Use of acoustic signals in Cape fur seal mother-pup reunions: individual signature, signal propagation and pup home range.

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.

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

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.

Mother-pup recognition mechanisms in Australia sea lion (Neophoca cinerea) using uni- and multi-modal approaches.

Communication is the process by which one emitter conveys information to one or several receivers to induce a response (behavioral or physiological) by the receiver. Communication plays a major role in various biological functions and may involve signals and cues from different sensory modalities. Traditionally, investigations of animal communication focused on a single sensory modality, yet communication is often multimodal. As these different processes may be quite complex and therefore difficult to disentangle, one approach is to first study each sensorial modality separately. With this refined understanding of individual senses, revealing how they interact becomes possible as the characteristics and properties of each modality can be accounted for, making a multimodal approach feasible. Using this framework, researchers undertook systematic, experimental investigations on mother-pup recognition processes in a colonial pinniped species, the Australian sea lion Neophoca cinerea. The research first assessed the abilities of mothers and pups to identify each other by their voice using playback experiments. Second, they assessed whether visual cues are used by both mothers and pups to distinguish them from conspecifics, and/or whether females discriminate the odor of their filial pup from those from non-filial pups. Finally, to understand if the information transmitted by different sensory modalities is analyzed synergistically or if there is a hierarchy among the sensory modalities, experiments were performed involving different sensory cues simultaneously. These findings are discussed with regards to the active space of each sensory cue, and of the potential enhancements that may arise by assessing information from different modalities.

Mutual mother-pup vocal recognition in the highly colonial Cape fur seal: evidence of discrimination of calls with a high acoustic similarity.

The Cape fur seal (Arctocephalus pusillus pusillus) is one of the most colonial mammal species in the world. Females exclusively nurse their pups for 9 to 11 months, during which they alternate frequent foraging trips at sea with suckling periods ashore. The survival of the pup thus depends on the ability of the mother-pup pair to relocate each other among thousands of individuals. Previous work has demonstrated identity information encoded in pup-attraction (PAC) and female-attraction (FAC) calls. Here, we investigated vocal recognition between mother and pup using playbacks of PAC and FAC performed during the breeding season at Pelican Point, Namibia. Both females and pups were able to specifically discriminate the voice of their pup or their mother from non-affiliated pup or mother. Females were able to memorize previous versions of their pup's calls (evidence of recognition up to 73 days after pup's calls recording). Vocal recognition was demonstrated in pups from 1- to 13-weeks old age. Females and pups did not respond differently to the non-filial or non-mother (for pups) stimulus even if it had a strong acoustic similarity with the filial or mother stimulus. This suggested that Cape fur seal mother-pup pairs have high perceptual and cognitive abilities, allowing individuals to identify kin's vocalizations in a very noisy and confusing environment.

Maternal responses to pup calls in a high-cost lactation species.

Bonding between mothers and their young is fundamental to mammalian reproductive behaviour and individual fitness. In social systems where the risk of confusing filial and non-filial offspring is high, mothers should demonstrate early, strong and consistent responses to their kin throughout the period of offspring dependence, irrespective of maternal traits. We tested this hypothesis through playback experiments in the northern elephant seal Mirounga angustirostris, a phocid species that breeds in high-density colonies. We found that mothers recognized their offspring throughout lactation and as early as 1-2 days after parturition. Measures of experience (age) and temperament (aggressivity) did not predict their response strength to filial playback treatments, nor did pup age or sex. Some mothers showed great consistency in behavioural responses throughout the lactation period, while others were less predictable. The strength of a female's response did not influence her pup's weaning weight; however, more consistent females weaned pups of higher mass. This is a rare demonstration of individual recognition among phocid mothers and their offspring, and suggests that consistency in maternal responsiveness may be an important social factor influencing the pup's growth and survival.

Feel the beat: cape fur seal males encode their arousal state in their bark rate.

The cape fur seal is one of the most colonial mammal species in the world. Breeding colonies are composed of harems held by mature males (older than 10 years) with up to 30 females and their pups, while roaming subadult males (younger and socially immature) are kept away from bulls' territories. As in other pinnipeds, cape fur seals are highly vocal and use acoustic signals in all their social interactions. Males produce barks-short vocalizations always produced in sequences-for territorial defense, mating behaviors, and agonistic interactions. These calls convey information about the sex, age class, and individual identity. This study investigated whether motivational cues such as the arousal state can be encoded in territorial males' barks and whether these cues are decoded by listening sub-adult males. The rate (number of calls per unit of time) and fundamental frequency of barks were found to significantly increase during high arousal state interactions (i.e., male-male confrontation) compared to spontaneous barks. Playback experiments revealed that subadult males responded with a higher level of vigilance when territorial males' barks had a faster bark rate. This mechanism of decoding the bulls' arousal state from barks will likely constitute an advantage for both bulls and the subadult males, by avoiding or reducing physical conflicts, and thereby reducing energy expenditure and the risk of injury. This study is the first experimental evidence of cape fur seals' using vocal rhythmic patterns to modulate their social interactions.

Chemical Profiles of Integumentary and Glandular Substrates in Australian Sea Lion Pups (Neophoca cinerea).

Recognition of individuals or classes of individuals plays an important role in the communication systems of many mammals. The ability of otariid (i.e., fur seal and sea lion) females to locate and identify their offspring in colonies after returning from regular foraging trips is essential to successful pup rearing. It has been shown that olfaction is used to confirm the identity of the pup by the mother when they reunite, yet the processes by which this chemical recognition occurs remain unclear. Using gas chromatography-mass spectrometry, we examined chemical profiles of integumentary and glandular secretions/excretions from pre- and post-molt Australian sea lion pups (Neophoca cinerea) and compared fur and swab samples to assess data collection methods. Multivariate statistics were applied to assess differences in chemical composition between body regions and sexes. We found differences among secretions from various body regions, driven by the distinctiveness of the oral odor mixture. The fine-scale trends in pre- and post-molt pups seem to differ due to changes in the behavior of pups and consequent decrease in the transfer of compounds among adjacent body regions in older pups. Volatile compounds from exocrine substrates were not distinct for different sexes. We also show that swab samples provide better data for exploring social olfaction than fur samples for this species. Obtaining fundamental chemical information, in this case chemical profiles of animals, and discerning differences in chemical composition is an important step toward fully exploring the intricacies of mother-offspring olfactory recognition and its underlying processes.

Geographic vocal variation and perceptual discrimination abilities in male Australian sea lions.

Vocal characteristics can vary among and within populations. In species with geographic variation in the structure of vocalizations, individuals may have the ability to discriminate between calls from local and non-local individuals. The ability to distinguish differences in acoustic signals is likely to have a significant influence on the outcome of social interactions between individuals, including potentially mate selection and breeding success. Pinnipeds (seals, fur seals, sea lions and walruses) are highly vocal yet the Australian sea lion (Neophoca cinerea) is the only eared seal known to show geographic vocal variation in male barks. Barks are produced in many social interactions and encode sufficient information for both individual and colony identity to be discriminable. Yet until now, whether males could themselves discriminate these bark differences was unclear. We performed playback experiments in four breeding colonies to investigate whether males can discriminate local from non-local barks. Overall, males responded more strongly to barks from their own colony compared to barks from other colonies regardless of whether those other colonies were close or distant. Competition for females is high in Australian sea lions, but mating periods are asynchronous across colonies. The ability to correctly assess whether a male is from the same colony, thus representing a potential competitor for mates, or merely a visitor from elsewhere, may influence how males interact with others. Given the high cost of fighting, the ability to discern competitors may influence the nature of male-male interactions and ultimately influence how they allocate reproductive effort.

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.

Behavioural response of Australian fur seals (Arctocephalus pusillus doriferus) to vessel noise during peak and off-peak human visitation.

Vessel traffic is the greatest contributor to marine anthropogenic noise pollution, and particularly affects species utilising coastal areas. Seal Rocks (Victoria), the largest Australian fur seal breeding colony, has a relatively small vessel exclusion zone during the pupping and breeding season, when vessel traffic is at its peak. It is necessary to understand the impacts of visitation at sensitive marine sites to ensure they are adequately protected from human disturbance. This study assessed the behavioural response of hauled-out Australian fur seals at Seal Rocks to controlled vessel noise exposure during peak and off-peak vessel visitation periods. High level noise exposure (76-80 dB) resulted in increased vigilance and interruption to vital behaviours in both peak and off-peak periods. These behavioural responses were limited to the period of noise exposure but are nevertheless indicative of disturbance. It is important to ensure regulations intended to protect sensitive sites are up-to-date and evidence based.

The response of sea turtles to vocalizations opens new perspectives to reduce their bycatch.

Incidental capture of non-target species poses a pervasive threat to many marine species, with sometimes devastating consequences for both fisheries and conservation efforts. Because of the well-known importance of vocalizations in cetaceans, acoustic deterrents have been extensively used for these species. In contrast, acoustic communication for sea turtles has been considered negligible, and this question has been largely unexplored. Addressing this challenge therefore requires a comprehensive understanding of sea turtles' responses to sensory signals. In this study, we scrutinized the avenue of auditory cues, specifically the natural sounds produced by green turtles (Chelonia mydas) in Martinique, as a potential tool to reduce bycatch. We recorded 10 sounds produced by green turtles and identified those that appear to correspond to alerts, flight or social contact between individuals. Subsequently, these turtle sounds-as well synthetic and natural (earthquake) sounds-were presented to turtles in known foraging areas to assess the behavioral response of green turtles to these sounds. Our data highlighted that the playback of sounds produced by sea turtles was associated with alert or increased the vigilance of individuals. This therefore suggests novel opportunities for using sea turtle sounds to deter them from fishing gear or other potentially harmful areas, and highlights the potential of our research to improve sea turtles populations' conservation.

Inter-site variability in the Cape fur seal's behavioural response to boat noise exposure.

The impact of man-made noise on wildlife is recognised as a major global concern affecting many taxa in both terrestrial and aquatic ecosystems, with the degree of impact varying among individuals or species. Understanding the factors inducing intra-species differences in response to noise is essential for the development of adapted and effective mitigation measures. This study compares the behavioural response of Cape fur seals to boat noise exposures at two study sites showing differences in their level of exposure to anthropogenic activities, and individual composition. Increased vigilance was found for Lambert's Bay seals exposed to high noise level (70-80 dB) compared to those tested at Cape Town harbour. Comparisons with a similar study performed in Namibia were made. Intrinsic factors such as individuals' age-class, sex or arousal state as well as extrinsic factors such as the ambient noise and the nature/extent of human-seal interactions were suggested to induce such variation.

First Description of the Underwater Sounds in the Mediterranean Monk Seal Monachus monachus in Greece: Towards Establishing a Vocal Repertoire.

The Mediterranean monk seal Monachus monachus is one of the most endangered pinnipeds in the world, and is classified as "Endangered" by the International Union for the Conservation of Nature. Any additional knowledge about the species is invaluable to its effective conservation. In the present study, we deployed an autonomous underwater recorder in an important reproductive area of the Mediterranean monk seal in Greece to describe its underwater vocal repertoire. Over the 330 h of continuous recordings, 9231 vocalizations were labelled as potentially produced by Mediterranean monk seals, and 1694 good quality calls were analyzed. We defined 18 call types divided into three main call categories: harmonic, noisy, and pulsative calls. We also described the soundscape in which this endangered species lives and found that human activities around the two main pupping caves had a strong impact on the sonic environment of these seals: the noise level produced by boat traffic was high, and occurred on an hourly (25 to 50 min/hour) and daily basis (10.8 to 16.9 h/day). Such high levels of noise might not only impair the communication of the species, but also impact its survival, as chronic noise can induce physiological stress.

Social calls in humpback whale mother-calf groups off Sainte Marie breeding ground (Madagascar, Indian Ocean).

Humpback whales (Megaptera novaeangliae) use vocalizations during diverse social interactions or activities such as foraging or mating. Unlike songs produced only by males, social calls are produced by all types of individuals (adult males and females, juveniles and calves). Several studies have described social calls in the humpback whale's breeding and the feeding grounds and from different geographic areas. We aimed to investigate for the first time the vocal repertoire of humpback whale mother-calf groups during the breeding season off Sainte Marie island, Madagascar, South Western Indian Ocean using data collected in 2013, 2014, 2016, and 2017. We recorded social calls using Acousonde tags deployed on the mother or the calf in mother-calf groups. A total of 21 deployments were analyzed. We visually and aurally identified 30 social call types and classified them into five categories: low, medium, high-frequency sounds, amplitude-modulated sounds, and pulsed sounds. The aural-visual classifications have been validated using random forest (RF) analyses. Low-frequency sounds constituted 46% of all social calls, mid-frequency 35%, and high frequency 10%. Amplitude-modulated sounds constituted 8% of all vocalizations, and pulsed sounds constituted 1%. While some social call types seemed specific to our study area, others presented similarities with social calls described in other geographic areas, on breeding and foraging grounds, and during migrating routes. Among the call types described in this study, nine call types were also found in humpback whale songs recorded in the same region. The 30 call types highlight the diversity of the social calls recorded in mother-calf groups and thus the importance of acoustic interactions in the relationships between the mother and her calf and between the mother-calf pair and escorts.

Characterizing the suckling behavior by video and 3D-accelerometry in humpback whale calves on a breeding ground.

Getting maternal milk through nursing is vital for all newborn mammals. Despite its importance, nursing has been poorly documented in humpback whales (Megaptera novaeangliae). Nursing is difficult to observe underwater without disturbing the whales and is usually impossible to observe from a ship. We attempted to observe nursing from the calf's perspective by placing CATS cam tags on three humpback whale calves in the Sainte Marie channel, Madagascar, Indian Ocean, during the breeding seasons. CATS cam tags are animal-borne multi-sensor tags equipped with a video camera, a hydrophone, and several auxiliary sensors (including a 3-axis accelerometer, a 3-axis magnetometer, and a depth sensor). The use of multi-sensor tags minimized potential disturbance from human presence. A total of 10.52 h of video recordings were collected with the corresponding auxiliary data. Video recordings were manually analyzed and correlated with the auxiliary data, allowing us to extract different kinematic features including the depth rate, speed, Fluke Stroke Rate (FSR), Overall Body Dynamic Acceleration (ODBA), pitch, roll, and roll rate. We found that suckling events lasted 18.8 ± 8.8 s on average (N = 34) and were performed mostly during dives. Suckling events represented 1.7% of the total observation time. During suckling, the calves were visually estimated to be at a 30-45° pitch angle relative to the midline of their mother's body and were always observed rolling either to the right or to the left. In our auxiliary dataset, we confirmed that suckling behavior was primarily characterized by a high average absolute roll and additionally we also found that it was likely characterized by a high average FSR and a low average speed. Kinematic features were used for supervised machine learning in order to subsequently detect suckling behavior automatically. Our study is a proof of method on which future investigations can build upon. It opens new opportunities for further investigation of suckling behavior in humpback whales and the baleen whale species.

Maritime traffic trends around the southern tip of Africa - Did marine noise pollution contribute to the local penguins' collapse?

The rapid increase in seaborn trade since the 1990s has resulted in an increase in vessel-derived noise pollution, yet there is little evidence linking these activities to a decline in many marine taxa, such as seabirds. Algoa Bay, South Africa, is a marine biodiversity hotspot, providing habitats for the largest populations of endangered African Penguins (Spheniscus demersus), as well as other endangered seabirds, cetaceans and seals. The bay is situated on a major shipping route and since 2016 has hosted the first offshore ship-to-ship (STS) bunkering operations in the country, i.e. the supplying of fuel from one ship to another outside of harbours. Using Automatic Identification System (AIS) data, we estimated noise emissions from vessels as a proxy for underwater ambient noise levels within the core penguin utilisation area. Frequency of vessels using the bay doubled during our study, with numbers of bulk carriers increasing ten-fold. Ambient underwater noise levels were generally high in the bay (ca 140 dB re 1 µPa since 2015) but significantly increased by 2 dB SPL after the initiation of STS bunkering in 2016, corresponding to double the underwater noise intensity. This increase coincided with a significant and dramatic decline by 85% in penguin numbers from St Croix Island since 2016. Algoa Bay is now one of the noisiest bays in the world. This is the first study to assess the potential impact of vessel-derived underwater noise levels on a seabird population. Penguins, like marine mammal species, are known to be sensitive to marine noise pollution and urgent management interventions are required to mitigate this recent disturbance, to preserve the remaining stronghold of the African penguin and the marine mammals' populations sharing the penguins' habitat.

Impact of Limited E-Health Literacy on the Overall Survival of Patients With Cancer.

PURPOSE: Digitalization of the health care system is transforming cancer patient care. Although many studies have investigated the determinants of a limited digital health literacy, the association between frailty factors and overall survival (OS) of these patients has never been assessed. METHODS: A retrospective noninterventional study included 15,244 adult patients with cancer diagnosed between January 1, 2015, and December 31, 2017, and treated at the Centre Léon Bérard. Limited e-health literacy was defined as the absence of an e-mail address in the electronic patient record. An Inverse Probability of Treatment-Weighted Kaplan-Meier estimate and a multivariate Cox proportional hazards model including interaction terms were used to adjust for confounding on measured covariates. RESULTS: In total, 15,244 adults with cancer were included: 55% women, with a median age of 62 years (19-103), and 35.5% had a metastatic disease. More than half (n = 8,771, 57.5%) had entered their e-mail address in their electronic patient record, and 4,020 (26.4%) opened their own patient portal. The median follow-up was 3.6 years (range: 0-6.8). Inverse Probability of Treatment-weighted Kaplan-Meier estimates showed a significantly better OS for patients with an e-mail address (P < .001). In multivariate analysis integrating interaction terms, male gender (hazard ratio [HR] = 1.27; 95% CI, 1.15 to 1.41; P < .001), older age (HR = 1.02; 95% CI, 1.02 to 1.03; P < .001), de novo metastatic setting (HR = 2.63; 95% CI, 2.47 to 2.79; P < .001), and no e-mail address (HR = 1.63; 95% CI, 1.33 to 2.00; P < .001) were significantly associated with worse OS. CONCLUSION: Our results support a strong association between the limited level of literacy and OS. A more in-depth study integrating variables such as socioeconomic level and location of residence would enrich these results.

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.

Note types and coding in Parid vocalizations: the chick-a-dee call of the boreal chickadee (Poecile hudsonicus).

An important first step in characterizing a vocalization is to classify, describe, and measure the elements of that vocalization. Here, this methodology is employed to study the chick-a-dee call of the boreal chickadee (Poecile hudsonicus). The note types (A, B, C, D, and D(h)) in a sample of boreal chickadee calls are identified and described, spectral and temporal features of each note type are analyzed, and production phenomena in each note type are identified and quantified. Acoustic variability is compared across note types and individuals to determine potential features used for note-type and individual discrimination. Frequency measures appear to be the most useful features for identifying note types and individuals, though total duration may also be useful. Call syntax reveals that boreal chick-a-dee calls follow a general rule of note-type order, namely A-B-C-D(h)-D, and that any note type in this sequence may be repeated or omitted. This work provides a thorough description of the boreal chickadee chick-a-dee call and will serve as a foundation for future studies aimed at elucidating this call's functional significance within this species, as well as for studies comparing chick-a-dee calls across Poecile species.