J Comp PhysiolA (1992) 170:565-574

Jom'l~l of Sensor-/,
and
Physlology
9 Springer-Verlag 1992

The refractive development of the eye

of the American kestrel (FMco sparverius):
a new avian model
M.E. Andison 1, J.G. Sivak 1. and D.M. Bird 2
z School of Optometry, University of Waterloo, Waterloo, Ontario, Canada N2L 3G 1
2 Macdonald Raptor Research Centre, Macdonald Campus of McGill University, 21, 111 Lakeshore Road, Ste. Anne de Bellevue,
Quebec, Canada H9X ICO
Accepted February 26, 1992

Summary. Most measures of avian visual performance deprivation myopia. First, myopia is not always
are carried out on commonly available domestic species produced in kestrels in response to form deprivation.
such as the chicken, and most of the data on avian Second, kestrels are severely myopic at hatching and
induced refractive error deals with chickens. Raptors are therefore, the direction of emmetropization is opposite
predatory birds in which good visual resolving ability is to that found in hatchling chicks.
particularly important. Behavioral studies indicate that
the eyes of raptors have two to three times the resolving Key words: Eye - Refractive error - Development -
ability of the human eye. The domestic chicken is preco- Kestrel - Myopia
cial at hatching whereas most raptors are semi-altricial.
This study was an effort to determine if the effect of early
visual deprivation on the refractive development of the
chicken eye can be reproduced in the American kestrel, Introduction
a species which is not domesticated and in which the need
for acute vision is particularly important. Form-deprivation myopia is a developmental anomaly
Visual deprivation was achieved by unilaterally apply- resulting from abnormal visual experience. The discovery
ing translucent plastic goggles over the eyes of kestrels in monkeys that form-deprivation by lid-suturing causes
two days after hatching. Refractive error was measured axial elongation and a myopic shift in refractive error
using a retinoscope and trial lenses. Ocular growth was was made by Hubel et al. (1975, cited by Curtin 1985)
monitored by A-scan ultrasonography, and frozen oc- during the course of other experimental work. Since this
ular sections of sacrificed birds. The effect of the experi- time, lid-suture myopia has been induced in monkeys
mental manipulation on the contralateral control eye and (Wiesel and Raviola 1977), tree shrews (Sherman et al.
body weight was evaluated each day over a 42-day 1977), cats (Wilson and Sherman 1977) and chicks (Wall-
period. The goggles did not significantly affect the nor- man et al. 1978).
mal changes in body weight or the normal pattern of In addition to lid-suturing and corneal opacification
ocular growth and refractive development in the un- (Wiesel and Raviola 1979), goggles of various types have
treated eyes. An analysis of the refractive state changes been used to degrade the retinal image. These include
as a result of form deprivation was made each week for opaque (Sivak et al. 1989), translucent (Wallman et al.
6 weeks after hatching on both the treated and untreated 1978; Pickett-Seltner et al. 1987) or partial occluders
eyes in a separate group of experimental birds. Visual (Wallman et al. 1978). Concave and convex spectacle
form deprivation caused a significant myopic shift in lenses (Schaeffel et al. 1988), concave and convex soft
refractive error and a significant increase in the vitreous contact lenses (Sivak et al. 1990) and concave and convex
chamber depth in the treated eyes at 3 and 6 weeks of age. hard contact'lenses fit to a modified goggle (Irving et al.
However, the amount of myopia produced is much less 1991) have been used to produce defocus of the retinal
than that induced in chicks, and in certain cases hyper- image. Restriction of the visual environment (Young
opia is produced. The kestrels recover from myopia and 1963), continuous light (Axsmith and Morin 1975) and
hyperopia within 10 days of goggle removal, after 3 to low-intensity blue light (Bercovitz et al. 1972) have
4 weeks of deprivation. produced refractive errors in a variety of animal models.
This study is the first indication that chickens may not Raising chickens in complete darkness has been shown
be a representative bird model for studying form- to produce hyperopia (Hodos 1990).
A number of different models and mechanisms of
* To whom offprint requests should be sent myopia development have been suggested. Even within
 566 M.E. Andison et al. : Eye development of American kestrel

the s a m e genus, i n v e s t i g a t o r s believe t h a t o n e m o d e l m a y Methods

n o t be sufficient. R a v i o l a a n d Wiesel (1990) h y p o t h e s i z e
t h a t t h e r e m a y be t w o different p r i m a t e m o d e l s , one for A total of 80 American kestrels were used in the study. Approxi-
rhesus m o n k e y s (Macaca mulatta) a n d a n o t h e r for mately 300 kestrels are bred per year at the Macdonald Raptor
s t u m p - t a i l e d m o n k e y s ( Macaca arctoides ). Research Centre, of McGill University in Montreal, Quebec, Cana-
da, primarily for pesticide research (Bird 1982). None of these birds
It is n o t p o s s i b l e to a p p l y d i r e c t l y the results f r o m
are normally released.
a v i a n m o d e l s o f m y o p i a to m a m m a l s / h u m a n s , d u e a
v a r i e t y o f a n a t o m i c a l a n d p h y s i o l o g i c a l differences. Care of the kestrels. All of the birds used were hatched under
T h e s e i n c l u d e such f e a t u r e s as eye s h a p e a n d v a s c u l a r i z a - artificial conditions in forced-air RolI-X incubators (Marsh Farms)
tion, the presence o f a n i c t i t a t i n g m e m b r a n e , a n n u l a r p a d maintained at 37.5 ~ and 45% humidity. At pip, eggs were placed
a n d scleral ossicles in b i r d s ( W a l l s 1942), differences in within marked wire mesh corrals to facilitate identification. They
the a c c o m m o d a t i v e m e c h a n i s m ( W e l t y 1982) a n d dif- were then transferred to a modified incubator in which the turning
ferences in r e s p o n s e to p h a r m a c o l o g i c a l agents (Walls grid was replaced with quarter-inch mesh hardware cloth covered
with krinoline cloth. The temperture was reduced to 37.0 ~ and
1942). H o w e v e r , the c h i c k e n (Gallus 9allus domesticus) the humidity was increased to 75 %. Within 24 h after hatching, the
has b e c o m e a w i d e l y u s e d a n d a c c e p t e d a v i a n m o d e l for chicks were dry. They were weighed to the nearest 1 x 10-2 g on a
s t u d y i n g m y o p i a . C h i c k e n s a r e inexpensive a n d easily Mettler top-loading balance prior to their first feeding. The chicks
m a i n t a i n e d . T h e y h a v e a r a p i d rate o f g r o w t h a n d de- were subsequently placed in a wooden still-air brooder
v e l o p m e n t a n d h a v e p r o p o r t i o n a t e l y large eyes ( H o d o s (60 cm • 55 cm x 18 cm) maintained between 34 ~ and 36 ~ at 50
1990). H o w e v e r , is the c h i c k e n a r e p r e s e n t a t i v e b i r d to 60% humidity. They remained in this brooder for 5-7 days in
cardboard corrals on a substrate of wood shavings in groups of 4-6.
model?
The chicks were then moved through a series of still-air brooders
F a l c o n i f o r m e s such as eagles, falcons a n d h a w k s are (55 cm • 55 cm x 30 cm). The temperature was reduced daily by
r e p u t e d to h a v e e x c e p t i o n a l l y keen visual acuity. T h e i r 0.55 ~ per day and the humidity was lowered to between 35 and
visual a c u i t y h a s b e e n e m p i r i c a l l y s h o w n to exceed t h a t 40%, until the chicks were able to survive at ambient room tem-
o f h u m a n s ( S h l a e r 1972; F o x et al. 1976). A n a t o m i c a l perature (27 ~ ~ at approximately two weeks of age. From
evidence to s u p p o r t this c l a i m is p r o v i d e d b y the fal- this time until they were sacrificed, chicks were housed on a sub-
strate of wood chips in cardboard boxes (30 cm • 30 cm x 35 cm)
c o n i f o r m r e t i n a w h i c h h a s a h i g h e r d e n s i t y o f cones t h a n with removable wire mesh tops.
the h u m a n r e t i n a ( W a l l s 1942). U s i n g an o p h t h a l -
m o s c o p i c m e t h o d , S h l a e r (1972) m e a s u r e d the retinal Controlbirds. A group of 10 ungoggled kestrels was used as controls
i m a g e q u a l i t y o f the A f r i c a n s e r p e n t eagle (Dryotriorchis to study normal refractive development and eye growth. These birds
spectabilis) a n d d e t e r m i n e d its visual r e s o l u t i o n to be- were weighed each day before their first feeding. For two days after
t w e e n 2.0 a n d 2.4 times h u m a n r e s o l u t i o n . hatching, it was not possible to measure the refractive error because
A classic t w o - c h o i c e d i s c r i m i n a t i o n t a s k has been used the chicks' eyelids were naturally constricted. At hatch, pulling the
to b e h a v i o r a l l y test the visual a c u i t y o f a n A m e r i c a n lower lid down revealed an opening only 1.5 mm in diameter. By
two days of age, it was possible to see a retinoscopic reflex and the
kestrel (Falco sparverius). T h e results s h o w e d t h a t the
refractive error could be assessed. Refractive measures were made
kestrel h a s a t h r e s h o l d v a l u e o f 160 cycles/degree, a value for both eyes to the nearest 0.5 diopter in the horizontal meridian
w h i c h is 2.7 t i m e s the h u m a n g r a t i n g a c u i t y value o f 60 each day using a standard clinical streak-retinoscope and trial
c y c l e s / d e g r e e ( F o x et al. 1976). lenses. The retinoscope was powered via a transformer to prevent
A m a j o r difference b e t w e e n kestrels a n d chick is t h a t fluctuations in the beam intensity during prolonged periods of use.
kestrels a r e s e m i - a l t r i c i a l while chicks a r e precocial. A t A working distance of 0.5 m was used. It was assumed that the
kestrels were fixating the environment beyond the experimenter.
h a t c h i n g , s e m i - a l t r i c i a l b i r d s a r e d o w n - c o v e r e d a n d are
Ultrasonography was performed on both eyes each day using an
c h a r a c t e r i z e d b y p a r t i a l l y c l o s e d eyes a n d a d e p e n d e n c y Oculometer 4000 A-scan ultrasound (Radionics Medical) to assess
u p o n t h e i r p a r e n t s f o r f o o d for s o m e t i m e after hatching. axial length. Control birds were sacrificed by decapitation at
A t h a t c h i n g , p r e c o c i a l b i r d s a r e d o w n - c o v e r e d , have 6 weeks of age.
o p e n eyes a n d a r e i n d e p e n d e n t o f their p a r e n t s f o r f o o d A freeze-sectioning technique was used to measure intraocular
( W e l t y 1982). T h e d e g r e e o f visual a c u i t y r e q u i r e d b y dimensions. The heads of 8 kestrels were placed on the stage of a
freezing microtome which was connected to a cylinder of pres-
each o f these species a t h a t c h i n g a n d as t h e y d e v e l o p m a y
surized carbon dioxide. The head was trimmed horizontally to the
be a n a d a p t a t i o n to t h e strategies t h e y use to o b t a i n f o o d . level of the eyes with the microtome blade. A single lens reflex
A n o t h e r p o i n t o f difference b e t w e e n chickens a n d kes- camera was mounted on a tripod and arranged over the sectioning
trels is t h a t c h i c k e n s a r e h i g h l y d o m e s t i c a t e d a n d kestrels apparatus. Photographs were taken of the head as serial sections
a r e wild. I t is c o n c e i v a b l e t h a t these f a c t o r s m a y be were removed. A millimetre ruler placed at the level of the head was
reflected in differences seen in the refractive d e v e l o p m e n t included in each frame taken as a control for magnification. Contact
sheets were developed and measured to establish the frame showing
o f e a c h o f these b i r d s a t h a t c h i n g a n d as t h e y m a t u r e .
the largest eye diameter, and hence equatorial eye dimensions.
T h e p u r p o s e o f the p r e s e n t s t u d y was to e x a m i n e a n d Slides of the selected frames were made and tracings were drawn of
e v a l u a t e w h e t h e r the c h i c k e n is a r e p r e s e n t a t i v e a v i a n the projected corneas in order to measure their radii of curvature.
m o d e l f o r s t u d y i n g the genesis o f f o r m - d e p r i v a t i o n m y o - The formula used to approximate corneal radius of curvature is,
pia. A n o t h e r a v i a n species, t h e A m e r i c a n kestrel, which r = y2/2S § S/2, where r=radius of curvature, 2y=any chord and
h a s different b e h a v i o r a l a n d visual a d a p t a t i o n s , was used S = sagitta of that chord. This formula assumes that the cornea is
to d e t e r m i n e w h a t effects f o r m - d e p r i v a t i o n w o u l d h a v e spherical within the limits of the chord (Fincham and Freeman
1974). The radius of curvature was converted to diopters using the
o n its r e f r a c t i v e d e v e l o p m e n t . formula, F = (n 1_ n)/r where n is the index of refraction of air (1.0),
r is the radius of curvature of the cornea and n 1 is the index of
refraction of the cornea. A corneal value of 1.33 is used instead of
M.E. Andison et al.: Eye development of American kestrel 567

1.37 to compensate for the negative effect of the posterior surface made and tracings were drawn of the projected corneas in order to
of the cornea (Fincham and Freeman 1974). measure their radii of curvature. Due to the fact that a limited
number of such tracings were possible, the corneal curvature data
Treated birds - Group L Once an initial refractive error could be for treated birds is small and sample sizes vary from only 1 to 7 for
determined, a group of 10 kestrels had goggles unilaterally applied the various age groups.
to the down surrounding the right eye. The contralateral eye served The remaining 5 kestrels had their goggles removed at 30 days
as a control. The goggles, 0.40 mm thick, measured 17.0 mm in of age and served as a recovery group. Each day refractive error
diameter and had a radius of curvature of 5.5 mm. Goggle clarity changes were assessed by retinoscopy. Ultrasound measures were
was degraded with 400-grade sandpaper to prevent sharp images made to determine changes in the treated or control eyes. These
from reaching the retina (Pickett 1986). This group of birds was birds were sacrificed at 40 days of age by decapitation.
treated in an identical manner to the control group, except for the
application of the goggle. Goggle transmittance properties. The transmittance properties of the
Each day, birds were weighed prior to their first feeding. Retino- goggles were determined using a portable spectroradiometer (model
scopy and ultrasonography were performed each day on the control LI-1800, LI-COR, Inc., Lincoln, Nebraska, USA). Wavelengths
(untreated) eye. The external surface of the goggles was cleaned with from 400 nm to 800 nm in 2 nm intervals were used. A tungsten
water and tissues as needed. 100 W light was used as the source illumination. Five goggles were
At 6 weeks of age, on the day of sacrifice, goggles were removed, tested and a composite plot of percent transmittance versus
refractive measures were made and ultrasonography was performed wavelength was produced.
on both treated and control eyes. Eight kestrels were used for
freeze-sectioning to examine possible differences in intraocular di-
mensions. Slides of the chosen frames were made and tracings were
drawn of the projected corneas in order to measure their radii of Results
curvature.
Body weight data
Treated birds - Group II. A group of 60 kestrels had goggles applied
to the down surrounding one eye; the contralateral eye served as T h e initial b o d y weights, m e a s u r e d p r i o r to the first
a control. Initial refractive errors were measured and ultrasound
measures were made on the second day after hatching. A goggle was feeding, were p o o l e d across g r o u p s giving a t o t a l s a m p l e
applied to the left eye of 10 birds and to the right eye of the size o f 80 birds. I n a few t r e a t e d cases, goggles fell of f
remaining 50 birds in order to control for any possible bias of b e f o r e a n e x p e r i m e n t w as t e r m i n a t e d . B o d y w e i ght s f or
laterality. Fifty-five birds were sacrificed by decapitation in small t r e a t e d birds i n c l u d e o n l y f o r t h o s e birds o n w h i c h a
groups at 7, 10, 14, 21 or 28 days of age. Birds from each of these goggle r e m a i n e d a t t a c h e d to the h e a d unt i l the t i m e o f
age groups were assessed for refractive error and eye-size differences sacrifice (n = 48). F o r the birds sacrificed at 42 days o f
between treated and control eyes following goggle removal and
before being sacrificed. Measurements from frozen sections were age ( n = 20) there w as no significant difference in t he
used to determine developmental changes for the treated and un- initial o r final b o d y w e i g h t s b e t w e e n the c o n t r o l a n d
treated eyes over time. Slides of the appropriate frozen sections were t r e a t e d ( g r o u p I) birds. F i g u r e 1 illustrates the b o d y

140

_E
. C~
m
{33

"O
O
m

Fig. 1. Body weight growth curves for

9 Control body weights the control (n = 10) versus group I
A Group I body weights (n = 10) kestrels for the first 6 weeks after
hatching. Means and standard deviations
are in grams
I I I I I I
10 20 30 40
Days
568 M.E. Andison et al. : Eye development o f American kestrel

10

O-

O.
o
"0

-10 -

>
O

N
rr

-20-

9 Control OD Fig. 2. M e a n refractive errors o f the

control birds (n = 10, O D and OS) and
z~ Control OS the group I kestrels (n = 10, OS only)
Group I OS for the first 6 weeks after hatching.
Means and standard deviations are in
-30 dioptres
t I t I ~ I t I
0 10 20 30 40
Days

weight growth curves for the control birds versus the

2
treated birds (group I) during the first 6 weeks after
hatching. Each point represents the average body weight
for 10 birds. There is virtually no difference between the
growth curves o f the birds in these two conditions. ~_ 0
O

b
Refractive error data -2

">
A comparison o f the changes in refractive error during "6 -3
the first 6 weeks o f age was made between the control and
treated (group I) birds. The average mean refractive error c

for each eye o f 9 control birds was compared to the

average mean refractive error for the untreated (left) eye -6 9 Untreated eye
of 10 birds in group I (Fig. 2). Each point on the graph [] Treated eye "~
in Fig. 2 represents the average o f 9 eyes of birds in the -7 I I J I I I

control group or 10 eyes o f birds in group I. It is evident 7 10 14 21 28 42

that there is virtually no difference in the changes in Days after hatch
refractive error between the two eyes of the control birds Fig. 3. The average final refractive error o f the treated and untreated
or the untreated eye o f the birds in group I. eyes for kestrels in each age group. Means and standard errors are
The normal refractive changes that occur after hatch- in dioptres
ing follow a very interesting course. At hatching, kestrels
are very myopic, in the - 20 to - 25 dioptre range. F r o m treated eyes, with a range o f +4.5 to - 1 2 . 0 dioptres.
about day 7 to day 12 there is a rapid change in refractive With the exception o f the 28 day-old birds, the treated
error towards emmetropia. F r o m this point in develop- eyes become more myopic with age while the untreated
ment, the refractive error centres about zero dioptres eyes centre about emmetropia.
(emmetropia). Initial refractive error data were available for a total
The difference in refractive error between the un- of 78 birds. The initial refractive error does not differ
treated and treated eyes increases with age, with the significantly among age groups (Table 1). There is no
exception of the 28 day-old birds (Fig. 3). This group had significant initial or final refractive error difference be-
an unusual degree of variability in refractive error in the tween the right and left eyes o f birds in the control group.
M.E. Andison et al. : Eye development of American kestrel 569

Table 1. Mean initial and final refractive errors in dioptres, the maxima, minima and standard deviations for the treated (T) and untreated
(C) eyes of kestrels at each age

Age Initial Mean Initial Dev. Maximum Minimum Final Mean Final Dev. Maximum Minimum
(days) Number Std. Number Std.
Refr. Err. Refr. Err.

42 OD (n=9) -21.0 4.56 - 12.0 -24.5 OD (n = 10) -0.2 0.44 9.5 -0.5
(control) OS (n=10) -22.6 3.81 -14.3 -25.5 OS (n=10) 0.0 0.50 7.5 -0.5
(group I) OD (n= 10) -22.2 3.71 - 13.5 -25.0 OD (n= 10) -6.3 5.48 0.5 -"i6.5
OS (n=10) -21.9 4.37 -12.0 -25.0 OS (n=10) -0.4 0.61 0.5 -1.5
28 T (n = 17) - 22.4 5.38 - 13.0 - 30.0 T (n = 8) - 1.3 5.86 4.5 - 12.0
C (n= 17) -21.3 6.10 -11.2 -30.0 C (n=8) 0.5 1.77 4.5 -1.5
21 T (n=20) -19.9 7.86 -2.0 -36.7 T (n=12) -3.5 4.81 3.5 -12.5
C (n=20) -23.2 6.61 -8.0 -40.0 C (n= 12) -0.2 1.70 1.5 -5.0
14 T (n=6) -26.4 2.40 -23.7 -30.0 T (n=5) -3.5 5.06 3.5 -9.5
C (n=6) -24.1 3.64 - 19.5 -30.0 C (n=5) -0.7 0.45 -0.5 -1.5
10 T (n= 10) -23.8 3.59 -17.5 -26.7 T (n=7) -2.6 3.86 0.5 -10.5
C (n = 10) - 22.0 3.91 - 13.9 - 26.7 C (n = 7) 0.5 1.75 3.0 - 1.5
7 T (n=6) -22.2 4.93 - 17.8 -28.3 T (n=4) -0.3 2.53 3.5 -2.0
C (n=6) -24.3 3.63 -16.7 -30.0 C (n=4) 1.8 2.87 3.5 -2.5

Table 2. Mean final axial lengths of the treated versus untreated

kestrel eyes in millimetres for each age as assessed by ultrasound

Age Untreated Standard Treated Standard

(days) (mm) Deviation (mm) Deviation

42 12.67 0.36 12.80 0.42

(n = 10) (n = 10)
28 12.33 0.53 12.61 0.77
(n = 12) (n = 12)
21 11.85 0.54 12.46" 0.60
(n = 12) (n = 12)
g~ 10 11.10 0.38 11.34 0.38
(n = 7) (n = 7)

Asterisk (*) denotes a significant difference between treated and

untreated eyes (P< 0.05)

2 3 4 5 6 7 8 9 10
Days Fig. 4. N o t all o f the t r e a t e d eyes were m y o p i c w h e n the
Fig. 4. The refractive error changes in dioptres of the treated eyes goggle was r e m o v e d . H o w e v e r , r e g a r d l e s s o f t h e refrac-
of kestrels in the recovery group in the 10 days following removal tive e r r o r o f the t r e a t e d eye w h e n t h e goggle w a s re-
of the goggle m o v e d , w i t h i n 10 d a y s t h e refractive e r r o r m a t c h e d t h a t
o f the u n t r e a t e d eye in 4 o f 5 birds.

F o r the t r e a t e d b i r d s ( g r o u p I) h o w e v e r , the m e a n final

refractive e r r o r o f the t r e a t e d eye ( - 6.25 d i o p t r e s ) dif- Eye size data
fered significantly f r o m t h a t o f the u n t r e a t e d eye ( - 0 . 4 0
dioptres (df=18, t=3.35, P<0,005). The only other (i) Ultrasound data. T e n m e a s u r e m e n t s o f a s t a n d a r d
age g r o u p h a v i n g a significant final refractive e r r o r dif- o b j e c t were m a d e w i t h the u l t r a s o u n d i n s t r u m e n t to
ference b e t w e e n the t r e a t e d a n d u n t r e a t e d eyes was the d e t e r m i n e i f a significant a m o u n t o f v a r i a b i l i t y in the
g r o u p a t 21 d a y s o f age ( - 3 . 5 4 d i o p t r e s versus - 0 . 2 1 e x p e r i m e n t a l m e a s u r e s was d u e to the device o r m e a s u r e -
d i o p t r e s , respectively). T h i s w a s r e v e a l e d b y a o n e - w a y m e n t process. T h e a m o u n t o f v a r i a b i l i t y (4-0.05 m m )
A N O V A using refractive e r r o r as the d e p e n d e n t vari- w a s n o t c o n s i d e r e d significant.
a b l e a n d age as the i n d e p e n d e n t v a r i a b l e ( d f = 1,22, C o m p a r i s o n s were m a d e o f b o t h eyes o f b i r d s in the
F = 5.13, P < 0.05). c o n t r o l g r o u p a n d the u n t r e a t e d (left) eye o f b i r d s in
It was also o f interest to d e t e r m i n e if the t r e a t e d eye g r o u p I f o r the first 6 weeks a f t e r h a t c h i n g . T h e r e w a s
w o u l d r e t u r n to a n o r m a l refractive state f o l l o w i n g a n v i r t u a l l y n o difference in the r a t e o f g r o w t h b e t w e e n the
e x t e n d e d p e r i o d ( 4 - 5 weeks) o f occlusion. F i v e b i r d s in right a n d left eyes o f b i r d s in the c o n t r o l g r o u p , o r
a r e c o v e r y g r o u p were r e f r a c t e d each d a y for 10 d a y s b e t w e e n these eyes a n d the u n t r e a t e d eye o f b i r d s in
a f t e r r e m o v a l o f the goggle. T h e s e d a t a a r e p r e s e n t e d in g r o u p I.
570 M.E. Andison et al. : Eye development of American kestrel

Table 3. Average dimensions and standard deviations in millimetres between the untreated eyes of the treated birds (group I)
of the treated and untreated eyes of birds at each age from frozen and both eyes of the control group on any o f the dimen-
sections sions. The treated eyes tended to be larger equatorially
Age Eq. Ax. Ant. Ch. Vit. Ch. Lens Ax. Lens Eq. ( d f = 14, t = - 3.35, P < 0 . 0 0 5 ) and had deeper vitreous
(days) Diam. Diam. (S.D.) (S.D.) (S.D.) (S,D.) chambers ( d f = 1 4 , t = - 2 . 7 6 , P < 0 . 0 5 ) than the un-
(S.D.) (S.D.) treated eyes for the birds in group I. Since only 6 of the
8 treated eyes were myopic, averages and standard devia-
42 days tions o f each dimension using only the myopic eyes were
controls 16.6 14.1 1.6 8.5 4.0 6.6 calculated and compared with the dimensions obtained
(OD, (0.32) (0.61) (0.38) ( 0 . 3 1 ) (0.16) (0.29) for the untreated eyes o f birds in group I (n = 8). The
OS) values obtained using the myopic eyes tended to give the
(n = 16)
largest values for the equatorial dimensions of the globe
group I 16.6 14.2 1.8 8.5 4.0 6.5 ( d f = 12, t = - 5.02, P < 0.0005) and the vitreous chamber
(UT, (0.22) (0.50) (0.32) (0.40) (0.14) (0.20)
n=8) depth ( d f = 12, t = - 2 . 9 6 , P < 0.01). F o r this reason, only
frozen sections of birds that had manifested a myopic
(T, 17.0"** 14.5 1.5 9.0* 4.1 6.3
n = 8) (0.26) (0.45) (0.23) (0.41) (0.20) (0.14) refractive error in the treated eye were used for each age.
The treated birds (group I) were the only group
(M, 17.1"***14.6 1.4 9.1"* 4.1 6.3
n = 6) (0.15) (0.49) (0.27) (0.42) (0.19) (0.12) having a significant difference in the average equatorial
diameter between the untreated and treated eyes (df = 12,
28 days 16.6 14.1 1.6 8.8 3.9 6.5 t = - 5 . 0 2 , P<0.0005). F o r all of the other age groups,
(UT, (0.26) (0.86) (0.62) ( 0 . 3 2 ) (0.12) (0.40) the treated eye tended to be larger equatorially, but the
n=3)
difference was not significant. The treated birds at
(M, 16.6 14.3 1.6 8.8 4.0 6.6 21 days of age were the only group showing a significant
n= 3) (0.17) (0.59) (0.45) ( 0 . 6 6 ) (0.15) (0.30)
difference in the average axial diameter between the
21 days 15.7 13.1 1.8 7.7 3.7 6.0 untreated and treated eyes (df = 12, t = - 2.38, P < 0.05).
(UT, (0.44) (0.36) (0.32) ( 0 . 2 4 ) (0.24) (0.51) Again, the treated eyes for all ages tended to be larger
n=7) than the untreated eyes with respect to axial diameter.
(M, 16.0 13.6" 1.3 8.5**** 3.9 5.9 There was no significant difference between the treated
n = 7) (0.35) (0.43) (0.21) ( 0 . 3 2 ) (0.21) (0.24)
and untreated eyes of birds at any of the ages with respect
14 days 14.9 12.1 1.3 7.0 3.9 5.5 to the average anterior chamber depth, and average axial
(UT, (0.10) (0.21) (0.42) ( 0 . 3 2 ) (0.15) (0.06) or equatorial lens dimensions. There was a significant
n=3) difference for birds at 42 days ( d f = 1 2 , t = - 2 . 9 6 ,
(M, 15.0 12.2 1.4 7.5 3.6 5.5 P < 0 . 0 1 ) and 21 days ( d f = 1 2 , t = - 5 . 2 3 , P < 0 . 0 0 0 5 )
n = 3) (0.44) (0.46) (0.00) ( 0 . 3 5 ) (0.21) (0.26) with respect to the average vitreous chamber depth. The
10 days 14.1 11.9 1.6 6.9 3.3 5.5 treated eyes for the birds at 14 days had a deeper average
(UT, (0.20) (0.15) (0.32) ( 0 . 0 6 ) (0.20) (0.25) vitreous chamber depth than the untreated eyes, but the
n=3) difference was not significant. There was no difference in
(M, 13.9 11.5 1.2 6.9 3.5 5.4 the average vitreous chamber depth between treated and
n=3) (0.23) (0.26) (0.17) ( 0 . 3 5 ) (0.32) (0.22) untreated eyes of birds at 10 and 28 days of age (Table 3).
The frozen sections versus ultrasound measurements
UTdenotes untreated eye, Tdenotes treated eye, M denotes myopic were well fitted by a regression line (Y=4.01 +0.59X,
eye.
n refers to the number of eyes. df = 17, F = 26.86, P < 0.0001). These two measurements
* P<0.05, ** P < 0 . 0 1 , *** P < 0 . 0 0 5 , **** P<0.0005 were positively correlated (R = 0.78). These results sup-
port the expectation that the ultrasound measures would
be smaller due to liquid expansion on freezing. Also,
the ultrasound measures were based on an instrument
Examination o f the ultrasound data revealed that for calibrated for average sound transmission through the
each age, the treated eye was longer axially than the h u m a n eye. I f average sound transmission in the kestrel
untreated eye. A one-way A N O V A using axial length as eye is higher, due to a relatively larger lens, such mea-
the dependent variable and age as the independent vari- sures m a y have underestimated axial length.
able revealed that this difference was only significant for
birds at 21 days of age (df = 1,22, F = 6 . 8 8 , P < 0 . 0 5 )
(Table 2). Corneal curvature data

(ii) Frozen sections data. Frozen sections were used from The measurement accuracy of the radii of curvature was
a total o f 32 birds. F r o m the frozen sections, com- estimated to be + 0.05 mm. The average corneal radii of
parisons were made o f the anterior and vitreous chamber curvature in the untreated eyes for the birds at 42, 28, 21,
depths, the axial and equatorial lens dimensions and the and 14 days of age were not significantly different. The
total axial length and equatorial diameter of the globe for range of curvatures (3.3 m m to 3.5 m m ) represented a
the treated and untreated eyes o f birds at each age at range of corneal powers from 94.3 to 100 dioptres. The
sacrifice (Table 3). There was no significant difference radii o f curvature of corneas for birds at 10 and 7 days
M.E. Andison et al. : Eye developmentof American kestrel 571

and at hatch were progressively shorter with decreasing largest myopic refractive errors. Thus, the hatchling
age. The range of curvatures (3.1 mm to 2.1 mm) repre- kestrels had the shortest corneal radii of curvature. The
sented a range of corneal powers from 103.1 to 157.1 radii of curvature of the corneas from progressively older
dioptres in the untreated eyes. The radii of curvature kestrels increased up to 14 days, whereupon they did not
were not significantly different in the untreated and differ significantly to 6 weeks of age. Thus, the corneal
treated eyes for birds aged 42, 28, 21, 14 and 10 days. results support the refractive error measurements which
The small radius of curvature (2.1 mm) and associated demonstrate extreme myopia in the very young chicks
corneal power (157.1 dioptres) of the hatchlings indicates and emmetropia from about day 12 to 6 weeks of age in
that the cornea may be involved in the extreme myopia the untreated eyes. However, the small sample sizes must
measured in the young kestrels. The radii of curvature be kept in mind in interpreting this data. Troilo (1990)
are progressively longer with increasing age up to reported that dark-rearing produced both hyperopia and
14 days, which corresponds to the progressively less ocular enlargement in chickens, but attributed the
myopic refractive errors measured in the untreated eyes hyperopia to an increase is corneal radius of curvature.
up to this age. The fact that such a high degree of variability was
found in the refractive errors of the treated eyes was
surprising. The goggle was applied before emmetropia
Goggle transmittance had been reached and the refractive error was still one of
severe myopia. The refractive errors of the treated eyes
The transmittance properties of 5 goggles were tested to from which goggles were removed before emmetropia
ensure that the kestrels were all receiving the same qual- should have been reached (7 and 10 day-olds) were closer
ity and quantity of light. There is no significant difference to emmetropia than when they were occluded. This was
between the 5 measures. The curves are slightly non- not anticipated since the goggle was expected to cause a
monotonic, having a small decrease between 560 nm and myopic shift in refractive error. The treated eyes which
630 nm. The longer (red) wavelengths are transmitted could have emmetropized (14, 21, 28 and 42 days-olds)
more by almost 15% than those in the blue range. This manifested progressively larger myopic shifts in refrac-
is to be expected because the goggles are slightly bluish tive error /f the initial refractive error was emmetropia,
in colour. Light transmittance of the goggles varied from with the exception of the group at 28 days of age. How-
about 58 to 64% from 400 to 700 nm. ever, the initial refractive error was, on average, - 2 2
dioptres, which means that these eyes were manifesting
progressively smaller myopic shifts in refractive error.
Discussion Since only the initial and final refractive errors of the
birds sacrificed at each of the 5 youngest ages were
This study is an attempt to determine if the chicken is a measured, it is assumed that their refractive errors follow
representative avian model for studying form-depriva- the same developmental changes as those of the 20 birds
tion myopia. It uses an accepted technique with a dif- refracted each day for 6 weeks.
ferent species, the American kestrel. The untreated eye It is possible that short periods of occlusion do not
of a monocularly occluded kestrel appears not to be interfere with the normal emmetropization process. The
affected by the contralateral treated eye, a finding which average refractive error in the treated eyes of birds at 10
is consistent with the results of form-deprivation experi- days of age (-2.61 + 3.86 dioptres, S.D.) matches the
ments using chickens. In both species, the untreated eye average refractive error of the untreated eyes of the
does not differ from the eyes of control birds with respect control and treated groups' refractive errors for this age.
to refractive error, intraocular dimensions, external di- Therefore, the eyes might be emmetropizing to a certain
mensions, weight or corneal curvature. extent despite the goggle. In fact, the extreme myopia in
Using chickens, previous investigators have reported the early period may mean that the occluders make little
substantial myopic shifts in refractive error and large difference in vision. By two weeks of age, the effect of
increases in the external dimensions and weight of the blurred retinal images may be affecting the refractive
treated eye following visual field restriction (Wallman et development of the eye. When compared to average
al 1978) and form deprivation (Pickett 1986). The sever- refractive errors of the eyes of the control group and the
ity of the myopia produced in the kestrels was, on av- untreated eyes of group I, the relative amount of myopia
erage, relatively minor even after prolonged periods of from 14 days onwards is increasing (with the exception
form deprivation. Thus, the kestrel data revealed that the of the 28 day-old birds.) Among all of the age groups,
dimensions of the treated eyes were only marginally there is the most variability in the refractive errors in the
larger than those of the untreated eyes. treated eyes of the 28 day-old birds. This group also had
From hatching to about 12 days of age, the eyes of all the second largest range of refractive errors of any of the
young kestrels approach emmetropia from an average treated eyes. There may be too much variability in the
refractive error of approximately - 22 dioptres. The av- refractive errors up to the first 10 days after hatching to
erage refractive state of the untreated eyes of kestrels draw any real conclusions about what is happening
aged 14 days to 6 weeks of age is emmetropia. during this period.
The dioptric power of the cornea was inversely If the distribution of the refractive errors of the un-
proportional to age. The corneas having the shortest treated eyes is considered, there were 3-4 birds showing
radii of curvature were from eyes which manifested the hyperopia in the untreated eye at 7 days of age. At 10 and
572 M.E. Andison et al.: Eye developmentof American kestrel

28 days of age, there was one bird in each group showing ined the normal refractive errors of chickens just before
hyperopia (3.0 and 4.5 dioptres), respectively. When the hatching and at hatching. At 21 days of incubation,
refractive errors of the birds in the control group and shortly before hatching, the average refractive error was
group I are examined at 7, 10 and 28 days of age, the + 15.5 + 4.70 dioptres (S.D.). At hatching, the refractive
variability in these data are sufficient to account for the error averaged +11.3:t:3.08 dioptres (S.D.). In a
hyperopic refractive errors measured at the younger ages. separate study, Pickett (1986) found the refractive errors
For this reason, it is assumed that the slightly hyperopic of chickens to average + 2.7 + 0.2 dioptres (S.E.) within
average refractive errors in the untreated eyes of the one day after hatching. Within the first 36 hours after
groups at 7 and 10 days are within the expected range of hatching, their refractive errors decreased rapidly and
refractive errors. The use of larger sample sizes would within 7 days they were within + 1.0 dioptres of em-
decrease the variability measured in these groups. Sam- metropia (Pickett 1986). The kestrels have an average
piing the birds at 4, 6, 8 and 10 days of age may give a myopic refractive error at hatching of -22.2 4- 5.5 diop-
better indication of what is happening to the treated eye tres (S.D.). They emmetropize within 12 days after hatch-
as the other eye is emmetropizing. It may be more valu- ing. This rate of emmetropization occurs at a slower rate
able to concentrate on the period between 10 and 42 days than that of the chickens.
after hatching. After an extended period (42 days) of occlusion, the
average amount of myopia produced in the kestrel eyes
( - 6.25 4- 5.48 dioptres, S.D.) was substantially less than
Emmetropization and recovery that measured in the chickens. The trend towards an
increasingly more myopic refractive state with longer
Experiments in which the development of refractive er- periods of occlusion agrees with studies of chickens (Selt-
rors result from manipulations of visual experience sup- ner et al. 1988). The magnitude of eye growth in the
port the claim that visual regulation of eye growth oc- treated versus the untreated eyes of the kestrels was also
curs. In addition, near work in humans (Curtin 1985) and significantly smaller than that found in chickens (0.5 mm
experimental restriction of the visual environment in versus 1.5 mm at 14 days), but again the direction of the
monkeys (Young 1963) have both been positively cor- change was the same. A longer period of occlusion was
related with myopia. accompanied by an increase in the axial difference be-
Wallman and Adams (1987) have suggested that tween the treated and untreated eyes. The form-depriva-
emmetropization is a vision-dependent phenomenon. In tion experiments of Seltner et al. (1988) using chickens
chickens, if the visual field is restricted during the period showed that within 14 days, there was a substantial
of rapid eye growth, high levels of myopia are produced. myopic shift in refractive error, averaging - 10.7 + 3.12
A return to a normal refractive state follows the restora- dioptres (S.D.). These changes in refractive error were
tion of clear vision during this time. Up to 4 weeks of age, accompanied by a 19% increase in the axial length and
the refractive state of the kestrel eye is "plastic" enough a 21% increase in the wet weight of the treated eyes when
to recover from induced refractive errors. It seems that compared to the contralateral controls (Seltner et al.
when the kestrel retina is presented with a blurred image, 1988).
the eye does not "know" in which direction to find em- A separate experiment examined the development of
metropia because the refractive errors are both hyperopic experimentally induced myopia in the Japanese quail,
and myopic after 3 or 4 weeks of occlusion. It is interest- Coturnix coturnix japonica (Andison, unpublished re-
ing to note that the eyes were capable of reaching em- suits). The quail became significantly myopic in the
metropia from either direction within 10 days. treated eye within 7 days after hatching when they were
In young kestrels, the earliest refractive errors mea- monocularly occluded. The quail are precocial hatch-
sured are extremely myopic. For the first two days after lings, like the chickens. These data agree with the chicken
hatching their eyes are partially closed. Therefore, no results. The findings with the quail are also valuable
clear images are reaching the retina during this time. because they provide a control for the methodology used
Over the next few days the young kestrels keep their eyes with the kestrels. The goggles used were identical to those
open for more extended periods of time. This factor applied to the kestrels; the refractive technique was also
might be involved in the process of emmetropization. identical. The principal difference between the quail and
The eyes become more emmetropic with more prolonged kestrels is that the quail are precocial and the kestrels are
periods of clear form vision. Troilo (1990) reported that semi-altricial. It was not possible to study quail em-
in chickens, emmetropization is achieved by changes in metropization in more detail, but the results of this initial
the vitreous chamber depth. Myopic and hyperopic eyes study do indicate that they are hyperopic when they
show decreased and increased growth rates, respectively, hatch, like the chickens.
in the vitreous chamber depth when recovering from
induced refractive errors.
Models of emmetropization are based on research Is the chicken a representative bird model?
using chickens. The present study has indicated a number
of differences between chickens and kestrels in their re- The results found with the quail corroborated previous
fractive development and response to occlusion. Just findings with chickens. Both of these species are preco-
prior to hatching, chickens are extremely hyperopic. A cial. When the same technique was used with the semi-
pilot study carried out prior to the present study exam- altricial kestrel, not only were the expected refractive
M.E. Andison et al. : Eye development of American kestrel 573

error changes and ocular enlargement less spectacular, (1982) suggests that the m y o p i a measured in premature
but the normal pattern o f emmetropization also differed infants is related to the incomplete development of the
f r o m that of chickens. This m a y be an indication that eye at the time of birth (in Goss 1985). Nissenkorn et al.
precocial and semi-altricial birds, as classes o f birds, (1983) have positively correlated prematurity and m y o -
differ with respect to their processes of emmetropization. pia in pre-term h u m a n infants. Is it conceivable that
Inter-genus differences in the response to form depriva- hatchling kestrels are just " p r e m a t u r e " birds at an in-
tion have been suggested (Raviola and Wiesel 1990). complete level o f ocular development?
These authors reported that even within the same genus
of monkeys, two different mechanisms of axial elonga-
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