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.     

Sex differences in antipredator tail-waving displays of the diurnal yellow-headed gecko Gonatodes albogularis from tropical forests of Colombia

Many vertebrate species show display behaviors when predators are in their vicinity. Some of these displays may inform the predator of the improbability of capturing the prey (i.e., pursuit-deterrent displays) and are potentially advantageous to both predator and prey. Here we present data on a tail display performed by Gonatodes albogularis, a diurnal tropical gecko. We performed transect surveys in three habitats near Bogotá in Colombia. Geckos detected during transects were approached by the observer in a standardized way, and details of their tail-waving displays were recorded. In control recordings animals were watched from a distant site without approaching them. Results showed sexual differences in tail-waving display: when approached by the observer, males performed this behavior more frequently than females. We found no significant differences between males and females in flight-initiation distances and height above the substratum when they were initially located. Results also showed that males displayed more frequently when approached than when the simulated predator remained stationary. We interpret these results as evidence that the display functions as a pursuit-deterrent signal to potential predators. However, as some tail displays were performed in the presence of conspecifics, the display may also have a social function.     

Automimicry destabilizes aposematism: predator sample-and-reject behaviour may provide a solution

Aposematism, the use of conspicuous colours to advertise unpalatability to predators, is perhaps the most studied signalling system in nature. However, its evolutionary stability remains paradoxical. The paradox is illustrated by the problem of automimicry. Automimics are palatable individuals within a population of unpalatable aposematics. Automimics benefit from predators avoiding warning coloration without carrying the models' cost of unpalatability, and should increase in the population, destabilizing the signalling system, unless selected against in some way. Cautious sampling, instead of avoidance, by predators may offer a solution to this problem. Here, we investigate the effect of automimic frequency on predator sampling behaviour, and whether predator sampling behaviour may provide a selection pressure against mimics. Domestic chicks (Gallus gallus domesticus) were subjected to the task of discriminating between green (signalling) and untreated brown chick crumbs. Some of the green crumbs were quinine treated and thus unpalatable. The frequency of palatable signalling prey items varied in four treatments; all unpalatable, low automimic frequency, high automimic frequency and all palatable. The results show that predator sampling behaviour is sensitive to automimic frequency and that predators may discriminate between models and mimics through sampling, and thereby benefit unprofitable prey. The results suggest somewhat surprisingly that aposematic signalling is stable only because of the actions of those predators not actually deterred by warning signals.     

Perspective: the evolution of warning coloration is not paradoxical

Animals that are brightly colored have intrigued scientists since the time of Darwin, because it seems surprising that prey should have evolved to be clearly visible to predators. Often this self-advertisement is explained by the prey being unprofitable in some way, with the conspicuous warning coloration helping to protect the prey because it signals to potential predators that the prey is unprofitable. However, such signals only work in this way once predators have learned to associate the conspicuous color with the unprofitability of the prey. The evolution of warning coloration is still widely considered to be a paradox, because it has traditionally been assumed that the very first brightly colored individuals would be at an immediate selective disadvantage because of their greater conspicuousness to predators that are naive to the meaning of the signal. As a result, it has been difficult to understand how a novel conspicuous color morph could ever avoid extinction for long enough for predators to become educated about the signal. Thus, the traditional view that the evolution of warning coloration is difficult to explain rests entirely on assumptions about the foraging behavior of predators. However, we review recent evidence from a range of studies of predator foraging decisions, which refute these established assumptions. These studies show that: (1) Many predators are so conservative in their food preferences that even very conspicuous novel prey morphs are not necessarily at a selective disadvantage. (2) The survival and spread of novel color morphs can be simulated in field and aviary experiments using real predators (birds) foraging on successive generations of artificial prey populations. This work demonstrates that the foraging preferences of predators can regularly (though not always) result in the increase to fixation of a novel morph appearing in a population of familiar-colored prey. Such fixation events occur even if both novel and familiar prey are fully palatable and despite the novel food being much more conspicuous than the familiar prey. These studies therefore provide strong empirical evidence that conspicuous coloration can evolve readily, and repeatedly, as a result of the conservative foraging decisions of predators.     

Avian predators attack aposematic prey more forcefully when they are part of an aggregation

Defended insects often advertise their unprofitability to potential predators using conspicuous aposematic coloration. Many aposematic insects are also gregarious, and it has been suggested that the aggregation of defended prey may have facilitated the evolution of aposematic coloration. Empirical studies have demonstrated that birds are more wary of aggregated aposematic prey, and learn to avoid them more quickly than solitary prey. However, many aposematic insects survive being attacked by birds, and the effect of aggregation on post-attack survival has not previously been investigated. Using domestic chicks as predators and artificially manipulated mealworms as prey, we provide empirical evidence that predators attack aggregated aposematic prey more forcefully than solitary prey, reducing the likelihood of prey surviving an attack. Hence, we suggest that previous works concluding that aggregation was an important pre-requisite for the evolution of aposematism may have overestimated the fitness benefits of aggregation, since aggregated prey may be attacked less but are also less likely to survive an attack.     

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.     

Frequency-dependent taste-rejection by avian predation may select for defence chemical polymorphisms in aposematic prey

Chemically defended insects advertise their unpalatability to avian predators using conspicuous aposematic coloration that predators learn to avoid. Insects utilize a wide variety of different compounds in their defences, and intraspecific variation in defence chemistry is common. We propose that polymorphisms in insect defence chemicals may be beneficial to insects by increasing survival from avian predators. Birds learn to avoid a colour signal faster when individual prey possesses one of two unpalatable chemicals rather than all prey having the same defence chemical. However, for chemical polymorphisms to evolve within a species, there must be benefits that allow rare chemical morphs to increase in frequency. Using domestic chicks as predators and coloured crumbs for prey, we provide evidence that birds taste and reject proportionally more of the individuals with rare defence chemicals than those with common defence chemicals. This indicates that the way in which birds attack and reject prey could enhance the survival of rare chemical morphs and select for chemical polymorphism in aposematic species. This is the first experiment to demonstrate that predators can directly influence the form taken by prey's chemical defences.     

Prey selection by wild birds can allow novel and conspicuous colour morphs to spread in prey populations

Conspicuous warning coloration helps to protect prey because it signals to potential predators that the prey is unprofitable. However, such signals only work once predators have come to associate the conspicuous colour with the unprofitability of the prey. The evolution of warning coloration is generally considered to be paradoxical, because it has traditionally been assumed that the first brightly coloured individuals would be at an immediate selective disadvantage because of their greater conspicuousness to predators that are naïve to the meaning of the signal. As a result, it has been difficult to understand how a novel conspicuous colour morph could ever avoid rapid extinction, and instead survive and spread in the population until predators have become educated about the signal. In the present study, we experimentally simulated the appearance of a single novel coloured mutant in small populations (20 individuals) of palatable artificial pastry "prey". The colour morph frequencies in each "generation" of prey (presented on successive days of a trial) were determined by the relative survival of the previous generation under predation by free-living birds. We found that the novel colour morphs regularly persisted and increased from a starting frequency of 1/20 to reach fixation (100%), despite being fully palatable, even when the novel morph was much more conspicuous against the background than the familiar morph. This was true for both green (not normally considered a warning colour) and red (a classic warning colour) novel morphs. Novel colours reached fixation significantly faster than could be accounted for by random drift, indicating differential predation in relation to prey colour by the birds. Our experiments show that the immediate demise of a fully palatable new prey morph is not an inevitable outcome of predator behaviour, because even very conspicuous prey can gain protection from conservative foragers, simply by being novel.     

Experimental Approaches to Studying the Initial Evolution of Conspicuous Aposematic Signalling

Aposematism, where prey species conspicuously advertise their unprofitability to predators, is a widespread defensive strategy. One feature of an aposematic anti-predatory strategy that is especially puzzling is conspicuousness. While conspicuousness aids associative learning in predators, it involves being more visible, which probably increases predation risk. Although aposematism is an old evolutionary question, experimental studies to its evolution have been scarce. Only 11 experiments address the potential benefits of conspicuousness, which have successfully manipulated conspicuousness. This is probably because it is difficult to separate conspicuousness from other characters of aposematic prey, e.g. colour. Furthermore since predators and prey species have coexisted for a long time, and there might be special adaptations other than conspicuous signalling, our experimental results might be confounded with, e.g. predatory biases. In this review, I will examine the problems of studying the costs and benefits of conspicuousness as well as the initial evolution of conspicuousness and the recent progress in the study of aposematism. This revised version was published online in July 2006 with corrections to the Cover Date.     

State-dependent risk-taking by predators in systems with defended prey

Even defended prey items may contain nutrients that can sustain predators in times of energetic need. Conversely, a well-fed predator might be expected to avoid attacking prey items that have a chance of being defended, particularly if there is an abundance of familiar palatable prey to support it. To further understand the implications of optimal state-dependent foraging behaviour by predators in systems that contain defended prey, I developed a stochastic dynamic programming model. This state-dependent approach formally accounts for the trade-off between avoiding starvation and minimising harm from attacking defended prey. It predicts that the mean attack probability of predators on defended models and their undefended mimics should decline in a sigmoidal fashion with increasing availability of alternative undefended prey, and that the foraging decisions of predators should in general be relatively insensitive to the probability that a potentially defended prey item is indeed defended. Some implications of these predictions are that conspicuous warning signals are more likely to evolve in systems that contain an abundance of alternative undefended prey, and that imperfect mimicry will provide almost complete protection to the mimic when predators are readily supported by alternative food sources. Somewhat surprisingly, increasing the density of nutritious undefended mimics while keeping the densities of all other prey types constant tended to decrease the attack rates of predators on encounter with mimics and their defended models. This increase in dietary conservatism arose because in these cases there would be more prey available to sustain the predator if it ever found itself critically low in energy.     

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.     

Prey perception of predation risk: volatile chemical cues mediate non-consumptive effects of a predator on a herbivorous insect

Predators can affect prey in two ways—by reducing their density (consumptive effects) or by changing their behavior, physiology or other phenotypic traits (non-consumptive effects). Understanding the cues and sensory modalities prey use to detect predators is critical for predicting the strength of non-consumptive effects and the outcome of predator–prey encounters. While predator-associated cues have been well studied in aquatic systems, less is known about how terrestrial prey, particularly insect larvae, detect their predators. We evaluated how Colorado potato beetle, Leptinotarsa decemlineata, larvae perceive predation risk by isolating cues from its stink bug predator, the spined soldier bug, Podisus maculiventris. When exposed to male “risk” predators that were surgically manipulated so they could hunt but not kill, beetles reduced feeding 29 % compared to controls. Exposure to risk females caused an intermediate response. Beetles ate 24 % less on leaves pre-exposed to predators compared to leaves never exposed to predators, indicating that tactile and visual cues are not required for the prey’s response. Volatile odor cues from predators reduced beetle feeding by 10 % overall, although male predators caused a stronger reduction than females. Finally, visual cues from the predator had a weak effect on beetle feeding. Because multiple cues appear to be involved in prey perception of risk, and because male and female predators have differential effects, beetle larvae likely experience tremendous variation in the information about risk from their local environment.     

Dangerous liaisons: the predation risks of receiving social signals

Individuals are at risk when communicating because conspicuous signals attract both conspecifics and eavesdropping predators. This predation cost of communicating has typically been attributed to signalling individuals because of their conspicuous role, and is a core concept within sexual selection and communication ecology. But, if predators are attracted to signals, then receivers, both intended or otherwise, may also find themselves at risk of predation. Here, we review the theoretical basis and empirical evidence that receiving also carries a risk of predation. We distinguish between the risks of receiving and responding to signals, and we argue that receivers of signals that are long lived, are highly predictable in time or place and/or cannot be received quickly are likely to be at greater risk of predation compared to receivers of signals without these properties. We review recent empirical evidence from a variety of taxa that supports the hypothesis that receivers (including heterospecific prey) are aware of these risks and that they modify their behaviour to balance the risks against the benefits of receiving under predation threat. We also discuss the wider implications of risky receiving for receiving and signalling behaviour in prey, as well as for the prey's predators.     

The coevolution of warning signals

It has long been recognized that defended prey tend to be conspicuous. Current theories suggest that the association ('aposematism') has arisen because predators more readily learn to avoid attacking defended phenotypes when they are conspicuous. In this paper, I consider why such psychology has evolved. In particular, I argue that aposematism may have evolved not because of an independent and pre-existing receiver bias, but because the conspicuousness of a prey item provides a reliable indicator of its likelihood of being defended. To develop my case I consider how warning signals might coevolve in a system containing a number of predators, whose foraging behaviour is also subject to selection. In these cases, models readily show that the greater the conspicuousness of a novel prey item, the more likely that it has been encountered by other predators and survived. As a consequence, naive predators should be less likely to attack highly conspicuous novel prey on encounter, or at least more inclined to attack them cautiously. This adaptive predator behaviour will greatly facilitate the spread of aposematic phenotypes from extreme rarity, which in turn will enhance selection for forms of predator behaviour under which aposematism will coevolve even more readily.     

Predators target rare prey in coral reef fish assemblages

Predation can result in differing patterns of local prey diversity depending on whether predators are selective and, if so, how they select prey. A recent study comparing the diversity of juvenile fish assemblages among coral reefs with and without predators concluded that decreased prey diversity in the presence of predators was most likely caused by predators actively selecting rare prey species. We used several related laboratory experiments to explore this hypothesis by testing: (1) whether predators prefer particular prey species, (2) whether individual predators consistently select the same prey species, (3) whether predators target rare prey, and (4) whether rare prey are more vulnerable to predation because they differ in appearance/colouration from common prey. Rare prey suffered greater predation than expected and were not more vulnerable to predators because their appearance/colouration differed from common prey. Individual predators did not consistently select the same prey species through time, suggesting that prey selection behaviour was flexible and context dependent rather than fixed. Thus, selection of rare prey was unlikely to be explained by simple preferences for particular prey species. We hypothesize that when faced with multiple prey species predators may initially focus on rare, conspicuous species to overcome the sensory confusion experienced when attacking aggregated prey, thereby minimizing the time required to capture prey. This hypothesis represents a community-level manifestation of two well-documented and related phenomena, the “confusion effect” and the “oddity effect”, and may be an important, and often overlooked, mechanism by which predators influence local species diversity.     

Conditions for the spread of conspicuous warning signals: a numerical model with novel insights

The initial evolution of conspicuous warning signals presents an evolutionary problem because selection against rare conspicuous signals is presumed to be strong, and new signals are rare when they first arise. Several possible solutions have been offered to solve this apparent evolutionary paradox, but disagreement persists over the plausibility of some of the proposed mechanisms. In this paper, we construct a deterministic numerical simulation model that allows us to derive the strength of selection on novel warning signals in a wide range of biologically relevant situations. We study the effects of predator psychology (learning, rate of mistaken attacks, and neophobia) on selection. We also study the how prey escape, predation intensity, number of predators, and abundance of different prey types affects selection. The model provides several important results. Selection on novel warning signals is number rather than frequency dependent. In most cases, there exists a threshold number of aposematic individuals below which aposematism is selected against and above which aposematism is selected for. Signal conspicuousness (which increases detection rate) and distinctiveness (which allows predator to distinguish defended from nondefended prey) have opposing effects on evolution of warning signals. A more conspicuous warning signal cannot evolve unless it makes the prey more distinctive from palatable prey, reducing mistaken attacks by predators. A novel warning signal that is learned quickly can spread from lower abundance more easily than a signal that is learned more slowly. However, the relative rate at which the resident signal and the novel signal are learned is irrelevant for the spread of the novel signal. Long-lasting neophobia can facilitate the spread of novel warning signals. Individual selection via the ability of defended prey to escape from predator is not likely to facilitate evolution of conspicuous warning signals if both the resident (cryptic) morph and the novel morph have the same escape probability. Predation intensity (defined as the proportion of palatable prey eaten by the predator) has a strong effect on selection. More intense predation results in strong selection against rare signals, but also strong selective advantage to common signals. The threshold number of aposematic individuals is lower when predation is intense. Thus, the evolution of warning signals may be more likely in environments where predation is intense. The effect of numbers of predators depends on whether predation intensity also changes. When predation intensity is constant, increasing numbers of predators raises the threshold number of aposematic individuals, and thus makes evolution of aposematism more difficult. If predation intensity increases in parallel with number of predators, the threshold number of aposematic individuals does not change much, but selection becomes more intense on both sides of the threshold.     

El Niño events,the lean versus fat scenario,and long‐term guild dynamics of vertebrate predators in a South American semiarid ecosystem

Abstract Predator assemblages are complex systems in which asynchrony in the dynamics of resources and consumers, and the idiosyncratic perception of environmental conditions by the predators may obscure the detection of expected patterns. We disentangle the specific effects of these variables on the guild structure of a vertebrate predatory assemblage in a semiarid ecosystem of western South America. Over 16 years, this system faced dramatic fluctuations in prey availability associated with four El Niño events. After controlling for other sources of variation, we tested if increased resource availability is associated with higher niche overlaps, as expected from the lean/fat scenario. We determined the existence of two trophic guilds of predators (specialized mammal‐eaters and omnivorous species with emphasis on arthropods) and found that they responded to increased productivity both at the guild and whole assemblage levels. However, the population response of arthropod prey (almost simultaneous) and of different small mammal prey (delayed by 1 or 2 years) to productivity imposed a degree of asynchrony in prey availability and in the response of predators. This resulted in the between‐guilds exchange of predator species depending on mammal prey scarcity or abundance. As a consequence, the observed pattern was an apparent lack of response at the assemblage level. Despite differences in the perception of prey levels by predators, we conclude that each one of them responded accordingly to theoretical predictions following a simple rule: if prey resources are not limiting, predators behave opportunistically converging over the most abundant resources, thus increasing niche overlap; if prey shortages occur, predators specialize on those prey resources that they gather most efficiently, thus lowering niche overlap; if resources become even scarcer, all predators converge again upon the few prey resources still available, thus increasing overlap – out of necessity.     

Why aren't warning signals everywhere? On the prevalence of aposematism and mimicry in communities

Warning signals are a striking example of natural selection present in almost every ecological community – from Nordic meadows to tropical rainforests, defended prey species and their mimics ward off potential predators before they attack. Yet despite the wide distribution of warning signals, they are relatively scarce as a proportion of the total prey available, and more so in some biomes than others. Classically, warning signals are thought to be governed by positive density-dependent selection, i.e. they succeed better when they are more common. Therefore, after surmounting this initial barrier to their evolution, it is puzzling that they remain uncommon on the scale of the community. Here, we explore factors likely to determine the prevalence of warning signals in prey assemblages. These factors include the nature of prey defences and any constraints upon them, the behavioural interactions of predators with different prey defences, the numerical responses of predators governed by movement and reproduction, the diversity and abundance of undefended alternative prey and Batesian mimics in the community, and variability in other ecological circumstances. We also discuss the macroevolution of warning signals. Our review finds that we have a basic understanding of how many species in some taxonomic groups have warning signals, but very little information on the interrelationships among population abundances across prey communities, the diversity of signal phenotypes, and prey defences. We also have detailed knowledge of how a few generalist predator species forage in artificial laboratory environments, but we know much less about how predators forage in complex natural communities with variable prey defences. We describe how empirical work to address each of these knowledge gaps can test specific hypotheses for why warning signals exhibit their particular patterns of distribution. This will help us to understand how behavioural interactions shape ecological communities.     

Better to be bimodal: the interaction of color and odor on learning and memory

Defended prey frequently advertise to potential predators usingmultimodal warning displays. Signaling through more than onesensory pathway may enhance the rate of avoidance learning andthe memorability of these learned avoidances. If this is so,then mimetic insects would gain more protection from mimickinga multimodal rather than a monomodal model. Day-old domesticchicks (Gallus gallus domesticus) were used to examine whethera common insect warning odor (pyrazine) enhanced learning andmemorability of yellow prey, a common warning color. Pyrazineincreased the rate at which the chicks learned to avoid unpalatableyellow prey, and how well this learned avoidance was rememberedafter a 96-h interval. After 96 h, mimics of the multimodalprey were avoided, whereas mimics of the monomodal prey werenot. In the absence of pyrazine, chicks generalized their learnedavoidance of the unpalatable yellow prey to palatable greenprey; however, the presence of pyrazine reduced this color generalization.These results suggest that much is to be gained from signalingmultimodally, for both models and mimetic prey species. Thepresence of multimodal prey in the habitat may also advantagethe predators as it allows it them to distinguish more easilybetween palatable and unpalatable prey.