Unpalatability of viceroy butterflies (Limenitis archippus) and their purported mimicry models,Florida queens (Danaus gilippus)

Summary Understanding the dynamics of defensive mimicry requires accurately characterizing the comparative palatability of putative models and mimics. The Florida viceroy butterfly (Limenitis archippus floridensis) is traditionally considered a palatable Batesian mimic of the purportedly distasteful Florida queen (Danaus gilippus berenice). I re-evaluated this established hypothesis by directly assessing palatability of viceroys and queens to red-winged blackbirds in a laboratory experiment. Representative Florida viceroys were surprisingly unpalatable to red-wings; only 40% of viceroy abdomens were entirely eaten (compared to 98% of control butterfly abdomens), and nearly one-third were immediately tasterejected after a single peck. In fact, the viceroys were significantly more unpalatable than representative Florida queens, of which 65% were eaten and 14% taste-rejected. Thus, viceroys and queens from the sampled populations exemplify Müllerian rather than Batesian mimicry, and the viceroy appears to be the stronger model. These findings prompt a reassessment of the ecological and evolutionary dynamics of this classic mimicry relationship.     

The interaction of thorns and symbiotic ants as an effective defence mechanism of swollen-thorn acacias

Evidence is provided for the interaction of ants (Crematogaster spp.) and thorns as a means of defence against browsing mammals for one species of African myrmecophyte, Acacia drepanolobium. Two experiments were conducted using goats as representative mammalian browsers. In the first experiment, the defences of individual branches were manipulated in order to assess the effectiveness of ants and thorns both on their own and together as anti-herbivore defences. It was shown that ants on their own are more effective defences for a single branch than having neither ants nor thorns, but ants from a single branch do not add significantly to the effectiveness of thorns as an anti-herbivore defence. The second experiment looked at the effect of a whole tree of ants and how they interacted with thorns in the defence of the tree. It was shown that ants from a whole tree do significantly add to the effectiveness of thorns as an anti-herbivore defence. In all cases, the goat refused to go back to and feed from a tree whose ants had just attacked it. Thorns on their own, however, do not act as total browsing deterrents. They slow down the rate of feeding but animals may compensate for this by feeding for longer periods of time. The interaction of a whole tree of ants and thorns is a very effective browsing deterrent which causes the animal to stop feeding almost immediately, therefore keeping the amount of foliage lost to a minimum. These results provide support for the hypothesis that the ant-acacia relationship (in the case of A. drepanolobium) evolved at least partly because of pressure from browsing mammals. Received: 20 October 1997 / Accepted: 28 February 1998     

Dynamics of the evolution of Batesian mimicry: molecular phylogenetic analysis of ant-mimicking Myrmarachne (Araneae: Salticidae) species and their ant models

Batesian mimicry is seen as an example of evolution by natural selection, with predation as the main driving force. The mimic is under selective pressure to resemble its model, whereas it is disadvantageous for the model to be associated with the palatable mimic. In consequence one might expect there to be an evolutionary arms race, similar to the one involving host-parasite coevolution. In this study, the evolutionary dynamics of a Batesian mimicry system of model ants and ant-mimicking salticids is investigated by comparing the phylogenies of the two groups. Although Batesian mimics are expected to coevolve with their models, we found the phylogenetic patterns of the models and the mimics to be indicative of adaptive radiation by the mimic rather than co-speciation between the mimic and the model. This shows that there is strong selection pressure on Myrmarachne, leading to a high degree of polymorphism. There is also evidence of sympatric speciation in Myrmarachne, the reproductive isolation possibly driven by female mate choice in polymorphic species.     

Polymorphic Müllerian mimicry and interactions with thermal melanism in ladybirds and a soldier beetle: a hypothesis

It is argued that groups of similarly coloured species of coccinellids are Müllerian mimicry rings. This is based on a synthesis of the literature about the nature of their biology and aposematic colour patterns, their highly developed chemical defence and the responses of bird predators to them. The system of multiple mimicry ‘rings’ is illustrated for the Dutch coccinellid fauna. Some polymorphic species, including Adalia, exhibit red forms and black melanic forms which are apparently components of different putative mimicry rings. A similar reasoning is put forward with regard to the orange and the black forms of the soldier beetle Cuntharis livida. Hypotheses involving spatial variation in comimics, as have been developed to account for some other cases of polymorphic Miillerian mimicry, predict that sympatric polymorphic species exhibiting similar sets of phenotypes will show parallels in their geographical variation. This is tested for A. bipunctata and A. decempunctata in The Netherlands. On this local scale there is no parallel variation; A. bipunctata exhibits marked geographical differentiation whereas A. decempunctata shows a general uniformity in morph frequency. Observations on their population biology show that only in A. bipunctata is there a major spring period of adult reproduction on shrubs exposed to direct sunshine. Previous work has demonstrated an influence of thermal melanism in this period of the life cycle. It is suggested that local responses in species such as A. bipunctata may reflect a partial ‘escape’ from stabilizing aposematic selection. The basis of a steep cline found in C. livida, which opposes one in A. bipunctata, is unknown and unlikely to be related to mimicry. There is some evidence that the polymorphism is influenced by non-random mating. When species and communities of coccinellids are considered on a wide geographical scale many observations about their colour patterns and spatial variation, especially those of Dobzhansky, support an interaction between selection favouring mimetic resemblance and forms of climatic selection, especially thermal melanism. The polymorphism in Adalia is discussed in relation to a system of multiple mimicry rings and to Thompson's recent theoretical treatment of the maintenance of some polymorphisms for warning coloration by a balance between aposematic and apostatic selection. This becomes more tenable in coccinellids because of evidence that bird predators show a variable response to them. Frequency-independent selection arising from thermal melanism can provide the basis of spatial variation in equilibrium points. An alternative to such a hypothesis is one in which differences in unpalatability between species of coccinellids are emphasized (after experiments of Pasteels and colleagues). Some less unpalatable species such as Adalia may have responded to periods of prolonged disruptive selection acting in a frequency-dependent way to promote polymorphic mimicry associated with different modal colour patterns and intermediate in nature between classical Batesian and Müllerian mimicry. The likely occurrence of a supergene controlling polymorphism in some coccinellids is consistent with such an explanation.     

Effects of a larval antipredator response and larval diet on adult phenotype in an aposematic ladybird beetle

Many ladybird beetles respond to a potential predation event by `reflex bleeding' or secreting a noxious defensive chemical that is similar to hemolymph. Both adults and larvae show this response. Reflex bleeding is known to reduce predator attack rates and increase prey survival after an attack, especially when reflex bleeding is employed in combination with other cues such as odor and warning coloration. In this experiment, we examined how variability in the number of reflex bleeding events and food quality in the larval stage of the aposematic ladybird beetle Harmonia axyridis affected elytral color, development time, and terminal size in adults. Effects of reflex bleeding were subtle and may have been influenced by diet treatments. Adult color did not differ between bleed treatment groups but beetles that reflex bled tended to take longer to develop and grow to smaller sizes than control group beetles. There were clear and strong effects of larval diet on adult phenotype: an ad libitum pollen diet resulted in paler adult coloration, shorter development time, and larger adult size relative to a limited-availability aphid diet. Our results suggest that the best environment for producing bright-red coloration may not be the best environment for favorable expression of life history characters, especially under stressful conditions. Interactions between different life history stages of H. axyridis are also discussed. Received: 20 April 1997 / Accepted: 30 September 1997     

Body size as a primary determinant of ecomorphological diversification and the evolution of mimicry in the lampropeltinine snakes (Serpentes: Colubridae)

Evolutionary correlations between functionally related character suites are expected as a consequence of coadaptation due to physiological relationships between traits. However, significant correlations may also exist between putatively unrelated characters due to shared relationships between those traits and underlying variables, such as body size. Although such patterns are often dismissed as simple body size scaling, this presumption may overlook important evolutionary patterns of diversification. If body size is the primary determinant of potential diversity in multiple unrelated characters, the observed differentiation of species may be governed by variability in body size, and any biotic or abiotic constraints on the diversification thereof. Here, we demonstrate that traits related to both predatory specialization (gape and diet preference) and predatory avoidance (the development of Batesian mimicry) are phylogenetically correlated in the North American snake tribe Lampropeltini. This is apparently due to shared relationships between those traits and adult body size, suggesting that size is the primary determinant of ecomorphological differentiation in the lampropeltinines. Diversification in body size is apparently not linked to climatic or environmental factors, and may have been driven by interspecific interactions such as competition. Additionally, we find the presence of a ‘key zone’ for the development of both rattle‐ and coral snake mimicry; only small snakes feeding primarily on ectothermic prey develop mimetic colour patterns, in or near the range of venomous model species.     

Salticid predation as one potential driving force of ant mimicry in jumping spiders

Many spiders possess myrmecomorphy, and species of the jumping spider genus Myrmarachne exhibit nearly perfect ant mimicry. Most salticids are diurnal predators with unusually high visual acuity that prey on various arthropods, including conspecifics. In this study, we tested whether predation pressure from large jumping spiders is one possible driving force of perfect ant mimicry in jumping spiders. The results showed that small non-ant-mimicking jumping spiders were readily treated as prey by large ones (no matter whether heterospecific or conspecific) and suffered high attack and mortality rates. The size difference between small and large jumping spiders significantly affected the outcomes of predatory interactions between them: the smaller the juvenile jumping spiders, the higher the predation risk from large ones. The attack and mortality rates of ant-mimicking jumping spiders were significantly lower than those of non-ant-mimicking jumping spiders, indicating that a resemblance to ants could provide protection against salticid predation. However, results of multivariate behavioural analyses showed that the responses of large jumping spiders to ants and ant-mimicking salticids differed significantly. Results of this study indicate that predation pressure from large jumping spiders might be one selection force driving the evolution of nearly perfect myrmecomorphy in spiders and other arthropods.     

An exceptionally high diversity of hoverflies (Syrphidae) in the food of the reed warbler (Acrocephalus scirpaceus)

Despite being considered a classical example of protective Batesian mimicry hoverflies (Syrphidae) are known to be preyed upon by various passerines. The aim of the present study was to examine in detail food brought by reed warblers Acrocephalus scirpaceus to their nests to better understand the importance of hoverflies in the diet of small passerines. Using neck collars, 273 food samples containing 8,545 food items delivered to reed warbler and parasitic common cuckoo Cuculus canorus nestlings in warbler nests were recorded. The study was conducted during three breeding seasons in South Moravia, Czech Republic. An unusually high diversity of hoverflies was found — 27 species, including Mesembrius peregrinus (critically endangered species in the Czech Republic) and Mallota cimbiciformis (endangered species) — a new taxon to the Czech Republic. This indicates that nestling diet analyses may provide not only information on avian foraging behaviour but also important faunistic data. Thus, without the detailed identification to species level of material from foraging behaviour studies valuable scientific information may be lost. Overall dominance of Syrphidae was 3.7%, the most common species being Episyrphus balteatus (55.7%, n = 318). However, this number seriously underestimates the importance of hoverflies in the diet of reed warblers as hoverflies are one of the largest prey taken by warblers. Both larvae and pupae were rare, imagines strongly dominating (92.7%). Both specific wasp mimics (e.g., Chrysotoxum verrali) and bee mimics (e.g., Eristalis spp.) were not avoided by foraging reed warblers. The presence of a parasitic cuckoo chick did not affect host foraging behaviour with respect to overall dominance of hoverflies in the diet (warbler 3.3%, cuckoo 3.8%).     

Evolution of mimicry in the New World Dysdercus (Hemiptera: Pyrrhocoridae)

Evolution of mimicry rings is reconstructed for the New World species of cotton-stainer bugs (Dysdercus, Hemiptera: Pyrrhocoridae). Using a cladistic analysis of 43 species (including D. silaceus Doesburg, 1968 stat. nov . and D. modestus Doesburg, 1968 stat. nov .), evolution of colour patterns and biogeographical history of the clade are hypothesized. Three probable mimicry rings are obtained from the analysis, together with data about their possible model–mimic or comimic–comimic structures: (a) ‘Yellow’ species in north-western South America and in the Andes (several possible models, D. rusticus, D. mimus part., D. imitator part., and D. collaris part. as mimics); (b) ‘Median Yellow–Black’ species with a median-forewing black pattern in north-western South America and Central America (several possible models, D. basialbus as a mimic); (c) ‘Median Red–Black’ species with a median-forewing black pattern in the Caribbean islands (D. andreae, D. discolor, D. neglectus–D. sanguinarius clade, and D. jamaicensis–D. fervidus–D. ocreatus clade as comimics). A few additional, less supported rings are also identified. Two highly polymorphic species (D. obscuratus, D. mimus) seem to enter different mimicry rings in different regions.     

Behavioural mimicry in flight path of Batesian intraspecific polymorphic butterfly Papilio polytes

Batesian mimics that show similar coloration to unpalatable models gain a fitness advantage of reduced predation. Beyond physical similarity, mimics often exhibit behaviour similar to their models, further enhancing their protection against predation by mimicking not only the model''s physical appearance but also activity. In butterflies, there is a strong correlation between palatability and flight velocity, but there is only weak correlation between palatability and flight path. Little is known about how Batesian mimics fly. Here, we explored the flight behaviour of four butterfly species/morphs: unpalatable model Pachliopta aristolochiae, mimetic and non-mimetic females of female-limited mimic Papilio polytes, and palatable control Papilio xuthus. We demonstrated that the directional change (DC) generated by wingbeats and the standard deviation of directional change (SDDC) of mimetic females and their models were smaller than those of non-mimetic females and palatable controls. Furthermore, we found no significant difference in flight velocity among all species/morphs. By showing that DC and SDDC of mimetic females resemble those of models, we provide the first evidence for the existence of behavioural mimicry in flight path by a Batesian mimic butterfly.     

Comparative unpalatability of mimetic viceroy butterflies (Limenitis archippus) from four south-eastern United States populations

Viceroy butterflies (Limenitis archippus), long considered palatable mimics of distasteful danaine butterflies, have been shown in studies involving laboratoryreared specimens to be moderately unpalatable to avian predators. This implies that some viceroys are Müllerian co-mimics, rather than defenseless Batesian mimics, of danaines. Here, I further test this hypothesis by assessing the palatability of wild-caught viceroys from four genetically and ecologically diverse populations in the southeastern United States. Bioassays revealed that viceroys sampled from three sites in Florida and one in South Carolina were all moderately unpalatable to captive redwinged blackbird predators, which ate fewer than half of the viceroy abdomens presented. Red-wings commonly exhibited long manipulation times and considerable distress behavior when attempting to eat a viceroy abdomen, and they taste-rejected over one-third of viceroys after a single peck. These findings, the first based on wild-caught butterflies, support the hypothesis that the viceroy-danaine relationship in some areas represents Müllerian mimicry, prompting a reassessment of selective forces shaping the interaction. Moreover, considerable variation in palatability of individual viceroys, and in behavior of individual birds, contributes to the complexity of chemical defense and mimicry in this system.     

Mimicry in hoverflies (Diptera: Syrphidae): a field test of the competitive mimicry hypothesis

Although most studies on the evolution of mimicry and warningcoloration in insects have considered predators as the majorselective force, it is possible that competition for food resourcescould also facilitate selection for these conspicuous signals.For example, when warningly colored social wasps visit flowers,then they frequently behave aggressively toward heterospecifics,and they also attack and feed on other flying insects. Underthese conditions, a resemblance to a wasp might provide a mimetichoverfly with improved access to floral resources by reducingthe frequency with which it is disturbed by other pollinators.We experimentally evaluated whether wasp-like colors and patternswere important in preventing other flower visitors from sharingthe same flower resource, using pairwise presentations of bothnatural and artificial prey in the field. Flower visitors weremore likely to visit unoccupied flowers compared with the flowerspinned with either natural or artificial specimens in 2 plantspecies with different inflorescences. However, flower visitorsdid not show a significantly reduced rate of visitation to flowerspinned with specimens bearing wasp-like colors and patternscompared with the flowers occupied by similar-sized specimensthat were nonmimetic. Overall, we found no compelling evidencein this study to support the contention that wasp-like warningsignals of hoverflies prevent other flower visitors from sharingflower resources, although insects showed a greater tendencyto avoid visiting flowers pinned with a wasp compared with flowerspinned with a nonmimetic fly.     

Sexual mimicry in Mormolyca ringens (Lindl.) Schltr. (Orchidaceae: Maxillariinae)

BACKGROUND AND AIMS: Pollination through sexual mimicry, also known as pseudocopulation, has been suggested to occur in some genera of the Neotropical orchid subtribe Maxillariinae. However, it has been demonstrated so far only for Trigonidium obtusum. This study reports and illustrates pollination through sexual mimicry in Mormolyca ringens. METHODS: A total of 70 h were dedicated to the observation of flowers and pollinator behaviour, which was photographically recorded. Flower features involved in pollinator attraction were studied using a stereomicroscope and by SEM analyses. Preliminary observations on the plant breeding system were made by manually self-pollinating flowers. The chemical composition of the fragrance volatiles was determined by GC/MS analysis. KEY RESULTS: The flower features of M. ringens parallel those of other pseudocopulatory flowers. The labellum shape and indument are reminiscent of an insect. Sexually excited drones of Nannotrigona testaceicornis and Scaptotrigona sp. (both in the Apidae: Meliponini) attempt copulation with the labellum and pollinate the flower in the process. In both bee species, the pollinarium is attached to the scutellum. Pollinator behaviour may promote some degree of self-pollination, but preliminary observations indicate that M. ringens flowers are self-incompatible. Flowers are produced all the year round, which ties in with the production of bee males several times a year. The phylogenetic relationships of M. ringens are discussed and a number of morphological and phenological features supporting them are reported. CONCLUSIONS: It is expected that further research could bring to light whether other Maxillariinae species are also pollinated through sexual mimicry. When a definitive and robust phylogeny of this subtribe is available, it should be possible to determine how many times pseudocopulation evolved and its possible evolutionary history.     

Phenological relationships of wasps, bumblebees, their mimics and insectivorous birs in northern Michigan

Abstract. 1. In northern Michigan 72% of the high fidelity dipterous Batesian mimics of bumblebees and vespoid wasps occurred in spring while they still outnumbered their models but before the great majority of fledgling birds left their nests to begin foraging for insects on their own.
2. This extends the known occurrence of this sort of phenology to several additional mimetic species and to an area which is radically different climatically and ecologically from the central Illinois areas in which this sort of phenology was first noted.
3. Our observations confirm the hypothesis that Batesian mimics may be selected to avoid the midsummer period when newly fledged insectivorous birds are abundant but have not yet learned to shun their stinging hymenopteran models.
4. The shortness of the warm season in Michigan reduces opportunities for temporal separation and may have forced the other 28% of the high fidelity mimics to occur when naive birds are abundant. The threat from naive birds was, however, presumably somewhat ameliorated by the abundance of models at that time.     

On the myrmecomorph Coquillettia insignis Uhler (Hemiptera: Miridae): arthropod predators as operators in an ant-mimetic system

The nature of female-limited mimicry in the myrmecomorphic plant bug Coquillettia insignis Uhler is described, including aspects of its relation to possible ant models and to co-occurring visual arthropod predators. Twelve species of ants were collected with C. insignis on its host plant Lupinus caudatus Kell., of which six species were common: third instar to adult female mimics closely resemble four of these six species, in both morphology and behaviour. The mimetic significance of these close correspondences is indicated by the results of over 500 feeding trials, using the three most common species of co-occurring visual arthropod predators as operators. Two of these three species (Sussacus papenhoei Gertsch: Salticidae; and Sinea diadema (Fabricius): Reduviidae), classified C. insignis with corresponding models and not with closely related, non-mimetic plant bugs. Furthermore, after having had a single 'unpleasant' experience with the ant Formica fusca assassin bugs that had previously accepted C. insignis as prey rejected them in 19 out of 23 trials. These findings indicate that C. insignis is a Batesian mimic, with visual arthropod predators functioning as one class of potential operator. Implications for future research on perception and learning in arthropod predators is briefly discussed.     

The role of escape in mimicry and polymorphism: I. The response of captive birds to artificial prey

The effectiveness of active escape as an alternative to chemical and physical irritants in defensive mimicry was tested. Philaenus spumarius is a polymorphic insect used to illustrate the hypothesis that an efficient escape mechanism could be associated with conspicuousness by potential predators causing them to avoid this type of prey.
Tile experiment used robins (Erithacus rubecula) as predators and mealworms {Tenebrio mulilur) , with colour bands of either green, orange or blue, as prey. To simulate escape the prey was offered from a lunged platform which could be dropped allowing the mealworm to roll away and out ol'sigln of the bird before it could be pecked. During the first half of the experiment (day 1–10) only one of the tin ee colours of mealworm was allowed to be caught, within a 180 s time limit. This was a cryptic non-mimetic (blue) form. The other two were the cryptic (green) and conspicuous (orange) escaping models. In the second half of the experiment (day 11–17) the platform was not lowered within the lime limit. The three forms of prey remain available; the models thus becoming the mimics.
During the first part of the experiment the birds took the non-mimetic form Ireely and learned to avoid the conspicuous and to a lesser degree the cryptic models. Throughout the second pan of the experiment the conspicuous form continued to be avoided more than the cryptic, illustrating the greater efficiency of conspicuous colour combined with escape.     

非小细胞肺癌中血管生成拟态和VEGF的表达及意义

目的探讨血管生成拟态(vasculogenic mimicry,VM)与血管内皮生长因子(vascular epithelial growth factor,VEGF)在非小细胞肺癌(non-small cell lung cancer,NSCLC)中的表达及意义。方法收集NSCLC术后标本160例和20例正常肺组织,应用免疫组化法和组织化学法检测NSCLC和正常肺组织中VM和VEGF的表达情况。结果在NSCLC组织和正常肺组织中,VM和VEGF的阳性率分别为36.9%、51.3%和0%、0%,差异有统计学意义;含有VM的NSCLC的VEGF表达高于无VM者(P<0.05),且VM与NSCLC的组织学分级、淋巴结转移及临床分期等有关(P<0.05);多因素分析:PTNM分期、VM、VEGF的表达是影响NSCLC根治术后患者预后的独立因素(P<0.05);VM阳性组与阴性组的5年生存率分别为1.7%和41.6%,差异有统计学意义;VEGF阳性组与阴性组的5年生存率分别为2.4%和52.6%,差异有统计学意义。结论具有VM的NSCLC组织分化低,患者临床预后差;VEGF的表达水平和VM与NSCLC的发展及预后有一定的关系。