Birgitta S. Tullberg

Aposematism and gregariousness: the combined effect of group size and coloration on signal repellence

Many aposematic species have evolved an aggregated lifestyle, and one possible advantage of grouping in warningly coloured prey is that it makes the aposematic signal more effective by generating a greater aversion in predators. Here we investigate the effect of prey group size on predator behaviour, both when prey are aposematic and when they are not aposematic, to separate the effects of warning coloration and prey novelty. Naive domestic chicks (Gallus gallus domesticus) were presented with either solitary or groups of 3, 9 or 27 live larvae of the aposematic bug Tropidothorax leucopterus. Other naive chicks were presented with larvae of the non–aposematic bug Graptostethus servus either solitary or in groups of 27. Attack probability decreased with increasing group size of aposematic prey, both when birds were naive and when they had prior experience, whereas prey gregariousness did not affect the initial attack probability on the G. servus larvae. In a separate experiment, groups of mealworms were shown to be even more attractive than solitary mealworms to naive chicks. We conclude that the aversiveness of prey grouping in this study can be explained as increased signal repellence of specific prey coloration, in this case a classical warning coloration. These experiments thus support the idea of gregariousness increasing the signalling effect of warning coloration.

Evidence for a Peak-Shift in Predator Generalization among Aposematic Prey

A previous theoretical model involving learning psychology and game theory has suggested how warning coloration in unprofitable prey could evolve and become stable. The model shows that in a dimension of increasing prey conspicuousness a displacement of the minimum in a predators’ generalization gradient (peak-shift), can produce a strong enough selection pressure towards a more conspicuous coloration that would balance the increased risk of discovery and thus stabilize an aposematic strategy. Using naive domestic chicks (Gallus gallus domesticus) as predators on three different instars of larvae of the aposematic bug Tropidothorax leucopterus (Heteroptera: Lygaeidae), we first show that their unconditioned aversion increases towards larger prey. This aversion is caused by increased aposematism–conspicuousness with increasing size, as no aversion at all was found in a control experiment increasing the size of edible prey. We then show that after one experience of aposematic prey, the chicks exhibit a greater aversion towards prey that are larger and thus more aposematic than those they had experienced. Our results thus provide evidence of a peak-shift in a predators’ generalization gradient in a stimulus dimension of increasing prey conspicuousness. The mechanisms behind this peak-shift are investigated and discussed.

Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds

Abstract. Pinnipedia contains some of the most spectacular examples of sexual size dimorphism, examples that are therefore frequently used to illustrate the theory of sexual selection. This paper addresses the question of whether a significant relationship between sexual selection and size dimorphism exists in a comparative context. Thus, harem size and body size data gathered from the literature were analysed with independent contrasts analyses. These investigations showed that sexual size dimorphism is not a consequence of an allometric relationship between male and female size. Instead, there is a clear relationship between harem size and sexual size dimorphism. Further analyses also revealed a significant relationship between harem size and male size whereas no such relationship existed for females. These results support the hypothesis that sexual size dimorphism in pinnipeds is the product of an exclusively male response to sexual selection.

Aposematism and crypsis combined as a result of distance dependence: functional versatility of the colour pattern in the swallowtail butterfly larva

The idea that an aposematic prey combines crypsis at a distance with conspicuousness close up was tested in an experiment using human subjects. We estimated detectability of the aposematic larva of the swallowtail butterfly, Papilio machaon, in two habitats, by presenting, on a touch screen, photographs taken at four different distances and measuring the time elapsed to discovery. The detectability of larvae in these images was compared with images that were manipulated, using existing colours either to increase or decrease conspicuousness. Detection time increased with distance for all colourations. However, at the closest distance, detection time was longer for the larvae manipulated to be more cryptic than for the natural and more conspicuous forms. This indicates that the natural colouration is not maximally cryptic at a short distance. Further, smaller increments in distance were needed to increase detection time for the natural than for the conspicuous larva. This indicates that the natural colouration is not maximally conspicuous at longer distances. Taken together, we present the first empirical support for the idea that some colour patterns may combine warning colouration at a close range with crypsis at a longer range. The implications of this result for the evolution of aposematism are discussed.

Experienced chicks show biased avoidance of stronger signals: an experiment with natural colour variation in live aposematic prey

An important factor for understanding the evolution of warning coloration in unprofitable prey is the synergistic effect produced by predator generalisation behaviour. Warning coloration can arise and become stabilised in a population of solitary prey if more conspicuous prey benefit from a predators previous interaction with less conspicuous prey. This study investigates whether domestic chicks (Gallus gallus domesticus) show a biased generalisation among live aposematic prey by using larvae of three species of seed bugs (Heteroptera: Lygaeidae) that are of similar shape but vary in the amount of red in the coloration. After positive experience of edible brownish prey, chicks in two reciprocal experiments received negative experience of either a slightly red or a more red distasteful larva. Attacking birds were then divided into two treatment groups, – one presented with the same prey again, and one presented with either a less red or a more red larva. Birds with only experience of edible prey showed no difference in attack probability of the two aposematic prey types. Birds with experience of the less red prey biased their avoidance so that prey with a more red coloration was avoided to a higher degree, whereas birds with experience of the more red prey avoided prey with the same, but not less red coloration. Thus, we conclude that bird predators may indeed show a biased generalisation behaviour that could select for and stabilise an aposematic strategy in solitary prey.

Evidence for a more effective signal in aggregated aposematic prey

Aposematic prey tend to live gregariously. A recent study using artificial prey has shown that a gregarious life style can be advantageous by generating faster avoidance learning in predators (Gagliardo & Guilford 1993, Proc. R. Soc. Lond. Ser. B, 286, 149-150). However, a predator may react diVerently to artificial and live prey. This study investigates whether chicks, Gallus gallus domesticus, react diVerently towards aggregations and solitary individuals of the seed bug Spilostethus pandurus (Heteroptera: Lygaeidae). There was no significant diVerence in the speed of avoidance learning between chicks presented with grouped prey and chicks presented with solitary prey. The aggregated prey did, however, generate greater unconditioned aversion than prey presented singly. This indicates that a possible advantage of grouping in aposematic prey is a more eVective aposematic signal. The greater unconditioned aversion is comparable to the generally greater initial reluctance of predators to attack aposematic than cryptic prey. ? 1996 The Association for the Study of Animal Behaviour

CONSTRAINED CAMOUFLAGE FACILITATES THE EVOLUTION OF CONSPICUOUS WARNING COLORATION

Abstract The initial evolution of aposematic and mimetic antipredator signals is thought to be paradoxical because such coloration is expected to increase the risk of predation before reaching a stage when predators associate it effectively with a defense. We propose, however, that constraints associated with the alternative strategy, cryptic coloration, may facilitate the evolution of antipredator signals and thus provide a solution for the apparent paradox. We tested this hypothesis first using an evolutionary simulation to study the effect of a constraint due to habitat heterogeneity, and second using a phylogenetic comparison of the Lepidoptera to investigate the effect of a constraint due to prey motility. In the evolutionary simulation, antipredator warning coloration had an increased probability to invade the prey population when the evolution of camouflage was constrained by visual difference between microhabitats. The comparative study was done between day‐active lepidopteran taxa, in which camouflage is constrained by motility, and night‐active taxa, which rest during the day and are thus able to rely on camouflage. We compared each of seven phylogenetically independent day‐active groups with a closely related nocturnal group and found that antipredator signals have evolved at least once in all the diurnal groups but in none of their nocturnal matches. Both studies lend support to our idea that constraints on crypsis may favor the evolution of antipredator warning signals.

Fruit or aposematic insect? Context-dependent colour preferences in domestic chicks

Colours are common stimuli in signalling systems. Requirements to function well as a signal sometimes conflict between different signallers, and the same colour stimulus is used to convey completely different messages to the same receiver. Fruits and aposematic insects both use red coloration as a signal, in the former case to signal profitability and in the latter case as a warning signal. In two experiments, we investigated whether the domestic chick, an omnivorous predator, differed in its unconditioned preference or avoidance of red and green stimuli depending on whether or not the stimulus was an insect. The experiments were designed as preference tests between red and green painted prey. The prey were live insects and artificial fruits (experiment 1), and, to investigate the effect of movement, live and dead insects (experiment 2). The chicks did not show any difference in pecking preference between red and green when fruit–like stimuli were used, but when the prey were insects, green prey were strongly preferred to red prey, and prey movement did not affect this bias. Thus, young chicks may recognize prey as insects and then discriminate between different prey colorations, or one type of food may elicit an unlearned colour preference–avoidance response that is absent with another type of food.

The effect of signal appearance and distance on detection risk in an aposematic butterfly larva (Parnassius apollo)

Aposematic coloration commonly involves patterns with contrasting colours. The early larva of Parnassius apollo is uniformly black, but the later instars develop two rows of dorsal orange spots. We tested the effect of these orange markings on the conspicuousness of the last-instar larva, by manipulating larval coloration in photographs from a natural habitat and measuring how fast human subjects could discover the larva on a touch screen. In the first experiment we compared the detectability of the natural phenotype with that of manipulated uniformly black and uniformly orange variants at different distances. In the second experiment with another set of photographs we added manipulations involving enlarged and reduced spot sizes. Generally, detection time increased with distance, and decreased with the proportion of orange in the coloration. The uniformly black larvae were surprisingly hard to detect even at the closest distances, suggesting that the young black instar has an efficient camouflage. Furthermore, even a small amount of orange colour increased the conspicuousness of the larva considerably, indicating that the orange markings are costly in terms of detectability. Importantly, as the increase in detection time over distances was larger for the natural coloration than for the orange coloration, we suggest that the natural coloration may involve a distance-dependent switch from conspicuousness to camouflage with increasing distance. Thus, even though the orange markings most probably have a signalling function, the coloration is not maximized for either crypsis or conspicuousness.

Stimulus Salience as an Explanation for Imperfect Mimicry

UNLABELLED The theory of mimicry explains how a mimic species gains advantage by resembling a model species [1-3]. Selection for increased mimic-model similarity should then result in accurate mimicry, yet there are many surprising examples of poor mimicry in the natural world [4-8]. The existence of imperfect mimics remains a major unsolved conundrum. We propose and experimentally test a novel explanation of the phenomenon. We argue that predators perceive prey as having several traits, but that the traits differ in their importance for learning. When predators learn to discriminate prey, high-salience traits overshadow other traits, leaving them under little or no selection for similarity, and allow imperfect mimicry to succeed. We tested this idea experimentally, using blue tits as predators and artificial prey with three prominent traits: color, pattern, and shape. We found that otherwise imperfect color mimics were avoided about as much as perfect mimics, whereas pattern and shape mimics did not gain from their similarity to the model. All traits could separately be perceived and learned by the predators, but the color trait was learned at a higher rate, implying that it had higher salience. We conclude that difference in salience between components of prey appearance is of major importance in explaining imperfect mimicry. VIDEO ABSTRACT