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.     

Beak marks on the wings of butterflies and predation pressure in the field

Beak marks on butterfly wings have been used as an indicator of predation pressure. The relationship between butterflies and their predators in the field was examined to evaluate the beak mark rate as an indicator of predation pressure. Transect censuses were conducted to measure the beak mark rate on butterflies from May to November, 2010, in Shiga Prefecture, Japan. A total of 1216 butterflies of 42 species from five families were observed during the study period. The beak mark rate in the Papilionidae was significantly higher than those of all other families. Analysis of the monthly fluctuations in the beak mark rate and relative abundance of predators revealed that the higher beak mark rates observed for two butterfly families (Papilionidae and Nymphalidae) were significantly and positively related to predation pressure, while no significant relationship was found for other families (Lycaenidae, Pieridae and Hesperiidae). Beak marks in larger butterflies (Papilionidae and Nymphalidae) can be used as an indicator to evaluate the relative intensity of predation pressure in the field.     

Evidence for the Deflective Function of Eyespots in Wild Junonia evarete Cramer (Lepidoptera,Nymphalidae)

Junonia evarete Cramer is a fast-flying butterfly that perches on the ground with wings opened exhibiting four eyespots close to wing borders. These eyespots presumably function either to intimidate predators, like insectivorous birds, or to deflect bird attacks to less vital parts of the body. We assessed the form, frequency, and location of beak marks on the wings of wild butterflies in central Brazil during two not consecutive years. We found that almost 50% of males and 80% of females bore signals of predator attacks (wing tears), most of them consisting of partially or totally V-shaped forms apparently produced by birds. Males were significantly less attacked and showed a lower proportion of attacks on eyespots than females, suggesting they are better to escape bird attacks. In contrast, females were heavily attacked on eyespots. Eyespot tears in females were higher (and significant different) than expected by chance, indicating that birds do attempt to reach the eyespots when striking on these butterflies. Other comparisons involving the proportion of tears directed or not directed to eyespots in males and females are presented and discussed.     

Beak marks on butterfly wings with special reference to Japanese black swallowtail

Birds are believed to be one of the principal predators of butterflies. The beak marks (BMs) left on the butterfly wings are useful indices of bird predation. We performed 84 collections in grasslands and woodlands during 2002–2006 in Ito, Shizuoka prefecture, and collected 893 specimens belonging to 48 species. In general, the larger was the body size the higher was the BM rate. There were two peaks in the BM rate and the peaks were higher by 13–14 % in autumn than in spring in both grasslands and woodlands. During 2007 and 2008, capture-mark-recapture surveys were conducted 82 times in a flight path of black swallowtail butterflies (BSBs). A total of 443 BSB were individually marked and released at a site 400 m away from the flight path after examining for BM, degree of wing damage, body size, sex and species. The BM% of BSB ranged from 40 to 46 %, which was the highest among the observed butterflies. The recapture rate was negatively correlated with the BM rate suggesting that the avian predation was strong enough to affect the survival rate of BSB adults. In addition, the BM rate showed a delayed positive response to BSB density in the previous month. Variation in the BM rate was analyzed with a multivariate model; it indicated that month and wing length were significant explanatory variables. In addition, the highest BM rate was observed at an intermediate wing size. These results strongly suggested that variation in the BM rate was caused by variation in avian life history and predator size. All the evidence suggested that an appreciable predation pressure by birds operated on BSB adult populations.     

Does bird predation influence the spot-number variation in Maniola jurtina (Lepidoptera)?

For six years samples of the satyrine butterfly Maniolajurtina L. were collected on small islands in southern Sweden and scored for beak marks, i.e. damage on wings presumably resulting from attacks by birds; in the present study area mainly Red-backed Shrike Lanius collurio L. An overall mean of 8% (5–1496 in different years) of the females and 1396 (10–2296) of the males had beak marks. Both sexes of M. jurtina show variation in spot-number on the hindwings and there is some evidence that in some years the frequencies of different spot-number phenotypes with beak marks differ significantly from randomness. Although it is not known how beak mark frequencies are related to predation pressure (reflecting rates of predation or escapes?) it is suggested that, due to behavioural differences of spot-number phenotypes, birds act as a selective factor influencing the spot-number variation. The results are discussed in relation to a recent model proposed by Brakefield attempting to account for variation in spot-number in M. jurtina.     

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.     

Bats as prey of diurnal birds: a global perspective

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Effects of opportunistic predation on anti-predator behavioural responses in a guild of ground foragers

We studied factors that affect prey selection by a generalist predator that opportunistically attacks prey species, and the associated inter- and intra-specific responses of prey to this type of predation. Our model system was a guild of ground-foraging birds that are preyed upon by magpies (Pica pica) during the breeding season. We found that magpies attacked up to 12 species during three consecutive breeding seasons. The overall capture success was estimated to be 4.9%. Magpies tended to attack from the air, targeting solitary prey, either on the ground or flying. Inter-specific prey responses to the risk of magpie predation included a reduction in the mean number of species occupying a foraging patch when magpies were present and a decrease in the distance between heterospecific neighbours. Intra-specific responses to magpie predation varied between species that were subject to different attack rates. Preferentially attacked prey enhanced their risk responses (increase in scanning time and scanning rate in the presence of magpies) relative to those species attacked in proportion to their abundance (increase only in scanning rate with magpies). Species attacked infrequently, relative to their abundance, showed no antipredator response. The probability of being attacked, rather than mortality rate, appears to be the factor to which prey species respond.     

Predation,thermoregulation, and wing color in pierid butterflies

Summary This paper explores two hypotheses about the relationships among predation, thermoregulation, and wing color in butterflies: First, that butterflies are susceptible to predation during thermally marginal periods (e.g., cool weather) when effective thermoregulation and flight are not possible; second, that Pieris butterflies are relatively unpalatable to visual predators, supporting the idea that the white wing pigment of Pieris represents aposematic coloration. Field experiments with Pieris and Colias in 1984 and 1985 demonstrate that substantial predation may occur during the morning period before butterflies are able to actively fly. Circumstantial evidence is presented to suggest that at least some of the predation is by small, cursorial mammals. Feeding experiments in the field using Grey Jays as predators indicate that Pieris napi and P. occidentalis are less palatable than other sympatric butterflies, including confamial Colias alexandra. These and previous results suggest that Pieris are edible but less preferred as prey by birds, and that the degree of palatibility may vary among Pieris species. The relatively low palatability of these Pieris is consistent with the hypothesis that their white pigmentation represents aposematic coloration; however, the cues by which potential bird predators might discriminate against Pieris have not been established.     

Palatablility and escaping ability in Neotropical butterflies: tests with wild kingbirds (Tyrannus melancholicus, Tyrannidae)

The palatability and the ability of neotropical butterflies to escape after being detected, attacked and captured by wild kingbirds ( Tyrannus melancholicus Vieillot), was investigated by the release of 668 individuals of 98 butterfly species close to the birds, during their usual feeding activities. Most of the butterflies were attacked and eaten. Only the troidine swallowtails ( Parities and Battus ; Papilionidae) were consistently rejected on taste and elicited aversive behaviours in birds. Most other aposematic and/or mimetic species in the gehera Danaus and Lycorea (Danainae), Dione, Eueides and Heliconius (Heliconiinae), Hypothyris, Mechanitis and Melinaea (Ithomfinae), Biblis, Callicore and Diaethria (Limenitidinae) were generally eaten. Cryptic and non-mimetic species were always attacked and, if captured, they were also eaten. All Apaturinae, Charaxinae, Nymphalinae, Hesperidae, most Limenitidinae, Heliconiinag ( Agraulis, Dryas, Dryadula and Philaethria ) and Papilionidae ( Eurytides, Heraclides and Protesilaus ) were in this group. Results indicate that the learning process in kingbirds may demand a large mortality in prey populations, even among species generally accepted as unpalatable and aposematic. They also support the assertion that escaping ability and unpalatability evolved in butterflies as alternative strategies to avoid predation by birds. Mimetic relationships among several species are discussed. Evidence for the evolution of aposematism not related to unpalatability, but to escaping ability, was found for two hard-to-catch Morpho species.     

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.     

Wing coloration and reflectance in Morpho butterflies as related to reproductive behavior and escape from avian predators

Summary Different species of large tropical butterflies belonging to the genus Morpho vary dramatically in both the amount of blue color on their wings and the associated irridescence (reflectance). This paper discusses how such a morphological properties may be related to both courtship behavior and effective means of reducing predation (especially by birds) in the low density adult populations. Essentially, the hypothesis is advanced that territorial species of Morpho can afford to possess very conspicuous wing coloration that may facilitate courtship interactions, in addition to spacing the territorial male population over the suitable habitat. While territoriality may be favored by natural selection, such behavior can only evolve if the species involved possess effective means of reducing predation, because territoriality in morphos is an extremely predictable form of behavior, toward which predators can easily orient. Two alternate hypotheses are advanced to account for low predation in a territorial morpho, Morpho amathonte, a species in which males are very bright and showy. The first hypothesis, which is more consistent with traditional ideas on the function of bright colors in morpho wings, maintains that predators learn quickly to avoid these butterflies as prey, since they are very difficult to catch. The second hypothesis, suggests that conspicuous territorial male morphos actually employ pursuit-stimuli to invite birds to attack and be subsequently unsuccessful.     

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.     

Bird predation as a selective pressure on the immature stages of the cabbage butterflies, Pieris rapae and P. brassicae

The importance of bird predation as a selective pressure on the eggs, larvae and pupae of the cabbage butterflies, Pieris rapae L. and P. brassicae L. has been investigated in a rural garden and an allotment. Birds are the main predators of all stages in a well-tended garden whereas in a field the eggs and young larvae are mainly preyed upon by arthropods. The species of avian predators vary according to the stage of development and species of prey. Consequently the relative survival rate of P. rupae and P. brussicue varies with stage of development. This changing pattern of survival has in turn acted as a selective pressure on their two main braconid parasites. Many aspects of the size, shape, colour and behaviour of the larvae and pupae of both species of Pieris appear to be adaptations to the selective pressures exerted by bird predation.     

Bird predation as a sex- and size-selective agent of the arboreal spider Pityohyphantes phrygianus

1. The solitary sheetweb spider Pityohyphantes phrygianus (Araneae: Linyphiidae) lives in canopies of coniferous trees. Earlier studies in Scandinavia have shown that bird predation affects the spider abundance negatively.
2. In a large-scale, 2-year field experiment, passerine birds were excluded from foraging on spruce branches. The experimental branches were net-enclosed, which prevented bird predation but left spiders free to leave and enter. Samples were taken in the autumn and spring for 2 years.
3. Removal of bird predation increased the mean number of subadult P. phrygianus per branch between 2·1 and 10·6 times the control number for each sex. Bird predation had approximately similar effects on the sexes, except in the second experimental spring when males were affected twice as much as females, and there was a significantly lower proportion of males on control branches exposed to bird predation than on net-enclosed branches.
4. The mean size of females was larger on net-enclosed branches than on controls in both spring samples. In males, this was the case in the first spring sample only.
5. This study shows that there are also mortality costs for both sexes associated with large size in the non-mating season. In certain winters, however, there is an additional mortality risk to males, presumably caused by a higher activity level than in females.     

Influence of driver ant swarm raids on earthworm prey densities in the Mount Kenya forest: implications for prey population dynamics and colony migrations

African driver ants are nomadic social mesopredators feeding on a highly diverse array of prey species at different trophic levels. Colonies of certain driver ant species have a biomass which can equal that of medium-sized mammalian carnivores and the ultimate cause of their nomadic life-style is thought to be local prey depletion. The impact of driver ant swarm raids is therefore expected to be strong but the degree to which they reduce prey populations has not been quantified and it is unknown whether these spectacular predators exert significant top-down effects. We examined the combined effect of driver ant (Dorylus molestus) and swarm-attending bird (Alethe poliocephala) predation on the population dynamics of earthworms, which constitute the ants’ main prey type in the montane forest of Mount Kenya. Pre-raid earthworm biomass densities in the soil layer down to a depth of 8 cm varied by a factor of 31. The immediate effect of swarm raids was a reduction in earthworm numbers in this layer, but 8 days later earthworm numbers had recovered to pre-raid levels. When earthworm biomass densities were compared, no significant effect of swarm raids was detected. The estimated proportion of earthworm prey biomass extracted from 0 to 8 cm layer by driver ants and birds together was about 2.2%. Although colony distribution was overdispersed as expected based on knowledge of D. molestus migratory behaviour, predation events were highly localized. Predation frequency was low (once every 62 days on average) and highly variable. These results indicate that earthworm prey is highly abundant but at the same time so difficult to harvest that swarm raids exert only a marginal influence on earthworm populations. Longer-term studies would be required to determine whether earthworm populations are limited by swarm raids. The small impacts of individual raids and rapid recovery of earthworm prey populations likely underlie the low frequency of migrations and short distances travelled by migrating colonies of D. molestus.     

Hybridization between two insectivorous bird species and the effect on prey-handling efficiency

Gene flow between closely related species is not always impeded by hybrid inviability or sterility but may be limited by behavioural or ecological factors. European common redstarts, Phoenicurus phoenicurus, and black redstarts, P. ochruros, are insectivorous passerine bird species which regularly interbreed in the wild and produce viable and fertile progeny. Yet, the isolation barriers, which prevent extensive gene flow between these distinct species, are unknown. I studied prey-handling time and efficiency in both species and the F₁-hybrids in captivity. All birds changed prey-handling mode from a single pick to more complex behaviour with increasing prey length and their handling time was a positive function of prey length. Common redstarts tended to handle their prey quicker than black redstarts. Hybrids appeared to be intermediate. However, individual differences were significant, but group membership was not. Handling efficiency decreased with increasing prey length and was determined by individual and family effects. Hybrid females handled their prey as efficient as hybrid males. Small differences in beak morphology could not explain individual differences in prey-handling behaviour. The results of this study suggest that prey-handling in F₁-hybrids is not a postzygotic barrier which prevent gene flow between common and black redstarts in the wild.     

The predatory behaviour of common kestrels facing various types of prey

Nine rehabilitated adult common kestrels (Falco tinnunculus) were tested for predatory behaviour. Tests were carried out individually on four different prey: two invertebrates (grasshopper and earthworm) and two vertebrates (lizard and laboratory mouse). The birds were offered prey randomly once daily, not necessarily on subsequent days. The latency to attack was similar. In contrast to predation tests with vertebrates, kestrels preying on invertebrates landed mostly (P<0.01 for earthworm and P<0.05 for grasshopper) a few centimetres from the prey itself, grasping it after a few steps. Earthworms were gripped almost invariably with the beak, but other prey with the toes. The birds struck the prey with their beak at highly variable rates (P<0.001): vertebrates mostly with the beak, while earthworms were never struck. The latency to ingest prey varied greatly (P<0.001) between prey. Captivity had only limited importance; it did not affect the behaviour sequence on any prey, but just induced kestrels in captivity for long time to attack mice with shorter latency and to strike them more with the beak. It is then demonstrated that the common kestrel has a strong behavioural plasticity even within the predatory sequence, which is then not stereotyped, and is able to modify its behaviour patterns in relation to different prey.An erratum to this article can be found at     

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.     

Does predation maintain eyespot plasticity in Bicyclus anynana?

The butterfly Bicyclus anynana exhibits phenotypic plasticity involving the wet-season phenotype, which possesses marginal eyespots on the ventral surface of the wings, and the dry-season form, which lacks these eyespots. We examined the adaptive value of phenotypic plasticity of B. anynana in relation to the defence mechanisms of crypsis and deflection. We assessed the visibility differences between spotless and spotted butterflies against backgrounds of brown (dry season) or green (wet season) leaves. Spotless butterflies were highly cryptic and less predated by adult bird predators than were spotted ones when presented against brown leaf litter. However, the advantage of crypsis disappeared in the wet-season habitat as both forms were equally visible. In later experiments, naive birds presented with resting butterflies in the wet-season habitat tended to learn more rapidly to capture spotless butterflies, suggesting a slight selective advantage of possessing eyespots. Moreover, marginal eyespots increased significantly the escape probability of butterflies that were attacked by naive birds compared to those attacked by adult birds, although there were no differences in prey capture success within naive predators. Our results show that natural selection acts against eyespots in the dry season, favouring crypsis, whereas in the wet season it may favour eyespots as deflective patterns.