Motion perception and visual signal design in Anolis lizards

Anolis lizards communicate with displays consisting of motion of the head and body. Early portions of long-distance displays require movements that are effective at eliciting the attention of potential receivers. We studied signal-motion efficacy using a two-dimensional visual-motion detection (2DMD) model consisting of a grid of correlation-type elementary motion detectors. This 2DMD model has been shown to accurately predict Anolis lizard behavioural response. We tested different patterns of artificially generated motion and found that an abrupt 0.3° shift of position in less than 100 ms is optimal. We quantified motion in displays of 25 individuals from five species. Four species employ near-optimal movement patterns. We tested displays of these species using the 2DMD model on scenes with and without moderate wind. Display movements can easily be detected, even in the presence of windblown vegetation. The fifth species does not typically use the most effective display movements and display movements cannot be discerned by the 2DMD model in the presence of windblown vegetation. A number of Anolis species use abrupt up-and-down head movements approximately 10 mm in amplitude in displays, and these movements appear to be extremely effective for stimulating the receiver visual system.     

Information‐gathering as a response to manipulated signals in the eastern fence lizard,Sceloporus undulatus

Colorful visual signals are used across taxa to convey information during agonistic male‐male encounters, which are important for sexual selection. Although much is known about the information content of color signals, less is known about how receivers interpret this information. Here, using territorial Sceloporus undulatus lizards in a natural setting, we examined receiver response to intruders with different color patch sizes to determine (a) if patch size conveys information assessed during male‐male interactions and (b) if/how receivers modulate their behavioral responses to different types of behavioral signals. We found that larger lizards had longer and wider patches, indicating that the size of the patches may be one of the many characteristics of these patches that is used by males to convey information. Free‐ranging subject males also produced more headbob displays in response to intruders with small patches and took marginally longer to react to intruders with large patches. However, we found no differences in the aggressiveness of the response (i.e., fullshows). This indicates that patch size conveys information that is employed during territorial disputes, but that the response is primarily in terms of timing, allowing lizards to gather more information about intruders, instead of aggressive behavior (i.e., fullshows).     

Preference for Male Traits Differ in Two Female Morphs of the Tree Lizard,Urosaurus ornatus

Non-random female mating preferences may contribute to the maintenance of phenotypic variation in color polymorphic species. However, the effect of female preference depends on the types of male traits used as signals by receptive females. If preference signals derive from discrete male traits (i.e., morph-specific), female preferences may rapidly fix to a morph. However, female preference signals may also include condition-dependent male traits. In this scenario, female preference may differ depending on the social context (i.e., male morph availability). Male tree lizards (Urosaurus ornatus) exhibit a dewlap color polymorphism that covaries with mating behavior. Blue morph males are aggressive and defend territories, yellow males are less aggressive and defend smaller territories, and orange males are typically nomadic. Female U. ornatus are also polymorphic in dewlap color, but the covariation between dewlap color and female behavior is unknown. We performed an experiment to determine how female mate choice depends on the visual and chemical signals produced by males. We also tested whether female morphs differ in their preferences for these signals. Female preferences involved both male dewlap color and size of the ventral color patch. However, the female morphs responded to these signals differently and depended on the choice between the types of male morphs. Our experiment revealed that females may be capable of distinguishing among the male morphs using chemical signals alone. Yellow females exhibit preferences based on both chemical and visual signals, which may be a strategy to avoid ultra-dominant males. In contrast, orange females may prefer dominant males. We conclude that female U. ornatus morphs differ in mating behavior. Our findings also provide evidence for a chemical polymorphism among male lizards in femoral pore secretions.     

Not All Signals are Equal: Male Brown Anole Lizards (Anolis sagrei) Selectively Decrease Pushup Frequency Following a Simulated Predatory Attack

The use of conspicuous communication signals often increases a signaler's risk of predation. Many species communicate with a repertoire of signals that may differ in their conspicuousness to predators. Few studies have examined the ability of prey to selectively decrease the use of individual signals in their displays under heightened predation risk. Here, I examined the behavior of male brown anole lizards (Anolis sagrei) in response to a simulated predatory attack from a model kestrel. This species communicates with three major visual signal types, the head‐bob, pushup, and dewlap extension, which vary in their motion and spectral characteristics. I predicted that lizards would decrease frequencies of the dewlap extension and pushup following the attack, but not the head‐bob. Males modulated their use of individual signals by decreasing pushup rates, but not head‐bob rates. Decreases in dewlap frequency were marginally significant. One explanation for these results is that lizards decrease frequencies of signal types based partly on their conspicuousness. The energetic cost of each signal type may be an equally important factor that determines the signaler's response to predators, particularly if a predatory attack is perceived as imminent.     

Divergent male and female mate preferences do not explain incipient speciation between lizard lineages

Diversification in sexual signals is often taken as evidence for the importance of sexual selection in speciation. However, in order for sexual selection to generate reproductive isolation between populations, both signals and mate preferences must diverge together. Furthermore, assortative mating may result from multiple behavioral mechanisms, including female mate preferences, male mate preferences, and male–male competition; yet their relative contributions are rarely evaluated. Here, we explored the role of mate preferences and male competitive ability as potential barriers to gene flow between 2 divergent lineages of the tawny dragon lizard, Ctenophorus decresii, which differ in male throat coloration. We found stronger behavioral barriers to pairings between southern lineage males and northern lineage females than between northern males and southern females, indicating incomplete and asymmetric behavioral isolating barriers. These results were driven by both male and female mate preferences rather than lineage differences in male competitive ability. Intrasexual selection is therefore unlikely to drive the outcome of secondary contact in C. decresii, despite its widely acknowledged importance in lizards. Our results are consistent with the emerging view that although both male and female mate preferences can diverge alongside sexual signals, speciation is rarely driven by divergent sexual selection alone.     

Male displays and female preferences in the courtship of a gregarious cricket

The courtship of males of the gregarious cricket Amphiacusta maya involves a variety of signals. The quantitative aspects of both successful and unsuccessful courtship sequences were examined to determine whether certain aspects of male displays were correlated with female mating preferences regardless of which male performed them. Although variability among males was high for most courtship components measured, I found no evidence of female choice with respect to the courtship variables studied. About 35% of the duration of each male courtship sequence is devoted to chirping, but there were no differences in either the likelihood of copulation or the latency to copulation between normal males and experimentally silenced males. The possibility that intrinsic differences in male quality explained the variability in courtship duration was examined with a two-way analysis of variance. The variance in courtship duration was attributable to variance among females, not to variance among males. Thus the courtship behaviour of male A. maya is variable enough to allow females to exert stabilizing or disruptive selection on displays, but there is no evidence that females use the available information.     

Dragon wars: Movement‐based signalling by Australian agamid lizards in relation to species ecology

It is evident that the environment has the potential to affect animal communication strategies. Species from diverse taxonomic groups using signals from different modalities are known to generate signals that suit the structure of their habitat in order to maximize efficiency. Studies of acoustically communicating species dominate the literature, but visual signals are also tailored to local conditions. There is now increasing evidence that dynamic visual signals, in the form of movement‐based displays, are also influenced by habitat characteristics. Australia's dragon lizards (Family: Agamidae) employ such dynamic signals in a variety of contexts but are particularly common in territory defence. With a few notable exceptions, the signalling behaviour of this group has been relatively overlooked, and the knowledge that does exist is contained in scientific papers focused on other topics or unpublished accounts from herpetologists. In this review, we collated information on the signalling behaviour of these animals and determined that 34 of the 78 species use movement‐based signalling. This number is likely to be an underestimate, as knowledge of the signalling behaviour of many species is lacking. The richly contrasting environments of Australia inhabited by these lizards provide considerable variation in ecological context, so our second objective was to place known signalling behaviour in the context of species ecology. After controlling for phylogeny, we found that broad habitat classifications do not strongly influence the likelihood of motion signalling, and specific motor patterns are not more likely to occur in particular microhabitats. We conclude by suggesting that fully understanding the motion signalling behaviour of Australia's agamids will require documenting the displays of species for which there are no data, while taking into account the high variability existing within motor patterns and considering in detail the environmental context under which signalling takes place.     

Interpopulational Variations in Sexual Chemical Signals of Iberian Wall Lizards May Allow Maximizing Signal Efficiency under Different Climatic Conditions

Sexual signals used in intraspecific communication are expected to evolve to maximize efficacy under a given climatic condition. Thus, chemical secretions of lizards might evolve in the evolutionary time to ensure that signals are perfectly tuned to local humidity and temperature conditions affecting their volatility and therefore their persistence and transmission through the environment. We tested experimentally whether interpopulational altitudinal differences in chemical composition of femoral gland secretions of male Iberian wall lizards (Podarcis hispanicus) have evolved to maximize efficacy of chemical signals in different environmental conditions. Chemical analyses first showed that the characteristics of chemical signals of male lizards differed between two populations inhabiting environments with different climatic conditions in spite of the fact that these two populations are closely related genetically. We also examined experimentally whether the temporal attenuation of the chemical stimuli depended on simulated climatic conditions. Thus, we used tongue-flick essays to test whether female lizards were able to detect male scent marks maintained under different conditions of temperature and humidity by chemosensory cues alone. Chemosensory tests showed that chemical signals of males had a lower efficacy (i.e. detectability and persistence) when temperature and dryness increase, but that these effects were more detrimental for signals of the highest elevation population, which occupies naturally colder and more humid environments. We suggest that the abiotic environment may cause a selective pressure on the form and expression of sexual chemical signals. Therefore, interpopulational differences in chemical profiles of femoral secretions of male P. hispanicus lizards may reflect adaptation to maximize the efficacy of the chemical signal in different climates.     

Eavesdropping in crabs: an agency for lady detection

Although conspicuous courtship displays are an effective way of attracting the attention of receptive females, they could provide valuable information to rival males on the location of these females. In fiddler crabs, males that see a receptive female wave their single, greatly enlarged claw in a highly conspicuous courtship display. We test whether other males use this courtship display to alert them to the presence of receptive females that they cannot directly see. We show that male fiddler crabs (Uca mjoebergi) eavesdrop on the courtship displays of nearby males to detect mate-searching females. This allows males to begin waving before a female becomes visible. Furthermore, males appear to adjust their waving according to the information available: eavesdropping males wave 12 times faster than non-courting males but only 1.7 times slower than males in full visual contact with the female.     

Evolutionary stasis and lability in thermal physiology in a group of tropical lizards

Understanding how quickly physiological traits evolve is a topic of great interest, particularly in the context of how organisms can adapt in response to climate warming. Adjustment to novel thermal habitats may occur either through behavioural adjustments, physiological adaptation or both. Here, we test whether rates of evolution differ among physiological traits in the cybotoids, a clade of tropical Anolis lizards distributed in markedly different thermal environments on the Caribbean island of Hispaniola. We find that cold tolerance evolves considerably faster than heat tolerance, a difference that results because behavioural thermoregulation more effectively shields these organisms from selection on upper than lower temperature tolerances. Specifically, because lizards in very different environments behaviourally thermoregulate during the day to similar body temperatures, divergent selection on body temperature and heat tolerance is precluded, whereas night-time temperatures can only be partially buffered by behaviour, thereby exposing organisms to selection on cold tolerance. We discuss how exposure to selection on physiology influences divergence among tropical organisms and its implications for adaptive evolutionary response to climate warming.     

Design of the Jacky dragon visual display: signal and noise characteristics in a complex moving environment

Visual systems are typically selective in their response to movement. This attribute facilitates the identification of functionally important motion events. Here we show that the complex push-up display produced by male Jacky dragons ( Amphibolurus muricatus) is likely to have been shaped by an interaction between typical signalling conditions and the sensory properties of receivers. We use novel techniques to define the structure of the signal and of a range of typical moving backgrounds in terms of direction, speed, acceleration and sweep area. Results allow us to estimate the relative conspicuousness of each motor pattern in the stereotyped sequence of which displays are composed. The introductory tail-flick sweeps a large region of the visual field, is sustained for much longer than other components, and has velocity characteristics that ensure it will not be filtered in the same way as wind-blown vegetation. These findings are consistent with the idea that the tail-flick has an alerting function. Quantitative analyses of movement-based signals can hence provide insights into sensory processes, which should facilitate identification of the selective forces responsible for structure. Results will complement the detailed models now available to account for the design of static visual signals.     

Active pollination favours sexual dimorphism in floral scent

Zoophilous flowers often transmit olfactory signals to attract pollinators. In plants with unisexual flowers, such signals are usually similar between the sexes because attraction of the same animal to both male and female flowers is essential for conspecific pollen transfer. Here, we present a remarkable example of sexual dimorphism in floral signal observed in reproductively highly specialized clades of the tribe Phyllantheae (Phyllanthaceae). These plants are pollinated by species-specific, seed-parasitic Epicephala moths (Gracillariidae) that actively collect pollen from male flowers and pollinate the female flowers in which they oviposit; by doing so, they ensure seeds for their offspring. We found that Epicephala-pollinated Phyllanthaceae plants consistently exhibit major qualitative differences in scent between male and female flowers, often involving compounds derived from different biosynthetic pathways. In a choice test, mated female Epicephala moths preferred the scent of male flowers over that of female flowers, suggesting that male floral scent elicits pollen-collecting behaviour. Epicephala pollination evolved multiple times in Phyllantheae, at least thrice accompanied by transition from sexual monomorphism to dimorphism in floral scent. This is the first example in which sexually dimorphic floral scent has evolved to signal an alternative reward provided by each sex, provoking the pollinator''s legitimate altruistic behaviour.     

Processing of simple and complex acoustic signals in a tonotopically organized ear

Processing of complex signals in the hearing organ remains poorly understood. This paper aims to contribute to this topic by presenting investigations on the mechanical and neuronal response of the hearing organ of the tropical bushcricket species Mecopoda elongata to simple pure tone signals as well as to the conspecific song as a complex acoustic signal. The high-frequency hearing organ of bushcrickets, the crista acustica (CA), is tonotopically tuned to frequencies between about 4 and 70 kHz. Laser Doppler vibrometer measurements revealed a strong and dominant low-frequency-induced motion of the CA when stimulated with either pure tone or complex stimuli. Consequently, the high-frequency distal area of the CA is more strongly deflected by low-frequency-induced waves than by high-frequency-induced waves. This low-frequency dominance will have strong effects on the processing of complex signals. Therefore, we additionally studied the neuronal response of the CA to native and frequency-manipulated chirps. Again, we found a dominant influence of low-frequency components within the conspecific song, indicating that the mechanical vibration pattern highly determines the neuronal response of the sensory cells. Thus, we conclude that the encoding of communication signals is modulated by ear mechanics.     

Consequences of complex signaling: predator detection of multimodal cues

Animals often evolve complex signals to enhance their detectabilityby intended receivers. But signals that are more detectableby intended receivers may also be more likely to be interceptedby others, including predators. Courtship signaling in maleSchizocosa ocreata wolf spiders (Lycosidae) includes morphologicaltraits (prominent foreleg tufts) and active behaviors that togetherproduce a complex signal with simultaneous broadcast of visualand seismic components. Females respond more readily to maleswith large tufts and are more likely to respond when multiplemodalities (visual and seismic) are present in a complex signal.These spiders cooccur with active predators that may interceptthese conspicuous courtship signals and use them as huntingcues. We used video/seismic playback to experimentally isolateand manipulate aspects of the complex signal produced by maleS. ocreata. We found that increasing the size of a visual signal(male tufts) and increasing the complexity of the courtshipsignal by adding a second modality (visual plus seismic versusvisual alone) increased the speed with which a common predator,the jumping spider Phidippus clarus (Salticidae), respondedto playbacks of courting male S. ocreata. These results indicatethat the benefits of increased signaling efficacy of large visualsignaling ornaments and complex, multimodal signaling may becountered by increased predation risks.     

Large-scale patterns of signal evolution: an interspecific study of Liolaemus lizard headbob displays

Although many factors have been shown to influence the evolution of species recognition signals in a wide variety of taxa, it is difficult to draw general conclusions because of fundamental differences in the morphologies and ecologies of the animals considered. In this study, two morphologically and ecologically similar lizard genera (Sceloporus and Liolaemus) are used to provide replicate examples of the evolution of a complex visual display. New data on the headbob displays of 16 Liolaemus species are presented. As in other taxa, phylogenetic analyses show that evolutionary changes in display structure have been rapid, leaving little, if any, phylogenetic information in the display structure. Evolutionary changes in display structure also do not appear to be closely associated with any major habitat characteristics. Despite this rapid evolution, Liolaemus lizards produce headbob displays that are remarkably simple in structure in comparison to those produced by Sceloporus, perhaps compensating for lower complexity by frequent use of other visual displays such as forelimb and tail waves.     

Chameleons communicate with complex colour changes during contests: different body regions convey different information

Many animals display static coloration (e.g. of feathers or fur) that can serve as a reliable sexual or social signal, but the communication function of rapidly changing colours (as in chameleons and cephalopods) is poorly understood. We used recently developed photographic and mathematical modelling tools to examine how rapid colour changes of veiled chameleons Chamaeleo calyptratus predict aggressive behaviour during male–male competitions. Males that achieved brighter stripe coloration were more likely to approach their opponent, and those that attained brighter head coloration were more likely to win fights; speed of head colour change was also an important predictor of contest outcome. This correlative study represents the first quantification of rapid colour change using organism-specific visual models and provides evidence that the rate of colour change, in addition to maximum display coloration, can be an important component of communication. Interestingly, the body and head locations of the relevant colour signals map onto the behavioural displays given during specific contest stages, with lateral displays from a distance followed by directed, head-on approaches prior to combat, suggesting that different colour change signals may evolve to communicate different information (motivation and fighting ability, respectively).     

Female preference for multi-modal courtship: multiple signals are important for male mating success in peacock spiders

A long-standing goal for biologists has been to understand how female preferences operate in systems where males have evolved numerous sexually selected traits. Jumping spiders of the Maratus genus are exceptionally sexually dimorphic in appearance and signalling behaviour. Presumably, strong sexual selection by females has played an important role in the evolution of complex signals displayed by males of this group; however, this has not yet been demonstrated. In fact, despite apparent widespread examples of sexual selection in nature, empirical evidence is relatively sparse, especially for species employing multiple modalities for intersexual communication. In order to elucidate whether female preference can explain the evolution of multi-modal signalling traits, we ran a series of mating trials using Maratus volans. We used video recordings and laser vibrometry to characterize, quantify and examine which male courtship traits predict various metrics of mating success. We found evidence for strong sexual selection on males in this system, with success contingent upon a combination of visual and vibratory displays. Additionally, independently produced, yet correlated suites of multi-modal male signals are linked to other aspects of female peacock spider behaviour. Lastly, our data provide some support for both the redundant signal and multiple messages hypotheses for the evolution of multi-modal signalling.     

Lizards speed up visual displays in noisy motion habitats

Extensive research over the last few decades has revealed that many acoustically communicating animals compensate for the masking effect of background noise by changing the structure of their signals. Familiar examples include birds using acoustic properties that enhance the transmission of vocalizations in noisy habitats. Here, we show that the effects of background noise on communication signals are not limited to the acoustic modality, and that visual noise from windblown vegetation has an equally important influence on the production of dynamic visual displays. We found that two species of Puerto Rican lizard, Anolis cristatellus and A. gundlachi, increase the speed of body movements used in territorial signalling to apparently improve communication in visually 'noisy' environments of rapidly moving vegetation. This is the first evidence that animals change how they produce dynamic visual signals when communicating in noisy motion habitats. Taken together with previous work on acoustic communication, our results show that animals with very different sensory ecologies can face similar environmental constraints and adopt remarkably similar strategies to overcome these constraints.     

Divergence in Female Duetting Signals in the Enchenopa binotata Species Complex of Treehoppers (Hemiptera: Membracidae)

Sexual communication often involves signal exchanges between the sexes, or duetting, in which mate choice is expressed through response signals. With both sexes acting as signalers and receivers, variation in the signals of males and females may be important for mate choice, reproductive isolation, and divergence. In the Enchenopa binotata species complex – a case study of sympatric speciation in which vibrational duetting may have an important role – male signals are species‐specific, females choose among males on the basis of signal traits that reflect species and individual differences, and female preferences have exerted divergent selection on male signals. Here, we describe variation in female signals in the E. binotata species complex. We report substantial species differences in the spectral and temporal features of female signals, and in their timing relative to male signals. These differences were similar in range to differences in male signals in the E. binotata complex. We consider processes that might contribute to divergence in female signals, and suggest that signal evolution in the E. binotata complex may be influenced by mate choice in both sexes.