Behavioural discrimination of polarized light in the damselfish Chromis viridis (family Pomacentridae)
Department of Biology, University of Victoria, PO Box 3020 Stn. CSC, Victoria, British Columbia, Canada V8W 3N5
* Author for correspondence (e-mail: chawrysh{at}uvic.ca)
Accepted 13 June 2005
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Summary |
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Key words: fish behaviour, visual behaviour, polarization sensitivity, e-vector, discrimination, fish vision
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Introduction |
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Planktivores, such as the damselfish Chromis viridis, form
stationary aggregations along the reef to feed on zooplankton delivered by
currents from the open ocean or during tidal events (Hobson,
1974,
1991
;
Williams, 1980
;
Thresher, 1983
). Damselfish
possess high cone photoreceptor density in their retina
(McFarland, 1991
), which
suggests exceptional visual acuity. Also, using electroretinogram (ERG)
recordings, Hawryshyn et al.
(2003
) showed that three
species of damselfish (Chromis viridis, Dascyllus melanurus and
Dascyllus trimaculatus) possess varied and complex polarization
sensitivity (PS) and four different types of cone photoreceptors: ultraviolet
(UV)-sensitive (UVS), medium-wavelength-sensitive (MWS),
short-wavelength-sensitive (SWS) and long-wavelength-sensitive (LWS)
cones.
The present study provides behavioural evidence for polarization vision in damselfish (green chromis, C. viridis). Our first objective was to assess the ability of C. viridis to discriminate between 0° and 90° e-vector orientations. These experiments were repeated, changing the brightness content of the positive and the negative stimuli alternately, to ensure that fish were choosing stimuli based on e-vector orientation rather than light intensity differences between the two stimuli. We then examined the importance of the contribution of UVS cone mechanism to e-vector sensitivity by eliminating the UV portion of the linearly polarized stimulus. Finally, we examined the ability of test fish to resolve small angular differences between e-vectors.
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Materials and methods |
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Optical system
Light was generated using a 150 W xenon lamp system, which offers a broad
spectrum of light, including the UV-A portion of the spectrum. A black metal
wall (30 cm high and 40 cm wide), with a hole, 5 cm in diameter, was placed in
front of the xenon lamp at a distance of 20 cm
(Fig. 1). The wall acted as a
light baffling system to avoid any undesired light or reflection into the
experimental area. The beam was projected through two UV-transmissive lenses
onto a beam-splitter, which transmitted 50% of the light to one optical window
of the behavioural chamber and 50% to a front-surface mirror to the second
optical window (13 cm spacing; Fig.
1). Finally, a 1.0 neutral density filter was placed in front of
the right-channel window in order to ensure that the light striking both
channels was equal in photon irradiance. Measurements of the light stimuli
within the test tank were taken using an integrating radiometer (Photodyne
model 88XLA radiometer/photometer; Optikon, Waterloo, ON, Canada). Light
passed through a diffuser (tracing paper) to remove any inherent polarized
light. Between the polarizer and the quartz windows in the test tank were two
UV-grade polarizing filters (Optics for Research, Caldwell, NJ, USA). The
diffusers and UV-grade polarizing filters were positioned in indexed holders,
which could fit onto the quartz windows of the behavioural chamber, and the
plane of polarization was manipulated as required.
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We conducted an experiment in which UV light content in the light field was blocked using a 450 nm long-pass filter (Corion Spectra Physics, Franklin, MA, USA; see Fig. 2).
Behavioural chamber
The flow-through seawater aquarium system and behavioural chamber were
connected to a seawater sump, where the water was heated, sterilized and
filtered. Prior to experiments, the behavioural chamber was filled with
seawater. Seawater from the sump fed both the aquaria and the behavioural
chamber. This maintained consistent physical and chemical properties of water
in the two areas. For each fish in the training or testing scenario, the
behavioural chamber was drained, cleaned and refilled with fresh seawater from
the sump. During training and testing, a heater and an air stone were placed
on the rear wall of the neutral compartment of the behavioural chamber to
maintain oxygenation and water temperature.
The behavioural chamber had two compartments: the response and the neutral compartments (Fig. 1). The neutral compartment (60 cm x 16 cm x 30.7 cm) was used to acclimatize the fish to the experimental tank and separate the fish from the response compartment by a gate. The gate was manually operated. The front of the response compartment (30.7 cm x 16 cm x 44.8 cm) had two round quartz optical windows (diameter 6.7 cm) partially separated by a black Plexiglas barrier, through which light was passed.
Training
An operant conditioning protocol was used to train fish to respond to
polarization stimuli. Learned-choice tests included a training session, where
fish were trained to select toward a particular e-vector orientation of UV
polarized light. Such experimental design can provide evidence of animal's
visual capabilities; however, because of the difficult training tasks, sample
size was limited. In fact, training began using 15 fish; six fish died and
five fish failed to learn the task. Four fish were used in this study, which
is typical in behavioural discrimination experiments, given the length of
experimentation required to assess visual performance for an individual fish
(Neumeyer, 1984,
2003
;
Degner and Hawryshyn, 2001
;
Parkyn et al., 2003
).
Fish were divided into two groups; one group was trained to select and swim
toward the vertical e-vector orientation (0°, relative to the
gravitational axis; positive stimulus 0°, negative stimulus 90°), and
the second group was trained to the horizontal e-vector orientation (90°;
positive stimulus 90°, negative stimulus 0°). Training began by
placing the fish in the neutral chamber for 30 min to allow it to acclimate.
During this time, the gate separating the response compartment from the
neutral compartment was closed. In addition, the light stimuli were turned
off, while the external fan was left running to familiarize the fish to the
background acoustic noise. At the end of 30 min, stimulus light was turned on,
the gate was raised and the fish entered the response chamber, where it was
exposed to the light patches having two different e-vector orientations.
During initial training, fish were gently guided with a rod toward the
positive stimulus. A small piece of mysis shrimp was provided following the
selection of the correct e-vector, i.e. when fish entered the choice area
containing the correct e-vector. To facilitate fish training, a positive
partial reinforcement method was used, where correct e-vector selections were
reinforced with food every five trials
(Hawryshyn et al., 1990).
Responses are much harder to extinguish when stimulus acquisition used partial
rather than continuous reinforcement
(Williams, 1989
;
Pearce et al., 1997
;
Sangha et al., 2002
) and there
is better control over motivational state.
Once the fish had consumed the food reward, it was guided back towards the neutral compartment, and the gate was closed. The position of the positive and negative stimuli was randomised for each trial, in order to ensure that choice was based on orientation of the e-vector rather than a bias towards a particular location. Training continued until each fish responded correctly (i.e. choosing the correct e-vector orientation) at least 70% of the time, based on 20 trials.
In all experimental trials, test fish made a choice responding correctly or incorrectly.
0° versus 90° e-vector discrimination experiments
Two groups of fish trained to either the vertical or to the horizontal
e-vector were presented with a choice between 0° and 90° stimuli
(N=4).
In the response compartment, fish had to enter the choice area entirely for a response to be scored (Fig. 1). The time required to enter the choice area (either positive e-vector or negative e-vector) was recorded using a timer. Trials were considered valid when the choice area was occupied for at least 120 s subsequent to the opening of the gate. Ten trials were conducted for each test day for an individual fish, with a total of 40 trials used to calculate the fish's choice performance.
Brightness test
To ensure that fish were choosing stimuli based on e-vector orientation
rather than light intensity differences between the two stimuli, brightness
tests were conducted (Jacobs,
1981). The light intensity of both positive and negative stimuli
was manipulated using a one neutral density filter (1.0 ND). A total of 80
trials were conducted for each fish (N=4), where 40 trials were
carried out by placing the neutral density filter in front of the 90°
window (90°+1 ND), and the other 40 trials with the filter in front of the
0° window (0°+1 ND). The neutral density filter was randomly placed in
front of the positive or negative stimulus. 10 trials were conducted each day
for an individual fish.
Eliminating UV light from the polarization stimuli
0° and 90° e-vector discrimination experiments were repeated using
a 450 nm long-pass filter. This optical filter eliminates the UV portion of
the spectrum from the light fields of the two stimuli.
Fig. 2 illustrates the spectral
distribution of the light field when the 450 nm long-pass filter was used. Two
fish were used; fish A, which was trained to select the 90° e-vector
orientation, and fish B, which was trained to select the 0° e-vector
orientation. Forty trials were conducted for each fish.
Minimum angular difference in e-vector discrimination
Experiments were conducted using the same two groups of fish used for the
0°/90° e-vector discrimination test (N=4). Group one, which
was trained to respond to the 0° e-vector, was presented with comparison
e-vectors between 5° and 45°. The comparison e-vectors were randomly
presented, and both choice frequency and time to respond were recorded. Forty
trials were conducted per fish for each comparison e-vector.
This protocol was repeated with the second group, where the reference
90° e-vector fish were randomly presented with e-vectors of comparison
between 85° and 45°. The angular difference between the positive
e-vector and the comparison e-vector was determined (termed
e-vector).
One fish (fish C) was re-trained to select 45° e-vector orientation to
investigate the possibility that e-vector may change with different
reference e-vectors. Such comparisons are necessary since, like colour vision,
photoreceptor mechanism interaction can affect discrimination performance.
The fish trained to 45° died before all sessions of comparison could be completed. Forty trials were conducted comparing 45° with each of 0°, 5°, 10°, 15°, 20°, 25°, 30°, 35°, 40° and 55°. Thirty trials were conducted comparing 45° with each of 50°, 60°, 75° and 90°, and 20 trials were conducted comparing 45° with 65°.
Statistical analysis
In all experiments, 10 trials were conducted for each test day for an
individual fish, and the correct choice frequency recorded. Four days of
experiments for each fish provided a total of 40 trials per fish to calculate
the fish's choice performance. The correct choice frequencies of each test day
were averaged, and the standard error calculated.
Statistical analyses for all four fish required the use of the binomial
distribution model of Bernoulli trials since the outcome of all the
experiments was either a correct or incorrect choice. Therefore, the
probability was calculated using the binomial probability formula:
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Results |
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The time to respond was recorded during both training sessions and experiments. During the experimental training, the time to respond after the opening of the gate diminished with consecutive training sessions in each fish, and in particular, it decreased considerably when fish began to select the correct stimulus (Fig. 3B).
0° versus 90° e-vector discrimination
All four of the C. viridis tested were capable of distinguishing
0° from 90° e-vectors over 40 trials
(Fig. 4). Fish A and C were
trained to swim towards 90° e-vector orientation (85% and 80% correct
choice frequency, respectively), whereas fish B and D were trained to select
0° e-vector orientation (80% correct choice frequency in both fish). The
probability of correct choices occurring by chance is
<104 in each case. A one-sample t-test of the
four frequencies against a null hypothesis of random choice was also highly
significant (t=25, d.f.=3, P<104).
During the trials, the positions of the reference e-vector and the comparison e-vector were changed randomly. To satisfy our concern that the fish might have a lateral bias for choice, the choice frequencies for either left or right presentation were compared with the left/right distribution of the e-vector of reference. Table 1 shows that choice frequencies were not biased by side preference.
|
The brightness test
The brightness test confirmed that the choice between the horizontal and
the vertical plane of polarized light (90° and 0° e-vector
orientation, respectively) was made based on the orientation of the e-vectors,
independent of the light intensity of the stimuli
(Fig. 5). A total of 80 trials
per fish (N=4) was conducted. Each circle in
Fig. 5 represents the
percentage of correct choice frequency (mean ±
S.E.M.) when 0° was dimmer than 90°.
Each square in Fig. 5
represents the percentage of correct choice frequency when 90° was dimmer
than 0°.
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Eliminating UV light from the polarization stimuli
Fish could no longer discriminate between their respective reference and
comparison e-vectors when the UV part of the spectrum in both stimuli was
filtered out using a 450 nm long-pass filter
(Fig. 6). A total of 40 trials
was used to test each fish (N=2), and choice frequency was
approximately 50%. This clearly indicated that fish chose randomly between the
two stimuli.
|
When fish C was re-trained to respond to 45° e-vector orientation, the
smallest e-vector detected was approximately 10°
(Fig. 8). The left side of
Fig. 8 shows the choice
frequencies between the reference e-vector 45° and the comparison
e-vectors of up to 0°. The right side of the figure shows the choice
frequencies between 45° and the comparison e-vectors of up to 90°.
Fish could distinguish between 45° and 35° (62.5% correct choice), and
between 45° and 60° (70% of correct choice), but not between 45°
and 40° (50% correct choice) or between 45°and 55° (50% correct
choice). The correct choice frequencies of the fish trained to 45° showed
a notably higher resolution of discrimination.
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Discussion |
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This research demonstrated the ability of C. viridis to perceive
and utilize polarized light cues, confirming the ERG results of Hawryshyn et
al. (2003). C.
viridis discriminated between 0° and 90° e-vector orientations of
polarized light, and the discriminative capabilities were not compromised by
manipulating the brightness content of the stimuli. Therefore, choice was made
based on the e-vector orientations regardless of brightness differences
between the two stimuli (1 log photons cm2
s1 difference in intensity). The light intensity of the
negative and the positive stimuli was randomly varied during the same session
of 10 trials. This approach avoids the problem that test fish may learn to
avoid stimuli brighter or dimmer than the positive stimulus.
By contrast, fish could no longer discriminate between 0° and 90°
e-vector orientations when the UV part of the spectrum was filtered out. The
use of a 450 nm long-pass filter narrowed the spectral width of the stimuli,
with the purpose of eliminating the UV portion of the spectrum from the
polarized light field. The use of the 450 nm long-pass filter demonstrates the
critical role played by the UV portion of the spectrum for polarization
vision; when UVS cones were not stimulated, fish were incapable of
discriminating between e-vectors. Similar conclusions were found in salmonids
(Hawryshyn et al., 1990;
Degner and Hawryshyn, 2001
;
Parkyn et al., 2003
). In
Hawryshyn et al. (2003
), a
UV-transmitting filter (Shott; UG-11; Corion Spectra Physics) was used to
produce UVS cone chromatic adaptation. This disabled polarization sensitivity
(PS). Therefore, stimulation of the UVS cone mechanism is an essential
requirement for e-vector discrimination.
Perception of polarized light in the UV part of the spectrum represents an
interesting aspect of polarization vision in animals. Polarization has been
shown to be significantly lower in the UV spectrum in comparison with the
longer wavelength spectrum under clear skies and underwater
(Cronin and Shashar, 2001;
Barta and Horvath, 2004
).
However, it has been suggested that celestial UV polarized light is the most
stable and detectable cue under clouds and forest canopies
(Pomozi et al., 2001
;
Barta and Horvath, 2004
).
Mechanisms of polarization vision in C. viridis
Measurements of e-vector discrimination facilitate characterization of
C. viridis polarization vision.
Fig. 8 shows the smallest
angular difference between the reference e-vector and the comparison e-vector
(termed e-vector) when the reference e-vector was either 0° or
90°. Low values of
e-vector indicate good discrimination acuity.
Below 25°
e-vector, fish could not distinguish between the two
stimuli, with choice frequencies approximating randomness. Interestingly, when
the reference e-vector was 45°, the lowest value of
e-vector was
1015° (Fig. 8).
Changes in reference e-vector from either 0° or 90° to 45° further
illustrates the complexity of polarization vision in C. viridis and
point to the possible opponent interaction between the vertical and horizontal
polarization detectors. This experimental finding also demonstrates the
importance of experimental design for discrimination experiments, not unlike
the considerations used in colour discrimination experiments. The differential
discriminative capabilities of fish tested at different reference e-vectors
provide an important foundation for understanding the neural processing
underlying polarization vision.
While it is likely that PS in damselfish and salmonids mediates different
behavioural activity, these two species could conceivably have the same
polarization detection/cone mechanisms. PS in salmonids has been investigated
using compound action potential (CAP) recording from the optic nerve, and a
two-channel system was found, where one detector was maximally sensitive to
0° e-vector orientation and the other to 90° e-vector orientation
(Hawryshyn and McFarland,
1987; Parkyn and Hawryshyn,
1993
; Coughlin and Hawryshyn,
1995
; Novales-Flamarique and
Hawryshyn, 1997
). ERG data
(Hawryshyn et al., 2003
)
showed that C. viridis has complex PS, with four peaks at 0°,
45°, 90° and 135° e-vector orientation. Recently, ERG recordings
have been conducted in rainbow trout (Oncorhynchus mykiss), revealing
the same four-peaked PS pattern at 0°, 45°, 90° and 135° as in
C. viridis (S. D. Ramsden, L. Anderson, M. Mussi, T. J. Thairnberger,
M. Kamermans and C. W. Hawryshyn, unpublished).
Polarization vision and colour vision
As indicated previously, e-vector discrimination could be considered
analogous to wavelength discrimination in colour vision. Colour can be
described by intensity, purity and wavelength, as polarization can be
described by intensity, degree of polarization and e-vector orientation
(Bernard and Wehner, 1977). As
for colour vision, polarization vision is characterized by the ability to
discriminate between two lights of the same brightness but of different
e-vector orientation or degree of polarization
(Bernard and Wehner, 1977
).
Wavelength discrimination responses could be compared to e-vector
discrimination. Wavelength discrimination was used to characterize the
goldfish colour vision system (Neumeyer,
1992
). Neural interactions were found between cone mechanisms; the
spectral sensitivity curve obtained from the behavioural experiments showed
their maxima at different points with respect to the relative spectral
absorbance of the photopigments (Neumeyer,
1984
). Cone responses were modified by inhibitory interactions
between cone mechanisms, and this opponency between cone mechanisms was
described by a linear subtractive interaction
(Neumeyer, 1984
).
Similarly, the high discrimination capabilities of C. viridis at 45° could be explained assuming that two mechanisms or channels were interacting and that discrimination was most effective in the region of angular disparity where the sensitivity of the two detectors shows the greatest degree of overlap.
Functional significance of polarization vision in C. viridis
Polarization vision in C. viridis, with its e-vector
discriminative capabilities, especially around 45°, could find its use in
a number of different visually mediated behaviours. In the underwater
environment, horizontal polarized light is predominant
(Cronin and Shashar, 2001), and
thus other e-vector orientations would elicit visual contrast between targets
and background. It has already been suggested
(Lythgoe and Hemmings, 1967
;
Loew et al., 1993
;
McFarland and Loew, 1994
;
Shashar et al., 1998
; Johnsen
and Widder, 2001; Hawryshyn et al.,
2003
) that special visual adaptations, such as UV vision and PS,
have likely evolved to increase visibility of transparent plankton. In fact,
polarization vision can reveal camouflage of transparent prey through
scattering of polarized light from the prey exoskeleton (Johnsen,
2001
,
2002
;
Novales-Flamarique and Browman,
2001
). The birefringence of calcium carbonate exoskeletons of
plankton can rotate the plane of polarization and make them conspicuous to a
polarization-sensitive visual system (Giguére and Dunbrak, 1990;
Shashar et al., 1998
; Johnsen,
2001
,
2002
;
Novales-Flamarique and Browman,
2001
). Therefore, higher discriminative capabilities at
intermediate e-vectors between 0° and 90° might be advantageous for
prey detection.
Also, C. viridis could advantageously utilize such polarization
vision for optical signalling. In fact, swimming modalities characteristic of
schooling behaviour and mate choice (nuptial displays) can produce changes in
colouration in C. viridis behaviour
(Allen, 1991). Damselfishes
possess chromatophores and iridophores, which provide many combinations of
body colouration and patterns (Fujii,
1993
). Iridophores reflect light through interference occurring in
the stacks of guanine crystals (Denton and
Nicol, 1965
; Fujii,
1993
; Herring,
1994
), and light reflected from iridophore crystals can be
polarized (Denton and Nicol,
1965
; Kasukawa et al.,
1987
; Fujii,
1993
). Both the plane and the degree of polarization produced by
reflective iridophores can change dramatically depending on the movements of
the fish (Denton and Nicol,
1965
; Denton and Rowe,
1994
; Shashar et al., 1996,
2001
;
Shashar and Hanlon, 1997
).
Moreover, through active movements of their motile iridophores
(Fujii and Oshima, 1986
;
Kasukawa and Oshima, 1987
;
Kasukawa et al., 1987
;
Fujii et al., 1989
;
Oshima et al., 1989
, Fujii,
1993
,
2000
), C. viridis
could change polarization patterns on their bodies. For C. viridis,
display of polarization patterns across the body surface would represent a
powerful resource for signalling and a reliable communication channel. This is
particularly true since the scales of fish produce a distinct polarization
reflection that is different from the polarization characteristics of the
underwater light field (Denton,
1970
; Rowe and Denton,
1997
; Shashar et al.,
2001
). Therefore, reflections off the fish body could provide
polarized light signals at e-vector orientations that would contrast those
surrounding the fish.
Conclusions
Investigation of the functional significance of polarization vision is a
relatively new research topic. Our research provides the first behavioural
evidence of e-vector discrimination in vertebrates, representing an important
step for understanding the dynamic nature of the damselfish visual system.
Here, we show that C. viridis is able to select and discriminate
between the horizontal and vertical planes of UV linearly polarized light
independent of the stimuli brightness content. The capacity for e-vector
discrimination disappeared when the UV portion of the light stimuli was
removed, indicating that the presence of UV polarized light is critical for
e-vector discrimination. Furthermore, fish were able to distinguish between
relatively small e-vector orientations of polarized light, and
e-vector varied based on the reference e-vector.
Our study offers compelling justification for future work in damselfish. Areas of particular interest include: the investigation of behavioural outputs of polarization vision in C. viridis; the examination of underlying physiological and neural mechanisms of polarization vision; and the functional significance of the e-vector discriminative capabilities. Our research provides an effective framework for experimental design and methodology of behavioural studies that examine PS in organisms.
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Acknowledgments |
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