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 predator's 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. This revised version was published online in July 2006 with corrections to the Cover Date.     

Predator mixes and the conspicuousness of aposematic signals

Conspicuous warning signals of unprofitable prey are a defense against visually hunting predators. They work because predators learn to associate unprofitability with bright coloration and because strong signals are detectable and memorable. However, many species that can be considered defended are not very conspicuous; they have weak warning signals. This phenomenon has previously been ignored in models and experiments. In addition, there is significant within- and among-species variation among predators in their search behavior, in their visual, cognitive, and learning abilities, and in their resistance to defenses. In this article we explore the effects of variable predators on models that combine positive frequency-dependent, frequency-independent, and negative frequency-dependent predation and show that weak signaling of aposematic species can evolve if predators vary in their tendency to attack defended prey.     

Perception of olfactory aposematic signals by jumping spiders

Studies of aposematism are mostly focused on visual aspects of warning signalization and based on experiments with avian predators. This study presents results of experiments with an arthropod predator, a jumping spider Evarcha arcuata (Araneae: Salticidae) and olfactory (i.e., noncontact chemical) aposematic signals. Spiders were presented with chemically protected firebug Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). After acquiring the negative experience with the bugs, the spiders were offered a choice between the firebug olfactory signal and a scentless control. Spiders actively avoided the firebug signal, showing that they are able to recognize an unprofitable prey by means of olfactory chemoreception. The results show that olfactory signals alone may function as effective means of aposematic signalization to spiders.     

Combination of local selection pressures drives diversity in aposematic signals

The diversity of aposematic signals is one of the most difficult phenomena for understanding the evolution of such signals because aposematic animals are most effectively protected when they are common. Theoretical and experimental studies predict that a combination of local selection pressures could maintain variation in aposematic signals. However, the application of this hypothesis to large-scale geographic variation in aposematic signals, other than mimicry systems, is yet to be tested empirically. I investigated geographic variation in morphological and behavioural aposematic signals of the newts, Cynops pyrrhogaster, and in predation pressures on them in populations ranging over 800 km of latitude. Field experiments demonstrated that local differences in predation pressures explain well the island-mainland variation in the aposematic colouration and behaviour of newts. Furthermore, I found a latitudinal gradient in aposematic colouration but not in behaviour, independent of predation pressures. The results suggested that island-mainland variation in aposematic signals resulting from local differences in predation pressures might also be shaped by several factors, such as temperature, body size variation, and genetic differences, and such factors might act on each aposematic trait differently.     

Sexual dimorphism and intra-populational colour pattern variation in the aposematic frog Dendrobates tinctorius

Despite the predicted purifying role of stabilising selection against variation in warning signals, many aposematic species exhibit high variation in their colour patterns. The maintenance of such variation is not well understood, but it has been suggested to be the result of an interaction between sexual and natural selection. This interaction could also facilitate the evolution of sexual dichromatism. Here we analyse in detail the colour patterns of the poison frog Dendrobates tinctorius and evaluate the possible correlates of the variability in aposematic signals in a natural population. Against the theoretical predictions of aposematism, we found that there is enormous intra-populational variation in colour patterns and that these also differ between the sexes: males have a yellower dorsum and bluer limbs than females. We discuss the possible roles of natural and sexual selection in the maintenance of this sexual dimorphism in coloration and argue that parental care could work synergistically with aposematism to select for yellower males.     

Wright's shifting balance theory and the diversification of aposematic signals

Despite accumulating evidence for selection within natural systems, the importance of random genetic drift opposing Wright's and Fisher's views of evolution continue to be a subject of controversy. The geographical diversification of aposematic signals appears to be a suitable system to assess the factors involved in the process of adaptation since both theories were independently proposed to explain this phenomenon. In the present study, the effects of drift and selection were assessed from population genetics and predation experiments on poison-dart frogs, Ranitomaya imitator, of Northern Peru. We specifically focus on the transient zone between two distinct aposematic signals. In contrast to regions where high predation maintains a monomorphic aposematic signal, the transient zones are characterized by lowered selection and a high phenotypic diversity. As a result, the diversification of phenotypes may occur via genetic drift without a significant loss of fitness. These new phenotypes may then colonize alternative habitats if successfully recognized and avoided by predators. This study highlights the interplay between drift and selection as determinant processes in the adaptive diversification of aposematic signals. Results are consistent with the expectations of the Wright's shifting balance theory and represent, to our knowledge, the first empirical demonstration of this highly contested theory in a natural system.     

The role of predators in maintaining the geographic organization of aposematic signals

Selective predation of aposematic signals is expected to promote phenotypic uniformity. But while these signals may be uniform within a population, numerous species display impressive variations in warning signals among adjacent populations. Predators from different localities who learn to avoid distinct signals while performing intense selection on others are thus expected to maintain such a geographic organization. We tested this assumption by placing clay frog models, representing distinct color morphs of the Peruvian poison dart frog Ranitomeya imitator and a nonconspicuous frog, reciprocally between adjacent localities. In each locality, avian predators were able to discriminate between warning signals; the adjacent exotic morph experienced up to four times more attacks than the local one and two times more than the nonconspicuous phenotype. Moreover, predation attempts on the exotic morph quickly decreased to almost nil, suggesting rapid learning. This experiment offers direct evidence for the existence of different predator communities performing localized homogenizing selection on distinct aposematic signals.     

Individual colour patches as multicomponent signals

Colour patches are complex traits, the components of which may evolve independently through a variety of mechanisms. Although usually treated as simple, two-dimensional characters and classified as either structural or pigmentary, in reality colour patches are complicated, three-dimensional structures that often contain multiple pigment types and structural features. The basic dermal chromatophore unit of fishes, reptiles and amphibians consists of three contiguous cell layers. Xanthophores and erythrophores in the outermost layer contain carotenoid and pteridine pigments that absorb short-wave light; iridophores in the middle layer contain crystalline platelets that reflect light back through the xanthophores; and melanophores in the basal layer contain melanins that absorb light across the spectrum. Changes in any one component of a chromatophore unit can drastically alter the reflectance spectrum produced, and for any given adaptive outcome (e.g. an increase in visibility), there may be multiple biochemical or cellular routes that evolution could take, allowing for divergent responses by different populations or species to similar selection regimes. All of the mechanisms of signal evolution that previously have been applied to single ornaments (including whole colour patches) could potentially be applied to the individual components of colour patches. To reach a complete understanding of colour patch evolution, however, it may be necessary to take an explicitly multi-trait approach. Here, we review multiple trait evolution theory and the basic mechanisms of colour production in fishes, reptiles and amphibians, and use a combination of computer simulations and empirical examples to show how multiple trait evolution theory can be applied to the components of single colour patches. This integrative perspective on animal colouration opens up a host of new questions and hypotheses. We offer specific, testable functional hypotheses for the most common pigmentary (carotenoid, pteridine and melanin) and structural components of vertebrate colour patches.     

Responses of domestic chicks (Gallus gallus domesticus) to multimodal aposematic signals

Many aposematic prey combine their visual warning signals withadditional signals. Together, these signals constitute a multimodalor multicomponent warning display. The additional signals arethought to increase the effects of the visual signals on predators.Olfactory signals are much emphasized, but later studies haveshown that also auditory signals like the buzzing of certaininsects might have multimodal effects. The wasp displays typicalvisual aposematic signals, black and yellow stripes, but doesalso emit a characteristic buzzing. We wanted to test if, andin what way, the visual and acoustic display of the wasp hasan aversive function on the predators. We therefore conducteda 12-trial discrimination-learning task on inexperienced chicksto study whether there are innate biases toward these signalsand how they affect the speed of avoidance learning. We alsoperformed three extinction-learning trials to study how memorablethe signals were to the chicks. We show that the visual signalsin the display of the wasp contribute to the protection frompredators but in different ways; the yellow color had an aversiveeffect on inexperienced predators, while the striped patternimproved the aversion learning. The sound did not enhance theinnate aversions but increased the aversion learning of stripesin green prey.     

Tail colour signals performance in blue tit nestlings

Indirect sexual selection arises when reproductive individuals choose their mates based on heritable ornaments that are genetically correlated to fitness. Evidence for genetic associations between ornamental colouration and fitness remains scarce. In this study, we investigate the quantitative genetic relationship between different aspects of tail structural colouration (brightness, hue and UV chroma) and performance (cell‐mediated immunity, body mass and wing length) in blue tit (Cyanistes caeruleus) nestlings. In line with previous studies, we find low heritability for structural colouration and moderate heritability for performance measures. Multivariate animal models show positive genetic correlations between the three measures of performance, indicating quantitative genetic variation for overall performance, and tail brightness and UV chroma, two genetically independent colour measures, are genetically correlated with performance (positively and negatively, respectively). Our results suggest that mate choice based on independent aspects of tail colouration can have fitness payoffs in blue tits and provide support for the indirect benefits hypothesis. However, low heritability of tail structural colouration implies that indirect sexual selection on mate choice for this ornament will be a weak evolutionary force.     

Studies of colour polymorphism in some marginal populations of the aposematic jersey tiger moth Callimorpha quadripunctaria

Callimorpha quadripunctaria (Lepidoptera, Arctiidae) is both genetically polymorphic for hindwing colour and well protected from predators. Polymorphic populations are, however, only found in the extreme northwest of its extensive distribution in Europe and Asia Minor. Use of a colour analyser confirmed the existence of three reasonably discrete colour classes: bright red, orange and yellow. These could each be subdivided into two further groupings of phenotypes, one of moths of pure colour and the other with a secondary colour. The species is polymorphic in SW England, where it became well established in villages and towns around the Exe estuary in the late 19th century. It now extends about 30 km east and west along the south coast of Devon and up to a similar distance inland along the river valleys. The rate of spread is consistent with the substantial dispersal of up to 500 m detected in a capture-recapture experiment performed at Exeter over the whole flight period in August 1984. This experiment also found no differences in timing of emergence, survivorship or within-habitat movement between the sexes or the colour classes. Males may show a higher rate of emigration than females. The species is polymorphic throughout S Devon. Its stronghold to the west of the Exe basin is characterized by a comparatively uniform morph frequency with 5045% red, 20–40% orange and 10–20% yellow. Yellow moths have their highest frequency in this area, red moths in the east and west and orange to the north. Adult activity is concentrated in the 2–3 h after dusk. Air temperatures of higher than 15°C are probably critical to pairing which involves sex pheromones released by females. This may be an important factor limiting the species' range. Our results suggest that climatic selection pressures involving non-visual differences in fitness account for the geographical variation. The lack of daytime activity of moths in comparison to that found by other workers on Rhodes and which is likely in other warmer climates suggests the hypothesis that expression of the polymorphism is favoured in the marginal populations of NW Europe by a relaxation of the stabilizing influence on the warning coloration exerted by visual predators.     

Evolutionary implications of the form of predator generalization for aposematic signals and mimicry in prey

Generalization is at the heart of many aspects of behavioral ecology; for foragers it can be seen as an essential feature of learning about potential prey, because natural populations of prey are unlikely to be perfectly homogenous. Aposematic signals are considered to aid predators in learning to avoid a class of defended prey. Predators do this by generalizing between the appearance of prey they have previously sampled and the appearance of prey they subsequently encounter. Mimicry arises when such generalization occurs between individuals of different species. Our aim here is to explore whether the specific shape of the generalization curve can be expected to be important for theoretical predictions relating to the evolution of aposematism and mimicry. We do this by a reanalysis and development of the models provided in two recent papers. We argue that the shape of the generalization curve, in combination with the nature of genetic and phenotypic variation in prey traits, can have evolutionary significance under certain delineated circumstances. We also demonstrate that the process of gradual evolution of Müllerian mimicry proposed by Fisher is particularly efficient in populations with a rich supply of standing genetic variation in mimetic traits.     

The influence of ultraviolet reflectance differs between conspicuous aposematic signals in neotropical butterflies and poison frogs

Warning signals are often characterized by highly contrasting, distinctive, and memorable colors. Greater chromatic (hue) and achromatic (brightness) contrast have both been found to contribute to greater signal efficacy, making longwave colored signals (e.g., red and yellow), that are perceived by both chromatic and achromatic visual pathways, particularly common. Conversely, shortwave colors (e.g., blue and ultraviolet) do not contribute to luminance perception yet are also commonly found in warning signals. Our understanding of the role of UV in aposematic signals is currently incomplete as UV perception is not universal, and evidence for its utility is at best mixed. We used visual modeling to quantify how UV affects signal contrast in aposematic heliconiian butterflies and poison frogs both of which reflect UV wavelengths, occupy similar habitats, and share similar classes of predators. Previous work on butterflies has found that UV reflectance does not affect predation risk but is involved in mate choice. As the butterflies, but not the frogs, have UV‐sensitive vision, the function of UV reflectance in poison frogs is currently unknown. We found that despite showing up strongly in UV photographs, UV reflectance only appreciably affected visual contrast in the butterflies. As such, these results support the notion that although UV reflectance is associated with intraspecific communication in butterflies, it appears to be nonfunctional in frogs. Consequently, our data highlight that we should be careful when assigning a selection‐based benefit to the presence of UV reflectance.     

Context-dependent memory: colour versus odour

An olfactory stimulus and a visual stimulus were employed in a context- dependent memory study using a prose passage as the to-be-remembered item. Ninety-five university students (aged 17-35 years) learned the passage of prose in the presence of one of the stimuli and were then asked to recall the passage with the original context either reinstated or not reinstated. The results revealed a significant context-dependent memory effect for the olfactory cue but not for the visual cue. They demonstrate support for the effectiveness of odours as context cues and it is suggested that context-dependent memory processes may underlie the formation and retrieval of odour-evoked autobiographical memories.      

Ontogenetic colour change signals sexual maturity in a non-territorial damselfly

Conspicuous colouration increases male reproductive success through female preferences and/or male–male competition. Despite the advantages of conspicuous colouration, inconspicuous male morphs can exist simultaneously in a population due to genetic diversity, condition dependence or developmental constraints. We are interested in explaining the male dichromatism in Xanthagrion erythroneurum damselflies. We reared these damselflies in outdoor insectaries under natural conditions and showed that this species undergoes ontogenetic colour changes. The younger males are yellow and change colour to red 6–7 days after their emergence. We took red and yellow male reflectance spectra and found that red males are brighter than yellow males. Next, we aimed to determine whether ontogenetic colour change signals sexual maturity with field observations and laboratory experiments. Our field observational data showed that red males are in higher abundance in the breeding territory, and they have a higher mating frequency than yellow males. We confirmed these field observations by enclosing a red and a yellow male with two females and found that yellow males do not mate in presence of red males. To determine whether colour change signals sexual maturity, we measured mating success of males before and after colour changes by enclosing a single male at different age (day 3-day 7) and colour (yellow, intermediate and red) with a single female in a mating cage. Males did not mate when yellow but the same male mated after it changed colour to red, suggesting the ontogenetic colour change signals sexual maturity in this species. Our study shows that male dichromatism can be age-dependent and ontogenetic colour change can signal age and sexual readiness in non-territorial insects.     

Fearful symmetry in aposematic plants

Symmetry has been proposed to increase the efficiency of visual aposematic displays in animals, and I suggest that it may also be true for many aposematic spiny or poisonous plants. For instance, in the very spiny plant taxa cacti, Aloe sp., Agave sp. and Euphorbia sp., which have been proposed to be aposematic because of their colorful spine system, the shoots, and in cacti, the spiny fruits as well, are usually radially symmetric. Moreover, in the radial symmetric shoots of Agave and Aloe their individual spiny leaves are also bilaterally symmetric. Spiny or poisonous fruits of various other taxa, the symmetric spiny leaf rosettes and flowering spiny heads of many Near Eastern species of the Asteraceae and other taxa, and poisonous colorful flowers in taxa that were proposed to be aposematic are also symmetric. Thus, in plants, like in animals, symmetry seems to be commonly associated with visual aposematism and probably contributes to its effectiveness. Symmetry may stem from developmental constraints, or like in flowers, have other signaling functions. However, because of the better perception of symmetry by animals it may exploit inherited modes of animal sensing that probably result in paying more attention to symmetric shapes. All these possible alternatives do not negate the probable deterring role of symmetry in plant aposematism.     

Floral colour versus phylogeny in structuring subalpine flowering communities

The relative number of seeds produced by competing species can influence the community structure; yet, traits that influence seed production, such as pollinator attraction and floral colour, have received little attention in community ecology. Here, we analyse floral colour using reflectance spectra that include near-UV and examined the phylogenetic signal of floral colour. We found that coflowering species within communities tended to be more divergent in floral colour than expected by chance. However, coflowering species were not phylogenetically dispersed, in part due to our finding that floral colour is a labile trait with a weak phylogenetic signal. Furthermore, while we found that locally rare and common species exhibited equivalent floral colour distances from their coflowering neighbours, frequent species (those found in more communities) exhibited higher colour distances from their coflowering neighbours. Our findings support recent studies, which have found that (i) plant lineages exhibit frequent floral colour transitions; and (ii) traits that influence local population dynamics contribute to community structure.