Plumage and song differences mediate species recognition between incipient flycatcher species of the Solomon Islands

Changes in mating signals among populations contribute to species formation. Often these signals involve a suite of display traits of different sensory modalities ("multimodal signals"); however, few studies have tested the consequences of multimodal signal divergence with most focusing on only a single divergent signal or suite of signals of the same sensory modality. Populations of the chestnut-bellied flycatcher Monarcha castaneiventris vary in song and plumage color across the Solomon Islands. Using taxidermic mount presentation and song playback experiments, we tested for the relative roles of divergent song and color in homotypic ("same type") recognition between one pair of recently diverged sister taxa (the nominate chestnut-bellied M. c. castaneiventris and the white-capped M. c. richardsii forms). We found that both plumage and song type influenced the intensity of aggressive response by territory-owners, with plumage color playing a stronger role. These results indicate that differences in plumage and song are used in homotypic recognition, suggesting the importance of multimodal signal divergence in the evolution of premating reproductive isolation.     

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.     

Multimodal alarm behavior in urban and rural gray squirrels studied by means of observation and a mechanical robot

Urbanization of animal habitats has the potential to affect the natural communication systems of any species able to survive in the changed environment. Urban animals such as squirrels use multiple signal channels to communicate, but it is un-known how urbanization has affected these behaviors. Multimodal communication, involving more than one sensory modality, can be studied by use of biomimetic mechanical animal models that are designed to simulate the multimodal signals and be pre-sented to animal subjects in the field. In this way the responses to the various signal components can be compared and contrasted to determine whether the multimodal signal is made up of redundant or nonredundant components. In this study, we presented wild gray squirrels in relatively urban and relatively rural habitats in Western Massachusetts with a biomimetic squirrel model that produced tail flags and alarm barks in a variety of combinations. We found that the squirrels responded to each unimodal component on its own, the bark and tail flag, but they responded most to the complete multimodal signal, containing both the acoustic and the moving visual components, providing evidence that in this context the signal components are redundant and that their combination elicits multimodal enhancement. We expanded on the results of Parian et al. (2009) by providing data on sig-naling behavior in the presence and absence of conspecifics, suggesting that alarm signaling is more likely if conspecifies are present. We found that the squirrels were more active in the urban habitats and that they responded more to tail flagging in the urban habitats as compared to the rural ones, suggesting the interesting possibility of a multimodal shift from reliance on audio to visual signals in noisier more crowded urban habitats.     

Female responses to isolated signals from multimodal male courtship displays in the wolf spider genus Schizocosa (Araneae: Lycosidae)

Male wolf spiders within the genus Schizocosa display considerable variation in foreleg ornamentation as well as in courtship communication. Multiple modes of male signalling have evolved in a number of species. Divergence in courtship signals among species within this genus may be directly associated with variation in the sensory sensitivities of conspecific females. We isolated the visual and vibratory courtship cues of four species of Schizocosa and recorded conspecific female receptivity to each isolated cue. We also examined female receptivity to complete multimodal courtship signals. We found that the sensory sensitivities of conspecific females were associated with the predominant modes of male courtship communication. Species in which females use mostly stridulatory cues in assessing conspecific males tended to have stridulation-based male courtship displays (S. duplex and S. uetzi) while the opposite was true for species in which females used more visual cues in male assessment (S. stridulans and S. crassipes). This study suggests coevolution between male signal design and female sensory design. We discuss possible scenarios that could be driving this coevolution, including hypotheses of sensory bias and environmental constraints. Copyright 1999 The Association for the Study of Animal Behaviour.     

Vibratory Communication in the Jumping Spider Phidippus clarus: Substrate‐borne Courtship Signals are Important for Male Mating Success

Recently, work has shown that multimodal communication is common throughout the animal kingdom but the function of multimodal signals is still poorly understood. Phidippus clarus are jumping spiders in which males produce multimodal (visual and vibrational) signals in both male–male (aggressive) and male–female (courtship) contexts. The P. clarus mating system is complex, with sex ratios and the level of male competition changing over the course of the breeding season. Vibrational signal components have been shown to function in male aggressive contests but their role in courtship has not been investigated. Here, we performed an experiment to test the role of vibrational signaling in courtship by observing mating success for males that were experimentally muted. We show that vibratory courtship signals, and in particular signaling rate, is an important component of mating success and potentially a target of female choice. While the ability to produce vibratory signals significantly increased mating success, some muted males were still able to successfully mate. In these trials, signaling rate also predicted mating success suggesting that redundant signal components may compensate for errors and perturbations in signal transmission or that vibratory signals function to enhance the efficacy of visual signals.     

FEMALES ARE CHOOSIER IN THE DARK: ENVIRONMENT‐DEPENDENT RELIANCE ON COURTSHIP COMPONENTS AND ITS IMPACT ON FITNESS

A broad understanding of multimodal courtship function necessitates knowledge of the potential information content of signal components, the efficacy of signal components in eliciting the appropriate receiver response, and the fitness consequences of mating decisions based upon various signal components. We present data addressing each of these requirements for the multimodal‐signaling wolf spider, Schizocosa floridana Bryant. Using diet manipulations, we first demonstrate that both visual and seismic courtship signals are condition‐dependent. Next, using high‐ and low‐quantity diet individuals in mate choice trials across manipulated signaling environments, we demonstrate that the seismic signal is crucial for mating success and further show that female choosiness is environment‐dependent. Females mated more with high diet males only in the absence of visual signals, showing no discrimination in the presence of visual signals. Finally, by quantifying the number of offspring produced by our mated females, we reveal that a female's mating environment, in conjunction with her potential resource availability, influences her fitness—in environments in which females exerted choice, heavier females produced more offspring. Together, this comprehensive set of experiments demonstrates that female choosiness varies across environments, leading to direct fitness consequences.     

Multimodal signalling in estrildid finches: song,dance and colour are associated with different ecological and life‐history traits

Sexual traits (e.g. visual ornaments, acoustic signals, courtship behaviour) are often displayed together as multimodal signals. Some hypotheses predict joint evolution of different sexual signals (e.g. to increase the efficiency of communication) or that different signals trade off with each other (e.g. due to limited resources). Alternatively, multiple signals may evolve independently for different functions, or to communicate different information (multiple message hypothesis). We evaluated these hypotheses with a comparative study in the family Estrildidae, one of the largest songbird radiations, and one that includes many model species for research in sexual selection and communication. We found little evidence for either joint evolution or trade‐offs between song and colour ornamentation. Some negative correlations between dance repertoire and song traits may suggest a functional compromise, but generally courtship dance also evolved independently from other signals. Instead of correlated evolution, we found that song, dance and colour are each related to different socio‐ecological traits. Song complexity evolved together with ecological generalism, song performance with investment in reproduction, dance with commonness and habitat type, whereas colour ornamentation was shown previously to correlate mostly with gregariousness. We conclude that multimodal signals evolve in response to various socio‐ecological traits, suggesting the accumulation of distinct signalling functions.     

Multimodal Signaling in Male and Female Foot-Flagging Frogs Staurois guttatus (Ranidae): An Alerting Function of Calling

In multimodal communication, individuals use several sensory modalities for information transfer. We report on novel observations of foot‐flagging in the Bornean ranid frog Staurois guttatus that is temporally linked to advertisement calling. In addition, we document the first case of foot‐flagging in a female anuran as well as additional visual displays in both males and females including arm‐waving, vocal‐sac pumping and open‐mouth display. In males, advertisement calls and foot‐flags were given throughout most of the day, suggesting that acoustic and visual signals form a multicomponent and multimodal display. We tested the efficacy‐based alerting signal hypothesis of multimodal communication using acoustic playback experiments with males. This hypothesis predicts that an initial signal draws the receiver's attention to the location of a subsequent more informative signal. Several lines of evidence supported the alerting hypothesis. First, the latency between foot‐flags and advertisement calls was significantly higher than that between advertisement calls and foot‐flags, suggesting a functional linkage with calls drawing attention to foot‐flags. Secondly, advertisement calling had a signaling function with males responding significantly more often with both calls and foot‐flags compared with pre‐ and post‐playback control periods. Finally, and most notably, all males tested turned towards the playback stimulus, suggesting that the advertisement call serves to focus their attention on subsequent signals. We discuss the potential of multimodal signaling for conspecific and heterospecific communication and the circumstances under which such a multimodal communication system could evolve.     

Comparing Apples and Oranges: Fold-Change Detection of Multiple Simultaneous Inputs

Sensory systems often detect multiple types of inputs. For example, a receptor in a cell-signaling system often binds multiple kinds of ligands, and sensory neurons can respond to different types of stimuli. How do sensory systems compare these different kinds of signals? Here, we consider this question in a class of sensory systems – including bacterial chemotaxis- which have a property known as fold-change detection: their output dynamics, including amplitude and response time, depends only on the relative changes in signal, rather than absolute changes, over a range of several decades of signal. We analyze how fold-change detection systems respond to multiple signals, using mathematical models. Suppose that a step of fold F₁ is made in input 1, together with a step of F₂ in input 2. What total response does the system provide? We show that when both input signals impact the same receptor with equal number of binding sites, the integrated response is multiplicative: the response dynamics depend only on the product of the two fold changes, F₁F₂. When the inputs bind the same receptor with different number of sites n₁ and n₂, the dynamics depend on a product of power laws, . Thus, two input signals which vary over time in an inverse way can lead to no response. When the two inputs affect two different receptors, other types of integration may be found and generally the system is not constrained to respond according to the product of the fold-change of each signal. These predictions can be readily tested experimentally, by providing cells with two simultaneously varying input signals. The present study suggests how cells can compare apples and oranges, namely by comparing each to its own background level, and then multiplying these two fold-changes.     

Candidate neural locus for sex differences in reproductive decisions

Sexual selection and signal detection theories predict that females should be selective in their responses to mating signals in mate choice, while the response of males to signals in male competition should be less selective. The neural processes underlying this behavioural sex difference remain obscure. Differences in behavioural selectivity could result from differences in how sensitive sensory systems are to mating signals, distinct thresholds in motor areas regulating behaviour, or sex differences in selectivity at a gateway relaying sensory information to motor systems. We tested these hypotheses in frogs using the expression of egr-1 to quantify the neural responses of each sex to mating signals. We found that egr-1 expression in a midbrain auditory region was elevated in males in response to both conspecific and heterospecific calls, whereas in females, egr-1 induction occurred only in response to conspecific signals. This differential neural selectivity mirrored the sex differences in behavioural responsiveness to these stimuli. By contrast, egr-1 expression in lower brainstem auditory centres was not different in males and females. Our results support a model in which sex differences in behavioural selectivity arise from sex differences in the neural selectivity in midbrain areas relaying sensory information to the forebrain.     

Vestibular-Somatosensory Interactions: Effects of Passive Whole-Body Rotation on Somatosensory Detection

Vestibular signals are strongly integrated with information from several other sensory modalities. For example, vestibular stimulation was reported to improve tactile detection. However, this improvement could reflect either a multimodal interaction or an indirect interaction driven by vestibular effects on spatial attention and orienting. Here we investigate whether natural vestibular activation induced by passive whole-body rotation influences tactile detection. In particular, we assessed the ability to detect faint tactile stimuli to the fingertips of the left and right hand during spatially congruent or incongruent rotations. We found that passive whole-body rotations significantly enhanced sensitivity to faint shocks, without affecting response bias. Critically, this enhancement of somatosensory sensitivity did not depend on the spatial congruency between the direction of rotation and the hand stimulated. Thus, our results support a multimodal interaction, likely in brain areas receiving both vestibular and somatosensory signals.     

Moths use multimodal sensory information to adopt adaptive resting orientations

Camouflage conceals animals from predators and depends on the interplay between the morphology and behaviour of animals. Behavioural elements of animals, such as the choice of a resting spot or posture, are important for effective camouflage, as well as the animals’ cryptic appearance. To date, the type of sensory input that mediates resting site choice remains poorly understood. Previously, we showed that bark‐like moths perceive and rely on bark structure to seek out cryptic resting positions and body orientations on tree trunks. In the present study, we investigated the sensory organs through which moths perceive the structure of bark when positioning their bodies in adaptive resting orientations. We amputated (or blocked) each one of the hypothetical sensory organs in moths (antennae, forelegs, wings, and eyes) and tested whether they were still able to perceive bark structure properly and adopt adaptive resting orientations. We found that visual information or stimulation is crucial for adaptively orienting their bodies when resting and tactile information from wings may play an additional role. The present study reveals multimodal information use by moths to achieve visual camouflage and highlights the sensory mechanism that is responsible for the adaptive behaviour of cryptic insects. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 900–904.     

Conserved visual sensitivities across divergent lizard lineages that differ in an ultraviolet sexual signal

The sensory drive hypothesis predicts the correlated evolution of signaling traits and sensory perception in differing environments. For visual signals, adaptive divergence in both color signals and visual sensitivities between populations may contribute to reproductive isolation and promote speciation, but this has rarely been tested or shown in terrestrial species. We tested whether opsin protein expression differs between divergent lineages of the tawny dragon (Ctenophorus decresii) that differ in the presence/absence of an ultraviolet sexual signal. We measured the expression of four retinal cone opsin genes (SWS1, SWS2, RH2, and LWS) using droplet digital PCR. We show that gene expression between lineages does not differ significantly, including the UV wavelength sensitive SWS1. We discuss these results in the context of mounting evidence that visual sensitivities are highly conserved in terrestrial systems. Multiple competing requirements may constrain divergence of visual sensitivities in response to sexual signals. Instead, signal contrast could be increased via alternative mechanisms, such as background selection. Our results contribute to a growing understanding of the roles of visual ecology, phylogeny, and behavior on visual system evolution in reptiles.     

Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance

Anthropogenic sensory pollution is affecting ecosystems worldwide. Human actions generate acoustic noise, emanate artificial light and emit chemical substances. All of these pollutants are known to affect animals. Most studies on anthropogenic pollution address the impact of pollutants in unimodal sensory domains. High levels of anthropogenic noise, for example, have been shown to interfere with acoustic signals and cues. However, animals rely on multiple senses, and pollutants often co-occur. Thus, a full ecological assessment of the impact of anthropogenic activities requires a multimodal approach. We describe how sensory pollutants can co-occur and how covariance among pollutants may differ from natural situations. We review how animals combine information that arrives at their sensory systems through different modalities and outline how sensory conditions can interfere with multimodal perception. Finally, we describe how sensory pollutants can affect the perception, behaviour and endocrinology of animals within and across sensory modalities. We conclude that sensory pollution can affect animals in complex ways due to interactions among sensory stimuli, neural processing and behavioural and endocrinal feedback. We call for more empirical data on covariance among sensory conditions, for instance, data on correlated levels in noise and light pollution. Furthermore, we encourage researchers to test animal responses to a full-factorial set of sensory pollutants in the presence or the absence of ecologically important signals and cues. We realize that such approach is often time and energy consuming, but we think this is the only way to fully understand the multimodal impact of sensory pollution on animal performance and perception.     

The Role of Visual Ornamentation in Female Choice of a Multimodal Male Courtship Display

The courtship behavior of male Schizocosa uetzi wolf spiders incorporates both visual and seismic signals into a multimodal display. These two signals have been shown to interact in such a manner that the seismic signal alters a female's response to the visual signal, leading to a putative increased importance of visual signaling in the presence of a seismic signal. Experiments leading to this attention‐focusing hypothesis relied in part on the video playback technique, eliciting the question of its significance under more biologically relevant conditions. Here, we directly examine female mate choice of males with differing visual signals (foreleg pigmentation) both in the presence and absence of a seismic courtship signal. We first quantified the natural variation of male foreleg pigmentation within a population of S. uetzi. The proportion of the tibia covered in pigmentation was found to be positively correlated with male weight, suggesting that this signal may convey reliable information about male size. Visual signals of live males were then manipulated into two treatments: black and brown male foreleg tibias, representing the extreme ends of the natural variation found. The seismic signaling environment was also manipulated into two treatments: seismic signal present and absent. Mating frequency was higher in the presence of a seismic signal than in its absence, but there was no interaction between the seismic and visual signaling treatments. Females mated with black and brown males equally whether a seismic signal was present or absent. This study suggests that inexperienced females do not distinguish between males of different manipulated foreleg pigmentations in mate‐choice decisions, even when in the presence of a seismic courtship signal.     

Modality interactions alter the shape of acoustic mate preference functions in gray treefrogs

Sexual selection takes place in complex environments where females evaluating male mating signals are confronted with stimuli from multiple sources and modalities. The pattern of expression of female preferences may be influenced by interactions between modalities, changing the shape of female preference functions, and thus ultimately altering the selective landscape acting on male signal evolution. We tested the hypothesis that the responses of female gray treefrogs, Hyla versicolor, to acoustic male advertisement calls are affected by interactions with visual stimuli. We measured preference functions for several call traits under two experimental conditions: unimodal (only acoustic signals presented), and multimodal (acoustic signals presented along with a video‐animated calling male). We found that females were more responsive to multimodal stimulus presentations and, compared to unimodal playbacks, had weaker preferences for temporal call characteristics. We compared the preference functions obtained in these two treatments to the distribution of male call characteristics to make inferences on the strength and direction of selection expected to act on male calls. Modality interactions have the potential to influence the course of signal evolution and thus are an important consideration in sexual selection studies.     

Eavesdropping on visual secrets

Private communication may benefit signalers by reducing the costs imposed by potential eavesdroppers such as parasites, predators, prey, or rivals. It is likely that private communication channels are influenced by the evolution of signalers, intended receivers, and potential eavesdroppers, but most studies only examine how private communication benefits signalers. Here, we address this shortcoming by examining visual private communication from a potential eavesdropper’s perspective. Specifically, we ask if a signaler would face fitness consequences if a potential eavesdropper could detect its signal more clearly. By integrating studies on private communication with those on the evolution of vision, we suggest that published studies find few taxon-based constraints that could keep potential eavesdroppers from detecting most hypothesized forms of visual private communication. However, we find that private signals may persist over evolutionary time if the benefits of detecting a particular signal do not outweigh the functional costs a potential eavesdropper would suffer from evolving the ability to detect it. We also suggest that all undetectable signals are not necessarily private signals: potential eavesdroppers may not benefit from detecting a signal if it co-occurs with signals in other more detectable sensory modalities. In future work, we suggest that researchers consider how the evolution of potential eavesdroppers’ sensory systems influences private communication. Specifically, we suggest that examining the fitness correlates and evolution of potential eavesdroppers can help (1) determine the likelihood that private communication channels are stable over evolutionary time, and (2) demonstrate that undetectable signals are private signals by showing that signalers benefit from a reduction in detection by potential eavesdroppers.     

Pyrazine odour makes visually conspicuous prey aversive

Unpalatable insects frequently adopt multimodal signals to ward off predators, incorporating sounds and odours into their colourful displays. Pyrazine is an odour commonly used in insect warning displays, and has previously been shown to elicit unlearned biases against common warning colours, e.g. yellow and red in naive predators. We designed two experiments to test for similar effects of pyrazine on the conspicuousness of prey, perhaps the most ubiquitous aspect of aposematic coloration. In the first experiment, we offered predators (Gallus gallus domesticus) a choice between conspicuous crumbs and cryptic crumbs in the presence or absence of pyrazine. In the second experiment, we manipulated the birds' experience of conspicuous prey during an initial training phase. Only in the presence of pyrazine did birds show a bias against conspicuously coloured food, and this occurred whether or not they had previously experienced food that contrasted with the background. This emergent behaviour relied upon the visual and odorous signal components being presented together. These unlearned, yet hidden, responses against conspicuousness demonstrate that there are initial benefits to prey being conspicuous when the multimodal nature of warning signals is accounted for.     

Multimodal signals enhance decision making in foraging bumble-bees

Multimodal signals are common in nature and have recently attracted considerable attention. Despite this interest, their function is not well understood. We test the hypothesis that multimodal signals improve decision making in receivers by influencing the speed and the accuracy of their decisions. We trained bumble-bees (Bombus impatiens) to discriminate between artificial flowers that differed either in one modality, visual (specifically, shape) or olfactory, or in two modalities, visual plus olfactory. Bees trained on multimodal flowers learned the rewarding flowers faster than those trained on flowers that differed only in the visual modality and, in extinction trials, visited the previously rewarded flowers at a higher rate than bees trained on unimodal flowers. Overall, bees showed a speed-accuracy trade-off; bees that made slower decisions achieved higher accuracy levels. Foraging on multimodal flowers did not affect the slope of the speed-accuracy relationship, but resulted in a higher intercept, indicating that multimodal signals were associated with consistently higher accuracy across range of decision speeds. Our results suggest that bees make more effective decisions when flowers signal in more than one modality, and confirm the importance of studying signal components together rather than separately.