Decision time and prey gregariousness influence attack probability in naïve and experienced predators

Aposematic coloration often has an element of conspicuousness. One suggested benefit of conspicuousness is that it enables the prey to be detected at a greater distance, allowing a predator more time to make a correct decision about attacking it and thus reducing possible recognition errors made by predators. I conducted an experiment, with chicks, Gallus gallus domesticus, as predators on live aposematic and nonaposematic prey, to investigate the effects of decision time and signal size on predator sampling behaviour. The chicks were subjected to different degrees of competition to influence how quickly decisions had to be made. Chicks in four treatment groups, either in the presence or absence of a competing chick, were presented with either solitary prey or prey in groups. In the presence of a competitor, chicks attacked the prey more often and more quickly and needed more attacks before they started to avoid the prey. With prey in groups, chicks took longer to attack, attacked less often, learnt to avoid prey more quickly and killed fewer aposematic prey. This experiment provides evidence for the importance of time and signal size for predators' attack decisions. More time to view prey prior to attack could produce a stronger image and thus encourage avoidance learning and produce a stronger neophobic avoidance effect. Copyright 2000 The Association for the Study of Animal Behaviour.     

Contrast versus colour in aposematic signals

Conspicuousness is an important feature of warning coloration. One hypothesis for its function is that it increases signal efficacy by facilitating avoidance learning. An alternative, based on the handicap hypothesis, suggests that the degree of conspicuousness holds information directly about the quality of the prey, and that predators associate and learn about the conspicuousness of the coloration, and not the actual colour pattern. We studied the relative importance of signal contrast and the colours of signals for predator attention during discrimination. We used young chicks, Gallus gallus domesticus, as predators and small blue or red paper cones on either matching or contrasting paper backgrounds as stimuli associated with palatable or unpalatable chick crumbs. In four treatment groups, birds could use either cone and/or background colour, cone colour only, background colour only or cone-to-background contrast as cues for discrimination. Only birds in the contrast treatment failed to learn their discrimination task. Birds that had a choice between cone and background colour as cues used the cone colour and they learned the task faster than did birds that had to use background colour as a cue. The results suggest that birds primarily attend to the colours of signals and disregard contrast in discrimination tasks; they thus fail to support a handicap function of conspicuous aposematic coloration. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey

Recently there has been debate over the importance of innateavoidance of aposematic prey by predators, particularly birds.There is evidence that the predators have innate or unlearned,thus, inherited avoidance against certain colors, but whetherthere is any innate avoidance against gregariousness or conspicuousnessis unclear. Previously predator behavior toward these charactersof aposematic prey have been tested in separate experiments.We designed an experiment to separate inheritance toward color,gregariousness, and conspiucuosness. We simultaneously offeredthe predators warningly colored and nonwarningly colored preyitems, both aggregated and solitary, on white (conspicuous)or brown (cryptic) backgrounds. The predators we used were naive (handraised), wild-caught yearling and adult great tits (Parus major L.).The results confirm previous results regarding the innate avoidanceof color. Naive predators seemed to have a genetically or culturallytransmitted avoidance of yellow and black prey compared to brownprey. Surprisingly, yearling wild-caught great tits were moreselective than adults, which did not show as strong avoidanceof yellow and black prey. More importantly, birds did not findgregarious prey more aversive than single prey, which indicatesthat grouping alone does not serve as an innate avoidance signal.Conspicuousness itself was not aversive to the predators. Ourresults suggest that the avoidance against a particular colorpattern probably has an inherited basis, whereas gregariousand conspicuous characters of prey presumably aid the avoidancelearning.     

Aposematic coloration, luminance contrast, and the benefits of conspicuousness

Many organisms use warning, or aposematic, coloration to signaltheir unprofitability to potential predators. Aposematicallycolored prey are highly visually conspicuous. There is considerableempirical support that conspicuousness promotes the effectivenessof the aposematic signal. From these experiments, it is welldocumented that conspicuous, unprofitable prey are detectedsooner and aversion learned faster by the predator as comparedwith cryptic, unprofitable prey. Predators also retain memoryof the aversion longer when prey is conspicuous. The presentstudy focused on the elements of conspicuousness that conferthese benefits of aposematic coloration. Drawing on currentunderstanding of animal vision, we distinguish 2 features ofwarning coloration: high chromatic contrast and high brightness,or luminance, contrast. Previous investigations on aposematicsignal efficacy have focused mainly on the role of high chromaticcontrast between prey and background, whereas little researchhas investigated the role of high luminance contrast. Usingthe Chinese mantid as a model predator and gray-painted milkweedbugs as model prey, we found that increased prey luminance contrastincreased detection of prey, facilitated predator aversion learning,and increased predator memory retention of the aversive response.Our results suggest that the luminance contrast component ofaposematic coloration can be an effective warning signal betweenthe prey and predator. Thus, warning coloration can even evolveas an effective signal to color blind 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.     

The effects of background coloration and dark spots on the risk of predation in poison frog models

Protective coloration is a well-known predator avoidance strategy in prey species. Aposematic species often display a contrasting color pattern consisting of dark spots of different shapes and sizes on a bright background coloration. Both elements, background color and spots are expected to serve different purposes. While the ecological function of the bright coloration has been addressed in many studies, the question of whether the interaction with differently sized spots influences predator behavior has received less attention by researchers. In a lowland rain forest in Costa Rica we used 2700 clay models that imitated the polytypic strawberry poison frog (Oophaga pumilio) as a proxy for an aposematic prey species. We manipulated the dorsal color pattern by using a local and a non-local aposematic and a non-local cryptic background color and combined them with black spots increasing in size (none, small, medium, large). The major objective was to test if spot size alters the survival rate of differently colored models. Background coloration and spot size were significant predictors of being attacked. However, the interaction between both effects was not. During five trials predators avoided the non-local aposematic color morph and did not discriminate between local aposematic and non-local cryptic models. Spot size and attack rate were negatively linear correlated which suggests that predator selection promotes the evolution of dark spots. We further conclude that spot size matters in a contrasting color pattern and plays an important role in predator avoidance.     

The effects of predator learning, forgetting, and recognition errors on the evolution of warning coloration

This paper demonstrates that the specifics of predator avoidance learning, information loss, and recognition errors may heavily influence the evolution of aposematism. I establish a mathematical model of the change in frequency over time of bright individuals of a distasteful prey species. Warning color spreads through green beard selection as reformulated by Guilford (1990); bright colored forms gain an advantage due to their phenotypic resemblance to other bright forms, which have been sampled by the predator. I use a general classical conditioning model to examine gradual predator learning and forgetting, and then consider the extreme of one-trial learning and no forgetting over time that may occur with very toxic prey. The advantage of conspicuous coloration under these latter conditions depends upon its role in lowering a constant probability of the prey being misidentified and thus mistakenly attacked by a predator, a rarely emphasized factor in the evolution of warning coloration. This constant probability of mistaken attacks can also be interpreted as a constant probability that forgetting has occurred (forgetting does not increase with time) or a periodic decision by the predator to resample avoided prey. I show that when predators learn and forget gradually, as under the general classical conditioning model, it is very difficult for aposematic coloration to become established unless bright individuals cross an often high threshold frequency through chance factors. In contrast, the conditions expected with highly toxic prey promote the evolution of warning coloration more easily, by means from the fixation of very bright mutations to the fixation of successive mutations each of which causes a small increase in a prey's conspicuousness. The results therefore predict that aposematic coloration may have evolved in a different manner in different predator and prey systems. They also suggest that it may be extremely difficult for warning coloration to evolve in more mildly toxic or distasteful prey outside of a mimicry system.     

Higher survival of an aposematic than of a cryptic form of a distasteful bug

Summary An experiment was performed to assess the relative survival of two forms of 5th instar larvae of Lygaeus equestris (Heteroptera, Lygaeidae) — the normal red form, called aposematic, and a mutant grey form, called cryptic — when given to hand-raised great tits (Parus major).Sixteen birds were presented with aposematic larvae and 16 were presented with cryptic larvae in 10 consecutive trials. One attack per trial was allowed. Both larval forms were presented against a background matching the grey larvae, but since both prey types were presented in a specific place known to the predator, detection rate for both was assumed to be unity.Birds learned to avoid both prey types. However, the survival of the aposematic larvae was higher than that of the cryptic ones due to three aspects of predator behaviour: i) a greater initial reluctance to attack, ii) a more rapid avoidance learning, and iii) a lower frequency of killing in an attack, when the prey was aposematic. Moreover, a greater number of birds learned to avoid prey without killing any individual, when the prey was aposematic. This result is considered to be due to prey coloration alone, since, in a separate test, no difference in prey distastefulness could be detected.This experiment shows that individual prey can benefit from being aposematic and indicates that individual selection can be a sufficient explanation for the evolution of aposematic coloration. It was concluded that, since the survivorship was 6.4 times higher for the aposematic prey, it could have a detection rate that is correspondingly higher than the cryptic in order for the two forms to have equal fitness.     

Avoidance of an aposematically coloured butterfly by wild birds in a tropical forest

1. Birds are considered to be the primary selective agents for warning colouration in butterflies, and select for aposematic mimicry by learning to avoid brightly coloured prey after unpleasant experiences. It has long been thought that bright colouration plays an important role in promoting the avoidance of distasteful prey by birds. 2. The hypothesis that warning colouration facilitates memorability and promotes predator avoidance was tested by means of a field experiment using distasteful model butterflies. Artificial butterflies with a Heliconius colour pattern unknown to local birds were generated using bird vision models, either coloured or achromatic, and hung in tree branches in a tropical forest. Two sequential trials were conducted at each site to test avoidance by naïve and experienced predators. 3. There was a significant reduction in predation in the second trial. Also, coloured models were attacked less than achromatic models. Specifically, coloured butterflies were attacked significantly less in the second trial, but there was no significant decrease in predation on achromatic models. 4. The present results imply an important role for colour in enhancing aversion of aposematic butterflies. It has also been demonstrated that previous experience of distasteful prey can lead to enhanced avoidance in subsequent trials, supporting mimicry theory.     

Experienced chicks show biased avoidance of stronger signals: an experiment with natural colour variation in live aposematic prey

An important factor for understanding the evolution of warning coloration in unprofitable prey is the synergistic effect produced by predator generalisation behaviour. Warning coloration can arise and become stabilised in a population of solitary prey if more conspicuous prey benefit from a predator's previous interaction with less conspicuous prey. This study investigates whether domestic chicks (Gallus gallus domesticus) show a biased generalisation among live aposematic prey by using larvae of three species of seed bugs (Heteroptera: Lygaeidae) that are of similar shape but vary in the amount of red in the coloration. After positive experience of edible brownish prey, chicks in two reciprocal experiments received negative experience of either a slightly red or a more red distasteful larva. Attacking birds were then divided into two treatment groups, – one presented with the same prey again, and one presented with either a less red or a more red larva. Birds with only experience of edible prey showed no difference in attack probability of the two aposematic prey types. Birds with experience of the less red prey biased their avoidance so that prey with a more red coloration was avoided to a higher degree, whereas birds with experience of the more red prey avoided prey with the same, but not less red coloration. Thus, we conclude that bird predators may indeed show a biased generalisation behaviour that could select for and stabilise an aposematic strategy in solitary prey. This revised version was published online in July 2006 with corrections to the Cover Date.     

The model of early evolution of aposematic coloration

First stages of evolution of aposematic coloration include a region of negative selection. During these stages, individuals with aberrant coloration remain to be rare, while predators are still not able to associate coloration with unpalatability. The simulation model is proposed, in which this "problematic zone" is overcome by individual selection for the increasing of unpalatable prey conspicuity in a small unisexual population. It is shown that under this assumption aposematic coloration develops within a wide range of parameters such as the cost of unpalatability, the cost of coloring, the survival rate of unpalatable prey after being attacked by na?ve predator, the probability of discovering of differently colored preys by predator as well as the predator's learning rate and memory depth. Thus, the early evolution ofaposematic coloration does not require any unusual or unique set of circumstances; aposematic coloration along with concomitant Bates mimicry inevitably evolve within a wide range of initial conditions. The loss of cryptic coloration by the original form (e.g., due to a change of food preferences, and thereby the structure of a background coloring, changes in habitat structure, color mutations etc.) is one such condition.     

Five species of passerine bird differ in their ability to detect Batesian mimics

Multiple predators affect the evolution of aposematic signals in nature and these predators may substantially differ in terms of ecological and cognitive parameters. However, most experimental studies testing the evolution of Batesian mimics use only a single species of predator (usually the great tit or a domestic chick). Therefore, in the present study, we experimentally tested the responses of five passerine predators to an artificially made Batesian mimic (a cockroach equipped with the warning pattern of the red firebug) with respect to their dietary ecology. Half of the individuals of each species were fed on unmodified roaches before the experiment, whereas the other half were fed with mealworms and thus had no previous experience with roaches. We found that Batesian mimics were better protected than inconspicuous prey against inexperienced great tits and robins alone. The other three bird species showed high level of neophobia; therefore, the effect of warning coloration could not be assessed. We also found that experienced birds attacked a greater number of Batesian mimics compared to inexperienced individuals of all tested species, with the exception of blackcaps. In the great tits, robins, and blue tits, a significant number of experienced birds attacked the Batesian mimic, which was possibly the result of a learned search image for a roach. Our results suggest that using a limited array of predators to describe evolutionary processes forming the diversity of antipredatory strategies of the prey may be biased and need not describe the situation occurring in nature.     

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.     

Aposematism and gregariousness: the combined effect of group size and coloration on signal repellence

Many aposematic species have evolved an aggregated lifestyle, and one possible advantage of grouping in warningly coloured prey is that it makes the aposematic signal more effective by generating a greater aversion in predators. Here we investigate the effect of prey group size on predator behaviour, both when prey are aposematic and when they are not aposematic, to separate the effects of warning coloration and prey novelty. Naive domestic chicks (Gallus gallus domesticus) were presented with either solitary or groups of 3, 9 or 27 live larvae of the aposematic bug Tropidothorax leucopterus. Other naive chicks were presented with larvae of the non-aposematic bug Graptostethus servus either solitary or in groups of 27. Attack probability decreased with increasing group size of aposematic prey, both when birds were naive and when they had prior experience, whereas prey gregariousness did not affect the initial attack probability on the G. servus larvae. In a separate experiment, groups of mealworms were shown to be even more attractive than solitary mealworms to naive chicks. We conclude that the aversiveness of prey grouping in this study can be explained as increased signal repellence of specific prey coloration, in this case a classical warning coloration. These experiments thus support the idea of gregariousness increasing the signalling effect of warning coloration.     

A test of an antipredatory function of conspicuous plastron coloration in hatchling turtles

Bright colorations in animals are sometimes an antipredatory signal meant to startle, warn, or deter a predator from consuming a prey organism. Freshwater turtle hatchlings of many species have bright ventral coloration with high internal contrast that may have an antipredator function. We used visual modeling and field experiments to test whether the plastron coloration of Chrysemys picta hatchlings deters predators. We found that bird predators can easily distinguish hatchling turtles from their backgrounds and can easily see color contrast within the plastron. Raccoons cannot easily discriminate within-plastron color contrast but can see hatchlings against common backgrounds. Despite this, we found that brightly-colored, high contrast, replica turtles were not attacked less than low contrast replica turtles, suggesting that the bright coloration is not likely to serve an antipredatory function in this context. We discuss the apparent lack of innate avoidance of orange coloration in freshwater turtles by predators and suggest that preference and avoidance of colors are context-dependent. Since the bright colors are likely not a signal, we hypothesize that the colors may be caused by pigments deposited in tissue from maternal reserves during development. In most species, these pigments fade ontogenetically but they may have important physiological functions in species that maintain the bright coloration throughout adulthood.     

Predator experience on cryptic prey affects the survival of conspicuous aposematic prey

Initially, aposematism, which is an unprofitable trait, e.g. noxiousness conspicuously advertised to predators, appears to be a paradox since conspicuousness should increase predation by naive predators. However, reluctance of predators for eating novel prey (e.g. neophobia) might balance the initial predation caused by inexperienced predators. We tested the novelty effects on initial predation and avoidance learning in two separate conspicuousness levels of aposematic prey by using a 'novel world' method. Half of the wild great tits (Parus major) were trained to eat cryptic prey prior to the introduction of an aposematic prey, which potentially creates a bias against the aposematic morph. Both prey types were equally novel for control birds and they should not have shown any biased reluctance for eating an aposematic prey. Knowledge of cryptic prey reduced the expected initial mortality of the conspicuous morph to a random level whereas control birds initially ate the conspicuous morph according to the visibility risk. Birds learned to avoid conspicuous prey in both treatments but knowledge of cryptic prey did not increase the rate of avoidance learning. Predators' knowledge of cryptic prey did not reduce the predation of the less conspicuous aposematic prey and additionally predators did not learn to avoid the less conspicuous prey. These results indicate that predator psychology, which was shown as reluctance for attacking novel conspicuous prey, might have been important in the evolution of aposematism.     

Chromaticity in the UV/blue range facilitates the search for achromatically background-matching prey in birds

A large variety of predatory species rely on their visual abilities to locate their prey. However, the search for prey may be hampered by prey camouflage. The most prominent example of concealing coloration is background-matching prey coloration characterized by a strong visual resemblance of prey to the background. Even though this principle of camouflage was recognized to efficiently work in predator avoidance a long time ago, the underlying mechanisms are not very well known. In this study, we assessed whether blue tits (Cyanistes caeruleus) use chromatic cues in the search for prey. We used two prey types that were achromatically identical but differed in chromatic properties in the UV/blue range and presented them on two achromatically identical backgrounds. The backgrounds had either the same chromatic properties as the prey items (matching combination) or differed in their chromatic properties (mismatching combination). Our results show that birds use chromatic cues in the search for mismatching prey, whereupon chromatic contrast leads to a ‘pop-out’ of the prey item from the background. When prey was presented on a matching background, search times were significantly higher. Interestingly, search for more chromatic prey on the matching background was easier than search for less chromatic prey on the matching background. Our results indicate that birds use both achromatic and chromatic cues when searching for prey, and that the combination of both cues might be helpful in the search task.     

Can experienced birds select for Mullerian mimicry?

Field experiments have shown that avian predators in the wildcan select for similarity of warning signals in aposematic prey(Müllerian mimicry) because a common signal is better protectedthan a signal that is novel and rare. The original theory ofMüllerian mimicry assumes that the mechanism promotingmimicry is predator learning; by sharing a signal, the comimicspecies share the mortality that is due to sampling by inexperiencedpredators. Predation events have not been observed in the wild,and learning experiments with naive bird predators in a laboratoryhave not unambiguously shown a benefit of a uniform signal comparedwith different signals. As predators in the field experimentsare likely to be more experienced compared with previous laboratoryexperiments, we studied selection by experienced predators ona novel imperfect mimic. We trained great tits Parus major toavoid artificial aposematic models and subsequently introducedperfect and imperfect mimics at different frequencies. Birdswith prior experience on the models selected against the imperfectmimics that were at a disadvantage also in a memory test conducteda week after their introduction. Selection against the imperfectmimics was antiapostatic. However, the imperfect mimics alsobenefited from some signal generalization to the models andpossibly gained protection because the birds were familiar withthe alternative cryptic prey that was also present. Our resultssuggest that experienced predators might be more important tothe evolution of mimicry than the learning-based theory assumes.     

Field but not lab paradigms support generalisation by predators of aposematic polymorphic prey: the Oophaga histrionica complex

The persistence of novel aposematic forms, and thereby the evolution of aposematic polymorphism, remain intriguing. Novel and rare forms could be disproportionally attacked by predators that already learned to avoid a pre-existing and more common aposematic form. Alternatively, novel forms could be less frequently attacked if predators are reluctant to attack unknown potential prey (neophobia) or if previous learning allows them to generalise and recognise the novel form as toxic. We used colour variation in polymorphic poison frogs (Oophaga histrionica complex) to test whether predators familiar with one aposematic form do generalise their avoidance behaviour to other aposematic forms. To strengthen our inference, we combined a field test of attack rates to local and non-local models with a lab experiment of generalisation capabilities by newly born chicks. Field predators attacked a significantly lower proportion of 529 aposematic compared to 150 cryptic models. Predators co-occurring with the local aposematic form of O. histrionica equally avoided non-local forms, especially in areas where the species was abundant. Forty-two lab chicks learned to discriminate between an aposematic and a cryptic image, but failed to generalise to other aposematic images, even though we tried with six combinations of aposematic forms. To better mimic the situation in the field, we further tested whether chicks trained with a set of four simultaneous aposematic images would generalise better. They failed to learn the discrimination task. Our data contrast with previous field studies on other poison frogs, and support a role for generalisation, and arguably not neophobia, in predator avoidance of novel aposematic forms.     

Teasing apart crypsis and aposematism – evidence that disruptive coloration reduces predation on a noxious toad

Both cryptic and aposematic colour patterns can reduce predation risk to prey. These distinct strategies may not be mutually exclusive, because the impact of prey coloration depends on a predator's sensory system and cognition and on the environmental background. Determining whether prey signals are cryptic or aposematic is a prerequisite for understanding the ecological and evolutionary implications of predator–prey interactions. This study investigates whether coloration and pattern in an exceptionally polymorphic toad, Rhinella alata, from Barro Colorado Island, Panama reduces predation via background matching, disruptive coloration, and/or aposematic signaling. When clay model replicas of R. alata were placed on leaf litter, the model's dorsal pattern – but not its colour – affected attack rates by birds. When models were placed on white paper, patterned and un‐patterned replicas had similar attack rates by birds. These results indicate that dorsal patterns in R. alata are functionally cryptic and emphasize the potential effectiveness of disruptive coloration in a vertebrate taxon.