Aposematic Prey Research Articles

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.

Predator selection on multicomponent warning signals in an aposematic moth.

Aposematic prey advertise their unprofitability with conspicuous warning signals that are often composed of multiple color patterns. Many species show intraspecific variation in these patterns even though selection is expected to favor invariable warning signals that enhance predator learning. However, if predators acquire avoidance to specific signal components, this might relax selection on other aposematic traits and explain variability. Here, we investigated this idea in the aposematic moth Amata nigriceps that has conspicuous black and orange coloration. The size of the orange spots in the wings is highly variable between individuals, whereas the number and width of orange abdominal stripes remains consistent. We produced artificial moths that varied in the proportion of orange in the wings or the presence of abdominal stripes. We presented these to a natural avian predator, the noisy miner (Manorina melanocephala), and recorded how different warning signal components influenced their attack decisions. When moth models had orange stripes on the abdomen, birds did not discriminate between different wing signals. However, when the stripes on the abdomen were removed, birds chose the model with smaller wing spots. In addition, we found that birds were more likely to attack moths with a smaller number of abdominal stripes. Together, our results suggest that bird predators primarily pay attention to the abdominal stripes of A. nigriceps, and this could relax selection on wing coloration. Our study highlights the importance of considering individual warning signal components if we are to understand how predation shapes selection on prey warning coloration.

In paired preference tests, domestic chicks innately choose the colour green over red, and the shape of a frog over a sphere when both stimuli are green

Many animals express unlearned colour preferences that depend on the context in which signals are encountered. These colour biases may have evolved in response to the signalling system to which they relate. For example, many aposematic animals advertise their unprofitability with red warning signals. Predators’ innate biases against these warning colours have been suggested as one of the potential explanations for the initial evolution of aposematism. It is unclear, however, whether unlearned colour preferences reported in a number of species is truly an innate behaviour or whether it is based on prior experience. We tested the spontaneous colour and shape preferences of dark-hatched, unfed, and visually naive domestic chicks (Gallus gallus). In four experiments, we presented chicks with a choice between either red (a colour typically associated with warning patterns) or green (a colour associated with palatable cryptic prey), volume-matched spheres (representing a generalised fruit shape) or frogs (representing an aposematic animal’s shape). Chicks innately preferred green stimuli and avoided red. Chicks also preferred the shape of a frog over a sphere when both stimuli were green. However, no preference for frogs over spheres was present when stimuli were red. Male chicks that experienced a bitter taste of quinine immediately before the preference test showed a higher preference for green frog-shaped stimuli. Our results suggest that newly hatched chicks innately integrate colour and shape cues during decision making, and that this can be augmented by other sensory experiences. Innate and experience-based behaviour could confer a fitness advantage to novel aposematic prey, and favour the initial evolution of conspicuous colouration.

Pattern variation is linked to anti-predator coloration in butterfly larvae.

Prey animals typically try to avoid being detected and/or advertise to would-be predators that they should be avoided. Both anti-predator strategies primarily rely on colour to succeed, but the specific patterning used is also important. While the role of patterning in camouflage is relatively clear, the design features of aposematic patterns are less well understood. Here, we use a comparative approach to investigate how pattern use varies across a phylogeny of 268 species of cryptic and aposematic butterfly larvae, which also vary in social behaviour. We find that longitudinal stripes are used more frequently by cryptic larvae, and that patterns putatively linked to crypsis are more likely to be used by solitary larvae. By contrast, aposematic larvae are more likely to use horizontal bands and spots, but we find no differences in the use of individual pattern elements between solitary and gregarious aposematic species. However, solitary aposematic larvae are more likely to display multiple pattern elements, whereas those with no pattern are more likely to be gregarious. Our study advances our understanding of how pattern variation, coloration and social behaviour covary across lepidopteran larvae, and highlights new questions about how patterning affects larval detectability and predator responses to aposematic prey.

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.

Social information use about novel aposematic prey depends on the intensity of the observed cue

Abstract Animals gather social information by observing the behavior of others, but how the intensity of observed cues influences decision-making is rarely investigated. This is crucial for understanding how social information influences ecological and evolutionary dynamics. For example, observing a predator’s distaste of unpalatable prey can reduce predation by naïve birds, and help explain the evolution and maintenance of aposematic warning signals. However, previous studies have only used demonstrators that responded vigorously, showing intense beak-wiping after tasting prey. Therefore, here we conducted an experiment with blue tits (Cyanistes caeruleus) informed by variation in predator responses. First, we found that the response to unpalatable food varies greatly, with only few individuals performing intensive beak-wiping. We then tested how the intensity of beak-wiping influences observers’ foraging choices using video-playback of a conspecific tasting a novel conspicuous prey item. Observers were provided social information from 1) no distaste response, 2) a weak distaste response, or 3) a strong distaste response, and were then allowed to forage on evolutionarily novel (artificial) prey. Consistent with previous studies, we found that birds consumed fewer aposematic prey after seeing a strong distaste response, however, a weak response did not influence foraging choices. Our results suggest that while beak-wiping is a salient cue, its information content may vary with cue intensity. Furthermore, the number of potential demonstrators in the predator population might be lower than previously thought, although determining how this influences social transmission of avoidance in the wild will require uncovering the effects of intermediate cue salience.

Avian predators taste reject mimetic prey in relation to their signal reliability

Aposematic organisms defend themselves through various means to increase their unprofitability to predators which they advertise with conspicuous warning signals. Predators learn to avoid aposematic prey through associative learning that leads to lower predation. However, when these visual signals become unreliable (e.g., through automimicry or Batesian mimicry), predators may switch from using visual signals to taste sampling prey to choose among them. In this experiment, we tested this possibility in a field experiment where we released a total of 4800 mealworm prey in two clusters consisting of either: (i) undefended prey (injected with water) and (ii) model-mimics (injected with either quinine sulphate [models] or water [mimics]). Prey were deployed at 12 sites, with the mimic frequency of the model-mimics ranging between 0 and 1 (at 0.2 intervals). We found that taste rejection peaked at moderate mimic frequencies (0.4 and 0.6), supporting the idea that taste sampling and rejection of prey is related to signal reliability and predator uncertainty. This is the first time that taste-rejection has been shown to be related to the reliability of prey signals in a mimetic prey system.

Birds learn to avoid aposematic prey by using the appearance of host plants

The conspicuous warning signal of aposematic animals is learned by their predators, and the resulting avoidance benefits both parties.1-4 Given evidence that birds can distinguish the profitability of prey from the environmental context in which they appear,5 aposematic insects' host plants might also provide an important cue to foraging predators.6 The aposematic cinnabar moth (Tyria jacobaeae) larva is a specialist on its ragwort (Senecio spp.) host plant,7 presenting a consistent environment with which it could be reliably associated. Additionally, ragwort's defensive toxins prevent non-specialist, profitable insects from feeding on it.8 Thus, avian predators may recognize cues from ragwort, most likely its conspicuous yellow flowers,9,10 and use this information to avoid cinnabars. To test this hypothesis, we exposed artificial cinnabar and non-signaling "caterpillar" targets to wild avian predation by presenting them on ragwort and non-toxic host plants. We also manipulated the presence or absence of ragwort flowers on hosts. In doing so, we show that both targets are better protected on the cinnabar's natural ragwort host and that birds use ragwort's distinctive yellow flowers as the cue to avoidance. Additionally, we found that naive predators do not make prey host foraging distinctions, indicating that this avoidance behavior is learned through experience. Our findings are among the first to suggest that a host plant's features act as an extended phenotype that signals the toxicity of the prey that live on it. This prey-host relationship may facilitate the initial evolution of toxicity in non-signaling prey, but also inhibit the evolution of aposematic signals themselves. VIDEO ABSTRACT.

Lack of neophobic responses to color in a jumping spider that uses color cues when foraging (Habronattus pyrrithrix).

Chemically defended prey often advertise their toxins with bright and conspicuous colors. To understand why such colors are effective at reducing predation, we need to understand the psychology of key predators. In bird predators, there is evidence that individuals avoid novelty—including prey of novel colors (with which they have had no prior experience). Moreover, the effect of novelty is sometimes strongest for colors that are typically associated with aposematic prey (e.g., red, orange, yellow). Given these findings in the bird literature, color neophobia has been argued to be a driving force in the evolution of aposematism. However, no studies have yet asked whether invertebrate predators respond similarly to novel colors. Here, we tested whether naive lab-raised jumping spiders (Habronattus pyrrithrix) exhibit similar patterns of color neophobia to birds. Using color-manipulated living prey, we first color-exposed spiders to prey of two out of three colors (blue, green, or red), with the third color remaining novel. After this color exposure phase, we gave the spiders tests where they could choose between all three colors (two familiar, one novel). We found that H. pyrrithrix attacked novel and familiar-colored prey at equal rates with no evidence that the degree of neophobia varied by color. Moreover, we found no evidence that either prey novelty nor color (nor their interaction) had an effect on how quickly prey was attacked. We discuss these findings in the context of what is known about color neophobia in other animals and how this contributes to our understanding of aposematic signals.

Numbers, neighbors, and hungry predators: What makes chemically defended aposematic prey susceptible to predation?

Many chemically defended aposematic species are characterized by relatively low toxin levels, which enables predators to include them in their diets under certain circumstances. Knowledge of the conditions governing the survival of such prey animals—especially in the context of the co‐occurrence of similar but undefended prey, which may result in mimicry‐like interactions—is crucial for understanding the initial evolution of aposematism. In a one‐month outdoor experiment using fish (the common carp Cyprinus carpio) as predators, we examined the survival of moderately defended aposematic tadpole prey (the European common toad Bufo bufo) with varying absolute densities in single‐species prey systems or varying relative densities in two‐species prey systems containing morphologically similar but undefended prey (the European common frog Rana temporaria). The density effects were investigated in conjunction with the hunger levels of the predator, which were manipulated by means of the addition of alternative (nontadpole) food. The survival of the B. bufo tadpoles was promoted by increasing their absolute density in the single‐species prey systems, increasing their relative density in the two‐species prey systems, and providing ample alternative food for the predator. Hungry predators eliminated all R. temporaria individuals regardless of their proportion in the prey community; in treatments with ample alternative food, high relative B. bufo density supported R. temporaria survival. The results demonstrated that moderately defended prey did benefit from high population densities (both absolute and relative), even under long‐term predation pressure. However, the physiological state of the predator was a crucial factor in the survival of moderately defended prey. While the availability of alternative prey in general should promote the spread and maintenance of aposematism, the results indicated that the resemblance between the co‐occurring defended and undefended prey may impose mortality costs on the defended model species, even in the absence of actual mimicry.

Intraspecific variation in responses to aposematic prey in a jumping spider (Phidippus regius)

AbstractAposematic signals often allow chemically defended prey to avoid attack from generalist predators, including jumping spiders. However, not all individual predators in a population behave in the same way. Here, in laboratory trials, we document that most individual Phidippus regius jumping spiders attack and reject chemically defended milkweed bugs (Oncopeltus fasciatus), immediately releasing them unharmed. However, a small number of individuals within the population kill and completely consume these presumably toxic prey items. This phenomenon was infrequent with only 14% of our sample (17/122) consuming the milkweed bugs over the course of the study. Individuals that killed and consumed bugs often did so repeatedly; specifically, individuals that consumed a bug in their first test were more likely to kill a bug in their second test and also tended to consume them again. We explored what might drive some (but not all) individuals to consume these bugs and found that neither sex, sexual maturity, body size, laboratory housing type, nor being wild‐caught or being laboratory‐reared, predicted milkweed bug consumption. Consuming bugs had no negative effects on spider mass or body condition; contrary to expectations, individuals that consumed milkweed bugs actually gained more body mass and increased in body condition. We discuss potential behavioural and physiological variation between individuals that may drive these rare behaviours and the implications for the evolution of prey defences.

The truth is in the detail: predators attack aposematic prey with less aggression than other prey types

AbstractAposematic organisms are often unprofitable to predators (e.g. because of defensive chemicals) which they advertise with a conspicuous signal (e.g. bright and conspicuous colour signals). Aposematism is thought to reduce predation of prey because the colour signal increases the ability of predators to learn, recognize and remember the prey’s defensive properties. The efficacy of aposematism has been extensively documented in laboratory studies, although its benefits seem to be harder to demonstrate in the field. In this study, we compared the levels of partial and overall predation among four prey types (undefended and cryptic, undefended and warning coloured, defended and cryptic, and aposematic prey). Overall, predation of warning coloured and defended (aposematic) prey was lower than the predation for cryptic and undefended prey; however, it was the same as predation of cryptic and defended prey. Moreover, aposematic prey had higher levels of partial predation (where prey was not wholly consumed by the predator) and lower attack intensities. This suggests that prey were being taste sampled, but also might be better able to survive attacks. Therefore, the benefits of aposematism may lie not only in reducing outright predation, but also in altering a predator’s post-attack behaviour, thus leading to greater escape opportunities and post-attack survival of prey. These results reinforce the importance of examining predation in more detail rather than simply examining attack rates.

Pattern contrast influences wariness in na\xefve predators towards aposematic patterns

An apparent and common feature of aposematic patterns is that they contain a high level of achromatic (luminance) contrast, for example, many warning signals combine black spots and stripes with a lighter colour such as yellow. However, the potential importance of achromatic contrast, as distinct from colour contrast, in reducing predation has been largely overlooked. Here, using domestic chicks as a model predator, we manipulated the degree of achromatic contrast in warning patterns to test if high luminance contrast in aposematic signals is important for deterring naïve predators. We found that the chicks were less likely to approach and eat prey with high contrast compared to low contrast patterns. These findings suggest that aposematic prey patterns with a high luminance contrast can benefit from increased survival through eliciting unlearned biases in naïve avian predators. Our work also highlights the importance of considering luminance contrast in future work investigating why aposematic patterns take the particular forms that they do.

The signal detection problem of aposematic prey revisited: integrating prior social and personal experience.

Ever since Alfred R. Wallace suggested brightly coloured, toxic insects warn predators about their unprofitability, evolutionary biologists have searched for an explanation of how these aposematic prey evolve and are maintained in natural populations. Understanding how predators learn about this widespread prey defence is fundamental to addressing the problem, yet individuals differ in their foraging decisions and the predominant application of associative learning theory largely ignores predators' foraging context. Here we revisit the suggestion made 15 years ago that signal detection theory provides a useful framework to model predator learning by emphasizing the integration of prior information into predation decisions. Using multiple experiments where we modified the availability of social information using video playback, we show that personal information (sampling aposematic prey) improves how predators (great tits, Parus major) discriminate between novel aposematic and cryptic prey. However, this relationship was not linear and beyond a certain point personal encounters with aposematic prey were no longer informative for prey discrimination. Social information about prey unpalatability reduced attacks on aposematic prey across learning trials, but it did not influence the relationship between personal sampling and discrimination. Our results suggest therefore that acquiring social information does not influence the value of personal information, but more experiments are needed to manipulate pay-offs and disentangle whether information sources affect response thresholds or change discrimination. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Methods for independently manipulating palatability and color in small insect prey.

Understanding how the psychology of predators shapes the defenses of colorful aposematic prey has been a rich area of inquiry, with emphasis on hypothesis-driven experiments that independently manipulate color and palatability in prey to examine predator responses. Most of these studies focus on avian predators, despite calls to consider more taxonomically diverse predators. This taxonomic bias leaves gaps in our knowledge about the generalizability of current theory. Here we have adapted tools that have been successfully used with bird predators and scaled them down and tested them with smaller predators (Habronattus jumping spiders) and small insect prey (termites, milkweed bug nymphs, pinhead crickets, fruit flies). Specifically, we test (1) the application of denatonium benzoate (DB) to the surface of live termites, crickets, and fruit flies, and (2) the effectiveness of manipulating the palatability of milkweed bug nymphs through diet. We also test the effectiveness of combining these palatability manipulations with various color manipulations. Across several experiments, we confirm that our palatability manipulations are not detectable to the spiders before they attack (i.e., they do not produce aversive odors that spiders avoid), and show that unpalatable prey are indeed quickly rejected and spiders do not habituate to the taste with experience. We also investigate limitations of these techniques by assessing possible unintended effects on prey behavior and the risk of contact contamination when using DB-treated prey in experiments. While similar tools have been used to manipulate color and palatability with avian predators and relatively large insect prey, we show how these techniques can be effectively adapted for use with small invertebrate predators and prey.

Social learning within and across predator species reduces attacks on novel aposematic prey.

To make adaptive foraging decisions, predators need to gather information about the profitability of prey. As well as learning from prey encounters, recent studies show that predators can learn about prey defences by observing the negative foraging experiences of conspecifics. However, predator communities are complex. While observing heterospecifics may increase learning opportunities, we know little about how social information use varies across predator species.Social transmission of avoidance among predators also has potential consequences for defended prey. Conspicuous aposematic prey are assumed to be an easy target for naïve predators, but this cost may be reduced if multiple predators learn by observing single predation events. Heterospecific information use by predators might further benefit aposematic prey, but this remains untested.Here we test conspecific and heterospecific information use across a predator community with wild‐caught blue tits (Cyanistes caeruleus) and great tits (Parus major). We used video playback to manipulate social information about novel aposematic prey and then compared birds’ foraging choices in ‘a small‐scale novel world’ that contained novel palatable and aposematic prey items.We expected that blue tits would be less likely to use social information compared to great tits. However, we found that both blue tits and great tits consumed fewer aposematic prey after observing a negative foraging experience of a demonstrator. In fact, this effect was stronger in blue tits compared to great tits. Interestingly, blue tits also learned more efficiently from watching conspecifics, whereas great tits learned similarly regardless of the demonstrator species.Together, our results indicate that social transmission about novel aposematic prey occurs in multiple predator species and across species boundaries. This supports the idea that social interactions among predators can reduce attacks on aposematic prey and therefore influence selection for prey defences.

Attacks by predators on artificial cryptic and aposematic insect larvae

AbstractColour and colour patterns seem to be especially important visual warning signals for predators, which might have innate or learned ability to avoid aposematic prey. To test the importance of larval colour pattern of the aposematic ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), an invasive alien species in Europe, we presented the plasticine models of aposematic larvae to wild and naïve birds. We studied the attacks on aposematic larvae of various patterns and colours in nature and in an outdoor aviary. The larvae were cryptic (green), aposematic (resembling those of the H. axyridis larvae), and semi‐aposematic (i.e., black but missing the typical orange patches of H. axyridis larvae). We detected attacks on 71 larvae out of 450 (i.e., 2.6% daily predation). Twenty‐nine attacks were made by birds, 37 by arthropods, and five by gastropods. Wild birds attacked green and black larvae significantly more often than aposematic larvae. Colour did not have an effect on attacks by arthropods. The experiment with naïve birds was conducted in an outdoor aviary, where naïve great tits, Parus major L., were offered the same artificial larvae as in the first experiment. In total, 57 of 90 exposed larvae were attacked by birds (i.e., 28% daily predation), and green larvae were attacked significantly more than the aposematic larvae (but not more than black larvae). Our results imply that aposematic larvae of H. axyridis are more than 12× less likely to be predated by birds than green larvae in nature. The aposematic pattern represented a more effective signal than the semi‐aposematic signal. The ability to reject aposematic prey seemed to be innate in our birds.

Transparency improves concealment in cryptically coloured moths.

Predation is a ubiquitous and strong selective pressure on living organisms. Transparency is a predation defence widespread in water but rare on land. Some Lepidoptera display transparent patches combined with already cryptic opaque patches. A recent study showed that transparency reduced detectability of aposematic prey with conspicuous patches. However, whether transparency has any effect at reducing detectability of already cryptic prey is still unknown. We conducted field predation experiments with free avian predators where we monitored and compared survival of a fully opaque grey artificial form (cryptic), a form including transparent windows and a wingless artificial butterfly body. Survival of the transparent forms was similar to that of wingless bodies and higher than that of fully opaque forms, suggesting a reduction of detectability conferred by transparency. This is the first evidence that transparency decreases detectability in cryptic terrestrial prey. Future studies should explore the organization of transparent and opaque patches in animals and their interplay on survival, as well as the costs and other potential benefits associated with transparency on land.

Weak warning signals can persist in the absence of gene flow

Aposematic organisms couple conspicuous warning signals with a secondary defense to deter predators from attacking. Novel signals of aposematic prey are expected to be selected against due to positive frequency-dependent selection. How, then, can novel phenotypes persist after they arise, and why do so many aposematic species exhibit intrapopulation signal variability? Using a polytypic poison frog (Dendrobates tinctorius), we explored the forces of selection on variable aposematic signals using 2 phenotypically distinct (white, yellow) populations. Contrary to expectations, local phenotype was not always better protected compared to novel phenotypes in either population; in the white population, the novel phenotype evoked greater avoidance in natural predators. Despite having a lower quantity of alkaloids, the skin extracts from yellow frogs provoked higher aversive reactions by birds than white frogs in the laboratory, although both populations differed from controls. Similarly, predators learned to avoid the yellow signal faster than the white signal, and generalized their learned avoidance of yellow but not white. We propose that signals that are easily learned and broadly generalized can protect rare, novel signals, and weak warning signals (i.e., signals with poor efficacy and/or poor defense) can persist when gene flow among populations, as in this case, is limited. This provides a mechanism for the persistence of intrapopulation aposematic variation, a likely precursor to polytypism and driver of speciation.

Evolution of aposematism and mimicry in butterflies: Causes, consequences and paradoxes

Evolution of aposematism and mimicry in butterflies: Causes, consequences and paradoxes