Male house mice (Mus musculus) emit ultrasonic vocalizations (USVs) during courtship, which attract females, and we aimed to test whether females use these vocalizations for species or subspecies ...recognition of potential mates. We recorded courtship USVs of males from different Mus species, Mus musculus subspecies, and populations (F1 offspring of wild-caught Mus musculus musculus, Mus musculus domesticus (and F1 hybrid crosses), and Mus spicilegus), and we conducted playback experiments to measure female preferences for male USVs. Male vocalizations contained at least seven distinct syllable types, whose frequency of occurrence varied among species, subspecies, and populations. Detailed analyses of multiple common syllable types indicated that Mus musculus and Mus spicilegus could be discriminated based on spectral and temporal characteristics of their vocalizations, and populations of Mus musculus were also distinctive regardless of the classification model used. Females were able to discriminate USVs from different species, and showed assortative preferences for conspecific males. We found no evidence that females discriminate USVs of males from a different subspecies or separate populations of the same species, even though our spectral analyses identified acoustic features that differ between species, subspecies, and populations of the same species. Our results provide the first comparison of USVs between Mus species or between Mus musculus subspecies, and the first evidence that male USVs potentially facilitate species recognition.
Across the entire distribution of a species, populations may have variable responses to environmental perturbations. Many bat species experience mortality in large portions of their range during ...hibernation and along migratory paths to and from wintering grounds, from White-nose syndrome (WNS) and wind energy development, respectively. In some areas, warm temperatures may allow bats to remain active through winter, thus decreasing their susceptibility to WNS and/or mortality associated with migration to wintering grounds. These areas could act as a refugia and be important for the persistence of local populations. To determine if warmer temperatures affect bat activity, we compared year-round activity of bat populations in the Coastal Plain and Piedmont of North Carolina, USA, two regions that differ in winter temperature. We established six recording stations, four along a 295-kilometer north-south transect in the Coastal Plain, and two in the Piedmont of North Carolina. We recorded bat activity over two years. We supplemented our recordings with mist-net data. Although bat activity was lower during winter at all sites, the odds of recording a bat during winter were higher at Coastal Plain sites when compared with Piedmont sites. Further, bats in the Piedmont had a lower level of winter activity compared to summer activity than bats in the Coastal Plain that had more similar levels of activity in the winter and summer. We found high bat species richness on the Coastal Plain in winter, with winter-active species including those known to hibernate throughout most of their range and others known to be long distance migrants. In particular, two species impacted by WNS, the northern long-eared bat (Myotis septentrionalis) and tricolored bat (Perimyotis subflavus), were present year round in the Coastal Plain. The tricolored bat was also present year-round in the Piedmont. In the Coastal Plain, the long distance migratory hoary bat (Lasiurus cinereus) was active in the winter but not present during the other seasons, and the long distance migratory silver-haired bat (Lasionycteris noctivagans) was active primarily in the winter, suggesting the Coastal Plain may be an overwintering ground for these two species. We suggest that the winter activity exhibited by populations of bats on the North Carolina Coastal Plain has important conservation implications and these populations should be carefully monitored and afforded protection.
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.
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.
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.
Forest edges often have increased species richness and abundance (edge effect) and affect spatial behaviors of species and dynamics of species interactions. Landscapes of intensively managed pine ...(Pinus spp.) stands are characterized by a mosaic of patches and linear forest edges. Managed pine forests are a primary landscape feature of the southeastern United States, but the effects of intensive management on bat communities are poorly understood. Insectivorous bats are important top predators in nocturnal forest food webs. We examined bat foraging behavior along forest edges and in 4 structurally distinct stand types (open-canopy pine, prethinned pine, thinned pine, and unmanaged forest) within a managed pine forest in the coastal plain of North Carolina, USA. During May–August, 2006 and 2007, we recorded echolocation calls using Pettersson D240X bat detectors linked to digital recorders at 156 sites. We also sampled nocturnal flying insects at each site using Malaise insect traps. We used negative binomial count regression models to describe bat foraging behavior relative to forest edges, stand types, and prey availability. Although some species showed affinities for certain stand types and prey items, bat activity patterns were most strongly related to forest edges. Edges were used extensively by 6 aerial-hunting bat species, but avoided by Myotis species. Forest edges function similarly to natural forest gaps, by providing foraging opportunities for aerial-hunting bat species. Therefore, the maintenance of forest edges in managed pine landscapes may enhance foraging habitat for aerial-hunting bat species.
Low winter temperatures are a major driver of hibernation and migration in temperate North American bats. Hibernation and migration in turn affect bat mortality via white-nose syndrome and collisions ...with wind turbines. To describe winter bat acoustic activity across a wide temperature gradient and to understand species-specific responses to low temperatures, we recorded nightly acoustic activity of bats at 15 sites across the state of North Carolina, United States, from December through February 2016 – 2018. Bat acoustic activity was recorded at all sites during both winters. Nightly probability of bat acoustic presence regressed positively on ambient temperature. Nightly probability of presence in Lasionycteris noctivagans (silver-haired bat) and Eptesicus fuscus (big brown bat) regressed negatively on wind speed. The mean probability of presence within the same winter condition was highest for L. noctivagans, followed by E. fuscus, Perimyotis subflavus (tricolored bat), and Lasiurus cinereus (hoary bat). Differences in species' mean body weight and roosting preference explained part of the variation of the species-specific probability of presence. Our results can be used to predict bat acoustic presence for these species across the southeastern United States in winter, and better understand the potential threats to bats such as white-nose syndrome and wind turbine interactions.
The luxury effect describes the positive relationship between affluence and organism diversity or activity in urban ecosystems. Driven by human activities, the luxury effect can potentially be found ...at a broader scale across different landscapes. Previously, the luxury effect relationship has been established within a city for two bat species, the red bat (Lasiurus borealis) and the evening bat (Nycticeius humeralis). We examined landscape-scale patterns of bat activity distribution--using empirical data for seven bat species for the luxury effect. We also identified bat-land cover associations for each species. Across North Carolina, USA, we used the mobile transect survey protocol of the North American Monitoring Program to record bat activity at 43 sites from 2015 to 2018. We collected land cover and income data at our transect locations to construct generalized linear mixed models to identify bat-land cover and bat-income relationships. We found that across landscapes, activity of the red bat and the evening bat was positively correlated to income independent of land cover, consistent with previous single-city results. We found a negative relationship between hoary bat (Lasiurus cinereus) activity and income. All seven species had specific land cover associations. Additionally, we found a positive interaction term between income and evergreen forest for the red bat and a positive interaction term between income and woody wetland for hoary bat. Our results demonstrated that the luxury effect is an ecological pattern that can be found at a broad spatial scale across different landscapes. We highlight the need for multi-scale ecology studies to identify the mechanism(s) underlying the luxury effect and that the luxury effect could cause inequity in how people receive the ecosystem services provided by bats.
The steroid hormone testosterone (T) is a well-known mediator of male sexual behavior in vertebrates. However, less is known about T's rapid effects on sexual behavior, particularly those involving ...ultrasonic vocalizations (USVs), a mode of communication that can influence mate acquisition in rodents. Using the monogamous California mouse, Peromyscus californicus, we tested whether T rapidly alters male USV production by giving T or saline injections to non-paired (sexually naïve) males and paired (paternally experienced and pair-bonded) males immediately prior to a brief exposure to an unrelated, novel female. Among non-paired males, no differences in the total number of USVs were observed; however, T increased the proportion of simple sweeps produced. Among paired males, T decreased the number of USVs produced, and this change was driven by a reduction in simple sweeps. These results suggest a differential rapid effect of T pulses between non-paired and paired males upon exposure to a novel female. Additionally, we observed a positive correlation in the production of USVs made between males and novel females, and this relationship was altered by T. Given the importance of USVs in sexual communication, our study supports an essential concept of monogamy in that mate fidelity is reinforced by decreased responsiveness to prospective mates outside of the pair bond. The central mechanism in pair bonded males that decreases their responsiveness to novel females appears to be one that T can trigger. This is among the first studies to demonstrate that T can inhibit sexually related behaviors and do so rapidly.
Modulation of baseline testosterone (T) via long‐lasting T implants alters territorial, sexual, and social behavior of animals in the field. Transient T increases occur in numerous species after ...social interactions, but these transient increases in T have not been manipulated in the field. In the laboratory, these T increases can influence future behavior for days, causing changes in social behavior and inducing preferences for specific locations. We manipulated transient increases in T in the field at the nests of the monogamous and territorial California mouse (Peromyscus californicus) to examine long‐term (>24 hr) changes in ultrasonic vocalizations (USVs). Males of bonded male–female dyads (=pair) were administered a T injection (vs. saline) three times over seven days and USVs of the male–female dyad were measured for three days after the last injection. At T nests, the male–female dyad produced significantly more 1SV (one call SV: an SV is a sustained vocalization that is long in duration and low in modulation) and 4SV (four call SV) type USVs than controls, but no significant changes in aggressive barks. Overall, male–female dyad mice at T nests produced a greater diversity in call types such that 1SV, 4SV, 5SV, and a complex sweep were produced at T nests but not control nests. There were significantly more USVs produced at T nests on night 2 after the final injection. There were no differences in spectral characteristics of SV calls or aggressive barks between T and control nests. The function of the changes that occurred is unknown, but is consistent with increased long‐term changes in behavioral interactions with nest mates and may reflect T‐induced conditioned place preferences to the nest site. Significantly, transient increases in T influence future acoustic communication under field conditions with competing biotic and abiotic stimuli.
Understanding the ephemerality of trees used as roosts by wildlife, and the number of roost trees needed to sustain their populations, is important for forest management and wildlife conservation. ...Several studies indicate that roosts are limiting to bats, but few studies have monitored longevity of roost trees used by bats over several years. From 2004–2007 in Cypress Hills Interprovincial Park, Saskatchewan, Canada, several big brown bats (Eptesicus fuscus) from a maternity group roosted in cavities in trembling aspen (Populus tremuloides) trees approximately 7 km southeast away from their original known roosting area (RA1). Using a long-term data set of the roost trees used by bats in this area from 2000–2007, we evaluated whether the movement of bats to the new roosting area (RA4) corresponded with annual and cumulative losses of roost trees. We also determined whether longevity of the roosts from the time we discovered bats first using them differed between the 2 roosting areas based on Kaplan-Meier estimates. Bats began using RA4 in addition to RA1 in 2004, when the cumulative loss of roost trees in RA1 over 3 consecutive years reached 18%. Most bats exclusively roosted in RA4 in 2007, when the cumulative loss of roost trees over 6 consecutive years had reached 46% in RA1. Annual survival for roost trees, from when we first discovered bats using them, was generally lower in RA1 than in RA4. Our results suggest that the movement of bats to the new roosting area corresponded with high losses of roost trees in RA1. This provides additional evidence that to maintain high densities of suitable roost trees for bats in northern temperature forests over several decades, management plans need to recruit live and dead trees in multiple age classes and stages of decay that will be suitable for the formation of new cavities.
Time of peak bat activity during the night differs among bat species due to temperature, prey availability, habitat availability, and/or interactions between species. Habitat availability is altered ...in urban areas, which may affect insect prey availability and interspecies interactions. Our objectives were to use mobile acoustic monitoring to determine when bat species were active in a single night in urban and nonurban sites and if nightly bat activity patterns differed in urban versus nonurban sites. Bat echolocation call sequences were recorded using Anabat acoustic detectors while driving transects through the night at five sites (three “urban” and two “nonurban”) located in the Piedmont region of north-central North Carolina from May through August 2016. Transects were driven three times per night starting 45 min, 180 min, and 300 min after sunset. Recorded echolocation call sequences were analyzed manually using AnalookW and automatically using Bat Call Identification and Echoclass software. Total bat activity was not different between urban and nonurban sites. However, total bat activity was lower later in the night in urban sites, but stayed the same in nonurban sites. Species specifically, there were more
Eptesicus fuscus
,
Lasionycteris noctivagans
, and
Tadarida brasiliensis
call sequences and fewer
Lasiurus borealis
,
Nycticeius humeralis
, and
Perimyotis subflavus
call sequences in urban sites than nonurban sites. There were also fewer
E. fuscus
,
L. noctivagans
, and
N. humeralis
call sequences later in the night in both urban and nonurban sites. Only
Lasiurus borealis
activity in urban sites later in the night reduced and
L. borealis
activity in nonurban sites remained at the same. These results suggest that bats in urban areas partition time differently, which is important to consider for urban conservation efforts and planning.
PDF
