Effects of traffic noise on tree frog stress levels,immunity, and color signaling

During the last decade, many studies have focused on the detrimental effects of noise pollution on acoustic communication. Surprisingly, although it is known that noise exposure strongly influences health in humans, studies on wildlife remain scarce. In order to gain insight into the consequences of traffic noise exposure, we experimentally manipulated traffic noise exposure as well as the endocrine status of animals to investigate physiological and phenotypic consequences of noise pollution in an anuran species. We showed that noise exposure increased stress hormone level and induced an immunosuppressive effect. In addition, both traffic noise exposure and stress hormone application negatively impacted H. arborea vocal sac coloration. Moreover, our results suggest profound changes in sexual selection processes because the best quality males with initial attractive vocal sac coloration were the most impacted by noise. Hence, our study suggests that the recent increases in anthropogenic noise worldwide might affect a broader range of animal species than previously thought, because of alteration of visual signals and immunity. Generalizing these results to other taxa is crucial for the conservation of biodiversity in an increasingly noisy world.     

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.     

Strong responsiveness to noise interference in an anuran from the southern temperate forest

Animals adopt different strategies to communicate by means of sound in noisy environments. Some animals increase, while others decrease, their vocal activity in the presence of interference. Anuran amphibians from diverse latitudes exhibit both kinds of responses. Recent studies have shown that males of Batrachyla taeniata and Batrachyla antartandica from the temperate austral forest do not call in response to the presentation of advertisement calls of sympatric congeneric species, but their responsiveness to other kinds of interference has not been tested. To explore the diversity in responsiveness to acoustic intrusion in a single species, we exposed males of B. taeniata to prolonged prerecorded natural abiotic noises of wind, creek, and rain and to a band-pass noise centered at 2,000 Hz, at 67 dB sound pressure level (SPL). The subjects drastically increased their call rate when exposed to all four sounds. Frogs also responded by augmenting their vocal activity to exposures of band-pass noise at increasing intensities (55–79 dB SPL). The increase in vocal activity in response to noise is strong relative to those of other anurans from the temperate forest studied previously under similar exposures. These results reveal a remarkable activation of vocal response to acoustic interference of continuous abiotic noise, which would allow compensating for limitations in the active communication space under background sounds. This strategy contrasts with the decrease in vocal output amid interference from heterospecific signals reported formerly for this frog, a tactic that would restrict energy expenditure to relevant acoustic competition with conspecifics.     

Effect of visual background complexity and light level on the detection of visual signals of male <Emphasis Type="Italic">Schizocosa ocreata</Emphasis> wolf spiders by female conspecifics

For visual signaling to be effective, animal signals must be detected and discriminated by receivers, often against complex visual backgrounds with varying light levels. Accordingly, in many species, conspicuous visual displays and ornaments have evolved as a means to enhance background contrast and thereby increase the detection and discrimination of male courtship signals by females. Using video playbacks, we tested the hypothesis that visual courtship displays and leg decorations of male Schizocosa ocreata wolf spiders are more conspicuous against complex leaf-litter backgrounds. Video exemplars of courting males with manipulated leg tufts were superimposed on different backgrounds (complex leaf litter in sun or shade, featureless gray background) and presented to female spiders. Females were more likely to orient to males presented against lighter backgrounds (litter in sun, gray) than the darker ones (litter—shade). Males with larger tufts were also more likely to be detected, as latency to orient was shortest for enlarged and longest for removed tufts. Latency of females to approach was shorter against lighter backgrounds, and approach latency was longest for males without tufts. Female receptivity scores were significantly greater for males against lighter backgrounds, and males with larger tufts had higher scores. These results suggest that both complexity and light level of display backgrounds affect the detection of male visual courtship signals by females and that aspects of the male phenotype may increase chances of detection (and receptivity) against visually complex backgrounds.     

Here comes the sun: multimodal displays are associated with sunlight incidence

Conspicuousness of courtship signals in animals likely evolved to maximize mate attraction while minimizing predator detection. It is assumed, though largely unknown, that environmental and luminosity conditions affect the detectability of ornaments and motor displays and could thus strongly influence behavior. We combined visual models and behavioral observations to test whether the multimodal display of the blue-black grassquit (Volatinia jacarina) is influenced by environmental conditions, predicting that males should display more often in moments with high sunlight incidence upon their bodies. By displaying in such a context-dependent fashion, males would be able to maximize conspicuousness of their iridescent blue-black plumage and avoid displaying continuously, since the latter would involve higher energetic investment. We recorded the rates of both complete displays (leap with singing) as well as incomplete ones (singing while perched) for males during repeated 30-min focal observations in varying environmental situations in the field. We found that when bathed directly in sunlight, males increased their rates of displays, tending to exhibit more complete rather than incomplete displays in this condition and suggesting a potential trade-off between display types. Our results suggest that animals may adjust the timing and precise location of signal activity to improve the efficiency or likelihood of detection of some signal elements.     

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     

Age-related changes in an insect mating signal have no effect on female choice

The structure of male mating signals is often influenced by age. The causes and consequences of age-based signal variation have been much studied in visual, acoustic, and chemical signaling modalities, but are less explored in species that use vibrational signals for mate attraction. However, the complex structure of many vibrational signals makes them ideal for investigating the relationships between age, signal variation, and patterns of female choice. In the thornbug treehopper, Umbonia crassicornis, females mate more often with older males, but the mechanism underlying older male mating success is unknown. Our goals in this study were to determine whether male vibrational mate advertisement signals vary with age, and, if so, whether females prefer the signals of older males. We recorded male signals over four consecutive weeks beginning at the onset of signaling (a period spanning most of the male reproductive lifespan), and measured ten temporal, spectral, and energy-related parameters from each signal. Several features of male signals changed markedly with age. However, females responded similarly to signals representing males of different ages, indicating that they do not favor older males on the basis of long distance mate advertisement signals. Nonetheless, the results reveal that even in short-lived, determinate growth species age can have surprisingly large effects on mating signals, and we discuss some factors that may contribute to age-related signal variability in U. crassicornis.     

Information content is more important than sensory system or physical distance in guiding the long-term evolutionary relationships between signaling modalities in Sceloporus lizards

Long-term signal evolution is shaped by a variety of selective pressures including the need to convey additional information or to improve message transfer to specific receivers or through multiple environments. Here, we test the relative importance of information and sensory modality in shaping the long-term evolution of multimodal signals in Sceloporus lizards. To broadcast identity at territorial boundaries, male Sceloporus use both visual motion (headbob) and chemical signals, whereas they use color (blue belly patches) to signal aggression. Using modern phylogenetic comparative methods, we found a negative correlation between evolutionary changes in visual motion (headbobs) and chemical (femoral pore) signals, but only indirect ties between the evolution of color and motion signals (both of which are perceived visually) through viviparity, and no evidence of an evolutionary link between color and chemical signals. We also find a negative correlation between arboreality and chemical signals. Thus, information content (in this case, broadcasting individual identity versus signaling aggression) appears to play a more important role than sensory modality or physical distance in guiding long-term signal evolution. Additional insights into the underlying evolutionary processes are described, illustrating the utility of a phylogenetic approach.     

Habitat-induced changes in song consistency affect perception of social status in male chickadees

The ability of male black-capped chickadees to maintain consistent internal structure between successive iterations of their songs is affected by both their social rank and the quality of their habitat. Lab studies reveal that female chickadees discriminate between songs of dominant and subordinate males, which vary in acoustic structure. We investigate whether males also rely on acoustic structure to assess rival quality during agonistic interactions, and whether habitat-induced differences in song consistency affect the perception of male rank. We conducted a playback experiment to simulate territorial intrusions by dominant, stimuli males into the territories of dominant, subject males; stimuli males were recorded either in low-quality (young forest) or high-quality (mature forest) habitats. Stimuli from low-quality habitat had lower song consistency than those from high-quality habitats, despite being recorded from males of equivalent social rank. Subject males for playbacks (also socially dominant males) were chosen from either habitat type. Subject males in mature forest responded less to young-forest stimuli compared to mature-forest stimuli, despite the stimuli in both cases being recorded from dominant males. Conversely, male subjects in young forest did not differentiate between stimuli, but their response to both stimuli was lower than that of mature-forest subject males to mature-forest stimuli. We demonstrate that the ability to maintain internal song structure in the black-capped chickadee constitutes a signal that appears to be used by males to assess the level of threat of intruders, and that this perception is affected by habitat from which the stimulus males were recorded.     

Salience of multimodal flower cues manipulates initial responses and facilitates learning performance of bumblebees

Visual and olfactory cues are the first interface between flowers and their visitors and are adaptations to facilitate successful pollination. Initial responses to and associative learning of multimodal cues by flower visitors are based on the perception of colours and volatiles. In this study, we tested how visual, olfactory and multimodal stimuli affect the behaviour of bumblebees (Bombus terrestris) and correlated the properties of 28 stimuli in relation to the insects’ sensory equipment to these behaviours. Initial responses and associative learning were recorded using a radio frequency identification system, tracking the visitation sequences of individual bumblebees to artificial flowers treated with naturally occurring pigments and/or volatiles. The salience of the stimuli was evaluated as the colour contrast to the background and as electroantennogram responses. The main finding was that both initial responses and learning performance were positively correlated to the salience of the stimuli, suggesting that salience is a key feature of flower cues in the interactions with insects. The salience of compound stimuli consisting of two or more pigments and/or volatiles was largely additively determined by the saliences of individual compounds. Potentially, the valence of the stimuli may interfere with the positive relationship between salience and behaviour, which is indicated by our results, too. The salience of multimodal cues depends on the species-specific equipment of visual and olfactory receptors and thus enables flowers to be advertising for some but rather inconspicuous for other flower visitors.     

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.     

Effects of multiple-speaker playbacks on aggressive calling behavior in the treefrog <Emphasis Type="Italic">Dendropsophus ebraccatus</Emphasis>

In addition to producing signals, males of chorusing species also act as receivers by adjusting properties of their vocalizations in response to those of other nearby individuals. Although it is likely that males are responsive to more than one other individual, most playback studies investigating male response have involved dyads in which vocal responses are measured to stimuli presented from a single speaker. In this study, I explored changes in both the propensity to give aggressive calls and the temporal properties of those calls in response to the playback of multiple aggressive call stimuli in the treefrog Dendropsophus ebraccatus. I found that males were sensitive to both the number of simulated aggressive callers and their specific call characteristics. Males generally gave a highly aggressive response to the first stimulus presented, but their response to the modification of this stimulus by the addition or subtraction of a simulated competitor depended on the degree of aggressiveness of the stimuli. Males tended to decrease their aggressive responses when either a more aggressive call was silenced or a less aggressive call was added and to increase their aggressive responses in the opposite situation. Aggressive calling in this species is clearly affected by complex changes in the social environment and I suggest that future studies explore these issues in other species to improve the understanding of communication interactions.     

A game theoretic approach to multimodal communication

Over the last few decades the animal communication community has become increasingly aware that much communication occurs using multiple signals in multiple modalities. The majority of this work has been empirical, with less theoretical work on the advantages conferred by such communication. In the present paper, we ask: Why should animals communicate with multiple signals in multiple modalities? To tackle this question we use game theoretic techniques, and highlight developments in the economic signaling literature that might offer insight into biological problems. We start by establishing a signaling game, and investigate signal honesty under two prevailing paradigms of honest communication – costly signaling and cheap talk. In both paradigms, without further constraint, it is simple to show that anything that can be achieved with multiple signals can be achieved with one. We go on to investigate different sets of possible constraints that may make multiple signals and multimodal signals in particular more likely to evolve. We suggest that constraints on cost functions and bandwidths, orthogonal noise across modalities, strategically distinct modes, multiple qualities, multiple signalers, and multiple audiences, all provide biologically plausible scenarios that theoretically favor multiple and multimodal signaling.     

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.     

Effects of Traffic Noise on Occupancy Patterns of Forest Birds

Abstract: Noise may drive changes in the composition and abundance of animals that communicate vocally. Traffic produces low‐frequency noise (<3 kHz) that can mask acoustic signals broadcast within the same frequency range. We evaluated whether birds that sing within the frequency range of traffic noise are affected by acoustic masking (i.e., increased background noise levels at the same frequency of vocalizations reduce detection of vocalization) and are less abundant in areas where traffic noise is loud (44–57 dB). We estimated occupancy, the expected probability that a given site is occupied by a species, and detection probabilities of eight forest‐breeding birds in areas with and without traffic noise as a function of noise and three measures of habitat quality: percent forest cover, distance from plot center to the edge of forest, and the number of standing dead trees or snags. For the two species that vocalize at the lowest peak frequency (the frequency with the most energy) and the lowest overall frequency (Yellow‐billed Cuckoo [Coccyzus americanus] and White‐breasted Nuthatch [Sitta carolinensis]), the presence of traffic noise explained the greatest proportion of variance in occupancy, and these species were 10 times less likely to be found in noisy than in quiet plots. For species that had only portions of their vocalizations overlapped by traffic noise, either forest cover or distance to forest edge explained more variation in occupancy than noise or no single variable explained occupancy. Our results suggest that the effects of traffic noise may be especially pronounced for species that vocalize at low frequencies.     

Giant pandas attend to androgen-related variation in male bleats

Although androgen-dependant traits are predicted to signal overall male quality, no study has examined the response of a nonhuman animal to variation in a known acoustic cue to male androgen levels (steroid hormones that are key drivers of male sexual behaviour). Here, we use a single-speaker approach to present male and female giant pandas with re-synthesised male bleats representing callers with high and low androgen levels. Our results revealed that male and female giant pandas had significantly greater-looking responses, spent more time pacing, and were faster to respond to playbacks of bleats simulating high androgen males. When we analysed the sexes separately, a slightly different response pattern was revealed: whereas males and females still had significantly greater-looking responses and were faster to respond to bleats simulating high androgen males, only male giant pandas tended to spend more time pacing. These findings suggest that vocal cues to male androgen levels are functionally relevant to male and female giant pandas during the breeding season, and constitute the first demonstration that a nonhuman animal could be using a vocal signal to assess male hormonal state. We go on to discuss the ecological relevance of signalling androgen levels in this species’ sexual communication and the possible application of our results to conservation breeding.     

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.     

No relationship between long-distance acoustic mate attraction signals and male fertility or female preference in spring field crickets

To father offspring, a male must succeed at two processes of sexual selection: (1) mate with a female and (2) fertilize her eggs. We investigated the relationships between pre- and post-copulatory male traits and female mating responses in wild-captured and laboratory-reared spring field crickets, Gryllus veletis. The phenotype-linked fertility hypothesis suggests that females may receive a direct benefit, enhanced fertilization efficiency, by mating with males that signal attractively. We measured fine-scale components of male acoustic mate attraction signals as well as how much time males spent signalling, measured female preference for males in mating trials and then quantified sperm number and viability. We found no relationship between male signalling traits and male fertility or female preference, providing no evidence for the phenotype-linked fertility hypothesis. We also found no difference in sperm metrics between wild-captured and laboratory-reared males. While female crickets may receive benefits by choosing males based on acoustic signal characteristics, whether the benefits are a result of genetic quality, seminal fluid contents or some other male trait remains unknown.     

Shouting the odds: vocalization signals status in a lizard

Many species possess multiple sexually dimorphic traits, which incorporate different sensory modalities (e.g., acoustic, olfactory and visual), although their relative roles in sexual selection and in determining reproductive success are still poorly understood for most taxa. We assessed the role of multiple male traits, including one acoustic (dominant call frequency) and one visual (yellow throat patch) trait, in residency advertisement, contest behavior, and breeding success in barking geckos (Ptenopus garrulus garrulus). We show that male barking geckos maintain largely exclusive home ranges, with a trend for larger males to maintain larger home ranges. We also show that larger males have a lower dominant calling frequency. When aggressive behavior was elicited in the field using a recorded call of average frequency, resident males with low frequency calls were more likely to respond aggressively and charge the speaker compared to males with high frequency calls. However, body size and small relative throat patch size, rather than call frequency, were the best predictors of overall aggressiveness. Body size was also the best predictor of whether males bred. We suggest that call frequency in this crepuscular species constitutes an effective long-range signal of body size, used by males for remote rival assessment and to advertise home range boundaries in low-light environments.