Prey snapping and visual distance estimation in Texas horned lizards, Phrynosoma cornutum
1 Institute for Anatomy, University of Tübingen, Österbergstrasse
3, 72074 Tübingen, Germany
2 Allgemeine Psychologie, University of Konstanz, Postfach 5560 C36, 78457
Konstanz, Germany
3 Southwestern Research Station, American Museum of Natural History, Portal,
AZ 85632, USA
* Author for correspondence (e-mail: ott{at}anatu.uni-tuebingen.de)
Accepted 18 June 2004
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Summary |
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Key words: visual depth perception, accommodation, horned lizard, tongue protrusion, fixed-action pattern
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Introduction |
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The initial goal of the present study, the evaluation of accommodation as a
distance cue, was inspired by previous work on chameleons. Although distances
to objects can be estimated visually by a number of monocular and binocular
cues (Collett and Harkness,
1982; Davies and Green,
1994
), it was found that chameleons rely solely on accommodation
to judge the distance of prey items
(Harkness, 1977
;
Ott and Schaeffel, 1995
). We
were interested in finding out whether this mechanism of depth perception is
also predominant outside the Chamaeleonidae, in other lizards with different
feeding strategies. The question was whether Phrynosoma would judge
prey distances mainly by accommodation, similar to chameleons, or whether
their different prey capture requirements, on the ground and at relatively
short distances, would promote the use of other mechanisms of visual distance
estimation.
In our experiments, the focal plane of the eye was experimentally shifted
by ophthalmic lenses that were placed in front of one or both eyes. Such
treatment should result in a systematic error of depth perception
corresponding to the power of the ophthalmic lens if accommodation is used to
judge distance (Harkness, 1977;
Ott et al., 1998
). Our results
clearly show that (1) accommodation was used by Phrynosoma to judge
distances but that (2), in contrast to chameleons, accommodation was
apparently used in combination with additional cues in determining prey
distance, such as binocular vision and/or a simple trial and error task. This
was suggested by the observation that animals with lens treatment showed an
increased duration of the tongue strike according to the lizard's unusual
ability to adjust the length and direction of the tongue's movement during
prey snapping.
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Materials and methods |
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Lizards were allowed to move freely in a glass terrarium (60 cmx30 cmx30 cm) with a sand-covered bottom. Illumination was provided by the fluorescent lights of the laboratory, and heat was supplied by an infrared bulb. Ants were collected into a short plastic tube. The tube was covered by a piece of foam rubber through which a small aperture was left that allowed the ants to crawl out one after the other. The lizards usually captured the ants directly from the foam rubber cover. Prey snapping was recorded with a high-speed video system at 500 frames s-1 (Speedcam +500; Weinberger, Dietikon, Switzerland), with two cameras for simultaneous recordings from above and from one side.
To evaluate the use of accommodation as a distance cue, the animals were
allowed to catch their prey either under binocular or monocular conditions and
with or without ophthalmic lenses. Monocular vision was achieved by placing a
small piece of cardboard in front of one eye so that the frontal visual field
was occluded. Commercially available contact lenses were used as ophthalmic
lenses and placed in front of the eye with the aid of a wire fixed to the
cranium by adhesive tape. If accommodation was being used for visual distance
estimation, the lizards would be expected to make predictable errors
corresponding to the power of the ophthalmic lens. For example, a negatively
powered lens increases the focal length of the eye and the lizard has to
accommodate more in order to compensate for the lens. Accordingly, the lizard
would judge the distance of the prey to be closer than it actually was and the
snap would be too short. The opposite would be expected for a lens with
positive power. In order to exclude tactile information when the tongue hits
the prey, it was initially planned to produce an illusory target by placing
prism spectacles in front of the eyes, similar to the study of Harkness
(1977) in chameleons. However,
we found that spectacles were not useful in Phrynosoma, which has a
much shorter tongue than the chameleon and, due to the closer distance of its
prey, would require high powers of spectacles in order to obtain a reasonable
optical displacement of the prey image. Apparently, the thick prism glass
excessively distorted the image of the prey, resulting in either no
prey-snapping response at all or random errors. As an alternative, we
restricted our experimental design to lenses of negative power that prevented
tactile information because the focal plane was shifted to a point in front of
the prey (and not behind, as with positive lenses). The powers must be strong
enough to change the focal plane to a measurable extent. The shorter the prey
distance, the weaker is the effect of the ophthalmic lens power on the overall
accommodation that the animal must exert to bring the prey into focus. Two
lens powers were used in the experiments: -9 diopters (-9 D) and -12 D. The
changes in focal point of the two lens powers used are shown in
Fig. 1. Compared with the
untreated line, both lenses induced a substantial shift in focal plane within
the typical range of prey-snapping distances (2-5 cm). Stronger lens powers
were not used in order to avoid image distortions due to thick lenses. Also,
the distance between the ophthalmic lens and the eye cannot be ignored with
higher lens powers.
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Prey distance was measured as the distance between the tip of the snout and the prey at the time when the tongue had just reached its maximal extension. It was at this time that prey was hit by the tongue tip in untreated lizards. If an animal underestimated the prey distance, its tongue was fully extended before it hit the prey. As a result, the distance between snout tip and prey was longer at the moment of maximal tongue extension than in the untreated lizards. In the experimental procedure, we determined the position of the snout tip when the tongue had reached 75% of its maximal extension. By this time in tongue protrusion, no tactile information was available to the animal, even in those cases where the distance was correctly estimated (Fig. 3A).
We were not able to investigate the refractive state of the eye directly by
infrared retinoscopy, as was done in an earlier study of the chameleon
(Ott et al., 1998). At ambient
light levels required for horned lizard activity, the fundus of the eye did
not reflect enough light to allow measurements.
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Results |
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Plasticity of the tongue strike
From inspection of the high-speed video recordings, it became apparent that
the horned lizards were able to adjust the trajectory of their tongue during
the strike in response to the moving ant
(Fig. 2). This seemed to be a
prerequisite for a successful strike since quickly running ants often moved
several millimeters during the duration of the tongue strike (100-150 ms). The
reaction time of the lizard was difficult to determine exactly since the ants
were continuously moving and, accordingly, the lizards were constantly
adjusting their heads (Fig.
2C). Nevertheless, some video sequences included sudden stops and
starts of the ants. From these, we estimated a very short lizard reaction time
of 4-6 ms after the ants started to move again. Further measurements with a
suitable experimental setup are needed to confirm this estimate. From
Fig. 3, it is apparent that
during the strike not only was the direction of the head axis to the prey
adjusted but also the lizards modified the duration of the tongue strike
according to the experimental situation.
Fig. 3B shows the change of the
protrusion length of the tongue and of the distance of snout to prey with time
in an untreated, normal-sighted animal. The protruding tongue reached its
final length within 50-80 ms. In Fig.
3C, the same animal is shown but now with a -9 D lens in front of
the left eye and an occluder in front of the right eye. Vision was now
monocular and the plane of focus shifted. As a consequence, the lizard
underestimated the prey distance and did not hit the ant at the expected
position. The animal then continued the protrusion of the tongue with lower
velocity (visible as a flattening of slopes of the black curves in
Fig. 3C) while the head was
still moving further towards the prey.
Effects of ophthalmic lenses
From Fig. 3B,C, it can be
seen that the distance of the head to the prey was variable when the animals
initiated the snap. During the strike, the head was moved forward up to a
position of 10-12 mm away from the ant. This final position was equivalent to
the length of the fully protruded tongue, which, at this time, hit the prey in
visually untreated lizards. Animals that wore negatively powered ophthalmic
lenses usually underestimated the distance towards the prey. The distance of
the head to the ant at the reference time of 75% tongue protrusion was then
longer than in untreated animals and the lizards had their tongues fully
protruded before the prey was hit. Such an underestimation was expected if the
animal uses accommodation as a distance cue. Under monocular conditions
(frontal field of one eye occluded and the other eye provided with or without
a negatively powered lens), the effect of the ophthalmic lens was noticeable
in both animals tested but to a different extent
(Fig. 4). A lens of -9 D
induced a significant underestimation of prey distance in animal 1 but not in
animal 2, where the effect of the -9 D lens was apparent but not significant
compared with the untreated situation. A significant change in the second
animal was only seen with the use of a lens of -12 D. Under binocular
conditions (both eyes without lenses or both covered with lenses of similar
power), the effect of the lens was reduced and not significant in either
animal (Fig. 4).
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Discussion |
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Effect of negatively powered ophthalmic lenses on distance estimation by accommodation
In horned lizards, we observed a clear underestimation of prey distance
after the focal plane of one eye had been changed by negative lenses (Figs
3B,C,
4). This was in accordance with
the hypothesis that horned lizards use accommodation as a distance cue,
similar to the previous report from chameleons
(Harkness, 1977;
Ott and Schaeffel, 1995
). The
effect was very clear and significant in both lizards tested even though it
was less prominent in the second lizard
(Fig. 4). Precision is a
prerequisite for the use of accommodation as a distance cue. Precise
accommodation requires high visual acuity. Based on the structure of the eye
(M.O., personal observation) and the retina
(Detwiler and Laurens, 1921
) it
is apparent that horned lizards have high visual acuity, comparable with that
of chameleons (Ott and Schaeffel,
1995
). Therefore, the eye of Phrynosoma should be capable
of detecting small deviations in image focus and, hence, be capable of precise
accommodation control. A variance of estimated distance values in each trial
might be associated with the tolerance that is caused by the depth of field of
the eye. The following calculation, however, shows that the depth of field is
very small in the eye of Phrynosoma at close distances. It is,
therefore, not a major reason for the observed variability of prey-snapping
distances. The depth of field can be calculated by the relation:
D=7.03/spatial frequency x pupil diameter
(Green et al., 1980
).
For the eye of Phrynosoma, this equation yields a value of 0.31 D
for the depth of field [pupil diameter=1.5 mm, as measured in the living eye,
and maximal resolved spatial frequency calculated by the equation
SF=PND/3 x photoreceptor-distance x 57.3
(Reymond, 1985
), assuming a
receptor spacing of 2 µm (after Detwiler
and Laurens, 1921
) and a posterior nodal distance (PND) of 0.6
x axial length (5 mm) of the eye]. With this conservative calculation
(it is very likely that the actual resolving power of the eye is higher than
estimated), the lizard would have a depth of field of 0.022 mm at a focal
distance of 2 cm, 0.06 mm at 3 cm, 0.1 mm at 4 cm and 0.159 mm at 5 cm. These
values are low compared with the experimental lens-induced shifts of the focal
plane (compare with Fig.
1).
Evidence of additional modes of prey distance estimation
While the lens-induced effect of underestimation was probably similar in
both animals, they might have used different strategies to deal with this
treatment, including other depth parameters such as motion parallax or inborn
or learned knowledge of prey size. For any animal it is advantageous to use
more than one visual distance cue and to weigh the information from each cue
according to its signal-to-noise ratio, which determines its reliability
(Davies and Green, 1994). The
kind of parameters that are used is determined by the physical constraints of
the visual system of the animal and its environment. For the toad, Collett and
Harkness (1982
) have estimated
that depth perception from disparity cues was 16 times more accurate than
distance estimation based on accommodation. The reverse was calculated by the
same authors for the eye of the chameleon, where accommodation was more
reliable than stereopsis.
The use of additional binocular cues in Phrynosoma was apparent in
the binocular trials, where both eyes were covered with lenses of similar
power (Fig. 4). In these cases,
the underestimation of prey distance nearly disappeared in both lizards
tested. It is not clear whether three-dimensional (3-D) vision was involved,
since stereopsis is difficult to determine in lower vertebrates that cannot be
trained on artificial stimuli containing nothing other than 3-D information.
Prisms that alter the direction of gaze while leaving the focus of the eye
unaffected have been used to demonstrate the presence of steropsis in toads
(Collett, 1977) and to exclude
this mechanism for chameleons (Harkness,
1977
). As mentioned earlier, we were not able to apply a similar
method in horned lizards because high-powered prisms were needed and these
distorted the image. Nevertheless, our data clearly demonstrate that horned
lizards have the ability to employ multiple systems, including accommodation,
in determining prey distances during tongue snapping.
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Acknowledgments |
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