Fearful symmetry: pattern size and asymmetry affects aposematic signal efficacy

Aposematic animals use anti-predator defence mechanisms such as distastefulness coupled with distinctive odours, sounds, or colour visual signals to predation from domestic chicks we show that the protective value of such visual warning displays is enhanced by increasing size of the signal pattern elements and decreased by pattern asymmetry. These results provide the first experimental evidence that predation may select for individual symmetry of visual warning displays, and concur with earlier demonstrations that asymmetric signals are more difficult to detect, learn, and remember, compared to symmetric signals. Collectively, our findings suggest that prey species possessing warning coloration should be subjected to selection for large and symmetric pattern elements. This revised version was published online in July 2006 with corrections to the Cover Date.     

The protective value of conspicuous signals is not impaired by shape, size, or position asymmetry

Various conspicuous signals in nature promote initial and learnedavoidance by predators. It is widely thought that such signalsare most effective when highly symmetrical in features suchas size and shape, supported by recent laboratory experimentswith domestic chicks and artificial prey. However, no studyhas investigated the effect of asymmetry on conspicuous signalsin a natural setting, where viewing distances, angles, predatorspecies, and light conditions vary and where predators encounterprey sequentially rather than simultaneously. We undertook 2field experiments with artificial gray-scale prey, marked witha pair of white markings presented to wild avian predators,to test the effect of asymmetry on the survival value of conspicuoussignals in the field. Experiment 1 had treatments with symmetricalspots or with spots asymmetrical in area between 5 and 50%.All marked treatments survived better than unmarked controls,but there was no benefit of being symmetrical. Experiment 2tested the effect of possessing markings asymmetrical for shapeor position and any additive effect of these 2 features. Again,symmetry conferred no benefit and targets with markings asymmetricalfor position and/or shape survived equally well as those withsymmetrical arrangements. These findings indicate that asymmetryin warning signals may not be costly to prey in nature or beof less importance compared with other features of the signal,such as color and overall size.     

Great tits (Parus major) searching for artificial prey: implications for cryptic coloration and symmetry

It has been suggested that bilateral symmetry may impose a costfor animals relying on camouflage because symmetric color patternsmight increase the risk of detection. We tested the effect ofsymmetry on crypsis, carrying out a predation experiment withgreat tits (Parus major) and black-and-white–patterned,artificial prey items and background. First, we found that detectiontime was significantly longer for a highly cryptic, asymmetricpattern based on a random sample of the background than forits symmetric variants. Second, we were able to arrange theelements of a prey pattern in a way that the resulting asymmetricpattern was highly cryptic and, furthermore, its symmetric variantwas highly cryptic as well. We conclude that symmetry may imposea substantial cost on cryptic patterns, but this cost variesamong patterns. This suggests that for prey, which predatorstypically view from an angle exposing their symmetry, selectionfor pattern asymmetry may be less important and selection fordecreased detectability cost of symmetry may be more importantthan previously thought. This may help to understand the existenceof so many prey with cryptic, symmetric color patterns.     

Fearful symmetry? Intra-individual comparisons of asymmetry in cryptic vs. signalling colour patterns in butterflies

The signalling role of asymmetry has attracted considerable recent interest among evolutionary biologists. Although it has been studied primarily within the context of sexual selection, symmetry of signals may play a role also in inter-specific communication, such as predator–prey interactions. Both theory and experimental evidence suggest that asymmetry may impair the efficacy of visual warning signals used to deter potential predators, but increase the protective value of non-signalling, cryptic colour patterns used to decrease the risk of detection. Here we tested the prediction from this hypothesis by means of intra-individual comparisons of asymmetry in colour pattern elements in three species of moths (Arctia caja (L.), Noctua orbona (L.), Smerinthus ocellata (L.)) that possess cryptic fore wing patterns and signalling hind wing patterns. Mean asymmetries constituted 4.3% (range 2.1–7.0%) of trait size for colour pattern elements, whereas individual asymmetry levels reached as high as 26%. Asymmetry tended to be somewhat larger in cryptic patterns on fore wings than in signalling patterns on hind wings in five of six comparisons, but in only one case was the difference statistically significant. In addition, pattern elements were somewhat more asymmetric on fore wings also in Saturnia pavonia (L.), which possesses identical signalling eyespots on both fore and hind wings. The relatively low levels of asymmetry also in cryptic patterns imply either that selection does not favour increased asymmetry in cryptic patterns, or that the evolution of pronounced asymmetry is developmentally or genetically constrained.     

Developmental stability and predation success in an insect predator-prey system

I investigated the relationships among developmental stability(as measured by individual bilateral asymmetry values), twomeasures of locomotory performance and predation success inan insect predator-prey system. In this system yellow dungfliesScathophaga stercoraria preyed upon houseflies Musca domesticainlaboratory-controlled conditions. There was no relationshipbetween locomotion and absolute asymmetry or mean size of twomorphological traits (fourth longitudinal wing vein, forelegtibia) in either species. Analysis of single predation trialsindicated that locomotion performance and trait size are notassociated with the probability of predation. However, Muscathat were captured had tibia that were more asymmetric thanMusca that survived. Similarly, Scathophaga that were successfulpredators had more symmetric forelegs than unsuccessful predators.There was no relationship between predation and wing vein asymmetry,which may indicate the importance of terrestrial-based predatoryavoidance tactics in this system. There were no relationshipsbetween morphology or locomotion with predation latency, preyhandling times, or the number of times a prey "escaped" froma predator. The mechanisms behind the relationship between tibiaasymmetry and predation success are discussed. This is the firstexperiment to reveal direct evidence for selection for symmetric,developmentally stable individuals through differential predation     

Non-warning odors trigger innate color aversions--as long as they are novel

Warning signals made by unpalatable insects to potential predatorscommonly target more than one sense: such signals are "multimodal." Pyrazines are odors produced by warningly colored insects whenattacked, and have been shown to interact with food coloration,biasing avian predators against novel and typically aposematicfood. However, at present it is not known whether this is anadaptation by prey to exploit a general feature of avian psychology,or an evolutionary response by birds to enhance their avoidanceof unpalatable prey. Here we investigate the effect of otherodors on the innate responses of naive domestic chicks (Gallusgallus domesticus) to food that is of novel color, or of acolor that is associated with warning coloration, yellow. Inthe first experiment, we demonstrate that natural and artificialodors that have no association with aposematism in the wildcan produce biases against both novel colored foods and yellowcolored foods. In a second experiment, we also show that odor novelty is vital for eliciting such effects. These results supportthe idea that warning odors have evolved in response to preexistingpsychological biases against novel odors in predators, ratherthan predators evolving specific responses against odors associatedwith unpalatable prey.     

Camouflage that is spot on! Optimization of spot size in prey-background matching

Camouflage is a key predation prevention mechanism. The most intuitive camouflage strategy is background matching, where a prey resembles the colour and pattern of its background. Spots (e.g. geometric ‘elements’ that constitute a pattern) are a common feature on the body of prey, but the effect of their size in relation to elements in the background is rarely examined in camouflage studies. Here, we test the survivorship of computer generated prey possessing patterns of elements grouped into eight size classes on backgrounds composed of elements of the same eight size classes. All 64 possible combinations were presented to human volunteers (n = 10) acting as ‘predators’ in a computer simulation. As hypothesised, prey survivorship was high when the prey-background element size difference was low. We found significant asymmetry, however, in survivorship pattern: prey morphs with elements larger than those of the backgrounds were harder to detect than morphs with elements smaller than those of the backgrounds. When testing for potential trade-offs we determined that, in a habitat consisting of an equal proportion of two backgrounds with a large element size difference between them, net survivorship of specialist prey morphs (same element size as one of the backgrounds) was similar to that of generalist morphs (intermediate element size). When the two backgrounds were less distinctive, i.e. reduced element size difference between the backgrounds, generalist prey morphs achieved significantly better net survivorship than specialists.     

The role of size and colour pattern in protection of developmental stages of the red firebug (Pyrrhocoris apterus) against avian predators

We investigated how predator/prey body‐size ratio and prey colour pattern affected efficacy of prey warning signals. We used great and blue tits (Parus major and Cyanistes caeruleus), comprising closely related and ecologically similar bird species differing in body size, as experimental predators. Two larval instars and adults of the unpalatable red firebug (Pyrrhocoris apterus), differing in body size and/or coloration, were used as prey. We showed that prey body size did not influence whether a predator attacked the prey or not during the first encounter. However, smaller prey were attacked, killed, and eaten more frequently in repetitive encounters. We assumed that body size influences the predator through the amount of repellent chemicals better than through the amount of optical warning signal. The larger predator attacked, killed and ate all forms of firebug more often than the smaller one. The difference between both predators was more pronounced in less protected forms of firebug (chemically as well as optically). Colour pattern also substantially affected the willingness of predators to attack the prey. Larval red–black coloration did not provide a full‐value warning signal, although a similarly conspicuous red‐black coloration of the adults reliably protected them. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 890–898.     

Deceptive color signaling in the night: a nocturnal predator attracts prey with visual lures

The role color signaling plays in the nocturnal condition ofthe terrestrial ecosystem is currently poorly understood. Ingeneral, arthropods active in the night are inconspicuouslycolored. However, in addition to inconspicuously colored dorsum,several genera of nocturnal orb spiders also have conspicuousventrum spots. In this study, we tested whether the inconspicuouslycolored dorsum functioned to reduce spiders‘ visibilityto diurnal predators while the spiders were perching on barkwith ventrum spots well concealed. We also evaluated when spiderssit on webs with conspicuous ventrum spots fully exposed, wouldthey serve as deceptive color signals to lure visually orientatednocturnal prey. We first quantified how diurnal hymenopteranpredators viewed the dorsum and nocturnal lepidopteran preyviewed the ventrum spots of nocturnal orb spiders Neoscona punctigeraby calculating color contrasts. The diurnal color contrast ofspiders’ dorsum when viewed by hymenopteran insects againstbark was lower than the discrimination threshold. However, thenocturnal color contrasts of spiders‘ ventrum spots whenviewed by moths were high. In the field, webs with N. punctigeraintercepted significantly more insects than those without. Whenthe color signal of ventrum spots was altered by paint, webs’prey interception rates decreased significantly. These resultsdemonstrate that even in the nocturnal condition certain terrestrialorganisms exhibit visual lures to attract prey.     

Warning coloration associated with nematocyst-based defences in aeolidiodean nudibranchs

This study examines the mechanisms of aposematism (unprofitabilityof prey combined with a conspicuous signal) in the aeolidioideanCratena peregrina (Gmelin, 1791). We investigated if marinefish avoid attacking aeolidioidean nudibranchs, which are anunprofitable group of prey for most predators. We analysed theinteraction between aeolids and predatory fish in laboratoryand field assays, with both live aeolids and artificial models.In the first experiment, we offered normal and blue-dyed C.peregrina to fish in the field. The number of attacks by fishwas independent of the density of the prey, albeit the normalaeolids were attacked less frequently than the blue ones. Thefact that all normal C. peregrina survived, whereas 12–20%of the blue aeolids died after fish attacks, suggests that aposematiccoloration provides a selective advantage against fish predators.Field and laboratory assays with artificial aeolids were employedto test the effects of different factors (number of cerata,colour pattern, nematocysts), or a combination of factors, onfish learning. Fish learned to avoid unpalatable models withthe colour pattern of C. peregrina. After three to four trainingsessions with unprofitable models, fish avoided profitable modelswith the same colour pattern. Our results suggest that the colourpattern of C. peregrina combined with the presence of dorsalappendages and nematocysts make fish avoid aeolids. (Received 22 January 2004; accepted 18 August 2006)     

Competitive Asymmetry Reduces Spatial Effects on Size-Structure Dynamics in Plant Populations

The growth of each individual in plant populations was simulatedby a spatial competition model for five density levels and fourdifferent spatial distribution patterns of individuals, varyingfrom highly clumped to regular. The simulation results wereanalysed using the diffusion model for evaluating the effectsof density and distribution pattern on the size-structure dynamicsin relation to the degree of competitive asymmetry. At low densities,changes in statistics of plant weight over time such as mean,coefficient of variation, skewness, and Box-Cox-transformedkurtosis differed greatly among spatial patterns, irrespectiveof the degree of competitive asymmetry. In completely symmetriccompetition, the spatial effect on size-structure dynamics remainedrelatively large irrespective of densities, although mean plantweight became similar among the spatial patterns with increasingdensity. However, the spatial effect diminished with increaseddensity in strongly asymmetric competition, when similar sizedistributions were realized irrespective of the spatial patterns.Therefore, it was concluded that: (1) irrespective of the degreeof competitive asymmetry, spatial pattern is important for size-structuredynamics at low densities; (2) spatial pattern is nearly immaterialunder strongly asymmetric competition at high densities; and(3) under crowded conditions, neighbourhood effects are muchmore apparent at the population level in less asymmetric competition.These processes and outcomes are linked to the forms of thefunctions of mean growth rate of individuals [G(t,x) function]and variance in growth rate [D(t,x) function]. These functionsare variable depending on the spatial pattern under symmetriccompetition, but are rather stable under strongly asymmetriccompetition at high densities irrespective of the spatial patterns.Therefore, size structure under strongly asymmetric competitioncan be regarded as a stable system, whereas that under symmetriccompetition is regarded as a variable system in relation tothe spatial pattern and process. From this, it was inferredthat: (1) the goodness-of-fit of spatial competition modelsfor crowded plant populations is higher in less asymmetric competition;and (2) higher species diversity in plant communities is associatedwith the lower degree of competitive asymmetry.Copyright 1994,1999 Academic Press Asymmetric competition, diffusion model, neighbourhood effect, size-structure stability, spatial competition model, spatial distribution pattern, species diversity, symmetric competition     

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.     

Antipredatory function of head shape for vipers and their mimics

Most research into the adaptive significance of warning signals has focused on the colouration and patterns of prey animals. However, behaviour, odour and body shape can also have signal functions and thereby reduce predators' willingness to attack defended prey. European vipers all have a distinctive triangular head shape; and they are all venomous. Several non-venomous snakes, including the subfamily Natricinae, commonly flatten their heads (also known as head triangulation) when disturbed. The adaptive significance of this potential behavioural mimicry has never been investigated.We experimentally tested if the triangular head shape typical of vipers offers protection against predation. We compared the predation pressure of free-ranging predators on artificial snakes with triangular-shaped heads against the pressure on replicas with narrow heads. Snakes of both head types had either zigzag patterned bodies, typical of European vipers, or plain (patternless) bodies. Plain snakes with narrower Colubrid-like heads suffered significantly higher predation by raptors than snakes with triangular-shaped heads. Head shape did not, however, have an additive effect on survival in zigzag-patterned snakes, suggesting that species which differ from vipers in colouration and pattern would benefit most from behavioural mimicry. Our results demonstrate that the triangular head shape typical of vipers can act as a warning signal to predators. We suggest that head-shape mimicry may be a more common phenomenon among more diverse taxa than is currently recognised.     

Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color

Predator-induced defenses are well studied in plants and invertebrate animals, but have only recently been recognized in vertebrates. Gray treefrog (Hylachrysoscelis) tadpoles reared with predatory dragonfly (Aeshnaumbrosa) larvae differ in shape and color from tadpoles reared in the absence of dragonflies. By exposing tadpoles to tail damage and the non-lethal presence of starved and fed dragonflies, we determined that these phenotypic differences are induced by non-contact cues present when dragonflies prey on Hyla. The induced changes in shape are in the direction that tends to increase swimming speed; thus, the induced morphology may help tadpoles evade predators. Altering morphology in response to predators is likely to influence interactions with other species in the community as well. Received: 17 April 1996 / Accepted: 18 September 1996     

Predation on snakes of Argentina: Effects of coloration and ring pattern on coral and false coral snakes

The occurrence of coral snake coloration among unrelated venomous and non‐venomous snake species has often been explained in terms of warning coloration and mimicry. In Argentina, no field tests have been conducted to confirm this mimetic association between one venomous coral species (Micrurus phyrrocryptus, Elapidae) and two non‐venomous snake species with a similar color pattern (Lystrophis pulcher and Oxyrhopus rhombifer, Colubridae). The aims of this work were to test for the possible aposematic or cryptic function of the ring pattern and coloration of coral snakes and false coral snakes from central Argentina, and to analyse whether the pattern is effective throughout the year. Predation on snakes was estimated by using non‐toxic plasticine replicas of ringed venomous and non‐venomous snakes and unbanded green snakes placed along transects in their natural habitat during the dry and rainy season. Ringed color pattern was attacked by predators despite the background color. One of the replica types was attacked more than expected during the dry season, suggesting that both shape and width of rings may influence the choice by predators. The reaction of predators towards replicas that mimic snake species with ringed patterns is independent of the geographical region, and we can conclude that mimicry characteristics are quite general when the true models are present in the area.     

Effect of sex and bright coloration on survival and predator‐induced wing damage in an aposematic lantern fly with startle display

1. Aposematic coloration in prey promotes its survival by conspicuously advertising unpalatability to predators. Although classical examples of aposematic signals involve constant presentation of a signal at a distance, some animals suddenly display warning colours only when they are attacked. 2. Characteristics of body parts suddenly displayed, such as conspicuous coloration or eyespot pattern, may increase the survival of the prey by startling the predator, and/or by signalling unpalatability to the predators at the moment of attack. 3. The adaptive value of such colour patterns suddenly displayed by unpalatable prey has not been studied. We experimentally blackened the red patch in the conspicuous red–white–black hindwing pattern displayed by an unpalatable insect Lycorma delicatula White (Hemiptera: Fulgoridae) in response to predator's attack. 4. There was no evidence that the presence of the red patch increased prey survival over several weeks. We hypothesise that predators generalised from the red–white–black patches on the hindwings of unpalatable L. delicatula to any similar wing display as a signal of unpalatability. Because a higher proportion of males than females stay put at their resting sites, displaying their wings in response to repeated attacks by predators, wing damage was more frequent in males than in females. 5. To our knowledge, this is the first experimental test of an adaptive role of aposematic signals presented by unpalatable prey during sudden displays triggered by direct predatory attack.     

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.     

Conspicuous visual signals do not coevolve with increased body size in marine sea slugs

Many taxa use conspicuous colouration to attract mates, signal chemical defences (aposematism) or for thermoregulation. Conspicuousness is a key feature of aposematic signals, and experimental evidence suggests that predators avoid conspicuous prey more readily when they exhibit larger body size and/or pattern elements. Aposematic prey species may therefore evolve a larger body size due to predatory selection pressures, or alternatively, larger prey species may be more likely to evolve aposematic colouration. Therefore, a positive correlation between conspicuousness and body size should exist. Here, we investigated whether there was a phylogenetic correlation between the conspicuousness of animal patterns and body size using an intriguing, understudied model system to examine questions on the evolution of animal signals, namely nudibranchs (opisthobranch molluscs). We also used new ways to compare animal patterns quantitatively with their background habitat in terms of intensity variance and spatial frequency power spectra. In studies of aposematism, conspicuousness is usually quantified using the spectral contrast of animal colour patches against its background; however, other components of visual signals, such as pattern, luminance and spectral sensitivities of potential observers, are largely ignored. Contrary to our prediction, we found that the conspicuousness of body patterns in over 70 nudibranch species decreased as body size increased, indicating that crypsis was not limited to a smaller body size. Therefore, alternative selective pressures on body size and development of colour patterns, other than those inflicted by visual hunting predators, may act more strongly on the evolution of aposematism in nudibranch molluscs.     

Conspicuousness,color resemblance,and toxicity in geographically diverging mimicry: The pan‐Amazonian frog Allobates femoralis

Predation risk is allegedly reduced in Batesian and Müllerian mimics, because their coloration resembles the conspicuous coloration of unpalatable prey. The efficacy of mimicry is thought to be affected by variation in the unpalatability of prey, the conspicuousness of the signals, and the visual system of predators that see them. Many frog species exhibit small colorful patches contrasting against an otherwise dark body. By measuring toxicity and color reflectance in a geographically variable frog species and the syntopic toxic species, we tested whether unpalatability was correlated with between‐species color resemblance and whether resemblance was highest for the most conspicuous components of coloration pattern. Heterospecific resemblance in colorful patches was highest between species at the same locality, but unrelated to concomitant variation in toxicity. Surprisingly, resemblance was lower for the conspicuous femoral patches compared to the inconspicuous dorsum. By building visual models, we further tested whether resemblance was affected by the visual system of model predators. As predicted, mimic‐model resemblance was higher under the visual system of simulated predators compared to no visual system at all. Our results indicate that femoral patches are aposematic signals and support a role of mimicry in driving phenotypic divergence or mimetic radiation between localities.     

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.