Contextual and combinatorial structure in sperm whale vocalisations.

Sperm whales (Physeter macrocephalus) are highly social mammals that communicate using sequences of clicks called codas. While a subset of codas have been shown to encode information about caller identity, almost everything else about the sperm whale communication system, including its structure and information-carrying capacity, remains unknown. We show that codas exhibit contextual and combinatorial structure. First, we report previously undescribed features of codas that are sensitive to the conversational context in which they occur, and systematically controlled and imitated across whales. We call these rubato and ornamentation. Second, we show that codas form a combinatorial coding system in which rubato and ornamentation combine with two context-independent features we call rhythm and tempo to produce a large inventory of distinguishable codas. Sperm whale vocalisations are more expressive and structured than previously believed, and built from a repertoire comprising nearly an order of magnitude more distinguishable codas. These results show context-sensitive and combinatorial vocalisation can appear in organisms with divergent evolutionary lineage and vocal apparatus.

Passive acoustic monitoring of sperm whales and anthropogenic noise using stereophonic recordings in the Mediterranean Sea, North West Pelagos Sanctuary.

A total of 147 days spread over 4 years were recorded by a stereophonic sonobuoy set up in the Mediterranean sea, near the coast of Toulon, south of France. These recordings were analyzed in the scope of studying sperm whales (Physeter macrocephalus) and the impact anthropic noises may have on this species. With the use of a novel approach, which combines the use of a stereophonic antenna with a neural network, 226 sperm whales' passages have been automatically detected in an effective range of 32 km. This dataset was then used to analyze the sperm whales' abundance, the background noise, the influence of the background noise on the acoustic presence, and the animals' size. The results show that sperm whales are present all year round in groups of 1-9 individuals, especially during the daytime. The estimated density is 1.69 whales/1000 km[Formula: see text]. Animals were also less frequent during periods with an increased background noise due to ferries. The animal size distribution revealed the recorded sperm whales were distributed in length from about 7 to 15.5 m, and lonely whales are larger, while groups of two are composed of juvenile and mid-sized animals.

Changes in the acoustic activity of beaked whales and sperm whales recorded during a naval training exercise off eastern Canada.

Experimental research has shown that beaked whales exhibit strong avoidance reactions to naval active sonars used during antisubmarine warfare training exercises, including cessation of echolocation and foraging activity. Behavioural responses to sonar have also been linked to strandings and mortality. Much of the research on the responses of beaked whales and other cetaceans to naval active sonar has occurred on or near U.S. naval training ranges, and the impacts of sonar in other regions remain poorly understood, particularly as these impacts, including mortality, are likely to go unobserved in offshore areas. In September 2016 the multinational naval exercise 'CUTLASS FURY 2016' (CF16) was conducted off eastern Canada. We used passive acoustic recordings collected in the region to quantify the occurrence and characteristics of sonar signals, measure ambient noise levels, and assess changes in the acoustic activity of beaked and sperm whales. The number of hours per day with echolocation clicks from Cuvier's beaked whales and sperm whales were significantly reduced during CF16, compared to the pre-exercise period in 2016 (sperm whales) and to control data from 2015 (both species). Clicks from an unidentified Mesoplodont beaked whale species, sporadically detected prior to CF16, were absent during the exercise and for 7 days afterward. These results suggest that beaked and sperm whales ceased foraging in the vicinity of CF16 and likely avoided the affected area. Such disturbance may have energetic, health, and fitness consequences.

Towards a better characterisation of deep-diving whales' distributions by using prey distribution model outputs?

In habitat modelling, environmental variables are assumed to be proxies of lower trophic levels distribution and by extension, of marine top predator distributions. More proximal variables, such as potential prey fields, could refine relationships between top predator distributions and their environment. In situ data on prey distributions are not available over large spatial scales but, a numerical model, the Spatial Ecosystem And POpulation DYnamics Model (SEAPODYM), provides simulations of the biomass and production of zooplankton and six functional groups of micronekton at the global scale. Here, we explored whether generalised additive models fitted to simulated prey distribution data better predicted deep-diver densities (here beaked whales Ziphiidae and sperm whales Physeter macrocephalus) than models fitted to environmental variables. We assessed whether the combination of environmental and prey distribution data would further improve model fit by comparing their explanatory power. For both taxa, results were suggestive of a preference for habitats associated with topographic features and thermal fronts but also for habitats with an extended euphotic zone and with large prey of the lower mesopelagic layer. For beaked whales, no SEAPODYM variable was selected in the best model that combined the two types of variables, possibly because SEAPODYM does not accurately simulate the organisms on which beaked whales feed on. For sperm whales, the increase model performance was only marginal. SEAPODYM outputs were at best weakly correlated with sightings of deep-diving cetaceans, suggesting SEAPODYM may not accurately predict the prey fields of these taxa. This study was a first investigation and mostly highlighted the importance of the physiographic variables to understand mechanisms that influence the distribution of deep-diving cetaceans. A more systematic use of SEAPODYM could allow to better define the limits of its use and a development of the model that would simulate larger prey beyond 1,000 m would probably better characterise the prey of deep-diving cetaceans.

Behaviour and vocalizations of two sperm whales (Physeter macrocephalus) entangled in illegal driftnets in the Mediterranean Sea.

Illegal driftnetting causes each year several entanglements and deaths of sperm whales in different Mediterranean areas, primarily in the Tyrrhenian Sea. In summer 2020, during the June-July fishing season, two sperm whales were found entangled in illegal driftnets in the Aeolian Archipelago waters, Southern Italy. These two rare events were an exceptional chance to collect behavioural and acoustics data about entangled sperm whales. We analysed 1132 one-minute sets of breathing/behavioural data and 1575 minutes of acoustic recording, when the whales were found entangled, during the rescue operation, immediately after release, and in the days thereafter. The first whale was generally quiet showing a general status of debilitation/weakness, numerous skin lesions, and low breathing rate (0.31 (0.60)); it collaborated during rescue operations. On the contrary, the second whale showed a high level of agitation with a high breathing rate (1.48 (1.31)) during both the entanglement period and the net cutting operations, vigorously moving its fluke and pectoral fins, opening its mouth, sideway rolling or side fluking and frequently defecating. Acoustically, the first whale produced mainly single clicks in all phases except for two series of creaks during rescuing operations while the second whale produced a wide range of vocalizations (single clicks, likely either slow clicks or regular clicks, creaks, and codas). Our observations indicate that acoustics, respiratory and behavioural parameters may be useful to monitor the physical/physiological status of sperm whales during disentanglement operations.

Trumpet sounds emitted by male sperm whales in the Mediterranean Sea.

Sperm whale trumpets are sounds only occasionally documented, with a well recognisable and stereotyped acoustic arrangement. This study investigated the acoustic features of the trumpets and the context in which these sounds were recorded, using acoustic data collected over 22 years, in the Pelagos Sanctuary area (North-Western Mediterranean Sea). Analysed trumpets (n = 230), recorded at the beginning of a dive after the whale fluke-up, comprised a series of acoustic units organized in short sequences. Acoustic parameters were derived for the entire trumpet and for each distinguishable unit in a trumpet. Overall, trumpet durations and their initial frequencies were higher in recordings collected when multiple whales were visually or acoustically detected in the observation area. The identity of 68 whales was assessed through photo-identification, with 29 individuals producing trumpets within and between years. The variability of the acoustic parameters appeared to be higher within the same individuals rather than between different individuals, suggesting an individual plasticity in composing and arranging units in a trumpet. Different click patterns were observed before and after the trumpets, with more complex sequences when (1) other whales were visually/acoustically detected, and (2) individuals were in suitable foraging sites (i.e., canyon areas). Trumpets were commonly followed or preceded by click patterns suited for communication, such as codas and/or slow clicks. Significant relations between the trumpet emission and the male-only long-range communication click pattern (i.e. slow clicks) emerged, supporting the hypothesis that a trumpet is a sound emitted by maturing/mature males in feeding grounds. This study provides the first evidence that trumpets were conserved in the sperm whale acoustic repertoire at the decadal timescale, persisting across years and individuals in the same area. This persistence may be functionally specific to foraging activities performed by males in a well-established feeding area.

Long-term associations among male sperm whales (Physeter macrocephalus).

Little is known about the social structure of male sperm whales (Physeter macrocephalus) after they leave their natal units. While previous studies found no evidence for preferred associations among males, the observation of mass-strandings consisting exclusively of males, suggest that they have strong social bonds. To investigate the social associations among male sperm whales, we used half weight index of association, permutation tests and standardized lagged association rate models on a large photo-identification database collected between 2006 and 2017 in Nemuro Strait, Japan. Our results suggest that while male sperm whales are not as social as females, they do form long term associations, have preferred companionship, and forage in social proximity to each other. The best-fitting model to the standardized lagged association rate showed that associations among males last for at least 2.7 years and as most males leave the area after 2 years, associations may last for longer. Twenty dyads were observed associating over more than 2 years, for a maximum 5 years. One dyad was observed associating on 19 different days and clustered on 7 different days. Male associations may function to enhance foraging or to fend off predators. Such relationships seem to be adapted to a pelagic habitat with uncertain resource availability and predation pressure.

First evidence of terrestrial ambrein formation in human adipocere.

To date, the only known occurrence of ambrein, an important perfumery organic molecule, is in coproliths found in about one in a hundred sperm whales. Jetsam ambergris coproliths from the whale are also found occasionally on beaches worldwide. Here we report on the surprising occurrence of ambrein in human adipocere. Adipocere is a waxy substance formed post-mortem during incomplete anaerobic decomposition of soft tissues. Adipocere samples obtained from grave exhumations were analysed using gas chromatography-mass spectrometry (GC-MS). In addition to the typical fatty acids of adipocere, lesser amounts of ambrein were identified in the samples, in abundances similar to those of the major accompanying faecal steroids. The distribution of these compounds suggests that ambrein was produced post-mortem during the microbial decomposition of faecal residues and tissues. It is assumed that the adipocere matrix of saturated fatty acidsaided the preservation of ambrein over extended periods of time, because adipocere is stable against degradation. The association of ambrein formation in ageing faecal material, under moist, oxygen-depleted conditions, now requires more attention in studies of other mammalian and geological samples. Indeed, ambrein and its transformation products may be useful novel chemical indicators of aged faecal matter and decomposed bodies.

Deep Machine Learning Techniques for the Detection and Classification of Sperm Whale Bioacoustics.

We implemented Machine Learning (ML) techniques to advance the study of sperm whale (Physeter macrocephalus) bioacoustics. This entailed employing Convolutional Neural Networks (CNNs) to construct an echolocation click detector designed to classify spectrograms generated from sperm whale acoustic data according to the presence or absence of a click. The click detector achieved 99.5% accuracy in classifying 650 spectrograms. The successful application of CNNs to clicks reveals the potential of future studies to train CNN-based architectures to extract finer-scale details from cetacean spectrograms. Long short-term memory and gated recurrent unit recurrent neural networks were trained to perform classification tasks, including (1) "coda type classification" where we obtained 97.5% accuracy in categorizing 23 coda types from a Dominica dataset containing 8,719 codas and 93.6% accuracy in categorizing 43 coda types from an Eastern Tropical Pacific (ETP) dataset with 16,995 codas; (2) "vocal clan classification" where we obtained 95.3% accuracy for two clan classes from Dominica and 93.1% for four ETP clan types; and (3) "individual whale identification" where we obtained 99.4% accuracy using two Dominica sperm whales. These results demonstrate the feasibility of applying ML to sperm whale bioacoustics and establish the validity of constructing neural networks to learn meaningful representations of whale vocalizations.

Foraging activity of sperm whales (Physeter macrocephalus) off the east coast of New Zealand.

The occurrence and distribution of sperm whales in New Zealand waters is mainly known from whaling records or opportunistic sightings by the public and a systematic estimation of the abundance and distribution has never been conducted. In this study, we investigated the foraging activity and occurrence of sperm whales off the Eastern coast of New Zealand using passive acoustic monitoring techniques. Three acoustic recorders were moored to the ocean floor at different locations on the east side of the North and South Island to collect passive acoustic data from June 2016 until August 2017. A total of 53,823 echolocation click trains were recorded and analyzed to understand the spatial and temporal variation of sperm whale foraging activity. No difference in the foraging activity was found between night-time and day-time periods at any of the locations. Click train detections increased toward the south, suggesting increased foraging activity near Kaikoura. At each station, sperm whale foraging activity varied by month.

Commercial fishing patterns influence odontocete whale-longline interactions in the Southern Ocean.

The emergence of longline fishing around the world has been concomitant with an increase in depredation-interactions by odontocete whales (removal of fish caught on hooks), resulting in substantial socio-economic and ecological impacts. The extent, trends and underlying mechanisms driving these interactions remain poorly known. Using long-term (2003-2017) datasets from seven major Patagonian toothfish (Dissostichus eleginoides) longline fisheries, this study assessed the levels and inter-annual trends of sperm whale (Physeter macrocephalus) and/or killer whale (Orcinus orca) interactions as proportions of fishing time (days) and fishing area (spatial cells). The role of fishing patterns in explaining between-fisheries variations of probabilities of odontocete interactions was investigated. While interaction levels remained globally stable since the early 2000s, they varied greatly between fisheries from 0 to >50% of the fishing days and area. Interaction probabilities were influenced by the seasonal concentration of fishing effort, size of fishing areas, density of vessels, their mobility and the depth at which they operated. The results suggest that between-fisheries variations of interaction probabilities are largely explained by the extent to which vessels provide whales with opportunities for interactions. Determining the natural distribution of whales will, therefore, allow fishers to implement better strategies of spatio-temporal avoidance of depredation.

Shipping routes through core habitat of endangered sperm whales along the Hellenic Trench, Greece: Can we reduce collision risks?

The Mediterranean sperm whale population is listed as 'Endangered". The Hellenic Trench is the core habitat of the eastern Mediterranean sperm whale sub-population that numbers two to three hundred individuals. Major shipping routes running on or very close to the 1000 m depth contour along the Hellenic Trench are causing an unsustainable number of ship-strikes with sperm whales reviewed in this paper. Sperm whale sighting and density data were combined with specific information on the vessel traffic in the area (e.g., types of vessels, traffic patterns, speed and traffic density), in order to estimate the risk of a whale/ship interaction. Routing options to significantly reduce ship strike risk by a small offshore shift in shipping routes were identified. The overall collision risk for sperm whales in the study area would be reduced by around 70%, while a maximum of 11 nautical miles would be added to major routes and only around 5 nautical miles for the majority of ships. No negative impacts were associated with re-routing by shipping away from sperm whale habitat and there would be additional shipping safety and environmental benefits. A significant contribution to the overall conservation status of the marine Natura2000 sites in the area and very important population units of threatened species such as Cuvier's beaked whales, monk seals and loggerhead turtles would be achieved, by the reduction of shipping noise and reduced risk of any oil spills reaching the coasts, which are also important touristic destinations in Greece.

Beached bachelors: An extensive study on the largest recorded sperm whale Physeter macrocephalus mortality event in the North Sea.

Between the 8th January and the 25th February 2016, the largest sperm whale Physeter macrocephalus mortality event ever recorded in the North Sea occurred with 30 sperm whales stranding in five countries within six weeks. All sperm whales were immature males. Groups were stratified by size, with the smaller animals stranding in the Netherlands, and the largest in England. The majority (n = 27) of the stranded animals were necropsied and/or sampled, allowing for an international and comprehensive investigation into this mortality event. The animals were in fair to good nutritional condition and, aside from the pathologies caused by stranding, did not exhibit significant evidence of disease or trauma. Infectious agents were found, including various parasite species, several bacterial and fungal pathogens and a novel alphaherpesvirus. In nine of the sperm whales a variety of marine litter was found. However, none of these findings were considered to have been the primary cause of the stranding event. Potential anthropogenic and environmental factors that may have caused the sperm whales to enter the North Sea were assessed. Once sperm whales enter the North Sea and head south, the water becomes progressively shallower (<40 m), making this region a global hotspot for sperm whale strandings. We conclude that the reasons for sperm whales to enter the southern North Sea are the result of complex interactions of extrinsic environmental factors. As such, these large mortality events seldom have a single ultimate cause and it is only through multidisciplinary, collaborative approaches that potentially multifactorial large-scale stranding events can be effectively investigated.

Examining the effect of reoccurring disturbances on population persistence with application to marine mammals.

We develop a two-state Markov chain to describe the effect of reoccurring disturbances on a population that is modeled by discrete-time matrix model. The environment is described by three parameters that define the magnitude of impact of a disturbance, the average duration of impact of a disturbance, and the average time between disturbances. We derive an approximation for the stochastic growth rate in order to examine how these three parameters affect population growth. From this approximation, we calculate the sensitivity and elasticity of the growth rate with respect to the environmental parameters. We show that the average duration of impact of a disturbance and the average time between disturbances contribute equally to the stochastic growth rate. We also show that the elasticity of the stochastic growth rate is more sensitive to changes in the magnitude of impact than to changes in either the average duration of impact of a disturbance or the average time between disturbances. These conclusions hold irrespective of the population under consideration. We then provide an application of the model formulation to examine how disturbances, such as oil spills, may affect a sperm whale population. The model results suggest that, in oder to mitigate the impact of disturbances, management strategies should focus on reducing the magnitude of impact. Meanwhile, if it is more feasible to reduce either the duration of impact or the time between impacts, managers should focus on whichever is easier to obtain. In addition, when applied to a sperm whale population, our model shows that the probability of extinction can dramatically increase when disturbance frequency increases but is not greatly impacted by the assumption that all disturbances have the same magnitude.

Inter-individual differences in contamination profiles as tracer of social group association in stranded sperm whales.

Ecological and physiological factors lead to different contamination patterns in individual marine mammals. The objective of the present study was to assess whether variations in contamination profiles are indicative of social structures of young male sperm whales as they might reflect a variation in feeding preferences and/or in utilized feeding grounds. We used a total of 61 variables associated with organic compounds and trace element concentrations measured in muscle, liver, kidney and blubber gained from 24 sperm whales that stranded in the North Sea in January and February 2016. Combining contaminant and genetic data, there is evidence for at least two cohorts with different origin among these stranded sperm whales; one from the Canary Island region and one from the northern part of the Atlantic. While genetic data unravel relatedness and kinship, contamination data integrate over areas, where animals occured during their lifetime. Especially in long-lived animals with a large migratory potential, as sperm whales, contamination data may carry highly relevant information about aggregation through time and space.

Ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing.

The auditory ossicles-malleus, incus and stapes-are the smallest bones in mammalian bodies and enable stable sound transmission to the inner ear. Sperm whales are one of the deepest diving aquatic mammals that produce and perceive sounds with extreme loudness greater than 180 dB and frequencies higher than 30 kHz. Therefore, it is of major interest to decipher the microstructural basis for these unparalleled hearing abilities. Using a suite of high-resolution imaging techniques, we reveal that auditory ossicles of sperm whales are highly functional, featuring an ultra-high matrix mineralization that is higher than their teeth. On a micro-morphological and cellular level, this was associated with osteonal structures and osteocyte lacunar occlusions through calcified nanospherites (i.e. micropetrosis), while the bones were characterized by a higher hardness compared to a vertebral bone of the same animals as well as to human auditory ossicles. We propose that the ultra-high mineralization facilitates the unique hearing ability of sperm whales. High matrix mineralization represents an evolutionary conserved or convergent adaptation to middle ear sound transmission.

Vertebral bone microarchitecture and osteocyte characteristics of three toothed whale species with varying diving behaviour.

Although vertebral bone microarchitecture has been studied in various tetrapods, limited quantitative data are available on the structural and compositional changes of vertebrae in marine mammals. Whales exhibit exceptional swimming and diving behaviour, and they may not be immune to diving-associated bone pathologies. Lumbar vertebral bodies were analysed in three toothed whale species: the sperm whale (Physeter macrocephalus), orca (Orcinus orca) and harbour porpoise (Phocoena phocoena). The bone volume fraction (BV/TV) did not scale with body size, although the trabeculae were thicker, fewer in number and further apart in larger whale species than in the other two species. These parameters had a negative allometric scaling relationship with body length. In sperm whales and orcas, the analyses revealed a central ossification zone ("bone-within-bone") with an increased BV/TV and trabecular thickness. Furthermore, a large number of empty osteocyte lacunae was observed in the sperm whales. Quantitative backscattered electron imaging showed that the lacunae were significantly smaller and less densely packed. Our results indicate that whales have a unique vertebral bone morphology with an inside-out appearance and that deep diving may result in a small number of viable osteocytes because of diving depth-related osteocyte death.

Size and shape variations of the bony components of sperm whale cochleae.

Several mass strandings of sperm whales occurred in the North Sea during January and February 2016. Twelve animals were necropsied and sampled around 48 h after their discovery on German coasts of Schleswig Holstein. The present study aims to explore the morphological variation of the primary sensory organ of sperm whales, the left and right auditory system, using high-resolution computerised tomography imaging. We performed a quantitative analysis of size and shape of cochleae using landmark-based geometric morphometrics to reveal inter-individual anatomical variations. A hierarchical cluster analysis based on thirty-one external morphometric characters classified these 12 individuals in two stranding clusters. A relative amount of shape variation could be attributable to geographical differences among stranding locations and clusters. Our geometric data allowed the discrimination of distinct bachelor schools among sperm whales that stranded on German coasts. We argue that the cochleae are individually shaped, varying greatly in dimensions and that the intra-specific variation observed in the morphology of the cochleae may partially reflect their affiliation to their bachelor school. There are increasing concerns about the impact of noise on cetaceans and describing the auditory periphery of odontocetes is a key conservation issue to further assess the effect of noise pollution.

Critical Decline of the Eastern Caribbean Sperm Whale Population.

Sperm whale (Physeter macrocephalus) populations were expected to rebuild following the end of commercial whaling. We document the decline of the population in the eastern Caribbean by tracing demographic changes of well-studied social units. We address hypotheses that, over a ten-year period of dedicated effort (2005-2015), unit size, numbers of calves and/or calving rates have each declined. Across 16 units, the number of adults decreased in 12 units, increased in two, and showed no change in two. The number of adults per unit decreased at -0.195 individuals/yr (95% CI: -0.080 to -0.310; P = 0.001). The number of calves also declined, but the decline was not significant. This negative trend of -4.5% per year in unit size started in about 2010, with numbers being fairly stable until then. There are several natural and anthropogenic threats, but no well-substantiated cause for the decline.

Mediterranean Sperm Whales, Physeter macrocephalus: The Precarious State of a Lost Tribe.

First observed in the classical era, a population of sperm whales (Physeter macrocephalus) persists to this day in the deep waters of the Mediterranean Sea. Genetic and observational evidence support the notion that this is an isolated population, separated from its Atlantic neighbours. These whales depend on mesopelagic squid for food, and appear to occupy a very similar ecological niche to sperm whales in the open oceans. Recent evidence proving that individuals can pass between the eastern and western deep water basins confirms that this is a single population, not isolated into western and eastern stocks. We lack robust information on their population status, but they could number in the hundreds rather than thousands, and current densities appear to be much lower than those reported in the 1950s, suggesting that we should be very concerned about the conservation status of this population. This makes it vitally important to address the serious threats posed by ship strikes and entanglement in fishing nets, especially driftnets, and to carefully monitor other potential sources of anthropogenic impact. A step change in funding to collect better data and a clear shift in policy priorities are needed if we are to be serious about conserving this population.