Do responses of galliform birds vary adaptively with predator size?

Past studies of galliform anti-predator behavior show that they discriminate between aerial and ground predators, producing distinctive, functionally referential vocalizations to each class. Within the category of aerial predators, however, studies using overhead models, video images and observations of natural encounters with birds of prey report little evidence that galliforms discriminate between different raptor species. This pattern suggests that the aerial alarm response may be triggered by general features of objects moving in the air. To test whether these birds are also sensitive to more detailed differences between raptor species, adult chickens with young were presented with variously sized trained raptors (small, intermediate, large) under controlled conditions. In response to the small hawk, there was a decline in anti-predator aggression and in aerial alarm calling as the young grew older and less vulnerable to attack by a hawk of this size. During the same developmental period, responses to the largest hawk, which posed the smallest threat to the young at all stages, did not change; there were intermediate changes at this time in response to the middle-sized hawk. Thus the anti-predator behavior of the adult birds varied in an adaptive fashion, changing as a function of both chick age and risk. We discuss these results in light of current issues concerning the cognitive mechanisms underlying alarm calling behavior in animals.     

Prairie dog alarm calls encode labels about predator colors

Some animals have the cognitive capacity to differentiate between different species of predators and generate different alarm calls in response. However, the presence of any addition information that might be encoded into alarm calls has been largely unexplored. In the present study, three similar-sized human females walked through a Gunnison’s prairie dog (Cynomys gunnisoni) colony wearing each of three different-colored shirts: blue, green, and yellow. We recorded the alarm calls and used discriminant function analysis to assess whether the calls for the different-colored shirts were significantly different. The results showed that the alarm calls for the blue and the yellow shirts were significantly different, but the green shirt calls were not significantly different from the calls for the yellow shirt. The colors that were detected, with corresponding encoding into alarm calls, reflect the visual perceptual abilities of the prairie dogs. This study suggests that prairie dogs are able to incorporate labels about the individual characteristics of predators into their alarm calls, and that the complexity of information contained in animal alarm calls may be greater than has been previously believed.     

Alarm Signals and Prompts to Eliminate Large Urinary Accidents in a Woman with Multiple Disabilities

Urine-triggered alarm signals and prompts were used to help a woman with multiple disabilities halt wetting episodes and walk to the toilet (thus avoiding large urinary accidents). Data indicated that the woman had a mean frequency of 1 large accident nearly every 2 days during the baseline phases and every 20 days during the intervention phases. During the latter phases, large accidents were replaced by small accidents (i.e. only a disposable tissue inside the underwear was wet), which did not cause environmental disruptions and did not require changes of clothes. Implications of the findings are discussed.     

Reciprocal recognition of sifaka (<Emphasis Type="Italic">Propithecus verreauxi verreauxi</Emphasis>) and redfronted lemur (<Emphasis Type="Italic">Eulemur fulvus rufus</Emphasis>) alarm calls

Redfronted lemurs (Eulemur fulvus rufus) and Verreaux's sifakas (Propithecus verreauxi verreauxi) occur sympatrically in western Madagascar. Both species exhibit a so-called mixed alarm call system with functionally referential alarm calls for raptors and general alarm calls for carnivores and raptors. General alarm calls also occur in other contexts associated with high arousal, such as inter-group encounters. Field playback experiments were conducted to investigate whether interspecific recognition of alarm calls occurs in both species, even though the two species rarely interact. In a crossed design, redfronted lemur and sifaka alarm calls were broadcast to individuals of both species, using the alarm call of chacma baboons (Papio cynocephalus) as a control. Both species responded with appropriate escape strategies and alarm calls after playbacks of heterospecific aerial alarm calls. Similarly, they reacted appropriately to playbacks of heterospecific general alarm calls. Playbacks of baboon alarm calls elicited no specific responses in either lemur species, indicating that an understanding of interspecific alarm calls caused the responses and not alarm calls in general. Thus, the two lemur species have an understanding of each other's aerial as well as general alarm calls, suggesting that even in species that do not form mutualistic associations and rarely interact, common predator pressure has been sufficient for the development of heterospecific call recognition.     

Functional referents and acoustic similarity revisited: the case of Barbary macaque alarm calls

Barbary macaques (Macaca sylvanus) utter "shrill barks" in response to disturbances in their surroundings. In some cases, the majority of group members react by running away or climbing up a tree. In many other instances, however, group members show no overt reaction to these calls. We conducted a series of playback experiments to identify the factors underlying subjects' responses. We presented calls given in response to dogs that had elicited escape responses and calls that had failed to do so. We also presented calls given in response to snakes and to the observer approaching the sleeping-trees at night. An acoustic analysis of the calls presented in the playback experiments (electronic supplementary material, audioclip S1) revealed significant differences among calls given in response to dogs, the observer approaching at night, and snakes. However, the analysis did not detect any differences between calls given in response to dogs that were related to whether or not they had elicited escape responses in the first place. Correspondingly, after playback of calls given in response to dogs, we observed no difference in subjects' responses in relation to whether or not the calls had initially elicited escape responses. Subjects showed startle or escape responses significantly more often after playbacks of calls given in response to dogs than after calls given in response to observers. Playbacks of calls given in response to snakes failed to elicit specific responses such as standing bipedally or scanning the grass. Although these findings may imply that responses depend on the external referent, they also indicate that there is no clear-cut relationship between the information available to the listeners and their subsequent responses. This insight forces us to extend current approaches to identifying the meaning of animal signals. Accepted after revision: 15 May 2001 Electronic Publication     

Overt behavior and ultrasonic vocalization in a fear conditioning paradigm: a dose-response study in the rat

The behavioral analysis of laboratory rats is usually confined to the level of overt behavior, like locomotion, behavioral inhibition, instrumental responses, and others. Apart from such visible outcome, however, behaviorally relevant information can also be obtained when analyzing the animals' ultrasonic vocalization, which is typically emitted in highly motivational situations, like 22-kHz calls in response to acute or conditioned threat. To further investigate such vocalizations and their relationship with overt behavior, we tested male Wistar rats in a paradigm of Pavlovian fear conditioning, where a tone stimulus (CS) was preceding an aversive foot-shock (US) in a distinct environment. Importantly, the shock dose was varied between groups (0-1.1 mA), and its acute and conditioned outcome were determined. The analysis of visible behavior confirms the usefulness of immobility as a measure of fear conditioning, especially when higher shock doses were used. Rearing and grooming, on the other hand, were more useful to detect conditioned effects with lower shock levels. Ultrasonic vocalization occurred less consistently than changes in overt behavior; however, dose-response relationships were also observed during the phase of conditioning, for example, in latency, call rate and lengths, intervals between calls, and sound amplitude. Furthermore, total calling time (and rate) were highly correlated with overt behavior, namely behavioral inhibition as measured through immobility. These correlations were observed during the phase of fear conditioning, and the subsequent tests. Importantly, conditioned effects in overt behavior were observed, both, to the context and to the CS presented in this context, whereas conditioned vocalization to the context was not observed (except for one rat). In support and extent of previous results, the present data show that a detailed analysis of ultrasonic vocalization can substantially broaden and refine the spectrum of analysis in behavioral work with rats, since it can provide information about situational-, state-, and subject-dependent factors which are partly distinct from what is visible to the experimenter.     

Learning, memorizing and apparent forgetting of chemical cues from new predators by Iberian green frog tadpoles

Many antipredator adaptations are induced by the prey’s ability to recognize chemical cues from predators. However, predator recognition often requires learning by prey individuals. Iberian green frog tadpoles (Pelophylax perezi) have the ability to learn new potential predators. Here, we tested the memory capabilities of Iberian green frog tadpoles. We conditioned tadpoles with chemicals cues from a non-predatory fish in conjunction with conspecific alarm cues, and examined whether tadpoles retained their conditioned response (reduction of activity level). We found that conditioned tadpoles reduced their activity levels in subsequent exposures to the non-predatory fish cues alone. Tadpoles were able to remember this association and reduced movement rate at least for 9 days after. The ability to learn and memorize potential predators may be especially important for the survivorship of prey species that are likely to find a high variety of predators. However, after those 9 days, there was a lack of response to the non-predatory fish cues alone in the absence of reinforcement. This could be explained if tadpoles behave according to the threat-sensitive predator avoidance hypothesis, and the perceived risk to the learning cue diminished over time, or it could be due to an apparent forgetting process to avoid non-adaptative responses to chemical cues of non-dangerous species that were randomly paired with alarm cues. Thus, this study demonstrates that green frog tadpoles in the absence of reinforcement remember the chemical cues of a learned predator only for a limited time that may be adaptative in a threat-sensitive context.