Non-individualistic ultrasonic and audible isolation calls throughout ontogeny in a rodent, Eolagurus luteus.

Acoustic individuality is present in diverse taxa of mammals and birds, becoming especially prominent in those age groups for which discriminating conspecifics by voice is critically important. This study compares, for the first time, the ontogenetic changes of acoustic individuality of ultrasonic and audible calls (USVs and AUDs) across 12 age-classes (from neonates to adults) in captive yellow steppe lemmings Eolagurus luteus. We found that, in this rodent species, the isolation-induced USVs and AUDs are not individually distinct at any age. We discuss that this result is unusual, because discriminating individuals by individualistic vocal traits may be important for such a social species as yellow steppe lemming. We also discuss the potential role of acoustic individuality in studies including rodent models.

Discomfort-related changes of call rate and acoustic variables of ultrasonic vocalizations in adult yellow steppe lemmings Eolagurus luteus.

Potential of ultrasonic vocalizations (USVs) to reflect a degree of discomfort of a caller is mostly investigated in laboratory rats and mice but poorly known in other rodents. We examined 36 (19 male, 17 female) adult yellow steppe lemmings Eolagurus luteus for presence of USVs during 8-min experimental trials including 2-min test stages of increasing discomfort: isolation, touch, handling and body measure. We found that 33 of 36 individuals vocalized at isolation stage, i.e., without any human impact. For 14 (6 male and 8 female) individuals, a repeated measures approach revealed that increasing discomfort from isolation to handling stages resulted in increase of call power quartiles and fundamental frequency, whereas call rate remained unchanged. We discuss that, in adult yellow steppe lemmings, the discomfort-related changes of USV fundamental frequency and power variables follow the same common rule as the audible calls of most mammals, whereas call rate shows a different trend. These data contribute to research focused on searching the universal acoustic cues to discomfort in mammalian USVs.

Pup ultrasonic isolation calls of six gerbil species and the relationship between acoustic traits and body size.

Among Gerbillinae rodents, ultrasonic calls of adults of small-sized species are typically higher frequency than those of adults of large-sized species. This study investigates whether a similar relationship can be found in pups of six gerbil species (Dipodillus campestris, Gerbillus perpallidus, Meriones unguiculatus, Meriones vinogradovi, Sekeetamys calurus and Pachyuromys duprasi). We compared the average values of acoustic variables (duration, fundamental and peak frequency) of ultrasonic calls (20 calls per pup, 1200 in total) recorded from 6- to 10-day-old pups (10 pups per species, 60 in total) isolated for 2 min at 22°C and then weighed and measured for body variables. The longest calls (56 ± 33 ms) were found in the largest species, and the highest frequency calls (74.8 ± 5.59 kHz) were found in the smallest species. However, across species, call duration (ranging from 56 to 159 ms among species) did not display a significant relationship with pup body size; and, among frequency variables, only the minimum fundamental frequency depended on pup body size. Discriminant analysis assigned 100% of calls to the correct species. The effect of species identity on the acoustics was stronger than the effect of body size. We discuss these results with the hypotheses of acoustic adaptation, social complexity, hearing ranges and phylogeny.

Ontogeny of audible squeaks in yellow steppe lemming Eolagurus luteus: trend towards shorter and low-frequency calls is reminiscent of those in ultrasonic vocalization.

BACKGROUND: Rodents are thought to be produced their human-audible calls (AUDs, below 20 kHz) with phonation mechanism based on vibration of the vocal folds, whereas their ultrasonic vocalizations (USVs, over 20 kHz) are produced with aerodynamic whistle mechanism. Despite of different production mechanisms, the acoustic parameters (duration and fundamental frequency) of AUDs and USVs change in the same direction along ontogeny in collared lemming Dicrostonyx groenlandicus and fat-tailed gerbil Pachyuromys duprasi. We hypothesize that this unidirectional trend of AUDs and USVs is a common rule in rodents and test whether the AUDs of yellow steppe lemmings Eolagurus luteus would display the same ontogenetic trajectory (towards shorter and low-frequency calls) as their USVs, studied previously in the same laboratory colony. RESULTS: We examined for acoustic variables 1200 audible squeaks emitted during 480-s isolation-and-handling procedure by 120 individual yellow steppe lemmings (at 12 age classes from neonates to breeding adults, 10 individuals per age class, up to 10 calls per individual, each individual tested once). We found that the ontogenetic pathway of the audible squeaks, towards shorter and lower frequency calls, was the same as the pathway of USVs revealed during 120-s isolation procedure in a previous study in the same laboratory population. Developmental milestone for the appearance of mature patterns of the squeaks (coinciding with eyes opening at 9-12 days of age), was the same as previously documented for USVs. Similar with ontogeny of USVs, the chevron-like squeaks were prevalent in neonates whereas the squeaks with upward contour were prevalent after the eyes opening. CONCLUSION: This study confirms a hypothesis of common ontogenetic trajectory of call duration and fundamental frequency for AUDs and USVs within species in rodents. This ontogenetic trajectory is not uniform across species.

Audible calls and their ontogenetic relationship with ultrasonic vocalization in a rodent with a wide vocal range, the fat-tailed gerbil (Pachyuromys duprasi).

Ontogeny of audible and ultrasonic calls is poorly studied in Gerbillinae rodents. In this study, analysis of calls, emitted by pup and adult fat-tailed gerbils Pachyuromys duprasi during 420-s isolation-and-handling procedures, allowed testing two hypotheses. Hypothesis1 predicted that audible squeaks and clicks follow the same ontogenetic pathway (towards higher-frequency and shorter calls) that has been previously documented for the ultrasonic calls of fat-tailed gerbil. Hypothesis2 predicted that the audible call types would alternate with the ultrasonic call types along ontogeny in this species. Hypothesis1 was tested with comparison of acoustic variables of audible calls (squeaks and clicks), emitted by 1-10-day old pups and by adults. Clicks of 8.3-8.7 kHz and high-frequency squeaks of 1.92-3.57 kHz were present in pups and adults, whereas mid-frequency squeaks of 0.31-0.67 kHz and low-frequency squeaks of 0.04-0.11 kHz were only present in pups. In agreement with Hypothesis1, pup high-frequency squeaks were longer, lower in fundamental frequency and higher in peak frequency. Against predictions, clicks did not differ acoustically between pups and adults. Hypothesis2 was tested with comparison of percentages of test trials containing the audible and/or ultrasonic call types of pups, repeatedly tested in 15 age classes along ontogeny from 1 to 40 days of age and in adults. The audible calls occurred in all age classes, whereas the ultrasonic calls emerged from day five of pup life and then prevailed over the audible squeaks in all age classes. We discuss that, in fat-tailed gerbil, ontogenetic pathways of acoustic variables of audible and ultrasonic calls (towards higher-frequency and shorter calls) are unusual for rodents although are typical for social and echolocation calls of bats. The is another parallelism of acoustic communication between bats and rodents aside from the recently discovered similarity between bat ultrasonic echolocation and echo-based navigation with bouts of ultrasonic calls in blind leaping rodents.

Rapid development of mature vocal patterns of ultrasonic calls in a fast-growing rodent, the yellow steppe lemming (Eolagurus luteus).

Ultrasonic vocalizations (USV) of laboratory rodents may serve as age-dependent indicators of emotional arousal and anxiety. Fast-growing Arvicolinae rodent species might be advantageous wild-type animal models for behavioural and medical research related to USV ontogeny. For the yellow steppe lemming Eolagurus luteus, only audible calls of adults were previously described. This study provides categorization and spectrographic analyses of 1176 USV calls emitted by 120 individual yellow steppe lemmings at 12 age classes, from birth to breeding adults over 90 days (d) of age, 10 individuals per age class, up to 10 USV calls per individual. The USV calls emerged since 1st day of pup life and occurred at all 12 age classes and in both sexes. The unified 2-min isolation procedure on an unfamiliar territory was equally applicable for inducing USV calls at all age classes. Rapid physical growth (1 g body weight gain per day from birth to 40 d of age) and the early (9-12 d) eyes opening correlated with the early (9-12 d) emergence of mature vocal patterns of USV calls. The mature vocal patterns included a prominent shift in percentages of chevron and upward contours of fundamental frequency (f0) and the changes in the acoustic variables of USV calls. Call duration was the longest at 1-4 d, significantly shorter at 9-12 d and did not between 9-12-d and older age classes. The maximum fundamental frequency (f0max) decreased with increase of age class, from about 50 kHz in neonates to about 40 kHz in adults. These ontogenetic pathways of USV duration and f0max (towards shorter and lower-frequency USV calls) were reminiscent of those in laboratory mice Mus musculus.

High frequency audible calls in northern birch mice Sicista betulina in response to handling: effects of individuality, sex and body mass on the acoustics.

OBJECTIVES: This is the first study of the sonic and ultrasonic vocalization in a Dipodidae rodent. For the small-sized quadrupedal northern birch mouse Sicista betulina, phylogenetically related to the bipedal jerboas (Dipodidae), we report null results for ultrasonic vocalization and investigate the acoustic cues to individual identity, sex and body size in the discomfort-related high-frequency tonal sonic calls. RESULTS: We used a parallel audio recording in the sonic and ultrasonic ranges during weighting adult northern birch mice before the scheduled hibernation in captivity. The sonic (audible) high-frequency tonal calls (ranging from 6.21 to 9.86 kHz) were presented in all individuals (7 males and 4 females). The ultrasonic calls lacked in the recordings. Two-way nested ANOVA revealed the effects of caller individual identity on all 10 measured acoustic variables and the effects of sex on four out of 10 measured acoustic variables. Discriminant function analyses with 10 acoustic variables included in the analysis showed 85.5% correct assignment of calls to individual and 79.7% correct assignment of calls to sex; both values significantly exceeded the random values (23.1% and 54.3%, respectively) calculated with randomization procedure. Body mass did not differ between sexes and did not correlate significantly with the acoustic variables.

Ultrasonic vocalization of pup and adult fat-tailed gerbils (Pachyuromys duprasi).

Ultrasonic vocalizations (USVs) of laboratory rodents indicate animal emotional arousal and may serve as models of human disorders. We analysed spectrographically USV calls of pup and adult fat-tailed gerbils Pachyuromys duprasi during 420-s tests, including isolation, touch and handling. Based on combination of six different USV syllable contour shapes and six different note compositions, we classified 782 USV syllables of 24 pups aged 5-10 days to 18 types and 232 syllables of 7 adults to 24 types. Pups and adults shared 16 of these 26 USV types. Percentages of USV syllables with certain contour shapes differed between pups and adults. The contour shape and note composition significantly affected most acoustic variables of USV syllables in either pups or adults. The 1-note USV syllables were most common in either pups or adults. Pup USV syllables were overall longer and higher-frequency than adult ones, reminiscent of the USV ontogenetic pathway of bats and distinctive to rats and mice. We discuss that the USV syllable types of fat-tailed gerbils were generally similar in contour shapes and note compositions with USV syllable types of mice and rats, what means that software developed for automated classifying of mice ultrasound might be easily adapted or re-tuned to gerbil USV calls. However, using fat-tailed gerbils as model for biomedical research including control of USV vocalization is only possible since 6th day of pup life, because of the delayed emergence of USV calls in ontogeny of this species.

Vocal development during postnatal growth and ear morphology in a shrew that generates seismic vibrations, Diplomesodon pulchellum.

The ability of adult and subadult piebald shrews (Diplomesodon pulchellum) to produce 160Hz seismic waves is potentially reflected in their vocal ontogeny and ear morphology. In this study, the ontogeny of call variables and body traits was examined in 11 litters of piebald shrews, in two-day intervals from birth to 22 days (subadult), and ear structure was investigated in two specimens using micro-computed tomography (micro-CT). Across ages, the call fundamental frequency (f0) was stable in squeaks and clicks and increased steadily in screeches, representing an unusual, non-descending ontogenetic pathway of f0. The rate of the deep sinusoidal modulation (pulse rate) of screeches increased from 75Hz at 3-4 days to 138Hz at 21-22 days, probably relating to ontogenetic changes in contraction rates of the same muscles which are responsible for generating seismic vibrations. The ear reconstructions revealed that the morphologies of the middle and inner ears of the piebald shrew are very similar to those of the common shrew (Sorex araneus) and the lesser white-toothed shrew (Crocidura suaveolens), which are not known to produce seismic signals. These results suggest that piebald shrews use a mechanism other than hearing for perceiving seismic vibrations.

Measuring airborne components of seismic body vibrations in a Middle-Asian sand-dwelling Insectivora species, the piebald shrew (Diplomesodon pulchellum).

Self-produced seismic vibrations have been found for some subterranean rodents but have not been reported for any Insectivora species, although seismic sensitivity has been confirmed for blind sand-dwelling chrysochlorid golden moles. Studying the vocal behaviour of captive piebald shrews, Diplomesodon pulchellum, we documented vibrations, apparently generated by the whole-body wall muscles, from 11 (5 male, 6 female) of 19 animals, placed singly on a drum membrane. The airborne waves of the vibratory drumming were digitally recorded and then analysed spectrographically. The mean frequency of vibration was 160.5 Hz. This frequency matched the periodicity of the deep sinusoidal frequency modulation (159.4 Hz) found in loud screech calls of the same subjects. The body vibration was not related to thermoregulation, hunger-related depletion of energy resources or fear, as it was produced by well-fed, calm animals, at warm ambient temperatures. We hypothesize that in the solitary, nocturnal, digging desert piebald shrew, body vibrations may be used for seismic exploration of substrate density, to avoid energy-costly digging of packed sand for burrowing and foraging. At the same time, the piercing quality of screech calls due to the deep sinusoidal frequency modulation, matching the periodicity of body vibration, may be important for agonistic communication in this species.