Anthropogenic noise decreases activity and calling behavior in wild mice

Background Animals rely on sound to mediate a myriad of daily activities, and anthropogenic noise is a pollutant that alters the natural soundscape within which they are active. As human infrastructure expands, broadband anthropogenic noise increases, which can affect behaviors of free-living nocturnal animals. Mice are nocturnal animals that produce ultrasonic calls as part of their behavioral repertoire. Methods We assessed effects of anthropogenic and natural noise on the behaviors of wild deer mice (Peromyscus maniculatus) and woodland jumping mice (Napaeozapus insignis), two species of mice that produce ultrasonic calls. We measured activity, foraging behavior at a foraging tray, and calling behavior to broadcasts of natural and anthropogenic noise, compared to a baseline with no broadcasting, at 25 focal areas in the Southern Appalachian Mountain Range of North Carolina, USA. Results Deer mice exposed to anthropogenic noise spent less time in focal areas with broadcasted anthropogenic noise. Mice took longer to begin foraging in the presence of anthropogenic noise, they spent less time at the foraging tray, and left fewer husks but consumed the same number of seeds as mice exposed to natural noise. Deer mice were less likely than woodland jumping mice to be the first to enter the focal area and approach food when in the presence of anthropogenic noise. Both species produced few ultrasonic calls in the presence of broadcasted natural and anthropogenic noise compared to their baseline level of calling. We present the first calls recorded from woodland jumping mice. Conclusion Anthropogenic noise affects activity, foraging behavior, and calling behavior of nocturnal mice. Natural noise also affects the calling behavior of mice. Mouse species respond differently to anthropogenic noise, with deer mice appearing more sensitive to anthropogenic noise than woodland jumping mice. Responses to noise could have important effects on the ecology of mice and these two species respond differently. Species differences should be considered when mitigating the effects of noise in conservation ecology

The individual context of ultrasonic vocalizations produced by free-living Brush mice (Peromyscus boylii) with an emphasis on differences between males and females

Muroid rodents regularly use ultrasonic vocalizations (USVs). The majority of research work on USV communication in rodents comes from laboratory strains of rats (Rattus norvegicus) and mice (Mus musculus). Peromyscus boylii species like M. musculus is polygynous to promiscuous depending on population density that regularly produces USVs. The objective of my project was to examine the individual context of USVs produced by wild P. boylii with a specific focus of examining differences between males and females. USVs were recorded during the breeding season however there was no correlation between the number of USVs produce and the proportion of reproductive adult or sub-adult individuals in the population (Pearson's Correlation=0.582, 0.470). Adult P. boylii males with scrotal testis produced USVs when alone and in the presence of an estrous female. There were individual differences between males based on duration and frequency of USVs. Adult, P. boylii females residents produced USVs in the presence of another female and when pups are emerging from the nest. There were individual differences between females based on frequency and bandwidth of USVs. Females produce more 3SV vocalizations than males and the mean overall modulation and bandwidth were lower in males than females. My results suggest that vocalizations produced by males may serve to attract females and facilitate copulation whereas, vocalizations produced by females may serve to mediate social interactions with other females and as warning signals for newly weaned pups. Furthermore, sex is communicated through motif type and spectral characteristics of USV

The Bold, Silent Type: Predictors of Ultrasonic Vocalizations in the Genus Peromyscus

An ongoing question related to the evolution of monogamy is how behavioral traits that characterize individuals in monogamous species evolve, and whether monogamy influences the evolution of these traits. One of the most important models for the study of monogamy in mammals is the California mouse (Peromyscus californicus) that uses ultrasonic vocalizations (USVs) in multiple behavioral contexts, including pair-bonding and courtship. Because the genus Peromyscus has many species that both use USVs and express a variety of mating systems, we were able to examine the relationship among USVs, and other ecological (e.g., xeric habitat), physiological (testosterone), and behavioral (e.g., boldness) traits across species. We measured USVs from seven species at the Peromyscus Genetic Stock Center and derived character traits associated with the species' ecology, physiology, and behavior from published studies, including those that had used stocks from the Peromyscus Genetic Stock Center. We determined whether there were USV traits that were particular to monogamous species or whether traits other than mating system best predicted USVs. The trait that best predicted USVs was not related to mating system, but rather, species boldness. Bold species produced few aggressive barks (likely a defensive agonistic USV type) at a higher mean fundamental frequency than less bold species. In relation to mating system, the barks in monogamous species were shorter in duration than the barks in non-monogamous species. Our results suggest that boldness of a species has a higher selection on USVs than the species mating system, ecology, or physiology and that selection has acted on agonistic acoustic signals. Because another type of USV, the sustained vocalization or SV type, did not differ among species in spite of mating system differences, and because all species produced bark types, we suggest that the USVs in rodents evolved as general signals that have generally been co-opted for particular functions within the mating system context that differs across species, as opposed to signals that have been shaped by mating system type

Testosterone pulses paired with a location induce a place preference to the nest of a monogamous mouse under field conditions

Changing social environments such as the birth of young or aggressive encounters present a need to adjust behavior. Previous research examined how long-term changes in steroid hormones mediate these adjustments. We tested the novel concept that the rewarding effects of transient testosterone pulses (T-pulses) in males after social encounters alters their spatial distribution on a territory. In free-living monogamous California mice (Peromyscus californicus), males administered three T-injections at the nest spent more time at the nest than males treated with placebo injections. This mimics T-induced place preferences in the laboratory. Female mates of T-treated males spent less time at the nest but the pair produced more vocalizations and call types than controls. Traditionally, transient T-changes were thought to have transient behavioral effects. Our work demonstrates that in the wild, when T-pulses occur in a salient context such as a territory, the behavioral effects last days after T-levels return to baseline

Do physiological and environmental factors influence vocal communication and associated behaviors in Peromyscus?

Vocal communication is an integral component of animal behavior and individuals rely on vocal signals to mediate a myriad of daily activities. Despite valuable work from the laboratory, we do not understand how physiological and environmental factors alter vocal communication and activities in complex field settings where multiple competing stimuli occur simultaneously. The goal of my research is to understand how transient testosterone (T) pulses, a physiological factor, and anthropogenic noise, an environmental factor, alters the allocation of time and energy to influence vocal output, signal structure, and other reproductively related behaviors in free-living animals. Physiological Factor: T-pulses naturally occur after social interactions in a variety of species and can modulate call production and alter animal preferences for the physical location at which the T-pulse occurred (conditioned place preference; CPP). Manipulation of T-pulses has been conducted under controlled laboratory conditions; here, I ask how multiple T-pulses alter time allocation in complex field setting and influence future vocal behavior. H1: T-pulses reinforce behaviors in the area where the experience occurred in the form of conditioned placed preference (CPP) that in turn alter call production and the allocation of time and energy spent towards specific social interactions. To determine whether T-pulses induce CPPs and alter call production in the wild, I used a monogamous, territorial, and vocal rodent, the California mouse (Peromyscus californicus). California mice are well studied both in the laboratory and the wild, and in this species, males must balance mate attendance, offspring care, and territory defense with T being an important mediator of these social behaviors. I assessed the effects of three exogenously administered T-pulses or saline (control; C) on the following: 1) spatial preference 2) number of calls produced, and 3) spectral and temporal characteristics of calls (frequency, amplitude, and duration). I found that in the field, environmental location dictates the effects of T injections, suggesting that T-pulses are highly context dependent. At the nest, T-males spend more time at the nest and their noninjected mates spent less time at the nest. At the territory boundary, T-males and their non-injected mates spent less time at the boundary, but T-males traveled further outside their original territory than C-males. At the nest, T-mice produced more calls with a lower mean bandwidth whereas at the territory boundary T-males produced more short duration calls than C-males. In free-living and pair-bonded males, T-pulse induction of CPPs is based on the physical environment and the interactions that occur in that space. Together, these results suggest there is behavioral plasticity in inducing CPPs and that it is context dependent. Lastly, I found that independent of treatment type, the acoustic properties within a pair were more similar than among pairs, providing evidence for vocal convergence in pair-bonded California mice. Environmental Factor: Anthropogenic noise is a global pollutant that alters the natural soundscape which animals rely on for communication, foraging, navigation, exploring, and predator avoidance. Anthropogenic noise is pervasive in the audible range during the day, but it also extends into the ultrasonic range and into the night. Here, I ask how broadband (audible and ultrasonic) anthropogenic noise influences behaviors of free-living and nocturnal mammals. H2: Broadband anthropogenic noise alters the allocation of time and energy to influence activity, foraging, and vocal communication. To test my hypothesis, I broadcasted anthropogenic or familiar noise to examine 1) activity, 2) foraging and 3) call production of the deer mouse (Peromyscus maniculatus) and woodland jumping mouse (Napaeozapus insignis). I found that deer mice and woodland jumping mice spent less time at sites with anthropogenic noise compared to familiar noise. I also found that deer mice were less likely to approach food than woodland jumping mice during broadcasts of anthropogenic noise, however, both species spent less time foraging and vocalizing in the presence of anthropogenic noise. My results show species-specific responses to noise in nocturnal rodents that vocalize in the ultrasonic range. Overall, my data are consistent with previous research from other taxonomic groups, which demonstrate that anthropogenic reduces activity, foraging and vocalization production of animals

Differences in Ultrasonic Vocalizations between Wild and Laboratory California Mice (Peromyscus californicus)

BACKGROUND: Ultrasonic vocalizations (USVs) emitted by muroid rodents, including laboratory mice and rats, are used as phenotypic markers in behavioral assays and biomedical research. Interpretation of these USVs depends on understanding the significance of USV production by rodents in the wild. However, there has never been a study of muroid rodent ultrasound function in the wild and comparisons of USVs produced by wild and laboratory rodents are lacking to date. Here, we report the first comparison of wild and captive rodent USVs recorded from the same species, Peromyscus californicus. METHODOLOGY AND PRINCIPAL FINDINGS: We used standard ultrasound recording techniques to measure USVs from California mice in the laboratory (Peromyscus Genetic Stock Center, SC, USA) and the wild (Hastings Natural History Reserve, CA, USA). To determine which California mouse in the wild was vocalizing, we used a remote sensing method that used a 12-microphone acoustic localization array coupled with automated radio telemetry of all resident Peromyscus californicus in the area of the acoustic localization array. California mice in the laboratory and the wild produced the same types of USV motifs. However, wild California mice produced USVs that were 2-8 kHz higher in median frequency and significantly more variable in frequency than laboratory California mice. SIGNIFICANCE: The similarity in overall form of USVs from wild and laboratory California mice demonstrates that production of USVs by captive Peromyscus is not an artifact of captivity. Our study validates the widespread use of USVs in laboratory rodents as behavioral indicators but highlights that particular characteristics of laboratory USVs may not reflect natural conditions

Enriched laboratory housing increases sensitivity to social stress in female California mice (Peromyscus californicus)

Domesticated mice and rats have shown to be powerful model systems for biomedical research, but there are cases in which the biology of species is a poor match for the hypotheses under study. The California mouse (Peromyscus californicus) has unique traits that make it an ideal model for studying biological mechanisms underlying human-relevant behaviors such as intra-female aggression, biparental care, and monogamy. Indeed, peer-reviewed scientific publications using California mouse as a model for behavioral research have more than doubled in the past decade. Critically, behavioral outcomes in captive animals can be profoundly affected by housing conditions, but there is very limited knowledge regarding species-specific housing needs in California mice. Currently, California mouse investigators have to rely on guidelines aimed for more common laboratory species that show vastly different physiology, behavior, and/or ecological niche. This not only could be suboptimal for animals' welfare, but also result in lack of standardization that could potentially compromise experimental reproducibility and replicability across laboratories. With the aim of assessing how different housing systems can affect California mouse behavior both in the home cage as well as the open field and social interaction tests before and after social defeat stress, here we tested three different caging systems: 1. Standard mouse cage, 2. Large cage, and 3. Large cage + environmental enrichment (EE), which focused on increasing vertical complexity based on observations that California mice are semiarboreal in the wild. We found that the effects of housing were largely sex specific: compared to standard cages, in females large + EE reduced home cage stereotypic-like backflipping and rearing behaviors, while large cage increased social interactions. In males, the large+EE cage reduced rearing and digging but did not significantly affect backflipping behavior. Interestingly, while there were no significant differences in the open field and social interaction pre-stress behaviors, large and large+EE housing increased the sensitivity of these tests to detect stress induced phenotypes in females. Together, these results suggest that increasing social and environmental complexity affects home cage behaviors in male and female California mice without interfering with, but rather increasing the magnitude of, the effects of defeat stress on the open field and social interaction tests