Warning signals are seductive: Relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies

Visual signaling in animals can serve many uses, including predator deterrence and mate attraction. In many cases, signals used to advertise unprofitability to predators are also used for intraspecific communication. Although aposematism and mate choice are significant forces driving the evolution of many animal phenotypes, the interplay between relevant visual signals remains little explored. Here, we address this question in the aposematic passion‐vine butterfly Heliconius erato by using color‐ and pattern‐manipulated models to test the contributions of different visual features to both mate choice and warning coloration. We found that the relative effectiveness of a model at escaping predation was correlated with its effectiveness at inducing mating behavior, and in both cases wing color was more predictive of presumptive fitness benefits than wing pattern. Overall, however, a combination of the natural (local) color and pattern was most successful for both predator deterrence and mate attraction. By exploring the relative contributions of color versus pattern composition in predation and mate preference studies, we have shown how both natural and sexual selection may work in parallel to drive the evolution of specific animal color patterns.     

Acoustic and visual adaptations to predation risk: a predator affects communication in vocal female fish

Predation is an important ecological constraint that influences communication in animals. Fish respond to predators by adjusting their visual signaling behavior, but the responses in calling behavior in the presence of a visually detected predator are largely unknown. We hypothesize that fish will reduce visual and acoustic signaling including sound levels and avoid escalating fights in the presence of a predator. To test this we investigated dyadic contests in female croaking gouramis (Trichopsis vittata, Osphronemidae) in the presence and absence of a predator (Astronotus ocellatus, Cichlidae) in an adjoining tank. Agonistic behavior in T. vittata consists of lateral (visual) displays, antiparallel circling, and production of croaking sounds and may escalate to frontal displays. We analyzed the number and duration of lateral display bouts, the number, duration, sound pressure level, and dominant frequency of croaking sounds as well as contest outcomes. The number and duration of lateral displays decreased significantly in predator when compared with no-predator trials. Total number of sounds per contest dropped in parallel but no significant changes were observed in sound characteristics. In the presence of a predator, dyadic contests were decided or terminated during lateral displays and never escalated to frontal displays. The gouramis showed approaching behavior toward the predator between lateral displays. This is the first study supporting the hypothesis that predators reduce visual and acoustic signaling in a vocal fish. Sound properties, in contrast, did not change. Decreased signaling and the lack of escalating contests reduce the fish’s conspicuousness and thus predation threat.     

The behavioral context of visual displays in common marmosets (Callithrix jacchus)

Communication is important in social species, and may occur with the use of visual, olfactory or auditory signals. However, visual communication may be hampered in species that are arboreal have elaborate facial coloring and live in small groups. The common marmoset fits these criteria and may have limited visual communication. Nonetheless, some (contradictive) propositions concerning visual displays in the common marmoset have been made, yet quantitative data are lacking. The aim of this study was to assign a behavioral context to different visual displays using pre–post‐event‐analyses. Focal observations were conducted on 16 captive adult and sub‐adult marmosets in three different family groups. Based on behavioral elements with an unambiguous meaning, four different behavioral contexts were distinguished: aggression, fear, affiliation, and play behavior. Visual displays concerned behavior that included facial expressions, body postures, and pilo‐erection of the fur. Visual displays related to aggression, fear, and play/affiliation were consistent with the literature. We propose that the visual display “pilo‐erection tip of tail” is related to fear. Individuals receiving these fear signals showed a higher rate of affiliative behavior. This study indicates that several visual displays may provide cues or signals of particular social contexts. Since the three displays of fear elicited an affiliative response, they may communicate a request of anxiety reduction or signal an external referent. Concluding, common marmosets, despite being arboreal and living in small groups, use several visual displays to communicate with conspecifics and their facial coloration may not hamper, but actually promote the visibility of visual displays. Am. J. Primatol. 75:1084–1095, 2013. © 2013 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.     

Multiple behavioral contexts of a melanized tail display in a desert lizard

Conspicuous color displays in animals are often studied in the context of how they communicate an individual's reproductive value, ability to escape capture, or overall health. The study of sexual dichromatism often focuses on the evolution of male display traits balanced between detectability and mate acquisition, representing constraints stemming from both natural and sexual selection. Melanistic coloration and melanin color patterns play important roles in both intraspecific and interspecific signaling in animals; as melanin serves multiple purposes in organismal biology, the evolution of melanin-based visual displays might not be restricted to a single behavioral or ecological context. Here, we examine the behavioral contexts of the conspicuous melanin-based tail display in the greater earless lizard (Cophosaurus texanus), asking if this melanized tail pattern is associated with (a) female association preference of males varying in the concentration of melanin, (b) individual locomotor performance capacity, and (c) thermal ecology. We found the amount of tail melanin is linked with both locomotor performance and female association preference, with greater concentrations of melanin predicting the evolution of faster performance capacities and females preferring males with more discrete melanin bars. We found limited support that differences in melanin are linked with thermoregulation or thermal ecology. Overall, we find that multiple behavioral contexts shape the evolution of this melanized display trait. We conclude that behavioral constraints stemming from both natural and sexual selection can interact synergistically to favor the evolution and expression of a melanistic visual display, even in potentially costly ecological contexts.     

Negative Association Between Conspicuous Visual Display and Chemosensory Behavior in Two Phrynosomatid Lizards

Communication in one sensory modality can influence communication in others. Lizards in many phrynosomatid species use primarily visual but also chemical signals. The striped plateau lizard, Sceloporus virgatus , exhibits evolutionary loss of a male color signal that in many species is used during aggressive postural displays towards conspecific males. These patches are used similarly in Urosaurus , the sister genus to Sceloporus . We compared a species in which a color signal has been lost, S. virgatus , to a species retaining the ancestral character state of blue abdominal display patches, Urosaurus ornatus , the common tree lizard, to test two hypotheses: (i) conspicuous postural displays that reveal the abdominal patch location are used less in the species that has lost the color patches; and (ii) potential chemical signals are used more in the species with the color loss. We analyzed both visual display behavior (push-up, full-show) and chemosensory behavior (tongue flick and nose tap) of male lizards following their introduction to a resident conspecific male in his home terrarium. Resident males performed very low rates of all behaviors, but intruders exhibited sufficient behavior for analysis.
Supporting the first hypothesis, S. virgatus were less likely than U. ornatus to perform full-show, a display that reveals abdominal skin. Male S. virgatus were more likely to perform push-up than U. ornatus , although S. virgatus performed push-up infrequently. Push-up is a postural display that does not specifically reveal the abdominal patch location. Supporting the second hypothesis, S . virgatus were more likely to perform chemosensory behaviors and performed them at a greater rate than did U. ornatus . Work comparing more closely related species is warranted to determine whether a negative association between conspicuous visual displays and chemosensory behavior is a general pattern.     

Generalization of predator recognition: Velvet geckos display anti-predator behaviours in response to chemicals from non-dangerous elapid snakes

Many prey species detect chemical cues from predators and modify their behaviours in ways that reduce their risk of predation. Theory predicts that prey should modify their anti-predator responses according to the degree of threat posed by the predator. That is, prey should show the strongest responses to chemicals of highly dangerous prey, but should ignore or respond weakly to chemicals from non-dangerous predators. However, if anti-predator behaviours are not costly, and predators are rarely encountered, prey may exhibit generalised antipredator behaviours to dangerous and non-dangerous predators. In Australia, most elapid snakes eat lizards, and are therefore potentially dangerous to lizard prey. Recently, we found that the nocturnal velvet gecko Oedura lesueurii responds to chemicals from dangerous and non-dangerous elapid snakes, suggesting that it displays gen-eralised anti-predator behaviours to chemicals from elapid snakes. To explore the generality of this result, we videotaped the be-haviour of velvet geckos in the presence of chemical cues from two small elapid snakes that rarely consume geckos: the nocturnal golden-crowned snake Cacophis squamulosus and the diurnal marsh snake Hemiaspis signata. We also videotaped geckos in tri-als involving unsceted cards (controls) and cologne-scented cards (pungency controls). In trials involving Cacophis and Hemi-aspis chemicals, 50% and 63% of geckos spent long time periods (> 3 min) freezing whilst pressed flat against the substrate, re-spectively. Over half the geckos tested exhibited anti-predator behaviours (tail waving, tail vibration, running) in response to Ca-cophis (67%) or Hemiaspis (63%) chemicals. These behaviours were not observed in control or pungency control trials. Our re-sults support the idea that the velvet gecko displays generalised anti-predator responses to chemical cues from elapid snakes. Generalised responses to predator chemicals may be common in prey species that co-occur with multiple, ecologically similar, dangerous predators.     

Managing predators: The influence of kangaroo rat antipredator displays on sidewinder rattlesnake hunting behavior

Upon sensing predators in their vicinity, many prey species perform antipredator displays that are thought to provide information to the predator that deters it from attacking (predator‐deterrent signals). These displays can be complex, incorporating a variety of signaling elements as well as direct physical harassment of the predator. Although the display behaviors in these communication systems are often well characterized, evidence of the efficacy of these displays in deterring predators is limited due to the challenges associated with studying free‐ranging predators. Here, we examine how the anti‐snake signals of the desert kangaroo rat (Dipodomys deserti) influence the ambush hunting behaviors of sidewinder rattlesnakes (Crotalus cerastes). We found that, although desert kangaroo rats incorporate a number of signal elements into their antipredator display, only sand kicking behavior was a significant factor in motivating sidewinder rattlesnakes to cease hunting: high rates of sand kicking led to early abandonment of ambush coils. These results indicate that anti‐snake displays of small mammals may be especially effective at mitigating the threat posed by rattlesnakes when those displays incorporate physical harassment as well as signaling.     

Visual fields, eye movements, and scanning behavior of a sit-and-wait predator, the black phoebe (Sayornis nigricans)

Foraging mode influences the dominant sensory modality used by a forager and likely the strategies of information gathering used in foraging and anti-predator contexts. We assessed three components of visual information gathering in a sit-and-wait avian predator, the black phoebe (Sayornis nigricans): configuration of the visual field, degree of eye movement, and scanning behavior through head-movement rates. We found that black phoebes have larger lateral visual fields than similarly sized ground-foraging passerines, as well as relatively narrower binocular and blind areas. Black phoebes moved their eyes, but eye movement amplitude was relatively smaller than in other passerines. Black phoebes may compensate for eye movement constraints with head movements. The rate of head movements increased before attacking prey in comparison to non-foraging contexts and before movements between perches. These findings suggest that black phoebes use their lateral visual fields, likely subtended by areas of high acuity in the retina, to track prey items in a three-dimensional space through active head movements. These head movements may increase depth perception, motion detection and tracking. Studying information gathering through head movement changes, rather than body posture changes (head-up, head-down) as generally presented in the literature, may allow us to better understand the mechanisms of information gathering from a comparative perspective.     

Why do curly tail lizards (genus Leiocephalus) curl their tails? An assessment of displays toward conspecifics and predators

Animal display behaviors are used to convey specific messages to other animals, including potential mates, rivals, and predators. However, because these different types of interactions can be mediated by a single behavioral display, or conversely, multiple signals can be used to convey one specific message, interpretation of any particular behavioral display can be difficult. Leiocephalus lizards (i.e., curly tails) provide an excellent opportunity to study the use of display behaviors across multiple contexts. Previous research has demonstrated that the use of tail curling in these lizards is associated with predation risk, but less is known regarding the use of this behavior in social interactions with conspecifics. The goal of this study was to determine the extent to which tail curling display behavior is used to mediate both social and predatory interactions in two species, Leiocephalus barahonensis and L. carinatus. We found that in lizards of both species, tail curling was used in interactions with both conspecifics and potential (human) predators. However, tail curl intensity did not differ between lizards involved in social encounters and solitary lizards, although L. barahonensis lizards performed more headbobs during social than non‐social observations. Further, L. carinatus lizards exhibited greater intensity of tail curling upon fleeing from a human predator than during observations in which individuals interacted with conspecifics, and lizards that exhibited tighter tail curls fled from predators for a longer distance. Finally, tail curl intensity was not correlated with headbob displays in either species, suggesting that these two components of display communicate different information. Our results suggest that tail curling displays, while consistently a component of interactions with potential predators, are not a necessary component of social interactions. These data contribute to a more complete understanding of how and why visual signals evolve for use in communication across multiple contexts.     

Tail Autotomy Plays No Important Role in Influencing Locomotor Performance and Anti‐Predator Behavior in a Cursorial Gecko

We used the frog‐eyed sand gecko (Teratoscincus scincus) as a model system to evaluate the locomotor costs of tail loss, and to examine whether tailless geckos use alternative anti‐predator behavior to compensate for the costs of tail loss. Of the 16 field‐captured geckos, eight were used as experimental animals and the remaining ones as controls. Locomotor performance, activity level and anti‐predator behavior were measured for experimental geckos before and after the tail‐removing treatment. Control geckos never undergoing the tail‐removing manipulation were measured to serve as controls for the measurements taken at the same time for experimental geckos. Experimental geckos did not differ from controls in activity level before they underwent the tail‐removing manipulation, but became less active thereafter. The mean locomotor stamina of tailless geckos was reduced by about 30% of the mean value for tailed ones. However, as the maximum stamina predicted from the laboratory trials is seldom required in nature, we expect that the costs associated with the reduced locomotor stamina may be relatively minor in T. scincus. All other examined locomotor (overall speed, maximal speed and stride length) and behavioral (distance to refuge, approach distance and flight distance) traits were not affected by the tail‐removing manipulation. Overall, our results suggest that tail autotomy plays no important role in influencing locomotor performance and anti‐predator behavior in lizards where the tail has no direct role in locomotion but is used to direct predatory strikes away from the torso.     

DIVERSIONARY DISPLAY

.The theories which have been advanced to explain the origin of the various forms of distraction display are considered and found to be inadequate. It is suggested that distraction displays have arisen through the "displacement" of components from other behaviour contexts, particularly threat and epigamic display, which have become ritualized into new behaviour-patterns with survival value.     

Anti-Predator Signals as Advertisements: Evidence in White-Throated Magpie-Jays

Calls and displays elicited by predators usually function as alarms or to inform predators of their detection. However, predator encounters may afford some individuals the opportunity to demonstrate quality or signal their availability. Here, I report on a class of vocal signals produced in predator-elicited displays that share many characteristics with sexually selected song. White-throated magpie-jays ( Calocitta formosa ) display at low-threat predators while producing 'loud display calls' (LDCs). I use this term because the calls occur primarily in two display contexts (see below) though occasionally in other contexts as well. Such calls and displays are primarily produced by males, and also occur in one other context, at dawn. Playback experiments showed that despite being elicited by predators, males were more likely than females to respond to LDCs, and more likely to respond when their mate was fertile. Over 134 different call types were produced in over 200 displays by 34 males; the largest minimum repertoire size was 67. Presentations of taxidermic raptor mounts elicited some LDCs, but fewer calls and lower diversity than at dawn or in predator approach displays. The male bias and high diversity suggest that LDCs are an outcome of intersexual selection, while their elicitation by predators suggests an alarm function. I propose that male magpie-jays use predator encounters as opportunities to advertise their presence and availability as mates; they use LDCs as songs. Such a communication system seems to have been favored by the unusual social system of magpie-jays, in which female groups defend territories and males have little opportunity to defend resources for mate attraction, forcing them to advertise when females are paying the most attention, during predator encounters.     

Predator response to the coloured eyespots and defensive posture of Colombian four-eyed frogs

Deimatic displays, where sudden changes in prey appearance elicit aversive predator reactions, have been suggested to occur in many taxa. These (often only putative) displays frequently involve different components that may also serve antipredator functions via other mechanisms (e.g., mimicry, warning signalling, body inflation). The Colombian four-eyed frog, Pleurodema brachyops, has been suggested to gain protection against predation through putative deimatic displays where they inflate and elevate the posterior part of their body revealing eye-like colour markings. We exposed stationary artificial frogs to wild predators to test whether the two components (eyespot/colour markings, defensive posture) of their putative deimatic display, and their combination, provide protection from predation without the sudden change in appearance. We did not detect any obvious additive effect of defensive posture and eyespots/colour markings on predation risk, but found a marginally significant trend for model frogs in the resting posture to be less attacked when displaying eyespots/colour markings than when they were not, suggesting that the presence of colour markings/eyespots may provide some protection on its own. Additionally, we found that models in a resting posture were overall more frequently attacked on the head than models in a defensive posture, indicating that a defensive posture alone could help redirect predator attacks to non-vital parts of the body. The trends found in our study suggest that the different components of P. brachyops' coloration may serve different functions during a deimatic display, but further research is needed to elucidate the role of each component when accompanied by sudden prey movement.     

Evolution of Anoline Lizard Display Behavior

Based on my conceptual framework of anoline display behavior,I am suggesting the following evolutionary trends. Lateral presentationduring display was probably promoted by monocular vision. Alongwith lateral presentation, postures evolved to increase lateraloutline. These postures which magnified body size were probablyof selective advantage within aggressive social contexts sincelarger animals tend to dominate smaller ones through bluff.Body movement evolved along with lateral orientation and size-enhancingpostures. These movements would be most effective if they complementedlateral orientation. Effectors available for such movementswere primarily pre-adapted for vertical motion. The patternsof movement generated were probably simple oscillatory bobbingmovements by the head which were weakly stereotyped, interspecificallysimilar, appearing in many contexts, and having a weakly definedinformation content. Events having selective advantage for speciesrecognition promoted stereotypy of bobbing behavior into species-uniquedisplays; each species had its unique signature display whichserved in a manifold communicatory capacity. The signature displayappeared in assertion, courtship, and challenge contexts. Itsinformation content varied depending upon context and recipientof the display (e.g., male or female). Besides the stereotypedaspects of the display, certain features remained variable withpotential information significance. Core variability (see text)promotes individual recognition and may be the origin of newunique display patterns as sibling species emerge. Display modifiers(see text) are variable display features shared by members ofa population (many being shared interspecifically) that providea graded appearance to display performance; modifiers can indicatelevel of arousal and facilitate interspecific communication.For some species display repertoire size seems to have evolvedfrom a single display (signature display) to repertoires ofmultiple displays; these subsequent displays are generally restrictedto aggressive interactions.     

Inferring Predator Behavior from Attack Rates on Prey-Replicas That Differ in Conspicuousness

Behavioral ecologists and evolutionary biologists have long studied how predators respond to prey items novel in color and pattern. Because a predatory response is influenced by both the predator’s ability to detect the prey and a post-detection behavioral response, variation among prey types in conspicuousness may confound inference about post-prey-detection predator behavior. That is, a relatively high attack rate on a given prey type may result primarily from enhanced conspicuousness and not predators’ direct preference for that prey. Few studies, however, account for such variation in conspicuousness. In a field experiment, we measured predation rates on clay replicas of two aposematic forms of the poison dart frog Dendrobates pumilio, one novel and one familiar, and two cryptic controls. To ask whether predators prefer or avoid a novel aposematic prey form independently of conspicuousness differences among replicas, we first modeled the visual system of a typical avian predator. Then, we used this model to estimate replica contrast against a leaf litter background to test whether variation in contrast alone could explain variation in predator attack rate. We found that absolute predation rates did not differ among color forms. Predation rates relative to conspicuousness did, however, deviate significantly from expectation, suggesting that predators do make post-detection decisions to avoid or attack a given prey type. The direction of this deviation from expectation, though, depended on assumptions we made about how avian predators discriminate objects from the visual background. Our results show that it is important to account for prey conspicuousness when investigating predator behavior and also that existing models of predator visual systems need to be refined.     

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.     

Leaf‐footed bugs possess multiple hidden contrasting color signals,but only one is associated with increased body size

Antipredatory displays that incorporate hidden contrasting coloration are found in a variety of different animals. These displays are seen in organisms that have drab coloration at rest, but when disturbed reveal conspicuous coloration. Examples include the bright abdomens of mountain katydids and the colorful underwings of hawk moths. Such hidden displays can function as secondary defenses, enabling evasion of a pursuant predator. To begin to understand why some species have these displays while others do not, we conducted phylogenetic comparative analyses to investigate factors associated with the evolution of hidden contrasting coloration in leaf‐footed bugs. First, we investigated whether hidden contrasting coloration was associated with body size because these displays are considered to be more effective in larger organisms. We then investigated whether hidden contrasting coloration was associated with an alternative antipredatory defense, in this case rapid autotomy. We found that leaf‐footed bugs with hidden contrasting coloration tended to autotomize more slowly, but this result was not statistically significant. We also found that the presence of a body size association was dependent upon the form of the hidden color display. Leaf‐footed bugs that reveal red/orange coloration were the same size, on average, as species without a hidden color display. However, species that reveal white patches on a black background were significantly larger than species without a hidden color display. These results highlight the diversity of forms that hidden contrasting color signal can take, upon which selection may act differently.     

Display Behavior in Tortoises

When compared to lizards or snakes, signals related to warningand threat are not very important in land tortoises. Withinsocial and sexual contexts, tactile and chemical signals seemmore important than visual, and certainly than auditor)' ones.Color patterns are rarely, if ever, sexually discriminatory.Seasonal color differences are rare. In general, positionalsignals are rather limited, chiefly because of the shell. However,shell positional changes are an important part of the visualand tactile signal repertory of all land tortoises. Head movementsare also important in several groups. Audible signals are poorlydeveloped. They are largely concerned with courtship and theirrole is not understood. Chemical signals are pronounced, especiallyin displays related to sex identification, largely based onscents associated with the cloaca. Tactile displays are importantparticularly during courtship. They include biting and especiallyshell ramming by the male. The tail is used as a tactile organduring courtship of some species.     

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.