The responses of wild jacamars (Galbula ruficauda,Galbulidae) to aposematic,aposematic and cryptic,and cryptic butterflies in central Brazil

1. This article reports the responses of wild, adult jacamars to butterflies with distinct coloration types in central Brazil. Fully aposematic species, i.e. those exhibiting bright and/or contrasting colours on both wing surfaces (= A/A), were predominantly sight‐rejected by birds and, with one exception, the few butterflies attacked and captured were taste‐rejected afterwards. 2. Aposematic and cryptic butterflies, i.e. those exhibiting bright and/or contrasting colours on the upper and cryptic colours on the underwings (= A/C) were sight‐rejected while flying, when they show their conspicuous colours to predators. This suggests that birds associate butterfly colours with their difficulty of capture, as in the case of Morpho and several Coliadinae species. These butterflies, however, were heavily attacked at rest, when they are cryptic. 3, Fully cryptic butterflies, i.e. those exhibiting cryptic colours on both wing surfaces (= C/C) did not elicit sight rejections by birds. Comparisons involving the number of attacks and the capture success of flying and resting individuals showed no significant differences in species more frequently observed like some cracker butterflies (Hamadryas feronia and H. februa) and Taygetis laches. Compared with the A/C Coliadinae, these butterflies showed a lesser, although not significantly different, ability to escape while flying, but a greater and significantly different ability to escape while at rest. 4, A hunting tactic of jacamars, which consists of following flying A/C and C/C butterflies on sight, and waiting until they perch to locate and attack them, is described for the first time.     

EVOLUTION OF GREGARIOUSNESS IN APOSEMATIC BUTTERFLY LARVAE: A PHYLOGENETIC ANALYSIS

Gregariousness ought to be disadvantageous for palatable organisms that live exposed and are relatively immobile and small in comparison to potential predators. Therefore, the idea that unpalatability generally evolves before egg clustering/larval gregariousness in butterflies was tested. Aposematic coloration in the larva was used as the criterion of unpalatability (it is argued that Batesian mimicry is rare in butterfly larvae), and the relative order of evolution of aposematism and gregariousness was inferred through phylogenetic analysis. Here, existing phylogenies were used, and the analysis was based on an assumption of a minimum number of evolutionary changes (parsimony). A total of 23 cases of independent evolution of gregariousness and 12 cases of independent evolution of aposematic coloration were found. In five cases, gregariousness evolved in cryptic species, the palatability of which is unknown. For lineages in which both unpalatability, as evidenced by aposematic coloration, and gregariousness were found and the two evolutionary events could be separated, unpalatability always preceded gregariousness: five cases of independent evolution of warning coloration were followed by a total of 15 cases of independent evolution of gregariousness. In no lineage did gregariousness evolve before warning coloration. It is thus concluded that unpalatability is an important predisposing factor for the evolution of egg clustering and larval gregariousness in butterflies. Insofar as kin selection is related to larval gregariousness, this study indicates that kin selection is of minor importance for the evolution of both unpalatability and warning coloration.     

Does Müllerian Mimicry Work in Nature? Experiments with Butterflies and Birds (Tyrannidae)1

The selective advantage of Müllerian mimicry in nature was investigated by releasing live mimetic and nonmimetic butterflies close to wild, aerial‐hunting tropical kingbirds (Tyrannus melancholicus) and cliff‐flycatchers (Hirundinea ferruginea) in three Amazon habitats (rain forest, a city, and “canga” vegetation). Only mimetic butterflies elicited sight‐rejections by birds, but protection conferred by mimicry was restricted to sites in which both predators and mimics co‐occurred, as in the case of six mimicry rings at a forest site and two at a city site. Most other Müllerian mimics released at city and canga vegetation were heavily attacked and consumed by birds. These results appear to reflect the birds’previous experiences with resident butterfly faunas and illustrate how birds’discriminatory behavior varied among habitats that differed in butterfly species and mimicry ring composition.     

Field observations and feeding experiments on the responses of rufous-tailed jacamars (Galbula ruficauda) to free-flying butterflies in a tropical rainforest

Wild rufous-tailed jacamars (Galbula ruficauda) were shown to prey frequently, but selectively, upon butterflies in a Costa Rican rainforest. Two individually caged birds (a male and a female) were further tested with over 1000 butterflies of 114 morphs. Both wild jacamars and the two captive individuals were able to capture and handle all kinds and sizes of local butterflies. These butterflies (and other winged insects) were recognized by the jacamars as prey only through their movement. The captive birds discriminated between an unacceptable group of butterflies, which generally fly slowly or regularly, are warningly coloured and mimetic, with transparent, or white, orange, red, and/or black coloration, and an acceptable group that generally fly fast or erratically, are cryptic (on one or both sides), and have yellow, orange, green, blue, and/or brown coloration. These different morphological and behavioural characteristics of butterflies presumably helped the jacamars to assess their palatability. Most individuals of unacceptable butterflies (e.g. Battus and Parides (Papilionidae), some Pieridae, Diaethria and Callicore (Nymphalinae), Heliconiinae, Acraeinae, Ithomiidae, and Danaidae) were sight-rejected by the male jacamar (Jacamar 2), and many of the same were also sight-rejected by the female (Jacamar 1). In cases when the above butterflies were attacked, they were quickly released and usually unharmed. The captive female bird, after long periods without food, consumed many pierid and heliconiine butterflies that were consistently rejected by the male for their distasteful and dangerous qualities. In contrast, palatable butterflies (e.g. Papilio, Charaxinae, most Nymphalinae, Morpho, Brassolinae, and Satyrinae) were usually quickly attacked and consumed. The captive jacamars were able to discriminate between the very similar colour patterns of some Batesian mimics and their models, and could memorize the palatability of a large variety of butterflies. The discriminatory abilities of specialized insectivorous birds such as jacamars are likely to play a major role in the evolution of neotropical butterfly mimicry.     

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.     

European checkerspots (Melitaeini: Lepidoptera,Nymphalidae) are not aposematic – the point of view of great tits (Parus major)

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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.     

BIRD PREDATION AS A SELECTIVE AGENT IN A BUTTERFLY POPULATION

In a population of the checkerspot butterfly, Euphydryas chalcedona, the detached wings of 309 individuals that had been attacked and eaten by birds were collected during a single flight season. During this time period a representative sample of 296 live butterflies in this population was photographed. Comparison of sex ratio and coloration of those butterflies that had been attacked with those that had not showed, first, that birds attacked slightly more females than males; and second, that among males, which are extremely variable in the amount of red on the forewing, birds attacked the less red individuals.     

Avoidance of an aposematically coloured butterfly by wild birds in a tropical forest

1. Birds are considered to be the primary selective agents for warning colouration in butterflies, and select for aposematic mimicry by learning to avoid brightly coloured prey after unpleasant experiences. It has long been thought that bright colouration plays an important role in promoting the avoidance of distasteful prey by birds. 2. The hypothesis that warning colouration facilitates memorability and promotes predator avoidance was tested by means of a field experiment using distasteful model butterflies. Artificial butterflies with a Heliconius colour pattern unknown to local birds were generated using bird vision models, either coloured or achromatic, and hung in tree branches in a tropical forest. Two sequential trials were conducted at each site to test avoidance by naïve and experienced predators. 3. There was a significant reduction in predation in the second trial. Also, coloured models were attacked less than achromatic models. Specifically, coloured butterflies were attacked significantly less in the second trial, but there was no significant decrease in predation on achromatic models. 4. The present results imply an important role for colour in enhancing aversion of aposematic butterflies. It has also been demonstrated that previous experience of distasteful prey can lead to enhanced avoidance in subsequent trials, supporting mimicry theory.     

Sexual and seasonal differences in the frequency of beak marks on the wings of two Lethe butterflies

To assess bird predation pressure on butterflies, I investigated beak marks on the wings of two Lethe butterflies for 3 years in secondary temperate forests. If bird predation had significant effects on average longevity of butterflies, and if the number of specimens preyed upon was proportionate to the number of beak-marked specimens, the beak mark frequency would be negatively correlated with average longevity of a butterfly. Bird predation pressure is generally thought to influence average longevity of butterflies. Therefore, if there is a negative correlation between beak mark frequency and average longevity, bird predation pressure would be reflected in beak mark frequency. Beak mark frequency was negatively correlated with longevity in Lethe diana (Butler), the more abundant of the two species; thus, the beak mark frequency was considered to be a suitable index of bird predation pressure on the butterflies investigated in this study. In both Lethe species, beak mark frequency was higher in females than in males. Because female butterflies have a relatively smaller thorax and flight muscles and a larger abdomen that contains eggs, they are presumably weaker or less agile fliers than males, and are probably attacked more easily by birds. In autumn, butterflies were heavily attacked by birds irrespective of sex and species. Because the numbers of lepidopteran larvae, which are the preferred prey of many birds, decreased in autumn, birds were thought to shift their diets to alternative prey such as adult butterflies.     

Investigating Müllerian mimicry: predator learning and variation in prey defences

Inexperienced predators are assumed to select for similarity of warning signals in aposematic species (Müllerian mimicry) when learning to avoid them. Recent theoretical work predicts that if co-mimic species have unequal defences, predators attack them according to their average unpalatability and mimicry may not be beneficial for the better defended co-mimic. In this study, we tested in a laboratory environment whether a uniform warning signal is superior to a variable one in promoting predator learning, and simultaneously whether co-mimics are preyed upon according to their average unpalatability. There was an interaction of signal variation and unpalatability but inexperienced birds did not select for signal similarity in artificial prey; when the prey was moderately defended a variable signal was even learnt faster than a uniform one. Due to slow avoidance learning, moderately defended prey had higher mortality than highly defended prey (although this was not straightforward), but mixing high and moderate unpalatability did not increase predation compared with high unpalatability. This does not support the view that predators are sensitive to varying unpalatability. The results suggest that inexperienced predators may neither strongly select for accurate Müllerian mimicry nor affect the benefits of mimicry when the co-mimics are unequally defended.     

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.     

Does spatial variation in predation pressure modulate selection for aposematism?

It is widely believed that aposematic signals should be conspicuous, but in nature, they vary from highly conspicuous to near cryptic. Current theory, including the honest signal or trade‐off hypotheses of the toxicity–conspicuousness relationship, cannot explain why adequately toxic species vary substantially in their conspicuousness. Through a study of similarly toxic Danainae (Nymphalidae) butterflies and their mimics that vary remarkably in their conspicuousness, we show that the benefits of conspicuousness vary along a gradient of predation pressure. Highly conspicuous butterflies experienced lower avian attack rates when background predation pressure was low, but attack rates increased rapidly as background predation pressure increased. Conversely, the least conspicuous butterflies experienced higher attack rates at low predation pressures, but at high predation pressures, they appeared to benefit from crypsis. Attack rates of intermediately conspicuous butterflies remained moderate and constant along the predation pressure gradient. Mimics had a similar pattern but higher attack rates than their models and mimics tended to imitate the signal of less attacked model species along the predation pressure gradient. Predation pressure modulated signal fitness provides a possible mechanism for the maintenance of variation in conspicuousness of aposematic signals, as well as the initial survival of conspicuous signals in cryptic populations in the process of aposematic signal evolution, and an alternative explanation for the evolutionary gain and loss of mimicry.     

Butterfly visual characteristics and ontogeny of responses to butterflies by a specialized tropical bird

The responses of two adult and three hand-reared, naive young rufous-tailed jacamars (Galbula ruficauda) to local butterflies were studied in feeding experiments. Four behavioural characteristics distinguish jacamars from other less specialized avian predators: (1) Exposed to butterflies for the first time, naive young jacamars would attack butterflies without showing signs of inhibition. Unacceptable butterflies, once captured, were taste-rejected quickly, and most survived the sampling. The few presumably unacceptable butterflies consumed by the birds were not observed to cause vomiting. (2) After gaining some familiarity with butterflies, young birds, like the adults, developed a reluctance to attack. They visually rejected certain classes of butterflies, often failing to attack them during an entire four-hour feeding trial. However, occasional attacks were made on butterflies in these ‘rejected’ classes. When this did occur, the insects proved to be actually easier to catch than those that were more often attacked. Once captured, however, the majority of these butterflies were taste-rejected. (3) For a given butterfly species, most individuals were either consumed or rejected. Thus, each species could be clearly classified as either acceptable or unacceptable to the jacamars. This consistency in jacamar responses resulted in a bimodal acceptability distribution of sympatric butterflies. (4) Young jacamars were capable of rapid associative learning and their responses were closely associated with butterfly visual characteristics in which colour pattern, flight behaviour, and morphology were also closely correlated. Thus, a single butterfly morphological parameter termed body shape (body length/thoracic diameter ratio) can adequately predict the feeding responses of jacamars. Visually detectable traits associated with butterflies possessing chemical defences may represent a balance between the need to signal unambiguously to specialized and/or experienced predators and the need to escape attacks by generalized and/or opportunistic predators. Since the proportion of specialized predators is higher in the tropical rainforest than in other habitat types, we expect greater divergence of morphological and behavioural characteristics between palatable and unpalatable butterflies in rainforest habitats.     

REVISING A CLASSIC BUTTERFLY MIMICRY SCENARIO: DEMONSTRATION OF MÜLLERIAN MIMICRY BETWEEN FLORIDA VICEROYS (LIMENITIS ARCHIPPUS FLORIDENSIS) AND QUEENS (DANAUS GILIPPUS BERENICE)

Batesian and Müllerian mimicry relationships differ greatly in terms of selective pressures affecting the participants; hence, accurately characterizing a mimetic interaction is a crucial prerequisite to understanding the selective milieux of model, mimic, and predator. Florida viceroy butterflies (Limenitis archippus floridensis) are conventionally characterized as palatable Batesian mimics of distasteful Florida queens (Danaus gilippus berenice). However, recent experiments indicate that both butterflies are moderately distasteful, suggesting they may be Müllerian comimics. To directly test whether the butterflies exemplify Müllerian mimicry, I performed two reciprocal experiments using red-winged blackbird predators. In Experiment 1, each of eight birds was exposed to a series of eight queens as “models,” then offered four choice trials involving a viceroy (the putative “mimic”) versus a novel alternative butterfly. If mimicry was effective, viceroys should be attacked less than alternatives. I also compared the birds' reactions to solo viceroy “mimics” offered before and after queen models, hypothesizing that attack rate on the viceroy would decrease after birds had been exposed to queen models. In Experiment 2, 12 birds were tested with viceroys as models and queens as putative mimics. The experiments revealed that (1) viceroys and queens offered as models were both moderately unpalatable (only 16% entirely eaten), (2) some birds apparently developed conditioned aversions to viceroy or queen models after only eight exposures, (3) in the subsequent choice trials, viceroy and queen “mimics” were attacked significantly less than alternatives, and (4) solo postmodel mimics were attacked significantly less than solo premodel mimics. Therefore, under these experimental conditions, sampled Florida viceroys and queens are comimics and exemplify Müllerian, not Batesian, mimicry. This compels a reassessment of selective forces affecting the butterflies and their predators, and sets the stage for a broader empirical investigation of the ecological and evolutionary dynamics of mimicry.     

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.     

Aposematic signal variation predicts male-male interactions in a polymorphic poison frog

Many species use conspicuous "aposematic" signals to communicate unpalatability/unprofitability to potential predators. Although aposematic traits are generally considered to be classic examples of evolution by natural selection, they can also function in the context of sexual selection, and therefore comprise exceptional systems for understanding how conspicuous signals evolve under multifarious selection. We used males from a highly territorial poison frog species in a dichotomous choice behavioral test to conduct the first examination of how aposematic signal variation influences male-male interactions. Our results reveal two behavioral patterns: (1) male dorsal brightness influences the behaviors of male conspecifics such that males approach and call to brighter males more frequently and (2) a male's dorsal brightness predicts his own behavior such that bright males approach stimulus frogs faster, direct more calls to bright stimulus frogs, and exhibit lower advertising call pulse rates (a fitness-related trait). These findings indicate the potential for sexual selection by male-male competition to impact aposematic signal evolution.     

The model of early evolution of aposematic coloration

First stages of evolution of aposematic coloration include a region of negative selection. During these stages, individuals with aberrant coloration remain to be rare, while predators are still not able to associate coloration with unpalatability. The simulation model is proposed, in which this "problematic zone" is overcome by individual selection for the increasing of unpalatable prey conspicuity in a small unisexual population. It is shown that under this assumption aposematic coloration develops within a wide range of parameters such as the cost of unpalatability, the cost of coloring, the survival rate of unpalatable prey after being attacked by na?ve predator, the probability of discovering of differently colored preys by predator as well as the predator's learning rate and memory depth. Thus, the early evolution ofaposematic coloration does not require any unusual or unique set of circumstances; aposematic coloration along with concomitant Bates mimicry inevitably evolve within a wide range of initial conditions. The loss of cryptic coloration by the original form (e.g., due to a change of food preferences, and thereby the structure of a background coloring, changes in habitat structure, color mutations etc.) is one such condition.     

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.     

Evolution of the wave: aerodynamic and aposematic functions of butterfly wing motion

Many unpalatable butterfly species use coloration to signal their distastefulness to birds, but motion cues may also be crucial to ward off predatory attacks. In previous research, captive passion-vine butterflies Heliconius mimetic in colour pattern were also mimetic in motion. Here, I investigate whether wing motion changes with the flight demands of different behaviours. If birds select for wing motion as a warning signal, aposematic butterflies should maintain wing motion independently of behavioural context. Members of one mimicry group (Heliconius cydno and Heliconius sapho) beat their wings more slowly and their wing strokes were more asymmetric than their sister-species (Heliconius melpomene and Heliconius erato, respectively), which were members of another mimicry group having a quick and steady wing motion. Within mimicry groups, wing beat frequency declined as its role in generating lift also declined in different behavioural contexts. In contrast, asymmetry of the stroke was not associated with wing beat frequency or behavioural context-strong indication that birds process and store the Fourier motion energy of butterfly wings. Although direct evidence that birds respond to subtle differences in butterfly wing motion is lacking, birds appear to generalize a motion pattern as much as they encounter members of a mimicry group in different behavioural contexts.