Behavioral Ecology Vol. 12 No. 1: 65-70
© 2001 International Society for Behavioral Ecology
Can ultraviolet cues function as aposematic signals?
Department of Biological and Environmental Science, University of Jyväskylä, PO Box 35 (YAC413.1), FIN-40351 Jyväskylä, Finland
Address correspondence to A. Lyytinen. E-mail: alyytine{at}dodo.jyu.fi .
Received 13 September 1999; revised 21 January 2000; accepted 29 May 2000.
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ABSTRACT |
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The fact that birds are sensitive to ultraviolet light (UV, 320-400 nm) has been largely ignored by previous studies of aposematism. Therefore, in the present article we investigated whether great tits preferred ultraviolet-reflecting colors compared to colors without UV reflection and whether UV cues alone could function as aposematic signals. We were able to manipulate prey visibility in UV light by changing the UV reflectance of prey items as well as altering the lighting conditions. In order to perform a preference experiment we used three pairs of colors (green+UV vs. green, gray+UV vs. gray, yellow+UV vs. yellow) on a black background. The birds ate both UV types equally for all three colors. Thus, there was no avoidance of the UV-reflecting prey. Next we tested the possibility that UV reflection may affect avoidance learning. We used either green or green+UV as a signal for unpalatability. In this set-up the difference in UV did not allow avoidance learning to occur. Our experiment with great tits does not support the hypothesis that UV cues alone might work effectively as aposematic signals.
Key words: aposematism, ultraviolet, ultraviolet-reflecting, ultraviolet-absorbing, avoidance learning.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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Already by the early 1970s the fact that birds are also able to see in near-ultraviolet light (UV, 320-400 nm) was established for the hummingbird, Colibri serrirostris (Huth and Burkhardt, 1972
) and for the pigeon, Columbia livia
(Wright, 1972). Since then the
ability to see UV has been demonstrated for several other bird species
(Bennett and Cuthill, 1994;
Cuthill et al., 2000), perhaps
excluding nocturnal birds (Bowmaker and
Martin, 1978; Koivula et al.,
1997). Most diurnal birds have at least four kinds of
photopigments in the cones of their eyes
(Bowmaker et al., 1997;
Bowmaker and Hunt, 1999;
Cuthill et al., 2000)
including a spectral sensitivity peak in near-ultraviolet light at 360-380 nm
(Burkhardt and Maier, 1989;
Chen et al., 1984;
Chen and Goldsmith, 1986). The
vision of some bird species is even more sensitive to short wavelengths than
to the visible spectrum (Burkhardt and
Maier, 1989; Kreithen and
Eisner, 1978; Maier,
1994) and birds are able to discriminate between differences in
hues in the UV region (Emmerton and Remy,
1983). Among vertebrates the presence of UV sensitive cones is not
an unique feature of the avian eye. It also occurs among amphibians, reptiles,
fish, and mammals (reviews by Jacobs,
1992;
Tovée,
1995).
Four-dimensional color vision in birds has been ignored by many studies of
color signals (Bennett et al.,
1994). Recently, the function of UV vision in birds has received
much attention. Several studies have shown UV vision to play a role in mate
choice (Andersson and Amundsen,
1997, Andersson et al.,
1998; Bennett et al.,
1996,
1997;
Hunt et al., 1998;
Johnsen et al., 1998;
Maier, 1993;
Sheldon et al., 1999), but
studies of the role of UV vision in foraging are far fewer. It has been
suggested that kestrels (Falco tinnunculus) may use the UV-reflecting
scent marks of voles to locate feeding areas
(Viitala et al., 1995), and
blue tits (Parus caeruleus) found cabbage moth larvae faster in the
presence of UV light (Church et al.,
1998a).
Church et al. (1998b)
measured the reflectance spectra of both lepidopteran larvae and their natural
backgrounds. The data indicated that many caterpillars matched the leaf
background in the UV region as well as visibly and thus they were cryptic over
the entire range of wavelengths. On the other hand, caterpillars that seem to
be cryptic in those wavelengths visible to the human eye may be conspicuous in
UV. Larvae of the gray shoulder knot (Lithophane ornitopus) are
cryptic on the leaves of oak tree (Quercus robur) only in the range
400-700 nm, but not in UV (Church et al.,
1998b). The possibility thus arises that by being conspicuous in
UV prey animals might advertise unpalatability to predators. The use of
conspicuous colors (yellow, red, and orange) by prey in order to convey
distastefulness, or other unpleasant properties, is called aposematism
(Cott, 1940;
Edmunds, 1974;
Poulton, 1890). Predators are
able to learn to avoid prey exhibiting warning colors but they may also have
unlearned aversions towards certain colors or patterns
(Schuler and Hesse, 1985; see
review by Schuler and Roper,
1992).
There are no existing studies of aposematism that consider signals, which
use the reflection of UV light. Therefore, we investigated whether predators
exhibit a preference for (or avoidance of) UV-reflecting or UV-absorbing prey.
A preference experiment was conducted with three pairs of colors (green, gray,
and yellow) differing only in the UV region. Our second goal was to explore
whether a difference in the visibility of UV reflectance might play a role in
avoidance learning. In previous behavioral studies UV light has typically been
blocked by a filter (Bennett et al.,
1996,
1997;
Church et al., 1998a;
Maier, 1993) or with sunblock
(Andersson and Amundsen, 1997).
By contrast, Silberglied and Taylor
(1978) used a method where
they increased UV reflection with the use of chalk. We have combined these
approaches by reducing the reflection of UV light by titanium dioxide and
increasing UV reflection with the use of chalk.
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MATERIAL AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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Predators and training
We conducted the experiments on adult great tits (Parus major) in May 1998 at Konnevesi Research Station, in Central Finland. We had permission (Central Finland Regional Environment Center, permission LS-12/98) to keep birds in captivity. The birds captured by mist nets were maintained on a diet of sunflower seeds, peanuts, and water ad libitum on 18 h light/6 h dark conditions. They were held in individual, visually isolated cages (0.60 m x 0.60 m x 1.0 m). The birds were trained to consume almonds which were glued to pieces of white paper (see prey item section). The birds were accustomed to the experimental cage in order to ensure that they searched for food from the floor. To motivate the birds to forage they were deprived of food for at least 2 h before the trials. After the experiments we released the birds back into the wild.
Prey items
Slices of almond glued under pieces (1.0 x 1.5 cm) of colored paper
(light green, gray, and pale yellow) were used as prey items. The paper
coverings were designed to either reflect (green+UV, gray+UV, and yellow+UV)
or absorb (green, gray, and yellow) UV light. Those which reflected UV light
were covered with chalk, modifying the method used by Silberglied and Taylor
(1978; see also
Derim-Oglu and Maximov, 1994).
They used only one kind of chalk on each prey but we coated the ultraviolet
reflecting items with either both white and colored chalk (green or yellow) or
with white chalk only (gray). The chalk increased the brightness only in the
UV waveband. We coated the UV-absorbing prey items with a mixture of titanium
dioxide (TiO2) and chalk powder (2.5 g green, white or yellow
chalk/15 g TiO2). Chalk was added to the titanium dioxide in order
to make the UV-absorbing prey items exactly the same color as the
UV-reflecting ones. The mixture was then spread evenly over the paper
coverings. It reduced reflectance in the region of the light spectrum under
400 nm retaining almost the same spectral reflectance across the 400-720 range
(Figure 1). This method allowed
us to use only relatively pale colors. For us UV+ and UV- items appear
perfectly alike and so were impossible to separate from each other. However,
it was also necessary to exaggerate the sensation of UV colors by changing the
lighting conditions as explained below. Admittedly also UV- items reflected
some UV but they were less bright in UV than UV+ items. The difference was
perceivable to the birds (see Control test of the UV manipulation).
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The reflectance of the prey items in the range 320-720 nm was recorded at 2 nm intervals using a spectroradiometer (EG&G Gamma Scientific GS3100 Radiometer, Light Touch Software 1.04a) under the same light conditions as those used for the experimental cages (see below). Reflectances were measured as a proportion of the light reflected from a calibrated 98% white standard (LabSphereTM).
To visualize the set-up of the experiment, photographs of the prey were taken with a Nikon camera in daylight through the UV transmission filter (Nikon UV filter) and again without the filter on an UV-sensitive black and white film (Kodak Tmax 400pro). The UV-reflecting areas appear pale while the UV-absorbing areas appear dark in the UV photographs (Figure 2).
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Experimental cages and illumination
The experiments were performed in a matt black painted cage (0.50 m x
0.70 m x 0.96 m) inside a dark room to ensure that there was no
daylight. Since the sensation of colors is dependent on the amount and
spectral composition of the ambient light
(Endler, 1990), we used a
light regime that was much richer in UV than natural light. This was done by
using an Osram Eversun L40W/79K rich in UV together with an Osram L18W/72
Biolux fluorescence tube, which provided light from 320 to 720 nm in the
experimental cages (Figure 3).
Under these lighting conditions UV reflection, that matched the ambient light
peak, appeared brighter than under the light that would have contained low
levels of UV region. Thus, the difference in the UV region between UV+ and UV-
prey items was exaggerated. There was an opening of 12 cm x 33 cm in the
floor of the cage, through which prey items could be placed onto the tray
without disturbing the bird. A perch (at a height of 30 cm) was also available
for the bird. We observed the behavior of the birds through a small
net-covered window. During both the training and experimental periods water
was available ad libitum.
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Control test of the UV manipulation
Since both UV+ and UV- items appear similar to us, we tested whether we
managed to create a sufficiently large difference between the two prey types
(UV-absorbing vs. UV-reflecting). We tested these two prey types by placing
one UV-absorbing (i.e., cryptic) and one UV-reflecting (i.e., conspicuous)
palatable prey item side by side on a background with a color similar to that
of the UV-absorbing prey (Figure
2). Thus, the same mixture of titanium dioxide and chalk was used
for the background as for the UV-absorbing prey items. If the difference in
the UV spectrum is adequate between two prey types, then birds are able to see
simultaneously presented UV-reflecting items better than UV-absorbing ones in
the presence of UV, if presented on UV-absorbing background. Therefore, they
are expected to eat more UV-reflecting prey items in UV-present conditions
(both UV light and visible light sources switched on) than in UV-absent
conditions (only visible light source switched on). Due to the fact that even
Biolux fluorescence tubes emit small amounts of UV light and that birds are
excellent at color discrimination, we used plexiglass (thickness 1 cm) to
completely block the UV wavelengths in the UV-absent treatment (see
Figure 3). We conducted two
separate treatments for each bird (n = 10), one with UV present and
one with UV absent, in green, gray, and yellow, in random order. To each bird
we presented, in sequence, a choice session of five pairs (UV+ and UV-) of
each color (green+UV vs. green, gray+UV vs. gray, and yellow+UV vs. yellow).
We only allowed the birds to eat the first prey item attacked.
Preference experiment
If UV colors play an important role in aposematism it could be expected
that wild birds would exhibit an innate or learned avoidance of these colors.
We designed the experiment to compare the preferences between UV-reflecting
and UV-absorbing prey types (green+UV vs. green, gray+UV vs. gray, and
yellow+UV vs. yellow). Similar palatable prey items were used as explained
above but this time they all were clearly contrasted with the background. We
presented one UV-absorbing and one UV-reflecting item simultaneously to the
bird, on the black tray (9.0 cm x 10.0 cm) and then we recorded the
order of prey choice. We allowed the birds (n = 36) to eat both prey
items. For each of the three colors there were five consecutive replicate
pairs (UV+/UV-). The colors were tested in random order.
Learning experiment
We tested whether great tits could learn to discriminate the unpalatable
prey items from the palatable ones if their reflection of the light differed
only in the UV region. We chose the color green since the birds had not
exhibited any preference between the green and the green+UV items.
Furthermore, in nature green is usually an indicator that something is edible.
For the first group (n = 13), the green+UV prey items were made
unpalatable, while for the second group (n = 13) the green prey items
were made unpalatable. We made the almonds distasteful by soaking slices of
almond in a mixture of 40 g chloroquinine phosphate and one 1 water for an h,
after which we dried the almonds. The concentration of the solution
corresponds to that used in previous studies
(Alatalo and Mappes, 1996;
Lindström et
al., 1999). We presented green+UV and green items side by side
upon a black tray. The birds underwent four trials, separated by a 20 min
pause. During the trials, we offered sequentially six pairs of prey items.
During the first trial, we waited until the bird ate both items to make sure
that each bird at least tasted an unpalatable prey item. Thus, median of the
duration in the first trial was 57 s (green+UV unpalatable) and 54 s (green
unpalatable) for consuming both items. In the following three trials after the
bird consumed the first item in the pair we allowed the bird a maximum of 30 s
to take the remaining prey item.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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Control test of the UV manipulation
We tested two prey types used by placing them on the UV-absorbing background and introducing them to the birds. If the treatment was successful in the manipulation of UV then UV-reflecting items should be consumed more, from the UV-absorbing background, than UV-absorbing prey items when in the presence of ultraviolet light. Indeed, under UV light many more green+UV and yellow+UV were eaten compared to when UV light was absent (Wilcoxon matched pair test, z = -2.46, n = 10, after sequential Bonferroni correction p =.041 and z = -2.43, p =.030, respectively). There was a similar tendency with the color gray even though the difference was not quite significant (Wilcoxon matched pair test, z = -1.84, after sequential Bonferroni correction p =.066) (Figure 4). The results showed that bird ate more UV-reflecting prey items than UV-absorbing ones, which suggests that the manipulation succeeded.
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Preference experiment
To test whether wild great tits exhibit any preference for UV-reflecting
items compared to similar non-ultraviolet reflecting items we presented them
with both of these prey types under UV light. Both prey items were highly
conspicuous against a black background. There was no significant difference in
preferences between UV+ and UV- treated green or gray prey (Wilcoxon
matched-pair test, z = -0.75, after sequential Bonferroni correction
p =.901 and z = -0.34, p =.735, respectively,
n = 36). Both prey types were consumed in similar proportions. There
seemed to be a slight, but not significant, tendency of birds preferring more
yellow+UV prey to yellow prey (Wilcoxon matched pair test, z = -2.35,
after sequential Bonferroni correction p =.056, n = 36)
(Figure 5). These results
indicated that there was no avoidance of UV-reflecting items. If anything,
there seemed to be a slight preference for yellow+UV.
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Learning experiment
The proportion of cases, in which unpalatable items were consumed first,
from the items on offer, was used as the dependent variable for each trial. We
carried out an Arcsin square root transformation to normalize the data.
Two-way ANOVA with repeated measures over the four trials showed a significant
main effect (F1,24 = 22.12, p <.001) due to
the treatment (green+UV unpalatable versus green unpalatable). This indicated
that the proportion of unpalatable items the birds consumed during the trials
was lower when green was unpalatable
(Figure 6a). There was no
significant difference between the trials, indicating that the birds did not
learn to avoid unpalatable prey items (F3,22 = 1.87,
p =.165). There was also no interaction between the treatment and the
trial rank (F3,22 = 0.91, p =.454).
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To increase the power of the statistical test, we tested the learning process by comparing the first and last trials separately. When green+UV was unpalatable there was no difference between the first and last trials (paired t = -1.28, df. = 12, p =.225). However, when green was unpalatable (and green+UV was palatable), there was a slight difference between the first and last trials (t = -2.21, df. = 12, p =.048). This difference indicated that the birds had a weak predisposition to learn to distinguish between palatable and unpalatable items on the basis of UV cues, but we stress that pure UV signals as aposematic signals cannot be very effective.
The fact that the starting points of avoidance learning were on different level (Figure 6b) could suggest that there might be avoidance learning within the first trial. To test this we scored the first choice across the six pairs of prey within trial 1 (Figure 6b). If the bird took palatable prey item first it received value of zero. Unpalatable prey chosen first received value of one. There was no interaction between the treatment and the pair rank (GLM: F5,20 = 0.565, p =.725). Furthermore, birds did not learn to avoid unpalatable prey items within trial 1 (F5,20 = 0.752, p =.725) but green unpalatable was avoided relative to green+UV unpalatable (F1,24 = 8.526, p =.007). The result indicated that the lower starting point for green than for green+UV unpalatable prey was not the result of more rapid association of unpalatability within trial 1.
Control test of the learning experiment
To rule out the possibility that the negative result of the learning
experiment was due to the setup, we ran a test using the color red which is
well known to be used in a warning context. We used the same procedure as in
the learning experiment but with a new set of birds. The only difference was
the colors used. The proportion (± SE) of cases in which the birds
consumed red prey items before palatable green items, was, for the four
trials: 33.3% (± 6.6), 21.7% (± 7.5), 18.3% (± 8.8), and
13.3% (±. 6.0). Although the birds exhibited an initial avoidance of
red, the birds (n = 10) learned to avoid red unpalatable prey items
during the experiment (F3,7 = 9.48, p =.007).
When compared with the previous learning experiment the birds ate first significantly less red unpalatable prey items, in the last trial, than green+UV unpalatable prey items (Mann-Whitney test: Z = -2.643, p =.008) and equal proportion of red as green unpalatable (Z = -0.835, p =.446). But when we compared the proportion of unpalatable prey that birds refused to eat in the last trial the difference is even clearer (Table 1). The birds left untouched (i.e., refused even to taste) significantly more red unpalatable prey items, in the fourth trial, than green+UV (Mann-Whitney test: Z = -2.250, p =.026) or green unpalatable items (Z = -2.753, p =.005). Thereby, the birds exhibited significantly greater rejection of unpalatable prey items in the last trial of the control test than in the learning experiment. This proves that the inability of the birds to learn in the learning experiment was not due to deficiencies in the experimental design but due to the signal. We can also conclude that the concentration of chloroquinine used was aversive enough to produce avoidance learning over the time scale of the experiment if the visual signal is strong enough.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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We managed to produce UV-absorbing and UV-reflecting signals without greatly affecting the reflectance in the wavelengths above 400 nm. Both prey items appeared very similar in the visible light spectrum but there were clear differences in the UV region. When the UV- and UV+ prey types were presented simultaneously the great tits did not seem to have a clear preference for or an avoidance of UV-reflecting prey items in any of the color combinations used. If anything, the birds consumed slightly, but not significantly more yellow+UV than yellow prey items. This would indicate that there is not a strong avoidance of UV-reflecting prey items.
The birds had difficulties in learning to avoid unpalatable prey items
irrespective of whether the signal was UV+ or UV-. In a simultaneous choice
experiment, where a bird can compare two prey types side by side, any
differences in learning should be easy to find. The poor learning performance
of the birds was not due to the experimental design since the birds readily
learnt to associate red with unpalatable prey. One possibility is that the UV
cues were too weak to be learnt by the birds.
Lindström et al.
(1999) found that birds learnt
to avoid unpalatable signals from palatable ones only when the signals were
highly conspicuous. In the present paper, the mean (± SE) UV
reflectance (320-400 nm) in green+UV was 25% (± 0.20) and in green the
UV reflectance was 11% (± 0.23). Even though the difference in UV
between the treatments was rather slight the birds easily detected, in the
presence of UV light, UV+ items from the UV-absorbing background.
The result that the birds avoided green unpalatable items in trial 1 of the
learning experiment was somewhat unexpected. This avoidance was not due to
more rapid avoidance learning of green unpalatable already within trial 1.
Although the birds did not exhibit any avoidance of unpalatable items in the
green vs. green + UV preference experiment they still might have had some
initial preferences for UV+ items. These may appear only in a more critical
situation when they are also confronted with unpalatable items. Additionally,
the results suggest that birds, if anything, would be more capable of learning
to associate UV reflectance with palatable than with unpalatable prey. Natural
backgrounds, such as leaves, bark, and soil, absorb UV light
(Endler, 1993;
Finger and Burkhardt, 1994).
Thus the bird might associate UV reflection more easily with something edible
than with an inedible item.
We used a non-aposematic color, green, which allowed us to test whether UV cues alone could create the rejection of nasty tasting prey. If UV reflectance indicates unpalatability then birds should have an innate aversion towards UV colors in combination with any color. We found no such preferences in wild adult birds, which have most likely had previous experience of the warning colors used by prey animals and therefore should have exhibited an innate or learned avoidance. Another characteristic of aposematic prey is that the predator must be capable of learning to associate a particular color with inedibility and hence, to avoid catching similar prey at a later date. However, the birds were not capable of learning to avoid unpalatable prey items irrespective of whether they reflected or absorbed UV light. If anything, they seem to associate UV reflectance with palatability. UV cues alone did not seem to effectively signal unpalatability.
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ACKNOWLEDGEMENTS |
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We thank Helinä Nisu for the assistance with the birds, the staff of Konnevesi Research Station for the help during this project, Heli Siitari, and Jussi Viitala for the help with the spectroradiometer. We thank Mikael Puurtinen and Heli Siitari for helpful comments on the manuscript. Tabatha Lamont kindly corrected the language. Academy of Finland financed this project. Authors after senior author are in alphabetical order.
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