Benjamin J. Pitcher

Recognition of other species' aerial alarm calls: speaking the same language or learning another?

Alarm calls given by other species potentially provide a network of information about danger, but little is known about the role of acoustic similarity compared with learning in recognition of heterospecific calls. In particular, the aerial ‘hawk’ alarm calls of passerines provide a textbook example of signal design because many species have converged on a design that thwarts eavesdropping by hawks, and call similarity might therefore allow recognition. We measured the response of fairy-wrens (Malurus cyaneus) to playback of acoustically similar scrubwren (Sericornis frontalis) aerial alarm calls. First, if call similarity prompts escape independent of learning, then fairy-wrens should flee to playback of scrubwren calls outside their geographical range. However, fairy-wrens fled only in sympatry. Second, if call similarity is necessary for learning heterospecific calls, then fairy-wrens should not respond to sympatric species with different calls. We found, on the contrary, that fairy-wrens fled to the very different aerial alarm calls of a honeyeater (Phylidonyris novaehollandiae). Furthermore, response to the honeyeater depended on the specific structure of the call, not acoustic similarity. Overall, call similarity was neither sufficient nor necessary for interspecific recognition, implying learning is essential in the complex task of sifting the acoustic world for cues about danger.

Vocal recognition of mothers by Australian sea lion pups: individual signature and environmental constraints

As in all otariids, Australian sea lion, Neophoca cinerea, females alternate foraging trips at sea with suckling periods ashore, and each time they return, mothers and pups have to find each other among individuals at the colony. The need for a finely tuned mechanism of individual recognition is exacerbated by their habit of changing the suckling location. Using playback experiments with modified calls, we investigated the acoustic parameters involved in the discrimination of the mother by pups. The signature efficiency was also tested in the three environments in which reunions at the study site occur by performing propagation tests. Pups paid great attention to both amplitude and frequency modulations, and to the exact frequency values of the call to identify their mother. When severe modifications of AM and FM patterns were made to mothers’ calls pups no longer responded to them. This may have arisen because the calls fell outside the natural species range. The energy spectrum, even though highly individualized, was not important for individual recognition. Propagation tests revealed that one particular environment was extremely harsh and did not allow accurate transfer of the individual signature components whatever the distance. In two other environments, AM was only reliable to a distance of 16 m, but both FM and frequency spectrum could be transmitted with limited degradation over 32 m. The different environments greatly influenced the efficiency of the individual identification process. Accordingly, the area in which mother–pup reunions occur is an important factor in the success of individual recognition.

Alarming features: Birds use specific acoustic properties to identify heterospecific alarm calls

Vertebrates that eavesdrop on heterospecific alarm calls must distinguish alarms from sounds that can safely be ignored, but the mechanisms for identifying heterospecific alarm calls are poorly understood. While vertebrates learn to identify heterospecific alarms through experience, some can also respond to unfamiliar alarm calls that are acoustically similar to conspecific alarm calls. We used synthetic calls to test the role of specific acoustic properties in alarm call identification by superb fairy-wrens, Malurus cyaneus. Individuals fled more often in response to synthetic calls with peak frequencies closer to those of conspecific calls, even if other acoustic features were dissimilar to that of fairy-wren calls. Further, they then spent more time in cover following calls that had both peak frequencies and frequency modulation rates closer to natural fairy-wren means. Thus, fairy-wrens use similarity in specific acoustic properties to identify alarms and adjust a two-stage antipredator response. Our study reveals how birds respond to heterospecific alarm calls without experience, and, together with previous work using playback of natural calls, shows that both acoustic similarity and learning are important for interspecific eavesdropping. More generally, this study reconciles contrasting views on the importance of alarm signal structure and learning in recognition of heterospecific alarms.

Social olfaction in marine mammals: wild female Australian sea lions can identify their pup's scent

Historically, anatomical evidence has suggested that marine mammals are anosmic or at best microsmatic, i.e. absent or reduced olfactory capabilities. However, these neuroanatomical considerations may not be appropriate predictors for the use of olfaction in social interactions. Observations suggest that pinnipeds may use olfaction in mother–pup interactions, accepting or rejecting pups after naso-nasal contact. Such maternal–offspring recognition is a favourable area for investigating the involvement of odours in social recognition and selectivity, as females are evolutionarily constrained to direct resources to filial young. However, there is no experimental, morphological or chemical evidence to date for the use of olfaction in social contexts and for individual odour recognition abilities in pinnipeds. Here, we report unequivocal evidence that Australian sea lion (Neophoca cinerea) females can differentiate between the odour of their own pup and that of another, in the absence of any other distinguishing cues. This study demonstrates individual olfactory recognition in a free-ranging wild mammal and is clear evidence of the social function of olfaction in a marine mammal.

Individual identity encoding and environmental constraints in vocal recognition of pups by Australian sea lion mothers

Colonial living imposes strong selection pressures on the communication systems of species with many animals communicating on the same sensory channels simultaneously. Colonial species often exhibit complex individual vocal signatures that encode a caller’s identity in their vocalizations. During lactation, Australian sea lion, Neophoca cinerea, mothers and pups are repeatedly separated when mothers leave the colony to forage. After maternal foraging trips, mothers and pups must reunite in the colony. Both mothers and pups produce individually distinctive vocalizations during reunions and can recognize their counterpart’s calls. Using playback experiments with modified calls, we investigated the acoustic parameters involved in the recognition of pup vocalizations by mothers. We also examined the efficiency of the vocal signature in three habitat types within the colony using propagation tests. We found that Australian sea lion females used a combination of temporal, amplitude and frequency parameters to recognize their pup’s vocalizations. Pup vocalizations were severely degraded in the herbaceous dune habitat type with no vocal signature components reliably propagating to any measured distance. By contrast, calls propagated comparatively well in the shrubby dune habitat of the colony, as the vegetation appeared to act as a windshield. This study shows that the vocal signatures of Australian sea lion pups are both shaped and constrained by their environment and ecology, and that these signatures are of a moderate level of complexity when compared to those of other colonial vertebrates.

Intrasexual selection drives sensitivity to pitch, formants and duration in the competitive calls of fallow bucks

BackgroundMammal vocal parameters such as fundamental frequency (or pitch; fo) and formant dispersion often provide information about quality traits of the producer (e.g. dominance and body size), suggesting that they are sexually selected. However, little experimental evidence exists demonstrating the importance of these cues in intrasexual competition, particularly fo. Male Fallow deer (bucks) produce an extremely low pitched groan. Bucks have a descended larynx and generate fo well below what is expected for animals of their size. Groan parameters are linked to caller dominance, body size and condition, suggesting that groans are the product of sexual selection. Using a playback experiment, we presented bucks with groans that had been manipulated to alter vocal cues to these male characteristics and compared the response to the same, non-modified (natural) groans.ResultsWe experimentally examined the ability of bucks to utilise putative cues to dominance (fo), body size (formant frequencies) and condition (groan duration), when assessing competitors. We found that bucks treated groans with lowered fo (more dominant), and lowered formant frequencies (larger caller) as more threatening. By contrast, groans with raised formant frequencies (smaller caller), and shorter durations (more fatigued caller) were treated as less threatening.ConclusionsOur results indicate that intrasexual selection is driving groans to concurrently convey caller dominance, body size and condition. They represent the first experimental demonstration of the importance of fo in male competition in non-human mammals, and show that bucks have advanced perception abilities that allow them to extract information based on relatively small changes in key parameters.

Sex-Biased Sound Symbolism in English-Language First Names

Sexual selection has resulted in sex-based size dimorphism in many mammals, including humans. In Western societies, average to taller stature men and comparatively shorter, slimmer women have higher reproductive success and are typically considered more attractive. This size dimorphism also extends to vocalisations in many species, again including humans, with larger individuals exhibiting lower formant frequencies than smaller individuals. Further, across many languages there are associations between phonemes and the expression of size (e.g. large /a, o/, small /i, e/), consistent with the frequency-size relationship in vocalisations. We suggest that naming preferences are a product of this frequency-size relationship, driving male names to sound larger and female names smaller, through sound symbolism. In a 10-year dataset of the most popular British, Australian and American names we show that male names are significantly more likely to contain larger sounding phonemes (e.g. “Thomas”), while female names are significantly more likely to contain smaller phonemes (e.g. “Emily”). The desire of parents to have comparatively larger, more masculine sons, and smaller, more feminine daughters, and the increased social success that accompanies more sex-stereotyped names, is likely to be driving English-language first names to exploit sound symbolism of size in line with sexual body size dimorphism.

Cross-modal recognition of familiar conspecifics in goats

When identifying other individuals, animals may match current cues with stored information about that individual from the same sensory modality. Animals may also be able to combine current information with previously acquired information from other sensory modalities, indicating that they possess complex cognitive templates of individuals that are independent of modality. We investigated whether goats (Capra hircus) possess cross-modal representations (auditory–visual) of conspecifics. We presented subjects with recorded conspecific calls broadcast equidistant between two individuals, one of which was the caller. We found that, when presented with a stablemate and another herd member, goats looked towards the caller sooner and for longer than the non-caller, regardless of caller identity. By contrast, when choosing between two herd members, other than their stablemate, goats did not show a preference to look towards the caller. Goats show cross-modal recognition of close social partners, but not of less familiar herd members. Goats may employ inferential reasoning when identifying conspecifics, potentially facilitating individual identification based on incomplete information. Understanding the prevalence of cross-modal recognition and the degree to which different sensory modalities are integrated provides insight into how animals learn about other individuals, and the evolution of animal communication.

Chemical fingerprints reveal clues to identity, heterozygosity, and relatedness.

Olfaction is a key sense for mammals, and as a result chemical signals are an important means of communication for most mammalian species. It has long been established that most mammals make, distribute, and respond to chemosignals in a range of contexts, including reproduction, parent–offspring interactions, and social relationships (1). However, most aquatic mammals are unable to use olfaction when foraging, and evidence for its role in social behavior has been equivocal. Historically, reports in the literature have ranged from describing the semiaquatic pinnipeds as microsmatic (2) to those that have observed the high prevalence of naso-nasal inspection during social interactions (Fig. 1), and so inferred an important role for olfactory recognition (3). It is only recently that we experimentally confirmed in wild Australian sea lions that olfactory cues are a reliable mechanism in offspring recognition even in the absence of other sensory cues (4). Similarly, new experimental evidence in other large, wild mammals indicates the importance of olfactory cues in discrimination of potential mates and competitors as well as kin (5⇓–7). However, perhaps due to both the complexity of working with natural vertebrate populations and the complexity of vertebrate scents, the mechanistic basis of chemical communication has received little study (8). In PNAS, Stoffel et al. (9) provide an important advance in the understanding of chemical communication in wild mammals. They compared genetic similarity and the chemical profiles of Antarctic fur seals in two colonies. In so doing they revealed that individual-specific chemical fingerprints have both inherited and environmental components and seem to encode mother–offspring similarity, heterozygosity, and genetic relatedness. The implications of these findings for chemical communication in wild mammals are profound.

The role of visual cues in mother–pup reunions in a colonially breeding mammal

Parental care is an important factor influencing offspring survival and adult reproductive success in many vertebrates. Parent–offspring recognition ensures care is only directed to filial young, avoiding the costs of misallocated resource transfer. It is essential in colonial mammal species, such as otariids (fur seals and sea lions), in which repeated mother–offspring separations increase the risk of misdirecting maternal effort. Identification of otariid pups by mothers is known to be multi-modal, yet the role of visual cues in this process remains uncertain. We used three-dimensional visual models to investigate the importance of visual cues in maternal recognition of pups in Australian sea lions (Neophoca cinerea). We showed that the colour pattern of pup pelage in the absence of any other sensory cues served to attract the attention of females and prompt investigation. Furthermore, females were capable of accurately distinguishing between models imitating the age-class of their own pup and those resembling older or younger age-classes. Our results suggest that visual cues facilitate age-class discrimination of pups by females and so are likely to play an important role in mother–pup reunions and recognition in otariid species.