Social Information Embedded in Vocalizations Induces Neurogenomic and Behavioral Responses

Social cues facilitate relationships within communities. Zebra finches form long-term stable mate pairs and produce offspring within a multi-family, multi-generational community that can include hundreds of birds. Males use song to communicate in this complex environment. Males sing as part of their courtship display but also abundantly throughout each day, suggesting a role for their vocal signature outside of a reproductive context. One advantage of a vocal social cue is that it can be exchanged when birds are out of visual contact, as regularly occurs in a zebra finch community. Previous works have demonstrated that females hearing song are affected by their social relationship to the bird singing it, and the immediate social context. Here, we probed the question of whether or not the song itself carried social information, as would be expected from the situations when males sing outside of view of the female. We quantified behavioral and neurogenomic responses to two songs we predicted would have distinct “attractive” qualities in adult females housed in either mixed sex or female-only social communities. Our results show that only mixed sex-housed females show distinctive behavioral and neurogenomic responses to attractive songs. These data are consistent with the idea that the acoustic properties of song carry social information, and that the current social situation modulates the neural and behavioral responses to these signals.     

Sexual Differences in the Behavioral Response of Túngara Frogs, Physalaemus pustulosus, to Cues Associated with Increased Predation Risk

Engaging in mating behaviors usually increases exposure to predators for both males and females. Anti‐predator strategies during reproduction may have important fitness consequences for prey. Previous studies have shown that individuals of several species adjust their reproductive behavior according to their assessment of predation risk, but few studies have explored potential sexual differences in these strategies. In this study, we investigate whether the acoustic cues associated with predatory attacks or those associated with predators themselves affect the mating behavior of female and male túngara frogs, Physalaemus pustulosus. We compared the responses of females approaching a mate and those of calling males when exposed to mating calls associated with sounds representing increased hazard. When presented with mating calls that differed only in whether or not they were followed by a predation‐related sound, females preferentially approached the call without predation‐related sounds. In contrast to females, calling males showed greater vocal response to calls associated with increased risk than to a call by itself. We found significant differences in the responses of females and males to several sounds associated with increased hazard. Females behaved more cautiously than males, suggesting that the sexes balance the risk of predation and the cost of cautious mating strategies differently.     

Coevolution of Male and Female Response Preferences to Sexual Signals in Music Frogs

Male signaling influences both female choice and male-male competition. Although male signaling characteristics and female preferences have been shown to coevolve in many species, few studies have examined whether male signal characteristics and male receiver responses related to male-male competition also coevolve. The present study tested the hypothesis that male and female signal receiver preferences may coevolve in parallel for frogs in the genus Babina by comparing the acoustic structure of male advertisement calls of four closely related and geographically isolated Babina species. Then we assessed the behavioral responses of both male and female B. daunchina(Emei music frog) to male call playbacks from each of the four species. The results support the hypothesis that male and female signal receiver preferences have coevolved in this species. Specifically, both male and female B. daunchina respond strongly to the heterospecific calls of B. hainanensis, suggesting that preexisting biases exist in both females and males. Both male and female individuals showed a slight response to the calls of B. adenopleura while no response was evoked by the calls of B. lini. The manifestation of similar response profiles in male and female B. daunchina to the calls of the four species support the idea that male and female signal receiver preferences evolved in parallel and that the origin of these receiver biases reflects adaptations dependent on the same neural and cognitive systems in both sexes.     

Differential Behavioral Responses to Water-Borne Cues to Predation in Two Container-Dwelling Mosquitoes

Larvae of the mosquito Toxorhynchites rutilus (Coquillett) prey upon other container-dwelling insects, including larvae of Aedes albopictus (Skuse), which is native to Asia but was introduced into the United States, and on the native tree hole mosquito Ochlerotatus triseriatus (Say). Previous work has established that O. triseriatus adopts low-risk behaviors in the presence of predation risk from T. rutilus. It is unknown whether introduced A. albopictus show a similar response to this predator. Behavior of fourth instars of A. albopictus or O. triseriatus was recorded in water that had held either A. albopictus or O. triseriatus larvae alone (control) and in water that had held T. rutilus larvae feeding on either A. albopictus or O. triseriatus (predation). Activity and position of larvae were recorded in 30-min instantaneous scan censuses. In response to water-borne cues to predation, O. triseriatus adopted low-risk behaviors (more resting, less feeding and movement), but A. albopictus did not change its behavior. We also tested the species specificity of the cues by recording the behavior of A. albopictus in water prepared using O. triseriatus and vice versa. O. triseriatus adopted low-risk behaviors even in predation water prepared by feeding T. rutilus with A. albopictus, but A. albopictus did not alter its behavior significantly between predation and control treatments prepared using O. triseriatus. Thus, A. albopictus does not seem to respond behaviorally to cues produced by this predator and may be more vulnerable to predation than is O. triseriatus.     

Threat-Sensitive Behavioral Responses to Concentrations of Water-Borne Cues from Predation

Aquatic organisms often detect predators via water-borne chemical cues, and respond by showing reduced activity. Prey responses may be correlated with the concentration of predation cues, which would result in graded antipredator behavioral responses that adjust potentially costly behavioral changes to levels that are commensurate with the risk of predation. Larvae of the predatory mosquito Toxorhynchites rutilus prey upon other container-dwelling insects, including larvae of the mosquito Ochlerotatus triseriatus. Previous work has established that O. triseriatus reduce movement, foraging, and time below the surface, and increase the frequency of resting at the surface, in the presence of water-borne cues from predation by T. rutilus. We tested whether these responses by O. triseriatus are threat sensitive by recording behavior of fourth instar larvae in two runs of an experiment in which we created a series of concentrations (100, 10, 1, 0.1, and 0.01% and 100, 70, 40, 20, and 10%) of water that had held either O. triseriatus larvae alone (control) or a T. rutilus larva feeding on O. triseriatus (predation). We also tested whether associated effects on time spent feeding are threat sensitive by determining whether frequencies of filtering or browsing are also related to concentration of cues. The frequencies of resting and surface declined, whereas frequency of filtering (but not browsing) increased more rapidly with a decrease in concentration of predation cues compared with control cues. Thus, O. triseriatus shows a threat sensitive behavioral response to water-borne cues from this predator, adjusting its degree of behavioral response to the apparent risk of predation.     

Behavioral Response of Western Flower Thrips to Visual and Olfactory Cues

Behavioral responses of Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) to visual and olfactory cues were assessed in a cylindrical black box and a Y-tube olfactometer. Frankliniella occidentalis preferred circular shapes to other five geometrical patterns (rectangle, triangle, inverted triangle, diamond, and modified circle imitating flower petals) in multiple choice tests. In pair wise choice tests, the thrips preferred the yellow artificial flower shape to the geometrical patterns tested. Frankliniella occidentalis stayed on the artificial flower about four times longer than on the geometrical patterns. Higher numbers of thrips responded to a combination of p-anisaldehyde and artificial flower compared to the arm with only the olfactory or the visual cue. These results suggest that shape is an important cue for F. occidentalis.     

General Visual and Contingent Thermal Cues Interact to Elicit Attraction in Female Aedes aegypti Mosquitoes

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Parturition Signaling by Visual Cues in Female Marmosets (Callithrix jacchus)

New World monkeys have polymorphic color vision, in which all males and some females are dichromats, while most females are trichromats. There is little consensus about which selective pressures fashioned primate color vision, although detection of food, mates and predators has been hypothesized. Behavioral evidence shows that males from different species of Neotropical primates seem to perceive the timing of female conception and gestation, although, no signals fulfilling this function have been identified. Therefore, we used visual models to test the hypothesis that female marmosets show chromatic and/or achromatic cues that may indicate the time of parturition for male and female conspecifics. By recording the reflectance spectra of female marmosets’ (Callithrix jacchus) sexual skin, and running chromatic and achromatic discrimination models, we found that both variables fluctuate during the weeks that precede and succeed parturition, forming “U” and inverted “U” patterns for chromatic and achromatic contrast, respectively. We suggest that variation in skin chroma and luminance might be used by female helpers and dominant females to identify the timing of birth, while achromatic variations may be used as clues by potential fathers to identify pregnancy stage in females and prepare for paternal burdens as well as to detect oestrus in the early post-partum period.     

Dissecting the Contribution of Sensory Cues to Directional Responses by Female Crickets in a two-Loudspeaker Paradigm

Sound localization in insects is typically investigated using single loudspeaker paradigms to examine the impact of sensory cues. Here, the contribution of specific cues to turning responses in a two-loudspeaker paradigm equivalent to a choice situation was examined. For that, several sensory cues were systematically varied to determine their respective contribution to the strength of the turning response in female crickets. In three experimental sets (1) the temporal arrangement of chirp patterns broadcast from two speakers, (2) the relative timing of chirps and (3) the impact of phase differences of the carrier frequency were varied at different intensity levels between both speakers. While the arrangement of chirp patterns had little influence on the strength of turning responses, time delays up to 20 ms and phase differences of 90° and 270° clearly affected directional turning at otherwise equal intensities. In all three sets of experiments turning responses were sensitive to intensity differences and saturated at +/? 6 dB. Turning responses due to timing of pulses or phase differences were compensated by intensity differences of 2–3 dB. Building on a large body of literature on peripheral and central processing it was possible to assign the observed effects to specific processing stages in the auditory pathway of crickets.     

Sex-linked Correlated Responses in Female Reproductive Traits to Selection on Male Eye Span in Stalk-eyed Flies

Coevolution between male and female traits can result from correlatedresponses to selection or correlated selection on geneticallyindependent traits. This study examines the possibility thattraits involved in precopulatory sexual selection may influencethe evolution of traits involved in postcopulatory sexual selectiondue to the existence of correlated selection or correlated responsesto selection. Artificial selection on male eye span in Cyrtodiopsisdalmanni, a sexually dimorphic stalk-eyed fly, is used to testfor correlated changes in reproductive traits of male and femaleflies. Flies from replicate lines that had been under selectionfor 57 generations were matched for age and genotyped at fourX-linked microsatellite loci. Egg number and testis size increasedwith age, but did not differ among lines. Spermathecal areasand duct lengths differed among replicates, but not among selectiontreatments. Female relative eye span, size of the ventral receptacleand egg size exhibited significant correlated responses to selectionon male relative eye span. The absence of any change in spermlength or testis size between lines indicates that changes infemale traits are unlikely due to correlated selection mediatedby sperm competition. Significant effects of X-linked microsatellitegenotypes indicate instead that the correlated responses toselection were due, in part, to X-linked genes in linkage disequilibriumor that exhibit pleiotropy. The presence of nonadditive alleliceffects on genetically correlated female traits combined withadditive allelic effects on a male ornament provides a previouslyunrecognized mechanism by which genetic variation could be maintaineddespite strong sexual selection.     

Sexual Discrimination Using Visual Cues in the Checkered White Butterfly (Pieris protodice)

The cues used by ♂♂ and ♀♀ of the checkered white butterfly, Pieris protodice, were explored using an assay that involved timing the responses of free-flying butterflies to tethered animals (“angling”). The models included ones that were made from the wings of ♂♂ and ♀♀ that had been extracted in a dilute ammonia solution. This procedure removes an ultraviolet-absorbing pigment from the wings and renders them more ultraviolet reflectant than normal without altering any other aspect of their coloration. The results show that both sexes make sexual discriminations using the sexual dimorphism in ultraviolet reflectance found in this species rather than using differences in the melanic markings on the wings, movement patterns, or chemical signals.     

Formant Frequencies are Acoustic Cues to Caller Discrimination and are a Weak Indicator of the Body Size of Corncrake Males

Source–filter theory assumes that calls are generated by a vocal source and are subsequently filtered by the vocal tract. The air in the vocal tract vibrates preferentially at certain resonant frequencies, called formants. Formant frequencies can be a good indicator of the caller's characteristics, such as sex, age, body size or individual identity. Although source–filter theory was originally proposed for mammals, formants are also observed in birds, and some bird species have been shown to perceive formants. In this study, we evaluated the hypotheses that formant frequencies (1) are an indicator of body size and (2) can be used for individual discrimination by a nocturnal bird species, the corncrake (Crex crex). We analysed calls of 104 males from Poland and the Czech Republic. Linear regression models showed that the males with a longer head (including the bill length) had a significantly lower formant dispersion and lower fourth and fifth formant frequencies. However, we found no significant relationships between body weight and any filter‐related acoustic measurement. The formant frequencies had smaller within‐ than between‐individual coefficients of variation. This characteristic of the formant frequencies implies a high potential for individual coding. A discriminant function analysis correctly assigned 94.8% of the calls to the caller based on formants from second to fifth. Our results indicated that the formant frequencies are a weak indicator of the body size of the sender in the corncrake. However, even weak dependence between body size and acoustic properties of signal may be important in natural selection process. Alternatively, such a weak dependence may be observed, because receivers ignore the acoustical, formant‐based cues of body size. Simultaneously, the formants might potentially provide acoustic cues to individual discrimination and could be used to census and monitoring tasks.     

Male Advertisement and Female Choice in Frogs: Recent Findings and New Approaches to the Study of Communication in a Dynamic Acoustic Environment

SYNOPSIS. Typically, anuran amphibians communicate in a complexacoustic environment to which the calls of many males contribute.Although research has demonstrated that male vocal behavioris responsive to changes in this environment, a more thoroughunderstanding of male-male interactions should benefit fromthe use of computer based systems for data acquisition and interactiveplayback. I discuss how I have used such systems in studiesof note timing behavior, unison bout singing, aggressive behaviorand female choice. In addition, I indicate how energetic constraintsmay be involved in shaping the temporal dynamics of chorusing     

Role of Olfactory and Visual Cues in the Attraction/Repulsion Responses to Conspecifics by Gregarious and Solitarious Desert Locusts

Desert locusts [Schistocerca gregaria Forskål (Orthoptera, Acrididae)] change phase in response to population density: solitarious insects avoid one another, but when crowded they change to the gregarious phase and aggregate. The attraction/repulsion responses of gregarious and solitarious locusts maintain phase differences in locust populations. Despite considerable research, the cues for aggregation are poorly understood; moreover, the repulsion response of solitarious locusts has not previously been investigated. This study analyzes the role of visual and olfactory stimuli in triggering these different responses to conspecifics. Isolation-reared insects were repelled by both olfactory and visual stimuli from other locusts. Crowd-reared insects were attracted by the combination of olfactory and visual cues. In addition, olfactory stimuli affected other behaviors in both phases, and behavioral differences between isolation- and crowd-reared locusts were clear even in the absence of conspecifics. The sensory and neurological mechanisms underlying these responses are not well understood and will form the basis for neurobiological investigations of locust phase.     

不同物种雄性鸣声刺激下雌性凹耳蛙脑组织中ZENK的表达

通过免疫组化SABC法,研究在背景噪音刺激、雄性凹耳蛙(Odorrana tormota)声音刺激以及雄性大绿臭蛙(O. graminea)声音刺激下ZENK蛋白在雌性凹耳蛙脑部的表达。结果显示,上述三种声音刺激下雌性凹耳蛙的端脑、间脑和小脑区域均未发现ZENK蛋白的阳性细胞。在雄性凹耳蛙声音刺激下,雌性凹耳蛙中脑的视顶盖、脚间核、中脑深部核、被盖、半环隆枕以及延脑的孤束核、中缝核、网状核、网状结构、上橄榄核部位均有阳性细胞分布,在大绿臭蛙声音刺激下,这些部位的阳性细胞数量明显减少。本实验中ZENK蛋白阳性细胞表达部位的一部分是位于与两栖类处理听觉信息有关的中脑半环隆枕、被盖以及延脑的上橄榄核,由此可推断,在雌性凹耳蛙ZENK蛋白与听觉信息处理有着密不可分的联系。     

Predatory Cues Influence the Behavioral Responses and Metamorphic Traits of Polypedates maculatus(Anura: Rhacophoridae)

Mechanisms of predator detection and the influence of the presence of nonlethal predators on antipredator defense behavior and metamorphic traits were studied in the Indian tree frog, Polypedates maculatus. Exposure of P. maculatus tadpoles to chemical cues of caged predator(crabs, Barytelphusa spp.) fed with either conspecific or heterogeneric tadpoles, or were starved elicited defense behavior(by avoiding predator zone) in them. Such a behavior was not evident when exposed to predators housed in a glass beaker(visual cues). Both early(Gosner stage 27–28) and later(Gosner stage 35–36) stage tadpoles when exposed to caged predators(fed with conspecific tadpoles), prey tadpoles spent less time swimming and remained motionless for longer periods. Yet, the time spent by prey in feeding was unaffected. Further, the predator avoidance behavior exhibited by them was of the same intensity regardless of whether the caged predators were fed or starved implying the influence of predator's kairomones. Tadpoles reared with caged predator reached the metamorphic climax stage(MC stage; Gosner stage 42) earlier than those reared without a predator. Size at emergence(Gosner stage 46) was comparable in both the groups. The findings suggest that P. maculatus tadpoles assess predation risk chiefly by sensing kairomones of the predator in eliciting antipredator defense behaviors. Accelerated development and early metamorphosis without any compromise of the size at emergence may be due to their unaltered feeding activity.     

Recording Behavioral Responses to Reflection in Crayfish

Social behavior depends on sensory input from the visual, mechanical and olfactory systems. One important issue concerns the relative roles of each sensory modality in guiding behavior. The role of visual inputs has been examined by isolating visual stimuli from mechanical and chemosensory stimuli. In some studies (Bruski & Dunham, 1987: Delgado-Morales et al., 2004) visual inputs have been removed with blindfolds or low light intensity, and effects of remaining sensory modalities have been elucidated. An alternative approach is to study the effects of visual inputs in the absence of any appropriate mechanical and chemosensory cues. This approach aims to identify the exclusive role of visual inputs. We have used two methods to provide visual stimuli to crayfish without providing chemical and mechanical cues. In one method, crayfish are videotaped in an aquarium where half of the walls are covered in mirrors to provide a reflective environment, and the other half are covered in a non-reflective (matte finish) plastic. This gives the crayfish a choice between reflective and non-reflective environments. The reflective environment provides visual cues in the form of reflected images of the crayfish as it moves throughout half of the tank; these visual cues are missing from the non-reflective half of the tank. An alternative method is to videotape the behavior of crayfish in an aquarium separated by a smaller chamber at each end, with a crayfish in one small chamber providing visual cues and an inert object in the opposite small chamber providing visual input from a non-moving, non-crayfish source. Our published results indicate that responses of crayfish to the reflective environment depend on socialization and dominance rank. Socialized crayfish spent more time in the reflective environment and exhibited certain behaviors more frequently there than in the non-reflective environment; isolated crayfish showed no such differences. Crayfish that were housed in same-sex pairs developed a social rank of either dominant or subordinate. Responses to reflection differed between dominant and subordinate crayfish (May & Mercier, 2006; May & Mercier, 2007). Dominant crayfish spent more time on the reflective side, entered reflective corners more frequently and spent more time in reflective corners compared to the non-reflective side. Subordinate crayfish walked in reverse more often on the reflective side than on the non-reflective side. Preliminary data suggest similar effects from visual cues provided by a crayfish in a small adjoining chamber (May et al., 2008).Download video file.^{(129M, mp4)}