Recognition of order effects in squirrel monkey antiphonal call sequences

Squirrel monkeys exchange chuck vocalizations in antiphonal sequences that suggest a request for information, and a response to that request. Chucks are characterized by measurable acoustic differences, notably in peak frequency, related to their position in a sequence. To determine the cues by which animals might identify a chuck that is a request for information from one that is a response, first-in-sequence (α) and second-in-sequence (β) chucks, differing in peak frequency, were recorded from familiar individuals and strangers. These chucks, and a sham control, were played back, in the temporal context of a first-in-sequence call, to a target group of socially housed captive squirrel monkeys. Animals responded more strongly to α chucks than to β chucks for calls originating from familiar individuals. No distinction was made between the α and β chucks of strangers, and all strangers' chucks got a weaker response than did familiar α chucks. Squirrel monkeys probably use acoustic differences, rather than context, to discriminate the ordinal significance of a chuck, but cannot do so unless they are familiar with the caller. © 1993 Wiley-Liss, Inc.     

Chuck Vocalizations of Wild Female Squirrel Monkeys (Saimiri sciureus) Contain Information on Caller Identity and Foraging Activity

Analysis of the acoustic signal of the chuck vocalizations of adult female squirrel monkeys (Saimiri sciureus) in Parque Nacional de Manu, Peru, revealed consistent differences within and between individuals. We quantified four peak frequency parameters: (a) the peak frequency of single chucks, (b) the first and (c) the second peak frequencies of double chucks, and (d) the peak difference: the difference between the first and the second double chuck peaks. One-way ANOVAs and a posteriori comparisons of these variables revealed that each distinguished more than 70% of all possible pairs of females. When all double chuck measures were included in a discriminant analysis, 57% of double chucks were correctly assigned to the caller. Another category of information potentially encoded in the acoustic structure of chuck vocalizations is foraging activity. When the chucks of squirrel monkeys during foraging and nonforaging activities were compared, the single chuck peak frequency, and the first peak frequency and the peak difference of double chucks, were significantly reduced during foraging contexts. Previously Boinski and Mitchell (1992) concluded that chucks facilitate group cohesion among widely dispersed troop members by providing information of the location of callers; the rate of chucks produced by an adult female increases as she becomes more spatially and visually separated from other adult females. The additional information potentially conveyed by chucks on caller identity and foraging activity documented in these new analyses further emphasizes the role chucks serve to enhance group coordination and cohesion.     

Ecological and Social Factors Affecting the Vocal Behavior of Adult Female Squirrel Monkeys

Focal recordings of the vocalizations of squirrel monkeys, Saimiri sciureus, occupying an undisturbed Peruvian habitat were collected to evaluate the importance of both the ecological and social functions of female vocal behavior. The rates and sequences of six call types were examined by context: single, double, and multiple chuck, peep, tweet, and tweet-chuck. In contrast to laboratory studies, our findings emphasize the primacy of ecological functions in the wild, where calling permits females to operate as a convoy of spatially separated individuals in an arboreal habitat where visual contact is limited. Chuck calls are probably best interpreted as contact calls. The rate of chucks and tweet-chucks increased when the nearest adult female was > 5 m away. However, call production did not predict a change in the spatial separation between a female and her nearest adult female. During travel, the rate of single and double chucks was greater and the rate of multiple chucks was reduced. No direct relationship was found between foraging activities and vocal behavior. Although secondary, social factors did have a subtle effect on vocal behavior: the larger the social alliance of a female, the lower the rate and repetitiveness of her chuck vocalizations. We also consider the role of variations in vocalization rates among primates and the differing conclusions of field and captive studies of squirrel monkey vocal behavior.     

Does Gray Squirrel (Sciurus carolinensis) Response to Heterospecific Alarm Calls Depend on Familiarity or Acoustic Similarity?

In habitats in which multiple species are prey to the same predators, individuals can greatly benefit from recognizing information regarding predators that is provided by other species. Past studies have demonstrated that various mammals respond to familiar heterospecific alarm calls, but whether acoustic similarity to a familiar call can prompt a mammal's recognition of an unfamiliar call has yet to be shown. We presented alarm calls to free‐ranging eastern gray squirrels (Sciurus carolinensis) and recorded behavioral changes in vigilance and antipredatory response. Playbacks included alarm calls of a sympatric bird (American robin, Turdus migratorius), an allopatric bird with a call structure similar to that of the robin (common blackbird, Turdus merula), and an allopatric bird with a distinct call structure (New Holland honeyeater, Phylidonyris novaehollandiae). Squirrels responded significantly more frequently to squirrel alarm calls (positive control) than to robin song (negative control) or honeyeater calls. Squirrel response to robin and blackbird alarm calls was statistically similar to their response to squirrel alarm calls, indicating that squirrels responded to those alarm calls as if they provided information about the presence of predators. However, squirrel response to robin song was not statistically different from response to any of the other avian calls, including the robin and blackbird alarms, suggesting that squirrels neither respond to blackbird alarms as if they clearly signify danger, nor as if they clearly do not signify danger, perhaps reflecting some ambiguity in interpretation of the calls. These results suggest that squirrel responses to alarm calls are generally based on call familiarity, but that acoustic similarity of an unfamiliar allopatric call to a familiar call also can elicit antipredator behavior. The lack of response to honeyeater alarm calls also supports the hypothesis that call recognition by gray squirrels is dependent on familiarity, rather than simply detection of an acoustic feature common to alarm calls across a variety of avian species.     

Maternal recognition of individual infant squirrel monkeys from isolation call playbacks

Responses of six squirrel monkey (Saimiri sciureus) mothers to playback of a single call type, the “isolation peep,” made by their own infants were tested after mothers and infants had been separated for more than a week. The playback tapes were edited from tapes containing mixed vocal material recorded when infants and mothers could see but not touch each other. Mothers showed recognition of their own infants compared to other familiar infants by increases in four measures of proximity to the speaker. These data provide evidence that maternal recognition of infants by means of acoustic cues is possible when the test stimuli consist of examples of a single call type with demonstrated individuality.     

Do frog-eating bats perceptually bind the complex components of frog calls?

The mating calls of male túngara frogs, Physalaemus pustulosus, attract intended (conspecific females) and unintended (eavesdropping predators and parasites) receivers. The calls are complex, having two components: a frequency-modulated “whine” followed by 0–7 harmonic bursts or “chucks”. The whine is necessary and sufficient to elicit phonotaxis from females and the chuck enhances call attractiveness when it follows a whine. Although chucks are never made alone, females perceptually bind the whine and chuck when they are spatially separated. We tested whether an unintended receiver with independent evolution of phonotaxis, the frog-eating bat, Trachops cirrhosus, has converged with frogs in its auditory grouping of the call components. In contrast to frogs, bats approached chucks broadcast alone; when the chuck was spatially separated from the whine the bats preferentially approached the whine, and bats were sensitive to whine–chuck temporal sequence. This contrast suggests that although disparate taxa may be selected to respond to the same signals, different evolutionary histories, selective regimes, and neural and cognitive architectures may result in different weighting and grouping of signal components between generalist predators and conspecific mates.     

Age differences and developmental trends in alarm peep responses by squirrel monkeys (Saimiri sciureus)

Alarm calls can code for different classes of predators or different types of predatory threat. Acoustic information can also encode the urgency of threat through variations in acoustic features within specific alarm call types. Squirrel monkeys (Saimiri sciureus) produce an alarm call, known as the alarm peep, in highly threatening situations. Infant squirrel monkeys appear to have an innate predisposition to respond to alarm peeps but require experience to associate alarm peeps with the appropriate type of predatory threat [Herzog & Hopf, American Journal of Primatology 7:99-106, 1984]. Little is known about age-related differences in the type or frequency of response to alarm peeps, or the development of alarm peep response in infants. The purpose of this study was to test experimentally the response strategies of different age classes of squirrel monkey to the playback of alarm peeps that were produced by infants, juveniles, or adults. Results suggest that infants, juveniles, and female subadults respond more frequently to alarm peeps than do adult females. Infant squirrel monkeys showed different behavioral strategies in response to alarm peeps as a function of age. Adult females differentiate between infant and adult alarm peeps by responding more frequently to the alarm peeps of adult females. These data demonstrate that squirrel monkeys use acoustic information to discern when to respond to the alarm peeps from conspecifics, and that infants gradually develop an adult-like response to alarm peeps over the first year of development.     

Long-term memory for affiliates in ravens

Complex social life requires individuals to recognize and remember group members and, within those, to distinguish affiliates from nonaffiliates. Whereas long-term individual recognition has been demonstrated in some nonhuman animals, memory for the relationship valence to former group members has received little attention. Here we show that adult, pair-housed ravens not only respond differently to the playback of calls from previous group members and unfamiliar conspecifics but also discriminate between familiar birds according to the relationship valence they had to those subjects up to three years ago as subadult nonbreeders. The birds' distinction between familiar and unfamiliar individuals is reflected mainly in the number of calls, whereas their differentiation according to relationship valence is reflected in call modulation only. As compared to their response to affiliates, ravens responded to nonaffiliates by increasing chaotic parts of the vocalization and lowering formant spacing, potentially exaggerating the perceived impression of body size. Our findings indicate that ravens remember relationship qualities to former group members even after long periods of separation, confirming that their sophisticated social knowledge as nonbreeders is maintained into the territorial breeding stage.     

Individual variation in pup vocalizations and absence of behavioral signs of maternal vocal recognition in Weddell seals (Leptonychotes weddellii)

Individually stereotyped vocalizations often play an important role in relocation of offspring in gregarious breeders. In phocids, mothers often alternate between foraging at sea and attending their pup. Pup calls are individually distinctive in various phocid species. However, experimental evidence for maternal recognition is rare. In this study, we recorded Weddell seal (Leptonychotes weddellii) pup vocalizations at two whelping patches in Atka Bay, Antarctica, and explored individual vocal variation based on eight vocal parameters. Overall, 58% of calls were correctly classified according to individual. For males (n= 12) and females (n= 9), respectively, nine and seven individuals were correctly identified based on vocal parameters. To investigate whether mothers respond differently to calls of familiar vs. unfamiliar pups, we conducted playback experiments with 21 mothers. Maternal responses did not differ between playbacks of own, familiar, and unfamiliar pup calls. We suggest that Weddell seal pup calls may need to contain only a critical amount of individually distinct information because mothers and pups use a combination of sensory modalities for identification. However, it cannot be excluded that pup developmental factors and differing environmental factors between colonies affect pup acoustic behavior and the role of acoustic cues in the relocation process.     

Singing in the Face of Danger: the Anomalous Type II Vocalization of the Splendid Fairy-Wren

Males of certain species of fairy-wrens (Aves: Maluridae) emit a unique vocalization, the Type II vocalization, in response to the calls of potential predators. We conducted field observations and playback experiments to identify the contexts in which the Type II vocalization is emitted by splendid fairy-wren ( Malurus splendens ) males, and to examine social and genetic factors that influence its occurrence. In field observations and controlled playback experiments, Type II vocalizations were elicited most consistently by calls of the predatory gray butcherbird ( Cracticus torquatus ). Some vocalizations from other avian species also elicited Type II vocalizations, and the majority of these were vocalizations from avian predators. Splendid fairy-wrens are cooperative breeders, and males that responded with Type II vocalizations to playbacks of butcherbird calls tended to be primary rather than secondary males, had larger cloacal protuberances, and were older than those that did not respond. In addition, secondary males that were sons of resident females were more likely than non-sons to respond with a Type II vocalization. In another playback experiment, females responded similarly to the Type I song and Type II vocalizations of their mates. Although the Type II vocalization is emitted primarily in response to predator calls, it is inconsistent with an alarm call explanation. Patterns of reproductive success among Type II calling males suggest that it does not function as an honest signal of male quality. At present, the function of the vocalization remains anomalous, but indirect fitness benefits may play a role in its explanation.     

Effects of separation and novelty on distress vocalizations and cortisol in the common marmoset (Callithrix jacchus)

In socially-bonding species, separation from familiar attachment figures is widely known to stimulate a physiological and behavioral stress response. This study investigated the hormonal and vocal responses of adult common marmosets to separation from familiar group members and to 24 hr of cohabitation with an unfamiliar opposite-sex conspecific. All subjects were removed from their home cages and placed into a novel environment for 20 min. In one group, marmosets were exposed to an unfamiliar, opposite-sex partner in the novel environment and remained paired with this partner for the 24 hr test period. In three other groups, marmosets experienced the novel environment alone and subsequently were returned to their original social- or single-housing condition, or kept separate from their social groups for a 24 h period. Blood samples were collected the day before, and at 30 min, 90 min, and at 24 h after separation. Cortisol responses were differentially affected by the length of separation and the presence of unfamiliar conspecifics. Brief separation followed by the return to the social group had minimal effect on plasma cortisol levels. All marmosets produced high levels of separation calls in the novel environment, but there was no apparent relationship between calling and cortisol levels. The lack of a temporal relationship between the production of distress vocalizations and serum cortisol has previously been noted in squirrel monkey and rhesus monkey infant separation studies; the behavioral and physiological responses to separation appear to be similarly dissociated in the marmoset. Further, the characteristics of a separation environment can differentially affect the hormonal response by adult marmosets without differentially affecting their behavioral response.     

Reactions of adult and immature squirrel monkeys to intergroup exposure

Initial encounters between unfamiliar animals raise the practical problem of controlling aggression and provide the opportunity to examine changes in social structure that may occur as groups merge. Social interactions and spatial grouping patterns were examined in newly formed squirrel monkey groups, in which a subgroup of familiar adults was introduced to a subgroup of familiar immature squirrel monkeys. Yearlings (10–11 months) and subadults (20–50 months) generally remained spatially distinct from adults, and intergroup interactions often consisted of adult-initiated antagonism. Adults exhibited sexual segregation in their spatial grouping patterns and interactions, whereas yearlings and subadults generally showed sexual integration. These data suggest that there is considerable adult resistance to integration of unfamiliar immatures into established adult social groups. Zoo Biol 17:519–524, 1998. © 1998 Wiley-Liss, Inc.     

Aggression with mixed age-sex groups of bolivian squirrel monkeys following single animal introductions and new group formations

The social organization of the Bolivian squirrel monkey (Saimiri boliviensis boliviensis) is thought to be sexually segregated, with males and females forming separate social groups during the nonbreeding season. To investigate the influence of this social order on patterns of aggression, controlled single animal introductions within established groups and establishment of new groups were studied in a systematic manner. Behavioral observations were made using an all-occurrences technique to sample all agonistic interactions. In study I, 4 animals of each age-sex class (adult males and females, juvenile males and females) were introduced one at a time into 4 different social groups composed of 1 adult male and 8 to 10 adult females. Behavioral observations were made prior to and after the introductions. Newly introduced adult males received significantly more contact aggression than other age classes. Only the adult females increased aggression after the introduction of new animals. In study II, new social groups were formed and behavioral observations were made following formation. One group was formed from 7 pairs of familiar females and an unfamiliar adult male. This group had a high frequency of aggression during the first half hour, with contact aggression rising to peaks at 3 and 5 h. The second group consisted of 10 familiar females, 2 pairs of familiar females and an unfamiliar male. There was a significant peak in contact aggression 3 h into the observation.     

Sexual behaviour and its olfactory control in the desert woodrat (Neotoma lepida lepida)

In studies 1 and 2 nine pairs of desert woodrats (Neotoma lepida lepida) were observed for copulatory behaviour when the female was in a state of naturally occurring oestrus (study 1) and following ovariectomy and oestrogen and progesterone replacement (study 2). Males and females respond in a similar way under conditions of natural and hormone-induced oestrus. Males show a consummatory pattern involving multiple mounts and ejaculations, with ejaculations occurring after single intromissions. Females show the lordosis reflex accompanied by hop-and-dart and ear-wiggling responses. In addition, both sexes show appetitive precopulatory behaviours; the male emits an audible rasping vocalization as he trails and mounts the female, following a period of intense sniffing of the female's anogenital region. The female also frequently approaches and sniffs the male. In study 3, the role of female odours in the sexual behaviour of the male was examined in eight of the nine pairs used in studies 1 and 2. This was done by applying to the anogenital region of ovariectomized females a combination of urine and vaginal secretions taken from familiar and unfamiliar, and oestrogen-primed or non-oestrogen-primed females. The results show that odours from oestrogen-primed females are not sufficient to elicit male sexual behaviour, if the female is not sexually active. In study 4 the eight males were tested for their preferences for urine and vaginal secretion odours taken from females in different reproductive states and applied to cotton swabs. These males spent more time sniffing unfamiliar oestrous odours than unfamiliar non-oestrous odours and more time sniffing oestrous odours from a familiar female over those taken from an unfamiliar female.In study 5, 12 sexually active males were tested with oestrogen-primed females before and after either olfactory bulb removal or sham-surgery. Bulbectomized animals ceased copulating with females although females showed precopulatory approaches.Taken together, these studies suggest that normal sexual behaviour in the male woodrat requires that the female both possess the attractive odours (of oestrus) and that she engage in appetitive precopulatory behaviour.     

Vocal buffering of the stress response: exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets

For many species, the presence of a significant social partner can lessen the behavioral and physiological responses to stressful stimuli. This study examined whether a single, individually specific, signature vocalization (phee call) could attenuate the physiological stress response that is induced in marmosets by housing them in short-term social isolation. Utilizing a repeated-measures design, adult marmosets (n=10) were temporarily isolated from their long-term pair mate and exposed to three conditions: signature vocalizations from the pair mate, phee calls from an unfamiliar opposite sex individual, or no auditory stimuli. Levels of urinary cortisol were monitored as a physiological indicator of the stress response. Urinary cortisol levels were also monitored, while subjects remained undisturbed in their home cages to provide baseline levels. Temporarily isolated marmosets showed significantly higher levels of urinary cortisol than undisturbed marmosets. However, the nature of the acoustic stimulus experienced during isolation led to differences in the excretion of urinary cortisol. Isolated marmosets exposed to a familiar pair mate's vocalization showed significantly lower levels of urinary cortisol than when exposed to unfamiliar marmoset vocalizations (P <0.04) or to no auditory stimuli (P <0.03). Neither the duration of pairing nor the quality of relationship in the pair (indexed by spatial proximity scores) predicted the magnitude of reduction in cortisol in the familiar vocalization condition. The results presented here provide the first evidence that a single, individually specific communication signal can decrease the magnitude of a physiological stress response in a manner analogous to the physical presence of a social partner, a process we term "vocal buffering."     

Individual recognition in wild bottlenose dolphins: a field test using playback experiments

We conducted playback experiments with wild bottlenose dolphins, Tursiops truncatus, to determine whether there is sufficient information in their individually distinctive signature whistles for individual recognition. We conducted experiments with members of a resident community of dolphins in waters near Sarasota, Florida, during temporary capture-release projects. We used a paired playback design, wherein the same two whistle sequences were predicted to evoke opposite responses from two different target animals. This design controlled for any unknown cues that may have been present in the playback stimuli. We predicted that mothers would respond more strongly to the whistles of their own independent offspring than to the whistles of a familiar, similar-aged nonoffspring. Similarly, we predicted that independent offspring would respond more strongly to the whistles of their own mother than to the whistles of a familiar, similar-aged female. Target animals were significantly (P<0.02) more likely to respond to the predicted stimuli, with responses measured by the number of head turns towards the playback speaker. In bottlenose dolphin societies, stable, individual-specific relationships are intermixed with fluid patterns of association between individuals. In primate species that live in similar 'fission-fusion' type societies, individual recognition is commonplace. Thus, when taken in the context of what is known about the social structure and behaviour of bottlenose dolphins, these playback experiments suggest that signature whistles are used for individual recognition. Copyright 1999 The Association for the Study of Animal Behaviour.     

The influence of age and sex on the vocal repertoire of the Antillean manatee (Trichechus manatus manatus) and their responses to call playback

Limited information is available regarding the acoustic communication of Antillean manatees, however, studies have shown that other manatee taxa produce vocalizations as a method of individual recognition and communication. Here, the acoustic signals of 15 Antillean manatees in captivity were recorded, aiming to (1) describe their acoustic repertoire, (2) investigate the influence of sex and age on vocalization, and (3) examine manatee responses to call playback. Six acoustic signals ranging in mean fundamental frequencies from 0.64 kHz to 5.23 kHz were identified: squeaks and screeches were common to adult males, adult females, and juveniles; trills were common to adult males and females; whines were specific to males; creaks were specific to females; and rubbing was specific to juveniles. The structure of squeak vocalizations was significantly different between age and sex classes and screech structure was significantly different between age classes. Squeaks and screeches produced by juveniles had higher frequencies of maximum energy when compared to those produced by adult males and females. A significant increase in the vocalization rate following vocalization playbacks was found for all three age/sex groups. Our results introduce the potential of using acoustic signals in identifying and noninvasively monitoring manatees in the wild in Brazil.     

Contrasting effects of living in heterosexual pairs and mixed groups on the structure of social attraction in squirrel monkeys (Saimiri).

The structure of social attraction was assessed in pair- and group-living squirrel monkeys (Saimiri) using paired-comparison and single-stimulus preference tests. Effects of the social environment were most prominent in females. Females housed with a single male showed sharply increased attraction to like-sex strangers and less pronounced increase in attraction to opposite-sex strangers, as compared to group-living females. Differences between pair- and group-living males were in the same direction found with females, but less extreme. Most group-living monkeys strongly preferred familiar animals to strangers regardless of sex, and like-sex to opposite-sex familiars. Change in the structure of social attractions in response to variations in the composition of the social environment appears to be an important factor in the maintenance of the species-typical grouping pattern in the squirrel monkey.     

THE SENSORY BASIS OF SEXUAL SELECTION FOR COMPLEX CALLS IN THE TÚNGARA FROG,PHYSALAEMUS PUSTULOSUS (SEXUAL SELECTION FOR SENSORY EXPLOITATION)

Male túngara frogs (Physalaemus pustulosus) vocalize to attract females, and enhance the attractiveness of their simple, whine-only call by adding chucks to produce complex calls. Complex calls contain more total energy and are of longer duration. By virtue of the greater frequency range of the chuck, complex calls also simultaneously stimulate both the amphibian papilla and the basilar papilla of the frog's inner ear. Female phonotaxis experiments using synthetic stimuli demonstrate that an increase in the call's acoustic energy is not sufficient to account for the enhanced attractiveness of the complex call. However, the stimulation of either or both of the female's sound-sensitive inner-ear organs is sufficient to elicit her preference. We suggest that the female's sensory system generates selection that equally favors at least three evolutionary alternatives for enhancing call attractiveness and that historical constraints imposed by the male's morphology determined which of the alternatives was more likely to evolve. These data are consistent with our hypothesis of sensory exploitation, which states that selection favors those traits that elicit greater stimulation from the female's sensory system and which emphasizes the nonadaptive nature of female preference.     

Chemosensory Recognition of Familiar and Unfamiliar Conspecifics by the Scincid Lizard Eumeces laticeps

The ability of broad-headed skinks (Eumeces laticeps) to distinguish familiar from unfamiliar individuals of the opposite sex and themselves from other individuals of the same sex using only chemical stimuli was examined experimentally. Cloacal chemical stimuli were presented to lizards on moistened cotton swabs and numbers of tongue-flicks performed in 60 s were recorded. Males emitted significantly greater numbers of tongue-flicks in response to chemical cues from unfamiliar females than of female cagemates. Response rates of males housed with females and males housed alone to chemical stimuli from unfamiliar females did not differ. Chemical stimuli from unfamiliar males elicited significantly more tongue flicks from males than their own or deionized water, but their own stimuli elicited no more than the odourless control. Females tongue-flicked significantly more in response to cloacal chemical stimuli from unfamiliar males than from male cagemates. The findings indicate that both sexes of broad-headed skinks can discriminate between chemical stimuli of familiar and unfamiliar individuals of the opposite sex and that males can distinguish their own cloacal chemicals from those of unfamiliar males. The possible functions of these chemosensory capacities, including location of mates by scent-trailing and assessment of the presence of sexual competitors, are discussed in relation to the social behaviour of E. laticeps.