What is Communicated in the Antipredator Calls of Lemurs: Evidence from Playback Experiments with Ringtailed and Ruffed Lemurs

Two hypotheses of signal specificity in antipredator calls (“referential signalling” and “response urgency”) are discussed in light of prior research on ground squirrels and vervet monkeys. These hypotheses then are examined with data on responses of semi-captive ringtailed and ruffed lemurs to antipredator call playbacks. Although the responses of ringtailed lemurs support a referential-signalling interpretation of their antipredator calls, those of ruffed lemurs do not conform well to either hypothesis. Rather, ruffed lemur antipredator calls seem best viewed as “affective” signals that may only reflect underlying emotional/motivational states.     

Responses of Redfronted Lemurs to Experimentally Modified Alarm Calls: Evidence for Urgency-Based Changes in Call Structure

Abstract The aim of this study was to investigate how information about the affective state is expressed in vocalizations. Alarm calls can serve as model systems with which to study this general question. Therefore, we examined the information content of terrestrial predator alarm calls of redfronted lemurs ( Eulemur fulvus rufus ), group-living Malagasy primates. Redfronted lemurs give specific alarm calls only towards raptors, whereas calls given in response to terrestrial predators (woofs) are also used in other situations characterized by high arousal. Woofs may therefore have the potential to express the perceived risk of a given threat. In order to examine whether different levels of arousal are expressed in call structure, we analysed woofs given during inter-group encounters or in response to playbacks of a barking dog, assuming that animals engaged in inter-group encounters experience higher arousal than during the playbacks of dog barks. A multivariate acoustic analysis revealed that calls given during group encounters were characterized by higher frequencies than calls given in response to playbacks of dog barks. In order to examine whether this change in call structure is salient to conspecifics, we conducted playback experiments with woofs, modified in either amplitude or frequencies. Playbacks of calls with increased frequency or amplitude elicited a longer orienting response, suggesting that different levels of arousal are expressed in call structure and provide meaningful information for listeners. In conclusion, the results of our study indicate that the information about the sender's affective state is expressed in the structure of vocalizations.     

Interspecific Response to Playback of Bird Song

Responses to bird song have usually only been studied at the intraspecific level. I experimentally tested whether playback of the song of the black wheatear Oenanthe leucura in an area in S Spain resulted in responses from conspecifics as well as heterospecific birds by comparing the numbers of individuals singing before and after playback. The number of singing male black wheatears increased considerably, but also the number of singing males of five other passerine species increased significantly. The heterospecific response to playback may be due (1) to interspecific territoriality, (2) to black wheatear song signalling the absence of predators, or (3) to heterospecifics confusing the species-identity of the singer. The second alternative is considered more likely, since an ecologically wide array of species increased their song rate following playback. The conspicuous dawn (and dusk) chorus of bird song may be augmented by social facilitation due to the singing of conspecifics as well as heterospecifics.     

Responses to Playback of Local vs. Distant Contact Calls in the Orange-Fronted Conure, Aratinga canicularis

We conducted interactive playback experiments on foraging flocks of orange‐fronted conures, Aratinga canicularis, using loud contact calls that had been recorded at sites ranging from 0 to 30 km from the playback site. Responses were scored on the basis of the proximity of approach to the speaker, the number of different vocalizations produced by the responding flock, and the duration of respondent vocal interactions with the playbacks. Overall response strength decreased significantly as distance between playback and recording sites was increased up to 9 km, and remained at a steady low level for greater distances. As 9 km is the upper limit of conure home ranges measured in this study site, this nonlinear effect of response with distance suggests that response strength is partly determined by familiarity with calls of local birds. An additional and independent amount of the variation in response strength was explained by the structural similarity between respondent and stimulus calls. This correlation could be caused by a preference to interact with known stimulus birds whose calls have converged during prior associations. However, our data suggest that responding birds subtly changed their call structure during longer trials to more closely match the stimulus call. If subsequently verified as a common phenomenon, this finding could provide an important explanation for the remarkable imitative abilities of parrots.     

Complex Vocal Responses to Conspecific Calls in Whistling Frogs Eleutherodactylus johnstonei: Playback Experiments in the Field

We simulated the presence of an acoustic competitor by broadcasting conspecific playbacks to males of Johnstone's whistling frog, Eleutherodactylus johnstonei, in the field. We broadcast calls that differed in duration (short, typical, and long), dominant frequency (high, typical, and low), and period (short, typical, and long), and analyzed male vocal responses. We tested the hypothesis that males respond by escalating vocally when they are exposed to female‐attractive calls and by ignoring unattractive ones. At the population level, males responded to playbacks in ways that would potentially increase their attractiveness with regard to solo calling: males increased the duration, reduced the dominant frequency, and increased their calling effort (duty cycle), despite an increase in call period. The modification of call duration occurred only in response to playbacks of low‐frequency calls, long calls, and short‐period calls (selective response), while the modification of the dominant frequency was independent of the characteristic of the playback (fixed response). Contrary to the expected, males did not reduce the call period when they were exposed to attractive playbacks. At the ultimate level, the results suggest energy‐saving strategies. In addition, males seem to trade off call period for the avoidance of acoustic interference with attractive calls as calling effort was typically increased by increasing call duration but only rarely by reducing the call period. Interactive playbacks are necessary to better understand the calling strategies of males of E. johnstonei.     

Chemical Alarm Signalling in Terrestrial Salamanders: Intra- and Interspecific Responses

Chemical alarm cues are known to be important in mediating predator avoidance in a variety of taxonomic groups. The purpose of this study was to test whether three species of salamanders that co-occur in the coastal mountains of Oregon utilize chemical alarm cues in predator avoidance. In laboratory experiments, Western redback salamanders, Plethodon vehiculum, and Southern torrent salamanders, Rhyacotriton variegatus, exhibited an avoidance response to stimuli from injured conspecifics, while Dunn's salamanders, Plethodon dunni did not. Additional experiments demonstrated interspecific alarm responses. P. vehiculum and R. variegatus responded to each other's alarm cues but did not respond to the alarm cues of allotopic long-toed salamanders, Ambystoma macrodactylum. For R. variegatus, this is despite the fact that they are more closely related to the allotopic species (A. macrodactylum) than to the syntopic species (P. vehiculum). Thus phylogeny alone may not explain patterns of cross-species alarm responses. Instead, interspecific alarm responses may occur between syntopic species that belong to the same prey guild (i.e. those species that co-occur spatially and temporally and are exposed to the same suite of predators).     

Age Differences in the Responses to Adult and Juvenile Alarm Calls by Bonnet Macaques (Macaca radiata)

This study examined the differential responses to alarm calls from juvenile and adult wild bonnet macaques ( Macaca radiata ) in two parks in southern India. Field studies of several mammalian species have reported that the alarm vocalizations of immature individuals are often treated by perceivers as less provocative than those of adults. This study documents such differences in response using field-recorded playbacks of juvenile and adult alarm vocalizations. To validate the use of playback vocalizations as proxies of natural calls, we compared the responses of bonnet macaques to playbacks of alarm vocalizations with responses engendered by natural alarm vocalizations. We found that the frequency of flight, latency to flee, and the frequency of scanning to vocalization playbacks and natural vocalizations were comparable, thus supporting the use of playbacks to compare the effects of adult and juvenile calls. Our results showed that adult alarm calls were more provocative than juvenile alarm calls, inducing greater frequencies of flight with faster reaction times. Conversely, juvenile alarm calls were more likely to engender scanning by adults, a result interpreted as reflecting the lack of reliability of juvenile calls. Finally, we found age differences in flight behavior to juvenile alarm calls and to playbacks of motorcycle engine sounds, with juveniles and subadults more likely to flee than adults after hearing such sounds. These findings might reflect an increased vulnerability to predators or a lack of experience in young bonnet macaques.     

Eavesdropping on the Neighbourhood: Collared Pika (Ochotona collaris) Responses to Playback Calls of Conspecifics and Heterospecifics

The acoustic environment, composed in part by the vocalizations of sympatric animals, is a major source of information and can be used to fine-tune behavioural decisions. Active assessment of alarm calls within and between mammal species is not fully understood. We explored the behavioural responses of collared pikas to con- and heterospecific vocalizations, in order to determine whether they selectively attend to these calls. Pikas increased their vigilance after playback of alarm calls of heterospecific mammals (marmots and ground squirrels), but responded most strongly to conspecific calls. While responses to playback calls of their own, of neighbours and of a stranger did not differ, pikas did discriminate between individual callers in a habituation-discrimination experiment. The ability to make use of information from different sources in their acoustic environment likely facilitates pikas' behavioural decisions that affect foraging, predator avoidance and nepotism.     

非人灵长类动物的警报叫声

警报叫声是非人灵长类动物社会交往中的一种重要的通讯行为。本文从警报叫声系统及其作用、发展和影响因素入手, 综述了相关研究。根据叫声包含的信息, 警报叫声可以归纳为功能性参照系统和紧迫性参照系统。警报叫声使灵长类动物能够更好地躲避危险, 增加存活机率。各物种产生、理解和使用警报叫声的能力有其发展过程。天敌的捕食方式、个体差异和学习, 在不同层次上影响着警报叫声。川金丝猴警报叫声的初步研究发现不同性别、年龄个体的警报声所体现的危险程度不同。对更多物种进行更深入的研究将有助于了解非人灵长类警报叫声的全貌。     

Development of Antipredator Responses in Snakes

Individual and litter differences in the number of attacks directed by Mexican garter snakes (Thamnophis melanogaster) at a threatening stimulus were studied over the first year of life. Newborn snakes born to wildcaught females from the same population were tested the day after they were born and at 7, 16, 31, and 54 weeks of age on reactivity to a potent nonmoving and moving stimulus (a human finger). There were significant individual and interlitter differences in number of strikes directed at both stimuli but no significant effect of sex. Intercorrelations among the strike scores of individuals across test days averaged .54 for the nonmoving stimulus presentations and .63 for trials with the moving stimulus. Strike scores to the moving and nonmoving stimuli were significantly correlated at each age, however, attack responses to the moving stimulus declined over the year while those to the nonmoving stimulus remained constant. Measures of concordance showed that both individual strike scores and litter means were highly consistent, whereas consistency within litters was reduced. The results indicate that litter and individual differences among newborn snakes in the tendency to engage in antipredator behavior (“defensive temperament”) remain relatively stable from the first day after birth throughout the first year of life.     

Birds Learn Socially to Recognize Heterospecific Alarm Calls by Acoustic Association

1. Download high-res image (222KB)
2. Download full-size image

     

Functionally Referential Alarm Calls in Tamarins (Saguinus fuscicollis and Saguinus mystax) – Evidence from Playback Experiments

Studies on primate vocalisation have revealed different types of alarm call systems ranging from graded signals based on response urgency to functionally referential alarm calls that elicit predator‐specific reactions. In addition, alarm call systems that include both highly specific and other more unspecific calls have been reported. There has been consistent discussion on the possible factors leading to the evolution of different alarm call systems, among which is the need of qualitatively different escape strategies. We studied the alarm calls of free‐ranging saddleback and moustached tamarins (Saguinus fuscicollis and Saguinus mystax) in northeast Peru. Both species have predator‐specific alarm calls and show specific non‐vocal reactions. In response to aerial predators, they look upwards and quickly move downwards, while in response to terrestrial predators, they look downwards and sometimes approach the predator. We conducted playback experiments to test if the predator‐specific reactions could be elicited in the absence of the predator by the tamarins’ alarm calls alone. We found that in response to aerial alarm call playbacks the subjects looked significantly longer upwards, and in response to terrestrial alarm call playbacks they looked significantly longer downwards. Thus, the tamarins reacted as if external referents, i.e. information about the predator type or the appropriate reaction, were encoded in the acoustic features of the calls. In addition, we found no differences in the responses of S. fuscicollis and S. mystax whether the alarm call stimulus was produced by a conspecific or a heterospecific caller. Furthermore, it seems that S. fuscicollis terrestrial alarm calls were less specific than either S. mystax terrestrial predator alarms or either species’ aerial predator alarms, but because of the small sample size it is difficult to draw a final conclusion.     

Antiphonal Responses to Loud Contact Calls Produced by Saguinus oedipus

We report the results of an experiment designed to investigate whether captive cotton-top tamarins (Saguinus oedipus) selectively call back to an absent cagemate. We removed 2 individuals living in separate cages (cycling through the colony so that each individual was removed 10 times) from the homeroom and played back calls produced by one of them. The caller's cagemate, residing in the homeroom, was more likely to be the first individual to call back antiphonally than any other individual in the colony was. In support of previous work using both habituation-discrimination and phonotaxic techniques, our results show that cotton-top tamarins can recognize cagemates and possibly individuals by voice alone, and that the antiphonal playback method provides yet another tool for investigating acoustic perception in nonhuman primates.     

Collared Dove Responses to Playback: Slaves to the Rhythm

Temporal features are the most important parameters for differentiating among the perch coo vocalizations of doves in the genus Streptopelia . The role of temporal features in inducing territorial responses was studied for one of these species, the collared dove ( S. decaocto ), using playback experiments. The playback stimuli consisted of manipulated coos, which were tested against a preplayback period and against unmanipulated control coos. In a first set of three manipulations, the temporal structure was altered by removing an element from the species-typical three-element coos. A coo lacking the third element, which is a naturally occurring variant, was as equally effective as the control in eliciting a territorial response. The same applied to a coo lacking the second and longest element. In contrast, a coo lacking the first element did not elicit a significant increase in territorial activities compared with the preplayback period, and there was a significant reduction in response compared with the control coo. A second set of two manipulations concerned changes in the species-typical rhythm. The two variants both led to a significant reduction in response compared with the normal rhythm, although they were still effective in eliciting an increase in activities compared with the preplayback period. The results indicate that the rhythm of territorial cooing plays an important role in communicating to conspecifics. As different sympatrically living dove species differ in particular in temporal features, rhythm may be an important cue for species recognition and may contribute to reproductive isolation.     

Female Baboons' Responses to Male Loud Calls

Male baboons (Papio cynocephalus ursinus) give loud, two‐syllable ‘wahoo’ calls in response to predators (alarm wahoos) and during aggressive displays that may include multiple males chasing each other or females (contest wahoos). Although acoustic analysis has revealed significant differences between the two calls, these differences are subtle and the two subtypes can be difficult for humans to distinguish. Whatever the evolutionary mechanisms that might have acted on the production of acoustically graded loud calls, it would seem to be adaptive for listeners to discriminate among calls that are given in qualitatively different contexts. This is particularly true in the case of female baboons. Alarm wahoos, which are given during predator encounters, demand qualitatively different responses from contest wahoos, which are given in contexts when females are at risk of harassment and infanticide by males. In playback experiments, females responded for significantly longer durations to alarm than to contest wahoos. Moreover, only alarm wahoos caused females to flee. Despite their acoustic similarity, female baboons appear to associate alarm and contest wahoos with qualitatively different events.     

Social Context Influences the Antipredator Behaviour of Fathead Minnows to Chemical Alarm Cues

Prey fishes, like many organisms under fluctuating predation threat, rely on multiple sources of information to accurately gauge current risk. This includes the use of chemical cues such as alarm cues from damaged conspecifics or familiar heterospecifics, as well as the odour of known predators. While each fish is well equipped with its own array of sensory abilities, they should also be alert to the behaviours of nearby neighbours who may have information they lack. In the present study, we tested the ability of fathead minnows to use social cues in combination with the odour of damaged conspecifics and heterospecifics to mediate the assessment of predation risk. Specifically, we tested whether the presence of a shoal of conspecifics or familiar heterospecifics would significantly change a minnow's antipredator behaviour when exposed to the odour of a damage‐release cue from a conspecific or ecologically similar heterospecific. The results of our study showed a significant interaction between the damage‐release cues to which the minnows were exposed and the presence/absence of shoalmates. These findings have important implications for the design of future investigations of antipredator responses because most studies of group‐living prey have been conducted on solitary subjects.     

Antipredator Behavioral Responses of Native and Exotic Tadpoles to Novel Predator

Factors related to the invasion process, such as high abundance of invaders, residence time, and functional distinctiveness, are well documented, but less attention has been given to the effects of antipredator strategy of invasive species during colonization. In this study, we explored the antipredator strategy of an introduced species by comparing the predator avoidance behaviors of two native anuran species and one introduced(exotic) species in the presence of different predators. The two native anuran species used in the study were Black-spotted Pond Frog Rana nigromaculata and Terrestrial Frog Rana limnocharis. The introduced(invasive) species used was American bullfrog Lithobates catesbeianus. Chinese pond turtle Chinemys reevesii, Red-backed rat snake Elaphe rufodorsata, and Big-headed turtle Platysternon megacephalum were used as predator species. Chinese pond turtles and Red-backed rat snakes are native predators of Black-spotted Pond Frogs and Terrestrial Frogs, while Big-headed turtles are novel(unfamiliar) to the two frogs. All three predator species are novel(unfamiliar) to the American bullfrog. The results show that tadpoles of the two native species displayed behaviors of recognizing the two native predators, but did not display the capability of identifying the novel predator. Results from our study also suggest that American bullfrog tadpoles exhibited strong antipredator behavioral responses by displaying the capability of identifying unfamiliar predators without cohabitation history and prior exposure to them. Such antipredator behavioral responses could have resulted in more favorable outcomes for an invading species during the invasive introductory process.     

Comparison of Antipredator Responses of Two Related Water Striders to a Common Predator

This study compares the antipredator responses of two congeneric water striders that live in different habitats yet share a common predator. Aquarius nebularis and A. remigis are stream-dwelling species of water striders found in close association in central Kentucky. Aquarius nebularis typically inhabit third- and fourth-order streams that support diverse and complex fish communities; A. remigis inhabit adjacent first- and second-order tributaries that tend to have either no fish or relatively few fish patchily distributed. The ecological conditions for these two species are distinctly different, yet the green sunfish (Lepomis cyanellus) is a surface-feeding predator and a potential risk to both species. In experimental pools with sunfish, an initial fish strike caused A. remigis to move to the edge of the pool and become inactive. For the rest of the observation period, A. remigis reduced behaviour patterns that attract predators such as skating on open water, mating and male–male aggression. The proportion of A. remigis missing from sunfish pools was 5 times higher than in pools lacking fish, suggesting that 20% of water striders were killed by predation. In contrast, an initial fish strike caused A. nebularis to exhibit a burst of activity as individuals erratically skated over the open water. They then resumed the less active pre-attack behaviours a short time later. Aquarius nebularis showed none of the antipredator behaviours typical for A. remigis. Furthermore, the proportion of A. nebularis missing from sunfish pools did not differ from that in pools without fish. Although antipredator behaviour has been examined for relatively few species of water striders, this study suggests that the behaviour of the most commonly studied species, A. remigis, may not be indicative for water striders in general., Corresponding author: James J. Krupa, School of Biological Sciences, University of Kentucky, Lexington, KY 40506-0225, U.S.A. E-mail: bio149@pop.uky.edu bio149@pop.uky.edu