This research project into mother-pup communication in Australian sea lions (Neophoca cinerea) is a collaboration between the Marine Predator Research Group at Macquarie University, Australia and the Bioacoustics Team at CNRS, France. I began working on this research during my doctoral studies and was jointly supervised by Rob Harcourt at Macquarie University, and Isabelle Charrier and Thierry Aubin at Universite Paris Sud 11, CNRS France.
The project is now a CNRS International Associated Laboratories project linking collaborators from 7 international institutions. We are building on many of the findings from my PhD work to develop a comprehensive model of parent-offspring multimodal communication in mammals.
Background
Pinnipeds (seals, fur seals, sea lions and walrus) provide an excellent opportunity to examine the variation in pressures affecting the evolution of recognition behaviour within a single, relatively homogeneous taxa. Parent-offspring recognition in pinnipeds has been well described, but only experimentally examined in a small number of species. Mother-offspring recognition is likely to be favoured in those species of pinnipeds, particularly the otariids, which breed in colonies and where pups are not always with their mothers. Factors such as the length of maternal care, breeding colony density and maternal feeding strategy are likely selective pressures shaping individual recognition systems.
The Australian sea lion (Neophoca cinerea) is an endemic Australian otariid, that lives along the southern and south-western coasts of mainland Australia. They exhibit a breeding biology that is unique among pinnipeds; a 17 to 18 month breeding cycle, a pupping season lasting for approximately five to nine months, and a perinatal attendance period of 6-14 days during which the mother will fast in the colony while suckling her young, before returning to the sea to forage. This unique breeding biology may provide insights into the evolutionary pressures driving individual recognition by allowing comparisons with other pinniped species.
Preliminary observations suggested that multi-modal signalling is used during reunions, especially vocal, olfactory and visual signals and initial analysis of mother and pup vocalisations showed individual stereotypy, potentially used for recognition (Charrier and Harcourt, 2006).
My research examined three of the sensory channels potentially used by sea lions during reunions (auditory, visual and olfactory). By using playback experiments, manipulations and model prompts I examined these channels and how they interact, to understand the role of multi-modal signals in mother-pup reunions.
Australian sea lions display mutual mother-offspring recognition. The development of recognition and the individual vocal signatures involved suggest that the Australian sea lion is under a moderate level of selection for individual recognition. This selection is likely to come from the moderate colony densities in which they live and breed. The results suggest that while visual signals can be used in the recognition process at mid-range, acoustic signals are the most reliable cues at both long and short range. In addition, olfactory signals play a key role at close range for the final acceptance or rejection of pups. The multimodal individual recognition system of Australian sea lions is therefore adapted to their unique lifestyle.
This in-depth study of multi-modal signalling in Australian sea lions helps to explain the processes involved in recognition in pinnipeds, and the selection pressures imposed by their breeding biology, while for the first time providing a complete mammalian model of multi-modal communication.
Vocal Recognition
My Research has shown that in Australian sea lions mother-pup recognition is mutual with both parties being able to identify the other’s voice. However the onset of recognition varies between mothers and pups. Mothers recognise their pups rapidly, within two days of birth, but pups do not recognize their mother’s voice until after the end of the perinatal attendance period. Despite this slow onset, pups reliably identify their mother’s voice, and can do so at least two years after weaning. In both mothers and pups vocalizations are highly individually stereotyped potentially providing many cues as to the identity of the caller. These potential cues include amplitude and frequency modulation, exact frequency value and spectral energy distribution parameters. Experimental analysis of pup responses to their mother’s voice has revealed that they use both amplitude and frequency modulations as well as the exact frequency values of the vocalization when identifying the mother. Similar analysis of maternal responses to pup vocalizations has shown that mothers rely on the pattern of amplitude modulations and the exact frequencies contained within the call, but not the frequency modulations. Mothers also need multiple frequency bands to perform discriminations and it appears that the pups vocal signature is contained in the, potentially more stable, first half of their call. Further, when compared to other vertebrates this vocal signature appears to be of moderate complexity and is likely to be due to selection pressures imposed by the environment and the species’ ecology.
Long Term Memory in Australian Sea Lions
Playback of maternal calls to pups two years after weaning has shown that pups retain the ability to recognize their mothers’ calls even when they are independent of her. It is likely that this long-term memory is a by-product of the intense selection for vocal identification and memory in this species. While pups are dependant a failure to reunite with their mother or soliciting food from the wrong female could lead to injury, starvation and death.
Olfactory Recognition
Despite anecdotal observations in many species of pinnipeds that olfactory investigation was involved in the recognition process, there had been no experimental investigation of individual olfactory recognition in pinnipeds. I performed a novel experiment in which wild females were presented with a choice of two models impregnated with the scent of their own and a non-filial pup. Nine out of ten females spent more time investigating the model impregnated with the scent of their own pup than the model with a non-filial pup’s scent. This study provides unequivocal evidence that females can identify their pup’s scent in the absence of any other cues.
Olfactory choice test
Allosuckling Behaviour
Despite the presence of a multimodal individual recognition system Australian sea lions still occasionally engage in allosuckling, or provisioning non-filial young. Prior to this study, previous authors had described allosuckling as only occurring when a mother had lost her own young. During my research I observed allosuckling to occur in a variety of contexts and suggest that while rare, allosuckling is likely to occur in a situation in which recognition is absent or not yet developed.
Related Publications
Pitcher, B.J., Charrier, I., Harcourt, R.G. 2015. Chemical fingerprints reveal clues to identity, heterozygosity, and relatedness. Proceedings of the National Academy of Sciences USA doi: 10.1073/pnas.1514278112
Pitcher, B.J., Harcourt, R.G., Charrier, I. 2012. Individual identity encoding and environmental constraints in vocal recognition of pups by Australian sea lion mothers. Animal Behaviour
Pitcher, B.J., Ahonen, H., Charrier, I., Harcourt, R.G. 2011. Allosuckling behaviour in the Australian sea lion (Neophoca cinerea): An updated understanding. Marine Mammal Science 27 (4): 881-888
Pitcher, B.J., Harcourt, R.G., Schaal, B., Charrier, I. 2011. Social olfaction in marine mammals: wild female Australian sea lions can identify their pup’s scent. Biology Letters 7: 60-62
Pitcher, B.J., Harcourt, R.G., Charrier, I. 2010. Rapid onset of maternal vocal recognition in a colonially breeding mammal, the Australian sea lion. PLoS One 5: e12195
Pitcher, B.J., Harcourt, R.G., Charrier, I. 2010. The memory remains: Long-term vocal recognition in Australian sea lions. Animal Cognition 13: 771-776.
Attard, M.R.G., Pitcher, B.J., Charrier, I., Ahonen, H., Harcourt, R.G. 2010. Vocal discrimination in mate guarding male Australian sea lions: familiarity breeds contempt. Ethology 116: 704-712
Pitcher, B.J., Ahonen, H., Harcourt, R.G., Charrier, I. 2009. Delayed onset of vocal recognition in Australian sea lion pups (Neophoca cinerea). Naturwissenschaften 96: 901-909.
Charrier, I., Pitcher, B.J., Harcourt, R.G. 2009. Vocal recognition of mothers by Australian sea lion pups: individual signature and environmental constraints. Animal Behaviour 78: 1127-1134.
Conference Presentations
Pitcher, BJ, Harcourt, RG and Charrier I. Individual olfactory recognition of pups by wild female Australian sea lions (Neophoca cinerea).
18th Biennial Conference of the Society for Marine Mammalogy (2009). Quebec, Canada.
Pitcher, BJ, Harcourt, RG and Charrier I. Ecological influences shaping mother-pup recognition in Australian sea lions.
10th International Mammalogical Congress (2009). Mendoza, Argentina.
Pitcher, BJ, Harcourt, RG and Charrier I. Delayed onset of vocal recognition in Australian sea lion pups (Neophoca cinerea).
Vocal Communication in Birds and Mammals (2008). St Andrews, Scotland.
Pitcher, BJ, Harcourt, RG and Charrier I. Delayed onset of vocal recognition in Australian sea lion pups (Neophoca cinerea).
Acoustic Communication by Animals (2008). Corvalis, USA.
Pitcher BJ, Charrier, I and Harcourt, RG. Whos your mother? Individual recognition in the Australian sea lion.
5th Conference of the Australasian Evolution Society (2007). Sydney, Australia.
Benjamin PITCHER 