinivasan, Zhang, & Horridge, 1988).
Motion parallax computation is based on the fact that a translation of the eye induces a
displacement of the retinal image of an object. The translation of the eye xh and the
displacement of the retinal image of an object xr are related by the ratio of the focal length f
of the eye and the distance d of the object (Fig. 3).
x h
d = f --------x r
Figure 3: Motion parallax computation
where d is the distance to the object,
f is the focal length, xh is the
translation of the eye, and xr is
translation of the retinal image.
The displacement of the eye xh and the corresponding shift of the retinal image xr can well
be replaced by the respective velocities vh and vr:
vh
d = f ----vr
Whereas f is an anatomical constant and vr can be derived directly from the visual input, the
velocity of the eye with respect to the visual surroundings vh has to be determined
independently. In a walking bird this may be achieved by propioceptive and vestibular
information. In praying mantis the propioceptive cervical hair plate sensilla are involved in the
measurement of the distance to a jump target with the aid of motion parallax actively produced
by translatory head motion (Poteser et al., 1998).
1.4.4 Head-bobbing birds

Although head-bobbing behaviour has been very often discussed in the literature, there exists
no comprehensive list about which birds do and which ones do not. Frost (1978) reported that
head-bobbing occurs in at least 8 of the 27 orders of birds, such as pigeons, doves, hens,
starlings, pheasants, coots, moorhens, rails, sand-pipers, phalaropes, parrots, magpies, and
quails. Dagg (1977) listed 28 head-bobbing and 21 non head-bobbing species during
locomotion. These lists are rather incomplete and some birds could be misclassified, but they
suggest that at least 1/3 of the birds could show head-bobbing. Furthermore, the ecological
behavioural and phylogenetic information have been rarely considered in the study of headbobbing.
To our knowledge, apart from these reports there is a lack of information in the literature about
head-bobbing birds. Most of the articles focus on pigeons head-bobbing behaviour without
retrieving data about other species that could help to clarify its functional significance.
An unanswered question is why some birds bob their heads, whereas other birds walk without
bobbing their heads. Furthermore, it is not a clear answer why some species of birds walk with
or without displaying head-bobbing. Some birds like magpies can walk with head-bobbing, run
or hop. Head-bobbing during walking is used for low velocities, whereas running and out-ofphase hopping are alternative gaits for higher speed in magpies. Furthermore, it is not known
why some birds use running and hopping as alternative gaits and why they prefer hopping over
running at high speeds (Verstappen, Aerts, & Van Damme, 2000).
Dagg (1977) reported that Mynah birds and starlings alternated between walking with headbobbing and hopping, depending on the speed of the motion. Birds that walk and bob their
heads tend to be of intermediate size. Small birds like most of the Passeriformes, living in
bushes and trees, with short legs tend to hop rather than walk (Friedman, 1975).
Hopping behaviour in birds may be comparable to head-bobbing and may play a similar role
(Davies & Green, 1988; Friedman, 1975). A frame by frame analysis of hopping sparrows
(Passer domesticus) while foraging reveals that birds head is thrust forward before the legs
start to push the body into the air. Likewise, the head stops and is stabilized in the visual space
before the body finished landing from the hop. This behaviour is also observed in alert
sparrows but not in somnolent ones (Friedman, 1975).
Many birds show a characteristic forward and backward head movement while walking,
running, and during landing flight called head-bobbing. It is characterized by a hold phase and
a thrust phase. Typically, during the hold phase the head of the bird remains stable in space
while during the thrust phase the head is moved forward. Three main functions for headbobbing have been proposed: biomechanical function, image stabilization, and depth
perception through motion parallax. Although head-bobbing behaviour has been very often
discussed in the literature, most of the birds that bob their heads are not listed. Dagg (1977) and
Frost (1978) reported that head-bobbing occurs in at least 8 of the 27 orders of birds and in 28
species such as pigeons, doves, hens, starlings, pheasants, etc. It has been proposed that
hopping in birds could be comparable to head-bobbing. It is not known why head-bobbing
occurs in some species of birds but not in others. Further investigations are required to
investigate the functional and ecological significance of head-bobbing behaviour.
1.5 Anatomical substrate

The avian visual system is composed of two parallel visual pathways that process retinal
information from different parts of the retina: the thalamofugal and the tectofugal pathway. In
addition the accessory optic system is dedicated to the analysis of optic flow. A comprehensive
understanding of the three pathways is important for any attempt to understand the mechanisms
underlying visual asymmetries, inter- and intraocular transfer of information, and head
bobbing.
1.5.1 The avian eye

Birds have large eyes relative to their body size, suggesting that vision is an important sensory
modality in the class aves (Garamszegi, Moller, & Erritzoe, 2002; Martin, 1993). The small
tawny owl (450g) has eyes with a greater axial length than humans. The diameter of the ostrich
eye is considered to be amongst the largest of all terrestrial vertebrates, with an axial length
close to 40 mm (Martin, 1993; Martin, Ashash, & Katzir, 2001). The resolution power of the
eye does not depend entirely on its size, other important factors like the structure and
concentration of rods and cones on the retina should be considered. Diverse evolutionary
demands, as diurnal or nocturnal activity, result into different kind of eyes that vary in the
absolute size, position, and amplitude of movement (Martin 1993).
The avian retina like the mammals retina consist on by five layers: the outer nuclear and
plexiform layers, the inner nuclear and plexiform layers, and the ganglion cell layer. These
layers contain five kinds of cells: photoreceptors, bipolar cells, horizontal cells, amacrine cells
and ganglion cells (Fig. 4). The photoreceptors, bipolar cells, and horizontal cells make
synaptic contact in the outer retinal layer. The bipolar, amacrine, and ganglion cells make
contact in the inner retinal layer (Husband & Shimizu, 2001).
The avian retina shows some interesting differences compared to mammals. It contains no
blood vessels; the pecten, a highly vascular structure, is responsible for providing nutrients and
oxygen to the cells. Furthermore, it contains double cones, more richer intraretinal connections
like horizontal and amacrine cells (Hayes, 1982; Mariani, 1982, 1987), and complex ganglion
cell response properties (Pearlman & Hughes, 1976). Four different types of cones have been
observed in the avian retina, whereas only three types of cones have been described in the
mammalian retina. The spectral sensitivity ranges from ultraviolet (320nm) to the far red
(650nm) (Remy & Emmerton, 1991a). The presence of oil-droplets covering the cones add
another layer of complexity to the spectral composition of the photoreceptors in the retina.
Figure 4: Avian retina. The photoreceptors, bipolar cells,

and horizontal cells make synaptic contact in the outer
retinal layer. The bipolar, amacrine, and ganglion cells
make contact in the inner retinal layer. Figure from
Husband and Shimizu (2001).
The distribution of eye droplets in the retina defines two retinal areas (Fig. 5). The red field is
characterized by a high concentration of red and orange oil droplets and the yellow field with a
bigger concentration of yellow droplets.
RF
F
YF
Figure 5: Schematic representation of the pigeons retina (modified from Galifret,

1968), where RF is the red field, YF is the yellow field, P is the pecten and F is the
fovea centralis.
The red field located under the beak in the dorso-temporal retinal quadrant points into the
frontal visual field (Bloch & Martinoya, 1982b; Martin & Young, 1983; Martinoya, Rey, &
Bloch, 1981). Within the red field most birds also have an area of enhanced vision, the area
dorsalis which increases the acuity of the frontal binocular visual field (Martin & Katzir,
1999). This area is implicated in close sighting, feeding behaviour and the control of pecking
(Goodale, 1983).
The eyes of most birds are aligned laterally (Martin, 1993), which permits birds to receive and
process information of the lateral visual field through the yellow field. The lateral field also
contains an area of high ganglion cell density called the fovea centralis. This lateral visual
field serves far sighting, monitoring predators and conspecifics, as well as to detect food at
some distance (Fernndez-Juricic, Erichsen, & Kacelnik, 2004; Green et al., 1994). Hens tend
to view distant objects laterally while the preferentially observe objects less than 20-30 cm
away frontally (Dawkins, 2002).
Pigeons and some ground-foraging birds have a localized myopia in the temporal region. It can
be explained as an adaptation that permits pigeons to keep the ground in focus while foraging.
This localized myopia does not appear in the lateral visual field. In consequence, birds are
capable of maintaining in focus panoramic views and therefore monitor relevant information
like predators in the lateral visual field while foraging (Hodos & Erichsen, 1990).
The cyclopean area is the coverage of the total visual field of an animal around the head, that
is, the summation of the frontal and lateral visual fields (Martin & Katzir, 1999). Species with
large eyes have developed sunshade structures (e.g. eyebrows or eye lash-type feathering) and
larger blind areas to minimize sunlight glare (Martin & Katzir, 2000). Large blind areas
correspond to smaller cyclopean field, which might be reasonable in large species with low
predatory risk. However, species with small eyes generally have smaller blind areas and larger
cyclopean fields, because they may need a wider visual field for predators detection and are
not so strongly affected by sunlight (Fernndez-Juricic et al., 2004).
Martin and colleagues classified avian visual fields into 3 basic types and an additional
category (combination of two basic classes) (Martin et al., 2001; Martin & Coetzee, 2004;
Martin & Katzir, 1993, 1994, 1995, 1999, 2000).
Type 1. Visual guidance to food items taken in the bill: the visual projection of the bill tip
falls in the centre of the binocular region. The visual field is defined by an extensive cyclopean
field, with a long vertical but narrow binocular field. For example, rock pigeon, starling and
cattle egret.
Type 2. Non-visual guidance to food items taken with the bill: the projection of the bill falls
in the periphery of the visual field. A big cyclopean field is also expected with a narrow
binocular field, for example, Eurasian woodcock, mallard and teal.
Type 3. Non-visual guidance to food items taken with the feet: the projection of the bill fall
outside of the visual field. The blind area is relatively large and the binocular field is wide but
vertically small, for example tawny owl.
Combination of Types 1 and 3: similar to Type 1 in which individuals visually follow and take
mobile prey; but prey is taken with the feet, for example short-toed eagle.
1.5.2 Visual pathways in the avian brain
Two main visual pathways process visual information in birds: The thalamofugal pathway and
the tectofugal pathway (Fig. 6). The thalamofugal pathway corresponds to the geniculocortical
pathway in mammals, whereas the tectofugal pathway corresponds to the extrageniculocortical
pathway in mammals. These visual pathways are structurally and functionally independent,
although several connections and modulations between them have been described. The
accessory optic system in birds is a third independent visual pathway dedicated to optic flow,
self motion signals, and optokinetic stimulation processing.
left
right
Wulst
CT+CP
TO
TO
Gld
Rt
RF
RF
F
YF
YF
Figure 6: Schematic overview of the thalamofugal (green) and tectofugal pathways (red). Abbreviations: E,
entopallium; GLd, nucleus geniculatus lateralis, pars dorsalis; OT, optic tectum; Rt, nucleus rotundus.
1.5.2.1 Thalamofugal pathway
In pigeons, but not in chickens, the thalamofugal pathway receives visual input from the
yellow visual field (Gntrkn, Miceli, & Watanabe, 1993; Remy & Gntrkn, 1991), which
is transmitted to the contralateral thalamic nucleus geniculatus lateralis, pars dorsalis (GLd).
The GLd projects bilaterally to the visual wulst, a structure located in the telencephalon,
comparable to the striate cortex in mammals (Gntrkn, 2003; Jarvis et al., 2005).
In pigeons, the thalamofugal pathway mainly processes visual input from the lateral monocular
fields of the laterally placed eyes (Gntrkn & Hahmann, 1999; Remy & Gntrkn, 1991;
Vallortigara et al., 2001). However, in chicks, thalamofugal lesions affect frontal viewing in
chicks, suggesting that the thalamofugal system processes frontal visual field information in
chicks, but not in pigeons (Deng & Rogers, 2002).
In chicks, the thalamofugal system is asymmetrically structured by means of more contralateral
visual projections of the left nucleus geniculatus lateralis, pars dorsalis (GLd), to the right
hyperstriatum than vice versa (Deng & Rogers, 2002).
1.5.2.2 Tectofugal pathway

The tectofugal pathway processes visual information proceeding from the entire retina. The
visual input ascends from the retina to the contralateral optic tectum (OT), which projects
bilaterally to the entopallium (E) via the thalamic nucleus rotundus (Rt). The tectofugal
pathway is equivalent to the extrageniculocortical pathway in mammals: the optic tectum
corresponds to the superior colliculus, the nucleus rotundus to the lateral posterior-pulvinar,
and the entopallium to the extrastriate visual areas of the mammalian brain (Gntrkn, 2003;
Jarvis et al., 2005)
Morphological asymmetries have been found in the tectofugal system of the pigeon. In the
tectum and the Rt of pigeons, the soma size of visual cells is larger in the left hemisphere
(Gntrkn, 1997b; Manns & Gntrkn, 1999). The bilateral projections from the tectal
lamina 13 to the Rt lead to representations of both the ipsi- and the contralateral eye in the
tectofugal system of each hemisphere (Gntrkn, 2003). These ipsi- to contralareral
tectorotundal projections are asymmetric (Fig. 6). On the one hand, the quantity of ipsilateral
tectorotundal projections is similar. On the other hand, the number of neurons projecting
contralaterally from the right tectum to the left Rt are approximately twice in number than vice
versa. Therefore, the Rt on the left side receives a massive ipsilateral tectal input and also a
large number of afferents from the contralateral tectum (Gntrkn, Hellmann, Melsbach, &
Prior, 1998). Thus, the pigeons tectofugal system displays significant morphological
asymmetries which might be related to the behavioural lateralisation of the animals. In fact, the
left Rt is involved in acuity discrimination with the right and the left eye, whereas the right Rt
has minor relevance in participating in binocular acuity (Gntrkn & Hahmann, 1999).
Furthermore, there is evidence of asymmetries in the tectal and posterior commissures
connecting the tecta of both hemispheres. Field evoked potential (in response to a stroboscope
flash to the contralateral eye) recorded in the left and right tectum showed that the left-to-right
tectotectal modulation was more pronounced than vice versa (Keysers et al., 2000).
1.5.2.3 Tectofugal-thalamofugal projections

The tectofugal and thalamofugal pathways are not isolated systems, but they are interconnected
by projections from the thalamofugal system onto the tectofugal system and vice versa (Fig. 6
and Fig. 7). The visual wulst sends ipsilateral descending projections directly to the optic
tectum (Bagnoli et al., 1980; Karten, Hodos, Nauta, & Revzin, 1973; Miceli et al., 1987). This
projection is probably very important for the understanding of the functioning of the avian
visual system (Gntrkn et al., 1993). Recently, by recording from single units of the left and
right Rt of the tectofugal pathway, a modulation of the left visual wulst on both right and left
tectofugal systems has been described, whereas the right visual wulst showed only an
ipsilateral influence (Folta et al., 2004, Folta et al. in preparation).
Tectum opticum
Nucleus rotundus
Entopallium
RF
F
YF
Lateral geniculate nucleus
V. wulst
Figure 7: Schematic representation of the connections (in black) between the tectofugal (in red) and thalamofugal
systems (in green).
Tectofugal-thalamofugal projections have been also described, radial neurons located in the
optic tectum project to the dorsolateral thalamus (Gamlin & Cohen, 1986; Wild, 1989).
Furthermore, the information processes by both ascending visual pathways converge into the
entopallium, thanks to projections from the visual wulst to the entopallium (Husband &
Shimizu, 1999; Karten & Hodos, 1970; Shimizu, Cox, & Karten, 1995; Watanabe, Ito, &
Ikushima, 1985). In zebra finches, the visual wulst has a significant facilitatory influence on
the processing of the contralateral visual information of the entopallium (Engelage & Bischof,
1994).
1.5.2.4 The accessory optic system

In addition to these two ascending visual pathways, the accessory optic system (AOS) is a
distinct visual pathway dedicated to the analysis of optic flow fields and various visual signals
generated by self-motion or optokinetic stimuli (Simpson, 1984). Given that head-bobbing is
triggered by optic flow (Friedman, 1975; Friedman, 1975b), it is widely accepted that the AOS
is involved in head-bobbing. Furthermore, AOS is considered to play a role in the stabilization
of the retinal image (Simpson, 1984; Westheimer & Blair, 1974), a function attributed to the
hold phase of head-bobbing.
Numerous electrophysiological studies have shown that neurons in the AOS exhibit direction
selectivity in response to large visual stimuli moving in the contralateral visual field (Frost,
Wylie, & Wang, 1990). Some neurons have binocular receptive fields that encode optic flow
fields induced by self-translation or self-rotation (Frost et al., 1990; Wylie & Frost, 1990;
Wylie, Glover, & Aitchison, 1999; Wylie, Glover, & Lau, 1998). In birds, the AOS consists of
the nucleus of the basal optic root (nBOR) and the nucleus lentiformis mesencephali (nLM).
The nBOR receives input from the retinal displaced ganglion cells, the visual forebrain, the
contralateral nBOR and the ipsilateral nucleus lentiformis mesencephali (nLM), and projects to
diverse regions including the contralateral nBOR, the ipsilateral nLM, the vestibulocerebellum
and the oculomotor complex (Frost & Wylie, 2000; Wang, Gu, & Wang, 2000).
Neurons of the nBOR directly project onto the Rt of the same hemisphere (Diekamp,
Hellmann, Troje, Wang, & Gntrkn, 2001). Furthermore, projections from the nBOR onto
the GLd have been described (Wylie, Bischof, & Frost, 1998; Wylie, Linkenhoker, & Lau,
1997). The data suggest that the AOS is able to modulate both thalamofugal and tectofugal
ascending visual pathways. It is plausible that these projections are necessary to distinguish
self- and object-motion processed by the AOS and the ascending pathways, respectively
(Diekamp et al., 2001).

The retina of the pigeon has two areas of enhanced vision: the red field in the dorsotemporal
retina pointing into the frontal binocular field and the yellow field projecting into the lateral
monocular field. The entire retina projects to the contralateral optic tectum and continues via
the diencephalic nucleus rotundus to the entopallium (tectofugal pathway). The monocular area
also projects to the contralateral geniculate thalamic nucleus and continues to the wulst
(thalamofugal pathway). These two different visual systems possibly operate independently in
the pigeons eye, however they are not isolated. Both pathways converge into the entopallium,
the visual wulst sends ipsilateral descending projections directly to the optic tectum, and finally
radial neurons located in the optic tectum project to the dorsolateral thalamus.
In addition to these two ascending visual pathways, the accessory optic system, consisting of
the nucleus of the basal optic root and the nucleus lentiformis mesencephali, is a distinct visual
pathway dedicated to the analysis of optic flow fields and various visual signals generated by
self-motion or optokinetic stimuli.
1.6 Goals of this work

The main aim of this work is to combine two aspects of the visual system in birds: on the one
hand to contribute to a better understanding of information transfer and its asymmetries, and on
the other hand to investigate the functional significance of head-bobbing in birds together with
its evolutionary basis.
The first part of this work investigates how information perceived in different parts of the
pigeons retinas, which is processes by two independent visual systems in each hemisphere, is
generalised in the pigeons brain. To achieve this aim, several experiments were designed. In
the first experiment and the third experiment, we tested intraocular transfer of information
between the red and the yellow fields in walking pigeons. In the second experiment, interocular
transfer of information between the yellow fields of both eyes was investigated.
It is believed that head-bobbing acts as an optokinetic behaviour allowing pattern recognition
during the hold phase. The aim of the fourth experiment was to clarify the role of the headbobbing hold and thrust phases in pattern recognition. Therefore, we conducted an
experimental task in which the pigeons needed to discriminate between two stimuli presented
either in the thrust phase, the hold phase, or randomly. To our knowledge, although headbobbing behaviour has been often discussed in the literature, few head-bobbing birds have
been listed until now. In the fifth experiment, a comprehensive list of head-bobbing and non
head-bobbing birds is offered. Furthermore, field observations, video recordings and
phylogenetic information, together with an analysis of behavioural and ecological characters,
were combined to clarify the adaptive value of head-bobbing and its evolutionary foundations.
General Methods 32
2. GENERAL METHODS
Many experiments reported until now have been done in static or restrained pigeons in
detriment of the ecological validity. Here, we used an experimental arena, which allowed the
birds to walk between two feeders. In addition, a motion capture system was mounted in the
arena to track the animals walking behaviour and head position. In an initial training, the
pigeons were trained to discriminate between two stimuli, while walking between the two
feeders.
2.1 Experimental arena
An experimental arena of 125 cm length and 54 cm width was constructed (Fig.8), with a
feeder and two pecking keys on either end. The two pecking keys (2.5 cm diameter) were
horizontally placed at each side of the feeder (2 cm of diameter). The lower edge of each key
was 5 cm above the floor, and the two keys were spaced 23 cm apart. Two 15 LCD screens
were mounted on a track surrounding the arena, which permitted an easy displacement of the
screens around it. On one end of the arena, a light barrier was installed to detect the pigeon
walking between the two feeders.
All these devices were placed in a symmetric experimental chamber of 190 cm length, 100 cm
width and 80 cm height. On one end of the experimental chamber a camera was placed to
observe pigeons behaviour and to record the experimental sessions.
General Methods 33
Figure 8: The experimental arena. A track surrounding the experimental arena allowed situating the two LCD
screens in any position of the experimental arena.
2.2 Motion capture system
A motion capture system, constructed by the technical service of the Psychology department of
the Ruhr-University-Bochum was installed in the arena. Two high speed CMOS cameras (120
frames/s) tracked the movement of a 15mm retroreflective marker (provided by VICON) fixed
on the pigeons head (Fig. 9). The cameras (MV-D752-80 from Photon Focus) with a spatial
resolution of 600 x 440 pixels sent the information to two frame grabber cards (DT 3145 from
Data Translation) that digitized the images. Around the lenses, 30 ultra bright red LEDs were
mounted, which were flashing in synchrony with the cameras at a temporal resolution of 120
frames/s in order to provide the necessary illumination. The motion capture information was
processed and stored in a computer that also controlled the stimulus presentation on the screen,
delivered food as a reward or emitted a sharp sound as a punishment.
General Methods 34
Figure 9: Setup of the motion capture system (left) and placement of the marker on the pigeons head (right)
2.3 Subjects
Nine pigeons (Columba livia), males and females, between 3 and 7 years of age obtained from
the aviary of the biopsychology department (Ruhr-Uni-Bochum) were initially trained in the
pattern recognition task. They were kept in individual cages on a 12 hours light-dark cycle.
They had ad lib. access to drinking water and grit and were kept at 85% of their free-feeding
weight at the beginning of the experiment. Through the training, the birds learned to obtain
enough food in the training sessions to keep their weight at a normal level.
2.4 Training Procedure
Pigeons were initially trained in a pattern discrimination task, in which they need to
discriminate between two shapes: stimuli A and stimuli B (Fig. 10), by pecking with a fix
rate of 1, on one of the two keys. The stimuli were presented on a single LCD screen located in
a central position right behind the feeder with the two pecking keys. The centre of the stimulus
was situated in the middle of the screen 16 cm above the floor. The subjects were divided
randomly in two groups of 5 pigeons each. One group of birds was trained to peck the right key
General Methods 35
when stimulus A was presented and the left key when stimulus B was presented. For the
other group this pattern was reversed, i.e. the left key corresponded to stimulus A and the
right key to stimulus B.
Figure 10: Shapes presented in the discrimination task. From left to

right: stimulus A and stimulus B
By a shaping procedure, the pigeons were trained to progressively approximate the target
behaviour. First, the pigeons were trained to walk between two near feeders that were
alternatively activated during 2 seconds each. The feeders were separated, little by little,
throughout the training until they were at either end of the experimental arena (125 cm of
distance). When the pigeons were accustomed to walk between the distant feeders the second
phase of the shaping procedure started. The birds needed to peck on the keys located on one
side of the experimental arena (frontal part) to obtain food within a trial. After two seconds of
food reward in the frontal feeder, the pigeons walked to the other end of the arena (back part),
where they were rewarded, without pecking, during another 2 seconds. Third, the walking birds
had to peck on one of the keys according the shape presented in a screen, which was located in
one end of the experimental arena (Fig. 11 and 12).
Stimulus presentation
Pigeon cross the

light barrier
Reward in the back

feeder
Pigeon walks back
Incorrect
Pigeon walks towards

the back feeder
Pigeon walks towards

the pecking keys
Response
Correct
Reward in the
frontal feeder
Figure 11: Diagram of the pigeons steps

during the experimental procedure. The
pigeons task was to discriminate between
two shapes by pecking in one of two
pecking keys, located at one end of the
arena, while walking between two distant
feeders.
General Methods 36
To force pigeons to walk between the two feeders, the trials had two distinctive phases. The
front phase started with the presentation of the stimulus on the screen, the pigeon walked
towards the frontal pecking keys and feeder. The stimuli were presented on the screen until the
pigeons responded by pecking one of the two keys. A correct response was rewarded with 2 s
of food access. An incorrect response was punished with a sharp noise lasting 2 s. During the
back phase, regardless of the response of the pigeons, the animals were forced to walk back
towards the other end of the arena (Fig. 8). When they crossed a light barrier located near the
feeder, two consequences could follow: if the pigeons response was correct, the animal was
rewarded with 2 s of food access in the back feeder, afterwards the next trial started. If the
response was incorrect, the feeder was not activated and the next trial started with the stimulus
presentation (Fig. 11 and 12). Each animal was trained in 4 sessions a day. A session of
training consisted of 20 trials presented in random order: 10 stimulus A trials and 10
stimulus B trials.
Figure 12: A pigeon performing the task in the experimental arena. The animals were trained to peck on one of
the two pecking keys according to the stimuli presented in the frontal screen.
Finally, pigeons were accustomed to walking with a reflecting marker (15 mm of diameter)
fixed on top of the head. To attach the marker, a piece of Velcro (1 cm long 2 cm wide) was
affixed on the pigeons head by means of water-soluble non toxic crafts glue, after clipping the
surface of feathers. The counter piece of the Velcro was glued to the marker.
General Methods 37
The initial learning took 3-4 months depending on the animal. A smaller experimental arena
with mobile walls at the screen level would accelerate the learning process. For experiments 1,
2, and 3 a shorter experimental arena would facilitate the task, although the size was ideal for
experiment 4 in which the pigeons' head motions were analysed. A second mobile light barrier
would be useful to control the position of the pigeon in the arena at which the stimuli were
presented. This would provide an easier way to estimate at which point the pigeons were
observing the stimuli. In the present work, the stimuli presentation and the response key were
located exclusively in one end of the experimental arena. By presenting the task in both ends of
the alley, double amount of data would be collected in each session, but the complexity of the
task might be unnecessarily increased. Two animals (not used in these studies) were initially
trained using a go-nogo experimental procedure, the animals learned faster to discriminate
between the stimuli, but it was harder to keep them walking between the feeders. The overall
design of the experimental arena, might be improved for each individual experiment, but it was
optimal for the set of experiment that we performed.
Intraocular and Interocular Transfer in Pigeons 38

3. EXPERIMENT 1, 2 AND 3: INTRAOCULAR AND INTEROCULAR TRANSFER IN
PIGEONS.
In the first study, transfer of information within the same visual hemisphere was tested. While
the screen was gradually moved from its initial frontal position to a lateral position, we
measure the time required for retraining to new positions as a function of retinal stimulus
position. After this experiment the pigeons were able to perform the pattern discrimination
task observing the stimuli on a screen located in one of the lateral visual fields. In the second
study, interocular transfer of information between the yellow fields of the two eyes was tested
by presenting the stimuli on a screen located in the lateral visual field of the untrained
hemisphere. Subsequently six pigeons were trained in the naive hemisphere. In the third
study, for the animals capable of learning the task, an extension of the intraocular transfer
experiment was conducted in which the screen was moved back from lateral to frontal position.
3.1 Experiment 1: Limits of intraocular transfer in pigeons I: frontal to lateral direction.
Intraocular transfer experiments investigate how the information received within different
areas of the retina is being generalised in the pigeon visual system. Previous investigations in
pigeons observed information transfer from the lateral to the frontal visual field. However, a
lack of transfer was found from the frontal to the lateral visual field (Nye, 1973; Mallin &
Delius, 1983; Remy & Emmerton, 1991; Roberts et al, 1996).
To our knowledge, intraocular transfer between the red and the yellow visual fields in both
directions have been directly investigated in few experiments (Levine, 1952; Mallin & Delius,
1983; Nye, 1973; Remy & Emmerton, 1991b; Roberts et al., 1996). This is probably due to the
difficulty of training pigeons to solve visual tasks in the lateral visual field (Remy &
Watanabe, 1993) and the hitches to establish the retinal area in which the stimuli are presented
in freely moving subjects.

Levines (1952) jumping stand experiments do not provide direct evidence of switching from
the yellow field to the red field and vice versa. To avoid this problem, a couple of
investigations were done in head-fixed pigeons in detriment of the ecological validity (Mallin
& Delius, 1983; Remy & Emmerton, 1991b). In a later experiment, birds were trained to
discriminate stimuli inside a Skinner box, letting the animals free to move, but in practice the
animals did not walk (Roberts et al., 1996). In most cases, the experimental conditions of intraocular transfer studies prevent the birds to walk (Mallin & Delius, 1983; Nye, 1973; Remy &
Emmerton, 1991b; Roberts et al., 1996), which might deprive pigeons from important cues
such as visual flow and head-bobbing.
In the current experiment, intraocular transfer of information was tested in freely walking
pigeons, by using a pattern recognition task presented in different parts of the visual field.
3.1.1 Methods
Nine of the ten pigeons that completed the initial training were used for testing intraocular
transfer of information. The behaviour of the remaining bird was very instable, for this reason
it was excluded from the present experiment. The pigeons initial task was to discriminate
between two shapes (Fig. 10), randomly presented in the frontal visual field, by pecking on one
of the two keys located under the screen, while walking between the two feeders (see section
2.4) (Fig. 11). A correct response was rewarded with food; an incorrect response was punished
with a sharp tone. The animals were tested during 4 sessions of 20 trials each a day. When a
criterion of 70% correct responses in 4 consecutive sessions was reached, the screen was
moved step by step to the lateral side (Table 1 and Fig. 13). The pigeons were trained at each
position of the screen until achieving the criterion before moving the screen to the next
position. The screen was moved according to three rulers located at the frontal and in the
lateral sides of the experimental chamber.
40
30
20
10
10
20
30
40
10
PHILIP
S
10
20
20
30
30
45 degrees
40
PHILIPS
50
40
50
31cm
60
60
70
70
80
80
90
13 degrees
90
100
100
110
110
120
120
130
130
140
140
150
150
160
160
170
170
Figure 13: Scaled drawing of the experimental arena. Three rulers were located in the frontal and the lateral sides
of the arena indicating the distance in cm as references to move the screen from the frontal to the lateral positions.
Afterwards, the position of the stimuli in degrees was calculated assigning the centre of the circumference in the
equidistant point (31 cm) between two screens located in the centre and in the lateral visual field. The bold red
line indicates the position of the light barrier. The red angle corresponds to extend of the binocular field of the
pigeons, according to Martin and Young (1983), when the birds crossed the light barrier.

To calculate the positions of the stimuli in degrees, the centre of the circumference was
allocated in the width bisection of the arena at the equidistant point between the frontal and the
lateral screen (31 cm to each screen). In summary, the screen was located at 8, 13, 18, 23, 28,
and 45 cm according to the frontal ruler, 18, 28, 38, and 48 cm according to the a lateral ruler,
which corresponded to 14, 23, 29, 36, 41, 45, 48, 61, 76, and 95.
Stimuli location (in cm)

Degrees
8
14
Frontal ruler
13 18 23
23 29 36
28
41
45
45
Lateral ruler
18 28 38
48 61 76
48
95
Table 1: The screen was moved from the frontal side to the lateral side of the experimental arena in 10
consecutive steps according to frontal and lateral rulers located at the sides of the arena.
Nine of the ten birds trained in the initial task achieved the required criteria to move the screen
to the sides. For four of the birds, the screen was moved from the centre to the right side of the
arena. For three of the birds, the screen was moved from the centre to the left side of the arena
(Table 2). The two remaining birds were tested in both sides, dyhue to the difficulties
encountered to perform the tasks (see section 3.1.2.1),.
3.1.2 Results
Two different measures were taken in order to study intraocular transfer of information. On the
one hand the percentage of correct responses for the first 20 trials at each new screen position,
on the other hand the number of trials needed to achieve a criterion of 70% of correct responses
in four consecutive sessions were analysed.
3.1.2.1 Percentage of correct responses
Eight of the nine birds learned the task in the lateral visual field by moving the screen in
successive steps from 0 (frontal visual field) to 95 (lateral visual field). For pigeons 51, 321,

333 and 347, the screen was moved to the right visual field (RVF), whereas for pigeons 251,
512 and 988 the screen was moved to the left visual field (LVF).
Due to the experimental results pigeons 246 and 259 were tested on one side and afterwards in
the other. For pigeon 246 the screen was moved initially to the left side. The performance of
pigeon 246 dropped to chance level (around 50% of percentage of correct responses) when the
screen was located farther than 45 (Fig. 14 and Appendix A: Fig. A-1). Even after 600 trials
(30 sessions) of training at this position the pigeon did not achieve the criterion. For testing the
animal in the other direction, the screen was moved back to 0 where the pigeon was retrained
until reaching the criterion. Subsequently the screen was moved step by step to the right side.
A drastic drop of behaviour was also observed at 45 and the pigeon did not achieve the
criterion after 600 trials of training. In conclusion, pigeon 246 was not able to learn the task
beyond 45 in both left and right sides. Pigeon 259 was also tested moving the screen towards
right and left. After 600 trials of learning, the bird was incapable of achieving the criterion at
45 on the right side (Fig. 14 and Appendix A: Fig. A-1). However, after 380 trials of training
on the left side at 45, the animal achieved the criterion and the screen was moved step by step
until 95 were reached (Fig. 15-16 and Appendix A: Fig. A-1).
Pigeon 259 in the right visual field and pigeon 246 in both visual fields were incapable of
learning the task beyond 45. Pigeons 51, 321, 333, and 347 successfully learned the task in the
right visual field. Moreover pigeons 251, 512, 988 and 246 learned also learned successfully
the task in the left visual field. Regardless of the individual differences, all birds showed a
consistent and drastic decrease of performance at 45 (Fig. 15-16 and Appendix A: Fig. A-1).
For the data analysis, the results of 4 birds for each visual field, including pigeon 259 for the
left visual field were considered. At 45 the average percentage of correct responses for the
first 20 trials dropped to 58%. At 29 and 36 it was 67% and 68% respectively, while in the
remaining positions of the screen the percentage was above 70% of correct responses (Fig. 16).
The design employed for the percentage of correct responses data analysis was a 10*2 mixed
ANOVA. The first factor was the within-subject factor of screen position with 10 levels (14,

23, 29, 36, 41, 45, 48, 61, 76, and 95). The second factor was the inter-subject factor of
visual field with 2 levels. The data analysis revealed a significant effect for screen position
(F(9,54) = 2.55, p=0.01). The post hoc test accounted for significant differences between 45
with positions 14, 41, 61 and 76. Significant effects were also found between position 14
and positions 29 and 36 (Fig. 16 and Appendix A: Fig. 3-A), and between 48 and 76. The
statistic analysis should be interpreted with caution because different levels within the factor
screen position may not be statistically independent of each other. If this is the case, the data
analysis in the factor screen position could be biased in favour of non significant differences.
In comparison, the factor visual field the analysis could be biased in favour of a significant
effect. If this is the case we could underestimate the significances at 45, 29, and 36 with
respect to other positions. No significant effects were found for the visual field (F(1,6)=0.49,
p=0.51) an the interaction between the factors (F(9,54)=2.56, p=0.91).
% of correct responses
100
90
80
259-RVF
70
246-RVF
246-LVF
60
50
40
0
10
20
30
40
50
60
70
80
90
100
Position of the screen (degrees)
Figure 14: Percentage of correct responses for pigeons 259 and 246, which were incapable of learning the task
beyond 45. At 0, the performance level of the pigeons in the last 20 trials of the initial training.
100
251-LVF
259-LVF
90
512-LVF
988-LVF
51-RVF
321-RVF
80
333-RVF
347-RVF
70
60
50
40
0
10
20
30
40
50
60
70
80
90
100
Figure 15: Percentage of correct responses in the first 20 trials of training for each pigeon at different position of
the stimuli. At 0, the performance level of the pigeons in the last 20 trials of the initial training is plotted.
95
Total
LVF
90
RVF
85
80
75
70
65
60
55
50
0
10
20
30
40
50
60
70
80
90
100
Figure 16: Average percentage of correct responses in the first 20 trials of training at each position of the stimuli
in the left visual field (red), right visual field (yellow) and both visual field (blue). At 0 degrees, the average
percentage of correct responses of the pigeons in the last 20 trials of the initial training. The bars represent the
standard error of the mean.
3.1.2.2 Number of trials for achieving the criterion
The number of trials needed to achieve the criterion at each position of the screen was also
analysed for the eight birds that completed the training. Up to 45 eccentricity, moving the
screen to a farther position required an average of 144 trials; while at 45 the animals needed
an average of 302 trials to achieve the criterion. The average of trials to move the screen from
one position to another was 162, taking in account the training at 45. Increases of the required
number of trials to relearn the task with respect to the average were also observed at 29, 36,
and 95 (Fig. 17).
420
Total
LVF
380
RVF
Number of trials
340
300
260
220
180
140
100
60
0
10
20
30
40
50
60
70
80
90
100
Figure 17: Average number of trials needed to achieve the criterion at each position of the screen. The bars
represent the standard error of the mean
A data analysis was performed with the number of trials needed to achieve the criterion at each
position of the screen. A screen position x visual field ANOVA (10*2) revealed a significant
effect for screen position (F(9,54)=2.13, p=0.04). The post hoc test accounted for significant
differences between 45 and positions 14, 23, 36, 41, 61 and 76. Significant effects were
also found between 95 and positions 14, 23 and 61 (Fig. 17 and Appendix A: Fig. 4-A). As
in the percentage of correct responses analysis, if the screen position levels were not

independent of each other, the data analysis may underestimate the differences within the
factor position. No significant effects were found for the visual field (F(1,6)=0.32, p=0.59) and
the interaction between screen position and visual field (F(9,54)=0.01, p=0.91)
3.1.3 Discussion
Eight of the nine birds learned the discrimination task in the lateral visual field by moving the
stimuli step by step from 0 to 90. This contradict the results of Nye (1975) who found that
pigeons were not capable of colour and brightness discrimination in the lateral visual field after
moving the stimuli from the frontal to the lateral side in a sequence of 18 steps. Nye
concluded that pigeons lack the neural capabilities to learn a task in the lateral visual field.
Other evidence showed that pigeons are capable of learning a discrimination task in the lateral
visual field (Bloch & Martinoya, 1982b; Goodale & Graves, 1982; Mallin & Delius, 1983;
Remy & Emmerton, 1991b; Roberts et al., 1996), however none of those experiments tested
freely moving animals while moving the stimuli to the side in consecutive steps. The main
differences between Nyes experiment and the present one are the number of steps used to
move the screen to the 90 position and the amount of training at each step. Firstly, in the
present experiment the screen was moved at least in 10 consecutive steps while in Nyes
experiment only 5 steps were used. Secondly, Nye trained the birds at each position until they
reached a plateau level, whereas in the present experiment the pigeons were trained until they
reached the learning criterion (70% of correct responses in four consecutive sessions). The
amount of training seems to be the determinant factor for the birds to learn a task in the lateral
visual field. In the present experiment pigeons were trained in more steps and probably more
intensively within the steps.
The animals showed a significant decrease of performance at 29, 36, and especially at 45
degrees. Remarkably, at 45 performance in all pigeons decreased to values below 65%. The
average of trials needed to achieve the criterion was 302 trials (15.13 sessions) compared to an
average of 144 trials across all stimulus displacement. In addition, Pigeon 246 in both visual
fields and pigeons 259 in the RVF did not manage to learn the task beyond 45. We

hypothesize that this dramatic decrease of performance can be explained by a switch from
perceiving the stimuli with the frontal binocular red field to perceiving the stimuli with the
lateral monocular yellow field. The stimulus presentation occurred when the pigeons crossed
the light barrier which was located at 118 cm from the frontal screen. Therefore, this distance
corresponds to the maximum observation point of a pigeon. The frontal binocular field of the
pigeon, in the horizontal plane has a maximum extension of 27 (Martin & Young, 1983). The
edge of the frontal binocular field, when the observation point is set at 118 cm in the centre of
the arena, corresponds to a stimulus situated at 40 in the experimental arena. A 5x5 cm
stimulus presented at 41 in the experimental arena falls at least partially within the binocular
field, while a stimulus presented at 45 falls entirely in the lateral visual field (Fig. 13).
Therefore, all evidence indicated that at 45 the pigeons did not perceive any longer the stimuli
within the frontal visual field. Video recordings confirmed that birds did not twist their heads
to look at the stimuli. This discards the possibility that birds solved the task with the frontal
visual field by twisting their head, when the stimuli were presented at the sides.
At 45 a failure of intraocular transfer of information may occur and the pigeons required an
intensive training until the task was relearned in the lateral visual field. A lack of intraocular
transfer from the frontal to the lateral visual field have been previously observed in non
walking pigeons (Nye, 1973; Roberts et al., 1996) and head-fixed pigeons (Mallin & Delius,
1983; Remy & Watanabe, 1993). The decrease of performance at 45 degrees could be a
consequence of two different visual systems operating independently in the pigeon brain: the
thalamofugal system processing information from the lateral visual field and the tectofugal
system processing information from the entire retina.
Pigeons 512, 51, and 321 showed the lowest percentage of correct responses at positions 29
and 36. As a consequence, significant decreases of performance were observed at these
positions in the data analysis. Remarkably those birds scored the highest percentage (65%) of
correct responses at 45 in comparison to other birds (Appendix A: Fig. A-2). Taking in
consideration that the position at which the pigeons look at the screen is not very precisely
predetermined, it is plausible that birds 512, 51, and 321 observed the stimuli at closer
distances than the other birds. Probably those birds started to perceive the stimuli with the

yellow visual field around 30, but instead of learning the task by using the yellow field, they
have modified their behaviour to observe the stimuli within the red visual field from a farther
position.
A preliminary data analysis of the walking trajectory (motion capture data of 30 trials) of
pigeon 251 revealed that the pigeons trajectory changed, towards the correct response key at
different positions depending on the location of the stimulus. When the screen was located in
the lateral visual field the bird changed the trajectory approximately at 20 cm to the pecking
keys, while when the screen was located at 45 the bird trajectory changed approximately at 36
cm to the pecking keys (Appendix B: Fig. A-6 and A-7). This might indicate that the stimuli
were observed earlier when the screen was located at 45, than when it was located at 0.
At 95 significant effects were observed with respect to positions 14, 23, and 61. At this
position the screen is located 20 cm away from the pecking keys. Pigeons have a panoramic
vision of 245 (Martin & Young, 1983), which corresponds to 122.5 degrees in each lateral
visual field. A stimulus located at 95 according to our experimental arena, when a pigeons is
situated in the centre of the arena (i.e. 31 cm away from the horizontal plane of the stimulus),
falls at 130 with respect to the pigeon eye. This corresponds to the pigeon blind area.
Therefore, at this position pigeons need to memorize the response before arriving at the
pecking keys. This memory component could be responsible for the difficulties to achieve the
criteria at 95.
Contrary to previous experiments (Mallin & Delius, 1983; Nye, 1973), neither the amount of
training nor the percentages of correct responses were affected by the distance between the
stimulus and the pecking key. Certainly, significant differences between 48, 61, 76, and 95
were not found in any of the two variables. The effect of the spatial contiguity could be
counteracted by the intensive training at each position of the stimuli and by the amount of steps
used to move the screen from frontal to lateral. Less intensive training in fewer steps may
result in significant differences between the stimuli locations due to the spatial contiguity.
Finally, asymmetries between the LVF and the RVF were not observed neither in the
percentage of correct responses nor in the amount of trials.
In conclusion, the pigeons, after an intensive retraining, were capable of learning the task in the
lateral visual field. The dramatic decrease of performance observed around 45 may be due to a
switch from perceiving the shapes with the frontal field to perceiving the shapes with the
lateral field. This lack of intraocular transfer may have originated from the existence of two
independent visual systems in the pigeon: the tectofugal and the thalamofugal pathway. Non
significant differences were found between the animals trained in the left and the right visual
field.
3.2 Are pigeons capable of interocular transfer between the two yellow fields?
Interocular transfer has been widely investigated. A variety of tasks and experimental designs
have been used to clarify this phenomenon (see introduction). Although the retinal-locus
hypothesis claims that interocular transfer depends on whether the retinal projection of a
stimulus falls within the red or the yellow field, few experiments test directly interocular
transfer between the two yellow visual fields (Levine, 1952; Martin & Brooke, 1991; Nye,
1973; Remy & Emmerton, 1991b; Roberts et al., 1996). In most experiments, the stimuli were
either presented within the binocular red field, or the retinal projection of the stimuli was not
controlled. As in intraocular transfer experiments the two main difficulties reside in training
pigeons to solve visual tasks in the lateral field (Remy & Watanabe, 1993) and in controlling
the retinal projection of the stimuli. Often, the ecological validity has to be sacrificed in order
to control the retinal projection of the stimuli.
In the current experiment, we tested interocular transfer of information between the yellow
fields in an open arena, in which the pigeons were forced to move between two hoppers to
produce optic flow and display head-bobbing.

3.2.1 Methods
Eight of the nine pigeons (Columba livia) used in the previous experiment (section 3.1) were
tested in interocular transfer of information between the yellow fields.
Similarly to the previous experiment, the pigeons initial task was to discriminate between 2
shapes (Fig. 10) presented in the lateral visual field at 90, while walking between two feeders
and pecking on one of the two pecking keys situated at the end of the alley. Four pigeons were
trained in the left visual field (LVF), another four in the right visual field (RVF), as described
in the previous section. A correct response was rewarded with food. An incorrect response was
punished with a sharp tone. In the present experiment, in contrast to the final step of
experiment 3.1, the animals performed the task with the stimuli located at 90. When a criterion
of 70% correct responses was reached in two consecutive sessions of 44 trials each, 4 catch
trials (no punishment, no reward) presented on the trained side were randomly inserted into
each session. When the animals were accustomed to the lack of punishment or reward in 4 of
the 48 trials we started with the data collection. At this step, half of the catch trials were
presented in the trained visual field and the other half in the naive or untrained visual field.
After collecting 10 catch trials in each hemisphere (5 sessions with a total of 20 catch trials),
the pigeons were retrained at 90 in the naive hemisphere using the same pair of shapes over 10
experimental days, with 80 trials a day. Six birds continued the training until reaching the
criterion or for 5760 trials (72 sessions). Due to the difficulties encountered to train the animals
in the RVF, four of the six pigeons were retrained in the RVF and two birds were retrained in
the LVF. The initial goal was to train to pigeons to perform the task in each visual field.
Pigeons 51 and 347 initially trained in the RVF where retrained in the LVF, while pigeons 988,
51, 512 and 259 initially trained in the LVF were retrained in the RVF (Table 2).
Study description
Section
Frontal
RVF
LVF
Initial Training
2.4
all pigeons
Interocular: frontal-lateral
3.1
51, 321,
333, 347,
246, 259
251, 259,
512, 988,
246
Intraocular: catch trials
3.2.2.1
Opposite field training:

80 trials
Opposite field training:
5769 trials
Interocular: lateral-frontal
3.2.2.2
251, 259,
512, 988
251, 259,
512, 988
251, 259
512, 988
251
51, 321,
333, 347
51, 321,
333, 347
51, 347
Frontal test
3.3
259, 512, 988
259
Pattern recognition during HB
251, 259,
512, 988,
51, 347
51, 251,
347
3.2.2.3
3.3
Both
51, 347
259, 512,
988
251, 259,
512, 988,
51, 347
Table 2: History of birds over the series of experiments classified according to the visual field at which the
animals were trained in each study.
3.2.2 Results
Three types of data were analysed to investigate interocular transfer of information: the
percentage of correct responses for the catch trials, the learning curve of the first 800 trials (10
days of training) in the untrained hemisphere, and the learning curve in six pigeons for 5760
trials (72 days of training) or until reaching the criterion in the untrained hemisphere.
3.2.2.1 Percentage of correct responses for the catch trials
All birds had an average of correct responses above 70% in the learning trials. The average for
the LVF was 81.75 and for the RVF 84.5. There were no significant differences between the
LVF and the RVF. Regarding the catch trials, all birds except one showed a drop of
performance in the untrained hemisphere in comparison to the trained hemisphere. Pigeon 51 is
the only exception; it had 80% correct responses in the trained hemisphere and 100% in the
untrained hemisphere. The average percentage of correct responses for all pigeons in the
trained hemisphere was 85% and 56.25% in the untrained hemisphere (Fig. 18 and Appendix
A: Fig. A-5). A hemisphere x visual field mixed ANOVA (2*2) analysis revealed significant

differences between the trained and the untrained hemisphere (F(1,6)=11.10, p=0.02), and non
significant effects for the visual field (F(1,6) =0.69, p=0.44) and the interaction (F(1,6) =0.19,
p=0.68).
100
Catch trials
Trained
Naive
100
60
80
40
70
40
80
60
100
70
90
60
80
100
80
20
85
56.25
Learning trials
Catch trials
90
Pigeon
51
259
988
512
321
347
251
333
Average
Learning trials
LVF
RVF
82
85
75
85
78
95
85
80
81.75
84.5
80
85
85
82
70
60
56
50
40
LVF Learning RVF Learning
Trained
Naive
Figure 18: Percentage of correct responses for each pigeon in 220 learning trials, 10 catch trials in the trained
visual field and 10 catch trials in the naive visual field. The average of correct responses in the learning trials
(LVF and RVF) and catch trials (trained and nave hemisphere) is represented in panel.
3.2.2.2 Learning curve for the first 800 trials
Seven of the eight birds scored below the criterion at 70% during the first 10 days of training
(800 trials). The percentage of correct responses was around chance level for all birds except
for pigeons 251 and 512. Pigeon 251 showed clear signs of interocular transfer and reached the
criterion within the third day, with percentages of correct responses above 70%. Pigeon 512
reached levels of correct responses over 65% in the last 3 days of training (Fig. 19). However a
close analysis of the video recordings revealed that the bird was occasionally turning the head
to the screen which may discard a learning effect in the untrained hemisphere.
3.2.2.3 Learning curve in the untrained hemisphere
Pigeons 51 and 347, trained initially in the RVF, learned the task in the LVF after 5120 (64
days of training) and 2400 trials (30 days of training) respectively. Pigeons 988 and 259 trained
initially in the RVF were incapable of learning the task in the LVF after 5760 (72 days of

training). Another attempt to retrain a bird in the LVF, was made with pigeon 512. Even
though this bird reached the required criterion in several sessions, the behavioural results were
very unstable (Fig. 20). The analysis of the video recordings of pigeon 512 during the training
revealed that this pigeon reached the criterion in sessions during which it was turning the head
towards the screen, whereas this behaviour was not observed in any other pigeon.
Percentage of correct responses
95
85
251-RVF
259-RVF
75
512-RVF
988-RVF
65
51-LVF
321-LVF
55
333-LVF
347-LVF
45
35
80
160
240
320
400
480
560
640
720
800
Number of trials
Figure 19: Percentage of correct responses during the first 10 days of training in the untrained hemisphere. Each
point represents 80 trials (1 day) of training. Pigeons 251, 259, 512, and 988, trained initially in the LVF, were
retrained in the RVF, while pigeons 51, 321, 333 and 347, trained initially in the RVF, were retrained in the LVF
3.2.3 Discussion
Interocular transfer of information was not observed in 7 of the 8 pigeons. The performance
level in the untrained hemisphere was around chance level (50%), whereas in the trained
hemisphere birds obtained data above the criterion level (70%). In consonance to previous
experiments (Goodale & Graves, 1982; Levine, 1945b; Mallin & Delius, 1983), our results
confirm a lack of information transfer when the stimuli are perceived within the yellow visual
field. Pigeon 251 showed clear interocular transfer of information. We did not observe any

differences during the experimental procedure that could explain those results. Video
recordings of the animal training excluded that pigeon 251 was turning the head to observe the
stimuli with other areas of the visual field. In addition, the animal reached the learning criterion
after 3 sessions of training in the naive hemisphere. Most probably the bird did not reach the
criterion earlier due to an extinction phenomenon after being exposed to catch trials without
punishment and reward in the naive hemisphere. Further observations confirmed that pigeon
251 scored a higher percentage of correct responses in the RVF than in the LVF. Those results
could be a consequence of individual differences in the organization of the visual system.
95
85
251-RVF
259-RVF
512-RVF
75
988-RVF
51-LVF
65
347-LVF
55
45
35
0
500
1000
1500
2000
2500
3000
3500
4000
4500
5000
5500
6000
Number of trials
Figure 20: Learning curve of the originally untrained hemisphere. Each point represents 80 trials (1 day) of
training. Pigeons 251, 259, 512, and 988, trained initially in the LVF, were retrained in the RVF, while pigeons 51
and 347, trained initially in the RVF, were retrained in the LVF.
Birds initially trained in the RVF relearned the task in the LVF after a long lasting training,
whereas birds initially trained in the LVF (except pigeon 251) did not relearn the task in the
RVF at all. Learning to discriminate between two shapes in the lateral visual field while
walking between two feeders in an open arena has been demonstrated to be very a demanding
task for the pigeons. Long distances between the discriminative stimuli and the response site

may increase the difficulties of a discrimination task (Watanabe, 1986). In experiment 3.1 we
did not find any effect of the spatial contiguity, most probably because in this study the
distance between the stimuli and the response key was gradually increased, whereas in the
present experiment, the animals were directly trained to discriminate stimuli located 20 cm
away from the pecking keys. Pigeons are significantly better discriminating stimuli in their
frontal visual field than in their lateral visual field, but experiments with a closer spatial
contiguity (Mallin & Delius, 1983; Remy & Watanabe, 1993; Roberts et al., 1996) found fewer
difficulties to train the birds in the lateral visual field.
The organization of the avian visual system itself also seems to be responsible for the
performance of the pigeons. It has been demonstrated that pigeons detect movements in their
lateral visual fields significantly better than in their frontal binocular fields (Bloch &
Martinoya, 1982b). The lateral and the frontal visual fields may be specialised in solving
different environmental demands. Furthermore, it has been proposed that the right eye/left
hemisphere may be dominant for short distance tasks like feeding, while the left eye/right
hemisphere could be dominant for long distance tasks like vigilance (Rogers, 2000). This could
explain why the birds retrained in the naive RVF did not learn the task while the animals
retrained in the naive LVF did. However, stimulus discrimination in pigeons may be a task
mainly processed by the tectofugal pathway, which receives information from the entire retina.
It may occur that the visual information perceived in the lateral visual field is mainly processed
by the thalamofugal pathway, which may need the mediation of the tectofugal pathway to
process the information in a pattern discrimination task. More pronounced ipsilateral
projections from the right wulst into the right optic tectum than from the left wulst to the left
optic tectum have been recently described (Unpublished data from Patzke, Freund, Gntrkn
and Manns). If solving a discrimination task in the lateral visual field requires the contribution
of the thalamofugal and the tectofugal pathways, this weaker projection between the left visual
wulst to the left optic tectum may also explain why the animals retrained in the RVF-left
hemisphere did not manage to learn the discrimination task.

3.3 Limits of intraocular transfer in pigeons II: lateral to frontal direction.
Several investigations in pigeons have demonstrated a lack of transfer from the frontal visual
field to the lateral visual field (Levine, 1945a, 1945b; Mallin & Delius, 1983; Nye, 1973;
Remy & Watanabe, 1993; Roberts et al., 1996; Watanabe, 1986). However, information
transfer from the lateral to the frontal visual field has been rarely tested. Mallin and Delius
(1983) found a higher level of intraocular transfer from lateral to frontal position than vice
versa in a colour discrimination task using jaw movements as an operant response. Intraocular
transfer from the lateral to frontal visual field was observed in a stimulus detection task in head
fixed pigeons (Remy & Emmerton, 1991b) and in a matched to sample task (Roberts et al.,
1996).
Intraocular transfer of information was tested from the lateral to the frontal visual field by
moving the stimuli to the central visual field in consecutive steps. The pigeons task was to
discriminate between two shapes by pecking on one of the two keys located at the end of the
experimental arena.
3.3.1 Methods
Pigeons 51, 251, and 347, which in the previous experiment learned the task in the initially
naive hemisphere, were used for testing interocular transfer of information from lateral to
frontal direction. The pigeons initial task was to discriminate between two shapes (Fig. 10)
randomly presented on a screen located at 95 in the lateral visual field, by pecking on one of
the two keys located at one end of the experimental alley. The animals were trained to walk
between the two feeders while performing the task. Correct responses were rewarded with
food; incorrect responses were punished with a sharp tone. The animals were tested during 4
sessions of 20 trials each a day. When a criterion of 70% correct responses in 4 consecutive
sessions was reached, the screen was moved step by step to the frontal side. The pigeons were
retrained at each position of the screen, until achieving the criterion, before moving the screen

to the next position. The same stimuli position used in the previous interocular transfer
experiment were chosen, except that the screen was moved in the opposite direction. These
positions corresponded to 76, 61, 48, 45, 41, 36, 29, 23, 14 and 0. The performance of
correct responses for1 the first twenty trials for each positions and the number of trials to
achieve the criterion for each animal were analysed. The data obtained when the screen was
moved gradually from the lateral to the frontal visual field were compared with the data
obtained in experiment 3.1 in which the screen was moved from the frontal to the lateral visual
field.
Additionally, as a measure of the learning effect during the initial training, pigeons 988, 259
and 512 were tested in the same task exclusively at 0. These pigeons shared the same training
history as pigeons 51, 251, and 347 (Table 2). Initial training at this position (see section 2.4)
in the same task took place for the last time at least one year before for all pigeons. Therefore,
testing these birds at 0 may provide a valuable measure of the effect of the initial training in
transfer of information from the frontal to the lateral direction.
3.3.2 Results
Moving the screen from the lateral to the frontal visual field (lateral-frontal condition) took a
total amount of 800, 900, and 1180 trials for pigeons 251, 51, and 347 respectively. In study
3.1 moving the screen from the frontal to the lateral visual field (frontal-lateral condition) took
a total amount of 1260, 1820 and 900 trials for pigeons 251, 51, and 347 respectively (Fig. 21).
A one tailed t-test analysis between the number of trials needed at each position to move the
screen from frontal to lateral direction and vice versa, confirmed that pigeon 251 needed
significantly less sessions of training in the frontal-lateral condition than in the lateral-frontal
condition (t=2.29, df=9, p<.05). Similarly, pigeon 51 also needed significantly less sessions of
training in the frontal-lateral condition (t=2.29, df=9, p<.05).
Pigeon 347 did not show
significant differences between the frontal-lateral and lateral-frontal condition (t= 1.02, df = 9,
p >.05).
At position 45, pigeons 251, 51 and 347 needed 80, 100, and 240 trials in the lateral-frontal
condition whereas they needed 280, 400, and 140 trials in the frontal-lateral condition
respectively.
The percentage of correct responses in the frontal-lateral condition is similar to the lateralfrontal condition (Fig. 21). No significant differences were found for any of the three pigeons.
In both conditions a decrease of performance close to chance level in the first 20 trials was
observed at 45 for pigeons 51 and 347, while pigeon 251 showed percentages of correct
responses closed to chance level at 61, 48 and 45 in the lateral-frontal condition and at 39
and 48 in the frontal-lateral condition.
Pigeons 988, 259 and 512 tested at 0 (1 year after the initial training) showed a percentage of
correct responses around chance level in the first 400 trials. Pigeons 259 and 512 achieved the
training criterion after 640 and 1120 trials. Pigeon 988 reached a percentage of correct
responses superior to 70% after 840 trials of training in several sessions. However, due to the
instability of the behaviour, the bird never managed to achieve the criterion (70% of correct
responses in 4 consecutive sessions) after more than 3000 trials of training. In the initial frontal
training at 0 (see section 2.4) birds 988, 259 and 512 required 2820, 920, 1480 trials
respectively to achieve the criterion. A Wilcoxon statistic analysis was performed between the
numbers of trials needed to achieve the criterion in the frontal initial training and in the one
year later frontal retrained. Even assuming that pigeon 988 reached the criterion at 840 trials,
no significant differences were found (z=-1.61, N-Ties= 3, p=,11) between both trainings.
Bearing in mind that the number of birds tested is very small, we can conclude that the pigeons
encountered similar difficulties in learning the task during the initial frontal training and during
the later frontal training.
90
90
80
80
70
70
60
40
0
10
20
51-LVF
50
347-LVF
Average
30
40
50
60
70
80
90
100
100
90
80
40
70
60
50
40
30
20
251-LVF
380
51-RVF
340
347-RVF
420
251-RVF
51-LVF
347-LVF
Average
Average
300
10
420
60
251-RVF
251-LVF
51-RVF
347-RVF
Average
50
Number of trials
100
380
340
300
260
260
220
220
180
180
140
140
100
100
60
60
10
20
30 40
50 60
70 80
90
100
100
90
80
70
60
50
40
30
20
10
Figure 21: Percentage of correct responses for the first 20 trials at each position for moving the stimuli from
frontal to lateral (A) and from lateral to frontal (B) in 10 consecutive steps for pigeons 251, 51, and 347. Number
of trials needed to achieve the criterion at each position from frontal to lateral (C) and lateral to frontal (D) for
pigeons 251, 51, and 347.
3.3.3 Discussion
Moving the screen from the lateral to the frontal visual field took less training than vice versa
for two of the analysed pigeons. The third animal did not show significant differences between
the directions. This animal was exceptionally good in the frontal to lateral condition which may
explain the lack of differences. In the video recordings, no sign of turning the head towards the
screen was observed.
Number of trials
% of correct response
% of correct response
100
In two of the three animals, a smaller amount of trials was required to achieve the criterion at
45 when moving the stimuli from lateral to frontal direction than vice versa. Although the
percentage of correct response decreases around 45, the number of trials required to achieve
the criterion is comparable to other screen positions for the three animals in the lateral to
frontal direction. On the one hand, at 45 pigeons may switch from one visual mechanism to
another, which may result in the observed decrease of performance. On the other hand, after
this initial decrease of performance, at 45 pigeons needed an amount of trials comparable to
other positions in order to achieve the criteria. This result discards the influence of other
factors like, visibility problems and orientation of the screen in the performance. Nevertheless,
it may not demonstrate a higher level of intraocular transfer of information in lateral to frontal
direction. Two factors can explain the better performance of the pigeons in the lateral to frontal
direction: pigeons have previous experience solving the same task in the frontal visual field
and a closer spatial contiguity between stimuli and response keys may facilitate the task as
well.
The initial learning in the frontal visual field took place at least 1 year earlier for all pigeons.
To estimate the effect of the frontal initial training in the results, we tested at 0 pigeons 988,
259 and 512 which did not manage to relearn the task in the naive hemisphere (see
experiment 3.2) at 0. Surprisingly, during the first 400 trials of training all pigeons performed
at chance level and they needed more than 600 trials to achieve the criterion, although they had
no problems performing the task with the screen located at 90. The statistical analysis
suggested that most probably pigeons have forgotten the task in the frontal visual field.
However, a previous experiment found intraocular transfer of information from lateral to
frontal position in a matching to sample task in which the stimuli were presented in a lateral
key (at 90) and on a frontal key (Roberts et al., 1996). Pigeons 988, 259 and 512 were not
capable to perform the task neither due to the previous experience in the frontal visual field nor
to the presence of intraocular transfer.
These results are somehow contradictory: Three of the birds showed less difficulties solving
the task by moving the screen from lateral to frontal direction than vice versa. In addition, we

found no influence of the previous learning when three other birds were retrained on the frontal
visual field. On the one hand one could conclude that there is intraocular transfer of
information when the screen is moved from lateral to frontal direction, but on the other hand no
traces of intraocular transfer of information where found when retrained three of the birds for
the second time at 0 in the frontal visual field
Our data do not provide clear evidence supporting intraocular transfer from the lateral visual
field to the frontal visual field. In the frontal-lateral condition the distance between stimuli and
response key increases, while in the lateral-frontal condition the distance decreases. A decrease
of the distance between stimuli and response key when moving the stimuli from the lateral to
the frontal direction could facilitate the task.
In a colour discrimination task in head-fixed pigeons similar results were observed (Mallin &
Delius, 1983). A poor intraocular transfer when the stimuli were shifted from a frontal to a
lateral position and vice versa within the field of view of the same eye. Intraocular transfer was
about 10% higher from a lateral to a frontal condition than vice-versa, which could also be as a
result of the spatial contiguity between stimuli and response orientation. In contrast, more clear
evidence of intraocular transfer from the frontal to the lateral visual field was found in headfixed pigeons in a stimulus detection task. It occurred when the stimulus presentation was
changed from the lateral to the frontal visual field but not vice versa (Remy & Emmerton,
1991b).
The extent of intraocular transfer of information from the lateral to the frontal direction may be
task dependent. Remarkably, intraocular transfer was very poor or not observed in tasks with a
more manifest memory component, like colour discrimination (Mallin & Delius, 1983) and
pattern discrimination. However, intraocular transfer was observed in tasks without a clear
memory component, like stimulus detection (Remy & Emmerton, 1991b) and matching to
sample (Roberts et al., 1996).

The information received within the yellow field system may be transferred into the red visual
field system in order to switch attention to interesting or important environmental stimuli, in
this case information transfer of complex memories contents may not be necessary.
3.4 Interim summary
A lack of intraocular transfer of information in the same eye from the frontal to the lateral
visual field was observed in walking pigeons. Intraocular transfer of information from the
lateral to the frontal visual field was poor or inexistent. Transfer of information from the lateral
to the frontal visual field may be task dependent. The lack of intraocular transfer can be as a
result of two independent visual systems operating in the pigeons brain: the tectofugal and the
thalamofugal pathways.
Pigeons showed more difficulties to learn a pattern discrimination task directly presented in the
right than in the left monocular visual field. The left visual field might be specialised in
processing visual tasks that are more likely to be observed at far distances, whereas the right
visual field might be specialised in processing visual tasks which are more likely to be
observed at close distances. Interocular transfer between the yellow fields of both eyes was
rarely observed. It may be due to the poor interhemispheric connections described in pigeons.
Pattern Recognition During Head-bobbing 63
4. EXPERIMENT 4: PATTERN RECOGNITION DURING HEAD-BOBBING: ARE

PIGEONS CAPABLE OF PATTERN RECOGNITION DURING THE THRUST
PHASE?
It is commonly accepted that head-bobbing acts as an optokinetic behaviour, stabilizing the

retinal image and allowing pattern recognition (Davies & Green, 1988; Frost, 1978). The hold
phase of head-bobbing in which the retinal image is stabilized may be a determining factor for
object recognition. It also may allow birds to distinguish between visual motion due to external
movements and self-induced visual motion. The hold phase during head-bobbing is not
completely stabilized, but the head moves relative to the surrounding with a velocity that
serves as an error signal to stabilize the image (Frost, 1978; Troje & Frost, 2000). This error
signal is assumed to be processed by the accessory optic system which plays a central role in
the stabilization of the retinal image (Simpson, 1984; Westheimer & Blair, 1974).
According to this theory, pattern recognition would take place mainly during the hold phase.
Although this theory is widely accepted (Davies & Green, 1988; Frost, 1978; Morgan & Frost,
1981; Troje & Frost, 2000; Wylie& Frost, 1990) there is no direct behavioural data confirming
it.
To investigate the role of the hold phase and thrust phase in pattern recognition, we tested
pigeons in a pattern recognition task presenting the stimuli exclusively either in the hold or in
the thrust phase.
4.1 Methods
Pigeons 51, 251, 259, 347, 512, and 988 previously utilized in experiments 3.1, 3.2 and 3.3
were used in the present experiment. All of these birds were capable of discriminating between
two shapes (Fig. 10) located in the lateral visual field. In each trial, one of the two stimuli was
randomly presented simultaneously on the two TFT screens located at 90 in the experimental
arena (Fig. 13).
A reflecting marker was attached to the pigeons head to capture the head movements of the
animals. The pigeons were motion captured in real time (see section 2.2) during the
experiment. The temporal resolution of the motion capture system was 120 frames/s and the
spatial resolution was 1 mm. The time and x, y, z coordinates of the position of the head
trajectory was stored and analysed for each experimental condition.
Each day the pigeons were trained over 96 trials, divided in 4 consecutive sessions of 18
training trials and 6 catch trials each. For the data collection 15 sessions in which pigeons
achieved more than 70% of correct responses in the training trials, were considered. Opposed
to the previous experiments, the stimuli were presented intermittently for periods of maximally
75ms (see bellow for more details). In two hold catch trials the stimuli were presented
exclusively during the hold phase. A hold phase presentation occurred when the speed of the
head was smaller than 240 mm/s (Fig. 22C). In two thrust catch trials the stimuli were
presented exclusively during the thrust phase. A thrust phase presentation occurred when the
speed of the head was bigger than 480 mm/s (Fig. 22D). For two random catch trials and the
training trials the stimuli were randomly presented following two distributions of the hold and
thrust phase duration (Appendix B: Fig. B-2). Those distributions represents real head-bobbing
phases durations. They are calculated to obtain similar presentation patterns to the hold and the
thrust presentation, constructed according to very restrictive criteria.
For calculating the distributions that control the random presentation of the stimuli, a total
amount of 1907 head-bobbing cycles captured in 10 trials for each pigeon were analysed. A
threshold of 240 mm/s was used to differentiate between hold and thrust phases. For each
presentation of the stimuli, a virtual head-bobbing cycle was created. For this purpose, a hold
and a thrust phase duration was randomly chosen according to the distributions. In one phase
of the virtually created head-bobbing cycle, a stimulus was presented for a maximum interval
of 75 ms, while during the rest of the time and during the other phase the screen remained
black.
400
B
500
300
400
300
200
Distance (mm)
Distance (mm)
200
100
-100
100
0
-100
-200
-200
-300
-400
-300
-500
-400
0.8
1.2
1.4
1.6
1.8
2.2
2.4
0.2
0.4
0.6
Time (s)
400
0.8
1.2
1.4
1.6
Time (S)
D
500
300
400
300
200
Distance (mm)
Distance (mm)
200
100
-100
100
0
-100
-200
-200
-300
-400
-300
-500
-400
0.8
1.2
1.4
1.6
1.8
2.2
0.2
2.4
Time (s)
400
0.8
1.2
1.4
1.6
E
Figure 22: Samples of the head motion of the pigeons.
The x coordinate of the head motion was plotted in blue,
whereas the y coordinate was plotted in red. The grey
fills in figures A and B represent the real time detection
of the hold and the thrust phases, respectively. The grey
fills in figures C and D indicate stimulus presentation
times during the same trials. Grey fill in figure E stands
for the random presentation in a trial in which the
stimulus was not locked to the motion of the head.
200
Distance (mm)
0.6
Time (s)
300
100
-100
-200
-300
-400
0.4
0.4
0.6
0.8
1
Time (s)
1.2
1.4
1.6
The delay of the real time motion capture system was measured to be in a range from 8 to 17
ms, due to the refresh rate of the screen (60 Hz) and the temporal resolution of the motion
capture system (120 Hz). A maximum presentation time of 75 ms was established for all trials,
to avoid presenting the stimuli out of the target phase as a consequence of the possible delay.
In courting pigeons the mean durations of the hold and the thrust phases were 156 ms and 132
ms respectively (Troje & Frost, 2000). Initial measures in the present experiment revealed a
hold phase duration of around 95 ms and a thrust phase duration of around 100 ms in walking
pigeons. Taking into account the hold and thrust phase durations and the delay of the system, a
maximum presentation time of 75 ms (9 frames) ensured that the stimuli fell within the target
phase (Fig. 22).
In conclusion, to investigate the role of the hold phase and thrust phase in pattern recognition,
the pigeons were tested in a pattern discrimination task presenting the stimuli exclusively either
during the hold phase, during the thrust phase, or randomly for similarly short periods. First,
the six animals were tested until collecting 30 trials in each experimental condition in the
lateral visual fields, by a simultaneous presentation of the stimuli on two screens located at 90
on either side. Second, pigeons 988, 259, and 512 were tested exclusively in the right visual
field, whereas pigeons 251, 51, and 347 were tested in the left visual field, during 15 sessions
(i.e. another 90 catch trials). Finally, all animals were tested in the frontal visual field for
another 90 catch trials distributed in 15 sessions; the stimuli were presented in the centre of the
experimental arena at 0. If a pigeon did not achieve a percentage of correct responses in the
training trials superior to 70% the session, the session was excluded in the data analysis and the
session was repeated.
4.2 Results
Two dependent variables were analysed. On the one hand, we evaluated the percentage of
correct responses in the hold, thrust, and random catch trials. On the other hand, we analysed
the head-bobbing motion by calculating the average duration, amplitude, and speed of the hold
and thrust phases.
4.2.1 Percentage of correct responses
When the stimuli were presented simultaneously in both lateral visual fields at 90, the average
percentage of correct responses for the hold, thrust, and random presentations were 80%, 77%,
and 84%, respectively (Fig. 23). A one way within subjects ANOVA revealed no significant
differences (F(2,10)=1.41, p=0.29) between presenting the stimuli exclusively during the hold
phase, thrust phase, or randomly.
When the stimuli were presented for half of the birds in the right visual field and for the other
half in the left visual field, the average percentage of correct responses for the hold, thrust, and
random phases was 71%, 79%, and 77% respectively. The average percentage of correct
responses for the hold, thrust and random phase in the animal tested in the left visual field, was
70%, 81%, and 70% respectively, whereas for the right visual field was 74%, 78%, and 85%
respectively (Fig. 23). A 3*2 (presentation phase X visual field) mixed ANOVA design was
employed to analyse the data. There were no significant effects for presentation phase
(F(2,8)=1.54, p=0.27), or for the visual field (F(2,8)=2.28, p=0.21). Finally, the presentation x
visual field interaction was not significant (F(2,8)=2.07, p=0.19).
In the experimental condition in which the stimuli were presented on a screen located at 0 in
the frontal visual field, data from pigeon 988 were not taken into consideration. Pigeon 988
showed a very unstable behaviour solving the task in the frontal visual field, and it was not
possible to collect enough sessions in which the percentage of correct responses of the training
trials was superior to 70%. Therefore, data from 5 birds were analysed. The percentage of
correct responses for the hold, thrust, and random presentation was 73%, 80%, and 82%
respectively (Fig. 23). A one way within-subjects ANOVA showed no significant differences
between hold, thrust, and random presentation (F(2,8)=1.36, p=0.31).
A further 3*3 within-subjects ANOVA analysis was calculated for all birds except for pigeon
988 with factors presentation (levels: hold, thrust, and random presentation) and position
(levels: both lateral visual fields presentation, one lateral visual field presentation, and frontal
presentation). The main effect of presentation was not significant (F(2,16)=.33, p=0.73.
Significant effects were found for the position of the stimuli (F(2,16)=5.64 p=0.03). A post hoc
analysis revealed significant differences between presenting the stimuli in both lateral visual
fields and a single lateral visual field presentation (p=0.02). No significant differences were
observed between presenting the stimuli in the frontal visual field and other positions of the
screens (p>.11) The interaction between presentation and position of the screen was not
significant (F(4,16)=.54, p=0.71).
100
90
90
80
80
70
60
2 LFs
50
1 LF
40
FF
30
20
% of correct reponses
% of correct reponses
100
70
60
LVF
50
RVF
40
30
20
10
10
0
Hold%
Thrust%
Random%
Presentation of the stimuli
Hold%
Thrust%
Random%
Figure 23: Percentage of correct responses for the hold, thrust, and random trials in both lateral visual fields
(LFs), one lateral visual field (LF), and in the frontal visual field (FF) (Figure A). Percentage of correct responses
for the hold, thrust, and random trials in the left visual field (LVF) and the right visual field (RVF) when the
stimuli were presented exclusively on one screen (Figure B).
4.2.2 Head-bobbing motion
The individual head-bobbing motion of each pigeon during hold, thrust, and random trials were
analysed when the stimuli were presented in both lateral fields simultaneously and when they
were presented in the frontal visual field. The condition in which the birds observed the stimuli
in exclusively in one lateral visual field was excluded in order to reduce the complexity of the
data analysis. In addition, during the one lateral visual field presentation the animals did not
receive a double signal of the stimuli like in the other two conditions. In addition, initial
analysis revealed not significant differences in the motion, between presenting the stimuli in
one or two screens.
The head trajectory was divided into head-bobbing cycles. A thrust phase was defined when
the speed of the head was equal or bigger than 240 mm/s in 3 or more consecutive frames (25
ms). A hold phase occurred, when the speed of the head was smaller than 240mm/s in 3 or
more consecutive frames. For the data analysis only complete head-bobbing cycles were
considered. That is, a hold phase is considered if it is followed by a thrust phase. A thrust phase
is considered only if it is predated by a hold phase. If a head-bobbing cycle was not complete,
or more than two missing frames were observed (for example due to marker occlusion by the
pigeon body), it was not considered in the data analysis. If within a phase a single frame was
missing or did not fulfil the speed requirements, the phase was not interrupted and was counted
in the data analysis. The head-bobbing phases that were bigger than 32 frames (260ms) were
not considered in the data analysis.
Finally, for the hold, the thrust and the catch trials presented in the frontal and in both lateral
visual field, the duration, the amplitude, and the speed, of the hold and the thrust phase were
averaged over 200 head-bobbing cycles obtained from 30 trials in each condition.
4.2.2.1 Duration of the hold and thrust phases
The average duration for the hold and the thrust phase were calculated for the hold, thrust and
random catch trials. When the stimuli were presented simultaneously in both lateral visual
fields, the hold phase duration for the hold, thrust, and random catch trials was 93.1 ms, 92.7
ms, and 94.4 ms, respectively. The average thrust phase duration for the hold, thrust, and
random catch trials was 102.7 ms, 101.6 ms, and 102.35 ms, respectively. When the stimuli
were presented in the frontal visual field, the hold phase duration for the hold, thrust, and
random catch trials was 77.8 ms, 79.3 ms, and 76.2 ms, respectively. The thrust phase duration
for the hold, thrust, and random trials was 93.6 ms, 94.5 ms, and 93.1 ms, respectively (Fig.
24). The average duration of the hold phase in the frontal and the lateral visual fields was 78
ms and 93 ms, respectively. Whereas, the thrust phase average duration was 93 ms and 102 ms,
respectively. The hold phase took place during 45% of the time in the frontal visual field and
during 47% of the time in the lateral visual field. The head-bobbing frequency was 5.8 Hz and
5.1 Hz for the frontal and the lateral visual fields, respectively.
Frontal visual field
Lateral visual fields
C
110
100
100
100
90
90
90
80
70
80
70
60
60
50
50
hold
thrust
random
Time (ms)
110
Time (ms)
Ti me (m s)
A
110
Hold phase
80
Thrust phase
70
60
50
hold
thrust
random
lateral
frontal
Visual field
Figure 24: Hold and thrust phase duration for the frontal visual field (A) and the lateral visual fields (B) in the
hold, thrust and random catch trials. Total average of the hold and the thrust phase duration in the frontal and in
the lateral visual fields (C)
A 2*3*2 (visual field*presentation*phase) within-subject ANOVA was calculated was

calculated for 5 pigeons (all birds except 988). The visual field has two levels, lateral visual
fields and frontal visual field location of the stimuli. The presentation has three levels, hold
phase presentation, thrust phase presentation and random presentation. The phase has two
levels, hold phase and thrust phase. Significant differences were found between observing the
stimuli in the frontal visual field and in the lateral visual fields (F(1,4)= 9.65, p=0.03).
Therefore, the head-bobbing cycle lasted significantly longer when the stimuli were presented
in the lateral visual fields (171.5 ms) than in the frontal visual field (195.95 ms). No significant
differences were observed in presentation (F(2,8)=0.06, p=0.94), phase (F(1,4)=4.12, p=0.11), and
in the interactions between the factors (p>0.05).
Individual 2*3*2 (visual field*presentation*phase) analyses of the motion characteristics for

each pigeons were also calculated. The phase durations of 30 catch trials in each condition
were analysed. Pigeons 251, 347, 51, and 259 showed significant differences (Table 3 and
Appendix B: Fig. B-2) in visual field and phase. On the one hand, the head-bobbing cycle was
significantly longer when the stimuli were located in the lateral visual fields than in the frontal
visual field. On the other hand, the thrust phase duration was significantly longer than the hold
phase duration.
Pigeons 251, 347, and 51 showed significant differences in the interaction between visual
field*phase (Table 3 and Appendix B: Fig. B-2). For these three pigeons, the difference in the
hold phase duration between the lateral and the frontal visual field was significantly bigger
than the difference in the thrust phase duration between the lateral and the frontal visual field.
That is, the hold phase duration was longer in the lateral visual field than in the frontal visual
field. Pigeon 512 showed exclusively significant differences between the hold and thrust phase
durations. Any other factor or interaction between the factors was not significant (Table 3, and
Appendix B: Fig. B-2).
4.2.2.2 Amplitude of the hold and the thrust phases
The average amplitude for the hold and the thrust phases were calculated for the hold, thrust,
and random catch trials. When the stimuli were presented simultaneously in both lateral visual
fields, the hold phase amplitude for the hold, thrust, and random catch trials were 2.7 mm, 2.8
mm, and 2.6 mm, respectively. The average thrust phase distances for the hold, thrust, and
random catch trials were 80.5 mm, 79.5 mm, and 81.6 mm, respectively. When the stimuli
were presented in the frontal visual field, the hold amplitude distances for the hold, thrust, and
random catch trials were 2.2 mm, 2.3 mm, and 2.2 mm, respectively. The thrust phase
durations for the hold, thrust, and random trials were 75.4 mm, 78 mm, and 76.7 mm,
respectively (Fig. 25).
90
80
80
80
70
70
70
60
50
40
30
Amplitude (mm)
90
Amplitude (mm)
Amplitude (mm)
A
90
60
50
40
30
60
50
30
20
20
20
10
10
10
hold
thrust
random
Hold phase
Thrust phase
40
0
hold
thrust
random
lateral
frontal
Visual field
Figure 25: Hold and thrust phase average amplitude for the frontal visual field (A) and the lateral visual fields (B)
in the hold, thrust and random catch trials. Total average of the hold and the thrust phase amplitude in the frontal
and in the lateral visual fields (C).
A 2*3*2 (visual field*presentation*phase) within-subject ANOVA was also calculated with

the average amplitude in the hold and the thrust phases in five of the pigeons. No significant
differences were observed for factors visual field (F(1,4)=2.57, p=.18) and presentation
(F(1,4)=.18, p=.83). Significant differences were found for factor phase (F(1,4)=813.05, p<.001).
Therefore, as expected the hold phase amplitude was significantly smaller than the thrust phase
amplitude. No significant effects were found in the interactions between the factors (p>.05)
The individual 2*3*2 (visual field*presentation*phase) ANOVA for each pigeon revealed
significant differences in all pigeons for the factor phase (Table 3 and Appendix B: Fig B-2). In
addition, pigeon 251 also showed significant differences in factors visual field (F(1,29)=42.3,
p>.001), presentation
(F(1,28)=4.9, p=.01), in visual field*phase interaction (F(1,29)=34.2,
p>.001), and in presentation*phase interaction (F(2,58)=5.98, p=.005).
4.2.2.3 Speed of the hold and the thrust phases
The average speed for the hold and the thrust phases was calculated for the hold, thrust, and
random catch trials. When the stimuli were presented simultaneously in both lateral visual
fields, the hold phase speed for the hold, thrust, and random catch trials was 29.9 mm/s, 25.8
mm/s, and 25.4 mm/s, respectively. The average thrust phase speed for the hold, thrust, and
random catch trials was 810.4 mm/s, 797.5 mm/s, and 805.5 mm/s, respectively. When the
stimuli were presented simultaneously in the frontal visual field, the hold phase speed for the
hold, thrust and random catch trials was 30.1 mm/s, 30 mm/s, and 30.2 mm/s, respectively. The
average thrust phase speed for the hold, thrust, and random catch trials was 823.9 mm, 825.75
mm/s, and 806.5 mm/s, respectively (Fig. 26).
B
900
800
800
800
700
700
700
600
500
400
300
Speed (mm/s)
900
900
Speed (mm/s)
Speed (mm/S)
600
500
400
300
600
500
hold phase
400
thrust phase
300
200
200
200
100
100
100
0
hold
thrust
Visual field
random
hold
thrust
random
lateral
frontal
Visual field
Figure 26: Hold and thrust phase average speed for the frontal visual field (A) and the lateral visual fields (B) in
the hold, thrust and random catch trials. Total average of the hold and the thrust phase amplitude in the frontal and
in the lateral visual fields (C).
A 2*3*2 (visual field*presentation*phase) within-subject ANOVA was calculated with the

average speed for each pigeon in the hold and the thrust phases in five of the pigeons. No
significant differences were observed in factors visual field (F(1,4)= 2.01, p=.23) and
presentation (F(1,4)=.82, p=.47). Significant differences were found in factor phase
(F(1,4)=586.8, p<.001). No significant effects were found in the interactions between the factors
(p>.05).
The analysis of the individual motion of the pigeons revealed that the speed in the frontal field
presentation was significantly bigger than the speed in the lateral visual fields presentation for
pigeons 51, 259, and 347 (Fig. 27) The speed of the pigeon during the random catch trials was
significantly smaller than in the thrust and hold catch trials for pigeons 347 and 512.
Significant differences in the thrust phase speed between the random trials and both the hold
and thrust phase trials were observed in pigeons 259, 347, and 512. No differences were
observed between the hold presentation and the thrust presentation.
500
speed (mm/s)
450
p <.05
p <.05
p >.05
p >.05
p <.05
400
Figure 27: Head-bobbing cycle speed for each

individual pigeon, when the stimulus were presented
either simultaneously in both lateral visual fields or
in the frontal visual field
350
300
250
51
lateral visual fields
frontal visual field
251
259
347
512
Pigeon
In addition, the data analysis for pigeon 347 found significant differences in all interactions.
Pigeon 512 also showed significant differences in the interactions screen*presentation and
screen*presentation*phase. Finally, in pigeon 259, significant effects were observed in the
interactions also in presentation*phase.
In conclusion, significant differences were found between the hold and thrust phases in all
analysed parameters. The head-bobbing cycle duration was significantly longer in the lateral
visual fields than in the frontal visual field in three birds. This effect is mainly explained by a
longer hold phase duration in the lateral visual field than in the frontal visual field condition.
The overall speed of a head-bobbing cycle, and therefore the speed of the motion, was
significantly larger in the frontal visual field than in the lateral visual field. In some animals
significant differences were found in the speed, between the random trials and both thrust and
hold trials. No significant differences were found in duration, distance, and speed between
presenting the stimuli during the hold phase and during thrust phase.
Significant effects ( p<0.05 )
Duration
Visual
field (Vf)
51,251,
259,347,
all
251
Presentation
(Pr)
51,259,
347
347,512
251
Amplitude
Speed
Phase (Ph)
51,251,
259,347,
512
51,251,
259,347,
512, all
51,251,
259,347,
512, all
Vf.*Pr.
Vf.*Ph.
Pr.*Ph.
Vf.*Pr.*Ph
259,347,
512
347,512
51, 251,
347
251
347,512
347
Table 3: Names of the birds that showed significant effects (p<0.05) observed in the ANOVA for duration,
distances, and speed in the different experimental conditions.
4.3 Discussion
Pattern recognition in pigeons was studied by presenting two shapes either during the hold
phase, thrust phase, and random presentation. The pigeons were tested in both lateral visual
fields (90), a single lateral visual field (90), and the frontal visual field (0). Both the
percentages of correct responses were analysed and the motions of the pigeons heads were
analysed. For the hold and the thrust phase, the duration, the amplitude, and the speed were
calculated in the frontal and in both lateral visual fields presentation.
4.3.1 Pattern recognition during the thrust phase
During the head-bobbing hold phase, the head is stabilized in the space (Davies & Green,
1988; Friedman, 1975b; Frost, 1978; Troje & Frost, 2000) and saccadic eye movements have
rarely been observed (Bloch, Lemeignan, & Martinoya, 1987; Pratt, 1982; Wohlschlger,
Jger, & Delius, 1993). Therefore, it is believed that head-bobbing may aid in pattern
recognition by stabilizing the retinal image (Davies & Green, 1988; Frost, 1978). Furthermore,
it has been observed that the thrust phase, where the head is moving forward, is accompanied
by saccades. It has been proposed that during the thrust phase there is probably no visual input
and the sensitivity of the visual system is reduced by saccadic suppression (Brooks & Holden,
1973; Pratt, 1982). For this reason, we expected higher difficulties in solving the
discrimination task when the stimulus presentation occurred within the thrust phase.
Surprisingly, such differences were not found between presenting the stimuli during the hold
phase, thrust phase, or randomly within the percentage of correct responses. Contrary to our
initial predictions, the animals were able to discriminate the stimuli when they were presented
within the thrust phase as successfully as when presented within the hold phase, or randomly.
Given that pigeons eyes are located laterally, the amount of optic flow perceived during the
thrust phase when a stimulus is located in the lateral visual field must be greater than the optic
flow perceived in the frontal visual field. Therefore, we expected advantages in perceiving a
stimulus during the thrust phase in the frontal visual field with respect to the lateral visual field.
No significant differences between observing the stimuli in the frontal visual field and the
lateral visual field were found during the thrust phase. The presentation of the stimuli within
the thrust phase was strictly controlled.
Significant effects were observed between the different conditions of presentation in one lateral
visual field or simultaneously in both lateral visual fields. Taking into account that the pigeons
were trained in both visual fields, the double presentation might have enhanced the perception
of the stimuli and facilitated the task. No significant asymmetries were observed between the
left and the right visual fields.
The data provide solid evidence to affirm that pigeons are capable of pattern discrimination
during the trust phase. Two factors may help to explain that: the existence of saccadic eyes
movements during the thrust phase and the characteristics of the stimuli.
4.3.1.1 Eye movements during the thrust phase
Pratt (1982) found that saccadic eye movements in pigeons were present in around 80% of the
thrust phases, and were not made during hold phases. He proposed that the saccadic thrust
phases have no particular visual function, other than to move the eye to a new viewpoint. He
also suggested that the remaining 20% of thrust phases without saccades might serve to
calculate depth through motion parallax. Other authors observed three kinds of saccades in
unrestrained pigeons: embedded saccades in the thrust phase (86%), overlapping saccades that
started earlier or finished later than the thrust phase (7.2%), and saccades occurring during the
hold phase period (6.8%) (Wohlschlger et al., 1993). The possibility that pattern recognition
occurred during the thrust phases without saccadic eyes movements is very unlikely. Pigeons
performed 10 head-bobbing cycles on average while walking form the light barrier to the
feeders. Therefore, in this period of time a maximum of two thrust phases without saccades
may occur. In addition the stimuli were presented exclusively during 75 ms within the thrust
phase.
A pigeons oculomotor strategy depends on the visual field. An attention-calling stimulus

presented in the lateral field of one eye elicits an ipsilateral orienting saccade towards the target
which only sometimes coincides with the movement of the contralateral eye. In contrast, an
attention-calling stimulus presented in the frontal binocular visual field elicits coordinated
converging saccades (Bloch et al., 1987).
On the one hand, we found that pigeons are capable of pattern discrimination during the thrust
phase. On the other hand saccadic eye movements have been observed in pigeons exclusively
during the thrust phase during walking (Bloch, Jaeger, Lemeignan, & Martinoya, 1988; Pratt,
1982). The possibility that the saccadic eye movements may help to stabilize the retinal image
during the thrust phase should be taken into consideration. In fact backward and forward
saccadic movements, lasting around 22.8 ms, were observed in pigeons (Wohlschlger et al.,
1993). Although most of the saccades may serve to monocularly fixate visual features (Bloch
et al., 1988; Friedman, 1975; Wohlschlger et al., 1993), a fraction of the backward saccades
may be used to maintain fixation by compensating the retinal image shift due to the forward
head thrust (Wohlschlger et al., 1993).
4.3.1.2 Characteristic of the stimuli
Another possible explanation for the capability of the pigeons to discriminate stimuli within the
thrust phase could be the characteristic of the stimuli used. Although the difficulty level of the
task was very high, the patterns presented were easy to discriminate. They were two 5*5 cm
white shapes on a black background. It may well happen that, small objects, like seeds and
grains, are more difficult to discriminate during the thrust phase. Head-bobbing birds may have
difficulties to discriminate small features hidden in a low contrast complex background, like a
grain hidden in the yellow grass. In humans saccades are very fast at speeds up to 900/s, in
order to reduce the image blur to a minimum (Land, 1999), whereas the thrust phase in birds is
much slower, which may allow pattern recognition. In addition, the hold phase can be
substituted by a flexion phase in which the retinal image is no longer stabilized. Head-bobbing
should be involved in other important functions. Motion parallax is a strong candidate, but
most probably head-bobbing has some other unexplored functions in different birds.
The lateral visual field serves for far sighting, monitoring predators and conspecifics, as well as
to detect food at some distance (Fernndez-Juricic et al., 2004; Green et al., 1994). Even if
pigeons are not be capable of discriminating small and low contrast objects within the thrust
phase, being capable of perceiving a predator during the entire head-bobbing cycle may
constitute an ecological advantage. During foraging, pigeons mainly focus on targets with the
frontal visual field (Goodale, 1982) and longer periods of image stabilization have been
observed in hooded cranes (Cronin et al., 2005). Due to the lateral disposition of the pigeons
eyes, the amount of optic flow in the frontal visual field is reduced. Focusing small targets with
the frontal visual field might have the advantage of receiving a double signal, minimizing the
motion blur and increasing the visual acuity.
On the one hand, pigeons are capable of distinguishing medium sized easy patterns during the
thrust phase. On the other hand, head-bobbing may assist to discriminate small features at short
distances. Objects located at long distances are less affected by the optic flow provoked by the
birds motion. In addition, image stabilization could be achieved in some birds by rotating the
eyes, although in relation to the skull, birds have large eyes that limit eye mobility (Martin and
Katzir, 1995). The eye mobility of many birds may be enough to counteract the retina slip at
medium to long distances, but the blur of small features located at short distances may require
the contribution of head-bobbing. That would explain why about 75% of the head-bobbing
birds were foraging birds looking for small feeding sources, like seeds, grain, worms, etc (see
section 5).
4.3.2 Head-bobbing motion
The motion analysis of the pigeons heads revealed different strategies when observing a
stimulus in different parts of the visual field. First, four of the five pigeons, depending on the
stimulus presentation, varied the overall speed of the motion by decreasing the duration of the
head-bobbing cycle, while keeping the distance invariable. If the stimuli were located in the
frontal visual field, the speed of the animals was increased and the duration of the headbobbing cycle was reduced in comparison to the lateral visual field. Second, thrust phases were
longer than hold phases. Third, it was observed that an increase of the speed resulted in a
reduced hold phase. We observed significantly shorter hold phases in the frontal visual field
than in the lateral visual field in three animals. This phenomenon has previously been reported
in pigeons by single-frame analysis of walking pigeons. If the speed of the motion is increased,
the hold phase is reduced until speeds above 810mm/s (Davies & Green, 1988), in which the
hold phase is replaced by a flexion phase. It was suggested that head-bobbing is controlled by
the speed and the visuomotor requirements of the birds, but not by the form of locomotion
(Davies & Green, 1988).
Interestingly, one bird used a different strategy varying the head-bobbing frequency: it kept
constant the motion speed across the conditions, varying the amplitude and the duration of the
head-bobbing cycles. The head-bobbing frequency was bigger in the frontal visual field than in
the lateral visual field presentations, whereas the overall speed of the pigeon motion did not
vary. Although this strategy only appears in one of the birds, it may be a common strategy of
birds. Chickens confronted with new objects tend to walk slower and perform large head
movements (Dawkins, 2002). An extreme example occurs when static pigeons and other birds
are found doing head-bobbing while observing their environment. Variations in the headbobbing cycle duration independent of the motion speed can be useful to increase the optic
flow, and therefore enhance distance calculations. These data point out that head-bobbing
behaviour in birds is a rather flexible behaviour, which varies according to the situations.
Previous head-bobbing motion analyses found longer durations of the head-bobbing cycle than
in the present experiment. The mean duration of the hold phase found in courting birds and
during turning behaviour was 156 ms and 139 ms, respectively, whereas the mean duration for
the thrust phase was 132 ms and 96 ms, respectively (Troje & Frost, 2000). In the present
experiment, the average duration of the hold phase in the frontal and the lateral visual fields
was 78 ms and 93 ms, respectively, whereas the thrust phase average duration was 93 ms and
102 ms, respectively. The hold phase took place during 45% of the time in the frontal visual
field, and during 47% of the time in the lateral visual fields. In comparison, Frost (1978)
described that the hold phase took place during 63% of the time. Troje and Frost (2000) found
that the hold phase represented around 57% of the time.
Factors like different experimental conditions and techniques for capturing the head-bobbing
behaviour may explain the differences in the results, although the pigeons speed may be
mainly responsible of these differences. The average speed during the hold phase and the thrust
phase was around 27 mm/s and 818 mm/s respectively, while in previous experiments it was
found to be around 3.6 mm/s and 630 mm/s (Frost, 1978; Troje & Frost, 2000). The higher
speed, combined with the chosen threshold (240 mm/s) could result in the observed higher
speed during the hold phase.
Pigeons are capable of recognizing medium and big patterns during the thrust phase. Although
further investigations are needed, head-bobbing may help recognizing small features hidden in
complex backgrounds. In addition it may be involved in solving other visual challengers such
as depth perception. The capability of discriminating relevant stimuli, like predators, during the
entire head-bobbing cycle may increase the survival rate of birds. Pigeons can modify their
head-bobbing speed and frequency depending on the stimulus location in the visual field. In
addition, different visual inputs may lead into different head-bobbing styles.
Why Do Birds Bob Their Heads? 82

5. EXPERIMENT 5: WHY DO BIRDS BOB THEIR HEADS?
Although head-bobbing behaviour has been very often discussed in the literature, the birds that
bob their head are not listed, only around 30 species of head-bobbing birds have been listed in
the literature (Cronin et al., 2005; Daanje, 1951; Dagg, 1977b; Dunlap & Mowrer, 1930; Frost,
1978; Fujita, 2003, 2004). Frost (1978) reported that head-bobbing occurs in at least 8 of the 27
orders of birds. Dagg (1977) listed 28 head-bobbing species during locomotion such as
pigeons, doves, hens, starlings, pheasants, coots, rails, sand-pipers, phalaropes, parrots,
magpies and quails. These lists are very incomplete, but they suggest that at least 1/3 of the
birds could show head-bobbing. Comparisons between head-bobbing or non head-bobbing
birds have been rarely done and the ecological and behavioural characteristics were not often
considered. Many questions remain open. It is not known if all birds of a family or order are
head-bobbing birds. Furthermore, it is unknown if head-bobbing could be a determinant trait in
a phylogenetic classification.
Retinal stabilization is probably the most accepted head-bobbing function in pigeons, much
evidences suggest that head-bobbing might have other important contributions. Pigeons and
other birds can display head-bobbing without stabilising the head. It has been observed that
during landing and running the hold phase is replaced by a flexion phase, in which the velocity
of the head relative to the surrounding is different from zero. The Hooded crane stabilizes the
retinal image during foraging (Cronin et al., 2005). In contrast, The Kori bustard, also during
foraging, shows rapid thrust phases which most probably are used in order to amplify the
relative motion of an object on the ground, this facilitates object detection. Different birds may
need to afford diverse ecological and visual demands. Therefore, head-bobbing may play
different roles in different environments.
A list of head-bobbing birds and non head-bobbing birds may be a useful tool to estimate the
importance of the head-bobbing in the class aves. It would provide a frame in which to
integrate previous and future research in restricted conditions in the laboratory.

The aim of this study is to analyse the ecological and behavioural factors underlying headbobbing behaviour, such as predatory pressure, source of feeding, habitat, etc. An open
question is whether head-bobbing has evolved once or several times during the evolution.
Taking in account these findings together with previous laboratory investigations, the
functional significance and the phylogenetic origins of head-bobbing will be discussed.
5.1 Methods
This study was divided into three parts. Firstly, birds belonging to a variety of different orders
and families were observed and video recorded. The species were classified as head-bobbing,
non head-bobbing, hopping and/or other head movements birds following a 2004 update of
Clements classification (Clements, 2000). Second, those data were fed into Sibley &
Ahlquists (1990) taxonomy tree. Finally, the ecological and behavioural characters under
head-bobbing behaviour were analysed.
5.1.1 List of head-bobbing and non head-bobbing birds

Table C-1 (see appendix C) list 322 species of birds which were observed and/or videotaped in
their natural environment or in different zoos across Germany. The main aim was to establish a
list of head-bobbing and non head-bobbing birds covering all orders and most of the families of
the world. Birds observation was done in the natural environment in Europe, Africa, and
North America. Rare birds and species from other continents were observed in semi-captivity
in different zoos of Germany. The birds were organized following Clements checklist of birds
(Clements 2000; 2004 updated version). This classification is constantly being updated and
offers an easy and intuitive way of organizing birds especially useful in field observation.
From the 204 families of the birds of the world (Clements, 2000; 2004 updated version), 100
families and around 58% of the living birds belong to the Passeriformes order. Although data
about Passeriformes order were also collected, major efforts were done in collecting data in

non Passeriformes birds. In addition to the field observation data, bibliographic data from
previous studies were also incorporated to the list.
Each bird was classified as head-bobbing (HB), hoping bird (BB), non-bobbing bird (NB)
and/or showing other characteristics head movements (OHM).
Classifying a bird in one of these categories does not imply necessarily exclusion from another
category. For example, some birds were classified as HB and BB.
Head-bobbing behaviour occurs when a bird shows repeated backward and forward movement
of the head in the horizontal plane in any ecological or behavioural context like walking,
landing, swimming, etc. If the head-bobbing behaviour was exclusively observed during
courtship, the specie was not included in the HB bird category. Head-bobbing is a flexible
behaviour among the species. Some species of birds display it often and in a wide variety of
circumstances, while other species show head-bobbing occasionally and in very specific
situations. For this reason the following notation within the category HB was used:
- HB: Head-bobbing during walking
- HB(s): Head-bobbing during swimming.
- HB(ws) Head-bobbing during walking and swimming
- HB(wl): Head-bobbing during walking and landing
- HB(*): Rare or occasional Head-bobbing
The hopping behaviour observed in many birds may be similar to head-bobbing and may play a
similar role (Davies and Green, 1988; Friedman, 1975). Hopping can be described as having a
hold phase, while the birds stand in the ground, and a thrust face, while the birds are jumping.
For this reason hopping birds are classified as body-bobbing birds (BB).
Non-bobbing birds (NB) are those birds, which did show neither head-bobbing nor bodybobbing. In other words they do walk without a backward and forward horizontal movement of

head and they do not hop. A traditional example of this type of bird is the Silver Gull (Dagg,
1977b).
Under the category OHM, birds that move the head vertically, like plovers (Casperson, 1999),
were included. Birds that have side to side head movements, like owls (van der Willigen et al.,
2002) and parrots were also classified as OHM. Although, this category has been considered
to elaborate the bird list, it is not conceptually equivalent to the others. The other categories
corresponds to different head or body movements during locomotion, while birds observed
doing OHM were generally static.
Classifying a bird within a category is often a difficult task. A bird was classified only when
clear evidences were observed. However, we cannot exclude that a bird may be able to display
additional behaviours that we missed to observe.
The number of orders, families and species that showed HB, BB, NB, and OHM were counted
and analysed. In the list (Fig. 28 and Appendix: Table C-3) if two motion styles appear
separated by &, it means that the same bird shows both behaviours. For example magpies are
classified as HB&BB because they can display both kinds of behaviours. If within a family or
an order, any of those motion styles appears separated by a comma, it means that two or more
motion styles have been found in different species. For example, marabous are a NB birds and
white storks are HB birds, both of them belong to the Ciconiidae family, therefore the
Ciconiidae family is classified as HB, NB.
5.1.2 Taxonomic tree of head-bobbing and non head-bobbing birds

In order to investigate the evolutionary characteristics of head-bobbing, the observed species of
birds were classified following a taxonomic tree. A taxonomic tree was preferred instead a
phylogenetic tree, because a phylogenetic tree is always fluctuating and some taxa are better
known than other. A taxonomic tree has less detailed information and it is easier to handle and
less changeable (von Euler, 2001). For this reason we choose Sibley and Ahlquist taxonomy

(1990; 1988) to classify our list of birds, although phylogenetic would be considered in specific
cases. In this taxonomy, the species were divided in 16 different taxonomic levels by using
DNA-DNA hybridisation studies. Each of these levels refers to a particular range of genetic
distinctness weight (given in brackets) measured in T50H. The levels proposed by Sibley et al.
(1988) are the following: species (0-2.2), subtribe (2.2-4.5), tribe (4.5-7), subfamily (7-9),
family (9-11), superfamily (11-13), parvorder (13-15.5), infraorder (15.5-18), suborder (1820), order (20-22), superorder (22-24.5), parvclas (24.5-27), infraclass (27-29), subclass (2931), class (31-33), superclass (33-36) (Table 4). When the classification was first developed,
one T50H was equivalent to 4.5 million years. According to Sybley and Alquist (1990) it is
likely that this calibration factor is not applicable to all birds, but only to those with ages at first
breeding of ca. 2-4 years.
Category
Superclass
Class
Subclass
Infraclass
Parvclass
Superorder
Order
Suborder
Infraorder
Parvorder
Superfamily
Family
Subfamily
Tribe
Subtribe
Congeneric spp.
Ending
ornithes
aves
ae
morphae
iformes
i
ides
ida
oidea
idea
inae
ini
ina
Delta TsoH
33-36
31-33
29-31
27-29
24. 5-27
22-24.5
20-22
18-20
15.5-18
13-15.5
11-13
9-11
7-9
4.5-7
2.2-4.5
0-2.2
Table 4: Categories, endings of categorical names, and

T50H ranges for each categorical rank in Sybley and
Ahlquists taxonomy (1990)
Sibley and Ahlquists work has been often discussed in the literature, many critics have arisen
since the publication of their work {references and review can be found in O'Hara, 1991
#3329}, but many research support the overall topology of Sibley & Ahlquist (Cooper &
Penny, 1997; von Euler, 2001). The authors themselves do gather the different opinions about
their own work in the preface to the second printing of phylogeny and classification of birds
(Sibley & Ahlquist, 1990). In spite of the critics it is the most complete phylogenetic and
taxonomic tree found in the literature, an essential prerequisite for this work.
By creating this list of head-bobbing and non head-bobbing birds, it was observed that in most
of the cases if a member of a family has head-bobbing, the others members do also have headbobbing. In case of exceptions to this rule, the detailed phylogenetic relationship among the
birds of this family was considered, taking in account several points of view from different
authors and methods.
5.1.3 Analysis of behavioural and ecological factors under head-bobbing

For each covered family, a representative bird was selected. If a family contained different
species with different bobbing styles (HB, BB, NB), a representative bird of each style was
chosen. In total 73 species were analysed: 39 HB birds, 28 NB birds, and 6 BB birds. For each
of those birds, the following ecological and behavioural characters were analysed: feeding
source, feeding method, group size, peak of activity, habitat, flying abilities, and predator
pressure (Apeendix C: Table C-3).
The feeding source was classified in 6 categories. The food size was taked in consideration for
creating the categories: 0 = small molluscs, 1 = fruits, leaves, seeds, small vertebrates,
invertebrates, insects, 2 = small fishes, squid, crustaceans, 3 = small vertebrates, reptiles, frogs,
4 = vertebrates: birds and small mammals, and 5 = carrion.
Feeding method was classified in seven categories: 1 = foraging or wading, 2 = collecting in
trees and bushes, 3 = diving in water, 4 = stalking and spearing, 5 = hunting and searching
from the air, 6 = digging and scooping, and 7 = filtering.
The group size was ranked from zero to two: 0 = solitary or pairs, 1 = small groups (from 2 to
10 birds), 2 = big groups (up to 10 birds).
The peak of activity was range according to the intensity of the light, it has three categories: 1
= nocturnal, 2 = crepuscular, and 3 = diurnal.
The habitat was classified from dry to aquatic habitats: 1 = savannah and other open woodlands
like highlands, 2 = forests, 3 = swamps, marshes and muddy shores, 4 = lakes and rivers, and 5
= see, ocean and coastal areas.
The flying ability was classified from terrestrial birds to skilled fliers: 0 = terrestrial, 1 = fly
short distances (awkward), 2 = normal flyer, and 3 = elegant and skilled.
Finally, the predator pressure was ranged from 0 to 2, where 0 = low predator pressure, 1 =
medium pressure, 2 = high predator pressure.
The ecological and behavioural characteristics were evaluated by doing an exhaustive
bibliography search (Baran-Marescot, 2005; Jonsson, 1999; Perrins, 1991; Peterson & Hollon,
1983; Stevenson & Fanshawe, 2001). After collecting all necessary data in an initial list, values
were given for each bird in each character. Independent judgments from two experimented
persons in field observation were used. To simplify the data, each species was assigned
exclusively to one range in each trait. For example if the same specie lives in different habitats,
the most common habitat was chosen for the data analysis. Occasionally, it was difficult to
assign a bird to a range or category, in case of disagreement a third judger helped to classify
the bird. In spite of the careful method used, some controversy remained in a few cases.
Selecting only one bird from each family could be a problem regarding the representativeness
of this bird. In other words, the question might be if the selected species of bird share the main
ecological and behavioural characteristics with all the birds belonging to this family. In most of
the families this should not be a problem, given the fact that behavioural and ecological
characters are often use as an effective method for classifying birds (Hughes, 1996; Hughes &
Baker, 1999). The problems might arise in families in which there is not a general acceptance
about the classification due to the different methodology used. In this case, a bird which is not
on the centre of the controversy was chosen. Furthermore, in some cases the head-bobbing
behaviour might contribute to clarify some parts of birds classification.
5.2 Results
A total amount of 322 species of birds were observed and video recorded in their natural
environment or in semi-captivity conditions. From the 32 orders of Clements classification,
birds belonging to 26 orders were observed (Fig 28 and Appendix C: Table C-1). It was not
possible to collect data about species belonging to Caprimulgiformes, Apodiformes,
Dinornithiformes, Trochiliformes, Trogoniformes, and Opisthocomiformes orders. The
Caprimugiformes and Dinornithiformes (kiwis) order contains species of shy nocturnal birds
difficult to observe. Birds belonging to the Apodiformes (swifts and treeswitfs) and
Trochiliformes (hummingbirds) orders have tiny legs, are mainly aerial and walk rarely on the
ground. Trogons (Trogoniformes) and Hoatzin (Opisthocomiformes) are arboreal birds that
also walk rarely in the ground. As a result of it, it was not possible to gather any information
regarding head-bobbing in these species of birds.
Data about the Passeriformes order were collected, but the efforts were focused in observing
non Passeriformes birds. As a result of it, we collected data in 68 non Passeriformes families
and 25 Passeriformes families. Approximately half of the families of the birds of the world are
represented in the list.
5.2.1 Head-bobbing and non head-bobbing birds list

139 birds were classified as head-bobbing birds (HB), 64 were body-bobbing birds (BB), 6
birds showed other head movements (OHM), 23 species were classified as head-bobbing and
body-bobbing birds (HB&BB), 2 birds did have head-bobbing and other head movements
(OHM) and 87 species did display neither head-bobbing nor body-bobbing (Fig. 29 and
Appendix C: Table C-1 ).
In 85 families out of 93 families, all members observed belonged to the same category. For
example all species of pigeons are head-bobbing birds. In the remaining eight families,

different species within a family show different motion styles. For example, some species of
ovenbirds (Furnariidae) hop while others bob their heads. Six families (Musophagidae,
Furnariidae, Turdidae, Sturnidae, Ploceidae, Fringillidae) alternate between HB and BB. These
behaviours may be equivalent from the visual point of view (Davies & Green, 1988; Frost,
1978). Clear exceptions are found in three families Cuculidae, Charadriidae, and Ciconiidae.
The observed cuculidaes species, were BB or HB unless the Greater Roadrunner (Geococcyx
californianus). All charadridae birds were HB birds, unless Southern Lapwing (Vanellus
chilensis). Head-bobbing was observed in all storks (ciconiidae) unless Marabou (Leeptoptilos
crumeniferus). Eighteen of the 26 orders contain birds that share the same motion pattern.
Birds within Passeriformes order alternate between HB, BB and HB&BB. Seven orders
contain species showing different motion styles (Fig. 28 and Appendix C: Table C-1).
ORDER
FAMILY
SPECIES
HB
BB
NB
OHM
HB&BB
HB&OHM
HB, BB
HB, NB
BB, NB
HB, NB, OHM
BB, HB&BB
HB, HB&OHM
HB,NB,HB&OHM
HB,BB, HB&BB
NB, BB, HB, HB&BB
7
2
5
3
1
35
22
23
5
1
139
64
87
7
23
2
1
1
1
Total
Clements Checklist
26
32
93
204
3
1
1
2
1
3
1
Figure 28: Number of orders, families and species

that show head-bobbing (HB), hopping (BB), no
head-bobbing and no hopping (NB), and other
head movements (OHM). Within and order or a
family, if two bobbing styles are separated by a
comma, it means that two or more motion styles
have been found in different species. For example,
marabous are NB birds and white storks are HB
birds, both of them belong to the Ciconiidae
family, therefore this family is classified as HB,
NB. When two bobbing styles appear separated
by &, it means that the same specie shows both
behaviours. For example magpies are classified as
HB&BB.
322
~10.000
Head-bobbing was observed in 164 species (48%), 43 families and 15 orders. Body-bobbing
was observed was observed in 88 species (25%), 20 families and 7 orders. No-bobbing birds
were observed in 87 species (25%), 25 families and 12 orders. Other-head-movements were
observed in 8 species (2%), 6 families and 5 orders (Fig. 29).
NB
25%
HB
BB
NB
OHM
ORDER
FAMILY
SPECIES
15
7
12
5
44
29
25
6
165
88
87
8
OHM
2%
BB
25%
HB
48%
Figure 29: The first and the second columns represent the number of orders and families that contain species
displaying HB, BB, NB, and OHM. The third column represents the number of species that show any of the
bobbing styles. An order, family, or specie can be included in several categories. For example, Magpie is counted
twice as HB and as BB. The chart represents the percentage of species that show HB, BB, NB, or OHM.
Twenty species of birds showed a rare or occasional head-bobbing (HB*). In 10 species it was
possible to establish under which circumstances head-bobbing occurred (Table 5). Headbobbing was found in ostriches walking through long grasses in the savannah (Fig. 32), but not
while foraging or in captivity. Head-bobbing was also observed in Emu chicks in semicaptivity conditions, but not in adults. A related species, Greater Rhea (Rhea americana) did
not show head-bobbing in captivity and it was classified as NB, but it cannot be excluded that
under certain circumstances rheas may perform head-bobbing. Plovers and lapwings
(Charadriidae family) showed head-bobbing while walking slowly in tidal mudflats, shallow
flood pools, but not in open short-grass lands or bare soil. Bustards performed fast headmovements while walking very slowly in the savannah looking for food. Jackdaws, crows and
starlings showed head-bobbing in slow locomotion, but not at fast speed.
Other species like moorhens, grebes, and coots also exhibit occasional head-bobbing while
swimming, but it was not possible to undoubtedly establish when the head-bobbing behaviour
occurs. Nevertheless, longer periods of field observation in their natural environment revealed
that these aquatic birds showed head-bobbing while swimming slowly, when a novel stimulus
appears, and while approaching the shore. They did not show head-bobbing while swimming
fast, while escaping, or while moving towards a clear target like food.
In addition, marabous were classified as NB birds, because they normally do not show headbobbing. However, in a very specific situation, a flock of marabous showed traces of head-

bobbing behaviour. The birds were occupied in searching small pieces of carrion left by the
crocodiles, dragged by the water in a river, during migration time in Tanzania. Unfortunately,
it was not possible to record a clear footage of the birds.
Common name
Ostrich
Australian Emu
Little Ringed Plover
Egyptian Plover
Northen Lapwing
Blacksmith Lapwing
Kori Bustard
Black Bustard
Jackdaws & crows
Starling
Oystercatcher
Scientific name
Struthio camelus
Dromaius novaehollandiae
Charadrius dubius
Pluvianus aegyptius
Vanellus vanellus
Vanellus armatus
Ardeotis kori
Eupodotis afra
Corvus sp.
Starling sp.
Haematopus sp.
HB situation
Walking through long grasses
Chicks in captivity
Foraging in shallow flood pools
While foraging
While foraging
Walking slow
Walking slow
Walking slow
Table 5: In ten species of birds with rare or occasional head-bobbing, it was possible to establish the
circumstances under which head-bobbing occurs. Where sp. = all species contained in a genus
5.2.2 Taxonomic tree of head-bobbing and non-bobbing birds

The field observations about head-bobbing and non-bobbing birds were feed into Sibley and
Ahlquist taxonomy. Furthermore, the information given in this part regarding phylogenetic
relationships is based on the Sybley and Ahlquist taxonomy (Sibley & Ahlquist, 1990) unless
explicit citation. In this section, the information gathered in Fig. 30 and in Appendix C:
Table C-2 is described together with a resume of the birds ecological and behavioural
characteristics included in each taxon. In Fig. 30 when all observed birds within a taxon shared
a common bobbing style, further sub-taxa were not included. In comparison in Appendix C:
Table C-2 all studied taxa and sub-taxa were included.
In Sibley and Alhquists classification, the modern birds Neornithes are divided into two
infraclasses: Eoaves (Paleonagthae) and Neoaves (Neonagthae). All species belonging to the
infraclass Eoaves (ostriches, rheas, cassowaries, tinamous and emus) except for rheas (Ratites),
were head-bobbing birds. Ratites constitute a monophyletic group being the head-bobbers
tinamous their nearest living relatives. Rheas were exclusively observed in captivity and it can

not be discarded that these birds, like the closely related ostriches (Sibley & Ahlquist, 1990;
Sibley et al., 1988; van Tuinen, Sibley, & Hedges, 2000), may exhibit head-bobbing in the
natural environment under specific circumstances (Fig. 30 and Appendix C: Table C-2).
Infraclass Neoaves contains parvclasses Galloanserae, Turnicae, Picae, Coraciae, Colidae, and
Passerae. Parvclass Galloanserae (including ducks and fowls) are closer to paleognaths than to
other neognaths. Therefore they constitute and ancient group in birds evolution. All fowls
show very distinctive head-bobbing behaviour, while ducks do not exhibit head-bobbing. Only
one exception was observed in Wood Duck: head-bobbing was video recorded in a bird before
an escaping flight. Unfortunately, further observations could not confirm the data. These head
movements may be an alert signal for other birds. Therefore Wood Duck has been classified as
NB.
Parvclass Turnicae, containing the order Turniciformes and the family Turnicidae,
commonly called button-quails are also head-bobbing birds. Parvclass Picae that includes
woodpeckers, honyeguides, barbets, toucans, jacamars, and puffbirds (Fig. 30 and Appendix C:
Table C-2) are body-bobbing birds. Within the Parvclass Coracidae species from four families
were observed: ground hornbills (NB), typical hornbills (BB), hoopoes (HB), and groundrollers (NB).
The majority of the living birds are classified within the parvclass Passerae and a more detailed
analysis is needed. Superorders Cuculimorphae, Psittacimorphae, Strigimorphae and
Passerimorphae are included in parvclass Passerae. The superorder Cuculimorphae contains
cuckoos and the Hoatzin. All birds in this group are HB, BB, or both, the only exception is the
Great Roadrunner, this bird moves rarely at slow motion. Cuckoos are HB an ancient lineage
with much genetic diversity among the living groups. Unfortunately, data about Hoatzin are
lacking. The species observed within the Psittacimorphae superorder (parrots) were classified
as OHM, but more detailed observations are needed. However, casual observations revealed
that some species hop while others walk without head-bobbing. For example, recent
observations showed that Kea (Nestor notabilis) walk without head-bobbing.
Class Aves
Subclass Neornithes
Infraclass Eoaves , HB* (unless Rhea NB)
Infraclass Neoaves
Parvclass Galloanserae
Superorder Gallomorphae HB
Superorder Anserimorphae NB
Parvclass Turnicae HB
Parvclass Picae BB
Parvclass Coraciae
Superorder Bucerotimorphae
Order Bucerotiformes:
Family Bucerotidae BB
Family Bucorvidae NB
Order Upupiformes HB
Superorder Coraciimorphae
Order Coraciiformes NB
Order Coliiformes BB
Parvclass Colidae BB
Parvclass Passerae
Superorder Cuculimorphae HB, BB, HB& BB (unless roadrunners NB)
Superorder Psittacimorphae OHM
Superorder Strigimorphae
Order Musophagiformes HB&BB
Order Strigiformes OHM
Superorder Passerimorphae HB
Order Columbiformes HB
Order Gruiformes HB (unless kagus NB)
Order Ciconiiformes
Suborder Charadrii HB (unless thick-knees and Laoroidea superfamily NB)
Suborder Ciconii
Infraorder Falconides NB (unless Secretarybird HB)
Infraorder Ciconiides
Parvorder Podicipedida: HB
Parvorder Sulida: NB
Parvorder Ciconiida
Superfamily Ardeoidea HB
Superfamily Scopoidea HB
Superfamily Phoenicopteroidea NB
Superfamily Threskiornithoidea
Superfamily Pelecanoidea NB
Superfamily Ciconioidea
Family Ciconiidae
Subfamily Cathartinae NB
Subfamily Ciconiinae HB
Superfamily Procellarioidea NB
Order Passeriformes HB, BB, HB&BB
Figure 10: Short summary of the motion birds list following Sibley and Ahlquists (1990) taxonomy. When a
group is classified in a bobbing category, all subgroups contained in it are included in this category.
Superorder Strigimorphae includes Turacos (order Musophagiformes) and owls (order

Strigiformes). Turacos were traditionally classified as being related with cuckoos (superorder
Cuculimorphae), although DNA comparisons found that they are not one anothers closest
living relatives (See references and discussion in Sibley & Ahlquist, 1990). Turacos, like some
cuckoos, hop and bob their heads. It is well known that owls perform side-to-side head
movements that serve as a depth cue for motion parallax (van der Willigen et al., 2002). It was
not possible to observe the motion of other nocturnal birds like nightjars, nighthawks, oilbirds,
and frogmouths that also belong to the order Strigiformes.
Superorder Passerimorphae is divided in four orders: Columbiformes, Gruiformes,
Ciconiiformes, and Passeriformes. After observing 24 species within the Columbiformes order,
no exceptions were observed. All pigeons and doves are head-bobbing birds. The
Columbiformes family is a monophyletic taxon with no close living relatives.
The order Gruiformes (parvclass Passerae) is a highly divergent monophyletic taxon including
cranes, sunbitterns, bustards, limpkins, sungrebes, trumpeters, kagu, rails, and mesites. All
birds observed within this order are head-bobbing birds except kagu (family Rhynochetidae).
In semi-captivity, those birds run very fast from one side to another, never walking in slow
motion. Seriemas are closely related with kagus. Initially the seriemas were classified as non
head-bobbing birds, but further observations revealed short periods of head-bobbing, so they
were reclassified as HB*.
The order ciconiiformes is divided in suborders Charadrii and Ciconii. The Charadrii, with 366
species, is one of the largest avian suborders. It contains two infraorders: Pteroclides and
Charadriides. In addition, Charadriides infraorder is divided into Scolopacida and Charadriida
parvoorders. Infraorders Pteroclides (sandgrouse) and Parvoorder Scolapacida (seedsnipe,
woodcocks, snipes, curlews, pharalopes, etc) exclusively contain head-bobbing birds. Within
the Charadriida parvorder HB and NB have been observed. NB birds are observed in
Burhinidae (thick-knees), Glareolidae (Crab Plover and pantrincoles), Laridae (gulls and
allies), whereas occasional HB birds are observed in Charadriidae family (plovers, lapwings,

etc) (Appendix C: Table C-2). Phylogeny of suborder Charadrii has been broadly investigated
by using different methods which resulted into different phylogenetic trees (Chu, 1995; Ericson
et al., 2003; Sibley & Ahlquist, 1990). It constitutes an example in which head-bobbing can be
used as a characteristic that may help to clarify the phylogenetic tree of suborder Charadrii.
Ciconii suborder is a very eclectic group in terms of their motion styles: NB, HB, BB, and
OHM species have been observed within this group. Ciconii suborder is divided between
infraorders Falconides and Ciconiides. Species within infraorder Falconides (hawks, eagles,
vultures, etc), except for Secretary bird, do not show head-bobbing. Infraorders ciconiides
contains Podicipedida, Phaethontida, Sulida, and Ciconiiida parvorders. The grebes linage
(parvorder Podicipedida) classified as HB birds, branched earlier from the common ancestor in
the ciconiides and have no close living relatives. In Phaethontida parvorder, no convincing data
were collected, although a short video of a Red-tailed Tropic Bird (Phaeton rubricauda) from
Internet Bird Collection (Lynx Editions, 2005) show one of those animals hopping. Bobbies
and gannets belonging to the family Sulidae and cormorants belonging to Phalacrocoracoidae
family (parvorder sulida), are classified as non-bobbing birds. Anhingidae, the sister family of
Sulidae and Phalacrocoracoidae families, is integrated by anhingas and darters. As in
Phaethontida parvorder, clear data are lacking, but a very short internet bird collection video
(Lynx Editions, 2005) show one anhinga doing head-bobbing while emerging from the water.
Cormorants are classified as non-bobbing birds.
Herons, hammerkop, storks, ibises, flamingos, pelicans, albatrosses, petrels and allies have
been traditionally included in the Cinoniida parvorder. Pelicans (superfamily Pelecanidae),
flamingos (superfamily Phoenicopteridae), albatrosses, petrels, shearwaters, diving-petrels,
penguins, loons and frigatebirds (superfamily Procellarioidea) are non-bobbing birds.
Hammerkop (superfamily Scopoidea), herons and egrets (superfamily Ardeoidea) are HB
birds. Morphological similarities and DNA that New World vultures (family Catthartinae) and
storks (family Ciconiinae) are closely related, they have been included within superfamily
Ciconiidea. New world vultures are NB birds, while all storks except for the Marabou
(Leptoptilos crumeniferus) are HB birds.

The Passeriformes order contains around 5500 of the 10000 species classified within Clements
checklist (Clements, 2000, 2004 updated version). Data about 86 species covering 25 families
were collected. Further observations are required to obtain representative data. However, the
preliminary observations found that suborder Tyranniy (suboscines) contains HB and BB birds.
Similarly, the suborder Passeri (oscines) contains HB, BB and HB&BB birds. Most
Passeriformes are small, land-dwelling birds that feed primarily on insects, seeds, fruit, or
nectar. The Passeriformes diverged from the non-passeride clade composed of the
columbiformes, gruiformes and ciconiiformes birds. Columbirformes and gruiformes are
mainly HB birds, whereas ciconiiformes is a miscellaneous group where HB, NB and BB
species have been observed.
5.2.3 Analysis of behavioural and ecological factors under head-bobbing

Around 72% of the HB birds feed on seeds, fruits, small invertebrates, insects, etc., 18% feed
on fish, squids, and crustaceans, and 10% feed on small vertebrates, reptiles, and frogs. In
comparison, 35% of NB birds feed on seeds, fruits, small invertebrates, insects, etc., 36% feed
on fish, squids, and crustaceans, 21% feed on small vertebrates, reptiles, and frogs, 14% on
carrion, and 4 on tiny molluscs (Fig. 31 and Appendix C: Table C-3). Although it is
controversial to assume that the feeding source is rated according to the size, a Spearman
correlation revealed a significant negative correlation between head-bobbing and food size (r
=-.38, n=67, p<0.001). Head-bobbing birds prefer small sized food in comparison to nonbobbing birds that choose bigger sources of feeding.
The analysis of the feeding methods revealed that 78% of the head-bobbing birds look for food
by foraging or wading, 10% stalking and spearing, and the remaining 12% were divided
equally between diving, collecting in bushes and trees, digging, and hunting or searching from
the air. In contrast, 33% of the non-bobbing birds look for food foraging or wading, 25%
diving in water, 26% hunting or searching from air, 7% filtering, and the remaining 8% are
divided equally between stalking or spearing, and digging or scooping (Fig. 31 and Appendix
C: Table C-3). The group size analysis revealed that 36%, 31%, and 33% of HB birds live in

solitary, small groups, and in groups, respectively. While 46%, 25%, and 29% of NB birds live
in solitary, small groups, and groups, respectively (Fig. 31 and Appendix C: Table C-3).
All head-bobbing birds were diurnal birds. All NB birds were diurnal except one (Stone
curlew). Around 38% of the HB birds live in the savannah and other open woodlands, 38% live
in swamps, muddy shores, and marshes, 21% live in forests, and only 3% live on lakes and
rivers. 32% of NB birds live in the savannah and other open woodlands, 20% live in forests,
16% live on swamps, muddy shores and marshes, and 32% lives in sees, oceans, and coastal
areas (Fig. 31).
It was found that 46% of the HB birds have poor flying abilities (short distances, awkward),
26% are normal flyers, 18% are elegant and skilled, and 10% do not fly (terrestrial). In
comparison, 21% of the NB birds are awkward or fly short distances, 24% are normal flyers,
48% are elegant and skilled flyers, and 7% (penguins) do not fly (Fig. 31). Head-bobbing birds
are less skilled in flying than non head-bobbing birds. A negative correlation, between headbobbing and flying abilities, was found (r = -.312, n=67, p< 0.01).
NB birds: feeding
HB birds: feeding
3%
14%
18%
3%
24%
10%
21%
72%
35%
1 Fruits, leaves, seeds, small vertebrates, invertebrates, insects, etc.

2 Fishes, squids, crustaceans
3 Small vertebrates, reptiles, frogs
0 Molluscs
1 Fruits, leaves, seeds, small vertebrates, invertebrates, insects, etc.
2 Fishes, squids, crustaceans
3 Small vertebrates, reptiles, frogs
4 Vertebrates
5 Carrion
HB birds: feeding method

10%
3%
NB birds: feeding method
3%
4%
7%
3%
3%
33%
26%
78%
1 Foraging and wading
2 Collecting in trees and bushes
3 Diving in water
4 Stalking and spearing
5 Hunting, searching fron the air
6 Digging or scooping
4%
26%
1 Foraging and wading
3 Diving in water
4 Stalking and spearing
5 Hunting or searching fron the air
6 Digging or scooping
7 Filtering

HB birds: group size
HB birds: group size
33%
36%
33%
31%
0 Solitary or pairs
36%
31%
0 Solitary or pairs
1 Small groups (2-10)
1 Small groups (2-10)
2 Groups
2 Groups
HB birds: habitat
NB birds: habitat
3%
38%
38%
31%
31%
4%
21%
19%
15%
1 Savannah and other open woodlands

2 Forest
3 Swamps, marshes, and muddy shores
4 Lakes and rivers
1 Savannah and other open woodlands

2 Forest
3 Swamps, marshes, and muddy shores
4 Lakes and rivers
5 Seas, oceans, and coastal areas
NB birds: flying abilities
HB birds: flying abilities
7%
10%
18%
21%
48%
26%
46%
24%
0 Terrestrial
1 Short distances, awkward
2 Normal flyer
3 Elegant and skilled
0 Terrestrial
1 Short distances, aukward
2 Normal flyer
3 Elegant and skilled
HB birds: predator pressure
HB birds: predator pressure
4%
13%
30%
9%
67%
57%
0 Low
1 Medium
2 High
0 Low
1 Medium
2 High
Figure 31: The following ecological and behavioural characteristics of HB and NB birds were analysed: feeding
source, feeding method, group size, habitat, flying abilities, and predator pressure.
In HB birds, the predator pressure was low, medium, and high in 30%, 57%, and 13% of the
birds, respectively. In NB birds, the predator pressure was low, medium, and high in 67%,
29%, and 4%, respectively (Fig. 31 and Appendix C: Table C-3). A positive correlation
between head-bobbing and predator pressure was observed (r = .391, n=67, p< 0.001). Headbobbing birds are more likely to suffer a higher predator pressure than non head-bobbing birds.
Only six species of BB birds were analysed, therefore the sample may not be representative,
and further analysis would be needed. The analysed BB feed on fruit, leaves, invertebrate,
small vertebrate, etc. (45%). They also eat fishes, squids, and crustaceous (22%), small
vertebrates, and reptiles (33%). They are diurnal birds that collect food mainly in trees and
bushes (66%), foraging and wading (17%), and diving in water (17%). They prefer forests and
bushes to live (66%), but 34% of them are divided equally between open lands and marine
habitats. They live normally in solitary (67%) or in small groups (33%). They are generally
normal flyers (55%), or skilled (33%). The observed predator pressure was low in all species.
5.3 Discussion
A list of 322 species of head-bobbing, body-bobbing and non-bobbing birds was elaborated.
Approximately 80% of the orders and almost half of the families on all continents of the world
were represented in the list. Head-bobbing was found in 15 of the 26 orders analysed and in
163 species of birds. Almost half of the species observed were head-bobbing birds, 25% were
body-bobbing birds, and the remaining birds were non-bobbing birds. In addition, a small
percentage of birds (2%) were observed performing other-head-movements.
Previous reports found HB in 8 orders and in 28 of the 48 analysed species (Dagg, 1977b).
Until now, the occurrence of head-bobbing in birds may have been underestimated due to the
lack of data, but also because careful observations are needed to detect head-bobbing in species
that display it only occasionally. Around half of the living birds may be capable of doing
head-bobbing. The other half may be equally divided between NB birds and BB birds. The real

proportion of NB birds is probably even smaller because Passeriformes were under represented
in our sample The order Passeriformes includes around half of the living birds, and all of them
were either HB or BB birds.
The lack of data in Caprimulgiformes, Apodiformes, Dinornithiformes, Trochiliformes,
Trogoniformes, and Opisthocomiformes orders barely affect these estimations. On the one
hand, these orders contain few species of birds and on the other hand, predictions of the
locomotive behaviour of these birds can be made. Oilbirds, nightjars, frogmouths, and allies
(Caprimugiformes) are nocturnal birds which form a monophyletic group with owls, swifts and
hummingbirds (Trochiliformes) (Sibley & Ahlquist, 1990). All these groups are probably
integrated by NB nocturnal birds. In addition, Apodiformes and Trochiliformes are mainly
aerial species, which may not have head-bobbing. In this study it has been observed that HB
occurs more often in terrestrial species. Dinortithiformes (kiwis) are most probably headbobbing birds that together with cassowaries and the Emu form a monophyletic group,
although it may well occur that HB appears rarely in kiwis due to their nocturnal habits.
Trogons and Hoatzin are arboreal species, which may prefer hopping for moving between
branches and bushes, although HB behaviour cannot be discarded.
5.3.1 List of Head-bobbing and non-bobbing birds: exceptions within a family

Around 90% of families share the same bobbing style. In other words, if HB is observed within
a family, most probably all other members of the family are also HB birds. Approximately 7%
of the birds alternated between HB and BB, which, as discussed in section 5.3.3, may have
similar roles. Clear exceptions were found in three families Cuculidae, Charadriidae, and
Ciconiidae. These tree families were consisted only by HB birds except for one species.
Exceptions in non-bobbing families were not found. In addition the non-bobber Stone curlew
(Burhinus oedicnemus), and the head-bobber Secretary bird (Sagittarius serpentarius), were
considered in our analysis as exceptions, because all closed relatives of these species are nonbobbing birds. In this section, the selection pressures that may lead to an exception in closely
related birds are discussed.
The Greater roadrunner is the only specie observed within the Cuculidae family that shows
neither HB nor BB. It is a large, long-legged, long-tailed cuckoo that spends most of the time
on the ground. Roadrunners are capable of sprinting up to 25 km an hour and rarely seem to
walk slowly. The high speed during locomotion may explain the lack of head-bobbing. It has
been observed that at high speed head-bobbing is suppressed in pigeons (Davies & Green,
1988) and field observations in many other species have also confirmed that head-bobbing is
suppressed at high speeds (Dagg, 1977b).
The Southern lapwing (Vanellus Chilensis) is the only bird within the Vanellus genus
(Charadriidae family) that walks without head-bobbing. In other lapwings, head-bobbing while
walking is observed in marshes and other wet lands. Video recordings of the Southern lapwing
were done exclusively in grass areas. Therefore, further observations in marshes and wet lands
are needed to determinate whether the Southern lapwing is a HB bird.
All ciconiidaes, except Marabou, were observed walking with head-bobbing. The Marabou is
the only stork that feeds on carrion. The Marabou behaviour was observed during long periods
of time in natural conditions. When the animal was feeding from big carcasses no traces of
head-bobbing were found. Although in a very specific situation a flock of marabous showed
traces of head-bobbing. The birds were occupied in searching small peaces of carrion left by
the crocodiles, dragged by the water in a river, during migration time in Tanzania.
Unfortunately, it was not possible to record clear footage of the birds. For this reason the birds
were classified as NB birds. The feeding habitats and the life style of marabous may not
require head-bobbing, but that might occur under certain circumstances. During head-bobbing
walking, the necks of the marabous were extended, whereas during non head-bobbing walking
the necks were shrunk, which may be related to the lack of head-bobbing.
The Stone Curlew (Burhinus oedicnemus), an integrant of the Burhinidae family, is a bird
closely related with Charadriinae subfamily. It is active at night, and its large yellow eyes
enable it to locate food when it is dark. On the one hand it cannot be dismissed that Stone
Curlew may exhibit HB in certain conditions, as the animals were observed during the day and

they were not very active. On the other hand, all observed nocturnal birds did not display headbobbing which leads to the conclusion that most probably head-bobbing is no longer effective
during night. For nocturnal birds like owls having eyes located frontally and receiving a double
signal of the same visual area, may be an advantage which would increase the possibilities of
detecting a target.
The Secretary birds (Sagittarius serpentarius), belonging to the infraorder Falconides is the
only bird of prey capable of performing head-bobbing. It has long legs, it feeds on snakes or
other reptiles, amphibians, tortoises, rats and other small mammals as well as young game
birds. Secretary bird is the only terrestrial bird of prey hunting on the ground at medium or
short distances. Head-bobbing may aid these birds to distinguish preys hidden in the floor.
Assuming that all falconides have a common ancestor, this can be a case of head-bobbing
reinvention.
In conclusion, the study or exceptional cases, regarding the bobbing style in closely related
group of birds, revealed that head-bobbing may be suppressed in birds that move generally at
high speed, in non ground foraging birds, and in nocturnal birds. On the contrary, headbobbing may appear in ground foraging birds.
5.3.2 Rare or occasional head-bobbing behaviour

Ostriches, plovers and lapwings, bustards, crows, starlings, moorhens, coots and grebes display
rare or occasional head-bobbing. In these animals, the analysis of the situation in which headbobbing occurs may contribute to understanding the functional significance of head-bobbing.
Head-bobbing was found in ostriches walking through long grasses in the savannah (Fig. 32),
but not while foraging or in captivity. The predators of Ostrich are Cheetah, Lion, Leopard,
Wild Dog and Spotted Hyena. Adult males have been seen to kick out at, and wound, large
predators. In open lands, ostriches are able to outrun most of their enemies reaching 70 km per
hour in a short sprint in open country, and 50km per hour over a distance of 30km. A

vulnerable situation may occur when crossing long grasses, where a predator can be hidden.
Head-bobbing in ostriches may serve to seek for predators hiding in grasses. It has been
proposed that head-bobbing serves for pattern recognition and for distinguishing between own
and external motion (Davies & Green, 1988; Frost, 1978). By stabilizing the retinal image, the
ostriches may be more efficient detecting static and moving predators.
Plovers and lapwings (Charadriidae) showed head-bobbing while walking slowly in tidal
mudflats, and shallow flood pools, but not in open short-grasslands or bare soil. They feed on
insects, worms, spiders, molluscs, and shrimps (Jonsson, 1999).
Many members of the
Charadriidae family were observed performing head-bobbing and also a type of up-and-down
head movement. Those vertical head movements may aid a bird in acquiring visual information
avoiding the distortion caused by the water reflection and refraction (Casperson, 1999).
According to the model proposed by Casperson, the head-bobbing behaviour may not help
much solving this problem, because vertical movements are necessary. Therefore, headbobbing in shallow flood pools may have other functions most probably related with foraging.
Figure 32: A male ostrich walking

in Ngorongoro National Park
(Tanzania). The Ostrich (Struthio
camelus) shows a clear headbobbing while walking in its
natural environment through long
grasses. Head-bobbing was neither
observed during foraging nor in
captivity.
Foraging in mudflats and shallow food pools may require head-bobbing in order to localize
small animals hiding in the mud. Plovers and lapwings walk deliberately slowly, thus rapid
head movements may also help to identify objects lying in the mud at different distances. That
is, by moving the head fast, the relative displacement of a worm on the retina, which is lying
on the surface of the mud, will increase with respect to the relative displacement of the ground
on the retina.

Bustards have been observed bobbing their heads while walking slowly in grass-lands. The
head-bobbing behaviour of bustards is very peculiar because they perform fast and long thrust
phases, intercalated by very brief hold phases. They feed on variety of insects, small mammals,
lizards, snakes, seeds, and berries. The long thrust phase exhibited by bustards may serve for
distance calculations that may allow a better detection of small animals and seeds located in
uniform floors.
Jackdaws, crows and starlings showed head-bobbing in slow motion. In magpies (Pica pica), it
has been observed that running and hopping are alternative gaits at speeds higher than walking.
It is unknown why these birds can walk doing head-bobbing, run, or hop, and why they prefer
hop to run at high speeds. Kinematics studies of the three types of locomotion did not find any
suitable explanation (Verstappen et al., 2000). If hopping is equivalent to head-bobbing and
plays a similar role in visual perception, this may be an explanation why Corvidae birds prefer
hopping over running at high speeds. In addition, hopping may be more efficient for small
birds when moving through trees and bushes.
Other species like moorhens, grebes, and coots also exhibit occasional head-bobbing while
swimming. Head-bobbing was observed while walking (in coots and moorhens), swimming
slowly, when a novel stimulus appears, and while approaching to the shore. Head-bobbing was
not observed while swimming fast, while escaping, or moving towards a clear target like food.
It is not possible to clearly determinate when head-bobbing occur in these birds, but most
probably head-bobbing may facilitate prey detection, distance calculation and image
stabilization. Head-bobbing may be useful to keep a stabilized image of the environment while
the animal is pulled by a water string.
The analyses of the situations in which head-bobbing occurs in HB* birds revealed similar
results to the observation made on section 5.3.2. Head-bobbing occurs at slow motion, when
birds need to distinguish stimuli hidden in a complex background at short or medium distances.
5.3.3 Are body-bobbing birds head-bobbing birds?

It has been suggested that HB and BB may play similar functions from the visual point of view
(Davies and Green, 1988; Friedman, 1975, Davies, 1988 #2125; Frost, 1978 #1141). The data
collected from HB and BB birds support this hypothesis. Both types of locomotion have been
observed in turacos, blackbirds, jays, crows, magpies, weavers, and couas. Furthermore, six
families (Musophagidae, Furnariidae, Turdidae, Sturnidae, Ploceidae, and Fringillidae) and the
entire Passeriformes order alternate between HB and BB. Similarly to head-bobbing, bodybobbing may appear early in evolution. All observed birds within parvclass Picae
(woodpeckers, honeyguides, barbets, etc), one of the oldest avian lineage with living
descendants, are body-bobbing birds (Fig. 30).
Body-bobbing may facilitate the motion of small birds between branches and trees, without
losing the visual advantages of HB. Hopping can be described as having a hold phase, while
the birds stand on the ground, and a thrust face, while the birds are jumping. It may occur that
while foraging the hopping birds have longer period of head stabilization than during normal
locomotion. Frame by frame analysis of hopping sparrows (Passer domesticus) found that
birds head is thrust forward before the legs start to push the body into the air. Furthermore,
the head stops and is stabilized in the visual space before the body finished landing from the
hop. This behaviour is observed in foraging and alert sparrows but not in somnolent ones
(Friedman, 1975). Further analyses of the kinematics characteristics of body-bobbing and
head-bobbing are required to confirm this suggestion.
5.3.4 Are other-head-movements functions similar to head-bobbing functions?

Parrots and owls are not closely related, hence the head-movements found in these groups may
have a completely different origin. To our knowledge few data exists about head-movement in
parrots. Barn owls, with frontally located eyes, perform side to side head-movements that are
classified in the present study as OHM, which similarly to head-bobbing may aid head-

stabilization (Hyde & Knudsen, 2002) and motion parallax calculation (van der Willigen et al.,
2002). Owls may have frontally located eyes as a consequence of their nocturnal activity. For
retrieving parallax information head-bobbing is not longer effective and horizontal movements
are required. On the contrary, the vertical head movements observed in plovers may play
different role from head-bobbing. It has been proposed that these head-movements may aid in
acquiring visual information avoiding the distortion caused by water reflection and refraction
(Casperson, 1999).
5.3.5 Head-bobbing evolution

Two simplified evolutionary scenarios for head-bobbing evolution should be considered. On
the one hand head-bobbing may have evolved at some point in the evolution in a common
ancestor of all birds. On the other hand, similar selection pressures may have resulted into
several evolutions of head-bobbing at different moments in evolution. Probably, a combination
of these two simplified evolutionary scenarios is given in head-bobbing evolution. Headbobbing is a highly distributed trait in the avian phylogeny. Therefore, suppressions and
independent evolutions of head-bobbing may easily have occurred in 130 million years of
avian evolution.
5.3.5.1 Did head-bobbing appear in a common ancestor of the modern birds?

Ratites and tinamous (Eoaves) are traditionally located at the base of the phylogenetic tree of
modern birds (For discussion and references see Sibley, 1990) Morphologic and DNA
sequences analyses tend to support this traditional view (Sibley & Ahlquist, 1990; van Tuinen
et al., 2000), mitochondrial DNA analysis revealed that passeriforms occupy the most basal
position among all modern birds (Harlid, Janke, & Arnason, 1997, 1998). The discussion rests
on whether earlier aves were heavy-bodied, ground-dwelling birds, or arboreal perching birds.
According to our observations, the prototypical head-bobbing bird is terrestrial, with low flying

abilities and ground-foraging that normally does not live in marine habitats (except for tidal
areas).
Independently of these two hypotheses, head-bobbing has been found in both Passeriformes
and Paleonagtae (Eoaves) birds, which are postulated to be the oldest linage of modern birds.
Therefore, head-bobbing may have appeared early in the evolution and it may be a
characteristic inherited from a common ancestor of modern birds. In fact, head-bobbing does
not appear in more recently evolved birds like eagles, hawks, and kites, with frontally located
eyes. During evolution, selective pressures for binocularity may have lead to the loss of the
head-bobbing behaviour.
The relative brain and eye size of birds of prey and nocturnal birds is bigger than in ground
foraging birds. Hunting species, with larger eyes, may need to increase the amount and the
complexity of visual information processing (Garamszegi et al., 2002). Head-bobbing might be
an early solution for solving visual demands, such as pattern recognition, distance calculation,
and vigilance in birds with lateralised eyes.
The two major competing hypotheses on avian evolution are the "basal archosaur hypothesis"
and the "theropod dinosaur hypothesis". The basal archosaur hypothesis proposes that the
first birds descended directly from ancestral reptiles about 230 million years ago. The
"theropod dinosaur hypothesis" proposes that the aves derive from dinosaurs some 130 million
years ago (Shimizu & Karten, 1991). Most birds and reptiles have lateralised eyes (Husband &
Shimizu, 2001). Interestingly head movement behaviour connected with visual processing has
been found in lizards (Flanders, 1985, 1988; LeBas & Marshall, 2000). African chameleon
follows horizontal, sinusoidal cricket (bait) movement with sinusoidal head movement and no
apparent eye movement. The chameleons used head amplitudes that minimized the motion of
the bait relative to the head (Flanders, 1985, 1988). Head-bobbing in Scincid lizard
(Lampropholis guichenoti) serves to enhance visual acuity (Torr & Shine, 1994).
If head-bobbing evolved first in an ancestor of the class aves, it may have been suppressed
several times during evolution. As explained above, the development of binocularity can also

result in head-bobbing suppression. Convergent suppression of head-bobbing can be found in
palmate and totipalmate birds. Those birds constitute a polyphyletic non-bobbing group
belonging to different evolutionary lineages adapted to live in aquatic environments. Headbobbing suppression may be related to the evolution of anatomical adaptations in water birds,
like palmate fingers. Interestingly, grebes, coot and moorhens are good swimmers but lack
palmate fingers. Examples of head-bobbing suppression within a family can be found in Roadrunner adapted to move fast, Marabou adapted to feed on carcass, and Stone curlew adapted to
live during the night (see section 5.3.2).
5.3.5.1 Did head-bobbing evolved as a convergent trait due to similar selection pressure?
Although some evidences suggests the existence of a common ancestor for all head-bobbing
birds, it can not be dismissed that head-bobbing may have evolved independently at different
moments in evolution. Secretary bird is the only falconides with head-bobbing (see section
5.3.2), and assuming that all birds within infraorder Falconides share a non-bobber common
ancestor, this can constitute an example of independent head-bobbing development.
Furthermore, similar selection pressure may lead into a convergent HB behaviour in species
that belong to different evolutionary lineage. It may well happen that HB has evolved at least
10 times in evolutions (see Fig. 30) probably as a consequence of similar feeding habits or
predatory pressure. For example, in gallomorphaes (fowls), columbiformes (pigeons and
doves), ciconiinae (storks), charadrii (lapwings and plovers) which are ground foraging birds,
head-bobbing may have evolved independently as a mechanism to detect small features at
medium to short distances, while monitoring the environment for predators and other relevant
stimuli.
Interestingly, we observed, within a head-bobbing monophyletic family, examples of headbobbing suppressions, but we did not observe, within a non-bobbing monophyletic family,
examples of head-bobbing reinventions.

5.3.5.2 Bobbing style in monophyletic and polyphyletic groups of birds
Interestingly, within the aves, generally monophyletic groups share the same bobbing style,
while polyphyletic groups may not share the same motion style. With very few exceptions,
birds descended from a single ancestor share the same bobbing style; while birds descended
from different ancestors many not.
Monophyletic groups
Columbiformes and Gruiformes orders are monophyletic taxon containing HB birds. The
exception is the Kagu (Gruiformes order), a bird that always moves at high speed. Headbobbing may not be functional at high speeds (Davies & Green, 1988). Further observations
are needed to determinate whether kagus show occasional head-bobbing like seriemas (a sister
group of kagu). Gruiformes order is a highly divergent monophyletic taxon. The Kagu case can
be an example of head-bobbing suppression in evolution.
All fowls (Gallomorphae) show very distinctive head-bobbing behaviour, while waterfowls
(Anserimorphae) do not exhibit head-bobbing. These two closely related sister groups are both
monophyletic taxa that belong to the parvclass Galloanserae (Sibley & Ahlquist, 1990). Fowls
are ground foraging, whereas waterfowls seem to be adapted to feed in the water. Some ducks
are broad-billed and sieve water or mud to extract the small crustaceans or vegetable particles,
other ducks dive in water, geese and swans eat aquatic vegetation and grain (Jonsson, 1999;
Perrins, 1991). The feeding habits of the waterfowls, together with a common ancestor, can
explain the lack of head-bobbing in anserimorphes, this is an example of divergent evolution.
Furthermore, the lack of head-bobbing in waterfowls may be an example of head-bobbing
suppression in waterfowls or independent evolution of head-bobbing in fowls.
Polyphyletic groups
Within the Parvclass Coracidae species the following families were observed: Ground
Hornbills (NB), Typical hornbills (BB), Hoopoes (HB), and Ground-Rollers (NB). Many gaps

exist in the phylogeny of Parvclass Coracidae (Sibley & Ahlquist, 1990) which may be a
polygenetic group of birds. These may explain the different motion patterns observed within
Coracidae Parvclass.
Cuculiformes family is an ancient lineage with substantial genetic diversity among the living
groups, turacos may be the nearest living relative. That may explain why cuckoos and turacos
alternate between HB, BB, or both. The only exception is the Greater Roadrunner, a bird which
is never observed walking at slow motion. HB and BB behaviour appear often associated in
closely related birds.
Traditionally, the former Ciconiiformes order was divided into two orders: Ciconiiformes and
Pelecaniformes (Sibley & Ahlquist, 1990). Herons, storks, ibises, and allies which were
classified as Ciconiiformes, are head-bobbing birds. The former Pelecaniformes order
contained totipalmate birds like pelicans, boobies, gannets, cormorants, anhingas, frigate birds,
and tropicbirds. Apart from the non conclusive observations in anhinga, all totipalmate birds
(all four toes connected by a web) are NB birds. The traditional order Pelacaniformes is
polyphyletic and it may present the most complex and controversial group in the avian
phylogeny. It is possible that some shared characters of these birds have evolved more than
once, while other may have been lost during evolution (Sibley & Ahlquist, 1990). This may be
an example of a polyphyletic group that due to the selection pressure was lead into a
convergent evolution. Palmate and totipalmate birds adapted to live in aquatic environments
are non-bobbing birds (see section 5.3.4.1).
5.3.5.3 Systematic relationship among suborder Charadrii taking in account the bobbing style
The phylogeny of Charadriides (order Ciconiiformes) is very controversial. Morphological data
(Chu, 1995), DNA-DNA hybridization methods (Sibley & Ahlquist, 1990), and DNA sequence
data (Ericson et al., 2003) analyses resulted in different phylogenetic trees. The morphologic
and DNA-DNA hybridization analyses define 2 main groups of birds: on the one hand Laridea,
Charadriodea and Chionidoidea, on the other hand Scolopacoidea and Jacanoidea (Fig. 33). In

addition DNA-DNA hybridization divides the first group into two subgroups Laroidea and
Charadrioidea plus Chionidoidea. Nuclear DNA sequence also defines two main divisions, but
associate Laridea with Scolopacoidea plus Jacanoidea as sister groups, while Charadrioidea
plus Chionidoidea form an independent group.
The observation data on head-bobbing behaviour were feed onto the phylogenetic trees (Fig.
33). Three groups are defined: HB, HB* (rare or occasional head-bobbing) and NB birds. Nonbobbing species may be more closely related to species that show rare or occasional headbobbing than to head-bobbing species. Therefore, the head-bobbing data are more concordant
with the DNA-DNA hybridization phylogeny. In addition, DNA-DNA hybridization may
support the observations made on Stone Curlew (Burthinidae family), classified as a nonbobbing bird. However, it can not be excluded that future observations reveal occasional or
rare head-bobbing. Given that normally monophyletic groups share the same bobbing style,
knowledge about the motion style may help to clarify the systematic relationship between
groups of birds.
NB
NB
NB
NB
HB
HB*
HB
HB*
HB*
HB
HB*
HB*
HB*
HB*
HB
NB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
NB
NB
NB
NB
NB
NB
NB
NB
NB
NB
NB
HB
HB
HB
HB
HB
HB
HB
HB*
HB*
HB*
HB*
NB
HB
Figure 33: Systematic relationships among major groups of charadrii birds based on:
A) Parsimony analyses of morphological data set (Chu, 1995).
B) Analyses of DNA-DNA hybridization data (Sibley & Ahlquist, 1990).
C) Nuclear analyses of DNA sequence data (Ericson, Envall, Irestedt, & Norman, 2003)
Each phylogenetic tree was complemented with the observed bobbing information. Each taxa was
classified as head-bobbing (HB), occasional head-bobbing (HB*), or non-bobbing bird (NB).
5.3.6 Ecological and behavioural factors under head-bobbing, body-bobbing and nonbobbing
The analysis of the ecological and behavioural factors under head-bobbing revealed that the
prototypical head-bobbing bird is a ground-foraging bird, that feeds on seeds, small fruits,
insects, small vertebrates, worms, and other small prey. It has low flying ability, prefers open
woodlands, shores, and muddy areas to live, but is never observed in open oceans and seas. It
can live either in solitary, in small or big groups. The predator pressure is normally medium.
Non-bobbing birds feed on a variety of sources, like molluscs, fruits, seeds, fish, squids,
vertebrates, and carrion and they have very variable feeding habits, from foraging to hunting.
They are distributed in all kinds of habitats from open lands to oceans. They are normal or
good flyers and they can live in solitary, small or big groups. The predator pressure is generally
low; often they are predators themselves.
The main differences between these prototypes of birds are the feeding source, feeding habits,
flying abilities, and the predator pressure. Head-bobbing may have a double function, pattern
discrimination at short to medium distances and predator detection. Head-bobbing may aid the
detection of small stationary features such as seeds, or larger moving objects, such as
predators, against textured background (Wohlschlger et al., 1993). Searching for food on the
ground may increase the predator vulnerability of those birds. Furthermore, except for
migrating birds, high flying abilities are not required.
Further analyses in body-bobbing birds are needed, but observations on 6 species of birds
revealed that they feed on fruit, leaves, invertebrates, small vertebrates, etc. They are skilled
and normal flyers with low predator pressure and prefer living in bushes and trees, in solitary
or small groups. Furthermore, small birds like most of the Passeriformes, living in bushes and
trees, have short legs and tend to hop rather than walk (Friedman, 1975).

Head-bobbing birds may have lateralised eyes with big cyclopean fields in order to monitor
predators. It has been found that the Ostrich, the Cattle egret, the Rock pigeons, the Eurasian
Woodcock and three types of herons have binocular visual fields smaller than 22 and a
cyclopean visual field bigger than 290. Head-bobbing was not observed in birds with large
binocular visual field and small cyclopean visual field. In comparison, non-bobbing birds
visual field is very variable. There are birds with narrow binocular field and large cyclopean
field like Mallard, and birds with large binocular field and small cyclopean visual field like
Tawny owl. Mallard (Anas platyrhinchos), which have very narrow monocular field (5) and
large cyclopean field (360), like other ducks, search for food by sieving the water. Ducks may
require a large cyclopean field for searching for predators, but they do not need any
mechanism, like head-bobbing, to identify small targets at short to medium distances. Tawny
owl (Strix aluco) have a wide binocular fields (48) and smaller cyclopean fields (210) (Martin
et al., 2001; Martin & Coetzee, 2004; Martin & Katzir, 1993, 1994, 1995, 1999, 2000).
5.3.7 Interim Summary

Half of the modern birds may be head-bobbing birds, while the rest of the birds are equally
divided between body-bobbing and non-bobbing birds. Head-bobbing and body-bobbing
behaviours appear together in many families. They could be equivalent or related behaviours
playing similar roles. Generally, all species within a family share the same bobbing
behaviour. Detailed analyses of exceptions may provide useful data to understand the
functional significance of head-bobbing. On the one hand, head-bobbing may be a
characteristic inherited from a common ancestor of modern birds. During evolution, different
selective pressures may have caused a loss of the head-bobbing behaviour. On the other hand,
head-bobbing is a highly distributed trait in the avian phylogeny. Therefore, suppressions, and
independent evolution of head-bobbing may easily have occurred during evolution.
Comparisons between different phylogenetic trees revealed that birds closely related have the
same bobbing behaviour. Furthermore, monophyletic groups normally share the same bobbing
style, while polyphyletic groups may show different bobbing styles. Head-bobbing birds are
normally ground foraging birds seeking for small feeding sources like insects, grains, worms,

etc. They are bad to normal flyers with medium predator pressure and prefer to live in open
woodlands, marshes, and muddy areas. In addition, they may have lateralised eyes with narrow
binocular fields and large cyclopean fields. Non-bobbing birds have less remarkable
characteristics. They are good flyers, have low predator pressure, are highly distributed, and
feed on a variety of food. Head-bobbing may be an earlier mechanism to solve visual demands,
like food and predator detection. As soon as the visual demands are not present, or more
efficient mechanisms appear, head-bobbing may decrease or be suppressed. Complex feeding
habits may require more sophisticated and efficient visual mechanism like binocularity, which
may replace head-bobbing.
General Discussion 117

6. GENERAL DISCUSSION
The flying ability together with the feeding behaviours and predator monitoring are probably
among the greatest challenges for the avian visual system. Birds may need to solve different
visual demands leading to different visual specialisations. Most birds have lateralised eyes,
with a narrow binocular field and a broad monocular field (Martin, 1993; Martin & Katzir,
1999; Shimizu & Karten, 1993). Approximately half of the living birds are head-bobbing birds
and it is well known that head-bobbing is visually controlled (Friedman, 1975b; Frost,
Cavanagh, & Morgan, 1988). It may be a monocular mechanism to solve visual environmental
demands in birds with lateralised eyes.
6.1 Intraocular and interocular transfer of information
The pigeon retina is divided into the dorso-temporal binocular red field and the remaining
monocular yellow field. Two independent systems process the visual information in pigeons.
The entire retina projects to the contralateral optic tectum and continues via the diencephalic
nucleus rotundus to the entopallium (tectofugal pathway). The monocular area projects to the
contralateral geniculate thalamic nucleus and continues to the wulst (thalamofugal pathway).
The first part of this work investigated how information retrieved from both eyes and in
different retinal areas is generalised in the brain of walking pigeons. Intraocular transfer of
information between the frontal red field and the lateral yellow field was tested in both
directions: from frontal to lateral and vice-versa. Interocular transfer of information between
the yellow visual fields of both eyes was also tested. The second part of the work examined the
role of head-bobbing in pattern discrimination in walking pigeons by presenting the stimuli
either during the hold or the thrust phase. The third part elaborated a list of head-bobbing and
non head-bobbing birds. It investigated the development of head-bobbing in the evolution, as
well as the ecological and behavioural characteristics of head-bobbing and its functional
significance.

6.1.1 Intraocular transfer of information
In the first experiment it was found that pigeons are able to learn a pattern discrimination task
in the lateral visual field by shifting the stimulus presentation from frontal to lateral positions
in consecutive steps. Previous studies showed that pigeons are capable of pattern
discrimination and stimulus detection in the lateral visual field (Bloch & Martinoya, 1982b;
Goodale & Graves, 1982; Mallin & Delius, 1983; Remy & Emmerton, 1991b; Roberts et al.,
1996). However, the only precedent using a similar methodology in freely walking pigeons,
moving the stimulus presentation in consecutive steps from frontal to lateral direction, failed to
train the birds (Nye, 1973). An impressive amount of training to learn the task was required in
the current experiment. The increase of the distance between the pecking key and the stimulus
presentation can constitute a handicap, increasing the difficulty of the task (Mallin & Delius,
1983).
A dramatic decrease of performance to chance level was found at 45, by moving the stimulus
presentation from the frontal to the lateral visual field. In addition, at 45 pigeons needed twice
the amount of trials than in other positions to achieve a criterion of 70% of correct responses in
four consecutive sessions. During the experiment, the stimulus presentation occurred right after
the pigeon crossed a light barrier situated at 118 cm to the stimulus. The frontal binocular field
of the pigeon in the horizontal plane has a maximum extension of 27 (Martin & Young, 1983).
The edge of the frontal binocular field, when the observation point is set at 118 cm in the
centre of the arena, corresponds to a stimulus located at 40 in the experimental arena. A 5x5
cm stimulus presented at 45 in the experimental arena falls entirely within the lateral visual
field (Fig. 13). Therefore at 45 the pigeons may switch from processing the stimuli with the
tectofugal to the thalamofugal pathway. Information transfer between the frontal and the lateral
visual field was not found in freely walking pigeons. The finding confirm previous
investigations in head-fixed and non walking pigeons (Mallin & Delius, 1983; Nye, 1973;
Remy & Watanabe, 1993; Roberts et al., 1996).

The pigeons were also tested in the lateral-frontal direction. Three of the birds were tested in
the initially naive visual field (see section 3.2), by moving the stimulus location from the
lateral to the frontal visual field in ten consecutive steps. Three other pigeons that did not learn
the task in the opposite visual field of the initially trained one were exclusively tested in the
frontal visual field (0). It should be considered that the initial training in the frontal visual field
took place at least one year earlier. Contradictory results were found: on the one hand fewer
amounts of trials were needed in the lateral-frontal direction than in the frontal-lateral
direction. In contrast, no differences were found in the performance of the pigeons in the first
20 trials at each position between the frontal to lateral direction and vice versa. On the other
hand the pigeons exclusively tested at 0, having previous experience in the frontal visual field,
did not remember the task and did not transferred information. They needed almost the same
amount of trials to relearn the task as in the initial learning.
Taking all data together, probably no transfer or very poor transfer of information occurred
from the lateral to the frontal visual field. Similarly, a poor intraocular transfer from lateral to
frontal position was observed in a colour discrimination task (Mallin & Delius, 1983).
However, other studies found intraocular transfer of information, from lateral to frontal
position (Remy & Emmerton, 1991b; Roberts et al., 1996). Intraocular transfer of information
from the lateral to the frontal visual field may be task dependent. Intraocular transfer was very
poor or not observed in tasks with a more clear memory component, like colour discrimination
(Mallin & Delius, 1983) and pattern discrimination. In contrast, intraocular transfer was
observed in tasks without a clear memory component, like stimulus detection (Remy &
Emmerton, 1991b) and matching to sample (Roberts et al., 1996). In natural conditions, the
information received within the yellow field system may be transferred to the red visual field
system in order to switch attention to interesting or important environmental stimuli, whereas
transfer of memory from the frontal to the lateral visual field may not be needed. Projections
from the visual wulst (thalamofugal pathway) into the optic tectum (tectofugal pathway) can
mediate this transfer of information (Bagnoli et al., 1980; Karten et al., 1973; Miceli et al.,
1987).

In conclusion, pigeons are not capable of intraocular transfer from the frontal to the lateral
visual field, whereas information transfer from the lateral to the frontal visual field may depend
on the task. Further investigations are required to confirm this last observation.
6.1.2 Interocular transfer of information
Interocular transfer of information between the two yellow fields was investigated. Pigeons
initially trained in the LVF were tested in the RVF, and vice versa. In five of the six pigeons no
traces of interocular transfer of information were observed. Only one pigeon was capable of
performing the task in the untrained visual field. These data do not contradict any of the two
hypothesis explaining interocular transfer: the sensorimotor integration hypothesis
(Watanabe, 1986) and the retinal locus hypothesis (Goodale & Graves, 1982; Levine, 1945b;
Mallin & Delius, 1983). Interestingly, the only pigeon capable of information transfer, showed
in experiment 4 a different motion strategy than the other birds. It was the only bird that
instead of varying the overall motion speed thorough the experiment was varying the headbobbing frequency (see section 4.2.2). It may happen that only relevant information perceived
within the yellow fields that triggers an instantaneous motor response would be transferred.
Right eye/left hemisphere dominance in pattern discrimination presented in the frontal

binocular field has been observed in birds (Gntrkn, 1985, 1997a; Gntrkn & Bohringer,
1987). In contrast, in the intraocular transfer experiment, two animals trained in the right visual
field never learned the task beyond 45. Furthermore, in the interocular transfer experiments
(excluding pigeon 51 that was capable of transfer) after a long lasting training, birds initially
trained in the RVF relearned the task in the LVF, whereas birds initially trained in the LVF
(except the animal capable of information transfer) did not relearn the task in the RVF. A weak
left eye/right hemisphere dominance was observed in a symbolic delayed matching to sample
task in pigeons (Roberts et al., 1996). Other left eye/right hemisphere dominances were
observed in different tasks like predator detection, social recognition in chicks, and novel
stimuli detection (Evans et al., 1993; Rogers, 2000; Vallortigara et al., 2001). It has been
proposed that the left eye/right hemisphere may be dominant in the lateral visual field which is

mainly focused at long distances, whereas the right eye/left hemisphere may be dominant in
binocular vision which is specialised in short distance visual processes (Evans & Evans, 1999;
Evans et al., 1993; Rogers, 2000; Vallortigara et al., 2001). A lateralised brain may allow dual
attention to short distance tasks like feeding (using the right eye/left hemisphere system) and
long distance tasks like vigilance for predators (left eye/right hemisphere system) (Rogers,
2000).
The distance at which a stimulus is observed may not be the only factor for a visual
asymmetry. In fact, there are many evidences indicating that visual asymmetries may be taskdependent (Clayton & Krebs, 1994b; Gntrkn, 1997a; Nottelmann et al., 2002; Tommasi &
Vallortigara, 2001; Vallortigara, 2000; von Fersen & Gntrkn, 1990). Hemispheric
dominance may depend on both the distance at which the information is processed and on the
task itself. Visual demands, like vigilance, which appeared during evolution more often at long
distances, may be processed preferentially with the left monocular field/right hemisphere. In
contrast, other visual demands, like feeding, which during evolution appeared at short
distances, may be processed preferentially with the right binocular field/left hemisphere. If this
is the case, the key for an asymmetry may not be the visual field area were a visual task is
perceived, but the visual field area at which a task has been more often perceived during the
evolution. For example, left eye specialisation was found for spatial distribution of attention in
the frontal visual field (Diekamp et al., 2005). The left eye/right hemisphere may be specialised
in processing easy shapes at long distances, like silhouettes of predators.
Asymmetries in the birds visual system may serve to increase the computational speed of
certain processes by concentrating them into one hemisphere (Gntrkn et al., 2000; Rogers
et al., 2004). To the ecological advantages of being capable to attend to both predators and
feeding sources (Rogers, 2000), the computational advantages of processing information in one
hemisphere should be added. Most probably the asymmetric avian brain is a consequence of
the interaction between the ecological and computational advantages mediated by the
anatomical substrate.

6.2 Pattern recognition during head-bobbing
Around 50% of the birds of the world are head-bobbing birds. By excluding birds with eyes
located frontally, the proportion of head-bobbing birds is increased. Having lateralised eyes
can be a prerequisite for head-bobbing. Head-bobbing may aid pattern recognition, movement
detection and distance perception in birds with lateralised eyes.
A head-bobbing cycle is divided into a hold phase, when the head is stabilized, and a thrust
phase, when the head is moved forward (Davies & Green, 1988; Friedman, 1975b; Frost, 1978;
Troje & Frost, 2000). In addition, during the hold phase, saccadic eye movements have rarely
been observed (Bloch et al., 1987; Pratt, 1982; Wohlschlger et al., 1993). As a consequence, it
is broadly accepted that head-bobbing may aid in pattern recognition by stabilizing the retinal
image. Pattern recognition in pigeons was tested by presenting the shapes used in the previous
experiments during the hold phase, thrust phase and asynchronous. The pigeons were tested in
both lateral visual fields, one lateral visual field, and frontal visual field. Unexpectedly, no
significant differences were found between presenting the stimuli within the thrust or the hold
phase in any stimulus location. The presentation of the stimuli within the thrust phase was
strictly controlled. Therefore, pigeons were capable of pattern recognition during the entire
head-bobbing cycle.
The presented stimuli were easy to detect, in fact they were two 5x5 cm white shapes on a
black background. It is plausible that pigeons may have difficulties to discriminate small
features hidden in a low contrast complex background, like a grain hidden in the yellow grass
of the savannah at close distances. Objects located at long distances are less affected by the
optic flow provoked by the birds motion. In addition, image stabilization could be achieved in
some birds rotating the eyes, although in relation to the skull, birds have large eyes that limit
eye mobility (Martin and Katzir, 1995). The eye mobility of many birds may be enough to
counteract the retina slip at medium to long distances, but the blur of small features near-by
may require the contribution of head-bobbing.

The motions of pigeons during the hold and thrust phase, and during asynchronous
presentations was analysed when the stimuli were presented either in both lateral visual fields
or in the frontal field. For the hold and thrust phase, the duration, the amplitude, and the speed
was calculated for the frontal and for the lateral visual fields presentations. Significant
differences between the motion speeds were found between the frontal and the lateral visual
fields. Two different strategies were observed. The majority of the pigeons varied the overall
speed of the motion by decreasing the duration of the head-bobbing cycle, while keeping
constant the distance. It was observed that an increase of the speed resulted in a reduced hold
phase. This phenomenon has previously been observed in pigeons (Davies & Green, 1988).
Significantly shorter hold phase durations and faster speed were observed in the frontal visual
field with respect to the lateral visual fields.
Interestingly, one bird used a different strategy varying the head-bobbing frequency: it kept
constant the motion speed across the conditions, varying the amplitude and the duration of the
head-bobbing cycles. The amplitude and duration of the head-bobbing cycles were shorter in
the frontal visual field presentations than in the lateral visual field presentations. Although this
strategy only appears in one of the birds, it may be a common strategy of birds. An extreme
example occurs when static pigeons and other birds are found doing head-bobbing while
observing their environment. Variations in the head-bobbing cycle duration independently
from the motion speed can be useful to increase the optic flow, and therefore enhance distance
calculations.
In conclusion, pigeons are capable of recognizing easy features during the thrust phase. The
capability of discriminating relevant stimuli like predators during the entire head-bobbing cycle
may increase the survival rate of animals. Pigeons can modify the head-bobbing speed and
frequency depending on the stimulus location in the visual field. In addition, different visual
inputs may result in different head-bobbing styles.

6.3 Why do birds bob their heads?
In the last study, the ecological and behavioural factors under head-bobbing were investigated,
and the development of head-bobbing in evolution was analysed. Field observation of 322
species of birds was done in their natural environment and/or semi-captivity conditions. It was
found that around half of the living birds may have head-bobbing, around 25% are bodybobbing birds (hopping birds), and the rest are non-bobbing birds. Nocturnal birds and predator
birds are normally non-bobbing birds, whereas birds with more lateralised eyes can be headbobbing birds, non-bobbing birds, or body bobbing birds.
The question about the functional equivalence between body-bobbing birds and head-bobbing
birds remains unsolved. The analysis of the birds collections suggested that in six families and
the entire Passeriformes order, body-bobbing and head-bobbing were alternative behaviours. It
may well happen that body-bobbing have a double function: it may enhance the mobility of
small birds between tree branches and bushes and contribute to visual perception.
Generally, all species of birds belonging to a family share the same bobbing styles. The
analysis of the few observed exceptions revealed that the feeding source, the speed of the
motion, and the peak of activity, may be important factors for head-bobbing. Furthermore, all
species of birds observed within a monophyletic group share the same bobbing style. Headbobbing may help to distinguish monophyletic groups of birds from polyphyletic groups of
birds. Furthermore, the bobbing behaviour can serve as a cue for understanding the systematic
relationship among a group of birds. The analyses of birds with occasional or rare headbobbing pointed out that head-bobbing may serve to distinguish complicated patterns hidden
on the floor. For example, in ostriches head-bobbing may aid to detect a threatening lion in the
long grasses of the savannah, whereas in plovers and lapwings head-bobbing may aid to find
small invertebrates camouflaged in the mud. In addition, head-bobbing may occur to enhance
optic flow in order to calculate distances through motion parallax. For example, bustards have
been observed performing a very peculiar head-bobbing with long thrust phases while walking
very slowly searching for food.

Head-bobbing may have evolved initially in a common ancestor of all living birds. It may
appear early in the evolution as a mechanism to aid visual processing. Most recently evolved
species like birds of prey, are non head-bobbing birds with eyes located frontally. Both reptiles
and birds have lateralised eyes (Husband & Shimizu, 2001) and birds have descended from
reptiles (Shimizu & Karten, 1991). It has been observed that head-movements in lizards and
African chameleon are related to visual processing (Flanders, 1985, 1988; LeBas & Marshall,
2000; Torr & Shine, 1994). However, it cannot be discarded that head-bobbing have evolved
independently several times in evolutions. We found evidences for both suppressions and
independent evolutions of head-bobbing by feeding our observations in Sibley and Ahlquists
taxonomic tree (see section 5.3.5).
The prototype head-bobbing bird feeds on seeds, fruits, and small feeding of sources. It prefers
small sized food over big sized food and seeks for food by wading or ground foraging. It lives
either in woodlands or shallow waters. It can be either an awkward flyer or a normal flyer.
Actually, head-bobbing birds are normally worse flyers than non-bobbing birds. Head-bobbing
birds suffer higher predator pressure than non-bobbing birds. Although it is commonly
accepted that predator pressure is related to the flock size (Alcock, 1997), preferences were
observed between living in solitary, small groups, or flocks neither in head-bobbing nor in nonbobbing birds (Fig. 31 and Appendix C: Table C-3). Non-bobbing birds have very variable
sources and feeding habitats. However, foraging-birds are rarely non-bobbing birds. They are
broadly distributed in different kind of habitats. Non-bobbing birds are generally elegant and
skilled flyers with low predator pressure. As in head-bobbing birds, no preferences in group
size were observed. Further analyses in body-bobbing birds are needed, but the observations
revealed that they feed on fruits, leaves, invertebrates, small vertebrates, etc. They are small
birds that prefer bushes and trees to live. They live normally in solitary or small groups and
they are skilled and normal flyers with low predator pressure.
The ultimate causes of head-bobbing in evolution may be the feeding habits and the predator
pressure. Feeding on small targets, hard to detect lying on the floor may require both accurate
pattern detection and distance calculation. Ground-foraging birds may be more exposed to
predators, therefore a visual mechanism, like head-bobbing, compatible with a large cyclopean

visual field is required. Flying abilities may not be a demand for these ground feeding birds,
although it would develop in migrating birds like pigeons, cranes, and storks.
A prerequisite for head-bobbing behaviour is probably the lateral position of the eyes in the
skull. Birds with lateralised eyes as well as reptiles, have a more developed tectofugal pathway,
whereas predator birds (non-bobbing birds) have a more developed thalamofugal pathway
(Husband & Shimizu, 2001; Karten & Shimizu, 1989; Shimizu & Karten, 1991; Shimizu&
Karten, 1993). The need for complex and fast visual information analyses, as a consequence of
more complex feeding habits could explain the specialisation of the thalamofugal pathway to
the frontal visual field in birds of prey (Gntrkn & Hahmann, 1999). A relationship between
the lack of head-bobbing and the thalamofugal pathway development should be considered.
Although, several examples of non-bobbing species with lateralised eyes were observed. These
birds use methods of feeding that do not require a high visual specialisation. For example,
many species of ducks and flamingos search for food by filtering the water. Head-bobbing may
be an early mechanism for solving visual demands, like detection of small hidden features, as
soon as these demands are absent or are solved in a more efficient way, head-bobbing would
occur rarely or even disappear
6.4 Summary
Intraocular transfer of information was not observed from the frontal visual field to the lateral
visual field. From the lateral to the frontal visual field, information transfer may be taskdependent. These results may be a consequence of two independent visual systems in the
pigeon brain: the tectofugal pathway, receiving information from the entire retina, and the
thalamofugal pathway, processing information from the lateral visual field. Interocular transfer
of information between the two yellow fields was rarely observed. Interocular transfer between
the yellow fields may occur when a relevant visual input for the animal is accompanied by an
instantaneous motor response. Pigeons have difficulties to learn a pattern discrimination task in
the lateral visual field. It may be explained by the distance between the response key and the
stimulus. The right eye/left hemisphere may be specialised in processing stimuli located at

short to medium distances usually perceived within the frontal binocular field, whereas the
left/eye right hemisphere may be specialised in processing far away stimuli usually perceived
within the lateral visual field. Pigeons are capable of pattern discrimination during the thrust
phase of head-bobbing. Being able to discriminate relevant visual information during the entire
head-bobbing cycle may constitute an ecological advantage. The analysis of the head motion
revealed that pigeons walked slower when the stimuli were presented in the lateral visual field
than in the frontal visual field. Increases of the motion speed result into shorter hold phases.
Head-bobbing parameters may change according to the characteristics of the visual target. It
may be a visual mechanism in birds with lateralised eyes that appeared early in evolution to
solve visual demands like feature recognition and distance calculation. Head-bobbing may also
have other visual contributions. Around half of the modern birds are head-bobbing birds, one
fourth of them are body-bobbing birds, and the remaining birds are non-bobbing birds. The
importance of head-bobbing behaviour may be underestimated until now. Head-bobbing has
been observed broadly distributed in the taxonomy of Aves. Head-bobbing may have evolved
first in a common ancestor of the entire class Aves, but several independent evolutions and
suppressions should be considered. Species of birds closely related normally share the same
bobbing style. Ground foraging, low flying abilities and medium to high predator pressure are
correlated with head-bobbing behaviour. The development of stereopsis, nocturnal vision, or a
lack of the necessary visual challenge may be related with a suppression of head-bobbing.
Appendix 128
APPENDIX
A. Intraocular and interocular transfer
Pigeon
251-LVF
259-LVF
512-LVF
988-LVF
51-RVF
321-RVF
333-RVF
347-RVF
Av. Total
Av. LVF
Av. RVF
246-LVF
246-RVF
259-RVF
0
80
75
70
80
90
85
85
85
81,2
76,2
86,2
70
75
90
14
80
95
60
70
75
65
84
90
77,4
76,2
78,5
70
60
52
23
75
95
70
70
70
45
84
84
74,1
77,5
70,8
70
70
65
29
85
75
50
74
60
45
70
75
66,8
71
62,5
90
65
52
36
85
70
55
56
65
55
82
75
67,9
66,5
69,3
85
80
73
41
80
85
65
80
65
55
75
75
72,5
77,5
67,5
60
60
70
45
60
55
65
60
65
65
46
50
58,3
60
56,3
60
50
60
48
75
78
50
75
60
75
56
85
69,2
69,5
69
61
80
65
60
80
78
70
73
75
72,7
71,2
74
76
85
80
70
85
70
85
55
100
78,7
80
77,5
95
85
84
65
85
85
68
73
55
75
79,7
70,2
Table A-1: Percentage of correct responses for each pigeons in the first 20 trials at different positions of
the screen. In blue appears the percentage of correct responses of the pigeons in the last 20 trials or the
initial training. Half of the birds were tested in the left visual field (LVF), whereas the other half was tested
in the right visual field (RVF).
Pigeon
251-LVF
259-LVF
512-LVF
988-LVF
51-RVF
321-RVF
333-RVF
347-RVF
Av. Total
Av. LVF
Av. RVF
246-LVF
246-RVF
259-LVF
14
4
4
5
4
4
5
4
4
4,25
4,25
4,25
8
4
26
23
4
4
4
4
8
10
4
4
5,25
4,00
6,50
4
9
9
29
11
7
5
4
5
25
5
4
8,25
6,75
9,75
9
19
4
36
5
8
10
14
18
5
4
4
8,50
9,25
7,75
4
10
4
41
4
4
14
4
12
10
4
4
7,00
6,50
7,50
6
12
12
45
14
19
11
25
20
8
17
7
15,13
17,25
13,00
30
30
30
48
4
4
10
12
4
4
28
4
8,75
7,50
10,00
61
4
13
5
7
4
4
4
5
5,75
7,25
4,25
76
6
4
4
4
5
4
12
4
5,38
4,50
6,25
95
7
15
7
4
11
14
11
5
8,00
8,25
7,75
Table A-2: Number of sessions needed to achieve the criterion at different positions of the screen (1
session = 20 trials). Half of the birds were tested in the left visual field (LVF), whereas the rest of the birds
were tested in the right visual field (RVF).
Appendix 129
S.Position 14 23 29 36 41 45 48 61 76 95
% of C.R.
14
n.s. .014 .034 n.s. .032 .n.s. n.s. n.s. n.s.
23
n.s.
n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s.
29
.014 n.s.
n.s. n.s. n.s. n.s. n.s. n.s. n.s.
36
.034 n.s. n.s.
n.s. n.s. n.s. n.s. n.s. n.s.
41
n.s. n.s. n.s. n.s.
.046 n.s. n.s. n.s. n.s.
45
.032 n.s. n.s. n.s. .046
n.s. .011 .011 .009
48
n.s. n.s. n.s. n.s. n.s. n.s.
n.s. .009 n.s.
61
n.s. n.s. n.s. n.s. n.s. .011 n.s.
n.s. n.s.
76
n.s. n.s. n.s. n.s. n.s. .011 0.09 n.s.
n.s.
95
n.s. n.s. n.s. n.s. n.s. .009 n.s. n.s. n.s.
Table A-3: Post hoc analysis of the percentage of correct responses for the factor Screen Position.
Statistical test were considered non significant (n.s.) if p>.05
S.Position 14 23
Trials
14
n.s.
23
n.s.
29
n.s. n.s.
36
n.s. n.s.
41
n.s. n.s.
45
.004 .006
48
n.s. n.s.
61
n.s. n.s.
76
n.s. n.s.
95
.011 .018
29
36
41
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
45
48
61
76
95
.004 .n.s. n.s. n.s. .011

.006 n.s. n.s. n.s. .018
n.s. n.s. n.s. n.s. n.s.
n.s.
.009 n.s. n.s. n.s. n.s.
n.s. n.s.
.036 n.s. n.s. n.s. n.s.
n.s. .009 .036
n.s. .005 .004 n.s.
n.s. n.s. n.s. n.s.
n.s. n.s. n.s.
n.s. n.s. n.s. .005 n.s.
n.s. 0.29
n.s. n.s. n.s. .004 n.s. n.s.
n.s
n.s. n.s. n.s. n.s. n.s. .029 n.s.
Table A-4: Post hoc analysis of the number of trials required to achieve the criterion for the factor Screen
Position. Statistical test were considered non significant (n.s.) if p>.05
Appendix 130
100
100
100
100
95
90
90
80
85
82
85
80
70
60
80
78
75
70
85
80
80 80
70
60
60
60
Learning
50
Trained visual field
40
Naive visual field
40
40
30
20
20
10
0
LV
5
F2
1
LV
5
F2
9
LV
8
F9
8
LV
1
F5
F3
RV
21
F3
RV
47
F5
RV
F3
RV
33
Visual field and pigeon
Figure A-5: Percentage of correct responses for each pigeon in 220 learning trials, 10 catch trials in the
trained visual field and 10 catch trials in the naive visual field (Fig. 21A and 21B).
240
200
160
Y distnace (mm)
120
80
40
0
-40 0
100
200
300
400
500
600
-80
-120
-160
-200
-240
X distance (mm)
Table A-6: Sample of pigeon 251 walking trajectory towards the pecking keys when the screen was
located in the frontal visual field at 0. The pecking keys are represented by two isolated blue points. The
red circle represents the point at which the trajectory started to change. The centre of the coordinate system
was located in the middle of the arena at the pecking key level
Appendix 131
240
200
160
Y distance (mm)
120
80
40
0
-40 0
100
200
300
400
500
600
-80
-120
-160
-200
-240
X distance (mm)
Table A-7: Sample of pigeon 251 walking trajectory towards the pecking keys when the screen was
located in the corner at 45. The pecking keys are represented by two isolated blue points. The red circle
represents the point at which the trajectory started to change. The centre of the coordinate system was
located in the middle of the arena at the pecking key level
Appendix 132
B. Pattern recognition during head-bobbing
600
600
500
500
482
469
456
400
400
338
300
300
308
295
250
235
200
200
211
188
187
Std. Dev = 5,21

74
Mean = 9,1
62
N = 1907,00
32
0
2,5
7,5
5,0
12,5
10,0
17,5
15,0
22,5
20,0
Number of frames: hold phase
25,0
Frequency
Frequency
144
100
100
Std. Dev = 4,34

Mean = 10,6
39
0
2,5
7,5
5,0
12,5
10,0
N = 1907,00
17,5
15,0
22,5
20,0
Number of frames: thrust phase
Figure B-1: Distributions used for presenting the stimuli in the random catch trials and during the learning
trials. The temporal resolution of the system is 120 Hz. one frame is equivalent to 8,33 ms. The distribution
for the hold phase had a mean of 78 ms (9,4 frames) and a standard deviation of 47 ms (5,71 frames). The
distribution for the thrust phase had a mean of 88 ms (10.6 frames) and a standard deviation of 36 ms (4,34
frames).
25,0
Appendix 133
Visual field
(Vf)
Pigeon
51
251
259
347
512
Parameter
F (1,29)
Sig.
Duration
66.982
Distance
2.208
Speed
Phase
(Ph)
F(2,58)
Sig.
F (1,29)
.000
.311
.734
.148
1.037
.361
8.530
.007
.175
.840
Duration
24.982
.000
1.492
Distance
42.292
.000
4.970
Speed
1.503
.233
.056
Duration
4.785
.037
.338
Distance
.263
.612
2.615
.082
1849.7
Speed
5.489
.026
2.378
.102
3926.4
Duration
8.190
.008
1.060
.353
1777.1
Distance
.028
.869
.980
.381
3346.6
Speed
28.100
.000
8.063
.001
9528.3
Duration
.001
.981
.155
.856
1728.0
Distance
.921
.346
.040
.960
893.63
Speed
.911
.349
3.809
.029
5302.8
F (1,4)
Sig.
F(2,8)
Sig.
9.654
.036
.058
.944
Duration
All
Presentation
(Pr)
Vf.*Pr.
Sig.
F(2,58)
1083.8
.000
2313.6
.000
3258.8
.000
.236
4714.4
.011
4209.3
.945
.714
Vf.*Ph.
Pr.*Ph.
Vf.*Pr.*Ph.
Sig.
F(1,29)
Sig.
F(2,58)
Sig.
F(2,58)
Sig.
1.222
.302
10.353
.003
1.461
.241
.135
.874
.509
.604
2.774
.107
1.144
.326
.524
.595
.430
.653
1.669
.207
.205
.815
.624
.540
.000
.124
.884
13.271
.001
1.164
.321
2.518
.092
.000
1.036
.363
34.234
.000
5.983
.005
.863
.428
5046.8
.000
.084
.920
4.419
.077
.646
.529
.490
.616
3625.1
.000
.319
.728
.003
.954
.277
.759
1.276
.287
.000
.813
.449
.624
.436
2.761
.072
.824
.444
.000
.168
.845
24.442
.000
3.349
.042
.303
.740
.000
.013
.987
9.219
.005
.228
.797
1.121
.333
.000
.352
.705
.099
.756
.948
.393
.350
.706
.000
7.139
.002
29.467
.000
15.371
.000
15.219
.000
.000
.085
.919
1.126
.298
.283
.755
.184
.832
.000
1.224
.272
.275
.605
.269
.765
.386
.682
.000
6.668
.003
.077
.783
8.645
.001
10.980
.000
F (1,4)
Sig.
F(2,8)
Sig.
F (1,4)
Sig.
F(2,8)
Sig.
F(2,8)
Sig.
4.120
.112
.852
.462
3.984
.117
.061
.941
.177
.841
Distance
2.568
.184
.185
.835
813.954
.000
1.335
.316
1.651
.268
.377
.765
1.460
.288
Speed
2.003
.230
.817
.475
586.841
.000
3.510
.080
1.981
.232
1.476
.285
3.544
.079
Table B-2: Three within-subject 2*3*2 ANOVA analyses for the parameters duration, distance and speed
were performance for each pigeon. The first factor is the factor visual field with two levels: lateral visual
fields and frontal visual field. The second factor is the factor presentation with 3 levels: hold phase
presentation, thrust phase presentation and random presentation. The third factor is the factor phase with
two levels: hold phase and thrust phase values of the parameters. The same data analysis was calculated for
the average duration, distance and speed for all pigeons. Significant effects (p<.05) are marked in blue.
Appendix 134
C. Why birds bob their heads?
Behavioural observations following Clements 2000 checklist (2004 update)

Order
Struthioniformes
Rheiformes
Family
Struthionidae
Rheidae
Family members
Ostriches
Rheas
Casuariiformes
Casuariidae
Cassowaries
Dinornithiformes
Tinamiformes
Sphenisciformes
Gaviiformes
Podicipediformes
Dromaiidae
Apterygidae
Tinamidae
Spheniscidae
Gaviidae
Podicipedidae
Emus
Kiwis
Tinamous
Penguins
Loons
Grebes
Diomedeidae
Procellariidae
Hydrobatidae
Pelecanoididae
Phaethontidae
Pelecanidae
Albatrosses
Shearwaters and Petrels
Storm-Petrels
Diving-Petrels
Tropicbirds
Pelicans
Sulidae
Phalacrocoracidae
Boobies and Gannets

Cormorants
Anhingidae
Fregatidae
Ardeidae
Anhingas and Darters

Frigatebirds
Herons, Egrets and Bitterns
Procellariiformes
Pelecaniformes
Ciconiiformes
Common name
Ostrich
Greater Rhea
Lesser Rhea
Northern Cassowary
Dwarf Cassowary
Australian Emu
Scientific name
Struthio camelus
Rhea americana
Rhea pennata
Causarius unappendiculatus
Casuarius bennetti
Source
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Bobbing
HB*
NB
NB
HB
HB
HB*
Elegant Crested Tinamou

Humboldt Penguin
Common Loon
Great Crested Grebe
Little Grebe
Black-footed Albatross
Eudromia elegans
Spheniscus humboldti
Gavia immer
Podiceps cristatus
Tachybaptus ruficollis
Diomedea nigripes
Video recording
Field observation
Video recording
(Dagg, 1977)
Field observation
Field observation
HB
NB
NB
HB* (ws)
HB* (ws)
OHM
Red-tailed Tropicbird
Great White Pelican
Dalmatian Pelican
Northern Gannet
Great cormorant
Guanay cormorant
Anhinga
Phaeton rubricauda
Pelecanus onocrotalus
Pelecanus crispus
Morus bassanus
Phalacrocorax carbo
Phalacrocorax bougainvillii
Anhinga anhinga
(IBC,2005)
Field observation
Video recording
Video recording
Field observation
Video recording
(IBC,2005)
(IBC,2005)
BB?
NB
NB
NB
NB
NB
HB?
Gray Heron
Great Blue heron
Black Headed Heron
Little Egret
Intermediate Egret
Ardea cinerea
Ardea herodias
Ardea melanocephala
Egretta garzetta
Egretta intermedia
(Fujita, 2003)
Field observation
Video recording
(Fujita, 2003)
Video recording
HB (wl)
HB
HB
HB
HB
Appendix 135
Order
Family
Family members
Scopidae
Ciconiidae
Hamerkop
Storks
Balaenicipitidae
Threskiornithidae
Shoebill
Ibises and Spoonbills
Phoenicopteriformes
Phoenicopteridae
Flamingos
Anseriformes
Anhimidae
Anatidae
Screamers
Ducks, Geese and Swans
Common name
Snowy Egret
Western Reef-Heron
Little Bittern
Cattle Egret
Boat-billed Heron
Hamerkop
White Stork
Woolly-necked Stork
Abdim's Stork
Oriental Stork
African Openbill
Marabou
Yellow-billed Stork
Saddle-billed Stork
Shoebill
Scarlet Ibis
American White Ibis
Sacred Ibis
Glossy Ibis
Indian Black Ibis
Roseate Spoonbill
Eurasian Spoonbill
Madagascar Crested Ibis
Hadada Ibis
Greater Flamingo
Lesser Flamingo
Chilean Flamingo
Southern Screamer
Greylag Goose
Bar-headed Goose
Chiloe Wigeon
Specled Teal
Red-billed Duck
Hottentot Teal
Gadwall
Scientific name
Egretta thula
Egretta gularis
Ixobrychus minutus
Bubulcus ibis
Cochlearius cochlearius
Scopus umbretta
Ciconia ciconia
Ciconia episcopus
Ciconia abdimii
Ciconia boyciana
Anastomus lamelligerus
Leptoptilos crumeniferus
Mycteria ibis
ephippiorhynchus
senegalensis
balaeniceps rex
Eudocimus ruber
Eudocimus albus
Threskiornis aethiopicus
Plegadis falcinellus
Pseudibis papillosa
Platalea ajaja
Platalea leucorodia
Lophotibis cristata
Bostrychia hagedash
Phoenicopterus roseus
Phoenicopterus minor
Phoenicopterus chilensis
Chauna torquata
Anser anser
Anser indicus
Anas sibilatrix
Anas flavirostris
Anas erythrorhyncha
Anas hottentota
Anas strepera
Source
Field observation
Video recording
Video recording
Video recording
Field observation
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Bobbing
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
NB?
HB
Video recording
Video recording
Video recording
Video recording
(Dagg , 1977)
Field observation
Field observation
Video recording
Video recording
Video recording
Video recording
Video recording
Field observation
Video recording
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
HB
NB
HB
HB
HB
HB
HB
HB
HB
HB
HB
NB
NB
NB
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
Appendix 136
Order
Falconiformes
Family
Cathartidae
Family members
New World Vultures
Common name
Mallard
Northen Pintail
Yellow Billed Pintail
Common Teal
Egyptian Goose
Wood Duck
Lesser Scaup
Tufted Duck
Pochard
Ferruginous Pochard
Bean Goose
Red-breasted Goose
Black Brant
Goldeneye
Bufflehead
White-winged Duck
Long-tailed Duck
Mute Swan
Whooper Swan
White-faced Whistling
Duck
Harlequin Duck
Smew
Goosander
African Pygmy-Goose
Marbled Teal
Ruddy Duck
White-Headed Duck
Red-crested Pochard
King Eider
Spectacled Eider
Common Eider
Common Shelduck
Paradise Shelduck
Black Vulture
Andean Condor
Scientific name
Anas platyrhynchos
Anas acuta
Anas georgica
Anas crecca
Alopochen aegyptiacus
Aix sponsa
Aythya affinis
Aythya fuligula
Aythya ferina
Aythia nyroca
Anser fabalis
Branta ruficollis
Branta bernicla nigricans
Bucephala clangula
Bucephala albeola
Cairina scutulata
Clangula hyemalis
Cygnus olor
Cygnus cygnus
Source
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field obsrvation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field obsrvation
Field observation
Field observation
Bobbing
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)?
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
Dendrocygna viduata
Histrionicus histrionicus
Mergus Albellus
Mergus merganser
Nettapus auritus
Marmaronetta angustirostris
Oxyura jamaicensis
Oxiura leucocephala
Netta rufina
Somateria spectabilis
Somateria fischeri
Somateira m. mollisima
Tadorna tadorna
Tadorna variegata
Coragyps atratus
Vultur gryphus
Field observation
Video recording
Video recording
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
Field observation
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB (ws)
NB
NB
Appendix 137
Order
Galliformes
Family
Pandionidae
Accipitridae
Family members
Osprey
Hawks, Eagles and Kites
Sagittariidae
Falconidae
Secretary-bird
Falcons and Caracaras
Megapodiidae
Cracidae
Megapodes
Guans, Chachalacas and
Allies
Meleagridae
Turkeys
Tetraonidae
Grouses
Odontophoridae
Phasianidae
New World Quail

Pheasants and Partridges
Common name
Osprey
Eagles
Buzzards
Harriers
Kites
Eurasian Griffon
White-backed Vulture
Ruppells griffon vulture
Black Vulture
lammergeier
Steller's Sea-eagle
Bateleur
Lappet-faced Vulture
Hooded Vulture
White-Headed Vulture
Secretary bird
Eurasian Krestel
Southern Caracara
Australian Brush-turkey
Scientific name
Pandion haliaetus
Aquila sp.
Buteo sp.
Circus sp.
Milvus sp.
Gyps fulvus
Gyps africanus
Gyps rueppelli
Aegypius monachus
Gypaetus barbatus
Haliaeetus pelagicus
Terathopius ecaudatus
Torgos tragheliotus
Necrosyrtes monachus
Trigonoceps occipitalis
Sagittarius serpentarius
Falco tinnunculus
Caracara plancus
Alectura lathami
Source
(IBC,2005)
Field observation
Field observation
Field observation
Field observation
Field observation
Video recording
Video recording
Field observation
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
(IBC,2005)
Bobbing
NB
NB
NB
NB
NB
NB
NB
NB
NB
NB
NB
NB
NB
NB
NB
HB
NB
NB
HB
Razor-billed Curassow
Nocturnal Curassow
Black Curassow
Horned Guan
Blue-throated Piping-guan
Wild Turkey
Ocellated Turkey
Hazel Grouse
Eurasian Capercaillie
Black Grouse
California Quail
Partridges
Golden Pheasant
Domestic Chicken
Common Quail
Blue-breasted Quail
Mitu tuberosa
Nothocrax urumutum
Crax alector
Oreophasis derbianus
Pipile cujubi
Meleagris gallopavo
Meleagris ocellata
Bonasa bonasia
Tetrao urogallus
Tetrao tetrix
Callipepla californica
Perdix s.p.
Chrysolophus pictus
Gallus domesticus
Coturnix coturnix
Coturnix chinensis
Video recording
Field observation
Field observation
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
(Dagg, 1977)
Video recording
(Pratt, 1982)
Field observation
Video recording
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
Appendix 138
Order
Opisthocomiformes
Gruiformes
Charadriiformes
Family
Family members
Numididae
Opisthocomidae
Mesitornithidae
Turnicidae
Gruidae
Guineafowl
Hoatzin
Mesites
Button Quails
Cranes
Aramidae
Psophiidae
Rallidae
Limpkin
Trumpeters
Rails, Gallinules and Coots
Heliornithidae
Rhynochetidae
Eurypygidae
Cariamidae
Otididae
Sungrebes and Finfoots

Kagu
Sunbittern
Seriemas
Bustards
Jacanidae
Jacanas
Common name
Brown Quail
Vulturine Guineafowl
Indian Peafowl
Green Peafowl
Gray Brested Patridge
Crested Fireback
Satyr-tragopan
Malayan Peacock
Pheasant
Crested Francolin
Yellow Necked Spurfowl
Red Necked Spurfowl
Helmeted Guineafowl
Scientific name
Coturnix ypsilophora
Acryllium vulturinum
Pavo cristatus
Pavo muticus
Arborophila orientalis
Lophura ignita
Tragopan satyra
Source
(Dagg, 1977)
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Bobbing
HB
HB
HB
HB
HB
HB
HB
Polyplectron malacense
Francolinus sephaena
Francolinus leucoscepus
Francolinus afer
Numida meleagris
Video recording
Video recording
Video recording
Video recording
Field observation
HB
HB
HB
HB
HB
Barred Buttonquail
Demoiselle Crane
Black crowned-Crane
Red-crowned Crane
Hooded Crane
Common Crane
Turnix suscitator
Anthropoides Virgo
Balearica pavonina
Grus japonensis
Grus monacha
Grus grus
Field observation
Video recording
Video recording
Video recording
Video recording
Video recording
HB
HB
HB
HB
HB
HB
Gray-winged Trumpeter
Common Moorhen
Eurasian Coot
Giant Wood-rail
Black crake
Corncrake
Psophia crepitans
Gallinula chloropus
Fulica atra
Aramides ypecaha
Amaurornis flavirostris
Crex crex
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
HB
HB* (b)
HB* (b)
HB
HB
HB
Kagu
Sunbittern
Red-legged Seriema
Kori Bustard
Black Bustard
Wattled Jacana
African Jacana
Rhynochetos jubatus
Eurypyga helias
Cariama cristata
Ardeotis kori
Eupodotis afra
Jacana jacana
Actophilornis africanus
Field observation
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
NB
HB
HB*
HB*
HB*
HB
HB
Appendix 139
Order
Family
Rostratulidae
Family members
Painted-Snipe
Dromadidae
Crab Plover
Haematopodidae
Oystercatchers
Ibidorhynchidae
Recurvirostridae
Ibisbill
Avocets and Stilts
Burhinidae
Glareolidae
Charadriidae
Thick-knees
Pratincoles and Coursers
Plovers and Lapwings
Pluvianellidae
Magellanic Plover
Scolopacidae
Sandpipers and Allies
Pedionomidae
Thinocoridae
Chionididae
Stercorariidae
Laridae
Plains-wanderer
Seedsnipes
Sheathbills
Skuas and Jaegers
Gulls
Sternidae
Rynchopidae
Terns
Skimmers
Common name
Scientific name
Source
Bobbing
Oystercatcher
Blackish Oystercatcher
Magellanic Oystercatcher
Ibisbill
Avocet
Black-winged stilt
Stone-curlew
Haematopus ostralegus
Haematopus ater
Haematopus leucopodus
Ibidorhyncha struthersii
Recurvirostra avosetta
Himantopus himantopus
Burhinus oedicnemus
(Whiteside,
1967)
IBC
IBC
IBC
Video recording
Video recording
Video recording
HB*
HB*
HB*
HB
HB
HB
NB
Little Ringed Plover

Grey Plover
Charadrius dubius
Pluvialis squatarola
Egyptian Plover
Northen Lapwing
Southern Lapwing
Crowned Lapwing
Blacksmith Lapwing
Pluvianus aegyptius
Vanellus vanellus
Vanellus chilensis
Vanellus coronatus
Vanellus armatus
Turnstones
Sharp-tailed Sandpiper
Red-necked Stint
Common Snipe
Wilson's Phalarope
Common Redshank
Common Sandpiper
Ruff
Arenaria interpres
Calidris acuminata
Calidris ruficollis
Gallinago gallinago
steganopus tricolor
Tringa totanus
Actitis hypoleucos
Philomachus pugnax
Rufous-bellied Seedsnipe
Pale-faced Sheathbill
Great Skua
Gulls
Black Tailed Gull
Inca Tern
Attagis gayi
Chionis alba
Stercorarius skua
Larus sp.
Larus crassirostris
Larosterna inca
Field observation
Video recording
Field
Observation
Video recording
Video recording
Video recording
Video recording
(Whiteside,
1967)
(Dagg, 1977)
(Dagg, 1977)
(IBC,2005)
(IBC,2005)
Video recording
Video recording
Video recording
(IBC,2005)
(IBC,2005)
(IBC,2005)
(Dagg, 1977)
Video recording
Video recording
HB*& OHM
HB
HB*& OHM
HB*
NB, OHM
HB*
HB*
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
NB
NB
NB
NB
Appendix 140
Order
Pterocliformes
Family
Alcidae
Pteroclididae
Family members
Auks, Murres and Puffins
Sandgrouse
Common name
Atlantic Puffin
Namaqua Sandgrouse
Scientific name
Fratercula arctica
Pterocles namaqua
Columbiformes
Columbidae
Pigeons and Doves
Rock Dove
Speckled Pigeon
African Olive Pigeon
Columba livia
Columba guinea
Columba arquatrix
Doves
Zoe Imperial Pigeon
Squatter Pigeon
Victoria Crowned-Pigeon
Souther Crowned-pigeon
Squatter Pigeon
Laughing Dove
African Collared-Dove
Bronze-naped Pheasant
Pigeon
Wompoo Fruit-Dove
Emerald Dove
Cinnamon Ground Dove
Bar-shouldered Dove
Socorro Dove
Crested Pigeon
Diamond Dove
Mindanao Bleeding-heart
Ruddy Quail-Dove
Crested Quail-Dove
Orange-bellied Fruit-Dove
Namaqua Dove
Psittaciformes
Musophagiformes
Cacatuidae
Psittacidae
Musophagidae
Cockatoos and Allies

Parrots, Macaws and Allies
Turacos
Cuculiformes
Cuculidae
Cuckoos
Budgerigar
Violet Turaco
Purple-crested Turaco
Greater Roadrunner
Coral-billed Groundcuckoo
Crested Coua
Bobbing
NB
HB
Streptopelia sp.
Ducula zoeae
Geophaps scripta
Goura victoriae
Goura scheepmakeri
Geophaps scripta
Streptopelia senegalensis
Streptopelia roseogrisea
Source
(IBC,2005)
(IBC,2005)
(Dunlap &
Mowrer,1930)
Video recording
Video recording
(Dunlap &
Mowrer,1930)
Field observation
Field observation
(Dagg, 1977)
Field observation
Video recording
Video recording
Video recording
Otidiphaps nobilis
Ptilinopus magnificus
Chalcophaps indica
Gallicolumba rufigula
Geopelia humeralis
Zenaida graysoni
Geophaps Iophotes
Geopelia cuneata
Gallicolumba criniger
Geotrygon montana
Geotrygon versicolor
Ptilinopus iozonus
Oena capensis
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
Video recording
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
Melopsittacus undulatus
Musophaga violacea
Tauraco porphyreolophus
Geococcyx californianus
Field observation
Video recording
(IBC,2005)
OHM
HB& BB
HB& BB
NB
Carpococcyx renauldi
Coua cristata
Video recording
Video recording
HB
BB
HB (wl)
HB
HB
HB
HB
HB
HB
HB
HB
HB
HB
Appendix 141
Order
Family
Family members
Strigiformes
Tytonidae
Strigidae
Steatornithidae
Aegothelidae
Podargidae
Nyctibiidae
Caprimulgidae
Apodidae
Hemiprocnidae
Trochilidae
Coliidae
Trogonidae
Alcedinidae
Todidae
Momotidae
Meropidae
Coraciidae
Brachypteraciidae
Barn-Owls
Typical Owls
Oilbird
Owlet-Nightjars
Frogmouths
Potoos
Nightjars and Allies
Swifts
Treeswifts
Hummingbirds
Mousebirds
Trogons
Kingfishers
Todies
Motmots
Bee-eaters
Typical Rollers
Ground-Rollers
Leptosomidae
Upupidae
Phoeniculidae
Caprimulgiformes
Apodiformes
Trochiliformes
Coliiformes
Trogoniformes
Coraciiformes
Piciformes
Common name
Guira Cuckoo
Coppery-tailed Coucal
White-browed Coucal
Barn Owl
Tawny Owl
Scientific name
Guira guira
Centropus cupreicaudus
Centropus superciliosus
Tyto alba
Strix aluco
Source
Video recording
(IBC,2005)
(IBC,2005)
(IBC,2005)
Field observation
Bobbing
HB& BB
HB
HB
OHM
OHM
Blue-naped Mousebird
Urocolius macrourus
Video recording
BB
Common Kingfisher
Alcedo atthis
Field observation
OHM
Pitta-like Ground-roller
Long-tailed Ground-roller
Atelornis pittoides
Uratelornis chimaera
Video recording
Video recording
NB
NB
Cuckoo-Roller
Hoopoes
Woodhoopoes
Hoopoe
Upupa epops
Video recording
HB
Bucerotidae
Hornbills
Abyssinian Groundhornbill
Southern Ground-hornbill
Bucorvus abyssinicus
Bucorvus leadbeateri
Video recording
Video recording
NB
NB
Galbulidae
Bucconidae
Capitonidae
Jacamars
Puffbirds
Barbets
Ramphastidae
Indicatoridae
Picidae
Toucans
Honeyguides
Woodpeckers and Allies
Red-and-yellow Barbet
D'arnaud's Barbet
Keel-billed toucan
Trachyphonus erythrocephalus
Trachyphonus darnaudii
Ramphastos sulfuratus
Video recording
Video recording
Video recording
BB
BB
BB
Green Woodpecker
Northern Flicker
Picus viridis
Colaptes auratus
Field observation
Video recording
BB
BB
Appendix 142
Order
Family
Family members
Passeriformes
Eurylaimidae
Philepittidae
Furnariidae
Broadbills
Asities
Ovenbirds
Dendrocolaptidae
Thamnophilidae
Formicariidae
Conopophagidae
Rhinocryptidae
Phytotomidae
Cotingidae
Pipridae
Tyrannidae
Oxyruncidae
Pittidae
Woodcreepers
Typical Antbirds
Antthrushes and Antpittas
Gnateaters
Tapaculos
Plantcutters
Cotingas
Manakins
Tyrant Flycatchers
Sharpbill
Pittas
Atrichornithidae
Menuridae
Acanthisittidae
Alaudidae
Hirundinidae
Motacillidae
Scrub-birds
Lyrebirds
New Zealand Wrens
Larks
Swallows
Wagtails and Pipits
Campephagidae
Cuckoo-shrikes
Pycnonotidae
Bulbuls
Regulidae
Kinglets
Common name
Golden-fronted
Woodpecker
Green Broadbill
Scientific name
Source
Bobbing
Melanerpes aurifrons
Calyptomena Viridis
Video recording
Video recording
BB
BB
Pale-legged Hornero
Rufous-banded Miner
Cordilleran Canastero
Ochre-cheeked Spinetail
Furnarius leucopus
Geositta rufipennis
Asthenes modesta
Poecilurus scutatus
Video recording
Video recording
(IBC,2005)
(IBC,2005)
HB
HB
BB
BB
Narrow-billed
Woodcreeper
Lepidocolaptes angustirostris
Magellanic Tapaculo
Scytalopus magellanicus
(IBC,2005)
Long-wattled Umbrellabird
Cephalopterus penduliger
Video recording
Pittas
Blue-tailed Pitta
Black Crouned pitta
Banded pitta
Pitta sp.
Pitta arcuata
Pitta venusta
Pitta guajana
(Dagg, 1977)
Video recording
Video recording
Vidoe recordings
BB
BB
BB
BB
Lyre Bird
Menura superba
(Dagg, 1977)
HB
Lesser Striped Swallow

White Wagtail
African Pied Waigtail
Hirundo abyssinica
Motacilla alba
Motacilla Aguimp
Field observation
Field observation
Field observation
BB
HB
HB
Redwhiskered Bulbul
Common Bulbul
Pycnonotus jocosus
Pycnonotus barbatus
Video recording
Video recording
HB
HB
(IBC,2005)
BB
BB
Appendix 143
Order
Family
Family members
Chloropseidae
Aegithinidae
Ptilogonatidae
Bombycillidae
Hypocoliidae
Dulidae
Cinclidae
Troglodytidae
Mimidae
Prunellidae
Turdidae
Leafbirds
Ioras
Silky-flycatchers
Waxwings
Hypocolius
Palm Chat
Dippers
Wrens
Mockingbirds and Thrashers
Accentors
Thrushes and Allies
Cisticolidae
Sylviidae
Polioptilidae
Muscicapidae
Cisticolas and Allies

Old World Warblers
Gnatcatchers
Old World Flycatchers
Platysteiridae
Rhipiduridae
Monarchidae
Wattle-eyes
Fantails
Monarch Flycatchers
Petroicidae
Australasian Robins
Pachycephalidae
Whistlers and Allies
Picathartidae
Rockfowl
Timaliidae
Babblers
Common name
Scientific name
Source
Bobbing
Long Tailed Tit
Aeghithalos caudatos
Field observation
BB
Song thrush
Fieldfare
Robin
Mistle thrust
Redstarts
Turdus philomenos
Turdus philaris
Erithacus rubecula
turdus viscivorus
Phoenicurus sp.
BB
BB
BB
BB
BB
Blackbirds
Turdus meruls
Field observation
(Jonsson, 1993)
(Jonsson, 1993)
Field observation
(Jonsson, 1993)
(Whiteside,
1967)
Cettis Warblers
Cettia cetti
Field observation
BB
Chats
Cape robin-chat
Red-capped Robin-Chat
White-browed Scrub-robin
Spotted flycatcher
Cossypha sp.
Cossypha caffra
Cossypha natalensis
Cercotrichas leucophrys
muscicapa striata
(Jonsson, 1993)
Video recording
Video recording
Video recording
Field observation
BB
BB
BB
BB
BB
Capped wheatear
Oenanthe pileata
Video recording
BB
White Creasted Laughingthrush
Garrulax leucolophus
Video recording
BB
HB& BB
Appendix 144
Order
Family
Pomatostomidae
Paradoxornithidae
Orthonychidae
Cinclosomatidae
Aegithalidae
Maluridae
Acanthizidae
Epthianuridae
Neosittidae
Climacteridae
Paridae
Sittidae
Tichodromidae
Certhiidae
Rhabdornithidae
Remizidae
Nectariniidae
Melanocharitidae
Paramythiidae
Dicaeidae
Pardalotidae
Zosteropidae
Promeropidae
Meliphagidae
Oriolidae
Irenidae
Laniidae
Malaconotidae
Prionopidae
Vangidae
Dicruridae
Callaeidae
Family members
Pseudo-babblers
Parrotbills
Logrunner and Chowchilla
Whipbirds and Quailthrushes
Long-tailed Tits
Fairywrens
Thornbills and Allies
Australian Chats
Sitellas
Australasian Treecreepers
Chickadees and Tits
Nuthatches
Wallcreeper
Creepers
Philippine Creepers
Penduline Tits
Sunbirds and Spiderhunters
Berrypeckers and Longbills
Tit and Crested
Berrypeckers
Flowerpeckers
Pardalotes
White-eyes
Sugarbirds
Honeyeaters
Old World Orioles
Fairy-bluebirds
Shrikes
Bushshrikes and Allies
Helmetshrikes
Vangas
Drongos
Wattlebirds
Common name
Scientific name
Source
Bobbing
Yellow-throated Laughingthrush
Garrulax galbanus
Video recording
BB
Bearded Reedling
Panurus biarmicus
Tits
Parus sp.
Field observation
BB
Magpie Shrike
Common Gonolek
Corvinella melanoleuca
laniarius barbarus
Field observation
Field observation
BB
BB
Appendix 145
Order
Family
Grallinidae
Corcoracidae
Artamidae
Pityriaseidae
Cracticidae
Paradisaeidae
Ptilonorhynchidae
Corvidae
Family members
Mudnest-builders
White-winged
Chough&Apostlebird
Woodswallows
Bristlehead
Bellmagpies and Allies
Birds of Paradise
Bowerbirds
Crows, Jays and Magpies
Sturnidae
Starlings
Ploceidae
Weavers and Allies
Estrildidae
Waxbills and Allies
Common name
Scientific name
Source
Bobbing
White-winged Magpie
Magpie
Rook
Carrion Crow
Jay
Eurasian Magpie
Red-billed Chough
Alpine Chough
Azure-winged magpie
Euroasian Jackdaw
Cape Rock
Superb starling
Platysmurus leucopterus
Gymnorhina tibicen
Corvus frugilegus
Corvus corone
Garrulus glandarius
Pica pica
Pyrrhocorax pyrrhocorax
Pyrrochoras gragulus
Cyanopica cyana
Corvus monedula
Corvus Capensis
lamprotornis superbus
HB& BB
HB& BB
HB& BB
HB& BB
BB
HB& BB
HB& BB
HB& BB
HB& BB
HB& BB
HB& BB
HB*& BB
Starlings
Mynah Bird
European Starling
Ashy Starling
Red-billed Oxpecker
White-headed BuffaloWeaver
Village Weaver
Long-tailed Widowbird
Spleckle-fronted Weaver
Red billed Buffalo-weaver
Sturnus sp.
Acrhidotheres tristis
Sturnus vulgaris
Cosmopsarus unicolor
Buphagus erythrorhynchus
(Frost, 1978)
(Dagg, 1977)
(Frost, 1978)
(Dagg, 1977)
(Dagg, 1977)
Video recording
Field observation
Video recording
Video recording
Video recording
Field observation
Video recording
(Whiteside,
1967)
(Dagg, 1977)
Dinemellia dinemelli
Ploceus cucullatus
Euplectes progne
Sporopipes frontalis
Bubalornis niger
Video recording
Video recording
Video recording
Video recording
Video recording
HB& BB
HB& BB
HB& BB
HB& BB
HB& BB
Baglafecht weaver
Zebra Finch
Diamond Firetail
Ploceus baglafecht
Taeniopygia guttata
Stagonopleura guttata
Field observation
Field observation
BB
BB
BB
Pink-throated Twinspot
Hypargos margaritatus
HB*& BB
HB*& BB
HB*& BB
HB*& BB
BB
BB
Appendix 146
Order
Family
Family members
Viduidae
Vireonidae
Drepanididae
Peucedramidae
Parulidae
Coerebidae
Thraupidae
Indigobirds
Vireos and Allies
Hawaiian Honeycreepers
Olive Warbler
Wood Warblers
Banaquit
Tanager and Allies
Emberizidae
Buntings, Sparrows,
Seedeater and Allies
Cardinalidae
Icteridae
Fringillidae
Passeridae
Common name
Black-crowned Waxbill
Blue-capped Cordon-bleu
Scientific name
Estrilda nonnula
Uraeginthus cyanocephalus
Blue-necked Tanager
Golden Tanager
Tangara cyanicollis
Tangara arthus
BB
BB
Paradise Tanager
Tangara chilensis
BB
Yellowhammer
Saffron Finch
Black-hooded SierraFinch
Grey-hooded Sierra-Finch
Patagonian Sierra-Finch
Emberiza citrinella
Sicalis flaveola
Video recording
Video recording
BB
BB
Phrygilus atriceps
Phrygilus gayi
Phrygilus patagonicus
Video recording
Video recording
Video recording
BB
BB
BB
Saltators, Cardinals and

Allies
Blackbirds, orioles, crackles
Siskins, Crossbills and
Finches
Scarlet Headed Blackbird
Amblyramphus holosericeus
Old World Sparrows
Hawfinch
Oriole Finch
House Sparrow
Yellow-spotted Petronia
Grey-headed Sparrow
Chaffinch
Serin
Crossbill
Common Crossbill
Eurasian Bullfinch
Fringilla coelebs
Serinus serinus
Loxia leucoptera
Loxia curvirostra
pyrrhula pyrrhula
Coccothraustes
coccothraustes
Linurgus olivaceus
Passer domesticus
Petronya pyrgita
Passer griseus
Table C-1: Behavioural observations following Clements 2000 checklist (2004 update)
Source
Bobbing
BB
BB
BB
(Whiteside,
1967)
Field observation
Field observation
Video recording
Video recording
HB
BB
BB
BB
BB
Video recording
Video recording
Video recording
Video recording
BB
BB
BB
BB
BB
Appendix 147
Abbreviations:
HB: head-bobbing while walking
HB(s): head-bobbing while swimming.
HB(ws): head-bobbing while walking & swimming
HB(wl): head-bobbing while walking & landing
HB*: rare or occasional head-bobbing birds
NB: neither head-bobbing nor hoping birds
NB(ws): Non-bobbing during walking and swimming
BB: hoping birds
OHM: other head movement
? Further observations needed
Appendix 148
Behavioural observations following Sibley`s phylogenetic tree (1990)
Class Aves
Subclass Neornithes
Infraclass Eoaves
Parvclass Ratitae
Order Struthioniformes
Suborder Struthioni
Infraorder Struthionides
Family Struthionidae: Ostrich HB*
Infraorder Rheides
Family Rheidae: Rheas NB?
Suborder Casuarii
Family Casuariidae
Tribe Casuariini: Cassowaries HB
Tribe Dromaiini: Emus HB*
Family Apterygidae: Kiwis
Order Tinamiformes
Family Tinamidae: Tinamous HB
Infraclass Neoaves
Parvclass Galloanserae
Superorder Gallomorphae
Order Craciformes
Suborder Craci
Family Cracidae: Guans, Chachalacas, etc. HB
Suborder Megapodii
Family Megapodiidae: Megapodes HB
Order Galliformes
Parvorder Phasianida
Superfamily Phasianoidea
Family Phasianidae: Grouse, Pheasants, etc. HB
Superfamily Numidoidea
Family Numididae: Guineafowls HB
Parvorder Odontophorida
Family Odontophoridae: New World Quails HB
Superorder Anserimorphae
Order Anseriformes
Infraorder Anhimides
Superfamily Anhimoidea
Family Anhimidae: Screamers NB
Superfamily Anseranatoidea
Family Anseranatidae: Magpie Goose NB
Infraorder Anserides
Family Dendrocygnidae: Whistling-Ducks NB
Family Anatidae
Subfamily Oxyurinae: Stiff-tailed Ducks NB
Subfamily Cygninae: Swans
NB
Subfamily Anatinae
Tribe Anserini: Geese NB
Tribe Anatini: Typical Ducks NB
Parvclass Turnicae
Order Turniciformes
Family Turnicidae: Buttonquails(Turnix, Ortyxelos) HB
Parvclass Picae
Order Piciformes
Infraorder Picides
Family Indicatoridae: Honeyguides
Family Picidae: Woodpeckers, Wrynecks BB
Infraorder Ramphastides
Superfamily Megalaimoidea
Family Megalaimidae: Asian Barbets
Superfamily Lybioidea
Family Lybiidae: African Barbets BB
Superfamily Ramphastoidea
Family Ramphastidae
Subfamily Capitoninae: New World Barbets BB
Subfamily Ramphastinae: Toucans BB
Parvclass Coraciae
Superorder Galbulimorphae
Order Galbuliformes
Infraorder Galbulides
Family Galbulidae: Jacamars
Infraorder Bucconides
Appendix 149
Family Bucconidae: Puffbirds
Superorder Bucerotimorphae
Order Bucerotiformes
Family Bucerotidae: Typical Hornbills BB
Family Bucorvidae: Ground-Hornbills NB
Order Upupiformes
Infraorder Upupides
Family Upupidae: Hoopoes
HB
Infraorder Phoeniculides
Family Phoeniculidae: Wood-Hoopoes
Family Rhinopomastidae: Scimitarbills
Superorder Coraciimorphae
Order Trogoniformes
Family Trogonidae
Subfamily Apaloderminae: African Trogons
Subfamily Trogoninae
Tribe Trogonini: New World Trogons
Tribe Harpactini: Asian Trogons
Order Coraciiformes
Suborder Coracii
Superfamily Coracioidea
Family Coraciidae: Typical Rollers
Family Brachypteraciidae: Ground-Rollers NB
Superfamily Leptosomoidea
Family Leptosomidae: Cuckoo-Rollers
Suborder Alcedini
Infraorder Alcedinides
Parvorder Momotida
Family Momotidae: Motmots
Parvorder Todida
Family Todidae: Todies
Parrorder Alcedinida
Family Alcedinidae: Alcedinid Kingfishers
Parrorder Cerylida
Superfamily Dacelonoidea
Family Dacelonidae: Dacelonid Kingfishers
Superfamily Ceryloidea
Family Cerylidae: Cerylid Kingfishers
Infraorder Meropides
Family Meropidae: Bee-eaters
Parrclass Coliae
Order Coliiformes
Family Coliidae
Subfamily Coliinae: Typical Mousebirds BB
Subfamily Urocoliinae: Long-tailed Mousebirds
Parvclass Passerae
Superorder Cuculimorphae
Order Cuculiformes
Infraorder Cuculides
Parvorder Cuculida
Superfamily Cuculoidea
Family Cuculidae: Old World Cuckoos HB, BB
Superfamily Centropodoidea
Family Centropodidae: Coucals HB
Parvorder Coccyzida
Family Coccyzidae: American Cuckoos
Infraorder Crotophagides
Parvorder Opisthocomida
Family Opisthocomidae: Hoatzin
Parvorder Crotophagida
Family Crotophagidae
Tribe Crotophagini: Anis
Tribe Guirini: Guira Cuckoo HB&BB
Parvorder Neomorphida
Family Neomorphidae: Roadrunners, etc. NB
Superorder Psittacimorphae
Order Psittaciformes
Family Psittacidae: Parrots, Macaws, etc. OHM
Superorder Apodimorphae
Order Apodiformes
Family Apodidae: Typical Swifts
Family Hemiprocnidae: Crested Swifts
Order Trochiliformes
Family Trochilidae
Subfamily Phaethornithinae: Hermits
Subfamily Trochilinae: Typical Hummingbirds
Appendix 150
Superorder Strigimorphae
Order Musophagiformes
Family Musophagidae
Subfamily Musophaginae: Turacos HB&BB
Subfamily Criniferinae: Plaintain-eaters
Order Strigiformes
Suborder Strigi
Parvorder Tytonida
Family Tytonidae: Barn and Grass owls OHM
Parvorder Strigida
Family Strigidae: Typical Owls OHM
Suborder Aegotheli
Family Aegothelidae: Owlet-nightjars
Suborder Caprimulgi
Infraorder Podargides
Family Podargidae: Australian Frogmouths
Family Batrachostomidae: Asian Frogmouths
Infraorder Caprimulgides
Parvorder Steatornithida
Superfamily Steatornithoidea
Family Steatornithidae: Oilbird
Superfamily Nyctibioidea
Family Nyctibiidae: Potoos
Parvorder Caprimulgida
Superfamily Eurostopodoidea
Family Eurostopodidae: Eared Nightjars
Superfamily Caprimulgoidea
Family Caprimulgidae
Subfamily Chordeilinae: Nighthawks
Subfamily Caprimulginae: Nightjars
Superorder Passerimorphae
Order Columbiformes
Family Columbidae: Pigeons, Doves HB
Order Gruiformes
Suborder Grui
Infraorder Eurypygides
Family Eurypygidae: Sunbittern HB
Infraorder Otidides
Family Otididae: Bustards HB*
Infraorder Gruides
Parvorder Gruida
Superfamily Gruoidea
Family Gruidae: Cranes HB
Family Heliornithidae
Tribe Aramini: Limpkin
Tribe Heliornithini: New World Sungrebe (Podica& Heliopais )
Superfamily Psophioidea
Family Psophiidae: Trumpeters HB
Parvorder Cariamida
Family Cariamidae: Seriemas HB*
Family Rhynochetidae: Kagu NB
Suborder Ralli
Family Rallidae: Rails, Gallinules, Coots HB
Suborder Mesitornithi
Family Mesitornithidae: Mesites
Order Ciconiiformes
Suborder Charadrii
Infraorder Pteroclides
Family Pteroclidae: Sandgrouse HB
Infraorder Charadriides
Parvorder Scolopacida
Superfamily Scolopacoidea
Family Thinocoridae: Seedsnipe HB
Family Pedionomidae: Plains-wanderer
Family Scolopacidae
Subfamily Scolopacinae: Woodcock, Snipe HB
Subfamily Tringinae: Sandpipers, Curlews, Phalaropes HB
Superfamily Jacanoidea
Family Rostratulidae: Paintedsnipe
Family Jacanidae: Lily-trotters, Jacanas HB
Parvorder Charadriida
Superfamily Chionidoidea
Family Chionididae: Sheathbills HB
Superfamily Charadrioidea
Family Burhinidae: Thick-knees NB
Family Charadriidae
Appendix 151
Subfamily Recurvirostrinae
Tribe Haematopodini: Oystercatchers HB*
Tribe Recurvirostrini: Avocets, Stilts HB
Subfamily Charadriinae: Plovers, Lapwings HB*
Superfamily Laroidea
Family Glareolidae
Subfamily Dromadinae: Crab-plover NB
Subfamily Glareolinae: Pratincoles NB
Family Laridae
Subfamily Larinae
Tribe Stercorariini: Jaegers, Skuas NB
Tribe Rynchopini: Skimmers
Tribe Larini: Gulls NB
Tribe Sternini: Terns NB
Subfamily Alcinae: Auks, Murres, Puffins NB
Suborder Ciconii
Infraorder Falconides
Parvorder Accipitrida
Family Accipitridae
Subfamily Pandioninae: Osprey NB
Subfamily Accipitrinae: Hawks, Eagles, O.W. vultures, kites NB
Family Sagittariidae: Secretarybird HB
Parvorder Falconida
Family Falconidae: Falcons, Caracaras NB
Infraorder Ciconiides
Parvorder Podicipedida
Family Podicipedidae: Grebes HB
Parvorder Phaethontida
Family Phaethontidae: Tropicbirds BB?
Parvorder Sulida
Superfamily Suloidea
Family Sulidae: Boobies, Gannets NB
Family Anhingidae: Anhingas, Darters HB?
Superfamily Phalacrocoracoidea
Family Phalacrocoracidae: Cormorants NB
Parvorder Ciconiida
Superfamily Ardeoidea
Family Ardeidae: Herons, Bitterns, Egrets HB
Superfamily Scopoidea
Family Scopidae: Hammerhead HB
Superfamily Phoenicopteroidea
Family Phoenicopteridae. Flamingos NB
Superfamily Threskiornithoidea
Family Threskiornithidae: Ibises, Spoonbills HB
Superfamily Pelecanoidea
Family Pelecanidae
Subfamily Balaenicipitinae: Shoebill NB
Subfamily Pelecaninae: Pelicans NB
Superfamily Ciconioidea
Family Ciconiidae
Subfamily Cathartinae: New World vulture NB
Subfamily Ciconiinae: Storks HB (unless Marabou)
Superfamily Procellarioidea
Family Fregatidae: Frigatebirds
Family Spheniscidae: Penguins NB
Family Gaviidae: Loons NB
Family Procellariidae
Subfamily Hydrobatinae: Storm-Petrels
Subfamily Procellariinae: Shearwaters, Petrels, Diving-Petrels
Subfamily Diomedeinae: Albatrosses NB (OHM)
Order Passeriformes HB, BB, HB&BB
Suborder Tyranni (Suboscines)
Infraorder Acanthisittides
Family Acanthisittidae: New Zealand Wrens
Infraorder Eurylaimides
Superfamily Pittoidea
Family Pittidae: Pittas BB
Superfamily Eurylaimoidea
Family Eurylaimidae: Broadbills
Family Philepittidae: Asities
Infraorder Tyrannides
Parvorder Tyrannida
Family Tyrannidae
Subfamily Corythopinae: Corythopis, Mionectes, etc.
Subfamily Tyranninae: Tyrant Flycatchers
Subfamily Tityrinae
Appendix 152
Tribe Schiffornithini: Schiffornis
Tribe Tityrini, Tityras: Becards
Subfamily Cotinginae: Cotingas, Plantcutters, Sharpbills
Subfamily Piprinae: Manakins
Parvorder Thamnophilida
Family Thamnophilidae: Typical Antbirds
Parvorder Furnariida
Superfamily Furnarioidea
Family Furnariidae
Subfamily Furnariinae: Ovenbirds
Subfamily Dendrocolaptinae: Woodcreepers BB
Superfamily Formicarioidea
Family Formicariidae: Ground Antbirds
Family Conopophagidae: Gnateaters
Family Rhinocryptidae: Tapaculos BB
Suborder Passeri (Oscines)
Parvorder Corvida
Superfamily Menuroidea
Family Climacteridae: Australo-Papuan Treecreepers
Family Menuridae
Subfamily Menurinae: Lyrebirds HB
Subfamily Atrichornithinae: Scrubbirds
Family Ptilonorhynchidae: Bowerbirds
Superfamily Meliphagoidea
Family Maluridae
Subfamily Malurinae
Tribe Malurini: Fairywrens
Tribe Stipiturini: Emuwrens
Subfamily Amytornithinae: Grasswrens
Family Meliphagidae: Honeyeaters, incl. Ephthianura, Ashbyia
Family Pardalotidae
Subfamily Pardalotinae: Pardalotes
Subfamily Dasyornithinae: Bristlebirds
Subfamily Acanthizinae
Tribe Sericornithini: Scrubwrens
Tribe Acanthizini: Thornbills, Whitefaces, etc.
Superfamily Corvoidea
Family Eopsaltriidae: Australo-Papuan robins, Drymodes
Family Irenidae: Fairy-bluebirds, Leafbirds
Family Orthonychidae: Log-runners or Chowchillas
Family Pomatostomidae: Australo-Papuan babblers
Family Laniidae: True Shrikes (Lanius, Corvinella, Eurocephalus) BB
Family Vireonidae: Vireos, Greenlets, Peppershrikes
Family Corvidae
Subfamily Cinclosomatinae: Quail-thrushes, Whipbirds
Subfamily Corcoracinae: Australian Chough, Apostlebird
Subfamily Pachycephalinae
Tribe Neosittini: Sittellas
Tribe Mohouini: New Zealand Mohoua, Finschia
Tribe Falcunculini: Shrike-tits, Oreoica, Rhagologus
Tribe Pachycephalini: Whistlers, Shrike-thrushes
Subfamily Corvinae
Tribe Corvini: Crows, Magpies, Jays, Nutcrackers HB&BB
Tribe Paradisaeini: Birds of Paradise, Melampitta
Tribe Artamini: Currawongs, Woodswallows, Peltops, Pityriasis
Tribe Oriolini, Orioles: Cuckooshrikes
Subfamily Dicrurinae
Tribe Rhipidurini: Fantails
Tribe Dicrurini: Drongos
Tribe Monarchini: Monarchs, Magpie-larks
Subfamily Aegithininae: Ioras BB
Subfamily Malaconotinae
Tribe Malaconotini: Bush-shrikes BB
Tribe Prionopini: Helmet-shrikes, Batis, Platysteira, Vangas
Family Callaeatidae: New Zealand wattlebirds
Parvorder Passerida
Superfamily Muscicapoidea
Family Bombycillidae
Tribe Dulini: Palmchat
Tribe Ptilogonatini: Silky-flycatchers
Tribe Bombycillini: Waxwings
Family Cinclidae: Dippers
Family Muscicapidae
Subfamily Turdinae: True thrushes, incl. Chlamydochaera, BB, HB&BB
Brachypteryx, Alethe
Subfamily Muscicapinae
Appendix 153
Tribe Muscicapini: Old World Flycatchers
Tribe Saxicolini. Chats, Erithacus, etc.
Family Sturnidae
Tribe Sturnini: Starlings, Mynas HB&BB
Tribe Mimini: Mockingbirds, Thrashers, American Catbirds
Superfamily Sylvioidea
Family Sittidae
Subfamily Sittinae: Nuthatches
Subfamily Tichodromadinae: Wallcreeper
Family Certhiidae
Subfamily Certhiinae
Tribe Certhiini: Northern Creepers
Tribe Salpornithini: Afro-Asian Creeper
Subfamily Troglodytinae: Wrens
Subfamily Polioptilinae: Gnatcatchers, Verdin, Gnatwrens
Family Paridae
Subfamily Remizinae: Penduline-Tits
Subfamily Parinae: Titmice, Chickadees BB
Family Aegithalidae: Long-tailed Tits, Bushtits
Family Hirundinidae
Subfamily Pseudochelidoninae: River-Martins
Subfamily Hirundininae: Swallows, Martins BB
Family Regulidae: Kinglets
Family Pycnonotidae: Bulbuls HB
Family Hypocoliidae: Gray Hypocolius
Family Cisticolidae: African Warblers
Family Zosteropidae: White-eyes
Family Sylviidae
Subfamily Acrocephalinae: Leaf Warblers, Reed Wrablers, etc
Subfamily Megalurinae: Grassbirds, Songlarks, Fernbird
Subfamily Garrulacinae: Laughingthrushes, Liocichlas BB
Subfamily Sylviinae
Tribe Timaliini: Babblers, Minlas, Fulvettas, Yuhinas, Parrotbills
Tribe Chamaeini: Wrentit
Tribe Sylviini: Sylviine Warblers (Sylvia, Parisoma) BB
Superfamily Passeroidea
Family Alaudidae: Larks
Family Nectariniidae
Subfamily Promeropinae: African Sugarbirds
Subfamily Nectariniinae
Tribe Dicaeini: Flowerpeckers
Tribe Nectariniini: Sunbirds, Spiderhunters
Family Melanocharitidae
Tribe Melanocharitini: Melanocharis, Rhamphocharis
Tribe Toxorhamphini: Toxorhamphus, Oedistoma
Family Paramythiidae: Paramythia, Oreocharis
Family Passeridae
Subfamily Passerinae: Sparrows, Rock-Sparrows, etc.
Subfamily Motacillinae: Wagtails and Pipits HB
Subfamily Prunellinae: Accentors, Dunnock
Subfamily Ploceinae. Weaverbirds, incl. Amblyospiza, HB&BB, BB
Bubalornis, etc.
Subfamily Estrildinae
Tribe Estrildini: Waxbills, Estrildines BB
Tribe Viduini: Indigobirds, Whydahs
Family Fringillidae
Subfamily Peucedraminae: Olive Warbler
Subfamily Fringillinae
Tribe Fringillini: Chaffinches, Brambling HB, BB?
Abrebiations:
Tribe Carduelini: Goldfinches, Crossbills, etc. BB
Tribe Drepanidini: Hawaiian Honeycreepers
HB: head-bobbing birds
Subfamily Emberizinae
HB*: rare or occasional head-bobbing birds
Tribe Emberizini: Buntings, Longspurs, Towhees
NB: neither head-bobbing nor hoping birds
Tribe Parulini: Wood Warblers, incl. Zeledonia
BB: hoping birds
Tribe Thraupini: Tanagers, Swallow-tanager, Neotropical
OHM: other head movement
Honeycreepers, Plushcap,Tanager-finches
Tribe Cardinalini: Cardinals
?: Further observations needed
Tribe Icterini: Troupials, Meadowlarks American
Blackbirds Oropendolas
Table C-2: Behavioural observations according to Sibley`s phylogenetic tree (1990).
Appendix 154
Analysis of the ecological and behavioural characteristics of HB and NB birds

Feeding
source
Feeding
method
Group
size
Activity
Habitat
Flying
abilities
Predator
pressure
HB
HB
Ardea herodias
HB
Scopus umbretta
HB
HB
Order
Family
Common name
Scientific name
Bobbing
Casuariiformes
Casuariidae
Northern Cassowary
Causarius unappendiculatus
Tinamiformes
Tinamidae
Elegant Crested Tinamou
Eudromia elegans
Ciconiiformes
Ardeidae
Grey Blue Heron
Ciconiiformes
Scopidae
Hamerkop
Ciconiiformes
Ciconiidae
White Stork
Ciconia ciconia
Ciconiiformes
Threskiornithidae
Scarlet Ibis
Eudocimus ruber
HB
Falconiformes
Sagittariidae
Secretary Bird
Sagittarius serpentarius
HB
Galliformes
Megapodiidae
Australian Brush-turkey
Alectura lathami
HB
Galliformes
Cracidae
Razor-billed Curassow
Mitu tuberosa
HB
Galliformes
Cracidae
Horned Guan
Oreophasis Derbianus
HB
Galliformes
Meleagridae
Wild Turkey
Meleagris gallopavo
HB
Galliformes
Tetraonidae
Black Grouse
Tetrao tetrix
HB
Galliformes
Odontophoridae
California Quail
Callipepla californica
HB
Galliformes
Phasianidae
Peafowls
Pavo sp.
HB
Galliformes
Numididae
Helmeted Guineafowl
Numida meleagris
HB
Gruiformes
Turnicidae
Barred Buttonquail
Turnix suscitator
HB
Gruiformes
Gruidae
Demoiselle Crane
Anthropoides Virgo
HB
Gruiformes
Aramidae
Limpkin
Aramus guarauna
HB
Gruiformes
Psophiidae
Gray-winged Trumpeter
Psophia crepitans
HB
Gruiformes
Eurypygidae
Sunbittern
Eurypyga Helias
HB
Charadriiformes
Jacanidae
Wattle Jacana
Jacana jacana
HB
Charadriiformes
Ibidorhynchidae
Ibisbill
Ibidorhyncha struthersii
HB
Charadriiformes
Recurvirostridae
Avocet
Recurvirostra avosetta
HB
Charadriiformes
Scolopacidae
Common Redshank
Tringa totanus
HB
Charadriiformes
Thinocoridae
Rufous-bellied Seedsnipe
Attagis gayi
HB
Pterocliformes
Pteroclididae
Namaqua Sandgrouse
Pterocles namaqua
HB
Cuculiformes
Cuculidae
White-browed Coucal
Centropus superciliosus
HB
Coraciiformes
Upupidae
Hopooe
Upupa epops
HB
Appendix 155
Order
Family
Common name
Scientific name
Bobbing
Feeding
source
Feeding
method
Group
size
Activity
Habitat
Flying
abilities
Predator
pressure
Podicipediformes
Podicipedidae
Great Crested Grebe
Podiceps cristatus
HB
Gruiformes
Rallidae
Common Moorhen
Gallinula chloropus
HB
Ciconiiformes
Ardeidae
Gray Heron
Ardea cinerea
HB
Columbiformes
Columbidae
Rock dove
Columba livia
HB
Struthioniformes
Struthionidae
Ostrich
Struthio camelus
HB*
Rheiformes
Rheidae
Greater Rhea
Rhea americana
HB*
Casuariiformes
Dromaiidae
Australian Emu
HB*
Gruiformes
Otididae
Kori Bustard
Ardeotis kori
HB*
Charadriiformes
Haematopodidae
Oystercatcher
Haematopus ostralegus
HB*
Charadriiformes
Charadriidae
Northen Lapwing
Vanellus vanellus
HB*
Charadriiformes
Charadriidae
Little ringed Plover
Charadrius dubius
HB*
Sphenisciformes
Spheniscidae
Humboldt Penguin
Spheniscus humboldti
NB
Gaviiformes
Gaviidae
Common Loon
Gavia immer
NB
Pelecaniformes
Pelecanidae
Great White Pelican
Pelecanus omocrotalus
NB
Pelecaniformes
Sulidae
Northern Gannet
Morus bassanus
NB
Pelecaniformes
Phalacrocoracidae
Great Cormorant
Phalacrocorax carbo
NB
Ciconiiformes
Ciconiidae
Marabou
Leptoptilos crumeniferus
NB
Ciconiiformes
Balaenicipitidae
Shoebill
balaeniceps rex
NB
Phoenicopteriformes
Phoenicopteridae
Greater Flamingo
Phoenicopterus roseus
NB
Anseriformes
Anhimidae
Common teal
Anas rubripes
NB
Falconiformes
Cathartidae
Black Vulture
Coragyps atratus
NB
Falconiformes
Pandionidae
Osprey
Pandion haliaetus
NB
Falconiformes
Accipitridae
Eagles
Aquila sp.
NB
Falconiformes
Accipitridae
Cinereous Harrier
Circus cinereus
NB
Falconiformes
Accipitridae
Cinereous Vulture
Aegypius monachus
NB
Falconiformes
Falconidae
Eurasian Krestel
Falco tinnunculus
NB
Gruiformes
Rhynochetidae
Kagu
Rhynochetos jubatus
NB
Charadriiformes
Burhinidae
Stone-curlew
Burhinus oedicnemus
NB
Charadriiformes
Stercorariidae
Great Skua
Stercorarius skua
NB
Charadriiformes
Laridae
Gulls
Larus sp.
NB
Charadriiformes
Sternidae
Inca Tern
Larosterna inca
NB
Appendix 156
Order
Family
Common name
Scientific name
Bobbing
Feeding
source
Feeding
method
Group
size
Activity
Habitat
Flying
abilities
Predator
pressure
Charadriiformes
Alcidae
Atlantic Puffin
Fratercula arctica
NB
Cuculiformes
Cuculidae
Greater Roadrunner
Geococcyx californianus
NB
Coraciiformes
Brachypteraciidae
Pitta-like Ground-roller
Atelornis pittoides
NB
Coraciiformes
Bucerotidae
Southern Ground-hornbill
Bucorvus leadbeateri
NB
Anseriformes
Anhimidae
Southern Screamer
Chauna torquata
NB
Anseriformes
Anhimidae
Harlequin Duck
Histrionicus histrionicus
NB
Pelecaniformes
Phaethontidae
Red-tailed Tropicbird
Phaeton rubricauda
BB
Cuculiformes
Cuculidae
Crested Coua
Coua cristata
BB
Coliiformes
Coliidae
Blue-naped Mousebird
Urocolius macrourus
BB
Piciformes
Capitonidae
Red-and-yellow Barbet
Trachyphonus erythrocephalus
BB
Piciformes
Ramphastidae
Keel-billed Toucan
Ramphastos sulfuratus
BB
Piciformes
Picidae
Green Woodpecker
Picus viridis
BB
LEGEND
Feeding source:
0 = small molluscs
1 = Fruits, leaves, seeds, small vertebrates,
invertebrates, insects, etc.
2 = small fishes, squid, crustaceans
3 = small vertebrates, reptiles, frogs
4 = vertebrates: birds and small mammals
5 = carrion
Feeding method:
1 = foraging or wading
2 = collecting in trees and bushes
3 = diving in water
4 = stalking and spearing
5 = hunting and searching from the air
6 = digging and scooping
7 = filtering
Habitat:
1 = savannah and other open woodlands
2 = forests
3 = swamps, marshes and muddy shores
4 = lakes and rivers
5 = see, ocean and coastal areas
Flying ability:
0 = terrestrial
1 = fly short distances (awkward)
2 = normal flyer
3 = elegant and skilled.
Group size:
0 = solitary or pairs
1 = small groups (from 2 to 10 birds)
2 = big groups (up to 10 birds)
Activity:
1 = nocturnal
2 = crepuscular
3 = diurnal
Predator pressure:
0 = low predator pressure
1 = medium pressure
2 = high predator pressure
Bobbing Style:
HB = head-bobbing
BB = body-bobbing
NB = non-bobbing
Table C-3: Analysis of the ecological and behavioural characteristics of HB and NB birds: feeding source, feeding method, group size, habitat, flying abilities,
and predator pressure.
References 157
REFERENCES
Alcock, J. (1997). Adaptative response to predators. In Animal Behaviour: an

evolutionary approach (6th edition). Massachusset: Sinauer associates.
Alonso, Y. (1998). Lateralization of visual guided behaviour during feeding in zebra
finches (Taeniopygia guttata). Behavioural Processes, 43(3), 257-263.
Andrew, R. J. (1988). The development of visual lateralization in the domestic chick.
Behav Brain Res, 29(3), 201-209.
Andrew, R. J., & Dharmaretnam, M. (1993). Lateralization and strategies of viewing in
the domestic chick. In H. P. Zeigler & H. J. Bischof (Eds.), Vision, brain and
behavior in Birds (pp. 319-332). Cambridge: the Mit Press.
Bagnoli, P., Grassi, S., & Magni, F. (1980). A direct connection between visual Wulst
and Tectum opticum in the pigeon (Columba livia) demonstrated by horseradish
peroxidase. Arch Ital Biol, 118(1), 72-88.
Baran-Marescot, M. (2005). Birds of the world. New York: Harry N Abrams.
Bell, G. A., & Gibbs, M. E. (1979). Interhemispheric engram transfer in chick. Neurosci
Lett, 13(2), 163-168.
Beritov, I. S., & Chichinadse. (1935). Localisation of visual perception in the pigeon.
bulletin de biologie et de mdicine exprimentale, 11, 103-104.
Bischof, H. J., & Watanabe, S. (1997). On the structure and function of the tectofugal
visual pathway in laterally eyed birds. European Journal of Morphology, 35, 246254.
Bloch, S., Jaeger, R., Lemeignan, M., & Martinoya, C. (1988). Correlation between
ocular saccades and head movements in walking pigeons. Journal of Physiology,
406: 1-2 July(July), 173.
Bloch, S., Lemeignan, M., & Martinoya, C. (1987). Coordinated vergence for frontal
fixation, but independent eye movements for lateral viewing, in the pigeon. Eye
movements: from physiology to cognition, 48-56.
References 158
Bloch, S., & Martinoya, C. (1982a). Comparing frontal and lateral viewing in the pigeon.
I. Tachistoscopic visual acuity as a function of distance. Behav Brain Res, 5(3),
231-244.
Bloch, S., & Martinoya, C. (1982b). Specialization of visual function for different retinal
areas in the pigeon. In J. P. Erwert, R. R. Capranica & D. J. Ingle (Eds.), Advances
in Vertebrate Neuroethology (pp. 359-368). New York: Plehum Press.
Brooks, B., & Holden, A. L. (1973). Suppression of visual signals by rapid image
displacement in the pigeon retina: a possible mechanism for "saccadic"
suppression. Vision Res, 13(7), 1387-1390.
Budzynski, C. A., & Bingman, V. P. (2004). Participation of the thalamofugal visual
pathway in a coarse pattern discrimination task in an open arena. Behav Brain
Res, 153(2), 543-556.
Casperson, L. W. (1999). Head movement and vision in underwater-feeding birds of
stream, lake, and seashore. Bird Behaviour, 13, 31-46.
Catania, A. C. (1965). Interocular Transfer of Discriminations in the Pigeon. J Exp Anal
Behav, 47, 147-155.
Chu, P. C. (1995). Phylogenetic reanalyis of Strauch's osteological data set for the
Charadriiformes. Condor, 97, 174-196.
Clayton, N. (1992). Lateralization and unilateral transfer of spatial memory in marsh tits.
Journal of Comparative Physiology A, 171, 799-806.
Clayton, N., & Krebs, J. R. (1994). Lateralization and unilateral transfer of spatial
memory mash tits: are two eyes better than one? Journal of Comparative
Physiology A, 174, 769-773.
Clayton, N. S., & Krebs, J. R. (1994a). Hippocampal growth and attrition in birds
affected by experience. Proc Natl Acad Sci U S A, 91(16), 7410-7414.
Clayton, N. S., & Krebs, J. R. (1994b). memory for spatial and object-specific cues in
food-storing and non-storing birds. Journal of Comparative Physiology A, 174,
371-379.
Clements, J. F. (2000). Birds of the World: A Checklist (5th edition, 2004 update ed.):
Ibis Pub Co.
References 159
Collett, T. S. (1978). Peering-a locust behaviour pattern for obtaining motion parallax
information. J. exp. Biol., 76, 237-241.
Cooper, A., & Penny, D. (1997). Mass survival of birds across the Cretaceous-Tertiary
boundary: molecular evidence. Science, 275(5303), 1109-1113.
Cronin, T. W., Kinloch, M. R., & Olsen, G. H. (2005). Head-bobbing behavior in
foraging whooping cranes favors visual fixation. Curr Biol, 15(7), R243-244.
Daanje, A. (1951). On locomotory movements in birds and the intention movements
derived from them. Behaviour, 3, 48-96.
Dagg, A. I. (1977a). Running, Walking and Jumping: The Science of Locomotion.
London: Wykeham.
Dagg, A. I. (1977b). The walk of the Silver gull (Larus novaehollandiae) and of other
birds. Journal of Zoology, London, 182, 529-540.
Davies, M. N. O., & Green, P. R. (1988). Head-bobbing during walking, running and
flying: relative motion perception in the pigeon. Journal of Experimental Biology,
138, 71-91.
Davies, M. N. O., & Green, P. R. (1991). The adaptability of visuomotor control in the
pigeon during landing flight. Zool Jb Physiol, 95, 331-338.
Dawkins, M. S. (2002). What are birds looking at? Head movements and eye use in
chickens. Anim. Behaviour, 63, 991-998.
Deng, C., & Rogers, L. J. (2002). Factors affecting the development of lateralization in
chicks. In L. J. Rogers & R. J. Andrew (Eds.), Comparative Vertebrate
lateralization (pp. 206-246). Cambridge: Cabridge University Press.
Di Stefano, M., Kusmic, C., & Musumeci, D. (1987). Binocular interactions measured by
choice reaction times in pigeons. Behav Brain Res, 25(2), 161-165.
Diekamp, B., Hellmann, B., Troje, N. F., Wang, S. R., & Gntrkn, O. (2001).
Electrophysiological and anatomical evidence for a direct projection from the
nucleus of the basal optic root to the nucleus rotundus in pigeons. Neuroscience
Letters, 305, 103-106.
References 160
Diekamp, B., Prior, H., & Gntrkn, O. (1999). Functional lateralization,

interhemispheric transfer and position bias in serial reversal learning in pigeons
(Columbia livia). Anim. Cogn., 2, 187-196.
Diekamp, B., Regolin, L., Gntrkn, O., & Vallortigara, G. (2005). A left-sided
visuospatial bias in birds. Curr Biol, 15(10), R372-373.
Dunlap, K., & Mowrer, O. H. (1930). Head movements and eye functions of birds.
Journal of Comparative Psychology, 11, 99-113.
Ehrlich, D., & Saleh, C. N. (1982). Composition of the tectal and posterior commissures
of the chick (Gallus domesticus). Neurosci Lett, 33(2), 115-121.
Engelage, J., & Bischof, H. J. (1994). Visual wulst influences on flash evoked responses
in the ectostriatum of the zebra finch. Brain Res, 652(1), 17-27.
Ericson, P. G., Envall, I., Irestedt, M., & Norman, J. A. (2003). Inter-familial
relationships of the shorebirds (Aves: Charadriiformes) based on nuclear DNA
sequence data. BMC Evol Biol, 3(1), 16.
Evans, C. S., & Evans, L. (1999). Chicken food calls are functionally referential. Anim
Behav, 58(2), 307-319.
Evans, C. S., Evans, L., & Marier, P. (1993). On the meaning of alarm calls: functional
references in the avian vocal system. Anim Behav, 46(1), 23-28.
Fernndez-Juricic, E., Erichsen, J. T., & Kacelnik, A. (2004). Visual perception and
social foraging in birds. Trends in ecology and evolution, 19(1), 25-31.
Flanders, M. (1985). Visually guided head movement in the African chameleon. Vision
Res, 25(7), 935-942.
Flanders, M. (1988). Head movement co-ordination in the African chameleon.
Neuroscience, 24(2), 511-517.
Folta, K., Diekamp, B., & Gntrkn, O. (2004). Asymmetrical modes of visual bottomup and top-down integration in the thalamic nucleus rotundus of pigeons. J
Neurosci, 24(43), 9475-9485.
Friedman, M. B. (1975). How birds use their eyes. Neural and endocrine aspect of
behaviour in birds, in Wright, P. Caryl, P.G. Wowles, M., 182-204.
References 161
Friedman, M. B. (1975b). Visual control of head movements during avian locomotion.

Nature, 255(5503), 67-69.
Frost, B. J. (1978). The optokinetic basis of head-bobbing in the pigeon. Journal of
Experimental Biology, 74, 187-195.
Frost, B. J., Cavanagh, P., & Morgan, B. (1988). Deep tectal cells in pigeons respond to
kinematograms. Journal of Comparative Physiology, 162, 639-647.
Fujita, M. (2002). Head bobbing and the movement of the centre of gravity in walking
pigeons (Columba Livia). J. Zool., Lond., 257, 373-379.
Fujita, M. (2003). Head bobbing and the body movement of little egrets ( Egretta
garzetta) during walking. J Comp Physiol A Neuroethol Sens Neural Behav
Physiol, 189(1), 53-58.
Fujita, M. (2004). Kinematic parameters of the walking of herons, ground-feeders, and
waterfowl. Comp Biochem Physiol A Mol Integr Physiol, 139(1), 117-124.
Galifret, Y. (1968). [The various functional areas of the retina of pigeons]. Z Zellforsch
Mikrosk Anat, 86(4), 535-545.
Gamlin, P. D., & Cohen, D. H. (1986). A second ascending visual pathway from the optic
tectum to the telencephalon in the pigeon (Columba livia). J Comp Neurol,
250(3), 296-310.
Garamszegi, L. Z., Moller, A. P., & Erritzoe, J. (2002). Coevolving avian eye size and
brain size in relation to prey capture and nocturnality. Proc Biol Sci, 269(1494),
961-967.
Gaston, K. E. (1984). Interocular transfer of pattern discrimination learning in chicks.
Brain Res, 310(2), 213-221.
Goodale, M. A. (1982). Visuomotor organization of pecking in the pigeon. In J. P.
Erwert, R. R. Capranica & D. J. Ingle (Eds.), Advances in Vertebrate
Neuroethology (pp. 349-357). New York: Plehum Press.
Goodale, M. A. (1983). Visually guided pecking in the pigeon (Columba livia). Brain,
Behavior and Evolution, 22(1), 22-41.
References 162
Goodale, M. A., Ellard, C. G., & Booth, L. (1990). The role of image size and retinal
motion in the computation of absolute distance by the Mongolian gerbil (Meriones
unguiculatus). Vision Res, 30(3), 399-413.
Goodale, M. A., & Graves, J. A. (1982). Interocular transfer in the pigeon: Retinal locus
as a factor. In D. Ingle, M. A. Goodale & R. Mansfield (Eds.), Advances in
analysis of visual behavior (pp. 211-240). London: MIT Press.
Green, P. R. (1998). Head orientation and trajectory of locomotion during jumping and
walking in domestic chicks. Brain, Behavior and Evolution, 51(1), 48-58.
Green, P. R., Davies, M. N., & Thorpe, P. H. (1992). Head orientation in pigeons during
landing flight. Vision Research, 32(12), 2229-2234.
Green, P. R., Davies, M. N. O., & Thorpe, P. H. (1994). Head-bobbing and head
orientation during landing flights of pigeons. Journal of Comparative Physiology,
174, 249-256.
Gntrkn, O. (1985). Lateralization of visually controlled behavior in pigeons. Physiol
Behav, 34(4), 575-577.
Gntrkn, O. (1997a). Avian visual lateralization: a review. NeuropReport, 8(6).
Gntrkn, O. (1997b). Morphological asymmetries of the tectum opticum in the pigeon.
Experimental Brain Research, 116, 561-566.
Gntrkn, O. (2002). Hemispheric Asymmetry in the Visual System of Birds. In K. D.
Hugdahl, R. J. (Ed.), Brain Asymmetry (pp. pp. 3-36). Cambridge: MIT Press.
Gntrkn, O. (2003). Hemispheric Asymmetry in the Visual System of Birds. In K. H.
R. j. Davidson (Ed.), The Asymmetrical Brain (pp. 4-36). London: MIT Press.
Gntrkn, O., & Bohringer, P. G. (1987). Lateralization reversal after intertectal
commissurotomy in the pigeon. Brain Res, 408(1-2), 1-5.
Gntrkn, O., Diekamp, B., Manns, M., Nottelmann, F., Prior, H., Schwarz, A., et al.
(2000). Asymmetry pays: visual lateralization improves discrimination success in
pigeons. Current Biology, 10(17), 1079-1081.
Gntrkn, O., & Hahmann, U. (1994). Visual acuity and hemispheric asymmetries in
pigeons. Behav Brain Res, 60(2), 171-175.
References 163
Gntrkn, O., & Hahmann, U. (1999). Functional subdivisions of the ascending visual
pathways in the pigeon. Behav Brain Res, 98(2), 193-201.
Gntrkn, O., Hellmann, B., Melsbach, G., & Prior, H. (1998). Asymmetries of
representation in the visual system of pigeons. Neuroreport, 9(18), 4127-4130.
Gntrkn, O., & Kesch, S. (1987). Visual lateralization during feeding in pigeons.
Behav Neurosci, 101(3), 433-435.
Gntrkn, O., Miceli, D., & Watanabe, M. (1993). Anatomy of the avian thalamofugal
pathway. In H. P. Zeigler & H. J. Bischof (Eds.), Vision, Brain, and Behavior in
Birds (pp. 115-135). Cambridge, MA: MIT Press.
Harlid, A., Janke, A., & Arnason, U. (1997). The mtDNA sequence of the ostrich and the
divergence between paleognathous and neognathous birds. Mol Biol Evol, 14(7),
754-761.
Harlid, A., Janke, A., & Arnason, U. (1998). The complete mitochondrial genome of
Rhea americana and early avian divergences. J Mol Evol, 46(6), 669-679.
Hart, N. S., Partridge, J. C., & Cuthill, I. C. (2000). Retinal asymmetry in birds. Curr
Biol, 10(2), 115-117.
Hayes, B. (1982). The structural organization of the pigeon retina. In N. Osborne & G.
Chader (Eds.), Progress in retinal research (Vol. 1). Oxford: Pergamon press.
Hodos, W., & Erichsen, J. T. (1990). Lower-Field Myopia in Birds an Adaptation That
Keeps the Ground in Focus. Vision Research, 30(5), 653-658.
Horn, G. (1991). Imprinting and recognition memory: A review of neural mechanisms. In
R. J. Andrew (Ed.), Neural and Behavioral Plasticity: The Domestic Chick as a
Model (pp. 219-261). Oxford: Oxford University Press.
Hughes, J. M. (1996). Phylogenetic analysis of the cuculidae (aves, cuculidae) using
behavioral, and ecological characters. The Auk, 112(1), 10-22.
Hughes, J. M., & Baker, A. J. (1999). Phylogenetic relationships of the enigmatic hoatzin
(Opisthocomus hoazin) resolved using mitochondrial and nuclear gene sequences.
Mol Biol Evol, 16(9), 1300-1307.
Husband, S., & Shimizu, T. (2001). Evolution of the avian visual system. In R. G. Cook
(Ed.), Avian visual cognition. On line: www.pigeon.psy.tufts.edu/avc/husband.
References 164
Husband, S., & Shimizu, T. (1999). Efferent projections of the ectostriatum in the pigeon
(Columba livia). Journal of Comparative Neurology, 406(3), 329-345.
Hyde, P. S., & Knudsen, E. I. (2002). The optic tectum controls visually guided adaptive
plasticity in the owl's auditory space map. Nature, 415(6867), 73-76.
Jarvis, E. D., Gntrkn, O., Bruce, L., Csillag, A., Karten, H., Kuenzel, W., et al.
(2005). Avian brains and a new understanding of vertebrate brain evolution. Nat
Rev Neurosci, 6(2), 151-159.
Jonsson, L. (1999). Birds of Europe: With North Africa and the Middle East. London:
Chistopher Helm.
Karten, H. J., & Hodos, W. (1970). Telencephalic projections of the nucleus rotundus in
the pigeon (Columba livia). Journal of Comparative Neurology, 140, 35-52.
Karten, H. J., Hodos, W., Nauta, W. J., & Revzin, A. M. (1973). Neural connections of
the "visual wulst" of the avian telencephalon. Experimental studies in the piegon
(Columba livia) and owl (Speotyto cunicularia). J Comp Neurol, 150(3), 253-278.
Karten, H. J., & Shimizu, T. (1989). The origins of the neocortex: Connections and
lamination as distinct events in evolution. Journal of Cognitive Neuroscience, 1,
291-301.
Keysers, C., Diekamp, B., & Gntrkn, O. (2000). Evidence for physiological
asymmetries in the intertectal connections of the pigeon (Columba livia) and their
potential role in brain lateralisation. Brain Research, 852(2), 406-413.
Kral, K. (1998). Side-to-sie head movements to obtain motion depth cues: A short review
a researach on the praying mantis. Behavioral processes, 43, 71-77.
Kral, K. (2003). Behavioural-analytical studies of the role of head movements in depth
perception in insects, birds and mammals. Behav Processes, 64(1), 1-12.
Land, M. F. (1999). Motion and vision: why animals move their eyes. Journal of
Comparative Physiology A Sensory Neural & Behavioral Physiology, 185, 341352.
LeBas, N. R., & Marshall, N. J. (2000). The role of colour in signalling and male choice
in the agamid lizard Ctenophorus ornatus. Proc Biol Sci, 267(1442), 445-452.
References 165
Lehrer, M., Srinivasan, M., Zhang, S., & Horridge, G. (1988). Motion cues provide bee's
visual world with a third dimension. Nature, 332, 356-357.
Levine, J. (1945a). Studies in the interrelations of central nervous structures in binocular
vision: I. The lack of bilateral transfer of visual discriminative habits acquired
monocularly by the pigeons. The Journal of Genetic Psychology, 67, 105-129.
Levine, J. (1945b). Studies in the interrelations of central nervous structures in binocular
vision: II. The conditions under which interocular transfer of discriminative habits
takes place in the pigeon. The Journal of Genetic Psychology, 67, 131-142.
Levine, J. (1952). Studies in the interrelations of central nervous structures in binocular
vision: III. Localization of the memory trace as evidenced by the lack of inter- and
intraocular habit transfer in pigeons. The Journal of Genetic Psychology, 81, 131142.
Mallin, H. D., & Delius, J. (1983). Inter- and intraoccular transfer of colour
discriminations with mandibulation as an operant in the head-fixed pigeon.
Behaviour Analysis Letters, 3, 297-309.
Manns, M., & Gntrkn, O. (1999). 'Natural' and artificial monocular deprivation
effects on thalamic soma sizes in pigeons. Neuroreport, 10(15), 3223-3228.
Mariani, A. P. (1982). Association amacrine cells could mediate directional selectivity in
pigeon retina. Nature, 298(5875), 654-655.
Mariani, A. P. (1987). Neuronal and synaptic organization of the outer plexiform layer of
the pigeon retina. Am J Anat, 179(1), 25-39.
Martin, G. R. (1993). Producing the image. In H. P. Zeigler, & Bischof, H. J. (Ed.),
Vision, brain, and behavior in birds (pp. 5-25). Cambridge, MA: MIT Press.
Martin, G. R., Ashash, U., & Katzir, G. (2001). Ostrich ocular optics. Brain Behav Evol,
58(2), 115-120.
Martin, G. R., & Brooke Mde, L. (1991). The eye of a procellariiform seabird, the Manx
shearwater, Puffinus puffinus: visual fields and optical structure. Brain Behav
Evol, 37(2), 65-78.
Martin, G. R., & Coetzee, H. (2004). Visual field in hornbills: precision-grasping and
sunshades. ibis, 146, 18-26.
References 166
Martin, G. R., & Katzir, G. (1993). Visual fields in the Stone-curlew Burhinus
oedicnemus. Ibis, 136, 448-453.
Martin, G. R., & Katzir, G. (1994). Visual fields and eye movements in herons
(Ardeidae). Brain Behav Evol, 44(2), 74-85.
Martin, G. R., & Katzir, G. (1995). Visual fields in ostriches. Nature, 374, 19-20.
Martin, G. R., & Katzir, G. (1999). Visual fields in Short-toed Eagles, Circaetus gallicus
(Accipitridae), and the function of binocularity in birds. Brain Behav Evol, 53(2),
55-66.
Martin, G. R., & Katzir, G. (2000). Sun shades and eye size in birds. Brain Behav Evol,
56(6), 340-344.
Martin, G. R., & Young, S. R. (1983). The retinal binocular field of the pigeon (Columba
livia: English racing homer). Vision Research, 23(9), 911-915.
Martinoya, C., Rivaud, S., & Bloch, S. (1983). Comparing frontal and lateral viewing in
the pigeon. II. Velocity thresholds for movement discrimination. Behav Brain Res,
8(3), 375-385.
McKenzie, R., Andrew, R. J., & Jones, R. B. (1998). Lateralization in chicks and hens:
new evidence for control of response by the right eye system. Neuropsychologia,
36(1), 51-58.
Mench, J. A., & Andrew, R. J. (1986). Lateralization of a food search task in the
domestic chick. Behav Neural Biol, 46(2), 107-114.
Miceli, D., Reperant, J., Villalobos, J., & Dionne, L. (1987). Extratelencephalic
projections of the avian visual Wulst. A quantitative autoradiographic study in the
pigeon Columbia livia. J Hirnforsch, 28(1), 45-57.
Mihara, M., & Watanabe, S. (1982). Interocular transfer of cardiac conditioning in the
pigeon. Behav Brain Res, 4(4), 411-416.
Morgan, B., & Frost, B. J. (1981). Visual response characteristics of neurons in nucleus
of basal optic root in pigeons. Experimental Brain Research, 42, 181-188.
Nicol, A. U., Brown, M. W., & Horn, G. (1995). Neurophysiological investigations of a
recognition memory system for imprinting in the domestic chick. European
Journal of Neuroscience, 7(4), 766-776.
References 167
Nottelmann, F., Wohlschlager, A., & Gntrkn, O. (2002). Unihemispheric memory in

pigeons-knowledge, the left hemisphere is reluctant to share. Behav Brain Res,
133(2), 309-315.
Nye, P. W. (1973). On the functional differences between frontal and lateral visual fields
of the pigeon. Vision Res, 13(3), 559-574.
Parsons, C. H., & Rogers, L. J. (1993). Role of the tectal and posterior commissures in
lateralization of the avian brain. Behav Brain Res, 54(2), 153-164.
Patterson, T. A., Gilbert, D. B., & Rose, S. P. (1990). Pre- and post-training lesions of the
intermediate medial hyperstriatum ventrale and passive avoidance learning in the
chick. Exp Brain Res, 80(1), 189-195.
Pearlman, A. L., & Hughes, C. P. (1976). Functional role of efferents to the avian retina.
I. Analysis of retinal ganglion cell receptive fields. J Comp Neurol, 166(1), 111122.
Perrins, D. (1991). The photographic guide to birds of the world. New York: Reed
Unternational Books Limited.
Peterson, R. M. G., & Hollon, P. A. D. (1983). A field guide to the birds of Britain and
Europe.
Poteser, M., & Kral, K. (1995). The significance of head movements in distance
discrimination in praying mantis larvae. J Exp Biol, 198(Pt 10), 2127-2137.
Poteser, M., Pabst, M., & Kral, K. (1998). Proprioceptive contribution to distance
estimation by motion parallax in a praying mantid. J Exp Biol, 201 (Pt 9), 14831491.
Pratt, D. W. (1982). Saccadic eye movements are coordinated with head movements in
walking chickens. Journal of Experimental Biology, 97, 217-223.
Prior, H., & Gntrkn, O. (2001). Parallel working memory for spatial location and
food-related object cues in foraging pigeons: binocular and lateralized monocular
performance. Learn Mem, 8(1), 44-51.
Prior, H., Lingenauber, F., Nitschke, J., & Gntrkn, O. (2002). Orientation and
lateralized cue use in pigeons navigating a large indoor environment. J Exp Biol,
205(Pt 12), 1795-1805.
References 168
Prior, H., Wiltschko, R., Stapput, K., Gntrkn, O., & Wiltschko, W. (2004). Visual
lateralization and homing in pigeons. Behav Brain Res, 154(2), 301-310.
Remy, M., & Emmerton, J. (1991a). Behavioral spectral sensitivities of different retinal
areas in pigeons. Behav Neurosci, 103(1), 170-177.
Remy, M., & Emmerton, J. (1991b). Directional dependence of intraocular transfer of
stimulus detection in pigeons (Columba livia). Behav Neurosci, 105(5), 647-652.
Remy, M., & Gntrkn, O. (1991). Retinal afferents to the tectum opticum and the
nucleus opticus principalis thalami in the pigeon. J Comp Neurol, 305(1), 57-70.
Remy, M., & Watanabe, S. (1993). Two eyes and One World: Studies of Interocular and
Intraocular Transfer in Birds. In H. P. Zeigler & H. J. Bischof (Eds.), Vision, brain
and behavior in Birds (pp. 333-350). Cambridge: the Mit Press.
Roberts, W. A., Phelps, M. T., Macuda, T., Brodbeck, D. R., & Russ, T. (1996).
Intraocular transfer and simultaneous processing of stimuli presented in different
visual fields of the pigeon. Behav Neurosci, 110(2), 290-299.
Rogers, L. J. (2000). Evolution of hemispheric specialization: advantages and
disadvantages. Brain Lang, 73(2), 236-253.
Rogers, L. J. (2002). Advantages and disadvantages of lateralization. In L. J. Rogers & R.
J. Andrew (Eds.), Comparative Vertebrate lateralization (pp. 126-153).
Cambridge: Cabridge University Press.
Rogers, L. J., & Andrew, R. J. (2002). Comparative Vertebrate lateralization.
Cambridge: Cabridge University Press.
Rogers, L. J., Zucca, P., & Vallortigara, G. (2004). Advantages of having a lateralized
brain. Proc Biol Sci, 271 Suppl 6, S420-422.
Saleh, C. N., & Ehrlich, D. (1984). Composition of the supraoptic decussation of the
chick (Gallus gallus). A possible factor limiting interhemispheric transfer of visual
information. Cell Tissue Res, 236(3), 601-609.
Sandi, C., Patterson, T. A., & Rose, P. R. (1993). Visual input and lateralization of brain
function in learning in the chick. Neuroscience, 52(2), 393-401.
References 169
Shimizu, T., Cox, K., & Karten, H. J. (1995). Intratelencephalic projections of the visual
wulst in pigeons (Columba livia). Journal of Comparative Neurology, 359(4),
551-572.
Shimizu, T., & Karten, H. J. (1991). Central visual pathways in reptiles and birds:
Evolution of the visual system. In J. Cronly-Dillon & R. Gregory (Eds.), Vision
and Visual Disfuction, Vol 2: Evolution of the eye and visual system (pp. 421441). London: Macmillan Press.
Shimizu, T., & Karten, H. J. (1993). The avian visual system and the evolution of the
neocortex. In H. P. Zeigler, & Bischof, H. J. (Ed.), Vision, brain, and behavior in
birds (pp. 103-114). Cambridge, MA: MIT Press.
Sibley, C. G., & Ahlquist, J. E. (1990). Phylogeny and classification of birds: a study in
molecular evolution. New Haven and London: Yale University Press.
Sibley, C. G., Ahlquist, J. E., & Monroe, B. L. (1988). A classification of the living birds
of the world based on DNA-DNA hybridation studies. The AUK, 105(3), 409-423.
Simpson, J. I. (1984). The accessory optic system. Annual Review of Neuroscience, 7, 1341.
Skiba, M., Diekamp, B., Prior, H., & Gntrkn, O. (2000). Lateralized interhemispheric
transfer of color cues: evidence for dynamic coding principles of visual
lateralization in pigeons. Brain & Language, 73(2), 254-273.
Stevens, J. V., & Kirsch, W. R. (1980). Interocular transfer in pigeons of color
discrimination but not motor response training. Animal Learning & Behavior,
8(1), 17-21.
Stevens, J. V., & Klopfer, F. (1977). Interocular transfer of conditioning and extinction in
birds. Journal of comparative and physiological psychology, 91(5), 1074-1081.
Stevenson, T., & Fanshawe, J. (2001). Field Guide to the Birds of East Africa: Kenya,
Tanzania, Uganda, Rwanda, Burundi. London: Princeton University Press.
Tommasi, L., & Vallortigara, G. (2001). Encoding of geometric and landmark
information in the left and right hemispheres of the Avian Brain. Behav Neurosci,
115(3), 602-613.
References 170
Torr, G. A., & Shine, R. (1994). An ethogram for the small scincid lizar. AmphibiaReptilia, 15, 21-34.
Troje, N. F., & Frost, B. J. (1999). Evidence for active vision during the thrust-phase of
the pigeon's head-bobbing. Paper presented at the Ninth Annual Meeting of the
Canadian Society for Brain, Behaviour, and Cognitive Science.
Troje, N. F., & Frost, B. J. (2000). Head-bobbing in pigeons: How stable is the hold
phase? Journal of Experimental Biology, 203, 935-940.
Ulrich, C., Prior, H., Duka, T., Leshchins'ka, I., Valenti, P., Gntrkn, O., et al. (1999).
Left-hemispheric superiority for visuospatial orientation in homing pigeons.
Behav Brain Res, 104(1-2), 169-178.
Valenti, A., Sovrano, V. A., Zucca, P., & Vallortigara, G. (2003). Visual lateralisation in
quails (Coturnix coturnix). Laterality, 8(1), 67-78.
Vallortigara, G. (1992). Right hemisphere advantage for social recognition in the chick.
Neuropsychologia, 30(9), 761-768.
Vallortigara, G. (2000). Comparative neuropsychology of the dual brain: a stroll through
animals' left and right perceptual worlds. Brain Lang, 73(2), 189-219.
Vallortigara, G., Cozzutti, C., Tommasi, L., & Rogers, L. J. (2001). How birds use their
eyes: Opposite left-right specialization for the lateral and frontal visual hemifield
in the domestic chick. Curr Biol, 11(1), 29-33.
van der Willigen, R. F., Frost, B. J., & Wagner, H. (2002). Depth generalization from
stereo to motion parallax in the owl. J Comp Physiol A Neuroethol Sens Neural
Behav Physiol, 187(12), 997-1007.
van Tuinen, M., Sibley, C. G., & Hedges, S. B. (2000). The early history of modern birds
inferred from DNA sequences of nuclear and mitochondrial ribosomal genes. Mol
Biol Evol, 17(3), 451-457.
Verstappen, M., Aerts, P., & Van Damme, R. (2000). Terrestrial locomotion in the blackbilled magpie: kinematic analysis of walking, running and out-of-phase hopping.
Journal of Experimental Biology, 203 Pt 14, 2159-2170.
von Euler, F. (2001). Selective extinction and rapid loss of evolutionary history in the
bird fauna. Proc R Soc Lond B Biol Sci, 268(1463), 127-130.
References 171
von Fersen, L., & Gntrkn, O. (1990). Visual memory lateralization in pigeons.
Neuropsychologia, 28(1), 1-7.
Voss, J., & Bischof, H. J. (2003). Regulation of ipsilateral visual information within the
tectofugal visual system in zebra finches. J Comp Physiol A Neuroethol Sens
Neural Behav Physiol, 189(7), 545-553.
Wallace, G. K. (1959). Visual scanning in the desert locust schistocerca gregaria Forskal.
J. exp. Biol., 36, 512-525.
Watanabe, M., Ito, H., & Ikushima, M. (1985). Cytoarchitecture and ultrastructure of the
avian ectostriatum: afferent terminals from the dorsal telencephalon and some
nuclei in the thalamus. J Comp Neurol, 236(2), 241-257.
Watanabe, S. (1986). Interocular transfer of learning in the pigeon: visuo-motor
integration and separation of discriminanda and manipulanda. Behav Brain Res,
19(3), 227-232.
Weidner, C., Reperant, J., Miceli, D., Haby, M., & Rio, J. P. (1985). An anatomical study
of ipsilateral retinal projections in the quail using radioautographic, horseradish
peroxidase, fluorescence and degeneration techniques. Brain Res, 340(1), 99-108.
Westheimer, G., & Blair, S. M. (1974). Unit activity in the accessory optic system in alert
monkeys. Investigative Ophthalmology, 13, 533-534.
Wild, J. M. (1989). Pretectal and tectal projections to the homologue of the dorsal lateral
geniculate nucleus in the pigeon: an anterograde and retrograde tracing study with
cholera toxin conjugated to horseradish peroxidase. Brain Res, 479(1), 130-137.
Wohlschlger, A., Jger, R., & Delius, J. (1993). Head and Eye Movements in
Unrestrained Pigeons (Columba livia). Journal of Comparative Psychology,
107(3), 313-319.
Wylie, D. R., & Frost, B. J. (1990). The visual response properties of neurons in the
nucleus of the basal optic root of the pigeon: a quantitative analysis. Experimental
Brain Research, 82, 327-336.
Wylie, D. R. W., Bischof, W. F., & Frost, B. J. (1998). Common reference frame for
coding translational and rotational optic flow. Nature, 392, 278-282.
References 172
Wylie, D. R. W., Linkenhoker, B., & Lau, K. L. (1997). Projections of the nucleus of the
basal optic root in pigeons (Columba livia) revealed using biotinylated dextran
amine. Journal of Comparative Neurology, 384, 517-536.
Zeier, H. (1970). Lack of eye to eye transfer of an early response modification in birds.
Nature, 225(5234), 708-709.
Zeigler, H. P., & Bischof, H. J. (Eds.). (1993). Vision, brain, and behavior in birds.
Cambridge, MA: Mit Press.
Acknowledgements
I am very grateful to all the people who have helped me in innumerable ways through the past three
years of my PhD. I also would like to thank the protagonists of this work: the birds.
Professor Nikolaus F. Troje gave me the opportunity to work in this stimulating project, without
him, this work would have never been possible. I thank him for his enthusiasm, encouragement,
honesty, and bright ideas during this time.
I would like to thank Professor Onur Gntrkn for his wise advice, support, insights and
suggestions that helped me carry out the different studies of this work.
I am very thankful to the International Graduate School of Neuroscience (IGSN) of the RuhrUniversity Bochum, for providing everything that a PhD student may need: research and educational
opportunities, support, and funding.
Special thanks to the enthusiastic research assistants that helped collect the data. Katrin Stoppa and
Antigoni Marioli helped me with the pigeons training. The time we shared training the birds turned
into priceless data for my thesis and into fruitful friendships. Evgeny Bobrov did a wonderful
bibliographic search and helped to rank the birds characteristics. Luisa Moratalla patiently
organized and digitalized a great deal of the birds video collection.
Many thanks to all that participated in the construction of the experimental device. The workshop of
the Psychology department constructed the chamber; Thomas Jakubowski, programmed the first
version of the experimental arena software; Andre Meiske kept the computers and the data safe and
healthy. Special thanks to Tobias Otto who constructed and programmed the motion capture system
and developed a new software for the experimental arena. He helped me in so many aspects during
these three years that without him my live in Germany would be more complicated.
I am grateful to Elena Giakoumaki, Lea Soei, and Cord Westhoff for their valuable hints,
suggestions, and helpful comments on a preliminary version of my dissertation. In addition, I would
also like to thanks Cord Westhoff for his time, patient and brilliant sense of humor.
I am thankful to all members of the Biomotion Lab, Biopsychology department, and IGSN,
particularly to all who helped me on the background without being noticed: colleges, administration
staff, technicians, pigeon keepers, etc.
Thanks to my former adviser in Spain Dr. Pilar Herreros de Tejada, she introduced me to world of
science.
Juan M. Snchez Peral, my husband, taught me all I know about birds identification and
observation, without him the last part of this job would not have been possible: all my love for him.
My foremost thank to all that make my life extremely happy: my husband, parents, brothers,
nephews, Selim, and friends.
Curriculum Vitae
1. Personal Data:
Name:
Date of birth:
Place of birth:
Address:
Laura Jimnez Ortega

20.06.1975
Madrid, Spain
Inst. fr kognitive Neurowissenschaft
Fakultt fr Psychologie
Ruhr-Universitt-Bochum
44780 Bochum, Germany
2. Educational background:
- Primary school (1979-1990). Colegio J.A.B.Y.: Madrid

- High school (1990-1995). Instituto Palas Atenea: Madrid
- Degree in General Psychology (1995-1998). Universidad Complutense de Madrid
- Specialization in Cognitive Psychology (1998-2000). Universidad Complutense de Madrid
- M.Sc. Courses: Research Method in Psychology (2000-2001). University College of London
- Advanced research studies in Pshycology (2001). Universidad Complutense de Madrid
- PhD in Neuroscience: Fellowship (2003). International Graduate School of Neuroscience:
Ruhr-Universitt-Bochum
3. Research experience
- Research assistant (1998-1999). Universidad Complutense de Madrid, Department of
Psychobiology, Animal Visual Lab. Researching and teaching in animal behaviour
- Contrast sensibility function in mice (1999-2000). Universidad Complutense de Madrid,
Department of Psychobiology, Animal Visual Lab. Research project for the master thesis
- Research collaboration (September-December 2000). University College of London, Visual
Research Unit. Adult visual asymmetries using VEP
- Honorific collaborator in Psychobiology Department (January 2001-May 2002). Universidad
Complutense de Madrid, Department of Psychobiology, Animal Visual Lab. Electrophysiology in
rats and mice.

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Avian visual perception:

Interocular and intraocular transfer

A Dissertation submitted for

Laura Jimnez Ortega

Printed with permission of the International Graduate School of Neuroscience of the

2. GENERAL METHODS ...........................................................................................32

3. EXPERIMENT 1, 2 AND 3: INTRAOCULAR AND INTEROCULAR TRANSFER IN

4. EXPERIMENT 4: PATTERN RECOGNITION DURING HEAD-BOBBING: ARE

5. EXPERIMENT 5: WHY DO BIRDS BOB THEIR HEADS? ....................................82

6. GENERAL DISCUSSION .....................................................................................117

1.2 Intraocular and interocular transfer in pigeons

1.2.1 Intraocular transfer of information

1.2.2 Interocular transfer of information

1.2.3 Interim summary

1.3 Visual asymmetries in birds

1.3.1 Right eye/left hemisphere dominances

1.3.2 Left eye/right hemisphere dominances

1.3.3 Asymmetric interhemispheric transfer

1.4 Head-bobbing in birds

Horizontal displacement (pixels)

Head movement of a walking moorhen

1.4.1 Biomechanical function

1.4.2 Image stabilization

1.4.3 Motion parallax

1.4.4 Head-bobbing birds

1.5 Anatomical substrate

1.5.1 The avian eye

Figure 4: Avian retina. The photoreceptors, bipolar cells,

Figure 5: Schematic representation of the pigeons retina (modified from Galifret,

1.5.2.2 Tectofugal pathway

1.5.2.3 Tectofugal-thalamofugal projections

Lateral geniculate nucleus

1.5.2.4 The accessory optic system

1.5.3 Interim summary

1.6 Goals of this work

2.1 Experimental arena

2.2 Motion capture system

2.4 Training Procedure

Figure 10: Shapes presented in the discrimination task. From left to

Pigeon cross the

Reward in the back

Pigeon walks back

Pigeon walks towards

Pigeon walks towards

Figure 11: Diagram of the pigeons steps

Intraocular and Interocular Transfer in Pigeons 38

3.1 Experiment 1: Limits of intraocular transfer in pigeons I: frontal to lateral direction.

Intraocular and Interocular Transfer in Pigeons 39

Intraocular and Interocular Transfer in Pigeons 40

Intraocular and Interocular Transfer in Pigeons 41

Stimuli location (in cm)

3.1.2.1 Percentage of correct responses

Intraocular and Interocular Transfer in Pigeons 42

Intraocular and Interocular Transfer in Pigeons 43

Position of the screen (degrees)

Intraocular and Interocular Transfer in Pigeons 44

Position of the screen (degrees)

Position of the screen (degrees)

Intraocular and Interocular Transfer in Pigeons 45

3.1.2.2 Number of trials for achieving the criterion

Position of the screen (degrees)

Intraocular and Interocular Transfer in Pigeons 46

Intraocular and Interocular Transfer in Pigeons 47

Intraocular and Interocular Transfer in Pigeons 48

A 232 (visual fieldpresentationphase) within-subject ANOVA was calculated was

Individual 232 (visual fieldpresentationphase) analyses of the motion characteristics for

A 232 (visual fieldpresentationphase) within-subject ANOVA was also calculated with

A 232 (visual fieldpresentationphase) within-subject ANOVA was calculated with the