Ultrasound is commonly used for orientation and prey localization by diverse taxa, including bats, odontocete whales, insectivores, and rodents. Ultrasonic signals in these groups range from simple broadband clicks produced by whales, insectivores, and some megachiropteran bats, to highly modified, tonal signals that show structured change over time as in microchiropteran bats . However, in addition to their function in orientation, these signals may also have social functions, including communication of individual identity or group membership, kin recognition, alarm communication, information transfer, infant-mother communication, mate attraction, and territorial defence [2–5].
In contrast to our wealth of knowledge on the use of ultrasound by microchiropteran bats and odontocete whales, we know comparatively little about the use of ultrasound by rodents in the wild [but see ]. However, there has been extensive research on rodent ultrasound in the laboratory, where ultrasonic vocalizations (henceforth USVs) have been documented for a number of rodent species, particularly within the superfamily Muroidea [6, 7]. A major impetus for this large body of research is that the two major mammalian non-human models are muroids: the lab mouse (Mus musculus) and lab rat (Rattus norvegicus). Mice and rats have historically been used for classical human biomedical research and, more recently with the sequencing of both genomes [8, 9], have become the main models for the basis of human and mammalian development and behavior [10, 11]. Because both rat and mouse infants predictably produce USVs in the laboratory, their USVs are regularly used as phenotypic markers in neurobehavioral development . The study of USV production by rats and mice in the laboratory has become so prevalent that a recent effort was made to standardize methods in the study of laboratory rodent USVs . In addition, a detailed study of USVs within individual male mice revealed variation in syllable usage and timing, indicating that laboratory mice are capable of producing song .
Although the majority of research on USVs has occurred in only two model muroid rodent species, the Muroidea is the largest and most diverse superfamily of mammals with over 1300 species in 5 families [15, 16]. Based on laboratory research, it appears that USV production may be common within the Muroidea. Within the muroids, USVs have been documented in 18 genera (B. H. Blake, unpublished data) in the subfamilies Arvicolinae, Cricetinae, Gerbillinae, Murinae, and in the Neotominae-Sigmodontinae [17–22]. Muroids examined in the lab have been shown to produce USVs as juveniles, adults or both, but the context of USV production varies [6, 23]. Neonates and juveniles produce USVs in response to isolation from parents, cool temperatures, handling, anticipation of play, or painful stimuli [6, 17, 24–34]. Adult males and/or females produce USVs during agonistic (mostly intrasexual) interactions [35, 36] and during courtship and mating [6, 37, 38]. Adult males additionally produce ultrasonic songs when stimulated by conspecific urine , and adult females also produce ultrasound when their pups are removed from their nest .
Despite the valuable and extensive research on USVs in rodents in the lab, it is unclear if and when, these USVs are produced in the wild, and how they function in natural habitats. The exception to this is the recent discovery of the use of USVs by the Richardson's ground squirrel (Spermophilus richardsonii) to warn conspecifics of imminent danger . To our knowledge, this is the only test of the functional significance of USV production by rodents in the wild. Without understanding the context of USV production in the wild, it is difficult to understand the selective pressures leading to their evolution and maintenance. Furthermore, although it may be possible to attribute a function to the USVs produced in the lab, it is critical to understand their adaptive significance in a natural context. Understanding the context and function of USV production by wild muroid rodents is especially relevant given the prevalence of behavioral research related to USV production by lab rats and mice. It has been suggested recently that inbreeding of laboratory mice may have acted to reduce the variation in the USVs produced by laboratory mice, and that wild mice might exhibit higher diversity and complexity of USVs and ought to be used for comparisons of song production with other animals .
The purpose of our study was to passively record and characterize USVs given by free-living muroid rodents in the wild. Here we document and characterize, for the first time, USVs given by wild Peromyscus mice in the wild. We examined USV production in two syntopic species of Peromyscus (P. californicus and P. boylii) on long term study grids at the Hastings Natural History Reserve (HNHR), Monterey Co., California. Mice in the genus Peromyscus are models in both field and laboratory research relating to questions of mammalian evolution [39–41], ecology [42–44], and behavior [45–47]. We chose these two particular species of Peromyscus because long term studies of wild populations afforded us detailed knowledge of their ecology and behavior. In addition, time spent in the field has provided us with anecdotal observations of vocalizations being produced by these species.