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.     

Causes and Consequences of a Lack of Coevolution in Müllerian mimicry

Müllerian mimicry, in which both partners are unpalatable to predators, is often used as an example of a coevolved mutualism. However, it is theoretically possible that some Müllerian mimics are parasitic if a weakly defended mimic benefits at the expense of a more highly defended model, a phenomenon known as ‘quasi-Batesian mimicry’. The theory expounded by Müller and extended here for unequal unpalatability, on the other hand, suggests that quasi-Batesian mimicry should be rare in comparison with classical, or mutualistic Müllerian mimicry. Evolutionarily, quasi-Batesian mimicry has consequences similar to classical Batesian mimicry, including unilateral ‘advergence’ of the mimic to the model, and diversifying frequency-dependent selection on the mimic which may lead to mimetic polymorphism. In this paper, theory and empirical evidence for mutual benefit and coevolution in Müllerian mimicry are reviewed. I use examples from well-known insect Müllerian mimicry complexes: the Limenitis–Danaus (Nymphalidae) system in North America, the Bombus–Psithyrus (Apidae) system in the north temperate zone, and the Heliconius–Laparus (Nymphalidae) system in tropical America. These give abundant evidence for unilateral advergence, and no convincing evidence, to my knowledge, for coevolved mutual convergence. Furthermore, mimetic polymorphisms are not uncommon. Yet classical mutualistic Müllerian mimicry, coupled with spatial (and possibly temporal) variation in model abundances convincingly explain these apparent anomalies without recourse to a quasi-Batesian explanation. Nevertheless, the case against classical Müllerian mimicry is not totally disproved, and should be investigated further. I hope that this tentative analysis of actual mimicry rings may encourage others to look for evidence of coevolution and quasi-Batesian effects in a variety of other Müllerian mimicry systems. This revised version was published online in July 2006 with corrections to the Cover Date.     

DIFFERENTIAL AVOIDANCE OF CORAL SNAKE BANDED PATTERNS BY FREE-RANGING AVIAN PREDATORS IN COSTA RICA

Empirical studies of mimicry have rarely been conducted under natural conditions. Field investigations of some lepidopteran systems have provided a bridge between experiments examining artificial situations and the mimicry process in nature, but these systems do not include all types of mimicry. The presence of dangerous or deadly models is thought to alter the usual rules for mimicry complexes. In particular, a deadly model is expected to protect a wide variety of mimics. Avoidance of different types of mimics should vary according to how closely they resemble the model. Coral snake mimicry complexes in the neotropics may provide natural systems in which these ideas can be examined, but there is no direct evidence that the patterns of venomous coral snakes or potential mimics are avoided in the wild. Plasticine replicas of snakes were used to assess the frequency of avian predation attempts as a function of color pattern. Avian predators left identifiable marks on the replicas, the position of which indicated that replicas were perceived as potentially dangerous prey items by birds. The number of attacks on unmarked brown replicas was greater than that on tricolor coral snake banded replicas. This result was true whether replicas were placed on natural or plain white backgrounds, suggesting that coral snake banded patterns function aposematically. In a separate experiment, replicas representing all six patterns of proposed coral mimics at the study site were attacked less often than unmarked brown replicas. Within these six banded patterns, some were attacked significantly more often than others. This study provides direct field evidence that coral snake banded patterns are avoided by free-ranging avian predators and supports theoretical predictions about mimicry systems involving deadly models.     

华莱士在动物体色演化研究中的贡献和当代启示

华莱士不仅因为和达尔文分别提出了自然选择的理论而举世闻名, 还在马来群岛确定了现代生物地理学中区分东洋区和“澳大拉西亚区”的分界线(被后人称之为“华莱士线”), 因此也被称为是生物地理学的创始人之一。通过在不同地区的考察和标本采集, 华莱士获得了丰富的博物学经验, 以及探究环境和物种性状之间关系的机会。本文回顾了华莱士在动物体色演化规律研究领域中的贡献, 特别是他开创性地定义了动物的隐蔽色和拟态, 并初步提出了背后的驱动机制。华莱士关于动物体色演化所提出的定义和假说, 也鼓励着后来的生态学研究者通过实验和理论模型去探索。更为可贵的是, 一些动物类群的拟态机制还得到了基因组层面研究的揭示, 特别是近期证实了超级基因(supergene)和基因适应性渗入对于多物种之间拟态现象的重要贡献。随着研究方法的不断改进, 华莱士有关动物体色演化的观点会继续促进当代学者深入开展相关机制研究, 并对协同演化、物种形成、物种局部适应等研究提供重要的指导。     

Linking the evolution and form of warning coloration in nature

Many animals are toxic or unpalatable and signal this to predators with warning signals (aposematism). Aposematic appearance has long been a classical system to study predator–prey interactions, communication and signalling, and animal behaviour and learning. The area has received considerable empirical and theoretical investigation. However, most research has centred on understanding the initial evolution of aposematism, despite the fact that these studies often tell us little about the form and diversity of real warning signals in nature. In contrast, less attention has been given to the mechanistic basis of aposematic markings; that is, ‘what makes an effective warning signal?’, and the efficacy of warning signals has been neglected. Furthermore, unlike other areas of adaptive coloration research (such as camouflage and mate choice), studies of warning coloration have often been slow to address predator vision and psychology. Here, we review the current understanding of warning signal form, with an aim to comprehend the diversity of warning signals in nature. We present hypotheses and suggestions for future work regarding our current understanding of several inter-related questions covering the form of warning signals and their relationship with predator vision, learning, and links to broader issues in evolutionary ecology such as mate choice and speciation.     

Non-visual crypsis: a review of the empirical evidence for camouflage to senses other than vision

I review the evidence that organisms have adaptations that confer difficulty of detection by predators and parasites that seek their targets primarily using sensory systems other than vision. In other words, I will answer the question of whether crypsis is a concept that can usefully be applied to non-visual sensory perception. Probably because vision is such an important sensory system in humans, research in this field is sparse. Thus, at present we have very few examples of chemical camouflage, and even these contain some ambiguity in deciding whether they are best seen as examples of background matching or mimicry. There are many examples of organisms that are adaptively silent at times or in locations when or where predation risk is higher or in response to detection of a predator. By contrast, evidence that the form (rather than use) of vocalizations and other sound-based signals has been influenced by issues of reducing detectability to unintended receivers is suggestive rather than conclusive. There is again suggestive but not completely conclusive evidence for crypsis against electro-sensing predators. Lastly, mechanoreception is highly understudied in this regard, but there are scattered reports that strongly suggest that some species can be thought of as being adapted to be cryptic in this modality. Hence, I conclude that crypsis is a concept that can usefully be applied to senses other than vision, and that this is a field very much worthy of more investigation.     

Coincident disruptive coloration

Even if an animal matches its surroundings perfectly in colour and texture, any mismatch between the spatial phase of its pattern and that of the background, or shadow created by its three-dimensional relief, is potentially revealing. Nevertheless, for camouflage to be fully broken, the shape must be recognizable. Disruptive coloration acts against object recognition by the use of high-contrast internal colour boundaries to break up shape and form. As well as the general outline, characteristic features such as eyes and limbs must also be concealed; this can be achieved by having the colour patterns on different, but adjacent, body parts aligned to match each other (i.e. in phase). Such 'coincident disruptive coloration' ensures that there is no phase disjunction where body parts meet, and causes different sections of the body to blend perceptually. We tested this theory using field experiments with predation by wild birds on artificial moth-like targets, whose wings and (edible pastry) bodies had colour patterns that were variously coincident or not. We also carried out an experiment with humans searching for analogous targets on a computer screen. Both experiments show that coincident disruptive coloration is an effective mechanism for concealing an otherwise revealing body form.     

Can't tell the caterpillars from the trees: countershading enhances survival in a woodland

Perception of the body's outline and three-dimensional shape arises from visual cues such as shading, contour, perspective and texture. When a uniformly coloured prey animal is illuminated from above by sunlight, a shadow may be cast on the body, generating a brightness contrast between the dorsal and ventral surfaces. For animals such as caterpillars, which live among flat leaves, a difference in reflectance over the body surface may degrade the degree of background matching and provide cues to shape from shading. This may make otherwise cryptic prey more conspicuous to visually hunting predators. Cryptically coloured prey are expected to match their substrate in colour, pattern and texture (though disruptive patterning is an exception), but they may also abolish self-shadowing and therefore either reduce shape cues or maintain their degree of background matching through countershading: a gradation of pigment on the body of an animal so that the surface closest to illumination is darker. In this study, we report the results from a series of field experiments where artificial prey resembling lepidopteran larvae were presented on the upper surfaces of beech tree branches so that they could be viewed by free-living birds. We demonstrate that countershading is superior to uniform coloration in terms of reducing attack by free-living predators. This result persisted even when we fixed prey to the underside of branches, simulating the resting position of many tree-living caterpillars. Our experiments provide the first demonstration, in an ecologically valid visual context, that shadowing on bodies (such as lepidopteran larvae) provides cues that visually hunting predators use to detect potential prey species, and that countershading counterbalances shadowing to enhance cryptic protection.     

Empirical tests of the role of disruptive coloration in reducing detectability

Disruptive patterning is a potentially universal camouflage technique that is thought to enhance concealment by rendering the detection of body shapes more difficult. In a recent series of field experiments, artificial moths with markings that extended to the edges of their 'wings' survived at higher rates than moths with the same edge patterns inwardly displaced. While this result seemingly indicates a benefit to obscuring edges, it is possible that the higher density markings of the inwardly displaced patterns concomitantly reduced their extent of background matching. Likewise, it has been suggested that the mealworm baits placed on the artificial moths could have created differential contrasts with different moth patterns. To address these concerns, we conducted controlled trials in which human subjects searched for computer-generated moth images presented against images of oak trees. Moths with edge-extended disruptive markings survived at higher rates, and took longer to find, than all other moth types, whether presented sequentially or simultaneously. However, moths with no edge markings and reduced interior pattern density survived better than their high-density counterparts, indicating that background matching may have played a so-far unrecognized role in the earlier experiments. Our disruptively patterned non-background-matching moths also had the lowest overall survivorship, indicating that disruptive coloration alone may not provide significant protection from predators. Collectively, our results provide independent support for the survival value of disruptive markings and demonstrate that there are common features in human and avian perception of camouflage.     

Evolutionary significance of ontogenetic colour change in animals

Ontogenetic colour changes are non-reversible colour changes associated with normal progressive development of an individual of a species. This paper provides the first review of the evolutionary significance of this phenomenon in animals. Proximate mechanisms and environmental cues are briefly discussed and a conceptual framework for understanding the ultimate reasons for ontogenetic colour change is established. Changes in size, vulnerability, reproductive status, habitat and metabolism are often associated with ontogenetic colour change and can aid in understanding its adaptive significance. Neutral or non-adaptive ontogenetic colour changes due to phylogenetic inertia and developmental constraints are also considered. Existing studies of ontogenetic colour changes in marine invertebrates, terrestrial invertebrates, fish, amphibians, reptiles, birds and mammals are discussed within this framework. A need is identified for more experimental tests of hypotheses for the significance of ontogenetic colour change.