Vocal signature recognition of mothers by fur seal pups

Subantarctic fur seals, Arctocephalus tropicalis, come ashore to breed in dense colonies and lactating females have to alternate foraging trips at sea with periods ashore during which they suckle their pups. The effectiveness of vocal recognition between mothers and pups, has been shown experimentally. To see whether the recognition abilities of females differ from those of their offspring, we investigated how pups recognize their mother's calls. We used artificially modified signals in playback experiments to determine which acoustic parameters support the recognition process. Pups used both the energy spectrum and the ascending frequency modulation occurring at the beginning of each call. However, they seemed to rely mainly on spectral analyses. The vocal identification process at a perceptual level is therefore asymmetrical, as mothers mainly use temporal structures to recognize their pup's calls. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

人为疼痛刺激下金色中仓鼠幼鼠叫声的发育过程

金色中仓鼠幼鼠可以利用可听声和超声信号与母鼠进行交流,这些声音可以反映个体的寒冷、饥饿、疼痛等不同生理状态和需求。因疼痛诱发的叫声对于维持幼鼠的存活也有着重要意义。本实验通过录制人为疼痛刺激下,不同日龄金色中仓鼠的叫声,分析并比较了5 - 30 日龄金色中仓鼠不同发声信号特征(可听声出现频次、可听声持续时程、可听声主频率、超声出现频次、超声持续时程、超声主频率)的性别差异;同时记录了幼鼠的两种发声随日龄的变化趋势。结果发现:幼鼠两种叫声的各种参数均未表现性二型现象。幼鼠超声发生频次随日龄增加而逐渐减少。而可听声却正相反,随日龄增加而逐渐上升,并在20 日龄时达到最高峰,之后逐渐下降。可听声持续时程也随日龄而增加。综上,在人为疼痛刺激下,随着日龄增加,幼鼠更倾向于使用可听 声而非超声与母兽进行交流。     

Individual differences in threat calls of northern elephant seal bulls

This study describes the range and reliability of differences between individual elephant seal bulls, Mirounga angustirostris, on several parameters of the threat call: call type, spacing of pulses within calls, addition of snorts to calls, pulse rate of calls, and number of pulses in calls. In addition, some preliminary analyses of the social function of these individual differences are made. Two previously suggested hypotheses, that specific features of the call communicate dominance status and that differences in pulse rate represent dialects, are investigated.     

Small Mammals Ignore Common Rules: A Comparison of Vocal Repertoires and the Acoustics between Pup and Adult Piebald Shrews Diplomesodon pulchellum

A common rule for mammals vocalizing in the human audible frequency range (20 Hz–20 kHz) suggests that calls are higher in fundamental frequency (f0) in the young than in adults, because of the smaller sound‐producing structures of the young. Exclusions are rare, for example the pups of Asian house shrews (Suncus murinus) make some call types of the same or higher pitch than adults. In this study, calls from 62 piebald shrews (Diplomesodon pulchellum), 37 1 to 10‐d‐old pups from 10 litters and 25 adults were acoustically investigated in captivity. We found eight call types, all within the human audible frequency range: short and long low‐frequency squeaks with nearly flat contour, high‐frequency squeaks with modulated contour, high‐frequency squeaks with fractured contour, short and long screeches, clicks and whimpers. Seven call types were shared by pups and adults, suggesting that this vocal repertoire commences at birth. Against the common rule, the f0 of squeaks was the same in pups and adults, and the f0 of clicks and screeches was even higher in adults than in pups. These results suggest a non‐descending ontogenetic pathway that not follows the common physical relationship, of the lower f0 for the larger vocal folds.     

VOCAL INDIVIDUALITY OF IN-AIR WEDDELL SEAL (LEPTONYCHOTES WEDDELLII) PUP "PRIMARY" CALLS

As a result of selective pressures faced during lactation, vocal recognition may play a crucial role in maintaining the phocid mother–pup bond during the period of dependence. To investigate this possibility, we examined whether Weddell seal ( Leptonychotes weddellii ) pups produce individually distinctive "primary" calls. One temporal, nine fundamental frequency features, and two spectral characteristics were measured. A discriminant function analysis (DFA) of 15 Vestfold Hills pups correctly classified 52% of calls, while the cross-validation procedure classified 29% of calls to the correct pup. A second DFA of 10 known-age McMurdo Sound pups correctly classified 44% of "test" calls. For novel calls, the probabilities of attaining such classification rates by chance are low. The relationship between age and call stereotypy indicated that pups 2 wk and older may be more vocally distinctive. Overall, findings suggest that Weddell seal pup "primary" calls are moderately distinctive and only exhibit sufficient stereotypy to aid maternal recognition by approximately two weeks of age.     

INDIVIDUAL VARIATION OF THE FEMALE ATTRACTION CALL PRODUCED BY AUSTRALIAN FUR SEAL PUPS THROUGHOUT THE MATERNAL DEPENDENCE PERIOD

ABSTRACT

Australian fur seals are colonial breeding animals that give birth on crowded rookeries. Females leave their pups unattended for extended periods while they forage at sea. On return to the colony, a mother must relocate her pup amongst the hundreds of other pups. Vocal recognition is thought to play a vital role in maintaining the mother-pup bond. In the present study, four sets of 7 different pups were recorded once each at different times throughout the maternal dependence period. The Female Attraction Call was used to determine whether Australian fur seal pups produce individually distinct calls which could be used as a basis for vocal recognition. Results from three different analyses (PIC, DFA and CART) indicated that the fundamental frequency, number of parts per call, duration, quavering and peak frequency changes at the start, mid-point and end of the call (i.e., along PEAK Fl) were important to recognition. In 75% of cases using DFA, the Female Attraction Call was classified to the correct caller, suggesting that there is sufficient stereotypy within individual calls, and sufficient variation between them, to enable vocal recognition by females.     

The influence of behavioural context on Weddell seal (Leptonychotes weddellii) airborne mother-pup vocalisation

Previous mammalian studies have demonstrated that varying levels of signaller arousal are frequently expressed through vocal behaviour. The potential for callers to convey their motivational state may ensure that recipient responses are appropriate to their needs. The current study investigated the influence of behavioural context on Weddell seal mother-pup vocalisation. Mother and pup call rates were calculated within five and seven behavioural contexts, respectively, and the acoustic characteristics of 69 pup calls were measured within four contexts (total calls = 276). Context significantly influenced the temporal patterning of calls, with reuniting mothers and pups and lone active pups emitting more calls than during mother-pup contact periods. Reuniting and lone pup calls were also characterised by longer durations, higher fundamental frequencies, and increased energy in upper harmonics. Results suggest that reunion events and lone pup searching are characterised by calls reflective of heightened arousal, compared with mother-pup contact periods.     

Mother-Infant Communication in the Lesser Spear-nosed Bat Phyllostomus discolor (Chiroptera,Phyllostomidae) — Evidence for Acoustic Learning

When mother-offspring couples of Phyllostomus discolor (lesser spear-nosed bat) are reunited after separation, an intensive exchange of infants' isolation calls and mothers' directive calls can be observed. The directive calls of each mother show a distinctive frequency-time structure, which appears to represent her individual vocal signature. During ontogenesis the isolation calls of the young change gradually, adapting increasingly to the mother's call type. A comparison of calls of separated pups at different ages with their mothers' directives demonstrated the individually distinct call characteristics of the mother also to be characteristic of the isolation calls of her young by about 50 days of age. This suggests that acoustic signals may be learned in Phyllostomus discolor.     

Evolution and Diversity of Vibrational Signals in Mantophasmatodea (Insecta)

Vibrational communication for species identification and mate location is widespread among insects. We investigated the vibrational communication signals of 13 species of the insect order Mantophasmatodea (Heelwalkers). Males and females produce percussive signals by tapping their abdomens on the substrate to locate conspecific mates. We show that male and female calls are of similar general structure but differ in temporal characteristics. Using a principal component analysis, we demonstrate that most species can be distinguished by their calls only. Mapping the calls onto an existing molecular phylogenetic tree reveals a slow diverging drift of male call pattern but no specific trend. For females, a trend from faster towards slower pulse repetition times is indicated. Two sympatric species, Karoophasma biedouwense and Viridiphasma clanwilliamense (Austrophasmatidae), exhibit very different call parameters. The latter species produces calls rather different from all other investigated species, which might hint at reproductive character displacement.     

Development of echolocation and communication vocalizations in the big brown bat, <Emphasis Type="Italic">Eptesicus fuscus</Emphasis>

Big brown bats form large maternity colonies of up to 200 mothers and their pups. If pups are separated from their mothers, they can locate each other using vocalizations. The goal of this study was to systematically characterize the development of echolocation and communication calls from birth through adulthood to determine whether they develop from a common precursor at the same or different rates, or whether both types are present initially. Three females and their six pups were isolated from our captive breeding colony. We recorded vocal activity from postnatal day 1 to 35, both when the pups were isolated and when they were reunited with their mothers. At birth, pups exclusively emitted isolation calls, with a fundamental frequency range <20 kHz, and duration >30 ms. By the middle of week 1, different types of vocalizations began to emerge. Starting in week 2, pups in the presence of their mothers emitted sounds that resembled adult communication vocalizations, with a lower frequency range and longer durations than isolation calls or echolocation signals. During weeks 2 and 3, these vocalizations were extremely heterogeneous, suggesting that the pups went through a babbling stage before establishing a repertoire of stereotyped adult vocalizations around week 4. By week 4, vocalizations emitted when pups were alone were identical to adult echolocation signals. Echolocation and communication signals both appear to develop from the isolation call, diverging during week 2 and continuing to develop at different rates for several weeks until the adult vocal repertoire is established.     

Strain Differences in the Ultrasonic Behavior of Rats (Rattus Norvegicus)

Wistar rat pups are generally more "vocal" than Lister pups;the ultrasonic calls that they produce are usually louder andemitted at a greater rate than those of Lister pups of the sameage and studied under similar conditions of isolation or handling.These differences in ultrasonic behavior are apparently notrelated to differences in the development of homiothermy whichfollows a similar course in both strains. The calls of infantsof the two strains do not show any marked differences in durationor frequency pattern that are consistent over age or treatmentcondition, but the Wistar pups appear to show greater changeswith age than the Lister pups in certain parameters of the calls,while the latter strain show greater changes with treatmentcondition. Similar strain differences in the rate and intensity of callingwere seen during aggressive encounters between adult males,but these cannot be related to differences in aggressive behavior.The strains differ in the duration of both the long "22 kHz"calls (Lister greater than Wistar) and the shorter "50 kHz"calls (Wistar greater than Lister), as well as in the minimumfrequency of these shorter calls (lower in Wistar than in Listerrats).     

Begging signals in a mobile feeding system: the evolution of different call types

In some species, dependent offspring join foraging providers and beg for food. Mobile offspring might benefit from evolving begging signals adapted to the different situations they are exposed to, but this possibility has been ignored. In cooperatively breeding meerkats (Suricata suricatta), dependent offspring use a repertoire of several begging calls when joining foraging adults. We found that these calls can be differentiated on the basis of their acoustic structure and that pups adjusted the use of specific call types according to the social context. Pups continuously gave "repeat" calls when they accompanied foraging adults, and playback of these calls increased provisioning by the adults. When pups saw adults with food, they switched from repeat calls to vigorous "high-pitched" calls; adults also preferred to "feed" loudspeakers broadcasting high-pitched calls rather then loudspeakers broadcasting repeat calls. The elaboration of different begging calls might reflect an adaptation to a situation where dependent young must solicit food from potential feeders while at the same time directing feeders to bring the prey item to themselves and not to another begging pup. Here we show that mobile but dependent offspring adapt to different contexts in a mobile feeding system by using a repertoire of begging calls.     

The response of willow grouse chicks to auditory stimuli 2. Synthesized brooding calls attract machine-incubated chicks

Willow grouse (Lagopus l. lagopus) chicks appear to possess a ‘template’ of the hen's brooding call. Chicks newly hatched from machine-incubated eggs were therefore exposed to a number of electronically synthesized approximations to brooding calls. These sounds were either paired with a recording of a grouse hen's brooding call, or were played alone. Some of the synthesized calls (repetitive, low-frequency) attracted chicks, while others appeared to be aversive. None of the synthesized calls drew chicks away from the recorded hen call. These results suggest that grouse chicks will approach a wide range of attraction calls which have certain minimum features.     

Ultrasonic isolation calls in genetically high- and low-emotional rat pups.

The present study was undertaken to investigate the relationship between the emotionality and the modulation of ultrasonic vocalizations in Tsukuba High Emotional (THE) and Tsukuba Low Emotional (TLE) strain rat pups 3-18 days old. The THE pups, while isolated from their dam and littermates and placed in a cold environment, emitted ultrasonic isolation calls at a high rate until day 15. In contrast, ultrasound production was at a consistently low level throughout the test period in the TLE pups. The ultrasonic isolation calls of THE pups were attenuated to the same level as those of the TLE pups after administration of diazepam (1 mg/kg, s.c.), a benzodiazepine receptor agonist, at 6 and 12 days of age. These findings suggest that the high emotionality of the rat pups was reflected largely by the emission of ultrasounds in response to isolation distress rather than the number of the benzodiazepine receptors in the brain that might play a role in physiologic mediation of the rat pup isolation call.     

Correlated evolution between hearing sensitivity and social calls in bats

Echolocating bats are auditory specialists, with exquisite hearing that spans several octaves. In the ultrasonic range, bat audiograms typically show highest sensitivity in the spectral region of their species-specific echolocation calls. Well-developed hearing in the audible range has been commonly attributed to a need to detect sounds produced by prey. However, bat pups often emit isolation calls with low-frequency components that facilitate mother-young reunions. In this study, we examine whether low-frequency hearing in bats exhibits correlated evolution with (i) body size; (ii) high-frequency hearing sensitivity or (iii) pup isolation call frequency. Using published audiograms, we found that low-frequency hearing sensitivity is not dependent on body size but is related to high-frequency hearing. After controlling for high-frequency hearing, we found that low-frequency hearing exhibits correlated evolution with isolation call frequency. We infer that detection and discrimination of isolation calls have favoured enhanced low-frequency hearing because accurate parental investment is critical: bats have low reproductive rates, non-volant altricial young and must often identify their pups within large crèches.     

Nest defence in the American goldfinch

In the American goldfinch (Carduelis tristis), vocalizations during nest defence consist largely of two different types of calls: either ‘sweeet’ (SWT) or ‘bearbee’ (BB). By recording call rates and behaviour during controlled experiments, it was demonstrated that: (1) SWT calls have a rallying function and attract more goldfinches than BB calls; (2) goldfinches attempt to distract potential predators away from their nests; (3) BB calls cause a decrease in nestling conspicuousness, both audibly and visually; (4) call rates show a positive relationship with increasing conspicuousness of nestlings; (5) call rates of BB and SWT calls vary inversely with danger to the nest; (6) high call rates are given by parents with successful nests whereas low call rates are associated with failures caused by nest predation; (7) call rates show a positive relationship with clutch and brood size; (8) call rates and types did not vary with different potential predators; and (9) call rates and types used by males and females are related to their respective roles in the nesting cycle. Several hypotheses are discussed that might explain changes in call rates through the nesting cycle.     

Sex recognition in brown skuas: do acoustic signals matter?

Bird vocalisations are often essential for sex recognition, especially in species that show little morphological sex dimorphism. Brown skuas (Catharacta antarctica lonnbergi), which exhibit uniform plumage across both sexes, emit three main calls: the long call, the alarm call and the contact call. We tested the potential for sex recognition in brown skua calls of 42 genetically sexed individuals by analysing 8–12 acoustic parameters in the temporal and frequency domains of each call type. For every call type, we failed to find sex differences in any of the acoustic parameters measured. Stepwise discriminant function analysis (DFA) revealed that sexes cannot be unambiguously classified, with increasing uncertainty of correct classification from contact calls to long calls to alarm calls. Consequently, acoustic signalling is probably not the key mechanism for sex recognition in brown skuas.     

Juvenile vocalizations ofCtenomys talarum (Rodentia: Octodontidae)

We analysed the physical structure and functional interpretation of juvenile vocalizations ofCtenomys talarum Thomas, 1898. Two sounds, one true vocalization (care-elicitation call) and one mechanical sound (nursing sound) were recorded during the nestling period. Care-elicitation calls were emitted by isolated pups and caused the mother to respond by immediately approaching the pups to take care of them. This maternal response to the care-elicitation calls ofC. talarum pups, together with the production of these vocalizations during the first weeks after birth, when pups depend exclusively on their mother to obtain food and maintain their body temperature, give preliminary support for the recent theory that care-elicitation cries are honest advertisements of offspring need.     

Exchange of “signature” calls in captive belugas (Delphinapterus leucas)

Belugas (Delphinapterus leucas) produce echolocation clicks, burst pulses, and whistles. The sounds of 3 captive belugas were recorded using 2 hydrophones at the Port of Nagoya Public Aquarium. There were stable individual differences in the pulse patterning of one type of pulsed sounds (PS1 call), suggesting that belugas use these as “signature” calls. Eighty-eight percent of PS1 calls initiated PS1 calls from other animals within 1 s. PS1 calls repeated by the same individual occurred primarily when other belugas did not respond within 1 s of the first call. Belugas delayed successive PS1 calls when other belugas responded with a PS1 call within 1 s. There was no clear temporal pattern for whistles. It appears that the time limit for responding to calls is 1 s after the initial call. If other individuals do not respond to the PS1 call of a beluga within 1 s, belugas tend to repeat the call and wait for a response. The results of this study suggest that the belugas exchange their individual signatures by using PS1 calls, in a manner similar to that of signature whistles used by bottlenose dolphins.     

No pre-existing biases for heterospecific call traits in the frog Physalaemus enesefae

Previous phonotaxis studies with two species of the Physalaemuspustulosus species group indicated that female preferences for several heterospecific call traits resulted from sensory biases inherited from a common ancestor. In phonotaxis experiments, we determined whether Physalaemus enesefae, a distant relative of the P. pustulosus group, showed similar preferences for call traits not present in conspecific males. We presented females with a choice between the typical conspecific advertisement call and the same call to which we digitally appended a chuck from P. pustulosus, a squawk from P. freibergi, and an amplitude-modulated prefix from P. pustulatus. In addition we presented the advertisement call in doublets, a trait peculiar to P. coloradorum. We also analysed male vocal behaviour evoked in response to the same suite of stimuli. Physalaemus enesefae females did not prefer the calls of their own males with appended heterospecific traits over unmodified calls, nor conspecific calls in doublets over single calls. The lack of preference among females was not the result of a behavioural polymorphism. Female responses to repeated presentations of the same stimulus pair were not consistent. Males also did not show an enhanced vocal response to altered calls relative to the typical conspecific call. Consequently, there are no pre-existing biases for these heterospecific call traits in P. enesefae; pre-existing preferences in the P. pustulosus group could have been inherited from an ancestor not shared with P. enesefae, but data from other closely related species are needed to confirm this conclusion. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.