Sexual dimorphism and gonadal control of ultrasonic vocalizations in adult pine voles, Microtus pinetorum

We investigated the vocalizations produced by adult pine voles during various social interactions by presenting an experimental animal with either an anesthetized or awake (unanesthetized) conspecific. Ultrasonic vocalizations (USVs) occurred frequently during tests in which an awake male was present, but were rarely detected in tests involving only awake females, or when a female was presented with an anesthetized conspecific. Higher rates of USVs were produced when males were tested with a familiar female than when tested with an unfamiliar male or female. Equivalent rates were produced when males were presented with either anesthetized or awake animals, but female-soiled bedding failed to elicit USVs from males. Sonic vocalizations (SVs) were produced by both sexes and were associated with aggressive behavior, but occurred only in tests between awake, unfamiliar animals. Castration greatly reduced and testosterone therapy restored USVs emitted by males in response to anesthetized conspecifics. Our results suggest that (i) USVs are emitted predominantly by males; (ii) familiarity enhances USV response; (iii) SVs are produced during aggressive interactions; and (iv) androgens regulate the production of USVs by males. Possible roles for pine vole vocalizations are discussed.     

Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates

Tarsiers are small nocturnal primates with a long history of fuelling debate on the origin and evolution of anthropoid primates. Recently, the discovery of M and L opsin genes in two sister species, Tarsius bancanus (Bornean tarsier) and Tarsius syrichta (Philippine tarsier), respectively, was interpreted as evidence of an ancestral long-to-middle (L/M) opsin polymorphism, which, in turn, suggested a diurnal or cathemeral (arrhythmic) activity pattern. This view is compatible with the hypothesis that stem tarsiers were diurnal; however, a reversion to nocturnality during the Middle Eocene, as evidenced by hyper-enlarged orbits, predates the divergence of T. bancanus and T. syrichta in the Late Miocene. Taken together, these findings suggest that some nocturnal tarsiers possessed high-acuity trichromatic vision, a concept that challenges prevailing views on the adaptive origins of the anthropoid visual system. It is, therefore, important to explore the plausibility and antiquity of trichromatic vision in the genus Tarsius. Here, we show that Sulawesi tarsiers (Tarsius tarsier), a phylogenetic out-group of Philippine and Bornean tarsiers, have an L opsin gene that is more similar to the L opsin gene of T. syrichta than to the M opsin gene of T. bancanus in non-synonymous nucleotide sequence. This result suggests that an L/M opsin polymorphism is the ancestral character state of crown tarsiers and raises the possibility that many hallmarks of the anthropoid visual system evolved under dim (mesopic) light conditions. This interpretation challenges the persistent nocturnal–diurnal dichotomy that has long informed debate on the origin of anthropoid primates.     

Strengths and Weaknesses of a Population Viability Analysis for Philippine Tarsiers (<Emphasis Type="Italic">Tarsius syrichta</Emphasis>)

Population viability analysis (PVA) has been increasingly used to guide conservation planning for many primate species. I present an assessment of a PVA for Philippine tarsiers (Tarsius syrichta) in Corella, Bohol. The objectives were to determine 1) area requirements and 2) spatial configurations of habitat patches necessary for viable populations in Corella. I used available life history parameters and ecological data for the Philippine tarsier derived from a radiotelemetry study on 4 male and 6 female Tarsius syrichta in Corella from early March to October 1999. I used analysis of the likelihood of extinction (ALEX), a Monte Carlo simulation model that uses pseudorandom numbers to simulate a scenario involving different stochastic processes. Sensitivity analysis showed that the model output, i.e. extinction risk, was influenced by the values used for newborn, juvenile, and adult mortality but the effect of variation on adult mortality was more pronounced; a slight increase in adult mortality renders the population very unstable. Simulation of movements between habitat patches showed that addition of diffusion corridors and variation in diffusion parameters did not significantly alter the probability of extinction of the species. Models are only as useful as the data that are input, and a major weakness of this model is the lack of detailed life history and mortality data for Philippine tarsiers. Future studies should concentrate on obtaining more life history data and ecological data from additional localities. I discuss key priorities for future research that include use of alternative PVA software, a simpler modeling approach, and extensive genetic studies of different Philippine tarsier island populations.     

Polymorphic microsatellite markers for Philippine tarsiers (<Emphasis Type="Italic">Tarsius syrichta</Emphasis>)

This study reports the isolation and characterization of eight microsatellite markers for the study of Philippine tarsiers (Tarsius syrichta), small primates endemic to this Southeast Asian archipelago. The markers were used to screen 14 Tarsius syrichta for allelic diversity. This suite of highly polymorphic microsatellites provides the first chance to genetically study parentage and dispersal patterns in Philippine tarsiers.     

Sex differences in ultrasonic vocalizations and coordinated movement in the California mouse (Peromyscus californicus)

Geyer [Am. Zool. 21 (1981) 117] hypothesized that infant rodents increased the number of ultrasonic vocalizations when they moved in and out of the nest in order to elicit extended care from parents. We tested these hypotheses by recording ultrasonic vocalizations (USVs) and coordinated movements (locomotion and grooming) in California mouse and by recording USVs from pups before and after their parents retrieved them. In Experiment 1, USVs and coordinated movements were recorded from 2 to 30 days of age, in female and male Peromyscus californicus pups. USVs at 37, 42, 47, and 52kHz were digitized and recorded by computer and an event recorder program which was simultaneously used to record coordinated movement. Vocalizations persisted to 30 days of age. Vocalizations increased for both males and females after they spent more than 180s in coordinated movement and females vocalized more than males. Females also displayed more coordinated movement and earlier development of coordinated movement than males. There was no effect of litter size on USVs. In Experiment 2, the number of USVs emitted by pups and the latency of dams and sires to contact their pups and retrieve them was measured. There was no significant correlation between the number of USVs emitted by pups and the latency for a parent to contact or retrieve a pup. Results from Experiment 1 provided some support for Geyer's (1981) hypothesis and results from Experiment 2 did not support the hypothesis that the main function of USVs in California mouse pups was to elicit parental care.     

Silent or Vocalizing Rats Copulate in a Similar Manner

Both male and female rats produce 50 kHz ultrasonic vocalizations (USVs) in the presence of a sexual partner and during copulation. Previous studies showed that USVs have no incentive value for rats. In this study, we evaluated the role of USVs in behavior during copulation. Three groups of rats were used: sham males paired with sham females, devocalized females paired with sham males, and sham females paired with devocalized males. During the copulation test, the USVs emitted by the sham rat were recorded and the sexual behavior of both the male and the female were observed. The results revealed that devocalized and sham females showed similar patterns of sexual behavior and no difference was found in the copulatory behavior of devocalized and sham males. Also the behavior of the partner of a sham rat was comparable to the partner of a devocalized rat. In addition, almost no changes in USVs emission were found in the 5 seconds before and/or after a copulatory behavior. It can be concluded that USVs play no important role in rat copulatory behavior at least in sexually naïve rats.     

Biphonal calls in Atlantic spotted dolphins (Stenella frontalis): bitonal and burst-pulse whistles

Biphonation, the simultaneous production of two sounds by a single animal, is found in the vocalizations of a range of mammalian species. Its prevalence suggests it plays an important role in acoustic communication. Concurrent vocal and behavioural recordings were made of Atlantic spotted dolphins (Stenella frontalis) off Bimini, The Bahamas. The occurrence of two types of biphonal signals is reported: burst-pulse whistles with combined tonal and burst-pulse elements, and bitonal whistles. Biphonal whistles are rarely described in reports of dolphin acoustic repertoires, but were common in these dolphins: of all whistles analysed (n = 1211), 26.84% were burst-pulse whistles and 4.71% were bitonal whistles. A subset of whistles (n = 397) were attributed to dolphins of specific age classes, and used to compare prevalence of biphonation across age. Biphonation occurred in 61.54% of sexually mature and 48.32% of sexually immature dolphins’ whistles. Sexually immature dolphins emitted more burst-pulse whistles than older dolphins: 44.13% of sexually immature dolphins’ whistles were burst-pulse whistles, while 15.38% of adult whistles were burst-pulse whistles. Bitonal whistle production was more prevalent in sexually mature dolphins: 41.03% of adult whistles were bitonal, while only 4.19% of sexually immature dolphins’ whistles were bitonal. The prevalence of a biphonal component in specific repeated, stereotyped whistle contours suggests that these acoustic features could be important components of contact calls, or signature whistles. The biphonal components of spotted dolphin whistles may serve to convey additional information as to identity, age or other factors to conspecifics.     

Vocalizations of Belding's ground squirrels (Spermophilus beldingi)

Vocalizations of Belding's ground squirrels (Spermophilus beldingi) were recorded during the summer of 1982 near Tioga Pass in the central Sierra Nevada of California. Sonagrams were made and call parameters were measured. Discriminant function analyses revealed that multiple-note calls (‘trills’) differed acoustically depending on whether they occurred in response to a predator, or were given by males following copulations. The post-copulatory trills of males were individually distinctive. Among anti-predator trills there was no evidence of predator-specificity within the narrow range of predators tested: trills given to two species of (stuffed) weasels (Mustela), to dogs and to humans were statistically indistinguishable. Sonagrams of trills occurring in agonistic contexts suggest that a third general category of trills may exist, but agonistic trills were more variable than either anti-predator or post-copulatory trills. The ground squirrels also gave single-note calls in the three contexts described above, either repetitively (‘chirps’) or singly (‘whistles’). Neither chirps nor whistles encoded any obvious situation-specific information, except that whistles were typically associated with rapidly-moving predators, usually raptors. The post-copulatory chirps of males were individually distinctive. Vocalizations of Belding's ground squirrels may not vary among contexts as much as do the analogous calls of California ground squirrels (S. beecheyi).     

Ultrasonic Vocalizations of Male Mice Differ among Species and Females Show Assortative Preferences for Male Calls

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.     

Vocalizations and Behaviour of Pacific Humpback Dolphins Sousa chinensis

Very little is known about the acoustic repertoire of the Pacific humpback dolphin Sousa chinensis . This study, off eastern Australia, used concurrent observations of surface behaviour and acoustic recordings to gain an insight into the behavioural significance of humpback dolphin vocalizations. Humpback dolphins exhibit five different vocalization categories: broad band clicks; barks; quacks; grunts; and whistles. Broad band clicks were high in frequency (8 kHz to > 22 kHz), were directly related to foraging behaviour and may play a role in social behaviour. Barks and quacks were burst pulse sounds (frequency: 0.6 kHz to > 22 kHz, duration: 0.1–8 s) and were associated with both foraging and social behaviour. The grunt vocalization is a low frequency narrow band sound (frequency 0.5–2.6 kHz, duration 0.06–2 s) and was only heard during socializing. There were 17 different types of whistles, ranging widely in frequency (0.9–22 kHz) and vocal structure (n=329). The predominant whistle types used by the groups were type 1 (46%) and type 2 (17%). Most whistles were heard during both socializing and foraging. The number of whistles recorded in a group increased significantly as the number of mother–calf pairs increased, suggesting that whistles may be used as contact calls. Few vocalizations were heard during either travelling or milling behaviours. Broad band clicks, barks and whistle type 1 were the only vocalizations recorded during either travelling or milling.     

Male mice ultrasonic vocalizations enhance female sexual approach and hypothalamic kisspeptin neuron activity

Vocal communication in animals is important for ensuring reproductive success. Male mice emit song-like “ultrasonic vocalizations (USVs)” when they encounter female mice, and females show approach to the USVs. However, it is unclear whether USVs of male mice trigger female behavioral and endocrine responses in reproduction. In this study, we first investigated the relationship between the number of deliveries in breeding pairs for 4 months and USVs syllables emitted from those paired males during 3 min of sexual encounter with unfamiliar female mice. There was a positive correlation between these two indices, which suggests that breeding pairs in which males could emit USVs more frequently had more offspring. Further, we examined the effect of USVs of male mice on female sexual behavior. Female mice showed more approach behavior towards vocalizing males than devocalized males. Finally, to determine whether USVs of male mice could activate the neural system governing reproductive function in female mice, the activation of kisspeptin neurons, key neurons to drive gonadotropin-releasing hormone neurons in the hypothalamus, was examined using dual-label immunocytochemistry with cAMP response element-binding protein phosphorylation (pCREB). In the arcuate nucleus (Arc), the number of kisspeptin neurons expressing pCREB significantly increased after exposure to USVs of male as compared with noise exposure group. In conclusion, our results suggest that USVs of male mice promote fertility in female mice by activating both their approaching behavior and central kisspeptin neurons.     

Identification and Characteristics of Signature Whistles in Wild Bottlenose Dolphins (Tursiops truncatus) from Namibia

A signature whistle type is a learned, individually distinctive whistle type in a dolphin''s acoustic repertoire that broadcasts the identity of the whistle owner. The acquisition and use of signature whistles indicates complex cognitive functioning that requires wider investigation in wild dolphin populations. Here we identify signature whistle types from a population of approximately 100 wild common bottlenose dolphins (Tursiops truncatus) inhabiting Walvis Bay, and describe signature whistle occurrence, acoustic parameters and temporal production. A catalogue of 43 repeatedly emitted whistle types (REWTs) was generated by analysing 79 hrs of acoustic recordings. From this, 28 signature whistle types were identified using a method based on the temporal patterns in whistle sequences. A visual classification task conducted by 5 naïve judges showed high levels of agreement in classification of whistles (Fleiss-Kappa statistic, κ = 0.848, Z = 55.3, P<0.001) and supported our categorisation. Signature whistle structure remained stable over time and location, with most types (82%) recorded in 2 or more years, and 4 identified at Walvis Bay and a second field site approximately 450 km away. Whistle acoustic parameters were consistent with those of signature whistles documented in Sarasota Bay (Florida, USA). We provide evidence of possible two-voice signature whistle production by a common bottlenose dolphin. Although signature whistle types have potential use as a marker for studying individual habitat use, we only identified approximately 28% of those from the Walvis Bay population, despite considerable recording effort. We found that signature whistle type diversity was higher in larger dolphin groups and groups with calves present. This is the first study describing signature whistles in a wild free-ranging T. truncatus population inhabiting African waters and it provides a baseline on which more in depth behavioural studies can be based.     

Successful breeding attempt of a pair of Philippine tarsier (Tarsius syrichta) in a conservation center in Bilar,Bohol, Philippines and recommendations for tarsier husbandry

The Philippine tarsier (Tarsius syrichta) belongs to the least known nocturnal primates. Tarsiers and remaining biodiversity of the Philippines are under tremendous threats from increasing human expansion, with habitat loss and illegal pet trade being the main reasons for tarsier population decline. In addition, even though the attempts were made by western and local facilities, tarsiers have not survived well in captivity. In this paper, I present an example of successful breeding of the Philippine tarsier in captive conditions but in natural climate. As the most important elements of success, I see a large amount of space provided to tarsiers, the climate similar to their natural habitat and the food resembling their natural diet. Our pair of tarsiers were joined during the mating period and held separately outside the mating period, which corresponds with their behavior in the wild and may have played a crucial role in breeding success. Eliminating stress to animals is also important. The study can provide valuable guidelines for other facilities keeping tarsiers in the Philippines and help to improve tarsiers’ welfare and in the future help to establish a viable captive population of the Philippine tarsier that will serve as a backup population and also will decrease demand on tarsiers captured from the wild.     

Introducing an innovative semi‐captive environment for the Philippine tarsier (Tarsius syrichta)

In response to demands for research, captive breeding, and tourism, a semi‐captive environment was created for the Philippine tarsiers (Tarsius syrichta) in Corella, Bohol, Philippines. The 7600‐m² enclosure was continuous with the surrounding habitat, and utilized a unique predator control fence design and a lighting system to attract nocturnal insects. During 2 years of observation, the locations of over 500 tarsier sleeping sites were recorded. Tarsiers were found to prefer dense, low‐level vegetation in secondary forests, with perching sites averaging 2 m above the ground. Up to 10 tarsiers were observed within the enclosure at one time, which is a high density compared to densities based on home‐range estimates for wild tarsiers in the vicinity of the study site. In addition, the tarsiers were observed to be more social than previously reported. Zoo Biol 24:101–109, 2005. © 2005 Wiley‐Liss, Inc.     

ACOUSTIC IDENTIFICATION OF NINE DELPHINID SPECIES IN THE EASTERN TROPICAL PACIFIC OCEAN

Acoustic methods may improve the ability to identify cetacean species during shipboard surveys. Whistles were recorded from nine odontocete species in the eastern tropical Pacific to determine how reliably these vocalizations can be classified to species based on simple spectrographic measurements. Twelve variables were measured from each whistle ( n = 908). Parametric multivariate discriminant function analysis (DFA) correctly classified 41.1% of whistles to species. Non-parametric classification and regression tree (CART) analysis resulted in 51.4% correct classification. Striped dolphin whistles were most difficult to classify. Whistles of bottlenose dolphins, false killer whales, and pilot whales were most distinctive. Correct classification scores may be improved by adding prior probabilities that reflect species distribution to classification models, by measuring alternative whistle variables, using alternative classification techniques, and by localizing vocalizing dolphins when collecting data for classification models.     

Positional behavior and social organization of the philippine tarsier (Tarsius syrichta)

This study provides preliminary data on the positional behavior and habitat use of the Philippine tarsier,Tarsius syrichta, which was studied in its natural habitat on the island of Leyte. The locomotor behavior ofT. syrichta is quite comparable to the other species of tarsiers but frequency of use of different postures and support types does seem to distinguish this species from the others.Tarsius bancanus appears to be the most specialized, using vertical clinging postures the most frequently and sitting the least;Tarsius dianae uses vertical clinging the least frequently and sitting the most, andT. syrichta is intermediate. The Philippine tarsier has a small home range similar to that ofT. spectrum. On the other hand, this species likely does not have the small family groups typical of Sulawesi tarsiers but instead uses a noyau system likeT. bancanus. This data supports some apsects ofNiemitz’s (1977) model of anatomical and behavioral specialization among tarsier species.     

Contextual Information and Differential Responses to Alarm Whistles in California Ground Squirrels

In the field, we videotaped the reactions of squirrels to playbacks of 1, 3 and 5 whistle vocalizations at two sound intensities differing by 10 dB. The squirrels reacted by running to boulders or burrows and freezing. As time progressed following playbacks, freezing declined and squirrels resumed feeding, locomotion and grooming. With increasing numbers of whistles, squirrels were more likely to run and less likely to mount a boulder. With more high intensity whistles, squirrels froze quadrupedally more and bipedally less. Freezing postures did not vary as a function of the number of low-intensity whistles. Walking was suppressed least by 1 and 3 whistles at low intensity, and inhibited most by all high-intensity whistles as well as by the low-intensity 5-whistle playback. When the squirrel was on a boulder, quadrupedal freezing was more common than bipedal freezing. Off the boulder, the two freezing postures were equally likely. We propose that squirrels assessed risk from information encoded in the whistle(s) and contextual to it, and varied their reactions as a function of apparent risk.     

Isolation and characterization of 12 microsatellite loci for population studies of Sulawesi tarsiers (Tarsius spp.)

This study reports the development and characterization of the first 12 microsatellite markers for tarsiers. Nine loci were isolated from Dian's tarsier, Tarsius dianae and three from the Philippine tarsier, Tarsius syrichta. The 12 markers were used to screen 40 individuals of Dian's tarsier and 40 individuals of the Lariang tarsier, Tarsius lariang for allelic diversity. This suite of highly polymorphic microsatellites provides the first chance to genetically study parentage patterns in tarsiers.     

Playback experiment to test maternal responses of Japanese macaques (Macaca fuscata) to their own infant's call when the infants were four to six months old

Calls emitted by infants when the infant loses sight of its parents are useful to estimate the infant's requirement for parental care. When an Old World monkey infant loses sight of its mother it emits whistles. Therefore, it would be interesting to determine whether mothers could distinguish their own infant's whistles from the whistles of other infants. The response of each of seven Japanese macaque (Macaca fuscata) mothers to her own infant's whistle was compared with their responses to another infant's whistle. Matched control playback experiments were performed when the infants were four to six months old. The results showed that each mother could distinguish her own infant's whistle from that of another infant when the infants were four to six months old. Although a stricter experimental plan is required to further examine the issue, we found that the dominance rank of the infant's mother was another important factor in the female response to the infant's call. The finding suggests that females can associate a call emitted by an infant with its mother's rank, even before the infant begins to wander far from its mother.     

Ultrasonic vocalizations induced by sex and amphetamine in M2, M4, M5 muscarinic and D2 dopamine receptor knockout mice

Adult mice communicate by emitting ultrasonic vocalizations (USVs) during the appetitive phases of sexual behavior. However, little is known about the genes important in controlling call production. Here, we study the induction and regulation of USVs in muscarinic and dopaminergic receptor knockout (KO) mice as well as wild-type controls during sexual behavior. Female mouse urine, but not female rat or human urine, induced USVs in male mice, whereas male urine did not induce USVs in females. Direct contact of males with females is required for eliciting high level of USVs in males. USVs (25 to120 kHz) were emitted only by males, suggesting positive state; however human-audible squeaks were produced only by females, implying negative state during male-female pairing. USVs were divided into flat and frequency-modulated calls. Male USVs often changed from continuous to broken frequency-modulated calls after initiation of mounting. In M2 KO mice, USVs were lost in about 70-80% of the mice, correlating with a loss of sexual interaction. In M5 KO mice, mean USVs were reduced by almost 80% even though sexual interaction was vigorous. In D2 KOs, the duration of USVs was extended by 20%. In M4 KOs, no significant differences were observed. Amphetamine dose-dependently induced USVs in wild-type males (most at 0.5 mg/kg i.p.), but did not elicit USVs in M5 KO or female mice. These studies suggest that M2 and M5 muscarinic receptors are needed for male USV production during male-female interactions, likely via their roles in dopamine activation. These findings are important for the understanding of the neural substrates for positive affect.