The dominance of seismic signaling and selection for signal complexity in Schizocosa multimodal courtship displays

Schizocosa wolf spiders show tremendous diversity in courtship complexity, with different species employing varying numbers of components within and across sensory modalities. Using a comparative approach, we investigate the importance of each signaling modality in the courtship display of five Schizocosa species (three stridulating and two drumming) by assessing mating success under manipulated signaling environments. Irrespective of the degree of male ornamentation, the three stridulating species exhibit a dependence on the seismic, but not visual, signaling environment for mating success. Mating was independent of signaling environment for the two drumming species. We next ask whether the degree to which each species depends upon a signaling modality for mating (i.e., modality importance) is correlated with the estimated modality-specific signal complexity. We first calculate effect sizes for the influence of seismic versus visual signaling environments on the likelihood to mate for ten Schizocosa species and then use an element-counting approach to calculate seismic and visual signal complexity scores. We use a phylogenetic regression analysis to test two predictions: (1) the importance of seismic signaling is correlated with seismic signal complexity and (2) the importance of visual signaling is correlated with visual signal complexity. We find a significant relationship between visual signal importance and visual signal complexity, but no relationship between seismic signal importance and seismic signal complexity. Finally, we test the hypothesis that selection acts on complexity per se by determining whether seismic and visual signal complexity is correlated across species. We find support for this hypothesis in a significant relationship between seismic and visual signal complexity.     

Multimodal signals,imperfect information,and identification of sex in red-backed salamanders (<Emphasis Type="Italic">Plethodon cinereus</Emphasis>)

Theoretical treatments and empirical studies both suggest that signals that occur in multiple sensory modes have superior detectabilities, discriminabilities, and memorabilities. There is also an intuitive link between signal detectability, discriminability, and memorability and the quality of information that is transferred via the signaler. We investigated the role of information quality and sensory modality in the sexual identification of intruding conspecifics by territorial male red-backed salamanders (Plethodon cinereus). Our results imply that these salamanders are able to discriminate between intruding male and female conspecifics (based on the allocation of aggression) in bimodal scenarios (vision and olfaction) even under situations in which the information available about the intruders sexual identities is reduced in quality. In unimodal scenarios (olfaction only), male residents exhibited heightened levels of aggression toward male secretions and reduced levels of aggression toward female secretions. In unimodal scenarios where information pertaining to the sex of the stimulus was reduced in quality, male residents displayed intermediate levels of aggression relative to the responses that male and female stimuli received respectively. Although resident males touched bimodal stimuli significantly more than they touched unimodal stimuli, we were unable to find support for the notion that sensory modality greatly influences how male resident red-backed salamanders allocate aggression toward intruding male versus female stimuli.Communicated by H. Kokko     

Modulation of male aggressiveness through different communication pathways

Communication plays a large role in resource competition, especially for potential mates, and is used by members of the competing sex to assess each other, and simultaneously to evaluate the other sex, which may be advertising its status. To assess the effects of female advertisement on male aggression, males of the decapod Aegla were paired according to body and armament size. Males were left to interact in five different treatments: with receptive females that could use both chemical and visual cues, non-receptive females that could use both types of cues, receptive females that could use only one cue, or no female in the aquarium. Fight duration, time spent in the most aggressive acts, latency period, number of antennal whips/fight duration, and time spent near the female were analyzed. The males had shorter and less intense confrontations when there was a receptive female that could signal with at least one modality. Winning males spent significantly more time near the receptive female only when both chemical and visual cues were present, when compared to the other treatments. The low level of aggression shown by the males may be related to information asymmetry due to the female’s choice: only the preferred male would receive information from the female, or males could compete for other resources that attract females. However, male aggression was modified by the presence of female chemical cues, whereas mate guarding was initiated only when both chemical and visual cues were present. Hence, male aggression can be downregulated by female receptivity.     

Receiver sex differences in visual response to dynamic motion signals in Sceloporus lizards

Visual signal properties often vary greatly between and within individuals in a variety of social contexts. While it is widely known that visual displays emitted by senders can exhibit great variation in efficacy and content, far less is understood whether and how receivers vary in the ability to respond to variability in signal properties, such as motion. Here, we tested for receiver sex differences in visual response latency to motion signals in Sceloporus undulatus lizards. We used a moving robotic lizard model as a visual stimulus to assay response latency in male and female lizards. We measured visual reaction times to slow and fast, up-and-down motions, characteristic of territorial and courtship male motion displays, respectively. We found sex differences in response latency to the two different displays. Specifically, male lizards were faster than females at responding to slow motion produced by the robotic lizard, while female lizards were faster than males at responding to fast motion. These results demonstrate that dynamic visual signals that vary temporally under different social contexts can differ in eliciting a visual response from each sex. Our study highlights that physical differences in dynamic and complex visual signals exhibited during different social contexts (i.e., territorial and courtship contexts) can closely match sex differences in visual responses.     

Variation in the temporal and spatial use of signals and its implications for multimodal communication

The use of signals across multiple sensory modalities in communication is common in animals and plants. Determining the information that each signal component conveys has provided unique insights into why multimodal signals evolve. However, how these complex signals are assessed by receivers will also influence their evolution, a hypothesis that has received less attention. Here, we explore multimodal signal assessment in a closely related complex of island flycatchers that have diverged in visual and acoustic signals. Using field experiments that manipulated song and plumage colour, we tested if song, a possible long-range signal, is assessed before plumage colour in conspecific recognition. We find that divergent song and colour are assessed in sequence, and this pattern of sequential assessment is likely mediated by habitat structure and the extent of differences in signal characteristics. A broad survey of the literature suggests that many organisms from a wide range of taxa sequentially assess multimodal signals, with long-range signals attracting conspecifics for further assessment of close-range signals. Our results highlight the need to consider how signals are assessed when understanding multimodal signal evolution. Finally, given the results of our field experiments indicating sequential assessment of divergent song and colour in the recognition of conspecifics, we discuss the consequences of multimodal signal divergence for the origin of species, as changes in signals across different sensory modalities may influence the evolution of premating reproductive isolation.     

Interacting effects of ambient light and plumage color patterns in displaying Wire-tailed Manakins (Aves,Pipridae)

Sending color signals to conspecifics may attract predators, leading to opposing selection pressures on the evolution of signal expression and display behavior in animals. The costs of signaling can be reduced, however, because conspicuousness is the combined result of the reflectance spectra of the displayer's color pattern and the spectra of ambient light illuminating the animal. Changes in ambient light can alter conspicuousness, even when chemical and structural color-generating mechanisms remain constant, potentially allowing animals to display their colors most fully in light environments where the benefits are greatest relative to the costs. Using spectroradiometric methods, we determined how light habitat use affects conspicuousness in adult males of the Wire-tailed Manakin Pipra filicauda, a lekking bird species with vivid plumage colors. We studied three aspects of visibility, including properties of the entire color pattern, visual contrast within an individual's plumage and a bird's contrast relative to its visual background. Wire-tailed Manakins usually displayed in forest shade environments, which reduced their conspicuousness at larger viewing distances, while maximizing visual contrast within the plumage color pattern at close viewing distances. Compared to sunspots, ambient light in forest shade reduces the contrast of individual bird colors with the background at close viewing distance. However, background contrast of individual bird colors in the shade was still relatively higher during sunny than during cloudy weather which may explain why males were more active when the sun was not blocked by clouds. Assuming that the visual perceptions of predators and other manakins do not differ from the reflectance patterns we measured, Wire-tailed manakins tend to display in light environments that reduce the conflicts between avoiding long distance detection by predators and displaying conspicuous color signals to visiting females.     

Defeated chameleons darken dynamically during dyadic disputes to decrease danger from dominants

Research on intraspecific aggression has typically focused on dominant individuals, but a better understanding of the consequences and mechanisms of agonistic encounters requires a balanced perspective that includes knowledge of subordinate animal behaviors. In contrast to signals of fighting ability, signals of submission are an understudied component of agonistic communication that could provide important insights into the dynamics, function, and evolution of intraspecific competition. Here, I use a series of staged agonistic trials between adult male veiled chameleons Chamaeleo calyptratus to test the hypothesis that rapid skin darkening serves as a submissive signal to resolve agonistic activity. Concordant with this hypothesis, I found that losing chameleons darkened over the course of aggressive trials while winners brightened, and the likelihood of darkening increased when individuals were attacked more aggressively. Additionally, I found that the degree of brightness change exhibited by individual chameleons was tied to both overall and net aggression experienced during a trial, with chameleons who received high levels of aggression relative to their own aggression levels darkening to a greater extent than individuals receiving relatively less aggression. Lastly, I found that aggression increased for losers and winners prior to the onset of darkening by the eventual loser but that both chameleons reduced aggression after the losing chameleon began to darken. Based on the theoretical prediction that signals of submission should be favored when retreat options are restricted, I suggest that limited escapability imposed by chameleon morphology, physiology, and ecology favored the evolution of a pigment-based signal of submission in this group.     

A new heuristic for capturing the complexity of multimodal signals

Many animal signals are inherently multimodal, engaging more than one of the receiver’s sensory systems simultaneously, and it is the interaction between the two modalities that determines the signal’s function (s) and efficacy. It is hence necessary to quantify the effect of each modality relative to the other in order to fully understand animal communication. We have developed a new heuristic to aid in the identification and interpretation of the many distinct ways in which signals in multiple sensory modalities interact. Our approach represents natural variation in signal production for each modality and uses these to generate three-dimensional receiver response surface plots that map the relationships among the signal components and receiver behavior. We accommodate the extant hypotheses for the interactions between modalities, each of which makes a clear prediction about the shape of the response surface, and extend previous theory by considering new phenomena.     

Sympatric sexual signal divergence among North American Calopteryx damselflies is correlated with increased intra- and interspecific male–male aggression

Divergence of sexual signals in sympatry can arise as a consequence of (1) interspecific competition for resources, (2) selection against maladaptive hybridization, or (3) as a result of selection to reduce the cost of interspecific aggression; termed agonistic character displacement (ACD). Calopterygid damselflies have emerged as a model system for studying the evolution of divergent sexual signals due to the repeated evolution of sympatric species pairs with fully and partially melanized wings. Damselfly wing patterns function during both courtship and territory defense. However, the relative contributions of natural and sexual selection to phenotypic divergence and enhanced isolation in sympatry remain unclear in many cases. Here, we investigated the hypothesis that interference competition, in the form of increased interspecific male–male aggression, drives the evolution of character displacement in sympatry between two species of North American damselflies, Calopteryx aequabilis and Calopteryx maculata, that show no evidence of ecological divergence or ongoing hybridization. In paired behavioral trials, we found that interspecific male aggression related to territory defense varied between site, species, and as a function of the relative abundance of con- vs. hetero-specific males. Specifically, we found that large-spotted C. aequabilis males received increased intra- and interspecific aggression but that aggression against large-spotted males declined during the middle of the flight season when both species were equally abundant. Based on these results, we suggest that ACD leads to enhanced species recognition, and may be a common outcome of the antagonism between interspecific male–male competition and the countervailing force of intraspecific sexual selection favoring increased wing melanization among territorial damselfly species.     

Field presentation of male secretions alters social display in Sceloporus virgatus but not S. undulatus lizards

Lizards have communicative displays involving primarily vision and chemicals, and recent work suggests trade-offs between these two modalities. In reptiles, little work assesses effects of conspecific chemicals on subsequent signaling behavior. Here, we studied responses to conspecific secretions in two Sceloporus species differing in visual signaling: male Sceloporus undulatus have blue abdominal patches used in aggressive territorial encounters, while Sceloporus virgatus males have evolutionarily lost the patches and have low rates of aggressive display. We measured behavior of free-ranging males following presentation of swabs with conspecific male chemicals from femoral glands and the cloaca, or of clean swabs. For male S. undulatus (blue), neither likelihoods nor rates of behavioral responses differed between swab treatments. In contrast, male S. virgatus (white) presented with secretions had significantly higher likelihood of performing head bob, push-up, and shudder displays, than males in control swab trials. Rates of behavior also differed for S. virgatus, with higher rates of push-up display and tongue flick in trials with conspecific chemicals, but rates of other displays, number of moves, and mean total distance moved did not differ between treatments. Male S. undulatus moved significantly greater distances than S. virgatus, independent of treatment. In sum, male S. virgatus responded to conspecific male chemicals by increasing their low rates of display behavior, whereas male S. undulatus did not alter their already high rates of display or movement following chemical exposure. Chemical signals may play a different role in social signaling in the species with the loss of the abdominal color signal.     

Floral scents: their roles in nursery pollination mutualisms

Mutualisms are interspecies interactions in which each participant gains net benefits from interacting with its partner. In nursery pollination mutualisms, pollinators reproduce within the inflorescence they pollinate. In these systems, each partner depends directly on the other for its reproduction. Therefore, the signal responsible for partner encounter is crucial in these horizontally transmitted mutualisms, in which the association between specific partners must be renewed at each generation. As in many other interspecies interactions, chemical signals are suspected to be important in the functioning of these mutualisms. We synthesized and compared the published data available on the role of floral scents in the functioning of the 16 known independently evolved nursery pollination mutualisms. So far, attraction of pollinators to their specific hosts has been investigated in only seven of these systems, and the majority of the studies have been conducted on one of them, fig/fig wasp interactions. While such unevenness of the information limits the potential for meta-analysis, some patterns emerge from this review concerning the role of flower volatiles in maintaining the specificity of pollinator attraction, in signaling the appropriate phenological stage for pollinator visit, in attracting the pollinator toward the rewardless sex in dioecious plant species and in aiding the location and exploitation of resources by parasites and predators associated with these mutualisms. Finally, we highlight new perspectives on the evolution of signals in these diversified systems depending on the age and the degree of specificity of the interaction, and on the effect of phylogenetic inertia on the evolutionary dynamics of plant signals.     

The importance of white on black: unmelanized plumage proportion predicts display complexity in birds

Animal ritualized displays have been classically viewed as behavioral characters that decrease signal ambiguity or that facilitate the evaluation of costly exhibitions. It has been shown that their prevalence and level of complexity across species can reflect phylogenetic relationships between them, but the adaptive function of these behavioral traits is poorly known. Here, I hypothesize that, given that the efficacy of visual displays basically depends on conspicuousness and level of performance, species with low levels of conspicuousness may be forced to perform more complex varieties of a given display to get the same signal efficiency than other more conspicuous species. Thus, the evolution of display complexity, considered as the level of exaggeration of ritualized movements, may be explained as an adaptive trait and not only by phylogenetic inertia. I illustrate and test this hypothesis with the case of black-and-white plumage patches of pelecaniform birds. As predicted, there was a negative correlation between level of complexity and species conspicuousness (proportion of unmelanized plumage) for two different social displays. This indicates that classical ideas on the adaptiveness of ritualized displays should be considered to understand the present variation in signal form across species, which sheds light on the evolution of multiple signals.     

Antipredator responses to invasive lionfish, Pterois volitans: interspecific differences in cue utilization by two coral reef gobies

Understanding prey response to predators and their utilization of sensory cues to assess local predation risk is crucial in determining how predator avoidance strategies affect population demographics. This study examined the antipredator behaviors of two ecologically similar species of Caribbean coral reef fish, Coryphopterus glaucofraenum and Gnatholepis thompsoni, and characterized their responses to different reef predators. In laboratory assays, the two species of gobies were exposed to predator visual cues (native Nassau grouper predator vs. invasive lionfish predator), damage-released chemical cues from gobies, and combinations of these, along with appropriate controls. Behavioral responses indicate that the two prey species differ in their utilization of visual and chemical cues. Visual cues from predators were decisive for both species’ responses, demonstrating their relative importance in the sensory hierarchy, whereas damage-released cues were a source of information only for C. glaucofraenum. Both prey species could distinguish between native and invasive predators and subsequently altered their antipredator responses.     

Parental effects on carotenoid-based plumage coloration in nestling great tits, Parus major

Carotenoid pigments have attracted much interest in behavioural and evolutionary ecology because of their dual function in immune physiology and as color signals. In vertebrates, carotenoids must ultimately be obtained from the diet, and the mechanisms and magnitude of this environmental dependence are central for understanding carotenoid signal functions and evolution. In the present cross-fostering experiment with great tits Parus major, we investigate pre- and postnatal parental effects (egg yolk carotenoids, parental coloration) on nestling size and carotenoid coloration, using HPLC analysis of egg yolk carotenoids, and a reflectance-based measure of ‘chroma’ that reflects the plumage pigment concentration. Both rearing environment and origin influenced offspring size and plumage chroma. Maternal allocation of carotenoids to eggs had a weak positive effect on nestling plumage chroma, whereas we found no prenatal maternal effects (egg size or yolk carotenoid concentration) on size. Nestling plumage chroma was also significantly predicted by the chroma of the rearing father, but not by the color of the rearing mother or either of the original (genetical) parents. Thus, both prenatal maternal effects and postnatal paternal effects influence the carotenoid-based plumage coloration of nestling great tits. Future studies will reveal if parental effects have long-term consequences for plumage development and associated fitness components.     

A comparison of visual and olfactory learning performance in the bumblebee Bombus terrestris

Animals use cues from a range of sensory modalities to discriminate stimuli and as predictors of reward. Whilst there is appreciable variation in the cognitive performance of animals, we know surprisingly little about the extent to which learning varies among individuals across different sensory modalities. Do individuals that are good at learning in one sensory modality also perform well in another (performance is correlated between modalities), or do individuals demonstrate specialisation in learning performance in one modality (trading-off performance between modalities)? We tested these hypotheses by examining the performance of 76 Bombus terrestris workers, from four colonies, in both an odour-and visual learning task. Olfactory learning was assessed using proboscis extension reflex (PER) conditioning and visual (colour) learning was examined using a well-established free-flying paradigm. Our results showed neither a correlation, nor a trade-off, in individual performance for learning tasks using different sensory modalities. However, there was considerable variation among workers within each colony in their performance in both learning tasks. This extent of interindividual variation in learning ability across sensory modalities could be adaptive for colonies dealing with changeable foraging conditions. There was also significant intercolony variation in final task performance level in the olfactory learning task, and both the strength and persistence of blue preference in the colour learning task. This is the first study to demonstrate variation in olfactory learning performance across multiple bumblebee colonies using PER conditioning, suggesting this is an effective paradigm for assessing associative olfactory learning performance both within and among colonies.     

Plant-derived visual signals may protect beetle herbivores from bird predators

Insect herbivores often use chemical signals obtained from their food plants to deter enemies and/or attract sexual partners. Do plant-based visual signals act similarly, i.e., repel consumers' enemies and appeal to potential mates? We explored this question using the pollen-feeding beetle Pygopleurus israelitus (Glaphyridae), a specialized pollinator of Anemone coronaria's chemically defended red-morph flowers. We presented dead beetles, which had fed either on anemones or on cat food, to young domestic chicks on a red (anemone-like) or a green (leaf-like) background. We determined whether the beetles' background color and diet affected the chicks' feeding. Cuticle surface extracts from anemone-fed beetles, but not from cat food-fed beetles, contained a secondary metabolite characteristic of anemones. Latencies to the first picking up and consuming of beetles from green backgrounds were shorter than of beetles from red backgrounds. The picking up order of beetles also indicated that prey from the green background was preferred. The chicks retained this preference when re-tested, 3 days later. Handling times of anemone-fed beetles were longer than of cat food-fed beetles. A previous study showed that glaphyrids improve their mate-finding prospects by orienting to large red anemone flowers. Here, female beetles preferred cat food-fed to anemone-fed males in mate-choice assays, thus anemone-derived chemicals did not increase mating success. Instead, the combined results indicate that A. coronaria's red flowers provide a visual signal that may both deter its herbivore's predators and attract its mates. To our knowledge, this is the first experimental evidence for a potential protective role of plant-derived visual signals for insect herbivores/pollinators.     

Multimodal signals increase active space of communication by wolf spiders in a complex litter environment

Multimodal signals may compensate for environmental constraints on communication, as signals in different modalities vary in efficacy. We examined the influence of complex microhabitats on transmission of vibratory and visual signals of courting male Schizocosa ocreata wolf spiders (Araneae: Lycosidae) with laser Doppler vibrometry (LDV) and behavioral observations in lab and field. We measured maximum potential detection distance of visual and vibratory signals by females in laboratory mesocosms, recorded vibration signal attenuation on different substrates, and estimated transmission distances for male vibration signals in the field. We also determined effective line-of-sight visual detection distances in the field with laser distance measures. Together, these data were used to estimate the potential and effective active space of multimodal signals. LDV measures show leaves are highly conductive substrates for wolf spider vibratory signals compared to others (soil, wood, rock). For both visual and vibratory modes, lab estimates of maximum potential distance for signal transmission and detection (behavior studies) exceeded estimates of effective active space (signal attenuation, “vanishing point,” and “line-of-sight” measures). Field estimates of transmission distance for signal modes overlap, such that in close range (<20 cm), vibratory signals are more likely to be detected, while farther away, visual signals are more likely to be seen. These findings thus support current hypotheses regarding how multimodal communication might extend the range of overall signal active space or compensate for environmental constraints.     

Complex signal function: developing a framework of testable hypotheses

The basic building blocks of communication are signals, assembled in various sequences and combinations, and used in virtually all inter- and intra-specific interactions. While signal evolution has long been a focus of study, there has been a recent resurgence of interest and research in the complexity of animal displays. Much past research on signal evolution has focused on sensory specialists, or on single signals in isolation, but many animal displays involve complex signaling, or the combination of more than one signal or related component, often serially and overlapping, frequently across multiple sensory modalities. Here, we build a framework of functional hypotheses of complex signal evolution based on content-driven (ultimate) and efficacy-driven (proximate) selection pressures (sensu Guilford and Dawkins 1991). We point out key predictions for various hypotheses and discuss different approaches to uncovering complex signal function. We also differentiate a category of hypotheses based on inter-signal interactions. Throughout our review, we hope to make three points: (1) a complex signal is a functional unit upon which selection can act, (2) both content and efficacy-driven selection pressures must be considered when studying the evolution of complex signaling, and (3) individual signals or components do not necessarily contribute to complex signal function independently, but may interact in a functional way.Communicated by A. Cockburn     

Relative contribution of dietary carotenoids and vitamin E to visual and chemical sexual signals of male Iberian green lizards: an experimental test

Carotenoid-based sexual ornaments are widespread, but the role of carotenoids as honest signalers in the trade-off between coloration and antioxidant protection remains controversial. It has been suggested that the function of carotenoids might not be an antioxidant per se, but that colorful carotenoids may indirectly reflect the levels of nonpigmentary antioxidants, such as melatonin or vitamin E. We experimentally fed male Iberian green lizards (Lacerta schreiberi) additional carotenoids or vitamin E alone, or a combination of carotenoids and vitamin E dissolved in soybean oil, whereas a control group only received soybean oil. We examined the effects of the dietary supplementations on characteristics of lizard sexual coloration and of the chemical profile of femoral gland secretions. Results indicated that both carotenoids and vitamin E in the diet increased the expression of some visual signals (head and chest, but not dorsum) in comparison to controls. However, different traits were differentially affected, and in many cases, the addition of vitamin E, alone or in combination with carotenoids, had a greater effect on the expression of coloration than the addition of carotenoids alone, even for carotenoid-dependent ornaments. Our results support the idea that other nonpigmentary antioxidants, such as vitamin E, are needed in addition to carotenoids to increase the expression of coloration of L. schreiberi lizards. Therefore, coloration may only indirectly reflect the levels of nonpigmentary antioxidants. In contrast, an increase in dietary nonpigmentary antioxidant vitamin E was directly reflected in the chemical signals. Because of an observed concordance between visual and chemical signals, we suggest that both may be used in different contexts albeit conveying similar messages in different sensory channels.     

Movement signal choreography unaffected by receiver distance in the Australian Jacky lizard, <Emphasis Type="Italic">Amphibolurus muricatus</Emphasis>

Theory explains the structure of animal signals in the context of the receiver sensory systems, the environment through which signals travel and their information content. The influence of signalling context on movement-based signalling strategies is becoming clearer. Building upon recent findings that demonstrated changing environmental plant motion conditions resulted in a change of signalling strategy by the Australian lizard Amphibolurus muricatus, we examined whether receiver distance also influences signalling strategies. We found that signalling lizards did not modify their introductory tail flicking in response to distant viewers in the absence of competing, irrelevant plant image motion despite significant reductions in signal structure at the eye of the viewer. The magnitude of resultant effect sizes strongly suggests that receiver distance does not contribute to signalling strategies as much as the presence of motion noise in the environment.