Northern Elephant Seals Memorize the Rhythm and Timbre of Their Rivals’ Voices

Abstract

The evolutionary origin of rhythm perception, a cognitive ability essential to musicality, remains unresolved [1-5]. The ability to perceive and memorize rhythmic sounds is widely shared among humans [6] but seems rare among other mammals [7, 8]. Although the perception of temporal metrical patterns has been found in a few species, this ability has only been demonstrated through behavioral training [9] (but see [10] for an example of spontaneous tempo coordination in a bonobo), and there is no experimental evidence to indicate its biological function. Furthermore, there is no example of a non-human mammal able to remember and recognize auditory rhythmic patterns among a wide range of tempi. In the northern elephant seal Mirounga angustirostris, the calls of mature males comprise a rhythmic series of pulses, with the call of each individual characterized by its tempo and timbre; these individual vocal signatures are stable over years and across contexts [11]. Here, we report that northern elephant seal males routinely memorize and recognize the unique tempo and timbre of their rivals' voices and use this rhythmic information to individually identify competitors, which facilitates navigation within the social network of the rookery. By performing playbacks with natural and modified vocalizations, we show that males are sensitive to call rhythm disruption independently of modification of spectral features and that they use both temporal and spectral cues to identify familiar rivals. While spectral features of calls typically encode individual identity in mammalian vocalizations [12], this is the first example of this phenomenon involving sound rhythm.

Comparison of methods for rhythm analysis of complex animals’ acoustic signals

“…C. perspicillata sequences are shorter than 1 second and show a constant tempo, which would make the GAT approach the most suitable one. To give possible acoustic signal types for other paths, depending on the data might be from left to right in Fig 7: short call sequences of rodents, for example ultrasonic pulses of Typhlomus chapensis [42]; for sequences with a higher probability for individual differences that are above 1 second in duration and show a constant tempo one could think of male zebra finch song [5] or the vocalization sequences of pinnipeds such as the Northern elephant seal [6]. For a sequence with a changing tempo, one might think of a territorial song of some bat species that escalate and increase the tempo in the end [43][44][45].…”

“…Moreover, the first instance for a biologically relevant rhythm in non-human mammalian acoustic signals was found in the northern elephant seal, where males can discriminate between familiar and unfamiliar male opponents using the temporal structure of vocalizations. Rhythms apparently differ between individuals in a way that facilitates the discrimination of individuals [6].…”

“…wingbeats per second), independent from whether a bat might actually be flying in a vocalizing context or hanging in a roost [4]. Rhythmicality might also influence mate choice and individual recognition [5,6]. Furthermore, neural correlates might play a role so that careful rhythm analysis can give insights into internal clocks or the importance of certain brain waves on different behavioral aspects such as the production of acoustic signals [5,7].…”

Sonification of Animal Tracks as an Alternative Representation of Multi-Dimensional Data: A Northern Elephant Seal Example

“…Provided the trade-offs with aerial hearing it seems that underwater hearing should be of significant to the animals, which have been demonstrated to be able to detect acoustic signals at relatively low signal-to-noise ratios (Southall et al, 2000). Recently, northern elephants seals have been demonstrated to routinely memorize and recognize the unique tempo and timbre of other animal's voices and use this rhythmic information to individually identify them (Mathevon et al, 2017). This is the first demonstration of the capacity for individual mammalian identification involving sound rhythm, and provides evidence of the significance of sound and auditory skills of northern elephant seals.…”

Long‐term sound and movement recording tags to study natural behavior and reaction to ship noise of seals

“…Like cetaceans, pinnipeds have sensitive underwater hearing; their full hearing range extends from a few hundred Hz to 70–80 kHz (Cunningham & Reichmuth, ; Hemilä, Nummela, Berta, & Reuter, ). They rely on sound for communication (Mathevon, Casey, Reichmuth, & Charrier, ; Van Parijs, Hastie, & Thompson, ), predator detection (Deecke, Slater, & Ford, ), and possibly also for navigation and listening for prey (Schusterman, Levenson, Reichmuth, & Southall, ). Pinnipeds have been found to respond strongly to underwater tone pulses at 8–45 kHz in captivity (Götz & Janik, ; Kastelein et al, ; Kastelein, Heul, Terhune, Verboom, & Triesscheijn, ; Kastelein, Heul, Verboom, Triesscheijn, & Jennings, ) and to sounds from seismic surveys (Harris, Miller, & Richardson, ) and pile driving (Russell et al, ) in the wild.…”