Predators' toxin burdens influence their strategic decisions to eat toxic prey

Toxic prey advertise their unprofitability to predators via conspicuous aposematic coloration [1]. It is widely accepted that avoidance learning by naive predators is fundamental in generating selection for aposematism [2, 3] and mimicry [4, 5] (where species share the same aposematic coloration), and consequently this cognitive process underpins current evolutionary theory [5, 6]. However, this is an oversimplistic view of predator cognition and decision making. We show that predators that have learned to avoid chemically defended prey continue to attack defended individuals at levels determined by their current toxin burden. European starlings learned to discriminate between sequentially presented defended and undefended mealworms with different color signals. Once birds had learned to avoid the defended prey at a stable asymptotic level, we experimentally increased their toxin burdens, which reduced the number of defended prey that they ingested in the subsequent trial. This was due to the birds making strategic decisions to ingest defended prey on the basis of their visual signals. Birds are clearly able to learn about the nutritional benefits and defensive costs of eating defended prey, and they regulate their intake according to their current physiological state. This raises new perspectives on the evolution of aposematism, mimicry, and defense chemistry.     

Mimicry between unequally defended prey can be parasitic: evidence for quasi-Batesian mimicry

The nature of signal mimicry between defended prey (known as Müllerian mimicry) is controversial. Some authors assert that it is always mutualistic and beneficial, whilst others speculate that less well defended prey may be parasitic and degrade the protection of their better defended co-mimics (quasi-Batesian mimicry). Using great tits (Parus major) as predators of artificial prey, we show that mimicry between unequally defended co-mimics is not mutualistic, and can be parasitic and quasi-Batesian. We presented a fixed abundance of a highly defended model and a moderately defended dimorphic (mimic and distinct non-mimetic) species, and varied the relative frequency of the two forms of the moderately defended prey. As the mimic form increased in abundance, per capita predation on the model-mimic pair increased. Furthermore, when mimics were rare they gained protection from predation but imposed no co-evolutionary pressure on models. We found that the feeding decisions of the birds were affected by their individual toxic burdens, consistent with the idea that predators make foraging decisions which trade-off toxicity and nutrition. This result suggests that many prey species that are currently assumed to be in a simple mutualistic mimetic relationship with their co-mimic species may actually be engaged in an antagonistic co-evolutionary process.     

Investigating Müllerian mimicry: predator learning and variation in prey defences

Inexperienced predators are assumed to select for similarity of warning signals in aposematic species (Müllerian mimicry) when learning to avoid them. Recent theoretical work predicts that if co-mimic species have unequal defences, predators attack them according to their average unpalatability and mimicry may not be beneficial for the better defended co-mimic. In this study, we tested in a laboratory environment whether a uniform warning signal is superior to a variable one in promoting predator learning, and simultaneously whether co-mimics are preyed upon according to their average unpalatability. There was an interaction of signal variation and unpalatability but inexperienced birds did not select for signal similarity in artificial prey; when the prey was moderately defended a variable signal was even learnt faster than a uniform one. Due to slow avoidance learning, moderately defended prey had higher mortality than highly defended prey (although this was not straightforward), but mixing high and moderate unpalatability did not increase predation compared with high unpalatability. This does not support the view that predators are sensitive to varying unpalatability. The results suggest that inexperienced predators may neither strongly select for accurate Müllerian mimicry nor affect the benefits of mimicry when the co-mimics are unequally defended.     

Aversive reactions of two invertebrate predators to European red–black insects

Prey species gain protection by imitating signals of unpalatable models in defensive mimicry. Mimics have been traditionally classified as Batesian (palatable mimic resembling an unpalatable model) or Müllerian (unpalatable mimic resembling a similarly unpalatable model). However, recent studies suggest that rather than discrete categories, the phenomenon of mimicry can be better understood as a continuum. The level of unpalatability of defended prey is a key factor in determining the type of mimetic relationship. Herein, we used insects (ladybugs and true bugs) from a putative European “red–black” mimetic complex as experimental models of defended species and crickets as a control prey. We offered the prey to two species of sympatric invertebrate predators (praying mantis and spider) and video recorded the interactions. We tested three alternative hypotheses, namely (i) the three red–black species tested are similarly defended against both predators; (ii) some red–black species are better defended than others against both predator species, and (iii) the effectiveness of the red–black species defenses is predator dependent. Both predators attacked all prey types with a similar frequency. But while all three red–black species similarly elicited aversive behaviors in spiders, the mantises' aversive reactions varied depending on the prey species. Our results provide support to the third hypothesis, suggesting that the same prey species can fall into different parts of the spectrum of palatability–unpalatability depending on the type of predator.     

How weird can mimicry get?

Classical mimicry theory distinguishes clearly between the mutualistic resemblance between two or more defended species (muellerian mimicry), and the parasitic resemblance of a palatable species to a defended species (batesian mimicry). Modelling the behaviour of predators, without initially taking ecological complications into account, is a good strategy for exploring whether this division is valid. Two such behavioural models are described: conditioning theory, which simulates changes in motivational attack levels according to the norms of current learning theory; and saturation theory, which considers how a predator may become saturated with a particular toxic compound, and then cease feeding on the prey species that delivers it. This effect is to be clearly distinguished from simple satiation. Most formulations of the conditioning model allow the direction of reinforcement produced by a particular prey to change according the predator's current state of motivation: this leads to the existence of quasi-batesian mimicry, a parasitic mimicry between two species that could both be described as defended. At high densities, two prey species that share a chemical defense will be ‘muellerian mutualists’, mutually protecting each other against predators that have been saturated with the defensive compound. This mutualism may be accompanied by true muellerian mimicry of the colour patterns, or the patterns may be completely different. This can therefore be regarded as a form of mimicry in a non-visual communication channel. Even an apparently palatable prey species may be effectively unavailable to predators if its density is such as to deliver a particular nutrient in excess of the predator's need for a balanced diet. Such a nutrient in effect becomes a toxin, and such an abundant prey species would be partly defended and potentially able to act as the model in a mimicry system. Thus there might be protective mimicry between ‘palatable’ species, and a ‘palatable’ species might even function as the model for a ‘defended’ mimic. These unorthodox kinds of mimicry probably exist transiently during fluctuations of prey populations. It is less likely that these conditions persist for long enough to induce the evolution of mimicry, and the relationships perhaps usually occur when mimicry already exists for other reasons. Mimicry rings may be mutually stabilised by a combination of toxic mutualism and the exchange of species between the rings. Colour polymorphism in a defended species is strictly neutral whenever the population is dense enough to saturate the predator. This, as well as quasi-batesian mimicry, may help to explain the minority of warningly coloured species that are polymorphic. This revised version was published online in July 2006 with corrections to the Cover Date.     

Increased predation of nutrient-enriched aposematic prey

Avian predators readily learn to associate the warning coloration of aposematic prey with the toxic effects of ingesting them, but they do not necessarily exclude aposematic prey from their diets. By eating aposematic prey ‘educated’ predators are thought to be trading-off the benefits of gaining nutrients with the costs of eating toxins. However, while we know that the toxin content of aposematic prey affects the foraging decisions made by avian predators, the extent to which the nutritional content of toxic prey affects predators'' decisions to eat them remains to be tested. Here, we show that European starlings (Sturnus vulgaris) increase their intake of a toxic prey type when the nutritional content is artificially increased, and decrease their intake when nutritional enrichment is ceased. This clearly demonstrates that birds can detect the nutritional content of toxic prey by post-ingestive feedback, and use this information in their foraging decisions, raising new perspectives on the evolution of prey defences. Nutritional differences between individuals could result in equally toxic prey being unequally predated, and might explain why some species undergo ontogenetic shifts in defence strategies. Furthermore, the nutritional value of prey will likely have a significant impact on the evolutionary dynamics of mimicry systems.     

When more is less: the fitness consequences of predators attacking more unpalatable prey when more are presented

In 1879, Fritz Müller hypothesized that mimetic resemblance in which defended prey display the same warning signal would share the costs of predator education. Although Müller argued that predators would need to ingest a fixed number of prey with a given visual signal when learning to avoid unpalatable prey, this assumption lacks empirical support. We report an experiment which shows that, as the number of unpalatable prey presented to them increased, avian predators attacked higher numbers of those prey. We calculated that, when predators increase attacks, the fitness costs incurred by unpalatable prey can be substantial. This suggests that the survival benefits of mimicry could be lower than Müller proposed. An important finding is, however, that these costs decline in importance as the total number of available prey increases.     

Alternative prey can change model–mimic dynamics between parasitism and mutualism

Classical (conventional) Müllerian mimicry theory predicts that two (or more) defended prey sharing the same signal always benefit each other despite the fact that one species can be more toxic than the other. The quasi‐Batesian (unconventional) mimicry theory, instead, predicts that the less defended partner of the mimetic relationship may act as a parasite of the signal, causing a fitness loss to the model. Here we clarify the conditions for parasitic or mutualistic relationships between aposematic prey, and build a model to examine the hypothesis that the availability of alternative prey is crucial to Müllerian and quasi‐Batesian mimicry. Our model is based on optimal behaviour of the predator. We ask if and when it is in the interest of the predator to learn to avoid certain species as prey when there is alternative (cryptic) prey available. Our model clearly shows that the role of alternative prey must be taken into consideration when studying model–mimic dynamics. When food is scarce it pays for the predator to test the models and mimics, whereas if food is abundant predators should leave the mimics and models untouched even if the mimics are quite edible. Dynamics of the mimicry tend to be classically Müllerian if mimics are well defended, while quasi‐Batesian dynamics are more likely when they are relatively edible. However, there is significant overlap: in extreme cases mimics can be harmful to models (a quasi‐Batesian case) even if the species are equally toxic. A crucial parameter explaining this overlap is the search efficiency with which indiscriminating vs. discriminating predators find cryptic prey. Quasi‐Batesian mimicry becomes much more likely if discrimination increases the efficiency with which the specialized predator finds cryptic prey, while the opposite case tends to predict Müllerian mimicry. Our model shows that both mutualistic and parasitic relationship between model and mimic are possible and the availability of alternative prey can easily alter this relationship.     

Testing Müllerian mimicry: an experiment with wild birds

Experiments with wild birds feeding on pastry 'prey' were performed to test competing theories of Müllerian mimicry Conventional theories predict that all resemblances between defended prey will be mutually advantageous and, hence, Müllerian. In contrast, unconventional theories predict that, if there are inequalities in defences between mimetic species, the less well-defended prey may dilute the protection of the better defended species in a quasi-Batesian manner. This unconventional prediction follows from an assumption that birds learn about the edibilities of prey using rules of Pavlovian learning. We report on two experiments, each lasting 40 days, which showed that a moderately defended prey can dilute the protection of a better defended mimic in a quasi-Batesian fashion, but can add protection to a mimic which has the same moderate levels of defence. These results match predictions of unconventional theories of mimicry and go some way to resolving the long-running arguments over the nature of Müllerian mimicry.     

Robot predators in virtual ecologies: the importance of memory in mimicry studies

An important means of investigating gains and losses to prey caused by mimicry is through mathematical or computer constructs which represent and explore limited aspects of mimicry situations. Such studies use virtual predators which are usually simple automata, 'robots' that, through simple rules, vary virtual attack rates on virtual insect prey. In this paper I consider the effect of variations in predator memory and learning on mimicry dynamics. When there is mimicry between unequally noxious prey, the way that memory is modelled is shown to be crucial. If forgetting rates are fixed, an increase in the density of the least defended prey produces monotonic gains or losses in protection. However, if forgetting rate is inversely related in some way to degree of noxiousness of the prey then attack rates initially rise with the density of the least defended prey, reach a cusp and then fall. I show that the generation of this highly unconventional up-down result appears to be independent of variations in learning rate. This work shows how sensitive the predictions of virtual predators may be to relatively small changes in behavioural rules. Copyright 1999 The Association for the Study of Animal Behaviour.     

Better the devil you know: avian predators find variation in prey toxicity aversive

Toxic prey that signal their defences to predators using conspicuous warning signals are called ‘aposematic’. Predators learn about the toxic content of aposematic prey and reduce their attacks on them. However, through regulating their toxin intake, predators will include aposematic prey in their diets when the benefits of gaining the nutrients they contain outweigh the costs of ingesting the prey''s toxins. Predators face a problem when managing their toxin intake: prey sharing the same warning signal often vary in their toxicities. Given that predators should avoid uncertainty when managing their toxin intake, we tested whether European starlings (Sturnus vulgaris) preferred to eat fixed-defence prey (where all prey contained a 2% quinine solution) to mixed-defence prey (where half the prey contained a 4% quinine solution and the other half contained only water). Our results support the idea that predators should be more ‘risk-averse’ when foraging on variably defended prey and suggest that variation in toxicity levels could be a form of defence.     

Predator mixes and the conspicuousness of aposematic signals

Conspicuous warning signals of unprofitable prey are a defense against visually hunting predators. They work because predators learn to associate unprofitability with bright coloration and because strong signals are detectable and memorable. However, many species that can be considered defended are not very conspicuous; they have weak warning signals. This phenomenon has previously been ignored in models and experiments. In addition, there is significant within- and among-species variation among predators in their search behavior, in their visual, cognitive, and learning abilities, and in their resistance to defenses. In this article we explore the effects of variable predators on models that combine positive frequency-dependent, frequency-independent, and negative frequency-dependent predation and show that weak signaling of aposematic species can evolve if predators vary in their tendency to attack defended prey.     

Taste-rejection behaviour by predators can promote variability in prey defences

The evolution and maintenance of toxicity in a prey population is a challenge to evolutionary biologists if the investment in toxin does not benefit the individual. Recent experiments suggest that taste-rejection behaviour enables predators to selectively ingest less toxic individuals, which could stabilize investment in defences. However, we currently do not know if taste rejection of defended prey is accurate across different contexts, and that prey always benefit according to their investment. Using avian predators, we show that the rejection probability does not solely depend on the investment in defence by an individual, but also on the investment by other individuals in the same population. Therefore, taste rejection by predators could lead to destabilization in the investment in defences, and allow variability in prey defences to exist.     

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.     

Natural selection on unpalatable species imposed by state-dependent foraging behaviour

Müllerian mimicry is typically thought to arise as a consequence of defended prey species adopting a similar way of signalling their unprofitability, thereby reducing the costs of predator education. Here we consider subsequent selection on the morphology of prey species, in the potentially lengthy period of time when predators are generally aware of the noxious qualities of their prey (and so no further learning is involved). Using a pair of stochastic dynamic programming equations which describe both the toxin burdens of a predator and its energy level, we identified the optimal state-dependent rules that maximize a predator's long-term survivorship, and examined the implications of this behaviour for the evolution of prey morphologies. When palatable prey are in short supply then those prey species which contain relatively low doses of toxins become profitable to consume by hungry predators. Under these conditions, a weakly defended prey could gain selective advantage in the post educational period by resembling a prey species which contained a higher dose of the same or different toxins, although the precise nature of the ecological relationship between model and mimic could either be mutualistic or parasitic depending on how mimic density increases when favoured by selection. Our work formally demonstrates that one does not always need to invoke educational effects to explain why two or more unpalatable species have evolved a similar appearance, or to explain why mimetic similarity among distasteful species is maintained over time. When two species contain high levels of different toxins then they may gain mutual advantage by resembling one another, not only by educating the predator as to their common unprofitability (classical Müllerian mimicry), but also by increasing predator uncertainty as to the specific kind of toxin a prey item contains.     

Avian predators taste-reject aposematic prey on the basis of their chemical defence

Avian predators learn to avoid defended insects on the basis of their conspicuous warning coloration. In many aposematic species, the level of chemical defence varies, with some individuals being more defended than others. Sequestration and production of defence chemicals is often costly and therefore less defended individuals enjoy the benefits of the warning signal without paying the full costs of chemical production. This is a fundamental theoretical problem for the evolutionary stability of aposematism, since less defended individuals appear to be at a selective advantage. However, if predators sample aposematic prey and selectively reject individuals on the basis of their chemical investment, aposematism could become evolutionarily stable. Previous research aimed at testing whether birds can use taste to discriminate between palatable and unpalatable prey has been confounded by other experimental factors. Here, we show that birds can taste and reject prey entirely on the basis of an individual's level of chemical defence and more importantly, they can make decisions on whether or not to consume a defended individual based upon their level of chemical investment. We discuss these results in relation to the evolution of aposematism, mimicry and defence chemistry.     

The evolution of warning signals as reliable indicators of prey defense

It is widely argued that defended prey have tended to evolve conspicuous traits because predators more readily learn to avoid defended prey when they are conspicuous. However, a rival theory proposes that defended prey have evolved such characters because it allows them to be distinguished from undefended prey. Here we investigated how the attributes of defended (unprofitable) and undefended (profitable) computer-generated prey species tended to evolve when they were subject to selection by foraging humans. When cryptic forms of defended and undefended species were similar in appearance but their conspicuous forms were not, defended prey became conspicuous while undefended prey remained cryptic. Indeed, in all of our experiments, defended prey invariably evolved any trait that enabled them to be distinguished from undefended prey, even if such traits were cryptic. When conspicuous mutants of defended prey were extremely rare, they frequently overcame their initial disadvantage by chance. When Batesian mimicry of defended species was possible, defended prey evolved unique traits or characteristics that would make undefended prey vulnerable. Overall, our work supports the contention that warning signals are selected for their reliability as indicators of defense rather than to capitalize on any inherent educational biases of predators.     

Stabilimenta attract unwelcome predators to orb-webs

Conspicuous behaviour exposes animals to predation; prey-attraction thus often conflicts with antipredator behaviour. The fact that a conspicuous ultraviolet-light reflecting silken structure in the orb-webs of certain spider species, known as a stabilimentum, makes the webs obvious to both prey and predators has been used to argue that spiders benefit from building stabilimenta by attracting prey and/or defending against visually hunting predators. Here, we provide experimental evidence that stabilimenta can act as visual signals that attract web-invading spider-eating predators with acute vision to the webs. We also show that the predators can learn to remember a particular type of stabilimentum. Thus, stabilimentum-building spiders risk a high level of predation by attracting visually hunting predators.     

Heterogeneity in predator micro-habitat use and the maintenance of Müllerian mimetic diversity

Müllerian mimicry, where groups of chemically defended species display a common warning color pattern and thereby share the cost of educating predators, is one of the most striking examples of ecological adaptation. Classic models of Müllerian mimicry predict that all unpalatable species of a similar size and form within a community should converge on a single mimetic pattern, but instead communities of unpalatable species often display a remarkable diversity of mimetic patterns (e.g. neotropical ithomiine butterflies). It has been suggested that this apparent paradox may be explained if different suites of predators and species belonging to different mimicry groups utilize different micro-habitats within the community. We developed a stochastic individual-based model for a community of unpalatable mimetic prey species and their predators to evaluate this hypothesis and to examine the effect of predator heterogeneity on prey micro-habitat use. We found that community-level mimetic diversity was higher in simulations with heterogeneous predator micro-habitat use than in simulations with homogeneous predator micro-habitat use. Regardless of the form of predation, mimicry pattern-based assortative mating caused community-level mimetic diversity to persist. Heterogeneity in predator micro-habitat use led to an increased association between mimicry pattern and prey micro-habitat use relative to homogeneous predator micro-habitat use. This increased association was driven, at least in part, by evolutionary convergence of prey micro-habitat use when predators displayed heterogeneous micro-habitat use. These findings provide a theoretical explanation for an important question in evolutionary biology: how is community-level Müllerian mimetic diversity maintained in the face of selection against rare phenotypes?     

Balanced polymorphisms and their divergence in a Heliconius butterfly

The evolution of mimicry in similarly defended prey is well described by the Müllerian mimicry theory, which predicts the convergence of warning patterns in order to gain the most protection from predators. However, despite this prediction, we can find great diversity of color patterns among Müllerian mimics such as Heliconius butterflies in the neotropics. Furthermore, some species have evolved the ability to maintain multiple distinct warning patterns in single populations, a phenomenon known as polymorphic mimicry. The adaptive benefit of these polymorphisms is questionable since variation from the most common warning patterns is expected to be disadvantageous as novel signals are punished by predators naive to them. In this study, we use artificial butterfly models throughout Central and South America to characterize the selective pressures maintaining polymorphic mimicry in Heliconius doris. Our results highlight the complexity of positive frequency‐dependent selection, the principal selective pressure driving convergence among Müllerian mimics, and its impacts on interspecific variation of mimetic warning coloration. We further show how this selection regime can both limit and facilitate the diversification of mimetic traits.