Aposematic Signals Research Articles

Detectability of a poison frog and its Batesian mimic depends on body posture and viewing angle.

Aposematic signals warn predators that prey should be avoided due to dangerous secondary defences. However, as warning signals do not always produce avoidance, warning colors may evolve as a trade-off balancing detectability against signal saliency. For Batesian mimics, which display salient signals but lack secondary defenses, the costs of predator encounters are greater, potentially increasing the benefit of crypsis. This raises the question of whether imperfect mimicry may reduce detectability while retaining mimetic efficacy. We tested this hypothesis with the poisonous frog Ameerega bilinguis and undefended Batesian mimic Allobates zaparo, using computational visual modeling and screen-based detection trials with human participants. We found that both species incorporate camouflage into their warning colors, but to different degrees depending on viewing angle and behavior. Contrary to expectation, we found differences in detectability between model and mimic that do not adhere to the hypothesized cryptic mimetic phenotype. To aerial observers, we found the mimic to be more detectable than the model. To terrestrial observers, likely owing to the model's bright ventral color, we found the model more detectable in viewing angles that highlight the ventral coloration, whereas the mimic was more detectable in viewing angles that highlight the dorsal coloration. Consequently, we suggest that in addition to being the result of perceptual or developmental constraints, imperfect mimicry may also evolve as an adaptive strategy which balances camouflage with different signaling functions. Our findings complement the emerging view that aposematic signals may evolve in response to a multitude of selection pressures beyond aversion alone.

Correlated evolution of conspicuous colouration and burrowing in crayfish.

Conspicuous colours have fascinated biologists for centuries, leading to research on the evolution and functional significance of colour traits. In many cases, research suggests that conspicuous colours are adaptive and serve a function in sexual or aposematic signalling. In other cases, a lack of evidence for the adaptive value of conspicuous colours garners interest from biologists, such as when organisms that live underground and are rarely exposed to the surface are nevertheless colourful. Here, we use phylogenetic comparative methods to investigate colour evolution throughout freshwater crayfishes that vary in burrowing ability. Within the taxa we analysed, conspicuous colours have evolved independently over 50 times, and these colours are more common in semi-terrestrial crayfishes that construct extensive burrows. The intuitive but not evolutionarily justified assumption when presented with these results is to assume that these colours are adaptive. But contrary to this intuition, we discuss the hypothesis that colouration in crayfish is neutral. Supporting these ideas, the small population sizes and reduced gene flow within semi-terrestrial burrowing crayfishes may lead to the fixation of colour-phenotype mutations. Overall, our work brings into question the traditional view of animal colouration as a perfectly adapted phenotype.

Pattern Matters in the Aposematic Colouration of Papilio polytes Butterflies.

Many toxic animals display bright colour patterns to warn predators about their toxicity. This sometimes leads other sympatric palatable organisms to evolve mimetic colour patterns to also evade predation. These mimics, however, are often imperfect, and it is unclear how much their colour patterns can vary away from the model before they become ineffective. In this study, we investigated how predation risk of the palatable Common Mormon butterfly (Papilio polytes) is affected by two alterations of its wing pattern that make it progressively more distinct from its model, the Common Rose (Pachliopta aristolochiae). We deployed butterfly paper models in the field, where all models displayed the same colours but had different patterns. In the first modification from the Wildtype pattern, we exchanged the position of the red and white colour patches but kept the overall pattern constant. In the second modification, we created an eyespot-like shape from the pre-existing pattern elements by moving their positions in the wing, altering the overall wing pattern. Both modifications increased attack risk from predators relative to Wildtype patterns, with the eyespot-like modification having the highest predation risk. Our results show that avian predators can distinguish between all three patterns tested, and that pattern is important in aposematic signals. Predators learn to avoid aposematic colours, not in isolation, but as part of specific patterns.

Variation in Ventral Coloration Pattern and Aposematism in Tropical Warty Newts.

Aposematic coloration plays a crucial role in animal defense, and it is shaped by a complex interplay of factors such as physiological limitations and sexual and natural selection. Warty newts within the genus Paramesotriton exhibit significant variation in ventral coloration. In this study, we quantified the percentage of red ventral area to investigate aposematic ventral coloration in Paramesotriton deloustali and P. guangxiensis across eight populations in northern Vietnam. To assess the interaction between predators and the aposematic signals, we conducted experiments employing three types of clay replicas of newts: dorsal, red ventral, and black ventral models. Our findings revealed a significant variation in the red ventral area among different populations. Additionally, a significant correlation was detected between the red ventral area of the newt and the annual temperature range. In clay model experiments, a significant difference in predator attack rates was observed between dorsal and ventral clay models. Interestingly, there was no significant difference in attack rates between red and black ventral types. Our study suggested that the variation in the red ventral area of warty newts is probably influenced by multiple factors, including genetic constraints, sex, ambient environment, and diet. Furthermore, our results supported the effectiveness of displaying aposematic coloration as an antipredator defense mechanism in warty newts. However, variations in body size and the pressure of mammal predation might not play a significant role in determining aposematic coloration.

Color polymorphism and mating trends in a population of the alpine leaf beetle Oreina gloriosa.

The bright colors of Alpine leaf beetles (Coleoptera, Chrysomelidae) are thought to act as aposematic signals against predation. Within the European Alps, at least six species display a basal color of either blue or green, likely configuring a classic case of müllerian mimicry. In this context, intra-population color polymorphism is paradoxical as the existence of numerous color morphs might hamper the establishment of a search image in visual predators. Assortative mating may be one of the main factors contributing to the maintenance of polymorphic populations. Due to the marked iridescence of these leaf beetles, the perceived color may change as the viewing or illumination angle changes. The present study, conducted over three years, involved intensive sampling of a population of Oreina gloriosa from the Italian Alps and applied colorimetry and a decision tree method to identify the color morphs in an objective manner. The tertiary sex ratio of the population was biased in favor of males, suggesting that viviparous females hide to give birth. Seven color morphs were identified, and their frequencies varied significantly over the course of the study. Three different analyses of mating (JMating, QInfomating, and Montecarlo simulations) recognized a general trend for random mating which coexists with some instances of positive and negative assortative mating. This could help explain the pre-eminence of one morph (which would be favored because of positive selection due to positive assortative mating) in parallel with the persistence of six other morphs (maintained due to negative assortative mating).

Pervasive mimicry in flight behavior among aposematic butterflies

Flight was a key innovation in the adaptive radiation of insects. However, it is a complex trait influenced by a large number of interacting biotic and abiotic factors, making it difficult to unravel the evolutionary drivers. We investigate flight patterns in neotropical heliconiine butterflies, well known for mimicry of their aposematic wing color patterns. We quantify the flight patterns (wing beat frequency and wing angles) of 351 individuals representing 29 heliconiine and 9 ithomiine species belonging to ten color pattern mimicry groupings. For wing beat frequency and up wing angles, we show that heliconiine species group by color pattern mimicry affiliation. Convergence of down wing angles to mimicry groupings is less pronounced, indicating that distinct components of flight are under different selection pressures and constraints. The flight characteristics of the Tiger mimicry group are particularly divergent due to convergence with distantly related ithomiine species. Predator-driven selection for mimicry also explained variation in flight among subspecies, indicating that this convergence can occur over relatively short evolutionary timescales. Our results suggest that the flight convergence is driven by aposematic signaling rather than shared habitat between comimics. We demonstrate that behavioral mimicry can occur between lineages that have separated over evolutionary timescales ranging from <0.5 to 70 My.

Music as aposematic signal: predator defense strategies in early human evolution.

The article draws attention to a neglected key element of human evolutionary history-the defense strategies of hominins and early humans against predators. Possible reasons for this neglect are discussed, and the historical development of this field is outlined. Many human morphological and behavioral characteristics-musicality, sense of rhythm, use of dissonances, entrainment, bipedalism, long head hair, long legs, strong body odor, armpit hair, traditions of body painting and cannibalism-are explained as predator avoidance tactics of an aposematic (warning display) defense strategy. The article argues that the origins of human musical faculties should be studied in the wider context of an early, multimodal human defense strategy from predators.

Experience with Aposematic Defense Triggers Attack Bias in a Mantid Predator (Stagmomantis carolina)

Synopsis Studies of predator psychology in aposematism have suggested important effects of signal detection through space and time on outcomes of attack behavior. Both the integration of aposematic signals from prey and experience state of the predator can have important effects on attack decisions. The universality of these effects however, especially as it applies to non-avian predators such as arthropods, remains poorly understood. We examined the effects of multimodal aposematic signaling and prior experience with aposematism on attack latency and attack likelihood of the Carolina mantis (Stagmomantis carolina). Using artificial prey bearing visual and olfactory signals of the convergent lady beetle (Hippodamia convergens), we tested 2 cohorts of mantids (representing juvenile and adult stages) across 4 groups: visual only, odor only, combined signals, and control. We then used approaches in linear modeling to test the hypotheses that (1) prior experience with aposematism alters attack behavior toward aposematic prey and (2) multimodal signals have synergistic effects on attack behavior relative to either unisensory signal presented alone. We found support for the first hypothesis in that mantids employ attack biases against visual and olfactory aposematic signals, but only after prior exposure to aposematism and only as juveniles. While support is lacking for multimodal integration by the mantids, this study is the first to suggest a response of mantids to an aposematic olfactory signal (in addition to visual signal) and may suggest a developmental window for mantid predators to develop biases toward aposematic prey that are shaped by experience.

The function of red and banded patterns in snakes: a review of hypotheses and evidence

Abstract The functions of bright bands in coral and other snakes have long been a puzzle. The most common opinion is that coral snakes display aposematic marks and that other red and black banded snakes in the Americas are mimics of coral snakes. Although supported by some evidence, the notion comes with unresolved difficulties. Here, I review the proposed functions of the colour of coral snakes and similar-coloured snakes, taking a more comprehensive view than usual, from the plausibility of aposematism in coral snakes to the apparent existence of a selective force for red and black banded patterns across the world. Theoretical models of the maintenance of aposematic signals do not seem applicable, hence aposematism has a low a priori plausibility in coral snakes. Evidence of avoidance is weak, field studies rely on unsettled methods and do not reproduce well, and two laboratory studies reporting strong innate fear are questioned. Coral snakes predict the geography and richness of ‘mimics’ in the Americas, but not in line with expectations. Conversely, polymorphism and evidence of local selection and of a worldwide selective force for patterns similar to coral snakes, including complex banded patterns, contradicts aposematism and mimicry and points to an undefined alternative. In summary, aposematism and mimicry fail on too many fronts to be sustained, existing alternatives also fail to be supported sufficiently, and hypotheses need to be formulated to account for the widespread selection for red and black bands and for complex banded patterns in snakes.

Colour polymorphism associated with a gene duplication in male wood tiger moths.

Colour is often used as an aposematic warning signal, with predator learning expected to lead to a single colour pattern within a population. However, there are many puzzling cases where aposematic signals are also polymorphic. The wood tiger moth, Arctia plantaginis, displays bright hindwing colours associated with unpalatability, and males have discrete colour morphs which vary in frequency between localities. In Finland, both white and yellow morphs can be found, and these colour morphs also differ in behavioural and life-history traits. Here, we show that male colour is linked to an extra copy of a yellow family gene that is only present in the white morphs. This white-specific duplication, which we name valkea, is highly upregulated during wing development. CRISPR targeting valkea resulted in editing of both valkea and its paralog, yellow-e, and led to the production of yellow wings. We also characterise the pigments responsible for yellow, white, and black colouration, showing that yellow is partly produced by pheomelanins, while black is dopamine-derived eumelanin. Our results add to a growing number of studies on the genetic architecture of complex and seemingly paradoxical polymorphisms, and the role of gene duplications and structural variation in adaptive evolution.

Diving into dual functionality: Swim bladder muscles in lionfish for buoyancy and sonic capabilities.

Although the primary function of the swim bladder is buoyancy, it is also involved in hearing, and it can be associated with sonic muscles for voluntary sound production. The use of the swim bladder and associated muscles in sound production could be an exaptation since this is not its first function. We however lack models showing that the same muscles can be used in both movement and sound production. In this study, we investigate the functions of the muscles associated with the swim bladder in different Pteroinae (lionfish) species. Our results indicate that Pterois volitans, P. radiata and Dendrochirus zebra are able to produce long low-frequency hums when disturbed. The deliberate movements of the fin spines during sound production suggest that these sounds may serve as aposematic signals. In P. volitans and P. radiata, hums can be punctuated by intermittent louder pulses called knocks. Analysis of sonic features, morphology, electromyography and histology strongly suggest that these sounds are most likely produced by muscles closely associated with the swim bladder. These muscles originate from the neurocranium and insert on the posterior part of the swim bladder. Additionally, cineradiography supports the hypothesis that these same muscles are involved in altering the swim bladder's length and angle, thereby influencing the pitch of the fish body and participating in manoeuvring and locomotion movements. Fast contraction of the muscle should be related to sound production whereas sustained contractions allows modifications in swim bladder shape and body pitch.

Predation Risk Drives Aposematic Signal Conformity.

Contrary to expectations regarding efficient predator education mediated by lack of ambiguity and enhanced prey recognition, aposematic signals often show considerable intraspecific variability. For example, some striped skunks (Mephitis mephitis) are almost entirely white, others have black-and-white stripes of equivalent thicknesses, yet others are mostly black. We tested the ecological correlates of this variation in patterning using 749 museum skins collected across North America. Skunks had longer white-black borders and more bilaterally symmetrical stripes in areas with a greater number of potential predator species, and this effect was more marked for mammalian than avian predators, the latter of which may be less deterred by noxious defenses. Skunks from locations with greater predator diversity were less variable in extent of whiteness on their dorsa and less variable in the length of their white-black borders, suggesting strong selection from predators leads to greater conformity in stripe patterns, even at the same location, but weak selection from predators leads to relaxed selection on pattern conformity. Skunks exhibited greater areas of black pelage in areas of greater humidity conforming to Gloger's rule. Our results indicate that relaxed predation pressure is key to warning signal variation in this iconic species, whereas stronger pressure leads to signal conformity and stronger signals.

Hidden black and yellow thigh color acts as an aposematic signal in the Eastern Gray Treefrog (Hyla versicolor)

AbstractRecognizing form and function of animal defenses is paramount to understanding the ecological and evolutionary forces behind predator and prey dynamics. Color patterns are strongly related to defensive strategies in animals. Some rely on camouflage to avoid detection, while others are brightly colored and conspicuously signal their noxiousness to potential predators. Still others combine cryptic dorsal coloration with colorful patches that are concealed in resting position but are facultatively unveiled by special behavior or simply during activity. Such hidden conspicuous color patches may be an intermediate stage in the evolution from camouflage to aposematism. Many species, especially treefrogs of the family Hylidae, are generally considered to be cryptic, yet show colorful patches on their flanks or thighs and have defensive skin secretions that may have unpalatable properties. We investigated whether the conspicuous black and yellow spotted pattern on the thighs of Eastern Gray Treefrogs (Hyla versicolor) serve as an aposematic signal. We conducted a palatability study to test whether Gray Treefrog skin secretions are unpalatable, and a clay model field study to test whether the conspicuous black and yellow thigh pattern is an aposematic warning coloration that reduces predation. Frog secretions were discriminated against during palatability assays, and clay models painted with a spotted black and yellow pattern suffered lower predation rates. Our findings support the hypothesis that hidden color patches act as aposematic signals in Gray Treefrogs and suggest that more species benefit from aposematic coloration than currently appreciated.

Signal detectability and boldness are not the same: the function of defensive coloration in nudibranchs is distance-dependent.

Aposematic signals visually advertise underlying anti-predatory defences in many species. They should be detectable (e.g. contrasting against the background) and bold (e.g. using internal pattern contrast) to enhance predator recognition, learning and memorization. However, the signalling function of aposematic colour patterns may be distance-dependent: signals may be undetectable from a distance to reduce increased attacks from naïve predators but bold when viewed up close. Using quantitative colour pattern analysis, we quantified the chromatic and achromatic detectability and boldness of colour patterns in 13 nudibranch species with variable strength of chemical defences in terms of unpalatability and toxicity, approximating the visual perception of a triggerfish (Rhinecanthus aculeatus) across a predation sequence (detection to subjugation). When viewed from an ecologically relevant distance of 30 cm, there were no differences in detectability and boldness between well-defended and undefended species. However, when viewed at closer distances (less than 30 cm), well-defended species were more detectable and bolder than undefended species. As distance increased, detectability decreased more significantly than boldness for defended species. For undefended species, boldness and detectability remained comparatively consistent, regardless of viewing distance. We provide evidence for distance-dependent signalling in aposematic nudibranchs and highlight the importance of distinguishing signal detectability from boldness in studies of aposematism.

The protective value of the colour and shape of the mountain katydid's antipredator defence.

Deimatic behaviour is performed by prey when attacked by predators as part of an antipredator strategy. The behaviour is part of a sequence that consists of several defences, for example they can be preceded by camouflage and followed by a hidden putatively aposematic signal that is only revealed when the deimatic behaviour is performed. When displaying their hidden signal, mountain katydids (Acripeza reticulata) hold their wings vertically, exposing striking red and black stripes with blue spots and oozing an alkaloid-rich chemical defence derived from its Senecio diet. Understanding differences and interactions between deimatism and aposematism has proven problematic, so in this study we isolated the putative aposematic signal of the mountain katydid's antipredator strategy to measure its survival value in the absence of their deimatic behaviour. We manipulated two aspects of the mountain katydid's signal, colour pattern and whole body shape during display. We deployed five kinds of clay models, one negative control and four katydid-like treatments, in 15 grids across part of the mountain katydid's distribution to test the hypothesis that their hidden signal is aposematic. If this hypothesis holds true, we expected that the models, which most closely resembled real katydids would be attacked the least. Instead, we found that models that most closely resembled real katydids were the most likely to be attacked. We suggest several ideas to explain these results, including that the deimatic phase of the katydid's display, the change from a camouflaged state to exposing its hidden signal, may have important protective value.

Investigating signal modalities of aposematism in a poison frog.

Aposematic species combine a conspicuous signal with a secondary defence, the majority of which are studied in the context of a visual signal. While multimodality of the aposematic signal appears to be common in invertebrate species, we know very little about the presence or absence of multimodality in vertebrates. Here, we examine the possibility of multimodality of aposematism in the green-and-black poison frog, Dendrobates auratus. Using a non-visual predator (the cat-eyed snake, Leptodeira annulata) and extractions of chemicals in frog skins, we test whether there is sufficient non-visual information for predators to avoid this aposematic species without using visual cues. We found that experienced predators avoid chemicals in this poison frog's skin by olfactory cues alone in trials with live frogs and extracts from captive poison frogs, whereas extracts from wild poison frogs did not lead to avoidance behaviours in predators. Further, in our limited sampling, naïve predators demonstrate no avoidance. This not only indicates that predators can make informed decisions from the frog's odour, but also indicates that avoidance based on olfactory cue is a learned response.

Size-dependent colouration balances conspicuous aposematism and camouflage.

Colour is an important component of many different defensive strategies, but signal efficacy and detectability will also depend on the size of the coloured structures, and how pattern size interacts with the background. Consequently, size-dependent changes in colouration are common among many different species as juveniles and adults frequently use colour for different purposes in different environmental contexts. A widespread strategy in many species is switching from crypsis to conspicuous aposematic signalling as increasing body size can reduce the efficacy of camouflage, while other antipredator defences may strengthen. Curiously, despite being chemically defended, the gold-striped frog (Lithodytes lineatus, Leptodactylidae) appears to do the opposite, with bright yellow stripes found in smaller individuals, whereas larger frogs exhibit dull brown stripes. Here, we investigated whether size-dependent differences in colour support distinct defensive strategies. We first used visual modelling of potential predators to assess how colour contrast varied among frogs of different sizes. We found that contrast peaked in mid-sized individuals while the largest individuals had the least contrasting patterns. We then used two detection experiments with human participants to evaluate how colour and body size affected overall detectability. These experiments revealed that larger body sizes were easier to detect, but that the colours of smaller frogs were more detectable than those of larger frogs. Taken together our data support the hypothesis that the primary defensive strategy changes from conspicuous aposematism to camouflage with increasing size, implying size-dependent differences in the efficacy of defensive colouration. We discuss our data in relation to theories of size-dependent aposematism and evaluate the evidence for and against a possible size-dependent mimicry complex with sympatric poison frogs (Dendrobatidae).

A histological analysis of coloration in the Peruvian mimic poison frog (Ranitomeya imitator).

Aposematism continues to be a phenomenon of central interest in evolutionary biology. The life history of the mimic poison frog, Ranitomeya imitator, relies heavily on aposematism. In order for aposematic signals to be effective, predators must be able to learn to avoid the associated phenotype. However, in R. imitator, aposematism is associated with four different color phenotypes that mimic a complex of congeneric species occurring across the mimic frog's geographic range. Investigations of the underlying mechanics of color production in these frogs can provide insights into how and why these different morphs evolved. We used histological samples to examine divergence in the color production mechanisms used by R. imitator to produce effective aposematic signals across its geographic range. We measured the coverage of melanophores and xanthophores (the area covered by chromatophores divided by total area of the skin section) in each color morph. We find that morphs that produce orange skin exhibit a higher coverage of xanthophores and lower coverage of melanophores than those that produce yellow skin. In turn, morphs that produce yellow skin exhibit a higher coverage of xanthophores and lower coverage of melanophores than those that produce green skin. Generally, across the morphs, a high ratio of xanthophores to melanophores is associated with colors of brighter spectral reflectance. Together, our results contribute to the understanding of color production in amphibians and document divergence in the histology of a species that is subject to divergent selection associated with aposematism.

Warning Coloration, Body Size, and the Evolution of Gregarious Behavior in Butterfly Larvae.

AbstractMany species gain antipredator benefits by combining gregarious behavior with warning coloration, yet there is debate over which trait evolves first and which is the secondary adaptive enhancement. Body size can also influence how predators receive aposematic signals and potentially constrain the evolution of gregarious behavior. To our knowledge, the causative links between the evolution of gregariousness, aposematism, and larger body sizes have not been fully resolved. Here, using the most recently resolved butterfly phylogeny and an extensive new dataset of larval traits, we reveal the evolutionary interactions between important traits linked to larval gregariousness. We show that larval gregariousness has arisen many times across butterflies, and aposematism is a likely prerequisite for gregariousness to evolve. We also find that body size may be an important factor for determining the coloration of solitary, but not gregarious, larvae. Additionally, by exposing artificial larvae to wild avian predation, we show that undefended, cryptic larvae are heavily predated when aggregated but benefit from solitariness, whereas the reverse is true for aposematic prey. Our data reinforce the importance of aposematism for gregarious larval survival while identifying new questions about the roles of body size and toxicity in the evolution of grouping behavior.

Chemical aposematism: the potential for non‐host odours in avian defence

Many birds display plumage coloration and patterns that act as visual aposematic and mimetic signals for predators. Avian aposematism can also be communicated via chemical cues, where so‐called non‐host odours (NHO) emitted from the plumage, the uropygial (preen) gland or other chemical sources denote the status of birds as dangerous or unprofitable hosts for ectoparasitic and haematophagous arthropods. Avian NHO are aposematic signals that in natural concentrations repel nuisance arthropods or inhibit their attraction to hosts, as opposed to being generally unpalatable or toxic to predators. Birds that emit NHO preempt encounters with nuisance arthropods and the pathogens they transmit. Nuisance arthropods that respond to NHO avoid birds that exhibit disabling behavioural, anatomical, physiological and/or chemical defences. As with distinctive plumage patterns that evolved as visual warnings to predators, birds are selected to advertise their non‐host status to nuisance arthropods via distinctive semiochemicals. Short‐chain (C6–C10) aldehydes emitted from the plumage of some birds may act as NHO against a variety of nuisance arthropods. In some birds, the size of the uropygial gland (and presumably its secretory output) is negatively correlated with the degree of ectoparasite infestation or the incidence of malarial infection, thus implicating uropygial secretions in defence against dipteran vectors of haemosporidian pathogens. A field experiment demonstrates that volatiles emanating from the uropygial gland of the Eurasian Hoopoe Upupa epops deter some biting flies. Birds' risky habit of plucking hair from live mammals and incorporating the stolen hair tufts into their nests is hypothesized to serve as a mechanism of appropriating NHO from mammalian skin secretions for nest defence against arthropods. Feathers plucked from heterospecifics and shed snake skins that are incorporated into nests also may emit NHO. Behavioural assays measuring the repellence or attraction‐inhibition of arthropods are needed to elucidate avian NHO. Experimental efforts to elucidate the underlying defences that support avian NHO entail challenges that include the enactment of defences that are variously effective against different arthropods, and the emission of chemical signals that are variously ‘understood’, i.e. avoided, by different arthropods.