Acoustic classification of alarm calls by vervet monkeys (Cercopithecus aethiops) and humans (Homo sapiens): II. Synthetic calls

In 2 experiments classification of synthetic versions of species-typical snake and eagle alarm calls by vervet monkeys (Cercopithecus aethiops) and human (Homo sapiens) control subjects was investigated. In a 2-choice, operant-conditioning-based procedure, this work followed up acoustic analyses that had used various digitally based algorithms (Owren & Bernacki, 1988). All subjects were first tested with alarm-call replicas that were based on analysis data. These models were classified in the same manner as natural stimuli, which verified the appropriateness of the acoustic characterizations. Synthetic stimuli were then presented to test the importance of specific acoustic cues. Spectral patterning was found to be the most salient cue for classification by the monkeys, whereas results from the human subjects were mixed. Implications for the study of nonhuman primate vocalizations and Lieberman's (1984) theory of speech evolution are discussed.     

Responses of urban crows to con- and hetero-specific alarm calls in predator and non-predator zoo enclosures

Urban animals and birds in particular are able to cope with diverse novel threats in a city environment such as avoiding novel, unfamiliar predators. Predator avoidance often includes alarm signals that can be used also by hetero-specifics, which is mainly the case in mixed-species flocks. It can also occur when species do not form flocks but co-occur together. In this study we tested whether urban crows use alarm calls of conspecifics and hetero-specifics (jackdaws, Corvus monedula) differently in a predator and a non-predator context with partly novel and unfamiliar zoo animal species. Birds were tested at the Tiergarten Schönbrunn in the city of Vienna by playing back con- and hetero-specific alarm calls and control stimuli (great tit song and no stimuli) at predator (wolf, polar bear) and non-predator (eland antelope and cranes, peccaries) enclosures. We recorded responses of crows as the percentage of birds flying away after hearing the playback (out of those present before the playback) and as the number of vocalizations given by the present birds. A significantly higher percentage of crows flew away after hearing either con- or hetero-specific alarm calls, but it did not significantly differ between the predator and the non-predator context. Crows treated jackdaw calls just as crow calls, indicating that they make proper use of hetero-specific alarm calls. Responding similarly in both contexts may suggest that the crows were uncertain about the threat a particular zoo animal represents and were generally cautious. In the predator context, however, a high percentage of crows also flew away upon hearing the great tit control song which suggests that they may still evaluate those species which occasionally killed crows as more dangerous and respond to any conspicuous sound.     

Silhouettes elicit alarm calls from captive vervet monkeys (Cercopithecus aethiops).

In Part 1, we analyzed alarm calls produced by captive vervets (Cercopithecus aethiops) in response to naturally occurring stimuli. Females and juveniles regularly alarm called to airplanes, birds, and barking dogs. Juvenile females accounted for 60% of these alarm calls. In Part 2, we isolated several monkeys from the colony and presented them with life-sized silhouettes of a leopard, snake, eagle, baboon, vervet, and goose. Adult monkeys alarm called more than did juveniles. Alarm calls were elicited by leopard, snake, baboon, and vervet silhouettes, but none were elicited by eagle or goose silhouettes. Some leopard and snake alarm calls matched those recorded in the wild in the context of the vervets' natural predators. Results indicate that silhouette stimuli are a useful technique for eliciting monkey vocalizations in the laboratory.     

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.     

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.     

Open-ended categorization of chick-a-dee calls by black-capped chickadees (Poecile atricapilla)

The authors trained black-capped chickadees (Poecile atricapilla) in an operant discrimination with exemplars of black-capped and Carolina chick-a-dee calls, with the goal of determining whether the birds memorized the calls of conspecifics and heterospecifics or classified the calls by species. Black-capped calls served as both rewarded (S+) and unrewarded (S-) stimuli (the within-category discrimination), whereas Carolina chick-a-dee calls served as S-s (the between-category discrimination) in the black-capped chick-a-dee call S+ group. The Carolina call S+ group had Carolina calls as S+s and S-s (within-category) and black-capped calls as S-s (between-category). Both groups discriminated between call categories faster than within a call category. In 2 subsequent experiments, both S+ groups showed transfer to novel calls and propagation back to between-category calls. The results favor the hypothesis that the acoustically similar social calls of the 2 species constitute separate open-ended categories.     

Testing for transitive class containment as a feature of hierarchical classification

Three experiments investigated responding consistent with transitive class containment, a feature of hierarchical classification. Experiment 1 replicated key components of a preliminary attempt to model hierarchical classification (Griffee & Dougher, 2002) and tested for responding consistent with transitive class containment. Only 2 out of 5 participants showed the expected pattern. Experiment 2 tested whether repeated exposures to the Experiment 1 protocol would give rise to the expected pattern more reliably. None of 3 novel participants demonstrated the pattern. In Experiment 3, physically similar stimuli used in Experiments 1 and 2 were replaced across testing cycles by arbitrary stimuli. Transitive-class-containment-consistent responding was observed in all 3 novel participants. Implications, limitations and future research are discussed.     

Comparing responses of four ungulate species to playbacks of baboon alarm calls

A growing body of evidence suggests that a wide range of animals can recognize and respond appropriately to calls produced by other species. Social learning has been implicated as a possible mechanism by which heterospecific call recognition might develop. To examine whether familiarity and/or shared vulnerability with the calling species might influence the ability of sympatric species to distinguish heterospecific alarm calls, we tested whether four ungulate species (impala: Aepyceros melampus; tsessebe: Damaliscus lunatus; zebra: Equus burchelli; wildebeest: Connochaetes taurinus) could distinguish baboon (Papio hamadryas ursinus) alarm calls from other loud baboon calls produced during intra-specific aggressive interactions (‘contest’ calls). Overall, subjects’ responses were stronger following playback of alarm calls than contest calls. Of the species tested, impala showed the strongest responses and the greatest difference in composite response scores, suggesting they were best able to differentiate call types. Compared with the other ungulate species, impala are the most frequent associates of baboons. Moreover, like baboons, they are susceptible to both lion and leopard attacks, whereas leopards rarely take the larger ungulates. Although it seems possible that high rates of association and/or shared vulnerability may influence impala’s greater ability to distinguish among baboon call types, our results point to a stronger influence of familiarity. Ours is the first study to compare such abilities among several community members with variable natural histories, and we discuss future experiments that would more systematically examine development of these skills in young ungulates.     

Classification of domestic cat (Felis catus) vocalizations by naive and experienced human listeners

To test for possible functional referentiality in a common domestic cat (Felis catus) vocalization, the authors conducted 2 experiments to examine whether human participants could classify meow sounds recorded from 12 different cats in 5 behavioral contexts. In Experiment 1, participants heard singlecalls, whereas in Experiment 2, bouts of calls were presented. In both cases, classification accuracy was significantly above chance, but modestly so. Accuracy for bouts exceeded that for single calls. Overall, participants performed better in classifying individual calls if they had lived with, interacted with, and had a general affinity for cats. These results provide little evidence of referentiality suggesting instead that meows are nonspecific, somewhat negatively toned stimuli that attract attention from humans. With experience, human listeners can become more proficient at inferring positive-affect states from cat meows.     

The transfer of specific and general consequential functions through simple and conditional equivalence relations

The purpose of this study was to examine the transfer of consequential (reinforcement and punishment) functions through equivalence relations. In Experiment 1, 9 subjects acquired three three-member equivalence classes through matching-to-sample training using arbitrary visual forms. Comparison stimuli were then given conditioned reinforcement or punishment functions by pairing them with verbal feedback during a sorting task. For 8 of the 9 subjects, trained consequential functions transferred through their respective equivalence classes without additional training. In Experiment 2, transfer of function was initially tested before equivalence testing per se. Three of 4 subjects showed the transfer without a formal equivalence test. In Experiment 3, 3 subjects were given training that gave rise to six new three-member conditional equivalence classes. For 2 of the subjects, the same stimulus could have either a reinforcement or punishment function on the basis of contextual cues that defined its class membership. Experiment 4 assessed whether equivalence training had established general or specific consequential functions primarily by adding novel stimuli in the transfer test. Subjects treated even novel feedback stimuli in the transfer test as consequences, but the direction of consequential effects depended upon the transfer of specific consequential functions through equivalence relations.     

Audience effects on alarm calling in chickens (Gallus gallus)

The male domestic chicken (Gallus gallus) has been found to modulate the production of vocal signals in response to the presence or absence of a suitable audience. We investigated effects on alarm calling by presenting overhead predator models to cockerels in the presence of a variety of social companions. The production of aerial predator calls in response to hawk silhouettes varied with the presence or absence of a member of the same species. The kinds of audience investigated included the mate, unfamiliar females, other females and males with which subjects had had prior visual and auditory contact, and broody hens with and without young. Domestic chicks, unrelated to the subjects, were almost as effective an audience as conspecific adults. A member of another species, however, failed to potentiate alarm-call production. The subjects gave more alarm calls when they were in the presence of either a male or a female audience than when they were alone. By manipulating the visibility of overhead predator models to the subjects and to the audience, we showed that the subjects were not cued by alarm and escape behaviors of the audience. Comparisons with food calling indicate that, in deciding whether to emit a signal in response to the appropriate referent (e.g., food or predators), chickens respond to subtle differences in the nature of the audience with behaviors that vary from one communicative context to another.     

Identity concept learning in matching-to-sample tasks by tufted capuchin monkeys (Cebus apella)

The abstract concept of equivalence is considered one of the bases of higher-order cognition, and it has been the subject of considerable research in comparative cognition. This study examined the conditions under which tufted capuchin monkeys (Cebus apella) are able to acquire an identity concept. Six capuchin monkeys were trained to solve a visual matching-to-sample (MTS) task on the basis of perceptual identity. The acquisition of the identity rule was inferred from the subject’s ability to solve transfer tests with novel stimuli. We evaluated the ability of the capuchin monkeys to match the shape of novel stimuli after training with both several small stimulus sets (Experiment 1) and a large stimulus set (Experiment 2). Moreover, we examined the ability of capuchins to transfer the concept to novel visual dimensions, such as colour and size and to transfer to novel spatial arrangements of the stimuli (Experiment 2). We demonstrated that the ability of capuchins to match novel stimuli was improved by increasing the number of stimuli used during training (Experiments 1 and 2) and that after a widely applicable identity concept based on the stimulus shape was acquired, the capuchins were able to match stimuli according to an identity rule based on both the colour and size of the stimuli and when the spatial arrangement of the stimuli was varied (Experiment 2). This study is the first to demonstrate that the size of the training set affects the acquisition of an abstract identity concept in an MTS task in non-human primates.     

Asymmetric transfer of prototype information between vision and audition

Specific and nonspecific transfer of pattern class concept information between vision and audition was examined. In Experiment 1, subjects learned visually or auditorily to distinguish between two pattern classes that were either the same as or different from the test classes. All subjects were then tested on the auditory classification of 50 patterns. Specific intramodal and cross-modal transfer was noted; subjects trained visually and auditorily on the test classes were equivalent in performance and more accurate than untrained controls. In Experiment 2, the training of Experiment 1 was repeated, but subjects were tested visually. There was no evidence of auditory-to-visual transfer but some suggestion of nonspecific transfer within the visual modality. The asymmetry of transfer is discussed in terms of the modality into which patterns are most likely translated for the cross-modal tasks and in terms of the quality of prototype formation with visual versus a,ditory patterns.     

Naturalistic psychophysics: thresholds of ducklings (Anas platyrynchos) and chicks (Gallus gallus) to tones that resemble mallard calls

Neonatal ducklings and chickens were tested for responsiveness to a pulsing pure tone that was as similar as possible to the mallard maternal alarm call. It is known that ducklings momentarily cease vocalizing when they hear the alarm call and that chicks do the same when they hear pure tones. The duration of peep suppression can thus be used as a measure of whether subjects of either species heard the stimulus. Chicks might not be as sensitive as ducklings to a mallard alarm call because the signal is less significant to them. An adaptive or staircase procedure was used to estimate absolute thresholds, and group psychometric functions were reconstructed for each species from the trial-by-trial data. Ducklings had lower thresholds than chickens as well as steeper psychometric functions to this stimulus. The results suggest that more sensitive and consistent behavioral responses can be elicited by naturalistic sounds than by more arbitrary acoustic stimuli.     

Long-term memory for categories and concepts in horses (Equus caballus)

Three horses (Equus caballus) with a history of performing cognitive tasks including discrimination learning, categorization, and concept use were tested to evaluate their long-term memory (LTM) in three experiments. In addition, use of LCD multi-displays for stimulus presentation was incorporated into cognition testing protocol for the first time with horses. Experiment 1 tested LTM for discrimination learning that originally occurred 6 years earlier. Five sets of stimuli were used and the two horses tested showed no decrement in performance on four of the sets; however, both horses did score below chance on one set. Experiment 2 examined long-term categorization recall 10 years after horses had demonstrated the ability to make stimulus selections based on shared characteristics within a given category. The horse tested for LTM after the decade-long interval immediately and consistently applied the previously learned categorization rule to not only familiar but also novel sets of stimuli. Experiment 3 tested another horse for LTM for a relative size concept. This horse had originally demonstrated concept rule use in order to select stimuli based on their relative size to one another. More than 7 years later and without further training, this horse reliably applied the previously established size concept to both familiar and novel sets of stimuli. These findings are the first reports of long-term categorical and conceptual memory in horses and are consistent with observations of domestic and wild horses, which indicate that behavioral and ecological events may be remembered for long periods of time. These studies also demonstrate the adaptive nature of horses with regard to their ability to generalize over several different testing conditions.     

Children's identity matching and oddity: assessing control by specific and general sample-comparison relations.

After children in Experiments 1 and 2 learned identity matching or oddity, control by sample-comparison relations was assessed. Tests for generalized control displayed novel samples and two comparison stimuli, one identical to the sample. Specific relations were tested with identical or nonidentical sample-comparison stimuli from one set of stimuli and substitute comparisons from either the other training set or from a novel set. When tests displayed identical stimuli, patterns of comparison selection suggested control by generalized identity and oddity. However, selection patterns varied when stimuli were nonidentical and familiar or novel substitute comparisons were used. Therefore, control by specific relations is not a precondition for generalized identity and oddity. One set of training stimuli was used in Experiment 3, and generalized performances occurred again. Moreover, control by specific relations was shown by the oddity subjects and 2 of 6 identity subjects. Generalized and specific control may therefore exist simultaneously. In Experiment 4, selections were irregular on tests displaying substitute comparisons and samples and familiar comparison stimuli; this finding supported the relational account of specific sample-comparison control found in Experiment 3.     

Salience of caller identity in rhesus monkey (Macaca mulatta) coos and screams: perceptual experiments with human (Homo sapiens) listeners

Recent evidence from acoustic analysis and playback experiments indicates that adult female rhesus monkey (Macaca mulatta) coos are individually distinctive but their screams are not. In this study, the authors compared discrimination of individual identity in these sounds by naive human listeners who judged whether 2 sounds had been produced by the same monkey or 2 monkeys. Each of 3 experiments using this same-different design showed significantly better discrimination of vocalizer identity from coos than from screams. Experiment 1 demonstrated the basic finding. Experiment 2 also tested the effect of non-identity-related scream variation, and Experiment 3 added a comparison with human vowel sounds. Outcomes suggest that acoustic structural differences in coos and screams influence salience of caller-identity cues, with significant implications for understanding the functions of these calls.     

Degree of representation of the matching concept in pigeons (Columba livia)

In Experiment 1, 12 pigeons (Columba livia) were trained on a simultaneous matching-to-sample task with 2 stimuli and then tested with 2 novel stimuli. Half of the birds were trained with a fixed ratio schedule requirement of 1 (FR1) or 20 (FR20) pecks on the sample stimulus. None of the birds showed any evidence of concept-mediated transfer. In Experiment 2, 12 pigeons were trained with 3 stimuli and then tested with the same novel stimuli used in Experiment 1. Half of the birds in each group were trained with either an FR1 or FR20 requirement on the sample stimulus. Two of the FR20 birds showed high levels of transfer to the novel stimuli similar to that of monkeys in a previous study.     

The role of instructions in the transfer of ordinal functions through equivalence classes

In two experiments, adult subjects completed match-to-sample training and testing to establish four equivalence classes of four figures each. Then the subjects were taught one three-position sequence consisting of one stimulus from Class 1, one from Class 2, and one from Class 3. Inclusion of Class 4 stimuli in sequences was never reinforced, but two different stimuli from Class 4 appeared as distractors on each sequence trial. Tests assessed whether subjects would produce novel three-position sequences composed of members of Classes 1 through 3 that had not been used in sequence training. Three subjects in Experiment 1 received instructions about the match-to-sample and sequencing tasks, in addition to training contingencies. All 3 demonstrated equivalence class formation after match-to-sample training. After they were taught one sequence with one member of Classes 1 through 3, none of these subjects produced untrained sequences with other equivalence class members reliably. One additional sequence was trained directly; thereafter 1 subject showed some evidence of transfer of the trained ordinal functions across the remaining members of the equivalence classes, but the other 2 did not. Following a review of equivalence class training and testing and a review of the original sequence training, all 3 subjects produced most of the predicted, untrained sequences on tests. Experiment 2 replicated Experiment 1 with 2 adults but omitted all instructions except the minimal ones necessary to initiate responding. Unlike the subjects in Experiment 1, both of these subjects demonstrated virtually complete transfer of ordinal functions through the equivalence classes after direct training on just one sequence composed of one member of Classes 1 through 3.     

Inferences about the location of food in capuchin monkeys (Cebus apella) in two sensory modalities

The authors tested the ability of capuchin monkeys (Cebus apella) to make inferences about hidden food. In Experiment 1, we showed the content of 2 boxes, 1 of which was baited (visual condition, VC) or we shook both boxes producing noise from the baited box (auditory condition, AC). Seven subjects (out of 8) were above chance in the VC, whereas only 1 was above chance in AC. During treatment, by manipulating empty and filled objects subjects experienced the relation between noise and content. When tested again, 7 capuchins were above chance in the VC and 3 in AC. In Experiment 2, we gave visual or auditory information only about the empty box and, consequently, successful choice implied inferential reasoning. All subjects (out of 4) were above chance in the VC, and 2 in the AC. Control tests ruled out the possibility that success resulted from simply avoiding the shaken noiseless box, or from the use of arbitrary auditory information. Similar to apes (Call, 2004), capuchins were capable of inferential reasoning.