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

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.

Keywords: acoustic communication; cape fur seal; ontogeny; parent–offspring communication; pinnipeds; vocal recognition.

Figure 1.

Behavioural responses of mothers and pups to playback experiments conducted to assess the timing of the onset of the mother–pup vocal recognition. (a) Playback experiments set-up. Each tested individual was exposed to the broadcast of two series of calls from a related individual (mother or filial pup) or a stranger individual (non-mother or non-filial pup). (b) General behavioural response of mothers (n_ind = 38) to playback trials (n_trials = 59) conducted from 2–4 h to 12–24 h following parturition. Mothers' response is indicated by the composite score (PC1 scores) obtained from six behavioural variables. (c) General behavioural response of pup (n_ind = 36) to playback trials (n_trials = 57) conducted from 2–4 h to 24–48 h following birth. Pups’ response is indicated by the composite score (PC1 scores) obtained from two behavioural variables. LME followed by a post hoc analysis of estimated marginal means. Significance code is p-value [0, 0.001]: ***, (0.001, 0.01]: **, (0.01, 0.05]: *, (0.05, 1]: NS. Boxplots present median values with first and third quartiles (lower and upper hinges) and whiskers represent the min and max values.

Figure 2.

Link between mothers' and pups’ behavioural responses to playback trials conducted at 2–4 h after birth and their vocal activity during the first 2 h postpartum. (a) Relationship between pups' vocal activity during the first 2 h after birth (in number of calls produced per 10 min) and the difference in their mother's behavioural response to the filial and non-filial playback series broadcasted 2–4 h after parturition (PC1 scores filial – PC1 scores non-filial). (b) Relationship between mothers' vocal activity during the first 2 h postpartum and their behavioural response to the filial series (PC1 scores filial, in purple) and the non-filial series (PC1 scores non-filial, in grey). (c) Spectrograms of calls produced by a female (m44) showing a high vocal activity (average call rate = 55.9 calls/10 min) during recordings made within 2 h after parturition. (d) Relationship between mothers' vocal activity during the first 2 h after parturition (in number of calls produced per 10 min) and the difference in their pup's behavioural response to the mother and non-mother playback series broadcasted 2–4 h after birth (PC1 scores mother – PC1 scores non-mother). (e) Relationship between pups' vocal activity during the first 2 h after birth and their behavioural response to the mother (PC1 scores mother, in orange) and the non-mother series (PC1 scores non-mother, in grey). (f) Spectrograms of calls produced by a pup (p66) showing a high vocal activity (average call rate = 220.7 calls/10 min) during recordings made within 2 h after birth.