The gradual vocal responses to human-provoked discomfort in farmed silver foxes

Vocal indicators of welfare have proven their use for many farmed and zoo animals and may be applied to farmed silver foxes as these animals display high vocal activity toward humans. Farmed silver foxes were selected mainly for fur, size, and litter sizes, but not for attitudes to people, so they are fearful of humans and have short-term welfare problems in their proximity. With a human approach test, we designed here the steady increase and decrease of fox–human distance and registered vocal responses of 25 farmed silver foxes. We analyzed the features of vocalizations produced by the foxes at different fox–human distances, assuming that changes in vocal responses reflect the degrees of human-related discomfort. For revealing the discomfort-related vocal traits in farmed silver foxes, we proposed and tested the algorithm of “joint calls,” equally applicable for analysis of all calls independently on their structure, either tonal or noisy. We discuss that the increase in proportion of time spent vocalizing and the shift of call energy toward higher frequencies may be integral vocal characteristics of short-term welfare problems in farmed silver foxes and probably in other captive mammals.     

Vocalization toward conspecifics in silver foxes (Vulpes vulpes) selected for tame or aggressive behavior toward humans

We examined the production of different vocalizations in three strains of silver fox (unselected, aggressive, and tame) attending three kinds of behavior (aggressive, affiliative, and neutral) in response to their same-strain conspecifics. This is a follow-up to previous experiments which demonstrated that in the presence of humans, tame foxes produced cackles and pants but never coughed or snorted, whilst aggressive foxes produced coughs and snorts but never cackled or panted. Thus, cackle/pant and cough/snort were indicative of the tame and aggressive fox strains respectively toward humans. Wild-type unselected foxes produced cough and snort toward humans similarly to aggressive foxes. Here, we found that vocal responses to conspecifics were similar in tame, aggressive and unselected fox strains. Both cackle/pant and cough/snort occurred in foxes of all strains. The difference in the use of cackle/pant and cough/snort among these strains toward humans and toward conspecifics suggest that silver foxes do not perceive humans as their conspecifics. We speculate that these vocalizations are produced in response to a triggering internal state, affiliative or aggressive, that is suppressed by default in these fox strains toward humans as a result of their strict selection for tame or aggressive behavior, whilst still remaining flexible toward conspecifics.     

Potential Sources of High Frequency and Biphonic Vocalization in the Dhole (Cuon alpinus)

Biphonation, i.e. two independent fundamental frequencies in a call spectrum, is a prominent feature of vocal activity in dog-like canids. Dog-like canids can produce a low (f0) and a high (g0) fundamental frequency simultaneously. In contrast, fox-like canids are only capable of producing the low fundamental frequency (f0). Using a comparative anatomical approach for revealing macroscopic structures potentially responsible for canid biphonation, we investigated the vocal anatomy for 4 (1 male, 3 female) captive dholes (Cuon alpinus) and for 2 (1 male, 1 female) wild red fox (Vulpes vulpes). In addition, we analyzed the acoustic structure of vocalizations in the same dholes that served postmortem as specimens for the anatomical investigation. All study dholes produced both high-frequency and biphonic calls. The anatomical reconstructions revealed that the vocal morphologies of the dhole are very similar to those of the red fox. These results suggest that the high-frequency and biphonic calls in dog-like canids can be produced without specific anatomical adaptations of the sound-producing structures. We discuss possible production modes for the high-frequency and biphonic calls involving laryngeal and nasal structures.     

Vasotocin maintains multiple call types in the gray treefrog, Hyla versicolor.

The neuropeptide arginine vasotocin (AVT) influences vocalizations in some anuran amphibians but it is unknown whether AVT alters all vocal behaviors of a species similarly. We first characterized the vocal repertoire of male gray treefrogs (Hyla versicolor). Three different call types were distinguished by unique sets of temporal and spectral features. Second, we examined the effects of AVT on each call type by injecting frogs with either AVT (100 microg; intraperitoneal) or saline and recording subsequent behavior. In the field, AVT maintained advertisement calling, whereas calling ceased in saline-injected animals. Advertisement call rate in AVT-injected males fell significantly and dominant frequency of the call was significantly higher. In the laboratory, AVT induced advertisement calling in males that were not initially vocalizing and dominant frequency was also significantly higher in these males. AVT maintained aggressive calling similarly but the characteristics of aggressive calls were not altered by AVT. There were no significant differences in release call behavior between AVT- and saline-injected groups; however, release call duration decreased significantly in AVT-injected animals, compared with preinjection values for the same animals. The effects of AVT on vocal behavior in this species are therefore not the same for each call type. AVT may act at more general motivational levels in the central nervous system and other neural or endocrine factors may control choice of call type and direct motor output.     

A marker set for construction of a genetic map of the silver fox (Vulpes vulpes)

The silver fox, a variant of the red fox (Vulpes vulpes), is a close relative of the dog (Canis familiaris). Cytogenetic differences and similarities between these species are well understood, but their genomic organizations have not been compared at higher resolution. Differences in their behavior also remain unexplained. Two silver fox strains demonstrating markedly different behavior have been generated at the Institute of Cytology and Genetics of the Russian Academy of Sciences. Foxes selected for tameness are friendly, like domestic dogs, while foxes selected for aggression resist human contact. To refine our understanding of the comparative genomic organization of dogs and foxes, and enable a study of the genetic basis of behavior in these fox strains, we need a meiotic linkage map of the fox. Towards this goal we generated a primary set of fox microsatellite markers. Four hundred canine microsatellites, evenly distributed throughout the canine genome, have been identified that amplify robustly from fox DNA. Polymorphism information content (PIC) values were calculated for a representative subset of these markers and population inbreeding coefficients were determined for tame and aggressive foxes. To begin to identify fox-specific single nucleotide polymorphisms (SNPs) in genes involved in the neurobiology of behavior, fox and dog orthologs of serotonin 5-HT1A and 5-HT1B receptor genes have been cloned. Sequence comparison of these genes from tame and aggressive foxes reveal several SNPs. The close relationship of the fox and dog enables canine genomic tools to be utilized in developing a fox meiotic map and mapping behavioral traits in the fox.     

Genotyping-By-Sequencing (GBS) Detects Genetic Structure and Confirms Behavioral QTL in Tame and Aggressive Foxes (Vulpes vulpes)

The silver fox (Vulpes vulpes) offers a novel model for studying the genetics of social behavior and animal domestication. Selection of foxes, separately, for tame and for aggressive behavior has yielded two strains with markedly different, genetically determined, behavioral phenotypes. Tame strain foxes are eager to establish human contact while foxes from the aggressive strain are aggressive and difficult to handle. These strains have been maintained as separate outbred lines for over 40 generations but their genetic structure has not been previously investigated. We applied a genotyping-by-sequencing (GBS) approach to provide insights into the genetic composition of these fox populations. Sequence analysis of EcoT22I genomic libraries of tame and aggressive foxes identified 48,294 high quality SNPs. Population structure analysis revealed genetic divergence between the two strains and more diversity in the aggressive strain than in the tame one. Significant differences in allele frequency between the strains were identified for 68 SNPs. Three of these SNPs were located on fox chromosome 14 within an interval of a previously identified behavioral QTL, further supporting the importance of this region for behavior. The GBS SNP data confirmed that significant genetic diversity has been preserved in both fox populations despite many years of selective breeding. Analysis of SNP allele frequencies in the two populations identified several regions of genetic divergence between the tame and aggressive foxes, some of which may represent targets of selection for behavior. The GBS protocol used in this study significantly expanded genomic resources for the fox, and can be adapted for SNP discovery and genotyping in other canid species.     

A Cervid Vocal Fold Model Suggests Greater Glottal Efficiency in Calling at High Frequencies

Male Rocky Mountain elk (Cervus elaphus nelsoni) produce loud and high fundamental frequency bugles during the mating season, in contrast to the male European Red Deer (Cervus elaphus scoticus) who produces loud and low fundamental frequency roaring calls. A critical step in understanding vocal communication is to relate sound complexity to anatomy and physiology in a causal manner. Experimentation at the sound source, often difficult in vivo in mammals, is simulated here by a finite element model of the larynx and a wave propagation model of the vocal tract, both based on the morphology and biomechanics of the elk. The model can produce a wide range of fundamental frequencies. Low fundamental frequencies require low vocal fold strain, but large lung pressure and large glottal flow if sound intensity level is to exceed 70 dB at 10 m distance. A high-frequency bugle requires both large muscular effort (to strain the vocal ligament) and high lung pressure (to overcome phonation threshold pressure), but at least 10 dB more intensity level can be achieved. Glottal efficiency, the ration of radiated sound power to aerodynamic power at the glottis, is higher in elk, suggesting an advantage of high-pitched signaling. This advantage is based on two aspects; first, the lower airflow required for aerodynamic power and, second, an acoustic radiation advantage at higher frequencies. Both signal types are used by the respective males during the mating season and probably serve as honest signals. The two signal types relate differently to physical qualities of the sender. The low-frequency sound (Red Deer call) relates to overall body size via a strong relationship between acoustic parameters and the size of vocal organs and body size. The high-frequency bugle may signal muscular strength and endurance, via a ‘vocalizing at the edge’ mechanism, for which efficiency is critical.     

Effects of Male Vocal Learning on Female Behavior in the Budgerigar, Melopsittacus undulatus

Parrots are unusual among birds and animals in general in the extent of their ability to learn new vocalizations throughout life and irrespective of season. The budgerigar (Melopsittacus undulatus), a small parrot that is well suited for laboratory studies, has been the subject of numerous studies investigating the neurobiology of vocal learning. To date, few studies have focused on the function of vocal imitation by parrots. Previous work from our research group has shown that vocal imitation in budgerigars is sex‐biased, as males paired with females learn vocalizations from their new mates, but not vice versa. This bias led us to hypothesize that vocal learning has a reproductive function. To test this hypothesis, we conducted two experiments. In the first experiment, we tutored males so that they could produce a call similar to one shared by a group of experimental females. The experimental females were then presented with one of the tutored males and another, equally unfamiliar, male that had not been tutored. We found that the females spent a greater proportion of time in proximity of, and made more affiliative displays toward, the tutored males. In the second experiment, seven males received small bilateral brain lesions that disrupt vocal learning. These males and an equal number of control males were then released into an aviary containing females and reproductive resources. We found that lesioned and control males were equally successful in obtaining social mates, but females mated to lesioned males were more likely to engage in extra‐pair activities. These experiments indicate that a male's ability to imitate a female's call can influence the sexual behavior of the female even though lack of imitation ability does not appear to influence social pairing. We hypothesize that mate choice in budgerigars has multiple stages. Upon meeting a strange male, a female quickly assesses its ability for social acquisition of calls by the presence or absence of a call type similar to its own in its repertoire. As courtship proceeds into pair formation, the female assesses the ability of male to learn more directly by the extent of the male's perfection of imitation.     

Kind granddaughters of angry grandmothers: The effect of domestication on vocalization in cross-bred silver foxes

The genetic basis of the effects of domestication has previously been examined in relation to morphological, physiological and behavioural traits, but not for vocalizations. According to Belyaev [Belyaev, D.K., 1979. Destabilizing selection as a factor in domestication. J. Hered. 70, 301-308], directional selection for tame behaviour toward humans resulted in domestication. This hypothesis has been confirmed experimentally on the farm-bred silver fox Vulpes vulpes population that has undergone 45 years of artificial selection for tameness and 35 years of selection for aggressiveness. These foxes, with their precisely known attitudes toward people, provide a means of examining vocal indicators of tameness and aggressiveness to establish the genetic basis for vocal production in canids. We examined vocalizations toward people in foxes selected for tameness and aggressiveness compared to those of three kinds of crosses: Hybrids (Tame × Aggressive), A-Backcrosses (Aggressive × Hybrid) and T-Backcrosses (Tame × Hybrid). We report the effects of selection for tameness on usage and structure of different vocalizations and suggest that vocal indicators for tameness and aggressiveness toward people are discrete phenotypic traits in silver foxes.     

THE EFFECT OF VESSEL NOISE ON THE VOCAL BEHAVIOR OF BELUGAS IN THE ST. LAWRENCE RIVER ESTUARY,CANADA

During June-July 1991, we monitored the vocal behavior of belugas before, during, and after exposure to noise from a small motorboat and a ferry to determine if there were any consistent patterns in their vocal behavior when exposed to these two familiar, but different sources of potential disturbance. Vocal responses were observed in all trials and were more persistent when whales were exposed to the ferry than to the small boat. These included (1) a progressive reduction in calling rate from 3.4–10.5 calls/whale/min to 0.0 or <1.0 calls/whale/min while vessels were approaching; (2) brief increases in the emission of falling tonal calls and the theree pulsed-tone call types; (3) at distances <1 km, an increase in the repetition of specific calls, and (4) a shift in frequency bands used by vocalizing animals from a mean frequency of 3.6 kHz prior to exposure to noise to frequencies of 5.2-8.8 kHz when vessels were close to the whales.     

Efficiency and Significance of Multiple Vocal Signals in Sibling Competition

Animals can compete for resources by displaying various acoustic signals that may differentially affect the outcome of competition. We propose the hypothesis that the most efficient signal to deter opponents should be the one that most honestly reveals motivation to compete. We tested this hypothesis in the barn owl (Tyto alba) in which nestlings produce more calls of longer duration than siblings to compete for priority access to the indivisible prey item their parents will deliver next. Because nestlings increase call rate to a larger extent than call duration when they become hungrier, call rate would signal more accurately hunger level. This leads us to propose three predictions. First, a high number of calls should be more efficient in deterring siblings to compete than long calls. Second, the rate at which an individual calls should be more sensitive to variation in the intensity of the sibling vocal competition than the duration of its calls. Third, call rate should influence competitors’ vocalization for a longer period of time than call duration. To test these three predictions we performed playback experiments by broadcasting to singleton nestlings calls of varying durations and at different rates. According to the first prediction, singleton nestlings became less vocal to a larger extent when we broadcasted more calls compared to longer calls. In line with the second prediction, nestlings reduced vocalization rate to a larger extent than call duration when we broadcasted more or longer calls. Finally, call rate had a longer influence on opponent’s vocal behavior than call duration. Young animals thus actively and differentially use multiple signaling components to compete with their siblings over parental resources.     

STRUCTURE AND FUNCTION OF RED FOX VULPES VULPES VOCALISATIONS

ABSTRACT

A sonagraphic analysis of the structure of fox vocalisations, based on 512 adult and 73 cub vocalisations obtained from archive recordings, was combined with field data on the vocal behaviour of an urban fox population. Calls were described quantitatively by six variables: duration, lowest and second lowest frequency bands (from sonagrams), highest and second highest peak frequencies (from power spectra) and the number of components. They were separated into 20 call types, eight of which were cub vocalisations. Call types were used singly or in combination, and some gradation between particular call types was apparent. Hypotheses regarding call function were generated based on the matching of acoustic properties with their seasonal occurrence and the socioecological pressures acting on foxes at different times of the year. Calls that were structurally suited to agonistic and contact functions were found to be significantly more common during the winter, the time of mating and dispersal, when foxes move over greater areas.     

Family- and sex-specific vocal traditions in a cooperatively breeding songbird

Although songbirds provide well-known examples of cultural transmission of vocalizations, little is known about this process in species that live in stable social groups. Here I describe complex vocal traditions in a cooperatively breeding songbird, the stripe-backed wren (Campylorhynchus nuchalis). Repertoires of stereotyped calls were recorded from individually marked males and females in cooperative family groups. Males in the same patriline, whether in the same group or in different groups, had call repertoires that were nearly identical. Females in the same matriline also had identical call repertoires; however, female calls never matched the calls of males in the same group or in any nearby groups. Unrelated birds almost never shared calls. Call repertoires are apparently learned preferentially from same-sex relatives within family groups, so that call traditions separately follow patrilines and matrilines. This unique pattern of transmission results in vocal cues that reflect both sex and kinship.     

Sex differences in the vocal repertoire of adult red‐capped mangabeys (Cercocebus torquatus): a multi‐level acoustic analysis

Sex differences in the vocal behavior of nonhuman primates can take various forms: sex‐specific call types, differential production of shared call types, or sex discrepancy in phonation. Also, a growing literature is evidencing that systematically analyzing the vocal repertoires of primates at the call level might lead to underestimating their communicative abilities. Here, we present an extensive multi‐level analysis of the still unknown vocal repertoire of adult red‐capped mangabeys (Cercocebus torquatus), with a special emphasis on sex differences. We collected recordings from seven adult males and seven adult females housed in captivity. We present a structurally‐based classification of mangabey calls that we cross‐validated by an analysis of the associated contexts of emission. We found 12 sound units (including six sex‐specific) that were concatenated to form eight call types (including four sex‐specific), which were produced either singularly or in sequences composed of one (“repetition”) or several (“combination”) call types. We extracted organizational principles that ruled call composition and calling patterns. This revealed a high degree of potentially meaningful variability in terms of semantics and syntax. Male–female discrepancy in terms of phonation could be related to morphological dimorphism and would enable listeners to behave appropriately according to the sex of the caller. Sex differences in repertoire size, structural gradation, and call usage could reflect specificities of male–female social roles. We discuss the pertinence of these sex differences according to social system and habitat quality. Am. J. Primatol. 72:360–375, 2010. © 2010 Wiley‐Liss, Inc.     

SC-karyotyping on electronic microscopy (EM) analysis of synaptonemal complexes (SC) spermocytes of silver fox (Vulpes fulvus)

We present an electronic microscopy (EM) analysis of synaptonemal complexes (SC) spermatocytes of male silver fox Vulpes fulvus at the pachytene stage. The SC-karyotypes of pachetene cells were made and described. Knowledge of normal SC-karyotype is necessary to reveal synaptic abnormalities of autosome and sex bivalents during the pachytene. It was indicated that EM analysis of SC-spermatocytes—the study of synaptonemal complexes in agricultural animals—is a very good instrument for comparative analysis of normal SC-karyotype of foxes that carry chromosomal abnormalities and in fur-bearing animals as well.     

Response of foraging group members to sentinel calls in suricates,Suricata suricatta

In the suricate (Suricata suricatta), a cooperatively breeding mongoose, one individual typically watches out for predators while the rest of the group is foraging. Most of the time these sentinels announce their guarding duty with special vocalizations. The response of foraging group members to these calls was investigated by analysing observational data, and by performing playback experiments. The use of special calls by sentinels, and the responses of the foraging group members to them, suggest that the coordination of vigilance is strongly influenced by vocal communication. Sentinel calls decreased the time spent alert by the foraging group members. Other group members were less likely to go on guard when a sentinel was vocalizing. Both the proportion of time during which guards overlapped, and the proportion of time the group was unprotected without a guard, decreased when sentinels announced their duty, due to better coordination of the rotation of sentinels. Suricates, however, do not appear to use sentinel calls to mediate a strict rotation of guarding duty.     

Mutual dependencies between vocal and visual signals of squirrel monkeys

Visually recognizable social signals and structural call components, which had been demonstrated to be of social relevance within their own communication channel in previous experiments (disregarding or experimentally excluding other ones), were treated together, and their inter-dependencies analyzed when they were performed simultaneously in spontaneous behavior sequences of pairs of adult squirrel monkeys. It was found that: (1) all call classes were uttered within periods when either genital display or “triumph gesture” were shown; (2) production rates of particular vocal classes significantly deviated from no-display periods; (3) degree and direction of deviations (more/less frequent) were quite specific for both vocal and nonvocal classes (Figs. 1a & 1b); (4) differences depended also on which animal actually displayed (the vocalizing one, the other one, or both; Fig. 3); and (5) differences found for single animals when they played different roles in the experimental situation were smaller than those found between individuals, which could be related to dominance status (Table 2). The possibility of mutual modification of signals of different modalities and perspectives for future work are discussed.     

Cultural transmission of vocalizations in ravens, Corvus corax

As ravens have pronounced learning capabilities, especially in the vocal domain, cultural transmission might be a relevant factor affecting the composition of their vocal repertoires. We investigated how important cultural transmission is in establishing a raven's vocal repertoire and whether there are different pathways of transmission. We studied individually known free-ranging breeding pairs whose vocalizations were recorded during interactions with a caged pair. The mean repertoire size of these vocalizations was 12 call types per individual (from 79 types recorded from 74 individuals), with no difference between the sexes. In 81% of individuals the repertoire was composed entirely of calls also used by other individuals. Analysis of the distribution of call types among individuals regarding sex, partnership and neighbourhood and aspects of the geographical distribution of calls showed that the main pathway of cultural transmission was within the sexes. In addition, transmission occurred between pair partners, as well as between neighbouring and more distant pairs. About 40% of the calls in a raven's repertoire were transmitted within a sex and 10% between pair partners. Any two given birds in the population shared on average 20% (0-77%) of their calls. Cultural transmission within the sexes led to a pronounced sexual dimorphism in vocal behaviour. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.