The structure of stereotyped calls reflects kinship and social affiliation in resident killer whales (Orcinus orca)

A few species of mammals produce group-specific vocalisations that are passed on by learning, but the function of learned vocal variation remains poorly understood. Resident killer whales live in stable matrilineal groups with repertoires of seven to 17 stereotyped call types. Some types are shared among matrilines, but their structure typically shows matriline-specific differences. Our objective was to analyse calls of nine killer whale matrilines in British Columbia to test whether call similarity primarily reflects social or genetic relationships. Recordings were made in 1985–1995 in the presence of focal matrilines that were either alone or with groups with non-overlapping repertoires. We used neural network discrimination performance to measure the similarity of call types produced by different matrilines and determined matriline association rates from 757 encounters with one or more focal matrilines. Relatedness was measured by comparing variation at 11 microsatellite loci for the oldest female in each group. Call similarity was positively correlated with association rates for two of the three call types analysed. Similarity of the N4 call type was also correlated with matriarch relatedness. No relationship between relatedness and association frequency was detected. These results show that call structure reflects relatedness and social affiliation, but not because related groups spend more time together. Instead, call structure appears to play a role in kin recognition and shapes the association behaviour of killer whale groups. Our results therefore support the hypothesis that increasing social complexity plays a role in the evolution of learned vocalisations in some mammalian species.     

Two sympatric species of passerine birds imitate the same raptor calls in alarm contexts

While some avian mimics appear to select sounds randomly, other species preferentially imitate sounds such as predator calls that are associated with danger. Previous work has shown that the Greater Racket-tailed Drongo (Dicrurus paradiseus) incorporates predator calls and heterospecific alarm calls into its own species-typical alarm vocalizations. Here, we show that another passerine species, the Sri Lanka Magpie (Urocissa ornata), which inhabits the same Sri Lankan rainforest, imitates three of the same predator calls that drongos do. For two of these call types, there is evidence that magpies also use them in alarm contexts. Our results support the hypothesis that imitated predator calls can serve as signals of alarm to multiple species.     

The potential to encode sex,age, and individual identity in the alarm calls of three species of Marmotinae

In addition to encoding referential information and information about the sender’s motivation, mammalian alarm calls may encode information about other attributes of the sender, providing the potential for recognition among kin, mates, and neighbors. Here, we examined 96 speckled ground squirrels (Spermophilus suslicus), 100 yellow ground squirrels (Spermophilus fulvus) and 85 yellow-bellied marmots (Marmota flaviventris) to determine whether their alarm calls differed between species in their ability to encode information about the caller’s sex, age, and identity. Alarm calls were elicited by approaching individually identified animals in live-traps. We assume this experimental design modeled a naturally occurring predatory event, when receivers should acquire information about attributes of a caller from a single bout of alarm calls. In each species, variation that allows identification of the caller’s identity was greater than variation allowing identification of age or sex. We discuss these results in relation to each species’ biology and sociality.     

Altai pika (<Emphasis Type="Italic">Ochotona alpina</Emphasis>) alarm calls: individual acoustic variation and the phenomenon of call-synchronous ear folding behavior

Non-hibernating pikas collect winter food reserves and store them in hay piles. Individualization of alarm calls might allow discrimination between colony members and conspecifics trying to steal food items from a colony pile. We investigated vocal posture, vocal tract length, and individual acoustic variation of alarm calls, emitted by wild-living Altai pikas Ochotona alpina toward a researcher. Recording started when a pika started calling and lasted as long as possible. The alarm call series of 442 individual callers from different colonies consisted of discrete short (0.073–0.157 s), high-frequency (7.31–15.46 kHz), and frequency-modulated calls separated by irregular intervals. Analysis of 442 discrete calls, the second of each series, revealed that 44.34% calls lacked nonlinear phenomena, in 7.02% nonlinear phenomena covered less than half of call duration, and in 48.64% nonlinear phenomena covered more than half of call duration. Peak frequencies varied among individuals but always fitted one of three maxima corresponding to the vocal tract resonance frequencies (formants) calculated for an estimated 45-mm oral vocal tract. Discriminant analysis using variables of 8 calls per series of 36 different callers, each from a different colony, correctly assigned over 90% of the calls to individuals. Consequently, Altai pika alarm calls are individualistic and nonlinear phenomena might further increase this acoustic individualization. Additionally, video analysis revealed a call-synchronous, very fast (0.13–0.23 s) folding, depression, and subsequent re-expansion of the pinna confirming an earlier report of this behavior that apparently contributes to protecting the hearing apparatus from damage by the self-generated high-intensity alarm calls.     

Stability of acoustic individuality in the alarm calls of wild yellow ground squirrels Spermophilus fulvus and contrasting calls from trapped and free-ranging callers

The questions of individuality and stability of cues to identity in vocal signals are of considerable importance from theoretical and conservation perspectives. While individuality in alarm calls has been reported for many sciurids, it is not well-documented that the vocal identity encoded in the alarm calls is stable between different encounters with predators. Previous studies of two obligate hibernating rodents, speckled ground squirrels Spermophilus suslicus, and yellow ground squirrels Spermophilus fulvus demonstrated that, after hibernation, most individuals could not be identified reliably by their alarm calls. Moreover, in most speckled ground squirrels, individual patterns of alarm calls changed progressively over as little as 2 weeks. However, these previous data have been obtained using the collection of alarm calls from trapped animals. Here, we examined ten free-ranging dye-marked yellow ground squirrels to determine whether their alarm calls retain the cues to individuality between two encounters of surrogate predators (humans), separated on average by 3 days. Discriminant function analysis showed that the alarm calls of individual yellow ground squirrels were very similar within a recording session, providing very high individual distinctiveness. However, in six of the ten animals, the alarm calls were unstable between recording sessions. Also, we examined ten dye-marked individuals for consistency of acoustic characteristics of their alarm calls between the encounters of humans, differing in techniques of call collection, from free-ranging vs trapped animals. We found differences only in two variables, both related to sound degradation in the environment. Data are discussed in relation to hypotheses explaining the adaptive utility of acoustic individuality in alarm calls.     

Vocal acrobatics in a Chinese frog, <Emphasis Type="Italic">Amolops tormotus</Emphasis>

Although amphibians are highly vocal, they generally emit only a limited number of acoustic communication signals. We report here the extraordinarily rich vocal repertoire of Amolops tormotus, a ranid species in China. These frogs produce countless vocalizations, some of which share features of birdsong or primate calls, e.g., ultrasonic frequency components, multiple upward and downward FM sweeps, and sudden onset and offset of selective harmonic components within a call note. Frame-by-frame video analysis of the frog's calling behavior suggests the presence of two pairs of vocal sacs that may contribute to the remarkable call-note complexity in this species. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/s00114-002-0335-x.     

Unusually high-pitched neonate distress calls of the open-habitat Mongolian gazelle (<Emphasis Type="Italic">Procapra gutturosa</Emphasis>) and their anatomical and hormonal predictors

In neonate ruminants, the acoustic structure of vocalizations may depend on sex, vocal anatomy, hormonal profiles and body mass and on environmental factors. In neonate wild-living Mongolian gazelles Procapra gutturosa, hand-captured during biomedical monitoring in the Daurian steppes at the Russian-Mongolian border, we spectrographically analysed distress calls and measured body mass of 22 individuals (6 males, 16 females). For 20 (5 male, 15 female) of these individuals, serum testosterone levels were also analysed. In addition, we measured relevant dimensions of the vocal apparatus (larynx, vocal folds, vocal tract) in one stillborn male Mongolian gazelle specimen. Neonate distress calls of either sex were high in maximum fundamental frequency (800–900 Hz), but the beginning and minimum fundamental frequencies were significantly lower in males than in females. Body mass was larger in males than in females. The levels of serum testosterone were marginally higher in males. No correlations were found between either body mass or serum testosterone values and any acoustic variable for males and females analysed together or separately. We discuss that the high-frequency calls of neonate Mongolian gazelles are more typical for closed-habitat neonate ruminants, whereas other open-habitat neonate ruminants (goitred gazelle Gazella subgutturosa, saiga antelope Saiga tatarica and reindeer Rangifer tarandus) produce low-frequency (<200 Hz) distress calls. Proximate cause for the high fundamental frequency of distress calls of neonate Mongolian gazelles is their very short, atypical vocal folds (4 mm) compared to the 7-mm vocal folds of neonate goitred gazelles, producing distress calls as low as 120 Hz.     

Delayed onset of vocal recognition in Australian sea lion pups (Neophoca cinerea)

In pinnipeds, maternal care strategies and colony density may influence a species’ individual recognition system. We examined the onset of vocal recognition of mothers by Australian sea lion pups (Neophoca cinerea). At 2 months of age, pups responded significantly more to the calls of their own mothers than alien female calls demonstrating a finely tuned recognition system. However, newborn pups did not respond differentially to the calls of their mother from alien female calls suggesting that vocal recognition had not yet developed or is not yet expressed. These findings are in stark contrast to other otariid species where pups learn their mother’s voice before their first separation. Variance in colony density, pup movements, and natal site fidelity may have reduced selective pressures on call recognition in young sea lions, or alternatively, another sensory system may be used for recognition in the early stage of life.     

Mourning dove (Zenaida macroura) wing-whistles may contain threat-related information for con- and hetero-specifics

Distinct acoustic whistles are associated with the wing-beats of many doves, and are especially noticeable when doves ascend from the ground when startled. I thus hypothesized that these sounds may be used by flock-mates as cues of potential danger. To test this hypothesis, I compared the responses of mourning doves (Zenaida macroura), northern cardinals (Cardinalis cardinalis), and house sparrows (Passer domesticus) to audio playbacks of dove ‘startle wing-whistles’, cardinal alarm calls, dove ‘nonstartle wing-whistles’, and sparrow ‘social chatter’. Following playbacks of startle wing-whistles and alarm calls, conspecifics and heterospecifics startled and increased vigilance more than after playbacks of other sounds. Also, the latency to return to feeding was greater following playbacks of startle wing-whistles and alarm calls than following playbacks of other sounds. These results suggest that both conspecifics and heterospecifics may attend to dove wing-whistles in decisions related to antipredator behaviors. Whether the sounds of dove wing-whistles are intentionally produced signals warrants further testing.     

Colour mimicry and sexual deception by Tongue orchids (Cryptostylis)

Typically, floral colour attracts pollinators by advertising rewards such as nectar, but how does colour function when pollinators are deceived, unrewarded, and may even suffer fitness costs? Sexually deceptive orchids are pollinated only by male insects fooled into mating with orchid flowers and inadvertently transferring orchid pollinia. Over long distances, sexually deceptive orchids lure pollinators with counterfeit insect sex pheromones, but close-range deception with colour mimicry is a tantalising possibility. Here, for the first time, we analyse the colours of four sexually deceptive Cryptostylis orchid species and the female wasp they mimic (Lissopimpla excelsa, Ichneumonidae), from the perspective of the orchids’ single, shared pollinator, male Lissopimpla excelsa. Despite appearing different to humans, the colours of the orchids and female wasps were effectively identical when mapped into a hymenopteran hexagonal colour space. The orchids and wasps reflected predominantly red-orange wavelengths, but UV was also reflected by raised bumps on two orchid species and by female wasp wings. The orchids’ bright yellow pollinia contrasted significantly with their overall red colour. Orchid deception may therefore involve accurate and species-specific mimicry of wavelengths reflected by female wasps, and potentially, exploitation of insects’ innate attraction to UV and yellow wavelengths. In general, mimicry may be facilitated by exploiting visual vulnerabilities and evolve more readily at the peripheries of sensory perception. Many sexually deceptive orchids are predominantly red, green or white: colours that are all potentially difficult for hymenoptera to detect or distinguish from the background.     

Developmental changes of nasal and oral calls in the goitred gazelle <Emphasis Type="Italic">Gazella subgutturosa</Emphasis>, a nonhuman mammal with a sexually dimorphic and descended larynx

In goitred gazelles (Gazella subgutturosa), sexual dimorphism of larynx size and position is reminiscent of the case in humans, suggesting shared features of vocal ontogenesis in both species. This study investigates the ontogeny of nasal and oral calls in 23 (10 male and 13 female) individually identified goitred gazelles from shortly after birth up to adolescence. The fundamental frequency (f0) and formants were measured as the acoustic correlates of the developing sexual dimorphism. Settings for LPC analysis of formants were based on anatomical dissections of 5 specimens. Along ontogenesis, compared to females, male f0 was consistently lower both in oral and nasal calls and male formants were lower in oral calls, whereas the first two formants of nasal calls did not differ between sexes. In goitred gazelles, significant sex differences in f0 and formants appeared as early as the second week of life, while in humans they emerge only before puberty. This result suggests different pathways of vocal ontogenesis in the goitred gazelles and in humans.     

Individual differences and repeatability in vocal production: stress-induced calling exposes a songbird's personality

Recent research in songbirds has demonstrated that male singing behavior varies systematically with personality traits such as exploration and risk taking. Here we examine whether the production of bird calls, in addition to bird songs, is repeatable and related to exploratory behavior, using the black-capped chickadee (Poecile atricapillus) as a model. We assessed the exploratory behavior of individual birds in a novel environment task. We then recorded the vocalizations and accompanying motor behavior of both male and female chickadees, over the course of several days, in two different contexts: a control condition with no playback and a stressful condition where chick-a-dee mobbing calls were played to individual birds. We found that several vocalizations and behaviors were repeatable within both a control and a stressful context, and across contexts. While there was no relationship between vocal output and exploratory behavior in the control context, production of alarm and chick-a-dee calls in the stressful condition was positively associated with exploratory behavior. These findings are important because they show that bird calls, in addition to bird song, are an aspect of personality, in that calls are consistent both within and across contexts, and covary with other personality measures (exploration).     

Light-mimicking cockroaches indicate Tertiary origin of recent terrestrial luminescence

Bioluminescence is a common feature of the communication and defence of marine organisms, but this phenomenon is highly restricted in the terrestrial biota. Here, we present a geographical distribution of only the third order of luminescent insects—luminescent cockroaches, with all 13 known and/or herein reported new living species (based on deposited specimens). We show that, for the first time, photo-characteristics of three examined species are nearly identical with those of toxic luminescent click beetles, which they mimic. These observations are the evidence for the mimicry by light—a new type of defensive, Batesian and interordinal mimicry. Our analysis surprisingly reveals an evolutionary novelty of all living luminescent insects, while in the sea (and possibly in the soil) luminescence is present also phylogenetically in very primitive organisms.     

The reproductive choices of eavesdropping female black-capped chickadees,<Emphasis Type="Italic"> Poecile atricapillus</Emphasis>

In animals where males engage in signalling interactions, females might evaluate male–male contests to inform their reproductive choices. We used interactive playback to engage territorial male black-capped chickadees (Poecile atricapillus) of known dominance status in countersinging contests with an aggressive or submissive opponent. Previous analysis of these data showed that high-ranking males who received aggressive playback were more likely to be cuckolded. Here we describe the particular reproductive decisions of females whose partners received aggressive versus submissive playback. The proportion of extra-pair young per brood was higher for females paired to high-ranking males that received aggressive playback compared to submissive playback, and similar to levels in broods of females paired to low-ranking males. We found no strong predictors of whether high-ranking subjects lost paternity following aggressive playback. Females usually preferred extra-pair sires with high dominance status. When females had extra-pair fertilizations with low-ranking males, females chose males who had received submissive playback. We conclude that females mated to aggressive-playback, high-ranking males pursued mixed mating strategies similar to those of females mated to low-ranking males. Our results support the idea that male performance in song contests may influence multiple aspects of female reproductive choices.     

Predatory spider mimics acquire colony-specific cuticular hydrocarbons from their ant model prey

The integrity of social insect colonies is maintained by members recognising and responding to the chemical cues present on the cuticle of any intruder. Nevertheless, myrmecophiles use chemical mimicry to gain access to these nests, and their mimetic signals may be acquired through biosynthesis or through contact with the hosts or their nest material. The cuticular hydrocarbon profile of the myrmecophilous salticid spider Cosmophasis bitaeniata closely resembles that of its host ant Oecophylla smaragdina. Here, we show that the chemical resemblance of the spider does not arise through physical contact with the adult ants, but instead the spider acquires the cuticular hydrocarbons by eating the ant larvae. More significantly, we show that the variation in the cuticular hydrocarbon profiles of the spider depends upon the colony of origin of the ant larvae prey, rather than the parentage of the spider.     

Cross-cultural and cross-ecotype production of a killer whale ‘excitement’ call suggests universality

Facial and vocal expressions of emotion have been found in a number of social mammal species and are thought to have evolved to aid social communication. There has been much debate about whether such signals are culturally inherited or are truly biologically innate. Evidence for the innateness of such signals can come from cross-cultural studies. Previous studies have identified a vocalisation (the V4 or ‘excitement’ call) associated with high arousal behaviours in a population of killer whales in British Columbia, Canada. In this study, we compared recordings from three different socially and reproductively isolated ecotypes of killer whales, including five vocal clans of one ecotype, each clan having discrete culturally transmitted vocal traditions. The V4 call was found in recordings of each ecotype and each vocal clan. Nine independent observers reproduced our classification of the V4 call from each population with high inter-observer agreement. Our results suggest the V4 call may be universal in Pacific killer whale populations and that transmission of this call is independent of cultural tradition or ecotype. We argue that such universality is more consistent with an innate vocalisation than one acquired through social learning and may be linked to its apparent function of motivational expression.     

Living in a “stethoscope”: burrow-acoustics promote auditory specializations in subterranean rodents

Subterranean mammals rely to a great extent on audition for communication and to be alerted to danger. The only hitherto published report on burrow acoustics revealed that in tunnels of blind mole-rats (Spalax ehrenbergi), airborne sounds of 440 Hz propagated best whereas lower and higher frequencies were effectively attenuated. Morpho-functional analyses classify the ear of subterranean mammals as a low-sensitivity and low-frequency device. Concordantly, hearing is characterized by low sensitivity and a restricted frequency range tuned to low frequencies (0.5–4 kHz). Some authors considered the restricted hearing in subterranean mammals vestigial and degenerate due to under-stimulation. In contrast to this view stand a rich (mostly low-frequency) vocal repertoire and progressive structural specializations of the middle and inner ear. Thus, other authors considered these hearing characteristics adaptive. To test the hypothesis that acoustical environment in burrows of different species of subterranean mammals is similar, we measured sound attenuation in burrows of Fukomys mole-rats (formerly known as Cryptomys, cf. Kock et al. 2006) of two differently sized species at different locations in Zambia. We show that in these burrows, low-frequency sounds (200–800 Hz) are not only least attenuated but also their amplitude may be amplified like in a stethoscope (up to two times over 1 m). We suggest that hearing sensitivity has decreased during evolution of subterranean mammals to avoid over-stimulation of the ear in their natural environment. We dedicate this work to Mathias Kawalika, who died in March 2006.