Vocalizations of adult gelada baboons (Theropithecus gelada): acoustic structure and behavioural context

Vocalizations and accompanying behaviors of adult gelada baboons were studied in four one-male groups kept in large outdoor enclosures in the zoos of Stuttgart and Rheine. Twenty-two acoustically different vocal patterns were determined. According to behavioural context, they were grouped into two categories: (1) contact calls and (2) aggressive and defensive calls. Frequency of calling and the production of different vocalizations were related to social rank and to the age of the sender. Vocalizations in species of the closely related genera Papio and Macaca are compared and their evolution is discussed.     

Acoustic communication underground: vocalization characteristics in subterranean social mole-rats (Cryptomys sp., Bathyergidae)

In captive adult Zambian mole-rats 14 different sounds (13 true vocalizations) have been recorded during different behavioural contexts. The sound analysis revealed that all sounds occurred in a low and middle frequency range with main energy below 10 kHz. The majority of calls contained components of 1.6–2 kHz, 0.63–0.8 kHz, and/or 5–6.3 kHz. The vocalization range thus matched well the hearing range as established in other studies. The frequency content of courtship calls in two species of Zambian Cryptomys was compared with that in naked mole-rats (Heterocephalus glaber) and blind mole-rats (Spalax ehrenbergi) as described in the literature. The frequency range of maximum sound energy is negatively correlated with the body weight and coincides with the frequencies of best hearing in the respective species. In general, the vocalization range in subterranean mammals is shifted towards low frequencies which are best propagated in underground burrows. Accepted: 16 September 1996     

Acoustic signals of a solitary subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae): physical characteristics and behavioural correlates

The purpose of this study was to analyse and describe vocalizations of a solitary subterranean rodent, Ctenomys talarum. In adult C. talarum five different sounds (four true vocalizations and one mechanical sound) were recorded during different behavioural contexts. Using data from the laboratory and literature, we classified these vocalizations as territorial, distress, and mating calls. We found that the vocalization range in C. talarum is shifted towards low frequencies, which transmit better in underground burrows and match well the hearing range described for other species of subterranean rodents. These low-frequency vocalizations, also found in other non-related subterranean rodents, may reflect an adaptation to the acoustic conditions of the habitat. Electronic Publication     

BIOACOUSTIC PUBLICATIONS, 1989

ABSTRACT

Coruros Spalacopus cyanus, social fossorial rodents from Chile, use a complex acoustic repertoire with eleven different true vocalisations and one mechanical sound in various behavioural contexts. The complex of contact calls is particularly well differentiated. Juvenile coruros produced six true vocalisations of which four were structurally identical to adult calls. One vocalisation had components of two adult sounds and one occurred only in juvenile animals. Certain calls from the adult repertoire were lacking. The frequencies of sounds of juveniles were considerably higher than those of adults, with many sounds reaching the ultrasonic range. Nevertheless, pure ultrasonic sounds were not recorded.

The frequencies of the analysed sounds of coruros extended from 0.17 to 20.33 kHz with dominant frequency components between 0.17 and 10 kHz. The acoustic properties of calls are suitable for transmission above and below ground, thus providing further indirect evidence that coruros are not strictly confined to an underground way of life. Indeed, the great variability of frequency ranges, with lower frequencies always being included, reflects a specialisation for communication in variable acoustic environments.

The most distinctive and unique vocalisation of coruros is the long duration musical trilling (lasting up to two minutes), which is a long-distance call emitted in alarm and arousal contexts. Recordings of this call from natural burrows in the field in Chile showed similar structural features to vocalisations from captive colonies in the laboratory.

Our findings provide a further example of matching physical properties of vocalisations to the acoustic conditions of the habitat. However, vocalisations in subterranean rodents consist almost exclusively of short-distance calls, the trilling of coruros being the notable exception. Since the selective pressure of the acoustic environment upon the evolution of short-distance vocalisations is probably minimal, we suggest that during their evolution, subterranean mammals have matched their vocalisations primarily to their hearing range and not directly to the acoustics underground. Hearing probably has been the primary target of natural selection, serving not only for communication but also for detection of predators (and, in carnivores, of prey).     

Thermal biology of a strictly subterranean mammalian family,the African mole-rats (Bathyergidae,Rodentia) - a review

African mole-rats are subterranean rodents, which rarely if ever leave the safety of their burrow systems. The environment of the burrows is humid, with relatively stable temperatures, and may have a hypoxic and hypercapnic atmosphere. One of crucial problems related to the subterranean way of life in mammals is avoidance of overheating, because traditional mammalian cooling mechanisms are not effective under high humidity. In African mole-rats, a variety of adaptations have evolved in response to this and other challenges of the underground ecotope. Traditionally, attention has been devoted mainly to the naked mole-rat Heterocephalus glaber, which became popular as a result of its eusociality and absence of fur, both being unique phenomena in small mammals. Despite more recent research, information on other species is still relatively limited and patchy. I review the results of studies on African mole-rats that are relevant for the understanding of their energetics and thermal biology. Attention is paid to the parameters of the burrow environment, which represent the main selection pressures shaping their physiology. In addition, an overview is given of the morphological, physiological and behavioural adaptations helping mole-rats to face temperature extremes, mechanisms by which they deal with a surplus of metabolic heat and how changes in ambient temperature influence their daily activity. The naked mole-rat is compared to its furred relatives to determine whether this species is really exceptional from the point of thermal biology. An ordination analysis was conducted using published data on mole-rat body temperature, thermoneutral zone, resting metabolic rate and thermal conductance. Most of the variability in these characteristics was found to be explained by body mass, followed by temperature characteristics of climate, but not precipitation, of the species distributional ranges. This analysis shows that the naked mole-rat is comparable to the other mole-rat species in these physiological characteristics.     

VOCAL BEHAVIOUR AND CALL DEVELOPMENT IN THE BULLFINCH (PYRRHULA PYRRHULA)

ABSTRACT

A sonagraphic analysis of the vocalizations of bullfinches Pyrrhula pyrrhula is presented and their behavioural contexts and functions noted. The vocal repertoire of the bullfinch is compared to that of other finches with particular attention to repertoire size and sexual specificity; the repertoire of 14–17 vocal categories is comparatively greater than that of most carduelines and the majority of vocalizations were given by both sexes. The development of nestling, fledgling and some adult calls is described. Early vocal ontogeny in the bullfinch was similar to that previously described for the chaffinch. The earliest recorded calls of nestling bullfinches showed a single fundamental. The independent use of two sound sources became apparent on the second day after hatching and the major elements of the three best studied call types were all derived from the lower fundamental of the nestling begging call.     

Hearing in blind subterranean Zambian mole-rats (Cryptomys sp.): collective behavioural audiogram in a highly social rodent

Thresholds for pure tone detection were examined in the common mole-rat, Cryptomys sp. (Bathyergidae, Rodentia) using a positive reinforcement procedure. To bypass the problems connected with testing isolated individuals of this extremely social species, a collective behavioural audiogram was determined for a family group of seven mole-rats. Within the tested frequency range of 225 to 18 kHz, the lowest thresholds (as low as 7.5 dB SPL, on average 24 dB SPL) were found at 800 Hz, the upper limit of hearing (at the level of 60 dB SPL) was at 18 kHz. The behavioural audiogram combines the results of previous studies on hearing in this species. It resembles the distortion threshold curve but differs from neurophysiological data as far as the high frequency cutoff is concerned. On the other hand, the region of the best hearing sensitivity is narrow in behavioural audiogram and neurophysiological curves but rather broad in the distortion threshold curve. In general, the behavioural audiogram of Cryptomys is in many aspects comparable with the available audiograms of other subterranean rodents. Accepted: 18 February 1997     

Behavioural Tests Reveal Severe Visual Deficits in the Strictly Subterranean African Mole‐Rats (Bathyergidae) but Efficient Vision in the Fossorial Rodent Coruro (Spalacopus cyanus,Octodontidae)

Vision has long been considered purposeless in the dark underground ecotope. However, recent anatomical studies revealed an unexpected diversity of ocular and retinal features and various degrees of development of the visual system in mammals with predominantly subterranean activity, and have suggested retention of basic visual capabilities even in some strictly subterranean mammals such as the African mole‐rats. Behavioural tests assessing image‐forming vision have not yet been conducted in subterranean mammals. Here, we investigated the visual capacities in three species of the African mole‐rats, namely the giant mole‐rat Fukomys mechowii, the Mashona mole‐rat Fukomys darlingi and the silvery mole‐rat Heliophobius argenteocinereus, in the fossorial coruro Spalacopus cyanus and the inbred C57L/J mouse. The behavioural assays performed in this study revealed severe visual deficits in all three species of mole‐rats. The absence of the visual placing reflex suggested impairment of either image‐forming vision or visuomotor integration. The random choice between the shallow and the deep side of a visual cliff clearly demonstrated inability of mole‐rats to perceive depth. The nesting assay did not yield conclusive evidence regarding the capacity for visually guided spatial orientation in the only tested species, the giant mole‐rat. In contrast, both the coruro and the mouse exhibited a clear placing reaction and preferred the shallow side of the visual cliff, implying functional image‐forming vision. Thus, the behavioural data gathered in this study show that vision is seriously compromised in the strictly subterranean, congenitally microphthalmic African mole‐rats but efficient (i.e. comparable to that of surface‐dwelling rodents) in a species with regular surface activity, the coruro.     

Vocal communication of wild bonnet macaques (Macaca radiata)

Field observations and spectrographic analyses of sound recordings of South Indian bonnet macaques revealed a vocal repertoire of at least 25 basic patterns. The repertoire consists of well separated sound classes and acoustic categories connected by structural intergradation. Besides structural variations within and between different elements of the repertoire, the vocal system ofMacaca radiata is characterized by regular combinations of particular basic patterns. These combinations occurred not only between calls of similar structure and function but also between calls usually emitted in entirely different social contexts. According to the qualitative analysis, sex-specific asymmetries of the vocal behaviour were less pronounced than age-dependent characteristics. The comparison of clear call vocalizations ofMacaca radiata andM. fuscata revealed significant species-specific differences on the structural and the behavioural level. Evaluations of the structural features of alarm calls of various macaque species imply marked differences between members of thefascicularis group andsinica group on one hand and thesilenus group andarctoides group on the other.     

Intended Receivers and Functional Significance of Grunt and Girney Vocalizations in Free-Ranging Female Rhesus Macaques

We investigated the intended receivers and contexts of occurrence of grunt and girney vocalizations in rhesus macaques (Macaca mulatta) to assess whether these calls are best interpreted as signals of benign intent or as calls that may function to attract the attention of other individuals or induce arousal. We focally observed 19 free‐ranging adult female rhesus macaques. Female calls increased dramatically after infants were born, and most were directed toward mother–infant dyads. When infants were physically separated from their mothers, callers visually oriented toward infants in over 90% of the cases, suggesting that infants were the intended receivers of grunts and girneys. Approaches followed by vocalizations were more likely to lead to the caller grooming the mother, less likely to elicit a submissive response, and more likely to result in infant handling than approaches without calls. Infant handling, however, was not necessarily benign. Vocalizations were often emitted from a distance >1 m and were rarely followed by approaches or social interactions. Our results suggest that grunts and girneys are unlikely to have evolved as signals that encode information about the caller's intention or subsequent behavior. Whereas girneys may be acoustically designed to attract infants’ attention and elicit arousal, grunts may have no adaptive communicative function. Mothers, however, may have learned that other females’ grunts and girneys are unlikely to be associated with significant risk and, therefore, are generally tolerant of the caller's proximity and behavior.     

A preliminary study of vocal communication in wild long-tailed macaques (Macaca fascicularis). I. Vocal repertoire and call emission

Vocal communication in wild long-tailed macaques (Macaca fascicularis) is described in terms of (1) a preliminary vocal repertoire and the situations in which calls occur in the natural habitat of this species and (2) quantitative measurement of the natural occurrence of calls in the field. Although a number of calls are relatively discrete (e.g., a male loud call), gradation is pronounced for both wide-spectrum (“harsh”) and narrow-spectrum (“clear”) vocal signals. Thirteen general types of harsh calls are identified provisionally as elements of the vocal repertoire. The exact number of discrete clear calls contributing to the vocal repertoire could not be ascertained precisely, but these calls were classified operationally into six broadly acoustically different classes in order to measure natural vocal behavior. Vocalizations tended to occur in temporal “clusters” during sample, periods. Narrow-band clear or “coo” calls were more frequently performed by macaques than wide-band harsh calls. The possible functional implications of the correlated occurrence of multiple vocal signals are discussed.     

Vocal repertoire of cooperatively breeding Smooth‐billed Anis

Calls are functionally diverse signals that mediate behavior in a wide variety of contexts in both passerines and non‐passerines. However, the call‐based acoustic communication systems of non‐passerines have received less attention from investigators than those of passerines. We examined the vocal repertoire of Smooth‐billed Anis (Crotophaga ani), cooperatively breeding cuckoos that live in groups with multiple breeding pairs. We recorded calls from 22 groups over two breeding seasons at the Cabo Rojo National Wildlife Refuge in Puerto Rico. We identified 11 call types and one group vocalization, and used an automated sound measurement program to quantify their acoustic features. Discriminant function analysis (DFA) correctly classified 74.2% of calls based on these features. The vocal repertoire of Smooth‐billed Anis is larger than that reported for the three other species in the subfamily Crotophaginae. Smooth‐billed Anis have at least two alarm calls, two nest‐specific calls, and one nest defense call. We also identified one possible signal of aggressive intent, one possible appeasement signal, and two calls that may communicate identity. The relatively large vocal repertoire of Smooth‐billed Anis and association of distinct call types with different functions and contexts supports the main prediction of the social complexity hypothesis, i.e., species with more complex social systems will have more complex communication systems.     

The social structure and dominance hierarchy of the Mashona mole-rat, Cryptomys darlingi (Rodentia: Bathyergidae) from Zimbabwe

Cryptomys darlingi is a social subterranean rodent mole which inhabits the mesic regions of south-eastern and central Africa. Mashona mole-rats live in small colonies (5-9 animals) in which reproduction is normally restricted to the largest male and female in the colony. The non-reproductive members in a mature colony cannot be placed into clearly defined work-related groups based on body mass.
The dominance hierarchy of a young colony was found to be linear, with a value of 1.00 calculated from Landau's linearity index, while that of a mature colony of nine mole-rats was almost linear (0.77). Dominance was found to be related to gender in the mature colony, with males more dominant than females, and to age in the young colony. The reproductive mole-rats are the dominant animals within their respective genders. Dominance appears to correlate positively with body mass (rs = 0.77 in the mature colony and rs = 0.93 in the young colony).
Popularity studies show that smaller animals and females tend to be more popular than the larger massed individuals or males. In the mature colony which contained predominantly adult animals, the reproductive pair was among the least popular. While in the young colony, composed predominantly of sub-adult and juvenile animals, the reproductive pair was the most popular.
Social organization within Mashona mole-rat colonies is compared with other southern African Cryptomys species.     

Poikilothermic traits in Mashona mole-rat (Fukomys darlingi). Reality or myth?

The African mole-rats (Bathyergidae, Rodentia) is a mammalian family well known for a variety of ecophysiological adaptations for strictly belowground life. The smallest bathyergid, the hairless naked mole-rat from arid areas in Eastern Africa, is even famous as the only truly poikilothermic mammal. Another bathyergid, the Mashona mole-rat (Fukomys darlingi) from Zimbabwe, is supposed to have strong poikilothermic traits, because it is not able to maintain a stable body temperature at ambient temperatures below 20 °C. This is surprising because, compared to the naked mole-rat, this species, together with all congenerics, is larger, haired, and living in more seasonal environment. In addition, other Fukomys mole-rats show typical mammalian pattern in resting metabolic rates. In our study, we measured resting metabolic rate and body temperature of Mashona mole-rats from Malawi across a gradient of ambient temperatures to test its poikilothermic traits. We found that the adult mass specific resting metabolic rate was 0.76±0.20 ml O₂ g⁻¹ h⁻¹ and body temperature 34.8±1.1 °C in the thermoneutral zone (27–34 °C). Body temperature was stable (33.0±0.5 °C) at ambient temperatures from 10 to 25 °C. We thus cannot confirm poikilothermic traits in this species, at least for its Malawian population. Factors potentially explaining the observed discrepancy in Mashona mole-rat energetics are discussed.     

Contextual flexibility in the vocal repertoire of an Amazon parrot

Background

Understanding the role of avian vocal communication in social organisation requires knowledge of the vocal repertoire used to convey information. Parrots use acoustic signals in a variety of social contexts, but no studies have evaluated cross-functional use of acoustic signals by parrots, or whether these conform to signal design rules for different behavioural contexts. We statistically characterised the vocal repertoire of 61 free-living Lilac-crowned Amazons (Amazona finschi) in nine behavioural contexts (nesting, threat, alarm, foraging, perched, take-off, flight, landing, and food soliciting). We aimed to determine whether parrots demonstrated contextual flexibility in their vocal repertoire, and whether these acoustic signals follow design rules that could maximise communication.

Results

The Lilac-crowned Amazon had a diverse vocal repertoire of 101 note-types emitted at least twice, 58 of which were emitted ≥5 times. Threat and nesting contexts had the greatest variety and proportion of exclusive note-types, although the most common note-types were emitted in all behavioural contexts but with differing proportional contribution. Behavioural context significantly explained variation in acoustic features, where threat and nesting contexts had the highest mean frequencies and broad bandwidths, and alarm signals had a high emission rate of 3.6 notes/s. Three Principal Components explained 72.03 % of the variation in temporal and spectral characteristics of notes. Permutated Discriminant Function Analysis using these Principal Components demonstrated that 28 note-types (emitted by >1 individual) could be correctly classified and significantly discriminated from a random model.

Conclusions

Acoustic features of Lilac-crowned Amazon vocalisations in specific behavioural contexts conformed to signal design rules. Lilac-crowned Amazons modified the emission rate and proportional contribution of note-types used in each context, suggesting the use of graded and combinatorial variation to encode information. We propose that evaluation of vocal repertoires based on note-types would reflect the true extent of a species’ vocal flexibility, and the potential for combinatorial structures in parrot acoustic signals.

     

Seismic Signal Use by Fossorial Mammals

The subterranean environment is not favorable for the use ofvision or the audition of airborne sounds as means of long-distancesensory perception. However, seismic vibrations have been shownto propagate at least an order of magnitude better than airbornesound between the burrow systems of the mole-rat Georychus capensis.The use of the seismic channel for communication undergroundis well documented for other species of bathyergids, as wellas the spalacine mole-rat Nannospalax. It has recently beensuggested that the golden mole Eremitalpa granti namibensismay also be sensitive to ground vibrations, in this case usedin foraging in its desert habitat. In this paper, the use of seismic signals among these and otherfossorial mammals is reviewed from theoretical, behavioral andanatomical standpoints. The question of whether auditory orsomatosensory means are used to detect vibratory signals isexamined. Attempts to explain the distribution of seismic sensitivityand communication mechanisms among fossorial mammals are considered.The potential influences of different soil type and diggingmethods are discussed, and it is proposed that digging mechanismsinvolving the head might preadapt a fossorial mammal towardsthe development of seismic sensitivity.     

Wild squirrel monkey (Saimiri sciureus) “caregiver” calls: Contexts and acoustic structure

A field study of the vocal behavior of 22 wild adult female squirrel monkeys (Saimiri sciureus) in Parque Nacional del Manu, Peru, found that 21% of vocalizations were “caregiver” calls. Caregiver calls are brief, low frequency calls, often with numerous harmonics, that are addressed by caregivers to their own infants in three contexts: 1) prenurse, signalling the caregiver's location and willingness to nurse; 2) nurse, while nursing; and 3) end nurse, indicating the end of the nursing bout. Three measures (start, end, and peak frequency) of the acoustic structure of the fundamental frequency of the caregiver calls significantly differed across the contexts. Duration of caregiver calls, however, was not distinguished by context. Compared to other primate taxa, the specificity and importance of caregiver calls in squirrel monkey vocal behavior appears unusual, if not unique. That S. sciureus caregiver calls are highly developed and employed so extensively probably follows from an unusual combination of ecological and life history factors. These factors include delayed weaning and large infant body size, high levels of indirect foraging competition which encourages spatial separation, susceptibility to predation, and specialization on a densely foliated, branch-end microhabitat in which visual contact is often impeded. © 1995 Wiley-Liss, Inc.     

The study of vocal communication of wild mandrills in Cameroon in relation to their social structure

The vocal repertoire of the mandrill (Mandrillus sphinx), a forest living baboon, is described, and their vocal communication analyzed quantitatively. Although the vocal repertoire of mandrills corresponds well to that of savanna living baboons,Papio, some characteristics differed, such as the development of long-distance calls and differentiation of vocalizations between age-sex classes. Vocal communication within a group was closely related to changes in the spatial distribution of group members, and the two most common vocalizations, crowing and 2PG, appear to function as contact calls. Based on the wide dispersion of food trees, a group of mandrills divided into several feeding groups (subgroups). The two types of contact call were given in different and in some senses complementary contexts, and helped to facilitate and maintain group integration. According to their acoustic structure, these calls are long distance calls. Influenced by the high-level of attenuation of vocalization on the forest floor, the mandrill has developed them as contact calls, instead of using the contact “grunt,” which is common to the savanna living baboons. Comparing the patterns of vocal exchanges of mandrills with those of gelada and hamadryas baboons which have a multi-levelled society, the social structure of the mandrill is discussed. From the analysis of the spatial distribution of vocal emission, a number of clusters of vocalizations were obtained. These clusters correspond to subgroups. The frequent female-female and female-male vocal exchange between subgroups of mandrills suggest that the relationships between subgroups are less closed than between the one-male units of gelada and hamadryas baboons. Furthermore some of these clusters include more than two vocalizing adult males, while in other clusters there are no vocalizing adult males. Thus, the social structure of mandrills is suggested to be multi-male rather than a multilevelled type. The absence of contact calls specific for short distance and the functional replacement of the grunting of all group members by persistent emission of a loud call (2PG) by usually just one adult male suggests that the social structure of mandrills is not exactly equivalent to that of the multimale troop of savanna living baboons. Usually the use of 2PG is monopolized by one adult male travelling in the rear part of the group. Such monopolization of 2PG emission and the pattern of 2PG-2PG or 2PG-roar exchanges by adult males in some cases indicate the existence of strong dominance relationships among adult males, and especially the existence of a leader male within a multi-male group of mandrills.     

Observational Evidences of Vocal Learning in Southern Elephant Seals: a Longitudinal Study

Vocal learning in mammals is sparsely documented, and there are few reports of vocal learning by wild mammals. In particular, no information based on longitudinal data for identified individuals exists, even for well‐studied highly social species in which vocal communication is an important aspect of social life. We present such information for the southern elephant seal (Mirounga leonina). We studied a small breeding population in the Falkland Islands over 8 yr (1995–2002). We recorded approx. 2400 agonistic vocalizations from approx. 285 different males, including many recorded over more than one breeding season (55 males were recorded for >2 yr and 29 were recorded throughout vocal development). Vocalizations are a key element of male agonistic behaviour in this species, the world's most polygynous vertebrate. For male agonistic vocalizations, we show that: (1) a limited number of discrete vocal types exists; (2) proportions of vocal types change over time; (3) observed trends of increase or decrease of vocal types are well explained by a process of vocal learning, in which younger peripheral males imitate vocal types of older more successful breeders.     

Social and vocal behavior in adult greater tube-nosed bats (Murina leucogaster)

Many studies have revealed the significant influence of the social nature and ecological niche of a species on the design and complexity of their communication sounds. The knowledge of communication sounds and particularly of the flexibility in their use among mammals, however, remains patchy. Being highly vocal and social, bats are well suited for investigating vocal plasticity as well as vocal diversity. Thus, the overall aim of this study was to test the presence of structural overlap between calls used in social communication and echolocation pulses emitted during foraging in greater tube-nosed bats (Murina leucogaster). Acoustic analysis and spectrotemporal decomposition of calls revealed a rich communication repertoire comprising 12 simple syllables and 5 composites with harmonics in the ultrasonic range. Simultaneous recording of vocal and social behavior in the same species yielded a strong correspondence between distinct behaviors and specific call types in support of Morton's motivation-structure hypothesis. Spectrographic analysis of call types also revealed the presence of modified components of echolocation pulses embedded within social calls. Altogether, the data suggest that bats can parse complex sounds into structurally simpler components that are recombined within behaviorally meaningful and multifunctional contexts.