Ultrasonic Vocalizations of Six Taxa of Southern African Gerbils (Rodentia: Gerbillinae)

Ultrasonic calling during male-female encounters between individuals of the same species was investigated in six taxa of southern African gerbils, namely Tatera brantsii, Gerbillurus paeba paeba, G. p. cxilis, G. tytonis, G. setzeri, and G. vallinus. Vocalizations were detected by means of a bat detector utilizing a superheterodyne signal converter and a countdown circuit. Signals were recorded at audible frequencies and analysed with a sonograph. All taxa vocalized at ultrasonic frequencies by means of strongly modulated frequency “sweep” calls, which differed among taxa in duration, maximum and minimum frequency. “Clicks” were emitted by G. p. paeba and G. p. exilis, and G. tytonis emitted a “stutter” vocalization which consisted of a series of clicks. Long modulated “whistles” were identified from G. vallinus and T. brantsii at lower frequencies than “sweep” calls. Only one call type, a “sweep” call which differed in duration and frequency from all other taxa, was identified in G. setzeri. Cluster analysis was applied to the data using 7 acoustic characters. G. p. paeba and G. p. exilis displayed the highest similarity level between taxa and differed only in frequency of “sweep” vocalizations. G. paeba, G. tytonis and G. setzeri formed one cluster, while G. vallinus and T. brantsii formed a separate cluster. Numbers of calls in interspecific encounters were non-significantly less than in intraspecific encounters in all taxa except G. p. paeba, in which more vocalizations were recorded in inter- than intraspecific encounters. It is not clear whether species discrimination, measured by numbers of vocalizations in interspecific encounters, occurs.     

A Comparative Study of the Behaviour of Six Taxa of Male and Female Gerbils (Rodentia) in Intra- and Interspecific Encounters

Frequencies and sequences of visually-identifiable acts were investigated in male-female combinations of gerbils of the taxa Tatera brantsii, Gerbillurus paeba paeba, G. p. exilis, G. tytonis, G. setzeri, and G. vallinus. Sexual dimorphism of behaviour was most apparent in T. brantsii, G. setzeri, and G. vallinus, in which following, anogenital sniffing, and mounting were significantly more frequently performed by males than females. Females of all taxa presented and darted, while males did not perform these acts. Analysis of first-order transitions of acts in intraspecific encounters revealed remarkable similarity among species in the sequences identified as most significantly deviating from expected frequency. Species-specific patterns of behaviour were detected by discriminant analysis. G. p. paeba, G. p. exilis and G. vallinus were not clearly distinguished by discriminant analysis, and presented a behaviour pattern characterized by low levels of aggression and high levels of huddling behaviour. G. tytonis, G. setzeri and T. brantsii were characterized by low levels of huddling, G. tytonis performed the largest number of upright postures of all taxa, G. setzeri watched more than other taxa, and T. brantsii nasal sniffed less frequently than Gerbillurus taxa. Differences among taxa were more apparent in males than in females. Interspecific encounters were staged between G. p. paeba and G. p. exilis, G. p. paeba and G. tytonis, G. setzeri and G. vallinus. Males showed more evidence of changed behaviour in interspecific encounters than females. More sexual and less agonistic behaviour was detected in intraspecific encounters than in interspecific encounters, but this was statistically significant in only 5 of 12 combinations. Visual, tactile and olfactory communication during physical contact with another individual may complement auditory communication in promoting conspecific recognition in southern African gerbils.     

Male-Female Interactions in Hairy-footed Gerbils (Genus Gerbillurus)

Staged 10-min encounters between male and female gerbils of the same species were characterized by high levels of exploratory and solitary behaviour, variable levels of agonistic behaviour, and little contact-promoting behaviour. Female Gerbillurus paeba paeba, G. p. exilis and G. tytonis dominated males of these species, while male and female G. setzeri and G. vallinus were equally aggressive. Results of this study indicate that G. p. paeba, G. p. exilis and G. tytonis are aggressively solitary and that females behave aggressively towards unfamiliar males, while G. setzeri and G. vallinus are more tolerant. This is in partial agreement with findings for other gerbil species.     

A Comparative Study of Agonistic Behaviour in Hairy-footed Gerbils (Genus Gerbillurus)

Intraspecific agonistic behaviour was investigated by means of staged encounters in Gerbillurus paeba paeba, G. p. exilis, G. tytonis, G. setzeri and G. vallinus. Four groups of behaviour were identified by motivational analysis: i.e. “exploratory and solitary”, “aggressive”, “submissive”, and “sexual” behaviour. Frequencies of acts and levels of interaction differed among species and sexes. Cluster analysis of behaviour data revealed three clusters which agree partially with the karyology and taxonomy of the genus. G. p. paeba and G. tytonis were very aggressive and highly active; female G. p. exilis and G. setzeri less so; while male G. p. exilis and G. vallinus were least aggressive and active, performing more contact-promoting behaviour than other species. A range of social types is exhibited from solitary (G. p. paeba and G. tytonis) through semi-tolerant (G. setzeri and female G. p. exilis) to tolerant (male G. p. exilis and G. vallinus).     

Targeted Training of Ultrasonic Vocalizations in Aged and Parkinsonian Rats

Voice deficits are a common complication of both Parkinson disease (PD) and aging; they can significantly diminish quality of life by impacting communication abilities. ^{1, 2} Targeted training (speech/voice therapy) can improve specific voice deficits,^{3, 4} although the underlying mechanisms of behavioral interventions are not well understood. Systematic investigation of voice deficits and therapy should consider many factors that are difficult to control in humans, such as age, home environment, age post-onset of disease, severity of disease, and medications. The method presented here uses an animal model of vocalization that allows for systematic study of how underlying sensorimotor mechanisms change with targeted voice training. The ultrasonic recording and analysis procedures outlined in this protocol are applicable to any investigation of rodent ultrasonic vocalizations.The ultrasonic vocalizations of rodents are emerging as a valuable model to investigate the neural substrates of behavior.^5-8 Both rodent and human vocalizations carry semiotic value and are produced by modifying an egressive airflow with a laryngeal constriction.^{9, 10} Thus, rodent vocalizations may be a useful model to study voice deficits in a sensorimotor context. Further, rat models allow us to study the neurobiological underpinnings of recovery from deficits with targeted training.To model PD we use Long-Evans rats (Charles River Laboratories International, Inc.) and induce parkinsonism by a unilateral infusion of 7 μg of 6-hydroxydopamine (6-OHDA) into the medial forebrain bundle which causes moderate to severe degeneration of presynaptic striatal neurons (for details see Ciucci, 2010).^{11, 12} For our aging model we use the Fischer 344/Brown Norway F1 (National Institute on Aging).Our primary method for eliciting vocalizations is to expose sexually-experienced male rats to sexually receptive female rats. When the male becomes interested in the female, the female is removed and the male continues to vocalize. By rewarding complex vocalizations with food or water, both the number of complex vocalizations and the rate of vocalizations can be increased (Figure 1).An ultrasonic microphone mounted above the male''s home cage records the vocalizations. Recording begins after the female rat is removed to isolate the male calls. Vocalizations can be viewed in real time for training or recorded and analyzed offline. By recording and acoustically analyzing vocalizations before and after vocal training, the effects of disease and restoration of normal function with training can be assessed. This model also allows us to relate the observed behavioral (vocal) improvements to changes in the brain and neuromuscular system.     

Defects in Ultrasonic Vocalization of Cadherin-6 Knockout Mice

Background

Although some molecules have been identified as responsible for human language disorders, there is still little information about what molecular mechanisms establish the faculty of human language. Since mice, like songbirds, produce complex ultrasonic vocalizations for intraspecific communication in several social contexts, they can be good mammalian models for studying the molecular basis of human language. Having found that cadherins are involved in the vocal development of the Bengalese finch, a songbird, we expected cadherins to also be involved in mouse vocalizations.

Methodology/Principal Findings

To examine whether similar molecular mechanisms underlie the vocalizations of songbirds and mammals, we categorized behavioral deficits including vocalization in cadherin-6 knockout mice. Comparing the ultrasonic vocalizations of cadherin-6 knockout mice with those of wild-type controls, we found that the peak frequency and variations of syllables were differed between the mutant and wild–type mice in both pup-isolation and adult-courtship contexts. Vocalizations during male-male aggression behavior, in contrast, did not differ between mutant and wild–type mice. Open-field tests revealed differences in locomotors activity in both heterozygote and homozygote animals and no difference in anxiety behavior.

Conclusions/Significance

Our results suggest that cadherin-6 plays essential roles in locomotor activity and ultrasonic vocalization. These findings also support the idea that different species share some of the molecular mechanisms underlying vocal behavior.     

COMPARISONS OF THE VOCALIZATIONS AND SOCIAL BEHAVIOUR OF SOUTHERN AFRICAN PYCNONOTUS BULBULS

Lloyd, P., Hulley, P.E. & Craig, A.J.F.K. 1996. Comparisons of the vocalizations and social behaviour of southern African Pycnonotus bulbuls. Ostrich 67: 118–125.

Vocalizations and associated behaviour of three Pycnonotus species are described, based on field observations and tape recordings from which sonagrams were produced. These species, which are locally sym-patric and hybridize, have similar vocalizations and displays; differences are most apparent in their contact calls and songs. Quantitative analysis of the songs showed that P. barbatus and P. capensis are easily distinguished, whereas the song characteristics of P. nigricans overlap those of both the other species. Playback experiments with territorial male P. barbatus in an area of allopatry showed similar responses to songs of conspecifics and of P. nigricans, but almost no response to the song of P. capensis.     

Sex‐dependent effects of Cacna1c haploinsufficiency on juvenile social play behavior and pro‐social 50‐kHz ultrasonic communication in rats

As cross‐disorder risk gene, CACNA1C is implicated in the etiology of all major neuropsychiatric disorders characterized by deficits in social behavior and communication and there is evidence for sex‐dependent influences of single‐nucleotide polymorphisms within CACNA1C on diagnosis, course, and recovery in humans. In this study, we aimed, therefore, at further exploring the role of Cacna1c in regulating behavioral phenotypes, focusing on sex‐specific differences in social behavior and communication during the critical developmental period of adolescence in rats. Specifically, we compared rough‐and‐tumble play, concomitant emission of pro‐social 50‐kHz ultrasonic vocalizations, and social approach behavior in response to playback of 50‐kHz ultrasonic vocalizations between constitutive heterozygous Cacna1c ^+/? females and wildtype Cacna1c ^+/+ littermate controls, and contrasted present female findings to data previously reported in males. Our results show for the first time that partial depletion of Cacna1c leads to sex‐dependent alterations in social behavior and communication in rats. In females, Cacna1c haploinsufficiency led to hypermasculinization, with rough‐and‐tumble play behavior, in general, and pinning behavior, in particular, being even higher than in males without affecting concomitant 50‐kHz ultrasonic vocalizations. In males, in contrast, rough‐and‐tumble play behavior was not altered, yet emission of 50‐kHz ultrasonic vocalizations was diminished following partial Cacna1c depletion. The behavioral responses elicited by playback of 50‐kHz ultrasonic vocalizations were reduced upon partial Cacna1c depletion in both sexes. It thus can be concluded that Cacna1c plays a prominent sex‐dependent role in regulating juvenile rat social play behavior and pro‐social 50‐kHz ultrasonic communication with relevance to sex‐specific effects seen in neuropsychiatric disorders.     

Vocal repertoire of the social Mashona mole-rat (Fukomys darlingi) and how it compares with other mole-rats

Vocalizations play a major role in communication of mammals with subterranean lifestyles since other senses are dramatically restricted in the environment of below ground burrows. In our study, we recorded vocalizations of 10 adult males and 10 adult females of a social bathyergid, the Mashona mole-rat (Fukomys darlingi) in different behavioural contexts. Vocalizations were divided into four categories according to behavioural contexts. Similar to other subterranean mammals, the range of Mashona mole-rat calls is shifted towards lower frequencies. We described 10 types of true vocal signals and 2 mechanical sounds. The vocal repertoire of the Mashona mole-rat is less rich compared to other social mole-rats, corresponding with its low mean family size. Interestingly, this species has a higher diversity in contact and distress calls, while using a relatively low number of aggressive signals.     

Preliminary observations on squirrel monkey (Saimiri oerstedi) vocalizations in Costa Rica

This study was an initial attempt to analyze quantitatively vocalizations from the Central American squirrel monkey, Saimiri oerstedi. Vocalizations were recorded in the wild at P. N. Corcovado (S. o. oerstedi). and at P. N. Manuel Antonio (S. o. citrinellus). Additional recordings were made from captive individuals of both subspecies. The acoustic structure of analyzed vocalizations resembled most closely the vocal repertoire of South American Saimiri with the “gothic arch” phenotype, in agreement with the prominent gothic arch facial pattern of S. oerstedi. New structural subtypes of the twitter (“dog-tooth twitter”) and the chuck (“bent-mast chuck”) not previously found in an extensive library of South American Saimiri sound spectrograms were documented. Calls used by older infants when socially separated and when approaching an adult male were essentially identical (sharing typical “isolation peep” structural features) but had significantly different duration and peak frequency. Analysis of recordings from an escaped captive female calling outside her compound over a 3-day period indicated the presence of numerous structural intermediates between typical chuck, twitter, and peep calls.     

Maternal behaviour and neonatal development in three species of Namib Desert rodents

Gerhillurus paeba paeba, G. tytonis and Pelromyscus collinus inhabit arid areas of southern Africa. Several litters of each species were bred in the laboratory; aspects of maternal behaviour and development of neonates are reported. Pelromyscus collinus has a smaller litter size and the young are less altricial at birth than young of G. paeba or G. tytonis. Gerhillurus tytonis young have the slowest rate of physical and behavioural development, while P. collinus young develop most rapidly. Young of P. collinus nipple-cling from birth, but those of G. paeba and G. tytonis do not. This dichotomy may be related to phylogeny, mode of locomotion, and/or nesting habits.     

4. THE SOUTH AFRICAN CLIFF SWALLOW

Short, L.L. &; Horne, J. F. M. 1980, Vocal and other behaviour of the Green Barbet in Kenya. Ostrich 51:219–229.

Brief field studies of the Green Barbet Stactolaema olivacea in coastal Kenya, with emphasis on vocalizations, document its social behaviour, including communal roosting of four birds in a cavity. Green Barbets are aggressive, interacting strongly with a number of species. Erecting of the crown feathers, cocking of the tail, and woodpeckerlike swinging movements characterize displays. Wing Flutters and audible Bill Wiping are visual-auditory displays. Vocalizations include the Grating Call, Kek Call, Chuk Call and Chowp Call. These are agonistic and agonistic-reproductive in function. The Chowp Call comprises the song, used in simultaneous singing and duetting.     

Species-specific and shared features in vocal repertoires of three Eurasian ground squirrels (genus <Emphasis Type="Italic">Spermophilus</Emphasis>)

Along to alarm calls, Eurasian ground squirrels of the genus Spermophilus also produce other call types toward potential predators and rival conspecifics. Individually identified 50 speckled (Spermophilus suslicus), 18 European (S. citellus) and 59 yellow (S. fulvus) ground squirrels were examined for interspecies differences in their vocal repertoires. A separate sample of 116 (90 adult and 26 juvenile) S. suslicus was examined for presence of ultrasound in their alarm calls. In addition, all tonal calls in all the three species were checked for presence of nonlinear phenomena. Calls were elicited by approaching animals in live-traps or near burrows; some types of vocalizations were also recorded during handling. Eight call types, three tonal and five wideband ones, were described. Vocal repertoires were remarkably similar between species, excluding the alarm calls, which were species-specific. Alarm calls with ultrasonic components were found in two individuals of S. suslicus. Concerning nonlinear phenomena, biphonation in alarm calls of S. suslicus, frequency jumps and sidebands in screams of S. citellus, frequency jumps and subharmonics in screams of S. fulvus were found. Results are discussed with literature evidence on audible and ultrasonic vocalizations in ground squirrels.     

Geographical variation in temporal and spatial vocalization patterns of male harbour seals in the mating season

In the aquatically mating harbour seal, Phoca vitulina, oestrous females show marked differences in spatial and temporal distribution between geographical areas. This suggests that the males' display behaviour may also vary between areas. We recorded male vocalizations in two areas, the Moray Firth and Orkney, U.K. In the Moray Firth, females haul out on a few intertidal sandbars and travel along predictable routes to forage at sea. In Orkney, female haul out sites are much less influenced by tidal availability and females are much more dispersed. In the Moray Firth, males vocalized only during a short mating season, from 1 July to 12 August. Vocalizations varied significantly with the tide, the peak at high tide clearly coinciding with the period when most females were in the water. In contrast, vocalizations in Orkney were significantly related to both tidal and diel patterns. We suggest that the timing of male vocalizations reflects differences in female availability between sites. In the inner Moray Firth, vocalizations were heard throughout the females' range, whereas vocalizations in Orkney were heard only in two discrete areas. However, at both sites the density of vocalizing males was highest in narrow channels and/or along predictable female travel routes. Therefore, males clearly adapt their temporal and spatial behaviour patterns to variations in female distribution and density. These results suggest that male mating strategies in aquatically mating pinnipeds are more variable than was previously envisaged. Copyright 1999 The Association for the Study of Animal Behaviour.     

An ethogram of the common marmoset (Calithrix jacchus jacchus): General behavioural repertoire

The behavioural repertoire of four captive breeding pairs of Callithrix jacchus jacchus is described. Social communication took the form of postures, facial expressions, vocalizations and piloerection displays. Detailed analyses were made of piloerection displays, adult play, copulatory, aggressive, and prey-catching behaviour. Aggressive behaviour was uncommon in adult mated pairs. Play between adults showed a degree of temporal organization. Vocalizations were the main methods of intragroup communication whilst piloerection displays were directed towards members of other groups and also to unfamiliar objects. The behavioural repertoire of C. jacchus jacchus is compared with that of other Primates.     

ULTRASONIC VOCALIZATIONS AND THEIR ASSOCIATIONS WITH THE NON-VOCALIZATION BEHAVIOUR OF THE ENDANGERED TURKISH SPINY MOUSE ACOMYS CILICIUS SPITZENBERGER IN A CAPTIVE POPULATION

ABSTRACT

Although ultrasonic vocalizations (USVs) have been recorded in many species of rodent and in various contexts, e.g. sexual behaviour and aggression, it has not been demonstrated for the endangered Turkish Spiny Mouse Acomys cilicius Spitzenberger. This study investigated whether A. cilicius emits USVs and, if so, how these USVs associated with non-vocalization behaviour. Ultrasonic recording equipment was set up for 12 days in an off-exhibit enclosure of A. cilicius at Bristol Zoo. At least seven different types of USV were recorded. For eight of the 12 study days, ultrasonic and video recording equipment were run concurrently. From these observations it was found that emission of USVs were associated with sexual behaviour, aggression and social investigation. The results of this study show for the first time that captive A. cilicius produce USVs that resemble those produced by other rodent species, including its close relative the Egyptian Spiny Mouse A. cahirinus Desmarest. As these findings apply only to a captive Turkish Spiny Mouse population, additional work should be carried out to investigate the behaviour and USV production in the wild in addition to further research on captive populations investigating the apparent communicative function of these vocalizations.     

Larger body size on islands affects silvereye Zosterops lateralis song and call frequency

Differences in song repertoires and characteristics of island and mainland populations of the same avian species are usually explained by dispersal, cultural evolution and/or habitat differences. The influence of morphology is often overlooked, even though island populations are frequently morphologically distinct from mainland populations, and morphology could affect vocalizations. I compared morphological features, songs, contact calls and alarm calls of six isolated island populations of silvereye Zosterops lateralis with those of two mainland populations to examine whether differences between mainland and island vocalizations were consistent across vocalization types, and whether these differences could be linked to morphological differences. Vocalizations were lower in frequency on islands. Island individuals were larger (both in mass and body structure), and body mass was an important predictor of frequency in contact and alarm calls. I argue that this strong association results from the island rule (islands promote larger body sizes) and cascading effects of morphology on vocalization frequency in this species.     

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.     

EQUIPMENT REVIEWS

ABSTRACT

Research on African elephant (Loxodonta africana) vocal communication has increased in recent years, yet there has been very little data collected on the vocal production of infant African elephants. Vocalizations were recorded from a group of five adult female African elephants and 3 dependent offspring (1 male and 2 female) at Disney's Animal Kingdom, Florida, U.S.A., using custom-designed audio-recording collars worn by the adult females. We measured both source and filter features of infant ‘rumble’ vocalizations made during affiliative social interactions and after cessation of nursing from adult females. Rumble vocalizations produced in the ‘nurse cessation’ context exhibited an upward shift in formant frequency locations, compared to rumbles produced during the ‘affiliation’ context. Additionally, call duration increased and fundamental frequencies decreased after nurse cessations for the male, but both females showed the opposite acoustic response. When infant rumbles accompanied nurse cessations, nursing was more likely to resume within 30 seconds compared to nurse cessations without vocalizations. These results suggest that infant rumbles associated with cessation of nursing reflect the motivational state of infants and may influence maternal responsiveness.