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.     

Low Ability of Great Tits to Discriminate Similarly Inconspicuous Edible and Inedible Prey

Numerous studies have shown warning coloration to facilitate the discrimination of edible and inedible prey. However, inedible insect species may possess cryptic coloration as well. It has been shown that some other visual features (especially characteristic body shape) are sufficient for the recognition of some insect taxa (e.g. ladybirds, ants, wasps). We tested the ability of wild‐caught great tits (Parus major) to discriminate between the identically coloured edible (roach – Blaptica dubia) and the inedible (firebug – Pyrrhocoris apterus) as prey according to subtle peripheral visual traits (shape of legs and antennae, body posture, and means of locomotion). Both prey species were offered either simultaneously or alternately. The ability of the birds to learn was tested by means of fourteen trial repetitions in two sessions. In general, great tits were not able to learn to discriminate between firebugs and roaches by subtle shape cues alone during the two sessions. However, multivariate analysis of individual bird behaviour showed that they adopted one of three different attitudes to the presented prey. Most of the birds never attacked any or always attacked both prey. In addition, a small proportion of the birds was able to discriminate between the two prey types and attacked only roaches. Nevertheless, firebugs survived most of the attacks, which suggests that in case of chemically protected prey, the evolution of conspicuous coloration is not always the best/only option.     

Importance of colour in the reaction of passerine predators to aposematic prey: experiments with mutants of Pyrrhocoris apterus (Heteroptera)

Persistent questions concerning the warning coloration of unpalatable insects address whether the bright aposematic colour itself or its combination with a species-specific dark pattern is the key factor in their protection against insectivorous birds, and how chromatic polymorphism originates and is maintained in aposematics. In the present study, these questions were tested experimentally, using the birds Parus major , Parus caeruleus , Erithacus rubecula , and Sylvia atricapilla as predators, and chromatically polymorphic firebug Pyrrhocoris apterus : red wild form, white, yellow, and orange mutants (all four of them with the same black melanin pattern, the mutants differing in colour of pteridine pigments only) and the nonaposematic brown-painted wild form as prey. The results show that a specific colour is essential for the birds to recognize the specific aposematic prey; the melanin pattern is not sufficient. White mutants were no better protected than nonaposematic firebugs; red wild-type and orange mutants were equally well protected against all bird species; and the reaction of birds to yellow mutants was species-specific. An evolutionary scenario of 'recurrent recessive mutations' is formulated to explain the origin of colour polymorphism in some aposematics.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 143–153.     

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.     

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.     

Dietary conservatism may facilitate the initial evolution of aposematism

It has generally been assumed that warningly coloured organisms pay a cost associated with their increased visibility, because naïve predators notice and eat them. This cost is offset by their enhanced protection from educated predators who associate the colour pattern with unprofitability. However, some studies have suggested that avoidance of novel prey by avian predators ("dietary conservatism") can actually place novel colour morphs at a selective advantage over familiar ones, even when they are highly conspicuous. To test this idea, we experimentally simulated the appearance of a single novel-coloured mutant in small populations (20 individuals) of palatable artificial prey. The colour morph frequencies in each "generation" were determined by the relative survival of the previous generation under predation by birds. We used wild-caught European robins Erithacus rubecula foraging on pastry "prey" of different colours. The aim was to test whether prey selection by predators prevented or facilitated the novel colour morph persisting in the prey population over successive generations. We found that the novel colour morph quickly increased to fixation in 14/40 prey "populations", and at least once each in 8 of the 10 birds tested. Novel mutants of the classic aposematic colours (red and yellow) reached fixation most frequently, but even the green and blue novel morphs both increased to fixation in 2/40 trials. Novel colours reached fixation significantly faster than could be accounted for by drift, indicating active avoidance by the birds. These results suggest that a novel colour morph arising in a prey population can persist and increase under the selective pressure imposed by predators, even to the local exclusion of the original morph, despite being fully palatable. The consequences of this finding are discussed in relation to receiver psychology, the evolution of aposematism and the existence of polymorphism in Müllerian mimics.     

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.     

Can experienced birds select for Mullerian mimicry?

Field experiments have shown that avian predators in the wildcan select for similarity of warning signals in aposematic prey(Müllerian mimicry) because a common signal is better protectedthan a signal that is novel and rare. The original theory ofMüllerian mimicry assumes that the mechanism promotingmimicry is predator learning; by sharing a signal, the comimicspecies share the mortality that is due to sampling by inexperiencedpredators. Predation events have not been observed in the wild,and learning experiments with naive bird predators in a laboratoryhave not unambiguously shown a benefit of a uniform signal comparedwith different signals. As predators in the field experimentsare likely to be more experienced compared with previous laboratoryexperiments, we studied selection by experienced predators ona novel imperfect mimic. We trained great tits Parus major toavoid artificial aposematic models and subsequently introducedperfect and imperfect mimics at different frequencies. Birdswith prior experience on the models selected against the imperfectmimics that were at a disadvantage also in a memory test conducteda week after their introduction. Selection against the imperfectmimics was antiapostatic. However, the imperfect mimics alsobenefited from some signal generalization to the models andpossibly gained protection because the birds were familiar withthe alternative cryptic prey that was also present. Our resultssuggest that experienced predators might be more important tothe evolution of mimicry than the learning-based theory assumes.     

Both novelty and conspicuousness influence selection by mammalian predators on the colour pattern of Plethodon cinereus (Urodela: Plethodontidae)

Predators influence the evolution of colour pattern in prey species, yet how these selective forces might differ among predators is rarely considered. In particular, prey colour patterns that indicate unpalatability to some predator species may not carry the same signal for other predators. We test several hypotheses of selection on patterning between mammal predators and the polymorphic salamander Plethodon cinereus, which, under an avian visual system appears as a mimic of the toxic newt Notophthalmus viridescens. We fit each hypothesis against field observations of mammalian attacks on salamander clay replicas. We then develop a novel analytical procedure that enables the combination of multiple non‐exclusive models in a likelihood framework. We find that mammals do not follow any single hypothesis proposed, including the hypothesis of mimicry. Instead, mammals in this system use visual cues while foraging to avoid unfamiliar, novel prey and attack conspicuous prey. We propose that mammals may help to maintain colour pattern polymorphism within populations of P. cinereus by avoiding novel, unfamiliar colour morphs. Additionally, selective pressures from multiple predators and variation in predator communities among sites may contribute to the maintenance of colour polymorphism within and among localities in this salamander species.     

The importance of pattern similarity between Müllerian mimics in predator avoidance learning

Müllerian mimicry, where unpalatable prey share common warning patterns, has long fascinated evolutionary biologists. It is commonly assumed that Müllerian mimics benefit by sharing the costs of predator education, thus reducing per capita mortality, although there has been no direct test of this assumption. Here, we specifically measure the selection pressure exerted by avian predators on unpalatable prey with different degrees of visual similarity in their warning patterns. Using wild-caught birds foraging on novel patterned prey in the laboratory, we unexpectedly found that pattern similarity did not increase the speed of avoidance learning, and even dissimilar mimics shared the education of naive predators. This was a consistent finding across two different densities of unpalatable prey, although mortalities were lower at the higher density as expected. Interestingly, the mortalities of Müllerian mimics were affected by pattern similarity in the predicted way by the end of our experiment, although the result was not quite significant. This suggests that the benefits to Müllerian mimics may emerge only later in the learning process, and that predator experience of the patterns may affect the degree to which pattern similarity is important. This highlights the need to measure the behaviour of real predators if we are to understand fully the evolution of mimicry systems.     

Parasitoid wasp affects metabolism of cockroach host to favor food preservation for its offspring

Unlike predators, which immediately consume their prey, parasitoid wasps incapacitate their prey to provide a food supply for their offspring. We have examined the effects of the venom of the parasitoid wasp Ampulex compressa on the metabolism of its cockroach prey. This wasp stings into the brain of the cockroach causing hypokinesia. We first established that larval development, from egg laying to pupation, lasts about 8 days. During this period, the metabolism of the stung cockroach slows down, as measured by a decrease in oxygen consumption. Similar decreases in oxygen consumption occurred after pharmacologically induced paralysis or after removing descending input from the head ganglia by severing the neck connectives. However, neither of these two groups of cockroaches survived more than six days, while 90% of stung cockroaches survived at least this long. In addition, cockroaches with severed neck connectives lost significantly more body mass, mainly due to dehydration. Hence, the sting of A. compressa not only renders the cockroach prey helplessly submissive, but also changes its metabolism to sustain more nutrients for the developing larva. This metabolic manipulation is subtler than the complete removal of descending input from the head ganglia, since it leaves some physiological processes, such as water retention, intact.     

Do predators limit the abundance of alternative prey? Experiments with vole‐eating avian and mammalian predators

Predation has been invoked as a factor synchronizing the population oscillations of sympatric prey species, either because predators kill prey unselectively (the Shared Predation Hypothesis; hereafter SPH), or because predators switch to alternative prey after a density decline in their main prey (the Alternative Prey Hypothesis; APH). A basic assumption of the APH is that the impact of predators on alternative prey depends more on the density of main prey than on the predator/alternative prey ratio. Both SPH and APH assume that the impact of predators on alternative prey is at least periodically strong enough to depress prey populations. To examine these assumptions, we utilized data from replicated field experiments in large areas where we reduced the breeding densities of avian predators during three years and the numbers of least weasels (Mustela nivalis) in two years when vole populations declined. In addition, we reduced the breeding densities of avian predators in two years when vole populations were high. The reduction of least weasels increased the abundance of their alternative prey, small birds breeding on the ground, but did not affect the abundance of common shrews (Sorex araneus). In years when vole populations declined, the reduction of avian predators increased the abundance of their alternative prey, common shrews and small birds. Therefore, vole‐eating predators do at least periodically depress the abundance of their alternative prey. At high vole densities, the reduction of avian predators did not increase the abundance of common shrews, although the ratio of avian predators to alternative prey was similar to years when vole populations declined, which supported APH. In contrast, the abundance of small birds increased after the reduction of avian predators also at high vole densities, which supported SPH. The manipulations had no obvious effect on the number of game birds, which are only occasionally killed by these small‐sized predators. We conclude that in communities where most predators are small or specialize on a single prey type, the synchronizing impact of predation is restricted to a few similar‐sized species.     

Visual warning signals of the ladybird Harmonia axyridis: the avian predators’ point of view

Previous studies have suggested that spotted patterns are important in the protection of ladybirds against attack by avian predators. Nevertheless, these studies were based on the comparison of several ladybird species differing in colouration, but also in other traits (e.g., chemical protection). We presented natural as well as artificial colour modifications (using brown, red, and black paint) of the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) – an invasive alien species for Europe – to an avian predator, the great tit, Parus major L. (Passeriformes: Paridae). All forms were considered to be equal in size, but differed in colouration and in the presence of spots. The chemical protection was equal except for one form. The birds displayed strong avoidance of all forms with red and black colouration; beetles with artificially removed red colouration (painted brown) were attacked more often. The beetles painted brown with black spots were slightly better protected than the painted beetles without spots. We can sum up that spots are of some importance in the protection of ladybirds; nevertheless, red and black colouration is the main part of the visual signal.     

Importance of conspicuous colours in warning signals: the great tit’s (Parus major) point of view

Few studies have dealt with the importance of colours per se in warning signalling, with the use of a broader array of different colours. We tested the reactions of great tits (Parus major) to colour modifications (red, orange, yellow, white, blue, violet, and green) of the warning signal of the red firebug (Pyrrhocoris apterus), preserving its typical black pattern. We used the edible Guyana spotted roach (Blaptica dubia) as the prey, each of which carried a paper sticker shield of a particular colour on its back. With such prey, the effects of the other traits of the red firebug (e.g. shape of the legs and antennae or chemical signals) on the birds’ reactions were removed. All of the conspicuous forms of the prey, possessing a black pattern, were protected against great tits better than the non-patterned brown control form. The level of protection decreased from those forms with colours similar to the model and commonly occurring in warning signals in nature (red, orange, yellow), through other conspicuous colours rarely occurring in warning signals in nature (white, violet, blue), to the colour which usually occurs as cryptic in nature (green). In the green form, repeated encounters were necessary to reach avoidance. Avoidance learning came to pass despite the fact that the presented prey was neither inedible nor distasteful.     

Testing chemical defence based on pyrrolizidine alkaloids

Pyrrolizidine alkaloids are considered the primary defence mechanism in aposematic ithomiine butterflies and arctiid moths. Despite evidence that pyrrolizidine alkaloids are effective against some invertebrate predators, proof for a protective function of pyrrolizidine alkaloids against vertebrate predators is fragmented. The present work shows that the pyrrolizidine alkaloid monocrot-aline is unpalatable to the pileated finch,Coryphospingus pileatusand that the unpalatability is learned through association with a specific colour pattern (blue stripes). In a series of trials, using mealworms as model prey, birds rejected those to which pyrrolizidine alkaloid solution had been applied topically but accepted prey devoid of the alkaloid. Subsequent offerings of prey with pyrrolizidine alkaloid and a painted blue-striped pattern led to consistent rejections by the experimental birds. Birds were then offered blue-striped painted larvae without pyrrolizidine alkaloids (‘mimics’), which were rejected at levels similar to the previous trial. The predators learned to recognize the prey as unpalatable items based on their experience in the previous encounters. These results provide evidence for the protective capacity of the pyrrolizidine alkaloid against a vertebrate predator and supports the role of these chemicals in aposematism in the Lepidoptera.     

Imperfect Batesian mimicry—the effects of the frequency and the distastefulness of the model

Batesian mimicry is the resemblance between unpalatable models and palatable mimics. The widely accepted idea is that the frequency and the unprofitability of the model are crucial for the introduction of a Batesian mimic into the prey population. However, experimental evidence is limited and furthermore, previous studies have considered mainly perfect mimicry (automimicry). We investigated imperfect Batesian mimicry by varying the frequency of an aposematic model at two levels of distastefulness. The predator encountered prey in a random order, one prey item at a time. The prey were thus presented realistically in a sequential way. Great tits (Parus major) were used as predators. This experiment, with a novel signal, supports the idea that Batesian mimics gain most when the models outnumber them. The mortalities of the mimics as well as the models were significantly dependent on the frequency of the model. Both prey types survived better the fewer mimics there were confusing the predator. There were also indications that the degree of distastefulness of the model had an effect on the survival of the Batesian mimic: the models survived significantly better the more distasteful they were. The experiment supports the most classical predictions in the theories of the origin and maintenance of Batesian mimicry.     

Ringing or colour-banding does not increase predation mortality in redshanksTringa totanus

The use of metal and colour‐rings or bands as a means of measuring survival, movements and behaviour in birds is universal and fundamental to testing ecological and evolutionary theories. The practice rests on the largely untested assumption that the rings do not affect survival. However this assumption may not hold for several reasons, for example because the ‘oddity effect’ predicts predators select prey that appear different to their neighbours in order to avoid the ‘confusion effect’. We compared the foraging behaviour and the death rates of redshanks Tringa totanus conspicuously marked with six colour rings and one metal ring each to unmarked birds in a study system, where routinely up to 50% of the total population are killed by avian predators during a winter. If avian predators selectively target and/or have a higher capture success of ringed birds then we would predict the proportion of colour‐ringed birds in the population to decline through a winter. The proportion of colour‐ringed birds in the population did not change over the course of three separate winters, and in one winter the ratio of marked:unmarked birds found killed by sparrowhawks Accipiter nisus was the same as the ratio of marked birds alive in the population. In the year with largest sample size, power was sufficient to detect a greater than 2.2% difference in predation rate between ringed and unringed groups. The average kill rate difference between ringed and unringed birds across the three winters was less than 1% (0.73±2.2%) suggesting that even if there were differences in predation rate that were not detected because of low statistical power they were extremely small. There were no differences in any foraging measures comparing ringed and unringed birds, suggesting that the rings did not affect the ability of birds to meet their daily energy budgets. The results showed that colour‐ringed birds were not preferentially targeted or killed by avian predators, and suggest that the presence of a metal and even several large colour‐rings is unlikely to affect behaviour and predation mortality even under extreme selection.     

Frequency-dependent taste-rejection by avian predation may select for defence chemical polymorphisms in aposematic prey

Chemically defended insects advertise their unpalatability to avian predators using conspicuous aposematic coloration that predators learn to avoid. Insects utilize a wide variety of different compounds in their defences, and intraspecific variation in defence chemistry is common. We propose that polymorphisms in insect defence chemicals may be beneficial to insects by increasing survival from avian predators. Birds learn to avoid a colour signal faster when individual prey possesses one of two unpalatable chemicals rather than all prey having the same defence chemical. However, for chemical polymorphisms to evolve within a species, there must be benefits that allow rare chemical morphs to increase in frequency. Using domestic chicks as predators and coloured crumbs for prey, we provide evidence that birds taste and reject proportionally more of the individuals with rare defence chemicals than those with common defence chemicals. This indicates that the way in which birds attack and reject prey could enhance the survival of rare chemical morphs and select for chemical polymorphism in aposematic species. This is the first experiment to demonstrate that predators can directly influence the form taken by prey's chemical defences.     

Further evidence for apostatic selection by wild passerine birds -9 :1 experiments.

Apostatic selection occurs when predators concentrate disproportionately on the common varieties of non-mimetic polymorphic prey species. This has been tested in 14 experiments by presenting populations of green and brown lard-and-flour "baits" to inexperienced wild passerine birds in their normal surroundings. In seven experiments a 9 green : 1 brown population was presented for a number of days, followed by a 1 green : 9 brown population for a similar period. in the remaining seven experiments the populations were presented in the reverse order. The birds often had strong "natural" colour preferences (for example, blackbirds and songthrushes preferred browns) which were not caused by the relative conspicuousness of the two colours. The data within most of the experiments were very heterogeneous, but in every experiment there was good evidence that the birds tended to concentrate on the common colour. The consistency of the replicated experiements gives strong reason to believe that apostatic selection is a widespread phenomenon among avian predators, and provides an explanation for many of the non-mimetic colour and pattern polymorphisms found among their prey.     

Absorbance of retinal oil droplets of the budgerigar: sex,spatial and plumage morph-related variation

Intraspecific variation in photoreceptor physiology is known in several vertebrate taxa, but is currently unknown in birds, despite many avian traits varying intraspecifically, and avian visual ecology encompassing a wide range of environments and visual stimuli, which might influence spectral sensitivity. Avian retinal photoreceptors contain light absorbing carotenoid-rich oil droplets that affect vision. Carotenoids are also important plumage components. However, our understanding of the regulation of carotenoids in oil droplets remains rudimentary. Among birds, Melopsittacus undulatus has probably the best-studied colour vision, shows profound intraspecific variation in plumage colour, and increased plasma carotenoids during moult. We used microspectrophotometry to determine whether a relationship exists between oil droplet carotenoid concentration and plumage pigmentation, and tested for sex and spatial variation in droplet absorbance across the retina. Absorbance of one variety of P-type droplets was higher in males. No relationship was found between droplet absorbance and plumage colour. We found a spatial pattern of droplets absorbance across the retina that matched a pattern found in another parrot, and other avian species. Our work provides insights into the development and maintenance of retinal oil droplets and suggests a common mechanism and function for carotenoid deposition in the retina across bird species.