Carolynn L. Smith

Food-associated vocalizations in mammals and birds: what do these calls really mean?

Alarm calls and food-associated calls from a diverse range of species are said to be functionally referential, in that receivers can use these sounds to predict environmental events in the absence of other contextual cues. The evolutionary driver for referential alarm calls has been hypothesized to be the mutually incompatible escape behaviours required to avoid different predators. However, some species produce acoustically distinctive and referential alarm calls but do not show highly referential abilities in other domains. We examined whether food-associated calls in many species are likely to be functionally referential and whether they specifically communicate about characteristic features of food. Foodassociated calls are given in both feeding and nonfeeding contexts, and the types of information contained vary greatly. Most species do not produce unique calls for different foods; more common is variation in the call rate, which suggests that call structure reflects the callers’ internal state rather than the food type. We also examined the ultimate function of food-associated calls to evaluate whether there is a unifying explanation for the evolution of functionally referential food calls. Based on the literature, there does not appear to be a unifying function. In conclusion, while functionally referential foodassociated calls have been convincingly demonstrated in a few species, it is more common for these vocalizations to reflect arousal rather than additionally providing specific referential information about the feeding event. At this point, there is no compelling hypothesis to explain the evolution of functionally referential food-associated calls. Given the multiple functions of food-associated signals, we should not expect a unitary explanation.

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.

Tactical multimodal signalling in birds : facultative variation in signal modality reveals sensitivity to social costs

The presence of eavesdroppers within a communication network can increase the costs associated with signalling. Hence, selection should favour the ability to vary signal structure with social context. One possible mechanism is the flexible combination of the components that form a multimodal signal. This phenomenon clearly occurs in social mammals, particularly primates, and has been identified as one of the foundation elements for the evolution of complex communication. However, this flexibility in signal component composition in relation to social context has not previously been demonstrated in other taxa. Here we show that subordinate male fowl, Gallus gallus, show facultative variation in the structure of their multimodal signals. Intriguingly, signallers were not sensitive to the behaviour of the intended receivers (hens) but rather to the attentional state of eavesdropping rival males. Subordinates switched from multimodal displays (movements and calls) to unimodal (silent) displays when the alpha male was attentive. Unimodal and multimodal displays had equivalent efficacy in attracting hens, but multimodal signals were associated with more rapid approach by the alpha male and increased probability of severe attack. Variation in signal type is hence driven by social costs. This is the first demonstration of facultative multimodal signalling in birds.

Silent tidbitting in male fowl, Gallus gallus: a referential visual signal with multiple functions.

SUMMARY With the notable exception of bee dances, there are no established examples of multimodal referential signals. The food calls of male fowl, Gallus gallus, are functionally referential and the acoustic component of a multimodal display. However, the specificity of the receivers response to the visual component (tidbitting) has never been tested. Here we provide the first detailed analysis of tidbitting, and test the hypothesis that these characteristic movements are functionally referential. We conducted a playback experiment with five high-definition video stimuli: Silent tidbit, Matched-frequency motion in the opposite direction, Silent crows, Inactive male and Empty cage. Females searched for food more during Silent tidbitting than under any other condition, suggesting that this visual display specifically predicts the presence of food and hence has similar functional properties to food calls. Silent tidbitting was also singularly effective at evoking approach and close inspection, which may enhance signal memorability. These social responses suggest that the visual component of the display has the unique function of triggering assessment of signaler identity and quality as a potential mate. The acoustic and visual components are hence redundant as a food signal, but synergistic when additional functions are considered. These findings emphasize the perceptual complexity of multimodal displays and provide the first demonstration of multimodal referential signaling in a vertebrate.

On the function of an enigmatic ornament: wattles increase the conspicuousness of visual displays in male fowl

Males of many species perform elaborate displays in which multiple ornaments feature prominently. However, female preferences often depend upon both display movements and a subset of the ornaments. This response selectivity means that female choice cannot explain the function of nonpreferred ornaments. These structures may instead have an ancillary function (e.g. enhancing signal efficacy or modifying information content). Male junglefowl, Gallus gallus, possess multiple fleshy ornaments, which feature prominently during food-related displays (tidbitting). There is strong evidence for female choice based on display frequency and comb characteristics, but little evidence for choice based on wattles. Wattles are thin, elastic structures that hang loosely from a males lower mandibles and vary in size over a males lifetime. These structures swing rapidly during tidbitting, potentially increasing the area around the head and increasing image motion. Males also tidbit more vigorously with highly preferred food, increasing wattle displacement and thereby potentially affecting information content. We tested the prediction that wattles enhance signal efficacy and information content by conducting high-definition playbacks, using three-dimensional animations of tidbitting males with differing wattle properties. Results revealed that the food-searching response of receivers was robust to changes in wattle size and motion. Increased wattle displacement did not decrease orienting latency or increase food-searching duration, which suggests that wattles do not contribute significantly to information content. However, apparent wattle size significantly decreased orienting latency, demonstrating that wattles increase the conspicuousness of the tidbitting signal. These results suggest that wattles are maintained because they enhance signal efficacy.

How the Thatcher illusion reveals evolutionary differences in the face processing of primates

Face recognition in humans is a complex cognitive skill that requires sensitivity to unique configurations of eyes, mouth, and other facial features. The Thatcher illusion has been used to demonstrate the importance of orientation when processing configural information within faces. Transforming an upright face so that the eyes and mouth are inverted renders the face grotesque; however, when this “Thatcherized” face is inverted, the effect disappears. Due to the use of primate models in social cognition research, it is important to determine the extent to which specialized cognitive functions like face processing occur across species. To date, the Thatcher illusion has been explored in only a few species with mixed results. Here, we used computerized tasks to examine whether nonhuman primates perceive the Thatcher illusion. Chimpanzees and rhesus monkeys were required to discriminate between Thatcherized and unaltered faces presented upright and inverted. Our results confirm that chimpanzees perceived the Thatcher illusion, but rhesus monkeys did not, suggesting species differences in the importance of configural information in face processing. Three further experiments were conducted to understand why our results differed from previously published accounts of the Thatcher illusion in rhesus monkeys.

Female receptivity, mating history, and familiarity influence the mating behavior of cuttlefish

Animals attempt to maximize their reproductive fitness by employing discrimination tactics that increase their fertilization success. Semelparous species are faced with high energy and time constraints. These constraints are predicted to affect the extent of discrimination tactics that may be employed. The semelparous giant Australian cuttlefish, Sepia apama, seek multiple mates during their single breeding season, yet the discrimination tactics used to assess mates remain ambiguous. We combined field observations and laboratory-controlled mating experiments to determine (i) the relationship between the female signal (i.e., white lateral stripe) and mating outcome and (ii) the effects of the white lateral stripe, receptive postures, mating history, and familiarity on mating behavior. Females were less likely to mate when they expressed the white lateral stripe, suggesting that this signal conveys non-receptivity. Female mating history appeared to predict their likelihood of mating because females that had not recently mated were more likely to perform receptive postures and less likely to express the white lateral stripe. Familiarity with the males did not affect female expression of the white lateral stripe nor receptive postures. In males, mating behavior was not affected by the females’ expression of the white lateral stripe nor female receptive postures; however, familiarity with the female did affect male mating behavior. Males exerted a strong preference for unfamiliar females, providing evidence for familiarity discrimination. This research suggests that distinct selection pressures may be driving different discrimination capabilities in the sexes and provides the first empirical evidence of familiarity discrimination in a cephalopod species.

Individual recognition based on communication behaviour of male fowl.

Correctly directing social behaviour towards a specific individual requires an ability to discriminate between conspecifics. The mechanisms of individual recognition include phenotype matching and familiarity-based recognition. Communication-based recognition is a subset of familiarity-based recognition wherein the classification is based on behavioural or distinctive signalling properties. Male fowl (Gallus gallus) produce a visual display (tidbitting) upon finding food in the presence of a female. Females typically approach displaying males. However, males may tidbit without food. We used the distinctiveness of the visual display and the unreliability of some males to test for communication-based recognition in female fowl. We manipulated the prior experience of the hens with the males to create two classes of males: S(+) wherein the tidbitting signal was paired with a food reward to the female, and S (-) wherein the tidbitting signal occurred without food reward. We then conducted a sequential discrimination test with hens using a live video feed of a familiar male. The results of the discrimination tests revealed that hens discriminated between categories of males based on their signalling behaviour. These results suggest that fowl possess a communication-based recognition system. This is the first demonstration of live-to-video transfer of recognition in any species of bird.

Cuttlefish perform multiple agonistic displays to communicate a hierarchy of threats

Many animals produce multiple displays during agonistic interactions, but the roles of these displays often remain ambiguous. The hierarchical signaling hypothesis has been proposed to explain their occurrence and posits that different displays convey different levels of aggressive intent, allowing signalers to communicate graded series of threats. This hypothesis suggests that low-risk signals, typically performed at the beginning stages of an interaction, are strong predictors of high-risk signals but weak predictors of physical aggression. High-risk signals, typically produced at later stages of an interaction, are strong predictors of physical aggression. We used giant Australian cuttlefish, Sepia apama, to test these predictions. We combined field observations and laboratory video playback experiments to determine whether (i) male cuttlefish produce specific sequences of displays, (ii) displays in early stages of an interaction predict displays in later stages of an interaction, and (iii) displays produced in later stages of an interaction provide reliable predictors of physical aggression. Field observations suggested that males progressed from low-risk to high-risk signals (i.e., visual signaling to physical aggression). Video playback results zrevealed that the low-risk frontal display, produced during early stages of an interaction, conveys reliable information about the cuttlefish’s intent to escalate to later stages of visual signaling. Both the shovel and lateral displays were produced during the later stages of signaling and were reliable predictors of subsequent physical aggression. Our study supports the hierarchical signaling hypothesis and provides new empirical insights into how cuttlefish use progressive visual signaling to convey increasing levels of threat.Significance statementMany animals perform multiple displays during fights, but the roles of these displays often remain ambiguous. The hierarchical signaling hypothesis posits that animals produce multiple displays to convey different levels of aggressive intent, allowing signalers to communicate graded series of threats. We tested this hypothesis in giant Australian cuttlefish, Sepia apama. Specifically, we tested whether (i) displays in early stages of a fight predict displays in later stages of a fight and (ii) displays produced in later stages of a fight provide reliable predictors of physical aggression. Our results support these predictions and reveal that fighting cuttlefish progress from low-risk signals to high-risk signals to convey a hierarchy of threats. This study highlights the generality of hierarchical signaling during animal contests, as cuttlefish are evolutionary far removed from many of the species that have been reported to use this type of signaling.

Referential signalling in birds: the past, present and future

Many species produce specific signals in response to environmental events. The specificity of these signals allows receivers to react appropriately to an event in the absence of other contextual cues. These functionally referential signals can be auditory, visual or multimodal and occur in antipredator, food and social cohesion contexts. In birds, acoustic signals used in antipredator defence are the most often studied. However, several species of birds produce functionally referential signals in other modalities, including gestures, and in other contexts, including food and social contact. The prevalence of functionally referential visual or multimodal signals may be underestimated. More research using innovative techniques is needed to test these signals. Food calls, particularly those produced during food provisioning, also require further study and may shed light on the ontogeny of food signals. Comparative studies across closely related species of birds may also reveal differences in the development of functionally referential versus motivational signals. Taken together, the type of research into functionally referential signals suggested herein will likely further our understanding of the ecological, social and physiological pressures that have shaped communication in birds.