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.     

The role of olfactory cues in mother–pup,groupmate, and sex recognition of lesser flat‐headed bats,Tylonycteris pachypus

Tylonycteris pachypus is a gregarious bat species with tens of individuals in a colony. The mechanisms by which mother bats recognize their pups and adult bats recognize each other are not clear. We hypothesized that such recognition is achieved by chemical discrimination and performed experiments to test the hypothesis. Results showed that mother bats were much more attracted to the scent from their own pups. For adult bats, females were attracted to the scent from both male and female groupmates but had a higher preference to the scent from female than from male groupmates. Male bats were much more attracted to the scent from male groupmates while showed no preference to the scent from female groupmates. Within a group, both female and male bats had no difference in preference to the scent from the same or opposite sex. These results suggest that mother–pup and groupmate recognition of T. pachypus can be achieved by olfactory cues.     

The Semantic Representation of Event Information Depends on the Cue Modality: An Instance of Meaning-Based Retrieval

The semantic content, or the meaning, is the essence of autobiographical memories. In comparison to previous research, which has mainly focused on the phenomenological experience and the age distribution of retrieved events, the present study provides a novel view on the retrieval of event information by quantifying the information as semantic representations. We investigated the semantic representation of sensory cued autobiographical events and studied the modality hierarchy within the multimodal retrieval cues. The experiment comprised a cued recall task, where the participants were presented with visual, auditory, olfactory or multimodal retrieval cues and asked to recall autobiographical events. The results indicated that the three different unimodal retrieval cues generate significantly different semantic representations. Further, the auditory and the visual modalities contributed the most to the semantic representation of the multimodally retrieved events. Finally, the semantic representation of the multimodal condition could be described as a combination of the three unimodal conditions. In conclusion, these results suggest that the meaning of the retrieved event information depends on the modality of the retrieval cues.     

Maternal ‘imprinting’ or maternal ‘labelling’ in goats?

The present study on maternal ‘imprinting’ in goats initially failed to replicate previous findings that mothers discriminate between their own and alien young, accepting their own kid and rejecting alien kids. Rather, 62% of the mothers accepted both their own and alien kid. This disparity was not due to breed differences, age, or behaviour of the aliens but to length of time the alien kids had been with their own mother. When behaviour was eliminated through anaesthesia or left intact, older aliens that had had no contact with their mother were accepted by other mothers, while those aliens with more than 8 h of contact with their own mothers were rejected (whether anaesthetized or not) by other mothers. Maternal ‘imprinting’ in goats may take longer than previously reported, and mothers may ‘label’ their kids and learn to recognize the labels.     

Assessment of Rival Males through the Use of Multiple Sensory Cues in the Fruitfly Drosophila pseudoobscura

Environments vary stochastically, and animals need to behave in ways that best fit the conditions in which they find themselves. The social environment is particularly variable, and responding appropriately to it can be vital for an animal’s success. However, cues of social environment are not always reliable, and animals may need to balance accuracy against the risk of failing to respond if local conditions or interfering signals prevent them detecting a cue. Recent work has shown that many male Drosophila fruit flies respond to the presence of rival males, and that these responses increase their success in acquiring mates and fathering offspring. In Drosophila melanogaster males detect rivals using auditory, tactile and olfactory cues. However, males fail to respond to rivals if any two of these senses are not functioning: a single cue is not enough to produce a response. Here we examined cue use in the detection of rival males in a distantly related Drosophila species, D. pseudoobscura, where auditory, olfactory, tactile and visual cues were manipulated to assess the importance of each sensory cue singly and in combination. In contrast to D. melanogaster, male D. pseudoobscura require intact olfactory and tactile cues to respond to rivals. Visual cues were not important for detecting rival D. pseudoobscura, while results on auditory cues appeared puzzling. This difference in cue use in two species in the same genus suggests that cue use is evolutionarily labile, and may evolve in response to ecological or life history differences between species.     

Piñon seed assessment by the piñon jay, Gymnorhinus cyanocephalus

Piñon jays (Gymnorhinus cyanocephalus) distinguished accurately between good and bad seeds of piñon pines (Pinus edulis). This was investigated in captives of three age groups: wild-caught adults, hand-reared yearlings, and hand-reared juveniles. All appeared to use visual, tactile (apparently weight) and auditory (‘bill-clicking’) cues. Discrimination improved with practice. Bad seeds weighted with lead shot caused only temporary confusion. Inexperienced piñon jays demonstrated an immediate preference for piñon seeds over other objects. Distinguishing good seeds from bad was learned. ‘Bill-clicking’ apparently is unlearned, as it appears in young birds in a variety of contexts. The relationship between sounds perceived, external coloration, weight, and seed quality must be integrated by experiential processes.     

How mothers find their pups in a colony of Antarctic fur seals

In Antarctic fur seals, Arctocephalus gazella, mothers must identify their own young among hundreds or even thousands of pups, if they are to invest in their own offspring and avoid misdirecting their parental care. When returning to their breeding colony from a foraging trip of several days at sea, mothers have to find and identify their young before suckling can occur. There appears to be little confusion about which pup belongs to a mother, and adoption is absent or rare. Using behavioral observations, we investigated the means by which female Antarctic fur seals identified their pups in a breeding colony of about 750 mother-pup pairs on Kerguelen Island. We evaluated the importance of vision, scent communication, vocalizations, and rendezvous locations as possible explanations of how mothers find their pups. Every pup that a mother examined, whether her own or not, exchanged naso-nasal inspection with her, suggesting a strong role for olfactory communication in individual recognition. Both mothers and pups called to each other, and mothers that searched for pups over a longer period gave more calls and encountered more pups. Thus, vocalizations may have been used to attract pups that might be offspring. Nursing usually occurred in the same place from the end of one maternal visit to the colony and the arrival at the beginning of the next visit, suggesting that nursing locations may serve as a meeting place, or rendezvous, for mothers and pups. These results suggest that finding pups is a two-stage process for females, in which pups for sampling are attracted by calls or examined at the previous nursing location, and then individual identification is made by olfactory cues.     

Preference of 12-h-old kids for their mother goat is impaired by pre-partum-induced anosmia in the mother

We investigated whether kids were able to discriminate their own mother from an alien one in a two-choice test on the day of birth when they had access to acoustic, visual and olfactory cues from their mother, and whether this discrimination depended on the selective maternal behaviour of the mother (i.e. exclusive nursing of own kids). When given the choice between their own mother and an alien equivalent dam, 8-h-old kids did not show a significant preference for their dam, whereas 12- and 24-h-old kids did. When given the choice between their own and an alien mother that were both non-selective because they had been rendered peripherally anosmic by irrigation of the nostrils with zinc sulphate, 12-h-old kids did not show a significant preference for their mother. These results are similar to those reported in sheep and may suggest that the contrast of behaviour between their own and an alien mother existing in normosmic does is important for discrimination of dams by kids at this age. Finally, testing 8-h-old kids in a smaller enclosure resulted in some improvement of their performance, although they still failed to display a significant preference for their mother. On the whole, kids are able to discriminate between their own and an alien mother goat as early as previously reported in lambs. The impairment of this ability when mothers are anosmic and not selective suggests that acceptance behaviours displayed by the mother may serve as one of the cues orientating the choice of the kid when given the choice between intact mothers. Finally, the present results do not suggest the existence of fundamental differences in the establishment of a preference for the mother between lambs, which are followers, and kids, which are hiders.     

Lactating Females Do Not Discriminate Between Their Own Young and Unrelated Pups in the Communally Breeding Rodent, Octodon degus

Females in numerous rodent species engage in communal nesting and breeding, in which they share one or more nests to rear their young. A potential cost of communal nesting and breeding is that mothers divert resources to unrelated offspring. One way mothers could avoid this cost is to recognize and favour their own young over unrelated offspring when allocating maternal effort. We assessed whether female degus (Octodon degus), a communally nesting and breeding caviomorph rodent, discriminate between their own and unrelated offspring during lactation. Female degus previously have been shown to distinguish between their own and unrelated pups when exposed to odours from both. We measured pup discrimination based on differences in the retrieval behaviour of females that were in early or intermediate lactation directed towards their own and unrelated offspring; offspring presented were of similar or different age. Before any event of pup retrieval, lactating females spent similar amounts of time and interacted to a similar extent with their own and unrelated pups. During pup retrieval, all lactating females transported both pups to the nest. Neither relatedness to pups, nor pup‐age differences, influenced the order in which pups were retrieved to the nest. Dams waited similar amounts of time before retrieving the first pup when the first transported young was their own or unrelated. Likewise, females waited similar amounts of time before retrieving the second pup when the pup transported first was their own or unrelated. The time between first and second pup transport events was longer when dams were in early when compared with intermediate lactation, but only when pups were of similar age. All experimental subjects nursed unrelated pups after they were retrieved. Collectively, our results do not support the hypothesis that communally breeding female degus use their recognition ability to discriminate against unrelated offspring in favour of their own young.     

A species-specific view of song representation in a sensorimotor nucleus

Songbirds constitute a powerful model system for the investigation of how complex vocal communication sounds are represented and generated, offering a neural system in which the brain areas involved in auditory, motor and auditory–motor integration are well known. One brain area of considerable interest is the nucleus HVC. Neurons in the HVC respond vigorously to the presentation of the bird’s own song and display song-related motor activity. In the present paper, we present a synthesis of neurophysiological studies performed in the HVC of one songbird species, the canary (Serinus canaria). These studies, by taking advantage of the singing behavior and song characteristics of the canary, have examined the neuronal representation of the bird’s own song in the HVC. They suggest that breeding cues influence the degree of auditory selectivity of HVC neurons for the bird’s own song over its time-reversed version, without affecting the contribution of spike timing to the information carried by these two song stimuli. Also, while HVC neurons are collectively more responsive to forward playback of the bird’s own song than to its temporally or spectrally modified versions, some are more broadly tuned, with an auditory responsiveness that extends beyond the bird’s own song. Lastly, because the HVC is also involved in song production, we discuss the peripheral control of song production, and suggest that interspecific variations in song production mechanisms could be exploited to improve our understanding of the functional role of the HVC in respiratory–vocal coordination.     

Differential Growth of Own and Alien Pups in Mixed Litters of Mice: A Role for Genomic Imprinting?

Female mice are said to be unable to distinguish own from alien offspring and will indiscriminately nurse each other's young in communal nests. Here, we present results of a split‐litter experiment that tested whether offspring growth was affected depending on whether they were nursed by their own or unrelated foster mothers. Pups of reciprocal crosses between C57/B6 and CBA/Ca strains were fostered in mixed litters that consisted half of their natural siblings and half of unrelated littermates of the reciprocal genotype. Analysing the relative growth of the two pup types showed that offspring gained proportionally more weight when nursed by their own mothers than their cross‐fostered litter mates during the period from day 15 until weaning, during which maternal provisioning effort contributes to pup weight gain. Before day 15 of the pups’ life, however, we found no advantage of being nursed by biological mothers, and we suggest that this may be due to the effects of paternally expressed genes in young that mask their maternal identity, thus favouring indiscriminate nursing of all young in a communal nest.     

Responses of Male and Female Black Grouse to Male Vocal Display

The evolution of leks may be explained by several hypotheses. The ‘female preference’ hypothesis, which states that females favour males that have aggregated, has recently gained some empirical support. Low-quality, unattractive males may, however, settle near attractive males, as predicted by the ‘hotshot’ hypothesis. We tested whether black grouse Tetrao tetrix females use auditory cues to find the preferred leks, and whether males respond to vocal display emitted on leks. We conducted a playback experiment with male vocal display (rookooing) on leks, where the visiting females and displaying males were counted. The number of males tended to increase more on playback leks. Specifically, the number of 1-year-old males was greater on playback sites than on control sites. Also, the number of females, in relation to the lek size before the start of the experiment tended to increase. In addition, we used aviary playback trials to test whether females distinguish between single-male and multi-male displays. In a choice test, females showed greater preference for the ‘multi-male’ tape. The tendency for increased male numbers on playback leks resulted from increased visits of young, mobile males which were attracted to leks that they perceived to be large. This suggests a ‘hotshot’-type mechanism in the settlement of young males. Because females also responded to the supplemented auditory advertisement, or directly to the increased number of males, the ‘female preference’ hypothesis is also supported. Females may, at least in part, base their decision of which lek to visit on auditory cues, but visual contact to males may be also needed.     

Temporal correspondence of intracranial,cochlear and scalp-recorded human auditory nerve action potentials

Conventional, vertex-ipsilateral ear records (‘A’), as well as 3-channel Lissajous' trajectories (3-CLTs) of auditory brain-stem evoked potentials (ABEPs) were recorded from the scalp simultaneously with tympanic membrane electrocochleograms (‘TME’) and auditory nerve compound action potentials (‘8-AP’) recorded intracranially using a wick electrode on the auditory nerve between the internal auditory meatus and the brain-stem. The recordings were made during surgical procedures exposing the auditory nerve.The peak latency recorded from ‘TME’ corresponded to trajectory amplitude peak ‘a’ of 3-LLT and to peak ‘I’ of the ‘A’ channel ABEP. Peak latency of ‘8-AP’ was slightly longer than the latency of peak ‘II’ of ‘A’ when ‘8-AP’ was recorded from the root entry zone and the same or shorter when recorded from the nerve trunk. ‘8-AP’ peak latency was shorter than trajectory amplitude peak ‘b’ of 3-CLT regardless of where the wick electrode was along the nerve. Peak latencies from all recordings sites clustered into two distinct groups—those that included N1 from ‘TME’, peak ‘I’ of the ‘A’ record and trajectory amplitude peak ‘a’ of 3-CLT, and those that included the negative peak of ‘8-AP’ and trajectory amplitude peak ‘b’ of 3-CLT, as well as peak ‘II’ of the ‘A’ record, when present. In one case, the latency of peak ‘II’ and trajectory amplitude peak ‘b’ was manipulated by changing the conductive properties of the medium surrounding the auditory nerve.These results are consistent with other evidence proposing: (1) the most distal (cochlear) portion of the auditory nerve is the generator of the first ABEP component (‘I’, ‘a’); (2) the proximal auditory nerve is the major contributor to the ‘A’ channel ABEP component ‘II’; (3) in addition to the auditory nerve, more central structures participate in the generation of the 3-CLT ‘b’ component.     

Integration of Visual and Olfactory Cues in Host Plant Identification by the Asian Longhorned Beetle,Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae)

Some insects use host and mate cues, including odor, color, and shape, to locate and recognize their preferred hosts and mates. Previous research has shown that the Asian longicorn beetle, Anoplophora glabripennis (Motschulsky), uses olfactory cues to locate host plants and differentiate them from non-host plants. However, whether A. glabripennis adults use visual cues or a combination of visual and olfactory cues remains unclear. In this study, we tested the host location and recognition behavior in A. glabripennis, which infests a number of hardwood species and causes considerable economic losses in North America, Europe and Asia. We determined the relative importance of visual and olfactory cues from Acer negundo in host plant location and recognition, as well as in the discrimination of non-host plants (Sabina chinensis and Pinus bungeana), by female and male A. glabripennis. Visual and olfactory cues from the host plants (A. negundo), alone and combined, attracted significantly more females and males than equivalent cues from non-host plants (S. chinensis and P. bungeana). Furthermore, the combination of visual and olfactory cues of host plants attracted more adults than either cue alone, and visual cues alone attracted significantly more adults than olfactory cues alone. This finding suggests that adult A. glabripennis has an innate preference for the visual and/or olfactory cues of its host plants (A. negundo) over those of the non-host plant and visual cues are initially more important than olfactory cues for orientation; furthermore, this finding also suggests that adults integrate visual and olfactory cues to find their host plants. Our results indicate that different modalities of host plant cues should be considered together to understand fully the communication between host plants and Asian longhorned beetles.     

Wilson's Storm Petrels Oceanites oceanicus Recognise the Olfactory Signature of Their Mate

Chemical signals in birds have rarely been considered as recognition cues. Nevertheless, recent experiments showed that several petrel species are able to recognize their nest by smell, and in at least one species even their mate. But the use of smell may be different across the petrel species and olfactory nest recognition appears to be dependent on species’ breeding biology. To increase our knowledge of individual olfactory recognition in petrels and the relationships between breeding biology and use of smell, we tested Wilson’s storm petrels Oceanites oceanicus in Antarctica. In previous experiments, these birds failed to home if rendered anosmic, but the method employed to obtain anosmia (potentially stressing birds) and the fact that they breed in 24‐h daylight suggest that they might use visual, rather than olfactory, cues to recognize their nest. Our birds were tested in T‐maze experiments where nest odours or partner odours were presented. Wilson’s storm petrels preferred odours of their own nest and mate. Results on olfactory nest recognition confirm and complete previous results, viz. anosmic Wilson’s storm petrels do not home. Storm petrels olfactory mate recognition suggests that this ability may be widespread in burrowing petrels and implements olfactory nest recognition.     

Location and recognition of pups by adult female harp seals

Harp seal (Pagophilus groenlandicus) cows use visual, auditory and olfactory clues to locate and/or identify their pups. Identification is made at a close range and the pups are approached from a distance in a random manner. The topography of the ice supporting the pups changes frequently. These changes probably preclude or reduce the use of spatial memory by the adults. Because the pups cannot be identified at a distance, and because of the absence of stable landmarks, the adult must probably remain relatively close to her pup at all times. The large number of pups in the area suggests that random searching will not be efficient. The ability of various mammalian species to utilize spatial memory may well influence their modes of locating and identifying their young.     

Nursing Behavior in Mexican Free-tailed Bat Maternity Colonies

The nursing behavior of Mexican free-tailed bats (Tadarida brasiliensis mexicana) was examined in two large maternity cave roosts during six nursing seasons. After depositing pups in large creches, adults return to these creches two or more times daily to nurse. Densities, movements, and roosting associations of pups in creches were documented, and a night-vision device and infrared-sensitive video system were used to observe female-pup reunions and nursing affiliations. Densities of young (< 15 d) pups in creches averaged 4000 pups/m². Pups moved independently of one another between milk meals. Stable roosting associations among pups were absent, and females evidently could not predict where a given pup would be relocated. Upon returning to the creche, females searched for and relocated pups using vocal and olfactory cues. Experiments with marked individuals demonstrated that females nursed the same pups on subsequent nights. These same experiments indicated that female/pup recognition was mutual and that the pup participated in reunions by moving toward its putative mother. However, pups also attempted to suckle from other females and 35 instances of apparently successful milk “theft” were observed. Observed milk theft was insufficient to account for the frequency of alloparental nursing that was estimated independently using genotype tests. The high densities of bats within roosts and the lack of stable roosting associations among individuals argue against selection for shared nursing via kin selection and/or reciprocity. Errors in pup recognition, milk-dumping by females, and adoption by mothers whose own pup had died may occur, but high pup survival to weaning suggests that adoption is rare. The estimate of alloparental nursing obtained from genotype tests may be inflated as a result of increased opportunities for milk theft caused by our disturbance of adults. Current evidence suggests that energetic costs to females of alloparental nursing and searching for pups are compensated by mutualistic benefits obtained from aggregative roosting.     

Close-range, in-flight integration of olfactory and visual information by a host-seeking bark beetle

A long‐standing controversy questions whether foraging bark beetles assess the suitability of individual host trees using cues at close range while flying or engage in random landing followed by contact assessment. In most cases, visual discrimination mechanisms are ignored. We show that pheromone‐responding mountain pine beetles (MPB), Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae), can visually discriminate between ‘host’ (black) and ‘non‐host’ (white) traps arranged in small clusters, in the absence of additional host olfactory information, and that males (but not females) demonstrate a greater preference for combined host visual and olfactory cues. However, white, non‐host traps baited with a host volatile were as attractive as unbaited, black host traps. Our results support the hypotheses that when deciding to land, the MPBs integrate visual and olfactory information and can process cues in both sensory modes at relatively close range (≤2 m). Thus, host selection mechanisms in this species are unlikely to be random with respect to either sensory mode.     

Post-natal growth, mother-infant interactions and development of vocalizations in the vespertilionid bat Plecotus auritus

Female brown long-eared bats Plecotus auritus nurse their own young selectively. Choice experiments suggested that females recognized infants by using both olfactory and acoustic cues. Infant isolation calls (i-calls) showed individual variation, and vocal signatures allowed the females to recognize and suckle their own pup. As the pups grew, the i-calls increased in frequency and decreased in duration, and the i-calls appeared to change into orientation cries. Mothers were able to recognize recent calls of their own babies in preference to older calls. Echolocation sounds were distinguishable statistically between lactating females, and the behaviour of the babies during choice experiments suggested that in this species a mutual acoustic recognition occurs. The growth and development of wing shape in P. auritus are described.