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

Abstract

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 1 st 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.

Polyphony of domestic dog whines and vocal cues to body size

“…Experiments showed that a few rodent species use the whistling mechanism only for producing the ultrasonic calls ( Riede 2011 , 2013 , 2018 ; Pasch et al 2017 ; Riede et al 2017 ), whereas the audible calls are produced by vibration of the vocal folds ( Riede et al 2011 ; Pasch et al 2017 ). In laboratory rats Rattus norvegicus , domestic mice Mus musculus , fat-tailed gerbils Pachyuromys duprasi , and yellow steppe lemmings Eolagurus luteus , ultrasonic calls are produced in 2 different frequency ranges, so call fundamental frequency either jumps between these ranges or 2 fundamental frequencies are emitted in the different ranges simultaneously, which results in the biphonic call ( Scattoni et al 2008 ; Grimsley et al 2011 ; Riede 2011 , 2013 ; Zaytseva et al 2019 ; Yurlova et al 2020 ). Further experimental study in a helium–oxygen atmosphere ( Riede 2011 ; Pasch et al 2017 ) is necessary to confirm the potential whistling nature of domestic dog high-frequency whines.…”

“…At the same time, for the whistling ultrasonic calls of rodents, the available data about the relationship between the fundamental frequency and body size are contradictory. For example, with body growth, the fundamental frequency of the ultrasonic calls decreases in the yellow steppe lemming ( Yurlova et al 2020 ) but increases in the fat-tailed gerbil ( Zaytseva et al 2019 ).…”

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

“…Biphonation was denoted when two independent fundamental frequencies, the low (f0) and the high (g0) and their combinatory frequency bands (g0–f0, g0–2f0, etc.) were found in an ultrasonic call [ 85 , 88 ] ( figure 3 ). Following [ 88 ], we determined the type of the frequency contour with frequency jumps by virtually smoothing the contour as if the fundamental frequency trace was uninterrupted throughout a call.…”

“…confirmed this classification. This classification was based (with modifications) on classifications developed for domestic mice Mus musculus [85][86][87], fat-tailed gerbils [51] and yellow steppe lemmings Eolagurus luteus [88]. The flat contour was denoted when the difference between f0 min and f0max was less than 6 kHz.…”

“…For each USV, we noted the presence of nonlinear vocal phenomena (figure 3 and electronic supplementary material, audio S2): frequency jumps and biphonations [51,[88][89][90][91]. Frequency jump was denoted when f0 suddenly changed for ≥10 kHz up or down (figure 3) and following [51,[85][86][87][88]. In the previous study on the fat-tailed gerbils, the USVs with one frequency jump were termed royalsocietypublishing.org/journal/rsos R. Soc.…”