Behavioral Ecology Vol. 12 No. 6: 768-772
© 2001 International Society for Behavioral Ecology
Benefit by contrast: an experiment with live aposematic prey
Department of Zoology, Stockholm University, S-10691 Stockholm, Sweden
Address correspondence to G. Gamberale-Stille. E-mail: gabriella.gamberale{at}zoologi.su.se .
Received 9 February 2001; revised 15 March 2001; accepted 15 March 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Aposematic prey often have a coloration that contrasts with the background. One beneficial effect of such conspicuous coloration is that it produces faster and more durable avoidance by predators. Another suggested benefit is that prey that contrast with the background are more quickly discerned and recognized as unpalatable by experienced predators. To further investigate the effects of prey contrast on predator behavior, I conducted an experiment with young chicks (Gallus gallus domesticus) as predators on live aposematic and nonaposematic prey. Birds with prior experience of both prey types were allowed into an arena with both palatable prey and aposematic prey on backgrounds that either closely matched or contrasted with the coloration of the aposematic prey. Also, the time a bird had available to decide to attack a prey was manipulated by including a competing chick or not. The experienced birds showed greater attack latencies for aposematic prey on more contrasting backgrounds, and aposematic prey were also attacked to a greater extent when on a matching background. The presence of a competitor generated similar effects, where birds in high competition attacked more and faster compared to birds subjected to lower degree of competition, but there was no interaction between competition and contrast. Thus, the experiment provides evidence that prey contrast against the background may produce better recognition and avoidance, independently of predator viewing time.
Key words: aposematism, avoidance learning, defense, foraging behavior, Heteroptera, Lygaeidae, predation, signal intensity, warning coloration.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Many species are aposematic, which means that they are distasteful or possess some other kind of predatory defense and also signal this property to potential predators, often with a striking coloration (Bates, 1862
;
Darwin, 1871;
Poulton, 1898). One common
element of aposematic coloration is conspicuousness, and aposematic prey often
contrast with the background (Cott,
1940; Poulton,
1898). As conspicuousness entails the obvious cost of increased
risk of discovery by predators, it also has to be beneficial to aposematic
prey in some way to balance this cost. There are several possibly beneficial
effects of a conspicuous coloration. A contrasting coloration may, for
instance, increase the acquisition of avoidance. One reason is that the speed
of discrimination learning often depends on the difference between negative
and positive stimuli. As conspicuous coloration is noncryptic and thus
different from the cryptic palatable prey the predators usually hunt (the
positive stimuli), such coloration has been suggested to produce faster
avoidance learning (Coppinger,
1970; Guilford,
1990; Turner,
1975). Stimulus novelty has been shown to increase avoidance
learning (Roper, 1993). It has
also been shown that birds may reject novel prey on the basis of unfamiliarity
alone or neophobia (Coppinger,
1969,
1970;
Marples et al., 1998;
Schlernoff, 1984;
Wiklund and
Järvi, 1982).
Another similar suggestion of how conspicuousness may affect avoidance
learning is that contrasting coloration may produce a stronger impression of
the prey, a more intense stimulus. The intensity of a conditioned stimulus is
important for the rate of associative learning, and conditioning progresses
faster for stronger than for weaker stimuli
(Pearce, 1987). A contrasting
prey coloration may therefore increase the speed of avoidance learning
(Gittleman and Harvey, 1980;
Guilford, 1990), and there is
experimental evidence suggesting that birds associate unpalatability faster
when the prey contrasts against the background than when the prey matches in
coloration
(Lindström
et al., 1999; Roper and
Wistow, 1986; Roper and
Redston, 1987).
A conspicuous coloration may also be beneficial when encountering already
experienced predators. Conspicuous prey may be detected at a greater distance
and thereby increase the time the predator can study the prey while
approaching, which in turn could result in fewer recognition errors (Guilford,
1986,
1990). This hypothesis could
be difficult to test because it is hard to know when a predator actually sees
a prey. There is, however, some evidence that the time a bird is allowed to
view a prey is important for whether they attack or not. Young chicks make
more mistakes in a choice situation between differently colored, familiar
palatable and unpalatable crumbs if they get less time to view the
"prey" before attack
(Guilford, 1986). In
competition with another chick, chicks make more mistakes in that they attack
aposematic prey faster, more often, and need more attacks before starting to
avoid prey (Gamberale-Stille,
2000).
In the present experiment I investigated the importance of the two latter hypotheses by studying the effects of predator viewing time and prey contrast against the background on predator attacking behavior. I used live aposematic and non-aposematic prey, presented on different backgrounds, to produce a variation in conspicuousness. I also used domestic chicks with prior experience of both prey types as predators. The time a bird has available to decide whether to attack a prey was manipulated by either including a competing or an inactive companion chick.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Predators and prey
As predators in the experiment, I used male domestic chicks (Gallus gallus domesticus) that arrived from the hatchery in batches of about 40 individuals (permit Dnr N60/00 by Stockholms djurförsöksetiska nämnd). They were then less than 20 h old and had not yet eaten. Each batch of chicks were housed together in a cage with a 100 x 55 cm steel-net floor, 20-cm high wooden sides, and a roof made partly of wood and partly of chicken wire. The floor of the cage was covered with sawdust, and a 60 W carbon light bulb provided heat. The chicks were fed chick starter crumbs and water ad libitum throughout the housing period. During the second day after arrival, the chicks were occasionally also fed live mealworms (Tenebrio molitor) from petri dishes with white and orange-red papers in the bottom of the dishes as background (see below). This accustomed the birds both to live prey and to the two different background colors. Throughout the experiments birds in each batch were evenly divided among treatment groups.
As prey I used live larvae of two species of seed bugs (Heteroptera: Lygaeidae), one aposematic and one nonaposematic. The Tropidothorax leucopterus larvae have an aposematic orange-red coloration with black head, legs, and wing-buds and are clearly distasteful to chicks. The Graptostethus servus larvae are brownish gray in color, also with black legs, head, and wing-buds, and are palatable to chicks. T. leucopterus was reared on a diet consisting of seeds and green parts of their toxic host plant Vincetoxicum hirundinaria (Asclepiadaceae), husked sunflower seeds, and water, and G. servus was reared on a diet of husked sunflower seeds and water. All larvae were cultured at a 17:7 h light:dark regime, at a temperature of 27°C.
Experimental arena and training
The experiments took place in an arena (70 x 55 cm) made of the same
kind of cage that the chicks were housed in. The floor of this arena was
covered with a semitransparent plastic sheet. The experimental room, the same
room the birds were housed in, was lit by daylight lamps (OSRAM Biolux, L36W/
72-965) to resemble natural wavelengths.
On the third day after arrival, all chicks were trained in the experimental arena to eat palatable fifth-instar G. servus larvae from petri dishes (no paper background), and only birds that readily ate the G. servus larvae were used in the experiment. On the birds' fourth day they were given experience of the aposematic prey. One chick that had been fed with mealworms, which made it inactive and not interested in the experimental prey, became a companion to the experimental chicks during training. The use of a companion chick was necessary because the chicks became distressed if alone in the experimental arena. I presented birds, one at a time, with one aposematic T. leucopterus larva and one palatable G. servus larva in two separate petri dishes without paper background. Birds had access to the aposematic prey during the entire time of a 3-min trial, and I noted whether they attacked or not. Birds that had not attacked the aposematic prey during this trial were presented again with the aposematic prey for another 3 min.
To influence the conspicuousness of the aposematic prey in the experiment, I used two different colored paper backgrounds in the bottom of the petri dishes. One was ordinary white office paper, and one was orange-red. I chose the colored paper to match the color and brightness of the T. leucopterus larvae as closely as possible, and the reflectance spectra from paper and larvae were compared using a spectrometer (Figure 1).
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On the birds' fifth day they were all first trained in pairs to forage in the experimental setup. Eight petri dishes with a diameter of 5 cm had been placed in two rows in the middle of the arena with approximately 10 cm between dishes. During this training, every second dish contained white paper as background, and every other dish contained orange-red paper as background. One mealworm had been placed in each dish. All mealworms were eaten within a minute, and all birds attacked and ate mealworms without discriminating between the two backgrounds.
Experimental procedure
After training, I divided 114 birds into four treatment groups: low
competition/low contrast (n = 19), low competition/high contrast
(n = 19), high competition/low contrast (n = 19 pairs), and
high competition/high contrast (n = 19 pairs). Thus, experimental
birds were tested either with an inactive companion chick (low competition) or
in pairs of hungry chicks (high competition), and prey were either placed on
white paper background (high contrast) or on orange-red paper background (low
contrast). As I wanted the experimental birds to have similar experience of
the aposematic prey in the different treatment groups, birds were divided
between treatment groups so that all experimental birds in the low competition
treatment and at least one chick in each pair had attacked the aposematic prey
in the training session the previous day.
In the arena, four palatable G. servus prey and four aposematic
T. leucopterus prey were placed in alternating order in the eight
dishes. A thin layer of Fluon was put on the rim of the dishes to prevent the
insects from escaping. Birds were allowed into the arena for a 5-min trial.
The treatments were alternated and all trials were videotaped to facilitate
the observation of the birds' behaviors. I collected data for the time to
first attack, both of the aposematic and the nonaposematic prey, and the total
number of attacks on aposematic prey. In the analysis, I used data on behavior
toward aposematic prey only from one chick of a pair. This chick had attacked
aposematic prey during training and, if both had, one chick of a pair was
randomly selected. Total attack number and the time to attack were compared
between groups using two-way ANOVA on square root transformed data
(
y). For birds that did not attack aposematic prey during the
5-min trial, the time to attack was set to 300 s in the analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Chicks in all treatments generally attacked the palatable G. servus prey before they attacked the aposematic T. leucopterus prey (Wilcoxon signed-ranks test, Z = 5.62, p <.0001; Figure 2). The background color affected attack latencies of the two prey types differently (ANOVA, prey type x contrast, F = 8.58, df = 1,72, p =.004). Whereas noncontrasting aposematic prey, on orange-red background, were attacked faster by chicks in both the high and low competition treatments, there was no significant effect of background on attack latencies on the palatable prey (Table 1, Figure 2). Thus, birds were more affected by background color when prey were aposematic, and they hesitated longer before attacking the aposematic prey when the coloration was conspicuous against the background than when it matched the background.
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The total number of attacked aposematic prey was also affected by prey contrast against the background (Figure 3). Aposematic prey were attacked significantly more often on matching background than on contrasting background, both by birds in the high and in the low competition treatments (Table 1).
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Competition for prey seemed to speed up decision making in the birds. Birds in high competition attacked the aposematic T. leucopterus prey significantly faster (Figure 2, Table 1), but there was no significant effect of competition on latency to attack the palatable G. servus prey (Figure 2, Table 1). Higher competition also caused birds to attack the aposematic prey significantly more often (Figure 3, Table 1). However, the degree of competition did not interact with the degree of prey contrast in affecting bird behavior, neither for the latency to first attack on palatable or aposematic prey nor for the total attack frequencies (Table 1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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This study provides further evidence of benefits of a conspicuous coloration in aposematic prey. Higher contrast against the background made experienced birds hesitate longer in attacking the aposematic prey, and they also made fewer mistakes. There are two possible mechanisms that could produce such results. One is that the conspicuousness of the prey affected predator decision time so that prey were distinguished faster, and thereby viewed for a longer time, which could result in fewer recognition errors (Guilford, 1986
,
1990). The second is that the
aposematic signal was amplified on a contrasting background, so that the
conditioned stimulus was perceived as more intense, and thereby generated a
stronger avoidance response.
In the present experiment there was a separate effect of predator decision
time: birds that competed for prey attacked faster and also made more mistakes
in attacking aposematic prey. This result supports previous findings that the
time a bird has available in viewing a prey before attack results in fewer
mistakes (Gamberale-Stille,
2000; Guilford,
1986) and perhaps also results in faster avoidance learning
(Gamberale-Stille, 2000).
However, if difference in viewing time was the only factor affecting the
recognition of the aposematic prey, one would expect a smaller effect of
conspicuousness in birds from the low competition treatment where they were in
the least hurry to attack. There was no evidence for such an interaction
between degree of competition and prey contrast on any of the behaviors
investigated.
A more probable explanation for the effects of prey contrast against the
background in the present experiment would be that it affected the birds'
ability to recognize the aposematic prey as such. It is possible that prey on
a contrasting background produced a more intense warning signal and thereby
generated a stronger avoidance response. That more contrasting stimuli may be
more salient or more intense has been suggested as an explanation of why birds
learn faster and for longer to avoid more contrasting prey stimuli
(Roper and Redston, 1987;
Roper and Wistow, 1986). Also,
it is expected that birds responded more correctly in avoiding the prey in the
present experiment when on a more contrasting background, from findings that
generalization after discrimination along intensity dimensions often produces
an increased response with an increase in stimulus intensity (see, for
instance, Razran, 1949).
The effect of contrast here is similar to the effect of prey grouping in a
previous experiment, where groups of prey compared to solitary prey also
generated longer hesitation before attacks and fewer attacks
(Gamberale-Stille, 2000). It
has been suggested that larger size of warning signals gives a stronger
impression and thereby greater avoidance
(Edmunds, 1974; Gamberale and
Tullberg, 1996,
1998) and also that
gregariousness increases conspicuousness
(Sillén-Tullberg
and Leimar, 1988; Turner and
Pitcher, 1986; Vulinec,
1990).
A third, alternative explanation for the results could be that the orange-red background paper produced faster and more attacks by the chicks, independent of the contrast of the aposematic prey. If this was the case, I would expect birds to be affected by the paper backgrounds also when prey were palatable. However, latencies to attack the palatable prey were not affected by the paper backgrounds. Also, birds had similar previous experience with the two background papers and did not show any preference before the experiment.
Although conspicuousness is an important and common feature of aposematism,
it is not always prominent. Rothschild
(1964) proposed that some
warning coloration can be cryptic at a distance and aposematic close by
(Järvi et
al., 1981). Patterns consisting of stripes and spots can be very
contrasting at close range, and at the same time function cryptically by means
of disruptive coloration (Cott,
1940) when viewed from a distance. There are properties of warning
coloration, other than conspicuousness, that influence predator behavior
(Guilford, 1990;
Schuler and Roper, 1992).
Harvey and Paxton (1981)
suggested that particular hues or intensities of color may be more effective
than others, and accordingly birds seem to show differences in at least
unconditioned aversions to certain colors and patterns often used in warning
coloration (Roper, 1990;
Roper and Cook, 1989;
Sillén-Tullberg,
1985). In the present experiment I did not control for the effect
of coloration per se, as only reddish aposematic prey were used. Hence, there
is a possibility that the effects of prey contrast against the background
reported here are only applicable to red, and not to contrasting colors in
general. In any case, this experiment shows that aposematic prey may benefit
from contrasting against the background when faced with experienced
predators.
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ACKNOWLEDGEMENTS |
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I thank Bertil Borg, Stefano Ghirlanda, Magnus Enquist, and Birgitta S. Tullberg for their valuable comments on the manuscript and Christer Solbreck for providing the G. servus bugs. This study was financed by the Swedish Natural Science Research Council (to B.S. Tullberg).
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