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Early onset of postnatal individual vocal recognition in a highly colonial mammal species

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Proceedings of the Royal Society B
Authors:
Mathilde Martin at University of Zurich
Mathilde Martin
Tess Gridley at University of Cape Town/ University of Stellenbosch
Tess Gridley
  • University of Cape Town/ University of Stellenbosch
Simon Elwen at Stellenbosch University
Simon Elwen
Isabelle Charrier at French National Centre for Scientific Research
Isabelle Charrier
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Abstract

Mother-young vocal recognition is widespread in mammals. The features of vocal recognition are known to be shaped by the ecological constraints faced by each species. In some species, a rapid establishment of mother-young vocal recognition is crucial for offspring's survival. However, knowledge of the precise features of this recognition system, especially the timing of the onset in the first hours after birth, is often lacking. Here we show that Cape fur seal females can recognize their pup's voice 2-4 h after parturition and that pups develop this aptitude 4-6 h after birth. This study is the first to investigate this mechanism in a wild and free-ranging mammal from only 2 h after birth. We report the fastest establishment of mother-young vocal recognition for any mammalian species, including humans, described to date. Such early vocal identification in pups suggests an in utero vocal imprinting. These findings highlight the synergistic role of environmental constraints and biological traits in optimizing the timing of individual vocal recognition onset in vertebrates.
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Research
Cite this article: Martin M, Gridley T, Elwen
S, Charrier I. 2022 Early onset of postnatal
individual vocal recognition in a highly colonial
mammal species. Proc. R. Soc. B 289:
20221769.
https://doi.org/10.1098/rspb.2022.1769
Received: 7 September 2022
Accepted: 7 November 2022
Subject Category:
Behaviour
Subject Areas:
behaviour, cognition
Keywords:
acoustic communication, vocal recognition,
ontogeny, parent–offspring communication,
pinnipeds, cape fur seal
Authors for correspondence:
Mathilde Martin
e-mail: mathilde.martin@universite-paris-
saclay.fr
Isabelle Charrier
e-mail: isabelle.charrier@cnrs.fr
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.6296380.
Early onset of postnatal individual vocal
recognition in a highly colonial mammal
species
Mathilde Martin
1,2
, Tess Gridley
2,3
, Simon Elwen
2,3
and Isabelle Charrier
1
1
Institut des Neurosciences Paris-Saclay, CNRS, Université Paris-Saclay, UMR 9197, 91400 Saclay, France
2
Sea Search Research and Conservation NPC, 4 Bath Road, Muizenberg, Cape Town 7945, South Africa
3
Department of Botany and Zoology, Faculty of Science, Stellenbosch University, Stellenbosch 7605, South Africa
MM, 0000-0002-9314-4729; IC, 0000-0003-4873-2342
Mother–young vocal recognition is widespread in mammals. The features of
vocal recognition are known to be shaped by the ecological constraints faced
by each species. In some species, a rapid establishment of mother–young
vocal recognition is crucial for offspring’s survival. However, knowledge
of the precise features of this recognition system, especially the timing of
the onset in the first hours after birth, is often lacking. Here we show that
Cape fur seal females can recognize their pup’s voice 2–4 h after parturition
and that pups develop this aptitude 4–6 h after birth. This study is the first to
investigate this mechanism in a wild and free-ranging mammal from only
2 h after birth. We report the fastest establishment of mother–young vocal
recognition for any mammalian species, including humans, described to
date. Such early vocal identification in pups suggests an in utero vocal
imprinting. These findings highlight the synergistic role of environmental
constraints and biological traits in optimizing the timing of individual
vocal recognition onset in vertebrates.
1. Introduction
In most mammals, only the mother provides care to the offspring. Mother–
young individual recognition is a significant way to optimize maternal invest-
ment. It reduces costs by avoiding misdirected care and thus enhances mothers’
reproductive success and increases offspring’s chances of survival [1]. In many
mammal species, the acoustic channel plays a major role in this recognition pro-
cess as mother and young develop the ability to identify each other through the
vocal signals (i.e. vocalizations) they produce [2–8]. Although the occurrence of
individual vocal recognition has been well documented in mammals, some fea-
tures such as the timing of the onset of recognition, its temporal pattern
throughout lifetime and the individual signature are not well understood and
rarely investigated in wild mammals [9,10].
Rapid establishment of recognition between the mother and her young is
crucial to ensure the survival of the young, particularly in species experiencing
stringent ecological constraints such as a high risk of confusion between indi-
viduals, early pup mobility and early separations between mother and young
due to foraging needs. Experimentally testing the development of the vocal rec-
ognition in mother–young pairs of wild mammals within the first hours after
birth is challenging for reasons of access to the animals, tracking of births
and the ability to conduct experiments. Only a few studies have been carried
out so far, involving five domestic [11–15] and five wild species [3,16–19] (pin-
niped species only). In most cases, individuals were tested from a few days after
birth (i.e. later than 24–48 h), except in sheep (Ovis aries) for which ewes and
lambs were tested within 6–12 h after parturition [12] and for female Australian
sea lions (Neophoca cinerea), which were tested within 12 h after parturition [16].
The timing in development of vocal recognition, especially in the first 24 h after
birth, is thus poorly understood in mammals, including humans [2,20].
© 2022 The Author(s) Published by the Royal Society. All rights reserved.
... Experimental investigations confirmed a mutual mother-pup vocal recognition (Martin et al., 2022b). Such recognition is established remarkably early after the pup's birth: females recognise their pup's calls between 2 and 4 h after parturition and pups develop this ability when they are 4 to 6 h old (Martin et al., 2022a). Two aspects of the mother-pup vocal recognition process remain to be studied in this species: (1) the propagation of PACs and FACs as well as the reliability of the individual information transmission, and (2) the decoding process of the individual identity. ...
... As some tested pups were young (six were 6 days old or less), the behavioural response of pups was evaluated through their vocal production only. Indeed, newborn pups are not able to locate the sound source accurately and do not look towards the loudspeaker or approach it during playback experiments (Martin et al., 2022a). Response variables for pups were thus latency to call (s) and number of calls. ...
... Similar to what was done for a study on Cape fur seal mother-pup vocal recognition (Martin et al., 2022a), the overall behavioural response of each tested individual was obtained by combining the raw data of the response variables (four for mothers and two for pups) in a principal component analysis (PCA). This method allows us to obtain a composite score (McGregor, 1992) and facilitate the interpretation of the behavioural response of tested individuals to playback series. ...
Use of acoustic signals in Cape fur seal mother-pup reunions: individual signature, signal propagation and pup home range
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The Cape fur seal (Arctocephalus pusillus pusillus) is one of the most colonial mammals, with colonies of up to hundreds of thousands of individuals during the breeding season. During the lactation period, mothers and pups are regularly separated as females undertake multi-day foraging trips at sea. Mothers and pups use a mutual vocal recognition system to reunite after separation. Such communication is highly constrained by both high background noise and risk of individual confusion owing to the density of seals. This study aimed to experimentally assess the acoustic features relevant for mother–pup vocal identification and the propagation properties of their calls. Playback experiments revealed that mother and pup individual vocal signatures rely on both temporal and frequency parameters: amplitude and frequency modulations, timbre and fundamental frequency (f0). This is more parameters than in any colonial species studied so far. The combinational use of acoustic features reinforces the concept that both environmental and social constraints may have acted as selective pressures on the individual vocal recognition systems. Theoretical propagation distances of mother and pup vocalisations were estimated to be below the range of distances at which mother–pup reunions can occur. This suggests that Cape fur seals may have strong abilities to extract vocal signals from the background noise, as previously demonstrated in the highly colonial king penguin. Investigating the transmission of information throughout the propagation of the signal as well as the ability of the receiving individual to decipher vocal signatures is crucial to understanding vocal recognition systems in the wild.
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... Social interactions require communication among partners, and acoustic signaling is one such mode of communication that is pervasive among animals, where it serves diverse social roles ranging from the maintenance of territorial boundaries 8 to group cohesion 9 and many others 10 . It is therefore a useful context to understand how social interactions give rise to social structure in animal populations 11 . ...
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House mice (Mus musculus domesticus) are among the most widely studied laboratory models of mammalian social behavior, yet we know relatively little about the ecology of their behaviors in natural environments. Here, we address this gap using radiotelemetry to track social interactions in a population of wild mice over 10 years, from 2013 to 2023, and interpret these interactions in the context of passive acoustic monitoring data collected from August 2022 until November 2023. Using deep convolutional neural networks, we identify 1.3 million individual vocalizations and align them in time with continuously collected telemetry data recording social interactions between individually identifiable mice. We find that vocalization is seasonal and correlated with long-term dynamics in features of social groups. In addition, we find that vocalization is closely associated in time with entrances to and exits from those groups, occurs most often in the presence of pups, and is correlated with how much time pairs of mice spend together. This work identifies seasonal patterns in the vocalizations of wild mice and lays a foundation to investigate the social role of acoustic communication in wild populations of a classic laboratory model organism.
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... Early establishment of mother-offspring vocal recognition is essential for the survival of a young. Many researchers reported the fastest establishment of mother-young vocal recognition for any mammalian species, including humans, in Cape fur seal females and their pups voice 2-4 h after parturition and that pups develop this aptitude 4-6 h after birth 34,36 . Such early vocal identification in pups suggests vocal imprinting. ...
Mother -offspring vocal communication: A Review
Article
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  • Jan 2024
Parental care is one of the most important behaviour found in animals which ensures the safety of the new born offspring and also increases the chances of survival. Contact calls between mother and offspring are of various types and depend on the conditions they are in. Mother always takes care of its child even when the animals live in a huge group. A mother animal can never forget the vocalization of its offspring and can distinguish the acoustic signals of its own offspring from others. The young ones can also recognize the acoustic signals produced by their mother. Significant researches in the field of mother-offspring sound communication of different animal species published between 2000-2023 have been cited in this paper. Studies related to the mother-offspring communication may help in understanding the maternal behaviour of different animals and how bioacoustics aid animals to take care of their young ones.
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... Bottlenose dolphins use their learned whistles in matching interactions to address each other for affiliative purposes (Janik 2000;Chereskin et al. 2022). In other species, such as seals, where rapid mother-young social recognition is crucial for offspring survival, postnatal individual vocal recognition can occur within hours (Martin et al. 2022). The highly organized social structure of the naked mole rat is maintained using the social transmission of vocal dialects (Barker et al. 2021). ...
Context-dependent activation of a social behavior brain network during learned vocal production
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Full-text available
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Neural activation in brain regions for vocal control is social context dependent. This context-dependent brain activation reflects social context-appropriate vocal behavior but has unresolved mechanisms. Studies of non-vocal social behaviors in multiple organisms suggest a functional role for several evolutionarily conserved and highly interconnected brain regions. Here, we use neural activity-dependent gene expression to evaluate the functional connectivity of this social behavior network within zebra finches in non-social and social singing contexts. We found that activity in one social behavior network region, the medial preoptic area (POM), was strongly associated with the amount of non-social undirected singing in zebra finches. In addition, in all regions of the social behavior network and the paraventricular nucleus (PVN), a higher percentage of EGR1 expression was observed during a social female-directed singing context compared to a non-social undirected singing context. Furthermore, we observed distinct patterns of significantly correlated activity between regions of the social behavior network during non-social undirected and social female-directed singing. Our results suggest that non-social vs. social contexts differentially activate this social behavior network and PVN. Moreover, neuronal activity within this social behavior network, PVN, and POM may alter context-appropriate vocal production.
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... Bottlenose dolphins use their learned whistles in matching interactions to address each other for a liative purposes (Janik 2000;Chereskin et al. 2022). In other species, such as seals, where rapid mother-young social recognition is crucial for offspring survival, postnatal individual vocal recognition can occur within hours (Martin et al. 2022). The highly organized social structure of the naked mole rat is maintained using the social transmission of vocal dialects (Barker et al. 2021). ...
Context-dependent activation of a social behavior brain network associates with learned vocal production
Preprint
Full-text available
  • Feb 2023
In zebra finches, an avian brain network for vocal control undergoes context-dependent patterning of song-dependent activation. Previous studies in zebra finches also implicate the importance of dopaminergic input in producing context-appropriate singing behavior. In mice, it has been shown that oxytocinergic neurons originated in the paraventricular nucleus of the hypothalamus (PVN) synapse directly onto dopamine neurons in the ventral tegmental area (VTA), implicating the necessity of oxytocin signaling from the PVN for producing a context-appropriate song. Both avian and non-avian axonal tract-tracing studies indicate high levels of PVN innervation by the social behavior network. Here, we hypothesize that the motivation for PVN oxytocin neurons to trigger dopamine release originates in the social behavior network, a highly conserved and interconnected collection of six regions implicated in various social and homeostatic behaviors. We found that expression of the neuronal activity marker EGR1 was not strongly correlated with song production in any of the regions of the social behavior network. However, when EGR1 expression levels were normalized to the singing rate, we found significantly higher levels of expression in the social behavior network regions except the medial preoptic area during a social female-directed singing context compared to a non-social undirected singing context. Our results suggest neuronal activity within the male zebra finch social behavior network influences the synaptic release of oxytocin from PVN onto dopaminergic projection neurons in the VTA, which in turn signals to the vocal control network to allow for context-appropriate song production.
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Individual vocal recognition (IVR) has been well studied in mammals and birds. These studies have primarily delved into understanding IVR in specific limited contexts (e.g. parent–offspring and mate recognition) where individuals discriminate one individual from all others. However, little research has examined IVR in more socially demanding circumstances, such as when an individual discriminates all individuals in their social or familial group apart. In this review, we describe what IVR is and suggest splitting studies of IVR into two general types based on what questions they answer (IVR-singular, and IVR-multiple). We explain how we currently test for IVR, and many of the benefits and drawbacks of different methods. We address why IVR is so prevalent in the animal kingdom, and the circumstances in which it is often found. Finally, we explain current weaknesses in IVR research including temporality, specificity, and taxonomic bias, and testing paradigms, and provide some solutions to address these weaknesses. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.
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Mother–Offspring Vocal Recognition and Social System in Pinnipeds
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  • Mar 2020
In many species, parents and offspring have developed the ability to vocally identify each other. In avian species, a strong relationship between individual recognition system and social structure has been shown, with recognition systems being more elaborated in species exposed to strong selective pressures (e.g., colonial species vs. solitary species). Pinnipeds (seals, fur seals, sea lions, and walrus) are an excellent mammalian clade model for comparative studies of individual vocal recognition as they present a high diversity in both their social structures and breeding systems, and they use vocal signals in all their social interactions. The investigation of mother–pup vocal recognition systems demonstrates some clear evidence that pinniped species with the highest selective pressures for mother–pup recognition have developed the most complex recognition system. Indeed, such species show a high index of vocal stereotypy (IVS), a rapid onset of vocal recognition, a multi-parametric vocal signature mainly based on temporal analysis whereas species living in less constraining environments show a moderate to low IVS, a delayed onset of vocal recognition, a multi-parametric signature mainly based on a frequency analysis. Our understanding on how ecological and social constraints drive communication systems in vertebrates is essential. Our current knowledge on different taxa show that species encountering similar constraints for individual recognition has developed similar communication systems, suggesting common communication strategies in vertebrates.
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