Spatial Vision in Birds: Anatomical investigation of spatial resolving power
Mitkus, Mindaugas

2015

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Mitkus, M. (2015). Spatial Vision in Birds: Anatomical investigation of spatial resolving power. [Doctoral Thesis(compilation)]. Department of Biology, Lund University.

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Spatial Vision in Birds
Anatomical investigation of spatial resolving power

Mindaugas Mitkus

DOCTORAL DISSERTATION
by due permission of the Faculty of Science, Lund University, Sweden.
To be publicly defended in the Blue Hall, Ecology Building,
Sölvegatan 37, Lund, Sweden, on the 9 th of October 2015, at 13:15,
for the degree of Doctor of Philosophy
Faculty opponent
Prof. Graham R. Martin, Centre for Ornithology, School of Biosciences,
University of Birmingham, UK

Organization

Document name

LUND UNIVERSITY
Department of Biology,
Sölvegatan 35, SE-22362,
Lund, Sweden

DOCTORAL DISSERTATION

Author(s) Mindaugas Mitkus

Sponsoring organization

Date of issue

Title and subtitle
Spatial Vision in Birds: Anatomical investigation of spatial resolving power
Abstract
Avian eyes are big both in relative and absolute terms, thus the importance of vision to birds is obvious. Even
though the general eye plan is rather conservative throughout the group, there is a great variation in visual
capabilities. In this thesis I present four studies on different aspects of spatial vision in parrots, procellariiform
seabirds and birds of prey. In Paper I we studied retinal ganglion cell topography and anatomical spatial resolution
in two Australian parrots, budgerigar and Bourke’s parrot, inhabiting open terrain. Differently than expected, we
did not find a horizontal visual streak, an elongated area of increased ganglion cell density, which would be
predicted by the “terrain theory”. In addition, we found that anatomical spatial resolution based on ganglion celldensity is lower than behaviourally determined visual acuity. In Paper II, we compared spatial resolution andoptical sensitivity in two procellariiform seabirds with contrasting nesting and foraging strategies. As predicted,
the Leach’s storm-petrel had lower visual acuity than the Northern fulmar, however similar optical sensitivity at
the level of single rod photoreceptor. Additionally, both species had a well-pronounced horizontal visual streakthat supports the “terrain theory”. In Paper III, we studied the development of the visual and olfactory system inthe Leach’s storm-petrel juveniles. Our results indicated, that fine-tuning of retinal ganglion cell topography does
not happen early in development, and that the ganglion cell layer continues to mature throughout the nest period.
In addition, we found that two-weeks old juveniles lack basic phototactic and optokinetic reflexes. In Paper IV weused transmission electron microscopy and immunohistochemistry to investigate the presence of double cones in
the foveae of the red kite, common buzzard, Eurasian sparrowhawk and peregrine falcon. The double cone-freezones in the central fovea differed in size between species. We also found double cone-free zone in the temporal
fovea of the common buzzard and peregrine falcon, but not in the Eurasian sparrowhawk. In three species of
raptors, in which we studied opsin expression, we found violet and green sensitive cones in the central fovea, andthus assume that raptors have all four types of single cones in the central fovea. These findings indicate, that single
cones, not double cones, mediate the high spatial resolution in the raptor fovea.
Key words: Vision, Visual ecology, Visual spatial resolution, Retinal ganglion cells, Development, Double cones,
Birds, Parrots, Seabirds, Raptors
Classification system and/or index terms (if any)
Supplementary bibliographical information

Language English

ISSN and key title

ISBN (Print)
978-91-7623-466-2

Recipient’s notes

Number of pages 122

Price

Security classification
I, the undersigned, being the copyright owner of the abstract of the above-mentioned dissertation, hereby grant to
all reference sources permission to publish and disseminate the abstract of the above-mentioned dissertation.

SignatureDate: 2015-08-25

Spatial Vision in Birds
Anatomical investigation of spatial resolving power

Mindaugas Mitkus© Mindaugas Mitkus
Faculty of Science
Department of Biology
ISBN (print) 978-91-7623-466-2
ISBN (pdf) 978-91-7623-467-9
Pictures and line art: Mindaugas Mitkus,
except where otherwise statedPrinted in Sweden by Media-Tryck, Lund University
Lund 2015

"The outcome of any serious research can only be
to make two questions grow,where only one grew before"
Thorstein Veblen

Contents

Original papers and manuscripts

9

Populärvetenskaplig sammanfattning (Summary in Swedish)11

Introduction

13

Chapter 1 Principles of Spatial Resolution
Diffraction limit and the optical cut-off frequency
Optical defects
Imperfect focus
Aberrations
Retinal sampling frequency
Sensitivity

15
15
17
17
18
19
21

Chapter 2 The Avian Eye
General structure
Optical system of the eye
RetinaPhotoreceptor layer
Other retinal layers
Retinal specialisations

25
25
26
29
29
30
31

Chapter 3 Development of the Eye
Development of the retina
Eye growth

33
33
35

Chapter 4 Measuring Spatial Resolution
Behavioural measurements
Electrophysiological measurements
Anatomical measurements

37
37
42
43

Concluding Remarks

47

References

51

Paper I59

Paper II75

Paper III91

Paper IV107

Original papers and manuscripts

Paper I Mitkus, M., Lind, O., Chaib, S. & Kelber, A. (2014) Retinal ganglion cell
topography and spatial resolution of two parrot species: budgerigar (Melopsittacus
undulatus) and Bourke’s parrot (Neopsephotus bourkii). J. Comp. Physiol. A 200,
371 – 384
Paper II Mitkus, M., Nevitt, G., Danielsen, J. & Kelber, A. Spatial resolution andoptical sensitivity of a DMS-responder and a non-responder: Leach's storm-petrel
and Northern fulmar. Manuscript, to be submitted to Functional Ecology
Paper III Mitkus, M., Nevitt, G. & Kelber, A. Development of the visual andolfactory system in Leach’s storm-petrel nestlings. Manuscript
Paper IV Mitkus, M., Olsson, P., Toomey, M., Corbo, J. & Kelber, A. The
central fovea of raptors lacks double cones. Manuscript, to be submitted to Journalof Comparative Neurology
Paper I is reprinted with permission from the publisher.

Author contributions
Paper I MM performed 90% of the lab work, developed methods, analysed mostof the data and wrote the manuscript with feedback from OL and AK.
Paper II MM planned and performed the experiments with some contributions
from AK and JD, analysed all data and wrote the manuscript with feedback from
AK, JD and GN.
Paper III MM planned and performed the experiments with some contributions
from AK, analysed all data and wrote the manuscript with feedback from AK andGN.
Paper IV MM had the idea for the project, planned it in collaboration with AK,
MT, PO and JC, did the sampling and TEM work with contributions from PO,
analysed data and contributed to writing the manuscript together with the otherauthors.
9

Papers, which are not part of the thesis:
Lind, O., Sunesson, T., Mitkus, M. & Kelber, A. (2012) Luminance dependenceof spatial vision in budgerigars (Melopsittacus undulatus) and Bourke’s parrots(Neopsephotus Bourkii). J. Comp. Physiol. A 198, 69-77
Lind, O., Mitkus, M., Olsson, P. & Kelber, A. (2013) Ultraviolet sensitivity andcolour vision in raptor foraging. J. Exp. Biol. 216, 1819-1826
Lind, O., Mitkus, M., Olsson, P. & Kelber, A. (2014) Ultraviolet vision in birds:
the importance of transparent eye media. Proc. R. Soc. B 2014 281, 20132209, 1-9

10Populärvetenskaplig sammanfattning(Summary in Swedish)Fåglar har fascinerat människor i århundraden. Färgen på deras fjädrar, deras
flyghöjd och deras förmåga att fånga små byten har skapat den allmänna
uppfattningen att fåglar har en fantastisk syn. Föreställningen att fåglar har
skarpare syn än människor är väletablerad hos jägare och fiskare och finns att hitta
i litteraturen. Det finns emellertid tusentals fågelarter och deras synförmåga skiljer
sig åt. Idag känner man endast till några få rovfåglar som kan se finare detaljer –spatial upplösning – än människor. I den här avhandlingens kappa ger jag enöversikt av de teoretiska begränsningarna för spatial upplösning och hur denna
egenskap kan mätas, och jag ger en bild av mångfalden av fågelögon och deras
utveckling. Sammanlagt lägger jag fram fyra originalstudier om fåglars näthinnaoch spatiala upplösning.
I den första studien undersökte vi två papegojor, undulater och bourkesparakiter.
Dessa papegojor lever i ett öppet landskap i centrala Australien och vi förväntade
oss att de skulle ha ett brett lateralt område av skarp syn i näthinnan för att i detalj
kunna övervaka händelser utmed horisonten. Det hade de emellertid inte. Vi
upptäckte även att de har relativt låg anatomisk synskärpa som inte stämmer
överens med uppskattningar av synskärpan från beteendestudier.
I den andra studien undersökte vi två petrellfåglar: klykstjärtad stormsvala ochstormfågel. Den klykstjärtade stormsvalan är en mindre, kryptiskt färgad fågel
som bygger bo i hålor och förlitar sig på luktsinnet för att hitta mat. Stormfågeln ären större och färgglad fågel som bygger bo i öppna landskap och är mindre
beroende av luktsinnet för att hitta mat. Våra resultat visar att stormfågeln har
skarpare syn som den kan använda för att hitta andra fåglar ute till havs. Dessutom
hade båda arter näthinnor med breda lateral områden för skarp syn, vilket man
kunde förvänta sig av fåglar som behöver upptäcka föremål utefter horisonten på
ett öppet hav.
I den tredje artikeln studerade vi hur syn- och luktsystemen utvecklas i den
klykstjärtade stormsvalans ungfåglar. Vi upptäckte att synen inte är
färdigutvecklad hos två veckor gamla ungar och näthinnan fortsätter att utvecklas
under hela tiden i boet. Vi visar även att ögonstorleken ökar lika mycket som
luktbulberna från två veckors ålder till mogen ålder.
11

I den sista studien letade vi efter dubbeltappar i fovean hos fyra rovfåglar.
Dubbeltappar antas vara de synceller som ger skarp syn och för denna funktion bör
dubbeltappar vara rikligt representerade. Vi hittade emellertid inga dubbeltappar iden centrala regionen av foveorna. Däremot hittade vi lila- och grönkänsliga
enkeltappar och antar att alla enkeltappar finns representerade i fovean hosrovfåglar. Således förmedlar enkelltappar, men inte dubbeltappar, hög spatial
upplösning hos rovfåglar.

12

Introduction

Animals have evolved various senses to extract information from the environment.
Sensory information is present in many forms including light, sound, vibration andothers, but only light delivers instantaneous information about the position of
objects and enables immediate long-distance interactions. Not surprisingly vision
is used to guide so many behaviours including locomotion, orientation, navigation,
prey detection, predator avoidance, communication and mate choice. For some ofthese behaviours coarse visual information is sufficient, but for others highprecision in detecting the direction of light is needed. Depending on the lifestyle,some animals cope well with coarse images, but others require high spatial
resolution.
Birds have fascinated humans for centuries. A long lasting notion that birds have
sharper vision than humans is common not only in the idle talks of hunters andfishermen, but can be also found in the text books. However, even though thebasic morphological plan of the avian eye is as uniform throughout the group as it
is in other vertebrates (Walls 1942), the great deal of variation exists in its
function, and especially so in its spatial resolving power. To date only someraptorial birds are known to possess higher spatial resolution than humans do(Fischer 1969, Reymond 1985, 1987), whereas some others have more than ten
times lower visual acuity (Harmening et al. 2009).
This thesis comprises four chapters. Chapter 1 introduces theoretical principles,
which set the limit to the spatial resolution. Chapter 2 briefly overviews thediversity and morphology of avian eyes and Chapter 3 presents some knowledge
on avian eye development. In Chapter 4 several techniques used to measure spatial
resolution in birds are presented with the main emphasis on the anatomical
methods, which were used in Papers I, II, III and IV.
In Paper I we studied retinal ganglion cell topography and anatomical spatial
resolution in two parrot species, the budgerigar (Melopsittacus undulatus) and the
Bourke’s parrot (Neopsephotus bourkii). We discussed methodological issues indetail and compared the results with the behaviourally determined visual acuity
values obtained from the literature. In Paper II we investigated retinal ganglion
cell topography, anatomical spatial resolution and optical sensitivity in two
procellariiform seabirds with contrasting foraging strategies, the Leach’s stormpetrel (Oceanodroma leucorhoa) and the Northern fulmar (Fulmarus glacialis),and discussed the results from the perspective of foraging ecology. In Paper III we
13

compared the development of the visual and olfactory systems in the Leach’s
storm-petrel juveniles. Paper IV presents the result of the search of the double
cones in the central and temporal foveae of four raptor species, the common
buzzard (Buteo buteo), the Eurasian sparrowhawk (Accipiter nisus), the red kite
(Milvus milvus) and the peregrine falcon (Falco peregrinus).

14

Chapter 1 Principles of Spatial
Resolution

Both, evolution and technology have to follow the same rules of physics. Having
had a camera in your hands helps to understand the basic working principles andstructure of an eye. Resolution and sensitivity are two main properties of any typeof eye or camera. Interestingly, the wave nature of light sets the limit to theresolution and the quantum nature of light limits the sensitivity. The trade-off
between these two sides of the light is what determines the structure of an eye.

Diffraction limit and the optical cut-off frequency
The main point in understanding spatial resolution is that the image of a point is
not a point. Due to the wave nature of light, the image of a distant point lightsource, such as a star, falls on a retina as a pattern of a specific light intensity
distribution. This optical phenomenon known as diffraction sets the ultimate limit
to spatial resolution.
The parallel rays of light coming from a distant object may be more accurately
considered as the propagation of a flat wavefront. When passing through the lens,
the peripheral parts of the wavefront have to cross less optical material than thecentral part, which therefore gets delayed. This results in refraction - the wavefront
becomes curved (Fig. 1.1a). Refracted light continues to the focal point, where
different parts of the same wavefront meet. Because some light was delayed in thelens, different components of the wavefront arrive at the focal point in different
phases. Those parts, which are in phase, interact constructively and reinforce eachother, while other parts, which are out of phase, interact destructively and cancel
each other out. This phenomenon of interference results in a diffraction pattern,which, if light passed through a circular aperture, has a central bright spotsurrounded by a series of alternating dark and bright rings (Fig. 1.1b). Thus, thepoint of light is no longer a point.

15

b

a
wavefront

focal point

lensFig. 1.1. The light from a distant point source propagates as a flat wavefront. a - When passing
through a lens the light is refracted and focused to the focal point. b - The image of the point source
is not a point, but, if passed through a circular aperture, a diffraction pattern known as the Airy disc.
(b courtesy of Wikimedia Commons)

The central bright spot of the diffraction pattern is known as Airy disc. The width() of the bright spot at its half maximum intensity is used as a measure of the
Airy disc (Land and Nilsson 2012). Its angular size (expressed here in radians)
depends on the wavelength of light () and the diameter of the aperture (D):
 = /D.

[1]

The larger this spot, the more blurred is the image of the distant point. If the imageof any other object is smaller than approximately the half width of the Airy disc, itis blurred out (Land and Nilsson 2012). Thus the finest spatial frequency(expressed in cycles/radian) that the optics can pass is the reciprocal of the half
width of the Airy disc:co =1/  = D/.

[2]

This is also represented in the modulation (contrast) transfer function (MTF) (Fig.
1.2), which illustrates how the contrast in the image is attenuated when passing
through the optics. In an ideal optical system the highest spatial frequency, whichis passed, is indeed limited by diffraction. This equation indicates, that the larger
the pupil (and the lens) of the eye, the higher spatial resolution it can have.
However, larger lenses introduce other optical imperfections, which compromise
the spatial resolution of an eye.

16

Object

Image

ObjectImageContrast ratio

1

Ȟmax

Ȟco

0
0

Spatial frequency

1Fig. 1.2. The contrast transfer function. Because of diffraction, even the theoretically ideal lenses
convert a high contrast object into a lower contrast image. The contrast ratio between image andobject decreases as the detail in the object gets finer. At the optical cut-off frequency (co) there is nocontrast left in the image. The shaded area at the bottom of the figure illustrates how low photon
numbers limit the maximum spatial frequency (max) to the fraction of the cut-off frequency (co) at
low light levels. The contrast between black and white stripes of the grating pattern is defined as thedifference of their intensities divided by their sum: Contrast = (Imax-Imin)/(Imax+Imin). (Modified fromLand and Nilsson 2012)

Optical defects
Apart from the main optical limitation intrinsic to the nature of light, there areother optical problems, which can degrade the image on its way to the retina. The
most common and important are defocus, spherical and chromatic aberrations.

Imperfect focus
Objects in a 3D world are in different distances from the eye. Because nearby
objects are brought to a focus further from the lens than distant objects, many eyes
have to have a mechanism of accommodation. In fish, which have non-flexible
lenses, accommodation is achieved by moving the lens further away or closer to
17

a

Focus
defectb

Spherical
aberrationc

Chromatic
aberration

Fig. 1.3. Optical imperfections. a - Image is focused behind the focal plane. b - Spherical aberration– the light, which passes further away from the optical axis, is focused closer to the focal plane thanthe light passing near the axis. c - Chromatic aberration – even if entering the lens at a same
position, light of short wavelengths (blue) is refracted more strongly than light of long wavelengths(red).

the retina. Other vertebrates can change the refractive power of the lens or cornea,
or both, by changing the curvature of the refracting surfaces. If the image isrefracted too much or too little it will be focused in front or behind the retina, andthus will be blurred (Fig. 1.3a). Generally, small eyes with small apertures suffer
less from defocus, because small apertures provide larger depth of focus (DeValois and De Valois 1990).

Aberrations
In lenses with a short focal length, peripheral light has to be bent much more thanlight entering closer to the optical axis. In lenses with a spherical surface this is
hard to achieve, and peripheral rays are refracted too much resulting in sphericalaberration (Fig. 1.3b). One way to reduce this problem is to have a non-sphericallens. Indeed the front surface of the human lens is hyperbolic, while the rearsurface is parabolic (Martin 1983). Another solution to the problem is to have alens with a refractive index gradient, which is the case in many vertebrate species(Land and Nilsson 2012).
18

Another type of optical imperfection is longitudinal chromatic aberration, which
occurs because light of different wavelengths is refracted differently even if itenters a homogenous lens at the same point. Light of short wavelengths isrefracted more strongly than light of long wavelengths, which means that blue
light is focused closer to the lens than red light (Fig. 1.3c). To overcome thisproblem fish and some other vertebrates have evolved multifocal lenses (Kröger etal. 1999).
Both types of aberrations become more severe when the aperture is large relative
to the focal length. Thus while a large aperture in a large eye can help to reduce
diffraction, the large eye size itself cannot help to reduce aberrations. In a giveneye with a fixed focal length, the best image quality can be achieved whendiffraction blurring is about equal to the aberration blurring. Indeed, in humans,
pupil diameter can be changed from 2 to 8 mm (Land and Nilsson 2012), but thebest image quality in bright light is produced when the pupil is 2.4 mm in diameter(Miller 1979).

Retinal sampling frequency
According to the sampling theorem, a sampling system with N sampling units canfully resolve all spatial frequencies below N/2 (De Valois and De Valois 1990). In
other words, one sampling unit is needed for each node and antinode of asinusoidal grating, thus the number of sampling units needed is twice the spatial
frequency of the grating. To put it simply, a spatial frequency of for example 30
cycles/degree can be fully sampled by 60 sampling units per degree of visual
angle. Expressed in the opposite way, 60 sampling units in one degree of visual
angle can sample all spatial frequencies below 30 cycles/degree (De Valois and De
Valois 1990). How small do these sampling units, which can be simply called
photoreceptors, have to be to sample the spatial frequency at the optical cut-off
limit?
Each eye has a point, called a nodal point, that light passes through without being
bent (Fig. 1.4). The distance from the nodal point to the focal plane in the retina iscalled posterior nodal distance (PND, colloquially often simply called the focal
length). An object of a size O at a distance U, and the image of the object on theretina of a size I, then have the following relationship:
O/U = I/PND.

[3]

19

PND

U

1 cycle

dcc

I

ΔÞ

O

N

Fig. 1.4. Each eye has a nodal point N, that light passes through without being bent. The distancefrom the nodal point to the image plane is the Posterior Nodal Distance PND. The object O, at a
distance U from the nodal point, and its image I on the retina subtend the same angle
=O/U=I/PND. The angular separation between two adjacent receptors, packed in a square array,and sampling node and antinode of the sinusoidal grating is also  = dcc/PND, where dcc is thereceptor centre-to-centre distance. The angular width of one period (cycle) then is 2 , therefore thesampling frequency of the eye is R =1/(2)=PND/2dcc. (Modified from Land and Nilsson 2012)

It is easy to see from this relationship that the angular separation (; in radians)
between two adjacent receptors sampling node and antinode of the sinusoidal
grating (Fig. 1.4) is: = dcc/PND,[4]

where dcc is the receptor centre-to-centre distance. Then, for the spatial frequency
at the diffraction limit, the angular distance (in radians) between neighbouring
receptors, when they are packed in a square array, is:R = 1/2co = /2D.

[5]

However, in the highest density regions, photoreceptors are usually packed in ahexagonal instead of a square array (Snyder and Miller 1977); then the angulardistance (in radians) between the receptors is:H = 1/3co = /D3.
20[6]

Therefore, in order to sample the image provided by the diffraction-limited optics,
the receptor centre-to-centre distance has to be:
dcc = H PND = PND/D3.

[7]

Do photoreceptors of such size exist? In humans, photopic vision is maximallysensitive to light of 555 nm wavelength, and the best image quality is achieved
when the pupil diameter is 2.4 mm (Miller 1979). With a PND of 16.7 mm the dcc
is 2.2 am. This indeed agrees with histological measurements, which report
distances between adjacent cones in the human fovea of 2.0-2.3 am (Snyder andMiller 1977).
Can photoreceptors be even narrower? Yes, but not much. The narrowest
photoreceptors in both vertebrates and invertebrates are about 1 am wide (Landand Nilsson 2012). Again, due to the wave nature of light, when photoreceptor
diameter approaches the wavelength of light, total internal reflection no longer
holds. Photoreceptors do not act as a light-guiding fibre anymore. Light starts tointerfere and creates waveguide modes with uneven energy distribution. Some partof this energy even travels outside the photoreceptor and can be captured byneighbouring photoreceptors causing deterioration in resolution (Snyder 1979).
Thus, when the smallest photoreceptor diameter is achieved, the only way toincrease spatial resolution further is to increase PND and therefore eye size:

R =PND/(dcc )( 3)(57.3),[8]where factor 57.3 converts spatial frequency unit from cycles/radian tocycles/degree, because 1radian = 180°/, or 57.3°.
However, independently of the eye size, the brightest naturally occurring lightlevels are needed (close to 105 cd/m2) to resolve spatial frequencies of about 96%of the optical cut-off limit. Humans and some raptorial birds can indeed reachthese limits. If the light level is 100 times lower, only frequencies of about 80% of
the cut-off limit can be resolved (Snyder and Miller 1977), as is schematicallyindicated in the MTF (Fig. 1.2). Indeed as light level drops, spatial resolution
deteriorates drastically (Fig. 4.1).

Sensitivity
There are 1010 times more photons available under bright sunlight than under an
overcast starlit sky (Martin 1990). Every photographer knows three main ways
how to take better pictures when it gets darker. Reducing the F-number (focal
length/aperture diameter - f/D) of the lens increases image brightness (1/Fnumber)2. Increasing the ISO value of the camera chip (the gain) increases pixel
sensitivity. Prolonged exposure time increases the amount of photons collected.
21

The first two mechanisms can be easily seen in the equation describing
photoreceptor sensitivity S (measured in square micrometres times steradians(m2 sr; Warrant and Nilsson 1998):
S = 0.62 D2 (d/f)2 Pabs,[9]

where a larger pupil diameter D and shorter focal length f are analogous to a lower
F-number in a camera lens. The absorption rate Pabs, which is comparable to the
ISO value of the matrix, can be approximated by:Pabs = kL/(2.3+kL)[10]

for white light. Parameter k is the absorption coefficient describing the proportionof light absorbed per micrometre of the receptive structure length (L), for example
the outer segment of vertebrate rod or cone. It depends on the density ofphotopigment and the way it is packed. It is specific to the photoreceptor type and,for example, is 0.028 for a human rod (Warrant and Nilsson 1998). Longer
photoreceptor outer segments can pack more photopigment, thus larger L means
higher Pabs.
As the photoreceptor diameter d needs to be small for better spatial resolution (tothe limits described above) and the absorption coefficient k is limited by the
maximum packing density of photopigment, the only way to increase sensitivity
further is to increase photoreceptor outer segment length or lower the F-number ofthe eye. (However, long photoreceptors with highly packed photopigment sufferfrom high levels of thermal noise, thus a compromise with optimal signal to noise
ratio has to be found). Once the limits in these parameters are reached, narrow
receptors (small d) can be grouped into bigger units by summing their signals
neuronally (computationally larger d; Warrant 1999). This mechanism, called
spatial summation, allows using the same system for better resolution at high lightlevels and for lower resolution, but higher sensitivity in dim light. Yet another way
to increase sensitivity even more, though with a substantial cost of motion blur, is
to integrate photon catch over a longer period of time (Warrant 1999). This socalled temporal summation has exactly the same effect as choosing a longer
exposure time in photography.
The number of photons caught per photoreceptor determines the contrast that canbe detected at each light level (Land and Nilsson 2012). Due to the random natureof photon availability, Poisson statistics applies and the relation between photon
numbers (N) and detectable contrast (C) is as simple as:
N >1/C2, or C >1/N.

[11]

For instance, in order to detect 10% contrast, at least 100 photons are needed. If
we look back at the contrast transfer function (Fig. 1.2), we see that low photon
numbers, which limit the minimum detectable contrast, also set the lower value forthe optical cut-off frequency.
22

Thus, as we see, resolution and sensitivity - two features, which describe eye
performance – get intertwined together. The wave nature of light sets the limit tospatial resolution as it determines the minimum size of photoreceptors due toeffects of waveguide optics, and the optimum size of the pupil due to deleterious
effects of diffraction and aberrations. The quantum nature of light sets the limit tosensitivity, which limits the capability of the eye to make full use of its potential
spatial resolving power.

23

24

Chapter 2 The Avian Eye

As now we know something about the theoretical constrains on optical systems,
we will briefly look into the structure and diversity of avian eyes. These eyes,
which are no more spectacular than the eyes of any other vertebrate (Walls 1942),
however, fascinated humans for centuries, probably for no better reason than thatthey look at us from above.

General structure
The eye is an expensive organ and energy investment in it has to pay back. As
avian eyes are big both in relative and absolute terms (Walls 1942) the importanceof vision to birds is obvious. It is the ostrich (Struthio camelus), not the elephant,
which has the largest terrestrial eye, reaching 50 mm in axial length (Martin 1985)
and weighing more than the brain (Burton, 2008). Other “heavy-eyed” birds are
the wedge-tailed eagle (Aquila audax), Kori bustard (Ardeotis cori) and Europeannightjar (Caprimulgus europaeus) (Burton 2008). Indeed, the eyes of some birds
are so large that the interorbital bony septum is as thin as paper or even has a hole,and the eyes meet at the median sagittal plane (Fig. 2.1b). Because there is so little
room in the orbit most birds have low amplitudes of eye movements (7-20° in
various passerines, Fernández-Juricic et al. 2010; but up to 39° in tufted titmouse(Baeolophus bicolor), Moore et al. 2013), with nocturnal birds being extreme inhaving only minute eye movements (ca 1° in great horned owl (Bubo virginianus);
Steinbach and Money 1973). This shows that in some species, the eyes are as big
as the skull can accommodate, and some birds (like the Eurasian golden plover(Pluvialis apricaria)) even needed to build an extra structure on the skull toaccommodate the huge nocturnal eyes (Fig. 2.1a; Martin and Piersma 2009). On
the other extreme are kiwi birds, which have the relatively smallest eyes of all
birds (Walls 1942, Martin et al. 2007), and one can find the reason in the
behaviour and ecology of this nocturnal non-flying stranger of the bird kingdom.
Apart from their variation in size, avian eyes vary in shape too. However, theyshare one common property that the nearly hemispheric posterior segment of theeye globe is much larger than the anterior part (Jones et al. 2007). Thus, bird eyes
are never spherical as they are in e.g. humans, seals or mice (Land and Nilsson2012). There is also an asymmetry along the horizontal plane with the temporal
25

a

b

Fig. 2.1. The eye size is maximized in some avian species. a - The head of the Eurasian goldenplover (Pluvialis apricaria) as viewed from the back. Feathers and skin are partially removed to
expose large supraorbital protrusions - the supraorbital aliform bones (indicated with an arrowhead).
These bones increase orbital volume and allow accommodation of relatively large eyes in a small
skull. b - Freshly enucleated head of the red kite (Milvus milvus). The hole in the interorbital septum,
which is almost 1 cm wide, indicates that eyes of a large relative and absolute size are touching eachother in the centre of the skull of this species.

side of the eye being more extensive than the nasal side (Jones et al. 2007), whichis easily visible in some owls and waders (pers. obs.). But along the vertical plane
avian eyes are either flat (like in most diurnal birds with low resolution), globose(as in many diurnal birds with high resolution), or tubular (typical in owls, but also
in some raptors). A ring of ossical bones connects the anterior and posterior partsof the eye and creates the sclero-corneal sulcus, to support the optical system of
the eye against intraocular pressure, which rises slightly during accommodation(Walls 1942).

Optical system of the eyeMorphologically avian eye is of the camera-type (Land and Nilsson 2012) and its
optical system consists of the cornea, aqueous humour, lens and vitreous humour(Fig. 2.2a). In terms of function, it can be considered as a linear magnification
system (Martin 1983) and can be described, in a simplified manner, by the focal
length and minimum F-number of an equivalent theoretical single lens.
Since in a vertebrate eye, the image of the object is in a different refractive
medium than the object itself, it is the anterior focal length, which is of interest
here. The anterior focal length is equal to the posterior nodal distance (PND) and26

can be calculated by using Gullstrand’s simplified (No. 2) schematic eye model(Land and Nilsson 2012). This model uses the radii of curvature of the cornea andthe lens, their positions and refractive indices (Fig. 2.2b), which can be consideredas the main parameters to describe the optical system of the camera-type eye.
Variation in these parameters, or in other words variation in optical eye designs, isreflected in ecological needs of the animals.
One of the challenges posed by an amphibious lifestyle is a need to see relatively
well both in air and under water. Diving birds need to cope with the loss of corneal
refractive power while submerged, but still need to have not over-focused image
while on land. One solution to this problem is a relatively flat cornea, which does
not contribute much to the total refractive power of the eye (Kröger and Katzir
2008). Indeed, penguins have the flattest corneae of all birds (Martin 1999). Other
diving species, with more rounded corneae, thus more equal refractive power
distribution between the cornea and the lens, have to use strong accommodative
mechanisms when under water (Meyer 1977).
Avian accommodation is always for near vision and usually has a range of around20 diopters (Meyer 1977). Unlike fish or mammals, birds have lenticular as wellas corneal accommodation (Land and Nilsson 2012). Crampton’s muscles pull thecornea and reduce its radius of curvature to increase refractive power. Brücke’s
muscles contract the lens and sometimes so much that it is squeezed through thepupil supported by muscular iris and ossical bones.

aVitreous
humourbr2=3.62

PND=5.36
r3=-2.23

r1=2.60

Lens
F

N
D=3.10Cornea8.21

Aqueoushumour

4.24

2.85

0.98

Fig. 2.2. Optical system of the avian eye. a - Hemisected frozen eye of the Leach’s storm-petrel(Oceanodroma leucorhoa) showing the main optical components. b – Schematic representation of
the simplified schematic eye model (PND – Posterior Nodal Distance; F – focal plane; N – nodal
point; D – pupil diameter; r1, r2, r3 – radii of the cornea front, lens front and lens rear surfaces
respectively).

27scleral side
RPE - Retinal Pigment Epithelium

Direction of Light

PL - Photoreceptor Layer
ELM - External Limiting Membrane
ONL - Outer Nuclear Layer
OPL - Outer Plexiform Layer
INL - Inner Nuclear Layer
IPL - Inner Plexiform Layer
GCL - Ganglion Cell Layer
OFL - Optic Fiber Layer
ILM - Internal Limiting Membrane
vitreal side

Fig. 2.3. Cross-section through the Leach’s storm-petrel (Oceanodroma leucorhoa) central retina
showing the retinal layers. The RPE contains cells, which protrude their apical processes filled withmelanin granules into the PL, where inner and outer segments of the rods, single and double cones
are situated. The nuclei of photoreceptors are positioned in the ONL. The OPL contains synapses
connecting the photoreceptors to the bipolar and horizontal cells with nuclei in the INL, which also
contains amacrine cells. Accordingly, the IPL is built up of synapses connecting bipolar andamacrine cells to the retinal ganglion cells (RGCs) in the GCL. Some displaced RGCs are found in
the IPL and some displaced amacrine cells are present in the GCL. The axons of the RGCs heading
to the optic nerve form the OFL.

Again unlike in fish or mammals, the avian lens is soft and flexible, and especially
so in diving birds. By squeezing the lens through the pupil American dipper(Cinclus mexicanus) can create 50 diopters (Meyer 1977), hooded merganser(Mergus cucullatus) 67 diopters, and common goldeneye (Bucephala clangula) 78
diopters of extra power (Sivak et al. 1985) to compensate for the loss of corneal
refractive power upon submersion.
Apart from accommodation and image formation, the optical system also controls
the spectrum of light, which reaches the retina. Part of the light is scattered andpart is absorbed mainly by the cornea and lens, and mostly in the short-wavelength
region between 300 and 400 nm. Thus the optical system also works as a longpass filter for the incident light travelling to the retina (Lind et al. 2013, 2014).

28

Retina
The avian retina is of the typical vertebrate type with an inverted design (Land andNilsson 2012). It has several distinct neuronal layers, which light has to pass
before reaching photoreceptors that are located outermost (see Fig. 2.3 for naming
and abbreviations). Compared to the retinae of most other vertebrates, the avian
retina is considerably thicker (Walls 1942). This increased thickness is attributable
to the high density of cells in the inner nuclear layer and the high complexity ofneurite arborisation in the inner plexiform layer (Martin 1985). These layers areespecially thick in the regions with high photoreceptor density, which can be as
much as double of that in the human fovea (Miller 1979, Coimbra et al. 2015).

Photoreceptor layer
Birds have three types of morphologically distinct photoreceptors: rods, double
cones and single cones (Martin and Osorio 2008). Rods are active in dim light(scotopic conditions) and mediate achromatic vision. Cones are active in bright
light (photopic conditions) and mediate both chromatic and achromatic vision. Atintermediate light levels (mesopic conditions) all photoreceptors are functioning.
Not surprisingly, rods dominate the retina of nocturnal birds, while cones are themain photoreceptors in diurnal species (Nalbach et al. 1993).
Birds have four types of single cones. Ultraviolet or violet sensitive cones(UVS/VS, containing sws1 type of light sensitive pigment), short-wavelength
sensitive cones (SWS, sws2-pigment), medium-wavelength sensitive cones(MWS, rh2-pigment) and long-wavelength sensitive cones (LWS, m/lws-pigment)
are responsible for colour vision (Hart 2001). Double cones consist of principle
and accessory member (both containing m/lws-pigment) and are suggested tomediate motion perception and high resolution achromatic vision in bright light(Martin and Osorio 2008, Lind and Kelber 2011).
Photoreceptor size and shape varies not only between species, but also between
different regions of the retina. However, the general structure and position oforganelles within the photoreceptive cell is conservative (Fig. 2.4). Each cone
type, but not the rod, at the end of the inner segment, contains a specificpigmented oil droplet, which, similarly to the ocular media, acts as a high-passfilter and further attenuates light reaching the light-sensitive pigments in the disksof the outer segment. Apart from spectral filtering, oil droplets also have an optical
function, and together with the ellipsoid have a substantial effect on the light
guiding through the inner structures of the cones to their outer segments (Wilby etal. 2015). Once the light is converted into electrical signals, they are sent to thebrain via the complex network of neurons in the remaining layers of the retina.
29

Outersegment
Paraboloid

Innersegment

Oil droplet
Ellipsoid

Nucleus

Synaptic footRod

UVS/VS
cone

SWS
cone

MWS
cone

LWS
cone

Doublecone

Fig. 2.4. Schematic drawing of the domestic chicken (Gallus gallus domesticus) rod, single cones
and double cone representing six types of avian photoreceptors. UVS/VS – ultraviolet or violet
sensitive cone, SWS – short wavelength sensitive cone, MWS – medium wavelength sensitive coneand LWS – long wavelength sensitive cone. The ellipsoid is the region, where mitochondria arelocated. Paraboloid (called hyperboloid in rods) is the region, where glycogen is stored. (courtesy ofPeter Olsson)

Other retinal layers
The basic avian retinal design and its division in layers essentially resemble thoseof other vertebrates (Nalbach et al. 1993). In general, the signal fromphotoreceptors is sent to the retinal ganglion cells via dedicated bipolar cells, withhorizontal and amacrine cells providing intraretinal interactions (Land and Nilsson2012). On top of this basic plan, there is a lot of variation (Güntürkün 2000).
However, our knowledge on components and structure of the avian inner nuclear
layer and plexiform layers is very limited. Still today the classical Cajal’s workfrom 1893 is often referred to as the main source of knowledge on avian retinal
complexity. The reason for that is “a general belief from past research…that, formany cell types, the response characteristics and functions are similar across allvertebrate groups” (Martin 1985 p. 344). Therefore most of our knowledge on
retinal organization and function comes from the research on mammalian model
species (Masland 2012). Nevertheless, it is known that a lot of neural processing,which happens outside the retina in invertebrates, takes place already in the retina
of vertebrates (Cronin et al. 2014). A complex neural network performs firstcomputations and extracts relevant features for acuity, contrast, sensitivity andcolour determination (Rodieck 1998).
30

Accordingly, in the high acuity areas of the retina high photoreceptor densities
result in large numbers of bipolar and ganglion cells as compared to the peripheral
regions (Nalbach et al. 1993). At these specialized locations, the convergence ratio
from photoreceptors to ganglion cells is low and in some birds the ratio is 1:1 orclose to this (Oehme 1964, Fite and Rosenfield-Wessels 1975, Coimbra et al.
2015). Finally, all the signals from the retinal ganglion cells are sent to the brain
via the optic nerve, thus ganglion cells, not the photoreceptors, are the bottleneck
for the information capacity of the eyes (Land and Nilsson 2012).

Retinal specialisations
Apart from neural convergence and pre-computation within the retina, anotherway to reduce the amount of visual information sent to the brain, and also thethickness of the optic nerve, is to “concentrate visual effort” on the areas of“interest”. For species living in open habitats all approaching objects are imaged ina narrow horizontal band on the retina (Hughes 1977, Land and Nilsson 2012).
This lead Hughes (1977) to propose the “terrain theory” to explain why species
from open habitats have a narrow elongated band of increased RGC density.
Indeed, prey or predatory mammals from open savannah (Hughes 1977),
waterfowl (Lisney et al. 2013), or shallow water fish (Collin and Pettigrew 1988)
all have a zone of higher acuity stretching horizontally across the retina, the socalled visual streak. In Paper II we investigated RGC topography in two
procellariiform seabirds, the Leach’s storm-petrel and the Northern fulmar (Fig.
2.5), and found well-pronounced visual streaks in both species corroborating thetheory. Other animals from more cluttered three-dimensional environments, likeforest dwellers (Hughes 1977), ground-feeding birds (Dolan and Fernández-Juricic
2010), or coral reef fish (Collin and Pettigrew 1988), have a region in the retina,
where RGCs are concentrated in a circular area instead of an elongated streak.
However, as more and more species were studied, some examples contradicting
the theory emerged (Hayes and Brooke 1990, Lisney et al. 2012, Tyrrell et al.
2013). Additional factors, like prey capture and handling technique, weresuggested to have an effect too.
In Paper I we looked at RGC distribution in two parrot species, budgerigars andBourke’s parrots. Even though both species inhabit open terrain of the central
Australia, all but one specimen lacked the visual streak that would be predicted by
the “terrain theory”. In budgerigars, apart from the area centralis we also found apresumptive area nasalis, which has never been reported in birds before. Higher
visual acuity in the nasal retina serving temporal visual field would have an
advantage for budgerigars while climbing, when birds use the beak as a support,
and head mobility is therefore restricted.
31

a

b

Fig. 2.5. Northern fulmar (Fulmarus glacialis) in its most natural environment (a). Leach’s stormpetrel (Oceanodroma leucorhoa) in its most unnatural environment (b). (b courtesy of Almut Kelber)

However, neither Bourke’s parrots nor other parrot species studied recently(Coimbra et al. 2014) had similar retinal specialisation. Several other explanations
for the presence of the presumptive area nasalis were discussed in Paper I. They
include domestication, age, and general intraspecific variability, which were also
observed in pigeons (Columbia livia domestica) (Querubin et al. 2009) andJapanese quails (Coturnix japonica) (Budnik et al. 1984, Ikushima et al. 1986,
Lisney et al. 2012). The effect of domestication on the avian visual system is aninteresting question, which deserves more research in the future.
Apart from areae and visual streaks, many bird species have a third type of retinal
specialisation called fovea. It is a structural depression in the retina caused by apartial or full radial displacement of ganglion and inner nuclear layers to the sides.
Some foveae are shallow, but some are deep with steep walls (Meyer 1977).
Snyder and Miller (1978) suggested that a fovea acts as a negative lens of atelephoto system increasing spatial resolution at that particular area of the retina.
High variation of foveal depth, size and shape within single species (Oehme 1964,
Paper II) suggests that the function of foveal depression might be different fromthe widely spread hypothesis of the magnifying telephoto lens. Reymond (1985,
1987) has shown that spatial resolution in raptors with deep foveae can be
explained without this assumption. Indeed, optical, anatomical and behaviouralspatial resolution match quite closely in the wedge-tailed eagle – the animal withthe highest visual acuity discovered so far.

32

Chapter 3 Development of the Eye

Most of the knowledge on avian eye development undoubtedly comes from theresearch on domestic chickens (Gallus gallus domesticus). From regulatory genesthat control early neural development to experimental manipulations on visualenvironment during maturation, studies on chickens build the basis of ourunderstanding on the development of visual function in birds (Mey and Thanos
2000). However, in this chapter, we will briefly look only into the development of
the retina and the growth of the main optical compartments of the eye.

Development of the retina
The vertebrate retina develops from the neural epithelium. Early in development
the anterior portion of the neural tube divides into the forebrain, midbrain andhindbrain. The posterior part of the forebrain invaginates and forms twobilaminated eyecups. The outer layer of the eyecup forms into retinal pigment
epithelium, and the inner layer gives a rise to the neural retina (Mey and Thanos
2000).
In chickens, during the initial stages of retinal development, progenitor cells
proliferate uniformly across the retina. Around the fifth embryonic day(abbreviated as E5), proliferation slows down in the centro-temporal retina and by
E8 progenitor cell division is found only in the retinal periphery. Accordingly, theoldest cells in the developing chicken retina are found in the centre, andsubsequent neuron differentiation and maturation proceeds in an approximate
centro-peripheral direction (Mey and Thanos 2000). However, a temporal-nasal
gradient also exist as the nasal retina continues to grow for a longer period than thetemporal retina (Rager et al. 1993).
The first retinal neurons, which start to differentiate, are retinal ganglion cells(RGCs), followed by the photoreceptors, amacrine cells, horizontal cells, andfinally bipolar cells. However, the period of each cell type generation overlaps
with one another, and the photoreceptors are the last cells, which stop to
proliferate. In chickens, RGCs are morphologically developed at E16, but before
that a wave of apoptosis sweeps through the retina and more than one third of all
initially built RGCs die (Hughes and McLoon 1979, Straznicky and Chehade1987). Photoreceptor cells mature much later. Even though opsin expression starts
33

seven days before hatching (E14, Bruhn and Cepko 1996), retinal oil droplets
attain their mature colour and size only 15 days post-hatch in chickens (López etal. 2005). While the retina grows in size, it also grows in thickness at the sametime.
Retinal stratification, the formation of retinal layers (depicted in Fig. 2.3), is
happening as a result of vertical cell migration mainly between E6 and E16. The
RGCs and displaced amacrine cells move to form the ganglion cell layer;
amacrine, horizontal, bipolar and displaced ganglion cells form the inner nuclear
layer, and photoreceptors stay on the scleral (ventricular) side to form the outer
nuclear layer. Growing neurites and dendritic branching result in plexiform layers,which separate the nuclear layers. The first synapses appear in the inner plexiform
layer at E13, however in the outer plexiform layer synapses start to form only on
E17. Three days before chickens hatch (E18) only 3% of axons in the optic nerve
are covered in myelin, suggesting that most of the myelination takes place during
early post-hatching development (Mey and Thanos 2000).
Knowledge on retinal development in birds other than chicken is scarce. In
chickens, which are relatively mature and independent after hatching (precocial
birds), photoreceptor inner segments start growing 10 or 11 days before hatching(E9-E10; Wai and Yew 2002, Mey and Thanos 2000). In pigeons, which hatch
relatively immature and require parental care (altricial birds), budding
photoreceptor inner segments are found only on day 2 post-hatching (Bagnoli etal. 1985). By day 9 post-hatching most of the receptor outer segments of pigeons
are present, but they continue to grow and reach adult length only by day 20 posthatching (Bagnoli et al. 1985). In chickens, receptor outer segments appear 3 days
before hatching (E18) and get their adult form 1 day before hatching (E20) (Olson
1979), even though photoreceptors still continue to proliferate until some timeafter hatching (Mey and Thanos 2000). In pigeons, synapses in the outer plexiform
layer do not mature before day 9 after hatching (Bagnoli et al. 1985), while inchicken the first mature synapses are found 3 days before hatching (E18) (Meyand Thanos 2000). Apparently, the pigeon eye is much less developed at the timeof hatching than the chicken eye. These data illustrate that timing of the retinal
development in birds highly depends on the level of precocity.
Even though at the time of hatching the chicken visual system is basicallyfunctioning (Over and Moore 1981, Mey and Thanos 2000), other retinal
developmental processes take place as the eye continues to grow. In the area
centralis of the post-natal mammalian retina cell density increases due to cell
migration, but in the periphery it decreases because of general eye growth andretinal stretch (Hendrickson and Provis 2006). In birds the formation of the area
centralis was investigated only in chickens (Straznicky and Chehade 1987, Pradaet al. 1991, Rager et al. 1993, Chen et al. 2004). Differently from mammals,
chicken RGC density continues to drop after hatching and reaches the adult levelat the age of four weeks (Ehrlich 1981, Straznicky and Chehade 1987).
34

Preferential cell death and differential retinal expansion increase the centroperipheral gradient in RGC density and contributes to the well-pronounced area
centralis (Straznicky and Chehade 1987, Rager et al. 1993), the region with thehighest visual acuity.
In Paper III, we investigated the development of the RGC topography in the
Leach’s storm-petrel juveniles. Even though Leach’s storm-petrels are classified
as semi-precocial birds (Ricklefs et al. 1980), the chicks spend their first 61-67
days before fledging in a long and dark underground burrow. We had a chance toinvestigate juveniles at the age of 2, 4 and 6 weeks post-hatching. RGC
topography varied not only between, but also within different age classes, howeverat least one specimen in each age class had a well-pronounced visual streak (Figs.
2, 3, 4 in Paper III), similar to that found in the adult birds (Fig. 1 in Paper II).
These findings indicate that fine-tuning of RGC topography does not happen earlyin development, and RGC layer continues to mature throughout the nest period.
Differently from chickens, the peak RGC density of Leach's storm-petrels did notdecrease after week 2 post-hatching. It was similar in all investigated age groups,
and was comparable to that of adult birds (Paper II). Unfortunately, we had nochance to study younger birds or to do more elaborated retinal investigations toreveal more about the retinal development in this species.

Eye growth
While the retina develops from the neural epithelium, the lens starts to form fromthe epidermal epithelium as soon as the retinal cup approaches it (around 1.5 days
after start of incubation; Mey and Thanos 2000). As the task of the optical system
is to bring light rays into focus on the retina, the growth of the optical components,
and their product – the focal length, has to match the growth of the eyeball.
Different techniques are used to obtain optical parameters for the schematic eyemodel. It can be measured in a live animal, freshly fixed eyes or frozen eyes. The
measures from different techniques agree quite well (Lind and Kelber 2009, Avila
and McFadden 2010), especially when the natural level of variation and thenumber of assumptions used in constructing schematic eyes are considered(Martin 1983). To date, optical parameters of growing eyes exist for four species:
domestic chicken (e.g. Schaeffel and Howland 1988, Avila and McFadden 2010),
American kestrel (Falco sparverius) (Andison et al. 1992), common barn owl(Tyto alba) (Schaeffel and Wagner 1996) and Leach’s storm-petrel (Paper III).
Data summarised in figure 3.1 show how optical structures change during the firsttwo months post-hatching in these four species.

35

10

20

30

40

50

60 Adult
70

6
4

10

20

30

40

50

60 Adult
70

0

≈

1

10

20

30

40

50

60 Adult
70

10

20

30

40

50

60 Adult
70

20

30

40

50

60 Adult
70

8
6
4
2
0

2

10

20

30

40

50

60 Adult
70

2
0
−2
−4
−6

10

≈

4

4

Front

6

6

0

2

10

8

Lens
radius,lens
rearradius,mm
mm

Corneafront radius, mm
cornea front radius, mm

0

≈

2

≈

Lens
thickness, mm
lens thickness, mm

8

3

Back

0

4

≈

5

Anterior
chamber depth, mm
anterior chamber depth, mm

10Vitreouschamber
depth,
back vertex
distance,
mm mm

15

≈

Axial
length,mm
mm
axial length,

20Age, days
Fig. 3.1. Schematic eye parameters of the growing eyes. Blue symbols – Leach’s storm-petrel(Oceanodroma leucorhoa) (Paper III), red symbols – domestic chicken (Gallus gallus domesticus)(Schaeffel and Howland 1988), green symbols – American kestrel (Falco sparverius) (Andison et al.
1992), black symbols – common barn owl (Tyto alba) (Schaeffel and Wagner 1996). Open symbols
in the bottom right panel represent the radius of the lens back surface.

Chicken, American kestrel and common barn owl show considerable differencesin ametropia soon after they open their eyes. Chickens are hyperopic soon after
hatching (+3 to +6.5 diopters), American kestrels are highly myopic (-20 to -25
diopters) while common barn owl chicks show a high variation in the refractive
power of the eye when the eyelids open (-4 to +4 diopters). However, chickens
achieve near emmetropia in just 7 days, while it takes 10 days for American
kestrels, and 2 weeks for the common barn owl juveniles. In the study presented inPaper III we did not perform measurements on emmetropization as this wasdifficult to achieve under field conditions. However, we did preliminary negative
phototaxis and optokinetic nystagmus experiments, which indicated that spatial
vision is still not functioning at 2 weeks post-hatching in Leach’s storm-petrel
juveniles.
36

Chapter 4 Measuring Spatial
Resolution

We saw that the wave nature of light sets the limit to spatial resolution, and thequantum nature of light limits the optical sensitivity. We looked at the avian eyes,
which have to compromise between both in order to provide enough information
to their bearer to serve its ecological needs. In this chapter we will discuss how we
can determine the spatial resolution in birds.

Behavioural measurements
The most common behavioural method to estimate visual acuity is a classical twoalternative forced choice discrimination task, where an animal has to choose
between two simultaneously presented stimuli (Donner 1951, Martin and Gordon
1974, Dbrowska 1975, Fox et al. 1976, Lind et al. 2012). The negative stimulus
contains sinusoidal gratings of dark and lights bars, while the positive stimulus is ahomogeneous field of the same mean luminance as the negative one. Once theanimal is trained to choose the homogeneous stimulus field, which is rewarded
with food, trials are repeated with randomised stimulus position and level of‘difficulty’. The percentage of correct choices for each spatial frequency is plottedin a psychometric function, and the highest spatial frequency at which animal does
no more correct choices than could be predicted by chance is considered to be thespatial resolution threshold. The lowest behavioural visual acuities among birds
are reported for the common barn owl (2.3-4.5 cyc/deg, Harmening et al. 2009,
Orlowski et al. 2012) and the highest for the wedge-tailed eagle (138 cyc/deg;
Reymond and Wolfe 1981, Reymond 1985) (Table 4.1). Raptors are the only
group of all animals that have higher spatial resolution than humans.

37

-/62
-

6/6
6.6g
7.1g
6–7.5
7.6g
2.17/7.8
9.2g/9.4

European robin (Erithacus rubecula)

Tufted titmouse (Baeolophus bicolor)

Leach’s storm-petrel (Oceanodroma leucorhoa)

Great horned owl (Bubo virginianus)

American mourning dove (Zenaida macroura)

Reed bunting (Emberiza schoeniclus)

Bourke’s parrot (Neopsephotus bourkii)-

4.2-6.4/7/8.3-12.8g
12.9g
3/6/12/18

Domestic chicken (Gallus gallus domesticus)

Ring-necked pheasant (Phasianus colchicus)

Pigeon (Columba livia domestica)

38

11.9g

Mallard (Anas plathyrynchos)

5/50.5/160

8.8/12/8–11.1
6.9g/11.7

Tawny owl (Strix aluco)

Grey partridge (Perdix perdix)

Budgerigar (Melopsittacus undulatus)-

2.17/9.7
10.2g

Yellowhammer (Emberiza citrinella)

0.85/3.2/32/317-

3.5/16/---/50

1.53/19.1

-

9.6g
9.7g

Canada goose (Branta canadensis)

Japanese quail (Coturnix japonica)

1.53/19.1

-

80

-

-

1.53/19.1

-

4.8g

-

5.0g

4.7g

House finch (Carpodacus mexicanus)

2.7/30Carolina chickade (Poecile carolinensis)

2.6–4.0/4.1

Common barn owl (Tyto alba)

Stimulus luminance(cd/m2)

House sparrow (Passer domesticus)

Spatial resolution(cyc/deg)

Species name

Table 4.1. An overview of spatial resolution thresholds in birds.

Hodos et al. 1976

Lisney et al. 2012

De Mello et al. 1992/Jarvis et al. 2009/Ehrlich
1981, P. Olsson (pers. com)

Lisney et al. 2013

Paper I/Lind et al. 2012

Martin and Gordon 1974

Lisney et al. 2012

Donner 1951

Lisney et al. 2012

Fernández-Juricic et al. 2011

Paper I/Lind et al. 2012

Donner 1951

Dolan and Fernández-Juricic 2010

Fite 1973

Paper II

Moore et al. 2013

Donner 1951

Moore et al. 2013

Dolan and Fernández-Juricic 2010

Dolan and Fernández-Juricic 2010

Harmening et al. 2009

Reference

-

–/93e
980
1150
995

44.7c
46c/39.7–71.4e
104
135
135
52/57/73/76c
58/115/138/142c

Northern fulmar (Fulmarus glacialis)

American kestrel (Falco sparverius)

Griffon vulture (Gyps fulvus)

Egyptian vulture (Neophron percnopterus)

Indian vulture (Gyps indicus)

Brown falcon (Falco berigora)

Wedge-tailed eagle (Aquila audax)

Reymond 1985

Reymond 1987

Fischer 1969

Fischer 1969

Fischer 1969

Dvorak et al. 1983/Gaffney and Hodos 2003

Paper II

Moroney and Pettigrew 1987

Coimbra et al. 2015

Dbrowska 1975

Dbrowska 1975

Moroney and Pettigrew 1987

Coimbra et al. 2015

Donner 1951

Donner 1951

Hart 2002

Coimbra et al. 2015

Boire et al. 2001

Fite and Rosenfield-Wessels 1975

Coimbra et al. 2015

Reference

ganglion cell density counts, e -electroretinogram.

39

Note: if not indicated, values are obtained from behavioural experiments, otherwise by: c - photoreceptor centre-to-centre distance or photoreceptor density counts, g – retinal

2/20/2000/-

2/20/2000/-

-

-

-

40.8c
41g

9.5/60Laughing kookaburra (Dacelo novaeguineae)

23.7–29.5/29.5–33.3

Common magpie (Pica pica)

9.5/60--1.53/19.1

1.53/19.1--

Red wattlebird (Anthochaera carunculata)

26g
29.5/29.5

Rook (Corvus frugilegus)

Yellow-rumped thornbill (Acanthiza chrysorrhoa)

Sacred kingfisher (Todiramphus sanctus)

22.5/22.5
25.6c

Common chaffinch (Fringilla coelebs)

20.6g
22.5/22.5

Brown honeyeater (Lichmera indistincta)

Indian peafowl (Pavo cristatus)

19.8g
20.2c

Ostrich (Struthio camelus)

Common blackbird (Turdus merula)-

15–19gBlue Jay (Cyanocitta cristata)

-

18.5c

Silvereye (Zosterops lateralis)

Stimulus luminance(cd/m2)

Spatial resolution(cyc/deg)

Species name

Table 4.1 cont.

Spatial resolution, cyc/deg

100
brown falcon
wedge-tailed eagle

humanpigeon10

domestic chicken
common barn owl
1cat
great horned owl
10-5

10-4

10-3

10-2 10-1 100 101
Luminance, cd/m2

102

103

104

Fig. 4.1. The spatial resolution - luminance function of six species of birds, cat and human. Data
assembled from: wedge-tailed eagle (Aquila audax) - Reymond 1985, brown falcon (Falco berigora)- Reymond 1987, pigeon (Columba livia domestica) - Hodos et al. 1976, domestic chicken (Gallus
gallus domesticus) - Gover et al. 2009, great horned owl (Bubo virginianus) - Fite 1973, common
barn owl (Tyto alba) - Orlowski et al. 2012, human and cat - Pasternak and Merigan 1981. The
symbols on top depict relative sky conditions representing the luminance level.

The age (Hodos et al. 1991, Porciatti et al. 1991, Ghim and Hodos 2006) or therace of tested domesticated animals (Over and Moore 1981, Jarvis et al. 2009) canhave an effect on the spatial resolution threshold. However, one really importantparameter is the luminance of the stimulus. Spatial resolution deteriorates as thelight level drops, but many behavioural studies have investigated spatial resolution
only at one or two luminance levels (Table 4.1), and only few species have beentested at several light levels (Fig. 4.1).
The same two-alternative forced choice procedure can be repeated with stimuli ofdifferent contrast. Collected data allow to establish a contrast sensitivity function(CSF), which describes the ability of the visual system to discriminate intensity
contrast over a range of spatial frequencies (Fig. 4.2). The typical achromatic CSF
has an inverted U-shape with maximum contrast sensitivity somewhere in thelower half of spatial frequencies, and a roll-off at both low and high spatial
frequencies. Decline of sensitivity at high frequencies is explained by theimperfections of optics and decline at the low end is suggested to be due to lateral
inhibition in the receptive fields (De Valois and De Valois 1990).
40

Contrast sensitivity, 1/contrast threshold

human
cat

100

American kestrel

10
pigeoncommon barn owl
budgerigar

1
0.1

1
Spatial resolution, cyc/deg

10Fig. 4.2. Contrast sensitivity function of four species of birds, cat and human. Data assembled from:
pigeon (Columba livia domestica) - Hodos et al. 2002, common barn owl (Tyto alba) - Harmening etal. 2009, budgerigar (Melopsittacus undulatus) - Lind et al. 2012, American kestrel (Falco
sparverius) - Hirsch 1982, cat - Bisti and Maffei 1974, human - Berkley 1976.

While the shape of the CSF is similar for most animals, the peak contrast
sensitivity and its position, as well as the frequency range vary from species tospecies (Ulrich 1981) (Fig. 4.2, Table 4.2). In general, birds have lower contrast
sensitivity and narrower band-width as compared to mammals. Whichmechanisms are responsible for this phenomenon is still not fully resolved,
however several possible hypotheses exist (summarized in Ghim and Hodos
2006). The highest contrast sensitivity among birds was recorded for the American
kestrel (31; Hirsch 1982), and the lowest for the common barn owl (6; Ghim andHodos 2006) (Table 4.2). An effect of age on contrast sensitivity is indicated for
pigeons, American kestrels (Ghim and Hodos 2006) and Japanese quails (Lee etal. 1997).
Behavioural tests determine the ultimate spatial resolution of animals, but are hardto perform as they involve keeping birds in captivity and tedious training
procedures (Martin and Gordon 1974, Reymond 1985, 1987, Lind et al. 2012).
The alternative methods are described below.

41

Table 4.2. An overview of spatial contrast sensitivity thresholds in birds.
Stimulus
Species namePeak spatial Position of
luminance
contrast
peak(cd/m2)
sensitivity
sensitivity(cyc/deg)
American kestrel(Falco sparverius)
Wedge-tailed eagle(Aquila audax)
Common barn owl(Tyto alba)
Domestic chicken(Gallus gallus domesticus)
Budgerigar(Melopsittacus undulatus)
Japanese quail(Coturnix japonica)
Pigeon(Columba livia domestica)
Bourke’s parrot(Neopsephotus bourkii)
Red-bellied woodpecker(Melanerpes carolinus)
Common starling(Sturnus vulgaris)

References

Ghim and Hodos
2006/Hirsch 1982
Reymond and Wolfe
1981
Ghim and Hodos
2006/Harmening etal. 2009

30e/312.1e/1094e/40

14

10

20

6e/13

1a/1

94e/2.74

12

1

16

Jarvis et al. 2009

10

1.4

50

Lind et al. 2012

9.9

1

94

4.6e/8e/9.9

0.7e/1.3e/0.8

7

2.4

62

6.7

0.8

94

6.2

1.1

94

Ghim and Hodos
2006
Hodos et al.
2002/Ghim and16e/94e/100
Hodos 2006/ Hodos
et al. 2002
Lind et al. 2012
Ghim and Hodos
2006
Ghim and Hodos
2006

Note: if not indicated, values are obtained from behavioural experiments, otherwise by: e – electroretinogram.

Electrophysiological measurements
Spatial resolution, as well as contrast sensitivity, can be also measured using
electroretinograms (ERGs). During ERG measurements the bird is anesthetized
and immobilized. Cycloplegia (paralysis of the ciliary muscle to hinderaccommodation) and mydriasis (dilation of the pupil) are usually induced byvecuronium bromide. The recording electrode is inserted through the eyelid tocontact the sclera or the cornea. The reference electrode is inserted in the other eye
in a similar manner. The ground electrode is inserted subcutaneously in the scalp.
The bird eye is positioned in front of the stimulus monitor where gratings ofvarying spatial frequency and contrast are presented. The gratings are phasereversed usually at 7.5-7.7 Hz. The CSF using ERG was measured for the42

Japanese quail (Lee et al. 1997), pigeon (Hodos et al. 2002), American kestrel,common barn owl, common starling (Sturnus vulgaris) and red-bellied
woodpecker (Melanerpes carolinus) (Ghim and Hodos 2006). The spatial
resolution and peak contrast sensitivity measured with this method are somewhat
lower as compared to the behavioural estimations in pigeon and American kestrel(Table 4.2).

Anatomical measurements
Most studies on avian visual acuity are based on retinal whole-mount technique(Stone 1981, Ullmann et al. 2012) and RGC density counts. The peak cell density,
instead of centre-to-centre distance is most often used, and the Nyquist limit of
spatial resolution (Fn) for an assumed two-dimensional hexagonal array of RGCs
is calculated as:
Fn = 0.5 × RMF × (2G/3)1/2 ,[12]

where G is ganglion cell density in cells/mm2 and RMF is the retinal magnification
factor, which represents the distance on the retina subtended by 1° of visual space,and is calculated as:
RMF = 2PND/360.

[13]

Neither does RGC density approximate a hexagonal array, nor are they packed in
two dimensions, especially in the area of the highest cell density. Depending on
species and retinal eccentricity, RGCs can be positioned in several lamina, thehighest, up to seven or eight layers, reported in the perifoveal region of the sacredkingfisher (Todiramphus sanctus) (Moroney and Pettigrew 1987). As RGC nuclei
are much wider than photoreceptor inner segments, this type of packing is a resultof high RGC-photoreceptor ratio and extremely high photoreceptor density, which
indeed approximates a two-dimensional hexagonal array very well (Snyder andMiller 1977, Kram et al. 2010).
In Paper I we present and discuss several difficulties and other assumptions
associated with this method. Briefly, first, it is important to measure the actual
PND of the species studied. Often the PND is approximated by using a fixed
PND:axial length ratio, which was established based only on a very limited
number of species (Pettigrew et al. 1988). As this ratio can vary highly evenbetween closely related species with similar activity patterns (0.55 for the Manx
shearwater (Puffinus puffinus) (Martin and Brooke 1991) and 0.67 for the northern
fulmar (Paper II)) the spatial resolution estimate can be affected. Second, disregardof the retinal shrinkage during the histological tissue processing, inclusion of nonganglion cells in the RGC counts, or underestimation of the RGC density due tomultiple cell layers can affect precise estimation of spatial resolution. However,43the variability in anatomical spatial resolution due to the errors in the RGC density
or PND evaluation may still be in an acceptable range as the inter-individual
variation in visual acuity observed in behavioural studies is usually very high(summarised in Paper I).
Other studies, especially those on raptorial birds (Snyder and Miller 1978, Miller
1979, Reymond 1985, 1987) use photoreceptors instead of RGCs as retinal
sampling units. Coimbra et al. (2015) suggested that the peak density of retinal
neurons with the lowest population in the retinal pathway determines spatial
resolution. Indeed, in a primate fovea, where two to four midget RGCs connect toeach photoreceptor (Perry and Cowey 1988, Curcio and Allen 1990, Wässle et al.
1990), spatial resolution based on RGC density would be overestimated. Whether
a midget-like system exists in any bird species is currently unknown, however,Oehme (1964) traced RGC to photoreceptor connections in the central andtemporal foveae of a common buzzard and common kestrel (Falco tinnunculus),
and found one RGC for each foveal cone. Depending on how far and how
asymmetrically the RGCs are displaced in the fovea, regular RGC counts inwhole-mounts can provide highly unreliable density estimations. Therefore,
Coimbra et al. (2015) recommended to use RGC density in afoveate, andphotoreceptor density in foveate bird species. Indeed, as mentioned above,
Reymond (1985, 1987) has shown that the theoretical spatial resolution based on
the peak cone density in the central fovea of brown falcon (Falco berigora) andwedge-tailed eagle closely match behavioural visual acuity.
In Paper II, where we studied RGC topography and spatial resolution in two
procellariiform seabird species, we found a fovea in the centre of visual streak in
the Northern fulmar, but not in the Leach’s storm-petrel. In addition to the retinal
whole-mounts we did cross-sections through these areas and found that Leach’s
storm-petrel had thicker neuronal layers, but no retinal indentation (Fig. 3 in Paper
II). The Northern fulmar, however, had a fovea, and we estimated photoreceptor
density in the foveal pit based on the oil droplet diameter. Therefore, following thepresented reasoning, we calculated spatial resolution from the peak RGC density
in Leach’s storm-petrel (7.1 cyc/deg), but from the photoreceptor density in the
fovea of the Northern fulmar (44.7 cyc/deg).
We did not find a fovea in the two parrot species studied in Paper I. Still, we
calculated spatial resolution based on both peak RGC density and oil droplet
diameter in order to compare these values to the visual acuity thresholds measured
in behavioural studies. Surprisingly, spatial resolution measured behaviourally(Lind et al. 2012) was higher than resolution based on RGC density, but lower
than resolution based on oil droplet diameter in both species. As different
individuals were used for behavioural and anatomical studies with budgerigars, themismatch could be possibly explained by inter-individual variation. However, thesame Bourke’s parrots were investigated in both studies, and the mismatch
between these results remains unclear.
44

Yet another underlying assumption in the estimation of anatomical spatial
resolution is that there are no rods in the high-acuity region, and that all types ofcones in this region contribute equally to the high acuity tasks. Rod-free areas
were indeed found in the area centralis of the chicken (Bruhn and Cepko 1996)
and in the fovea of the pigeon (Querubin et al. 2009), some passerines (Coimbra etal. 2015) and the Northern fulmar (Paper II). However it is generally assumed that
only double cones mediate achromatic vision in birds (Campenhausen and
Kirschfeld 1998, Osorio and Vorobyev 2005, Lind and Kelber 2011). This
assumption is rarely addressed in studies on avian resolution.
As mentioned before, raptorial birds are the only animals with spatial resolution
higher than humans. They are also known to possess two foveae, a deep central
fovea, projecting to the lateral visual field and a deep or shallow temporal fovea
projecting to the frontal visual field (Meyer 1977). Therefore, if double cones are
assumed to mediate achromatic vision in birds, the raptor fovea should be densely
packed with double cones. This reasoning led us to Paper IV, where we usedtransmission electron microscopy (TEM) and immunohistochemistry toinvestigate the presence of the double cones in the central and temporal foveae offour raptor species.
Based on TEM micrographs, we found that the central fovea of the red kite andcommon buzzard had a double cone-free zone of approximately 200 ]m indiameter, but it was only around 30 ]m in the peregrine falcon. We could not
determine the size of double-cone free area in the central fovea of the Eurasiansparrowhawk, but results from the immunohistochemistry show that it also lacks
double cones. The temporal fovea of the common buzzard and peregrine falcon
had small (25-30 ]m) double-cone free zones, however the Eurasian sparrowhawk
temporal fovea contained double cones. In addition to this, we found VS and
MWS cones in the central fovea of the common buzzard, peregrine falcon andEurasian sparrowhawk. These results indicate, that most likely not only double
cones, but also single cones contribute to achromatic high-resolution vision inbirds, in general.

45

46

Concluding Remarks

Although this thesis has an extremely general title Spatial Vision in Birds, it isclear that only some aspects of spatial vision, and actually only some aspects ofspatial resolution, could be covered in this study. However, even though work on
only eight species is presented in this thesis, I have to admit, that I have touchedmore bird eyes than any other regular teenager. Around 0.5% of all extant bird
species have donated their eyes to us during these years, though many results arestill waiting to see the daylight.
However, in the studies presented here we see RGC topography maps in four new
bird species, high intra-species variation in the peak RGC density, a mismatch
between RGC based anatomical resolution and behavioural visual acuity, aputative area nasalis never before reported in birds, first estimations of spatial
resolving power in procellariiform seabirds, RGC topography development in only
the second bird species, foveal depth profiles for two new raptor and one seabird
species, the absence of double cones and presence of V and MVS cones in the
raptor fovea, indicating the contribution of single cones to high resolution vision.
Still, work presented in this thesis adds just a little bit to the knowledge on bird
spatial vision. While the theoretical constraints on spatial resolution are very wellunderstood, retinal development, retinal function and bird visual ecology haveenormous amounts of unanswered questions. Some of them stem directly fromeach of the studies presented in this thesis.
The effects of domestication have been investigated in chickens, quails andpigeons, but has selective breeding already affected the pet birds? How does
anatomical and behavioural spatial resolution match in other bird species (PaperI)? Can seabirds really forego vision for olfaction? What can they really see on theocean (Paper II)? Retinal development has been studied in detail in chickens, but
how does the retina develop in other birds (Paper III)? How does the avian fovea
form (Paper II and III)? What is the real function of the double cones? How istheir distribution in the retina controlled? Are double cones missing from theshallow central foveae (Paper IV)?
"The outcome of any serious research can only be to make two questions grow,where only one grew before" Thorstein Veblen

47

48

Acknowledgements
Thank you Almut! Thank you for bringing this amazing period and every single
detail of it into existence!
Thank you all the people of the present and past Vision Group for doing what you
are doing and making this group the way it is. Without your charm it would not be
The Vision Group. It is a great research environment indeed. A special thanks toeach of you in one way or another is spread somewhere between the front coverand the back cover of this book.
Thank you all PIs for teaching and explaining various science matters andpeculiarities of the science business in silent and loud ways. Thanks forconvincing funding bodies to support these crazy things we are doing here all
together.
Thank you all postdocs for practical advice when needed and explaining evenmore peculiarities of the science business.
Thank you all lab, workshop, administrative and technical personnel for making
impossible things possible and possible things impossible.
Thank you all PhD students for spinning together in this incredible whirlpool!

49

50

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