Five species of passerine bird differ in their ability to detect Batesian mimics

Multiple predators affect the evolution of aposematic signals in nature and these predators may substantially differ in terms of ecological and cognitive parameters. However, most experimental studies testing the evolution of Batesian mimics use only a single species of predator (usually the great tit or a domestic chick). Therefore, in the present study, we experimentally tested the responses of five passerine predators to an artificially made Batesian mimic (a cockroach equipped with the warning pattern of the red firebug) with respect to their dietary ecology. Half of the individuals of each species were fed on unmodified roaches before the experiment, whereas the other half were fed with mealworms and thus had no previous experience with roaches. We found that Batesian mimics were better protected than inconspicuous prey against inexperienced great tits and robins alone. The other three bird species showed high level of neophobia; therefore, the effect of warning coloration could not be assessed. We also found that experienced birds attacked a greater number of Batesian mimics compared to inexperienced individuals of all tested species, with the exception of blackcaps. In the great tits, robins, and blue tits, a significant number of experienced birds attacked the Batesian mimic, which was possibly the result of a learned search image for a roach. Our results suggest that using a limited array of predators to describe evolutionary processes forming the diversity of antipredatory strategies of the prey may be biased and need not describe the situation occurring in nature.     

Avoidance of aposematic prey in European tits (Paridae): learned or innate?

Predators may either learn to avoid aposematic prey or may avoidit because of an innate bias. Learned as well as innate avoidancehas been observed in birds, but the existing evidence is basedon experiments with rather few unrelated model species. We comparedthe origin of avoidance in European species of tits (Paridae).First, we tested whether wild-caught birds (blue tits, greattits, crested tits, coal tits, willow tits, and marsh tits)avoid aposematic (red and black) adult firebugs Pyrrhocorisapterus (Heteroptera) more than nonaposematic (brown painted)ones. Larger proportion of birds avoided aposematic than brown-paintedfirebugs in majority of species (except coal tits). Second,we tested whether naive hand-reared birds of 4 species (bluetits, great tits, crested tits, and coal tits) attack or avoidaposematic and nonaposematic firebugs, both novel for them.Behavior of the naive blue tits and coal tits was similar tothat of the wild-caught birds; majority of them did not attackthe firebugs. Contrastingly, the naive great tits and crestedtits behaved differently than the wild-caught conspecific adults;majority of the wild-caught birds avoided the aposematic firebugs,whereas the naive birds usually did not show any initial avoidanceand had to learn to avoid the aposematic prey. Our results showthat the origin of avoidance may be different even in closelyrelated species. Because blue tits and coal tits avoided notonly aposematic firebugs but also their brown-painted form,we interpret their behavior as innate neophobia rather thaninnate bias against the warning coloration.     

Generalization of Mimics Imperfect in Colour Patterns: The Point of View of Wild Avian Predators

Current research of imperfect mimicry brings ambiguous results. Experiments simulating more natural conditions rather than laboratory experiments show lower willingness of avian predators to attack less perfect mimics. We decided to simulate a natural situation by testing responses of wild‐caught adult avian predators (Great tit – Parus major) to variously perfect mimics of the red firebug (Pyrrhocoris apterus), which were in previous studies shown to elicit avoidance in Great tits. Presented mimics were perfect in all traits (firebug with its own colour pattern), imperfect in colour pattern (firebug with modified colour pattern), perfect in colour pattern, but imperfect in other visual traits (cockroach with firebug colour pattern), and imperfect in colour pattern as well as in other visual traits (cockroach with modified colour patterns). Modification of the pattern focused on the rounded spots on firebug's hemielytra, which is a conspicuous trait within the pattern. The pattern modification had no influence on the number of birds attacking the prey; nevertheless, birds spent more time observing the cockroaches that displayed the perfect firebug colour pattern than in the case of any other prey. Moreover, firebugs that displayed the perfect firebug colour pattern were observed for the shortest time (equal to that of the model – unmodified firebug). Cockroaches were attacked more often than firebugs, which suggest that birds were able to use additional visual cues (shape of legs and antennae) in prey recognition. Given these result, we conclude that differences in morphological traits characteristic for used prey taxa (true bugs, cockroaches) seem to be more important in the prey's protection than its colour pattern.     

Teasing apart crypsis and aposematism – evidence that disruptive coloration reduces predation on a noxious toad

Both cryptic and aposematic colour patterns can reduce predation risk to prey. These distinct strategies may not be mutually exclusive, because the impact of prey coloration depends on a predator's sensory system and cognition and on the environmental background. Determining whether prey signals are cryptic or aposematic is a prerequisite for understanding the ecological and evolutionary implications of predator–prey interactions. This study investigates whether coloration and pattern in an exceptionally polymorphic toad, Rhinella alata, from Barro Colorado Island, Panama reduces predation via background matching, disruptive coloration, and/or aposematic signaling. When clay model replicas of R. alata were placed on leaf litter, the model's dorsal pattern – but not its colour – affected attack rates by birds. When models were placed on white paper, patterned and un‐patterned replicas had similar attack rates by birds. These results indicate that dorsal patterns in R. alata are functionally cryptic and emphasize the potential effectiveness of disruptive coloration in a vertebrate taxon.     

Reactions of passerine birds to aposematic and non-aposematic firebugs (Pyrrhocoris apterus ; Heteroptera)

In spite of the existence of many experimental studies on the function of warning coloration in insects, little is known about the universality of reactions of different predators towards a particular warning signal. Reactions of nine passerine bird species, namely Parus major , Parus caeruleus , Aegithalos caudatus , Erithacus rubecula , Turdus merula , Sylvia atricapilla , Fringilla coelebs , Carduelis chloris and Emberiza citrinella , to the firebug Pyrrhocoris apterus wildtype (brachypterous adults) and its artificially obtained (painted) brown non-aposematic variant were compared. Most insectivorous birds (great tits, blue tits, robins and blackcaps) distinguished between aposematic and non-aposematic bugs, attacking the former less often. Partly granivorous buntings and finches did not distinguish between them, and attacked both variants equally. As all the birds were caught in the wild, the results can be interpreted in terms of the presence of a higher proportion of experienced individuals among insectivorous than among omnivorous species. Two insectivorous species differed from others. The heaviest blackbird attacked and killed aposematic as well as non-aposematic firebugs, and, in contrast, the lightest long-tailed tit avoided both variants. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78 , 517–525.     

Hierarchical response to prey stimuli and associated effects of hunger and foraging experience in the fifteen-spined stickleback, Spinachia spinachia (L.)

Responsiveness of fifteen-spined sticklebacks, Spinachia spinachia (L.) to motility (rotating or still). size (larger or smaller), colour (red or green), shape (rectangular or tapered) and location (near bottom or surface of water) was investigated by presenting fish with binary choices of artificial prey, constructed from frozen mysids, trimmed, dyed and fixed to adjustable, motorized rods. Responsiveness was in the order movement > size > colour > shape = location. In natural situations, movement may distinguish edible from inedible objects, while size indicates profitability and feasibility for attack. Colour, shape and location are more specific stimuli. Sticklebacks familiar with Artemia are more responsive to red coloration, tapered shape and pelagic location, as opposed to green, rectangular and benthic characterizing Gammarus .     

Cryptic differences in colour among Müllerian mimics: how can the visual capacities of predators and prey shape the evolution of wing colours?

Antagonistic interactions between predators and prey often lead to co‐evolution. In the case of toxic prey, aposematic colours act as warning signals for predators and play a protective role. Evolutionary convergence in colour patterns among toxic prey evolves due to positive density‐dependent selection and the benefits of mutual resemblance in spreading the mortality cost of educating predators over a larger prey assemblage. Comimetic species evolve highly similar colour patterns, but such convergence may interfere with intraspecific signalling and recognition in the prey community, especially for species involved in polymorphic mimicry. Using spectrophotometry measures, we investigated the variation in wing coloration among comimetic butterflies from distantly related lineages. We focused on seven morphs of the polymorphic species Heliconius numata and the seven corresponding comimetic species from the genus Melinaea. Significant differences in the yellow, orange and black patches of the wing were detected between genera. Perceptions of these cryptic differences by bird and butterfly observers were then estimated using models of animal vision based on physiological data. Our results showed that the most strikingly perceived differences were obtained for the contrast of yellow against a black background. The capacity to discriminate between comimetic genera based on this colour contrast was also evaluated to be higher for butterflies than for birds, suggesting that this variation in colour, likely undetectable to birds, might be used by butterflies for distinguishing mating partners without losing the benefits of mimicry. The evolution of wing colour in mimetic butterflies might thus be shaped by the opposite selective pressures exerted by predation and species recognition.     

Newly emerged Batesian mimicry protects only unfamiliar prey

The evolution of Batesian mimicry was tested experimentally using avian predators. We investigated the effect of a search image on the protection effectiveness of a newly emerged Batesian mimic. The two groups of predators (adult great tits, Parus major) differed in prior experience with prey from which the mimic evolved. The Guyana spotted roach (Blaptica dubia) was used as a palatable prey from which the mimic emerged, and red firebug (Pyrrhocoris apterus) was used as a model. Optical signalization of the insect prey was modified by a paper sticker placed on its back. The cockroaches with the firebug pattern sticker were significantly better protected against tits with no prior experience with cockroaches. The protection of the firebug sticker was equally effective on cockroaches as it was on firebugs. The cockroaches with firebug stickers were not protected against attacks of tits, which were familiar with unmodified cockroaches better than cockroaches with a cockroach sticker. We suppose that pre-trained tits acquired the search image of a cockroach, which helped them to reveal the “fake” Batesian mimic. Such a constraint of Batesian mimicry effectiveness could substantially decrease the probability of evolution of pure Batesian mimic systems.     

Body‐colour variation in an orb‐web spider and its effect on predation success

Animal body coloration serves several functions such as thermoregulation, camouflage, aposematism, and intraspecific communication. In some orb‐web spiders, bright and conspicuous body colours are used to attract prey. On the other hand, there are other species whose body colour does not attract prey. Using a spider species showing individual body‐colour variation, the present study aimed to determine whether or not the variation in body colour shows a correlation with predation rates. We studied the orb‐web spider (Cyclosa argenteoalba) using both field observations and T‐maze experiments, in which the prey were exposed to differently coloured spiders. Cyclosa argenteoalba has silver‐ and black‐coloured areas on its dorsal abdomen, with the ratio of these two colours varying continuously among individuals. The bright and conspicuous silver area reflects ultraviolet light. Results of both field observations and colour choice experiments using Drosophila flies as prey showed that darker spiders have a greater chance of capturing prey than silver spiders. This indicates that body‐colour variation affects predation success among individuals and that the bright silver colour does not function to attract prey in C. argenteoalba.     

Warning Signal Efficacy: Assessing the Effects of Color,Iridescence, and Time of Day in the Field

Warning coloration deters predators from attacking distasteful or toxic prey. Signal features that influence warning color effectiveness are not well understood, and in particular, we know very little about how effective short‐wavelength and iridescent colors are as warning color elements in nature and how warning signal effectiveness changes throughout the day. We tested the effect of these factors on predation risk in nature using specimens of the distasteful pipevine swallowtail butterfly, Battus philenor. B. philenor adults display both iridescent blue and diffusely reflecting orange components in their warning signal. We painted B. philenor wings to create five different model types: all‐black, only‐iridescent‐blue, only‐orange, iridescent‐blue‐and‐orange (intact signal), and matte‐blue‐and‐orange. We placed 25 models in each of 14 replicate field sites for 72 h and checked for attacks three times each day. Model type affected the likelihood of attack; only‐orange models were, the only model attacked significantly less than the all‐black model. Iridescence did not enhance or decrease warning signal effectiveness in our experiment because matte‐blue‐and‐orange models were attacked at the same rate as iridescent‐blue‐and‐orange models. Time of day did not differentially affect model type. Video recordings of attacks revealed that insectivorous birds were responsible. The results of this experiment, when taken with previous work, indicate that the response to blue warning coloration is likely dependent on predator experience and context, but that iridescence per se does not affect warning signals in a natural context.     

Birds exploit herbivore‐induced plant volatiles to locate herbivorous prey

Arthropod herbivory induces plant volatiles that can be used by natural enemies of the herbivores to find their prey. This has been studied mainly for arthropods that prey upon or parasitise herbivorous arthropods but rarely for insectivorous birds, one of the main groups of predators of herbivorous insects such as lepidopteran larvae. Here, we show that great tits (Parus major) discriminate between caterpillar‐infested and uninfested trees. Birds were attracted to infested trees, even when they could not see the larvae or their feeding damage. We furthermore show that infested and uninfested trees differ in volatile emissions and visual characteristics. Finally, we show, for the first time, that birds smell which tree is infested with their prey based on differences in volatile profiles emitted by infested and uninfested trees. Volatiles emitted by plants in response to herbivory by lepidopteran larvae thus not only attract predatory insects but also vertebrate predators.     

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.     

Prey Luring Coloration of A Nocturnal Semi‐Aquatic Predator

Body coloration serves a variety of purposes in animals. Diurnal and nocturnal predators such as spiders may use their body coloration to lure prey. We predicted here that the white patches on the forelegs on females of the nocturnal semi‐aquatic spider Dolomedes raptor lure prey, explaining why they are primarily displayed when the spider forages along the water edge. To test our prediction, we developed a color vision model assessing whether the patches are visible to pygmy grasshoppers, the spider's primary prey. We conducted a field experiment using cardboard dummies that resemble D. raptor in size, shape, and color, but with half of them lacking leg patches, and we staged interactions between pygmy grasshoppers and D. raptor with and without leg patches in a greenhouse. We found the white patches to be visible to grasshoppers. The dummies with white patches attracted more grasshopper prey than the dummies without the patches. Moreover, grasshoppers were more attracted to spiders when their white patches were present. Our results supported the hypothesis that the white patches of D. raptor lure prey. Our findings, nevertheless, could not be explained as the spider's body coloration acting as a sensory trap but it should not be ruled out. More studies on a wider range of predators and prey will give more meaningful insights into the co‐evolution of predatory lures and prey sensory modalities.     

The role of size and colour pattern in protection of developmental stages of the red firebug (Pyrrhocoris apterus) against avian predators

We investigated how predator/prey body‐size ratio and prey colour pattern affected efficacy of prey warning signals. We used great and blue tits (Parus major and Cyanistes caeruleus), comprising closely related and ecologically similar bird species differing in body size, as experimental predators. Two larval instars and adults of the unpalatable red firebug (Pyrrhocoris apterus), differing in body size and/or coloration, were used as prey. We showed that prey body size did not influence whether a predator attacked the prey or not during the first encounter. However, smaller prey were attacked, killed, and eaten more frequently in repetitive encounters. We assumed that body size influences the predator through the amount of repellent chemicals better than through the amount of optical warning signal. The larger predator attacked, killed and ate all forms of firebug more often than the smaller one. The difference between both predators was more pronounced in less protected forms of firebug (chemically as well as optically). Colour pattern also substantially affected the willingness of predators to attack the prey. Larval red–black coloration did not provide a full‐value warning signal, although a similarly conspicuous red‐black coloration of the adults reliably protected them. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 890–898.     

Are European White Butterflies Aposematic?

It has been suggested that the white coloration of Pieridae butterflies is a warning signal and therefore all white Pieridae could profit from a mimetic resemblance. We tested whether green-veined white (Pieris napi) and orange-tip (Anthocharis cardamines) butterflies benefit from white coloration. We compared their relative acceptability to wild, adult pied flycatchers (Ficedula hypoleuca) by offering live A. cardamines and P. napi together with two non-aposematic butterflies on the tray attached to birds' nesting boxes. Experienced predators equally attacked white and non-white butterflies, and the order of attack among the Pieridae was random. If anything, there was a slight indication that the female A. cardamines was the least favoured prey. Since birds did not avoid white coloration, we compared the palatability of these two species against known palatable and unpalatable butterflies by presenting them to great tits (Parus major). Pieris brassicae, which has been earlier described as unpalatable, was also included in the palatability test. However, there were no significant differences in the palatability of the butterflies to birds, and even P. brassicae was apparently palatable to the great tits. Our results do not unambiguously support the hypothesis that the white coloration of Pieridae would signal unpalatability. Nevertheless, in our last experiment, pied flycatchers often rejected or left untouched free flying P. napi and A. cardamines. This suggests that other features in a more natural situation, such as the agile flight pattern or odours might still make them unprofitable to birds. This revised version was published online in July 2006 with corrections to the Cover Date.     

Foraging Trade‐offs between Prey Size,Delivery Rate and Prey Type: How Does Niche Breadth and Early Learning of the Foraging Niche Affect Food Delivery?

Optimal foraging theory suggests that avian parents should prefer the most energetically efficient (largest) prey items when delivering food to offspring at a central place. However, during periods of high demand, selectivity of prey may decline, leading to the delivery of smaller and/or less nutritious items. We compared foraging trade‐offs between great tits (Parus major) which had a wider feeding niche than blue tits (Cyanistes caeruleus). We also compared the foraging efficiency of cross‐fostered young, which had learned the spatial foraging niche and prey size of the foreign species, to that of control conspecifics. Mean delivery rates did not differ between control and cross‐fostered parents of either species but as delivery rates increased, prey size declined for both species and both treatment groups. However, across the range of increasing delivery rates, parents were able to increase the total biomass of prey delivered. Cross‐fostering did not alter the proportion of different prey taxa in the diet, but cross‐fostered birds shifted the size of the prey taken to that of their foster species. Consistent with their broader feeding niche, great tits, but not blue tits, incorporated more unpalatable items (flies) as delivery rates increased. Although great tits foraged less efficiently in the blue tit niche, paradoxically, blue tits seem to deliver more prey biomass when foraging in the great tit niche.     

Cannibalism of parasitoid‐attacked conspecifics in a non‐carnivorous caterpillar

Cannibalism, the killing and consumption of conspecifics, can even occur in insect species typically considered to be non‐carnivorous. Of particular interest is the cannibalism of parasitoid‐attacked conspecifics, which could reduce parasitism levels in subsequent generations for that conspecific population. This study reports on the occurrence and some of the consequences of cannibalism in parasitoid‐attacked obliquebanded leafroller, Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae). We show that larvae of C. rosaceana, which is considered to be an herbivorous caterpillar species, did not prey upon live conspecifics, but readily consumed conspecifics attacked by Habrobracon gelechiae Ashmead (Hymenoptera: Braconidae). Further examination found that C. rosaceana larvae feeding on parasitoid‐attacked conspecifics, since their fourth instar, suffered a higher mortality and reduction in body size than those fed on plant material only. The cannibalism of attacked conspecifics did not appear to offer any nutrient benefits for the cannibal. To our best knowledge, this is the first empirical example of the occurrence and some of the consequences of cannibalism by a non‐carnivorous insect on its parasitoid‐attacked conspecifics. We discuss the adaptive significance of such cannibalism on parasitoid‐attacked conspecifics with respect to a trans‐generational fitness gain for the population through the killing of the parasitoids, thereby reducing parasitism in subsequent generations.     

The conceptual and practical implications of interpreting diet breadth mechanistically in generalist predatory insects

Seasonal polyphenism in animal colour patterns indicates that temporal variation in selection pressures maintains phenotypic plasticity. Spring generation of the polyphenic European map butterfly Araschnia levana has an orange–black fritillary‐like pattern whilst individuals of the summer generation are black with white bands across the wings. What selects for the colour difference is unknown. Because predation is a major selection pressure for insect coloration, we first tested whether map butterfly coloration could have a warning function (i.e. whether the butterflies are unpalatable to birds). In a following field experiment with butterfly dummies we tested whether the spring form is better protected than the summer form from predators in the spring, and vice versa in the summer. The butterflies were palatable to birds (blue tits Cyanistes caeruleus) and in the field the spring and summer form dummies were attacked equally irrespective of season. Therefore, we found no evidence that the map butterfly is warning‐coloured or that seasonal polyphenism is an adaptation to avian predation. Because insect coloration has multiple functions and map butterfly coloration is linked to morphology, life history and development it is likely that the interplay of several selection pressures explains the evolution of colour polyphenism. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Attacks by predators on artificial cryptic and aposematic insect larvae

Colour and colour patterns seem to be especially important visual warning signals for predators, which might have innate or learned ability to avoid aposematic prey. To test the importance of larval colour pattern of the aposematic ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), an invasive alien species in Europe, we presented the plasticine models of aposematic larvae to wild and naïve birds. We studied the attacks on aposematic larvae of various patterns and colours in nature and in an outdoor aviary. The larvae were cryptic (green), aposematic (resembling those of the H. axyridis larvae), and semi-aposematic (i.e., black but missing the typical orange patches of H. axyridis larvae). We detected attacks on 71 larvae out of 450 (i.e., 2.6% daily predation). Twenty-nine attacks were made by birds, 37 by arthropods, and five by gastropods. Wild birds attacked green and black larvae significantly more often than aposematic larvae. Colour did not have an effect on attacks by arthropods. The experiment with naïve birds was conducted in an outdoor aviary, where naïve great tits, Parus major L., were offered the same artificial larvae as in the first experiment. In total, 57 of 90 exposed larvae were attacked by birds (i.e., 28% daily predation), and green larvae were attacked significantly more than the aposematic larvae (but not more than black larvae). Our results imply that aposematic larvae of H. axyridis are more than 12× less likely to be predated by birds than green larvae in nature. The aposematic pattern represented a more effective signal than the semi-aposematic signal. The ability to reject aposematic prey seemed to be innate in our birds.     

Ultraviolet cues affect the foraging behaviour of blue tits

The function of avian ultraviolet (UV) vision is only just beginning to be understood. One plausible hypothesis is that UV vision enhances the foraging ability of birds. To test this, we carried out behavioural experiments using wild-caught blue tits foraging for cabbage moth and winter moth caterpillars on natural and artificial backgrounds. The light environment in our experiments was manipulated using either UV-blocking or UV-transmitting filters. We found that the blue tits tended to find the first prey item (out of four) more quickly when UV cues were present. This suggests that UV vision offers benefits to birds when searching for cryptic prey, despite the prey and backgrounds reflecting relatively little UV. Although there was no direct effect of UV on the time taken to find all four prey items in a trial, search performance in the absence of UV wavelengths tended to increase over the course of an experiment. This may reflect changes in the search tactics of the birds. To our knowledge, these are the first data to suggest that birds use UV cues to detect cryptic insect prey, and have implications for our understanding of protective coloration.