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.

The myodural bridges' existence in the sperm whale.

Recent studies have identified that the myodural bridge (MDB) is located between the suboccipital muscles and cervical dura mater in the posterior atlanto-occipital interspace within humans. The myodural bridge has been considered to have a significant role in physiological functions. However, there is little information about the myodural bridge in marine mammals; we conducted this study to investigate and examine the morphology of the myodural bridge in a sperm whale. We also aim to discuss the physiological functions of the myodural bridge. In this study, a 15.1-meter long sperm whale carcass was examined. Multiple methods were conducted to examine the bridges of the sperm whale which included dissection, P45 plastination and histological analysis. This study confirmed the existence of the myodural bridge in the sperm whale and shows there are two types of the bridge in the sperm whale: one type was the occipital-dural bridge (ODB), the other type was the MDB. A large venous plexus was found within the epidural space and this venous plexus is thought to contain a great amount of blood when in deep water and thus the movements of suboccipital muscles could be a unique power source that drives cerebrospinal fluid circulation.

Thorough study of persistent organic pollutants and halogenated natural products in sperm whale blubber through preparative sample cleanup followed by fractionation with countercurrent chromatography.

Marine mammals are top predators of the marine food chain and thus known to bioaccumulate high concentrations of polyhalogenated compounds. Yet, details of the organohalogen pattern are largely unknown. For this reason, we isolated the polyhalogenated compounds from 750 g blubber of a sperm whale (Physeter catodon), which deceased at the German North Sea coast in January 2016. The sample matrix was decomposed by sulfuric acid treatment and the polyhalogenated compounds were then fractionated by countercurrent chromatography (CCC). Seventy-three CCC fractions were taken and analyzed by gas chromatography with electron capture negative ion mass spectrometry (GC/ECNI-MS). The bulk of the polyhalogenated compounds in the sample originated from classic persistent organic pollutants (POPs). Altogether 90 polychlorinated biphenyl (PCB) congeners were detected in the sample including all possible octa- to decachloro congeners except one. The sample also featured 105 toxaphene congeners including 30 chlorobornenes (contribution ∼14% of the total toxaphene content) which were only detected after the CCC fractionation. In addition, several chlordane and mirex related compounds were detected which were never or very scarcely described before in biota. Classic POPs (PCBs, DDT, toxaphene, chlordane, mirex) were predominant, while new emerging contaminants were scarcely detected. The sample featured several halogenated natural products (HNPs) some of which were less stable and destroyed during the sample cleanup involving treatment with sulfuric acid. Sample fractionation by means of CCC was crucial for the detection and assignment of many of the uncommon polyhalogenated compounds.

Magnetic resonance imaging and computed tomography as tools for the investigation of sperm whale (Physeter macrocephalus) teeth and eye.

BACKGROUND: Scanning techniques such as magnetic resonance imaging (MRI) and computed tomography (CT) are useful tools in veterinary and human medicine. Here we demonstrate the usefulness of these techniques in the study of the anatomy of wild marine mammals as part of a necropsy. MRI and CT scans of sperm whale teeth (n = 4) were performed. The methods were compared and further compared to current standard methods for evaluation of tooth layering. For MRI a zero echo time sequence was used, as previously done for imaging of intact human teeth. For CT two different clinical scanners were used. RESULTS: The three scanners did not provide sufficient information to allow age estimation, but both MRI and CT provided anatomical information about the tooth cortex and medulla without the need for sectioning the teeth. MRI scanning was also employed for visualizing the vascularization of an intact eye from one of the stranded sperm whale. CONCLUSIONS: Clearly, MRI was useful for investigation of the retinal vasculation, but optimum results would require well-preserved tissue. It was not possible to estimate age based on CT scans of tooth growth lines. Further research is needed to clarify the usability of MRI and CT as tools for marine mammal research when samples need to remain intact or when a spatial (three dimensional) arrangement of features needs to be determined.

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.

Properties and architecture of the sperm whale skull amphitheatre.

The sperm whale skull amphitheatre cradles an enormous two-tonne spermaceti organ. The amphitheatre separates this organ from the cranium and the cervical vertebrae that lie in close proximity to the base of the skull. Here, we elucidate that this skull amphitheatre is an elastic, flexible, triple-layered structure with mechanical properties that are conjointly guided by bone histology and the characteristics of pore space. We contend that the amphitheatre will flex elastically to equilibrate forces transmitted via the spermaceti organ that arise through diving. We find that collisions from sperm whale aggression do not cause the amphitheatre to bend, but rather localise stress to the base of the amphitheatre on its anterior face. We consider, therefore, that the uniquely thin and extended construction of the amphitheatre, has relevance as an energy absorptive structure in diving.

Albicetus oxymycterus, a New Generic Name and Redescription of a Basal Physeteroid (Mammalia, Cetacea) from the Miocene of California, and the Evolution of Body Size in Sperm Whales.

Living sperm whales are represented by only three species (Physeter macrocephalus, Kogia breviceps and Kogia sima), but their fossil record provides evidence of an ecologically diverse array of different forms, including morphologies and body sizes without analog among living physeteroids. Here we provide a redescription of Ontocetus oxymycterus, a large but incomplete fossil sperm whale specimen from the middle Miocene Monterey Formation of California, described by Remington Kellogg in 1925. The type specimen consists of a partial rostrum, both mandibles, an isolated upper rostrum fragment, and incomplete tooth fragments. Although incomplete, these remains exhibit characteristics that, when combined, set it apart morphologically from all other known physeteroids (e.g., a closed mesorostral groove, and the retention of enameled tooth crowns). Kellogg originally placed this species in the genus Ontocetus, a enigmatic tooth taxon reported from the 19th century, based on similarities between the type specimen Ontocetus emmonsi and the conspicuously large lower dentition of Ontocetus oxymycterus. However, the type of the genus Ontocetus is now known to represent a walrus tusk (belonging to fossil Odobenidae) instead of a cetacean tooth. Thus, we assign this species to the new genus Albicetus, creating the new combination of Albicetus oxymycterus, gen. nov. We provide new morphological observations of the type specimen, including a 3D model. We also calculate a total length of approximately 6 m in life, using cranial proxies of body size for physeteroids. Lastly, a phylogenetic analysis of Albicetus oxymycterus with other fossil and living Physeteroidea resolves its position as a stem physeteroid, implying that large body size and robust dentition in physeteroids evolved multiple times and in distantly related lineages.

Morphology of the Nasal Apparatus in Pygmy (Kogia Breviceps) and Dwarf (K. Sima) Sperm Whales.

Odontocete echolocation clicks are generated by pneumatically driven phonic lips within the nasal passage, and propagated through specialized structures within the forehead. This study investigated the highly derived echolocation structures of the pygmy (Kogia breviceps) and dwarf (K. sima) sperm whales through careful dissections (N = 18 K. breviceps, 6 K. sima) and histological examinations (N = 5 K. breviceps). This study is the first to show that the entire kogiid sound production and transmission pathway is acted upon by complex facial muscles (likely derivations of the m. maxillonasolabialis). Muscles appear capable of tensing and separating the solitary pair of phonic lips, which would control echolocation click frequencies. The phonic lips are enveloped by the "vocal cap," a morphologically complex, connective tissue structure unique to kogiids. Extensive facial muscles appear to control the position of this structure and its spatial relationship to the phonic lips. The vocal cap's numerous air crypts suggest that it may reflect sounds. Muscles encircling the connective tissue case that surrounds the spermaceti organ may change its shape and/or internal pressure. These actions may influence the acoustic energy transmitted from the phonic lips, through this lipid body, to the melon. Facial and rostral muscles act upon the length of the melon, suggesting that the sound "beam" can be focused as it travels through the melon and into the environment. This study suggests that the kogiid echolocation system is highly tunable. Future acoustic studies are required to test these hypotheses and gain further insight into the kogiid echolocation system.

Sperm whales and killer whales with the largest brains of all toothed whales show extreme differences in cerebellum.

Among cetaceans, killer whales and sperm whales have the widest distribution in the world's oceans. Both species use echolocation, are long-lived, and have the longest periods of gestation among whales. Sperm whales dive much deeper and much longer than killer whales. It has long been thought that sperm whales have the largest brains of all living things, but our brain mass evidence, from published sources and our own specimens, shows that big males of these two species share this distinction. Despite this, we also find that cerebellum size is very different between killer whales and sperm whales. The sperm whale cerebellum is only about 7% of the total brain mass, while the killer whale cerebellum is almost 14%. These results are significant because they contradict claims that the cerebellum scales proportionally with the rest of the brain in all mammals. They also correct the generalization that all cetaceans have enlarged cerebella. We suggest possible reasons for the existence of such a large cerebellar size difference between these two species. Cerebellar function is not fully understood, and comparing the abilities of animals with differently sized cerebella can help uncover functional roles of the cerebellum in humans and animals. Here we show that the large cerebellar difference likely relates to evolutionary history, diving, sensory capability, and ecology.

Bony outgrowths on the jaws of an extinct sperm whale support macroraptorial feeding in several stem physeteroids.

Several extinct sperm whales (stem Physeteroidea) were recently proposed to differ markedly in their feeding ecology from the suction-feeding modern sperm whales Kogia and Physeter. Based on cranial, mandibular, and dental morphology, these Miocene forms were tentatively identified as macroraptorial feeders, able to consume proportionally large prey using their massive teeth and robust jaws. However, until now, no corroborating evidence for the use of teeth during predation was available. We report on a new specimen of the stem physeteroid Acrophyseter, from the late middle to early late Miocene of Peru, displaying unusual bony outgrowths along some of the upper alveoli. Considering their position and outer shape, these are identified as buccal maxillary exostoses. More developed along posterior teeth and in tight contact with the high portion of the dental root outside the bony alveoli, the exostoses are hypothesized to have developed during powerful bites; they may have worked as buttresses, strengthening the teeth when facing intense occlusal forces. These buccal exostoses further support a raptorial feeding technique for Acrophyseter and, indirectly, for other extinct sperm whales with a similar oral apparatus (Brygmophyseter, Livyatan, Zygophyseter). With a wide size range, these Miocene stem physeteroids were major marine macropredators, occupying ecological niches nowadays mostly taken by killer whales.

Measuring body length of male sperm whales from their clicks: the relationship between inter-pulse intervals and photogrammetrically measured lengths.

Sperm whales (Physeter macrocephalus) emit short, broadband clicks which often include multiple pulses. The time interval between these pulses [inter-pulse interval (IPI)] represents the two-way time for a pulse to travel between the air sacs located at either end of the sperm whale's head. The IPI therefore, is a proxy of head length which, using an allometric relationship, can be used to estimate total body length. Previous studies relating IPI to an independent measure of length have relied on very small sample sizes and manual techniques for measuring IPI. Sound recordings and digital stereo photogrammetric measurements of 21 individuals were made off Kaikoura, New Zealand, and, in addition, archived recordings of whales measured with a previous photogrammetric system were reanalyzed to obtain a total sample size of 33 individuals. IPIs were measured automatically via cepstral analysis implemented via a software plug-in for pamguard, an open-source software package for passive acoustic monitoring. IPI measurements were highly consistent within individuals (mean CV=0.63%). The new regression relationship relating IPI (I) and total length (T) was found to be T=1.258I+5.736 (r(2)=0.77, p<0.001). This new regression provides a better fit than previous studies of large (> 11 m) sperm whales.

Sometimes sperm whales (Physeter macrocephalus) cannot find their way back to the high seas: a multidisciplinary study on a mass stranding.

BACKGROUND: Mass strandings of sperm whales (Physeter macrocephalus) remain peculiar and rather unexplained events, which rarely occur in the Mediterranean Sea. Solar cycles and related changes in the geomagnetic field, variations in water temperature and weather conditions, coast geographical features and human activities have been proposed as possible causes. In December 2009, a pod of seven male sperm whales stranded along the Adriatic coast of Southern Italy. This is the sixth instance from 1555 in this basin. METHODOLOGY/PRINCIPAL FINDINGS: Complete necropsies were performed on three whales whose bodies were in good condition, carrying out on sampled tissues histopathology, virology, bacteriology, parasitology, and screening of veins looking for gas emboli. Furthermore, samples for age determination, genetic studies, gastric content evaluation, stable isotopes and toxicology were taken from all the seven specimens. The animals were part of the same group and determined by genetic and photo-identification to be part of the Mediterranean population. Causes of death did not include biological agents, or the "gas and fat embolic syndrome", associated with direct sonar exposure. Environmental pollutant tissue concentrations were relatively high, in particular organochlorinated xenobiotics. Gastric content and morphologic tissue examinations showed a prolonged starvation, which likely caused, at its turn, the mobilization of lipophilic contaminants from the adipose tissue. Chemical compounds subsequently entered the blood circulation and may have impaired immune and nervous functions. CONCLUSIONS/SIGNIFICANCE: A multi-factorial cause underlying this sperm whales' mass stranding is proposed herein based upon the results of postmortem investigations as well as of the detailed analyses of the geographical and historical background. The seven sperm whales took the same "wrong way" into the Adriatic Sea, a potentially dangerous trap for Mediterranean sperm whales. Seismic surveys should be also regarded as potential co-factors, even if no evidence of direct impact has been detected.

The giant bite of a new raptorial sperm whale from the Miocene epoch of Peru.

The modern giant sperm whale Physeter macrocephalus, one of the largest known predators, preys upon cephalopods at great depths. Lacking a functional upper dentition, it relies on suction for catching its prey; in contrast, several smaller Miocene sperm whales (Physeteroidea) have been interpreted as raptorial (versus suction) feeders, analogous to the modern killer whale Orcinus orca. Whereas very large physeteroid teeth have been discovered in various Miocene localities, associated diagnostic cranial remains have not been found so far. Here we report the discovery of a new giant sperm whale from the Middle Miocene of Peru (approximately 12-13 million years ago), Leviathan melvillei, described on the basis of a skull with teeth and mandible. With a 3-m-long head, very large upper and lower teeth (maximum diameter and length of 12 cm and greater than 36 cm, respectively), robust jaws and a temporal fossa considerably larger than in Physeter, this stem physeteroid represents one of the largest raptorial predators and, to our knowledge, the biggest tetrapod bite ever found. The appearance of gigantic raptorial sperm whales in the fossil record coincides with a phase of diversification and size-range increase of the baleen-bearing mysticetes in the Miocene. We propose that Leviathan fed mostly on high-energy content medium-size baleen whales. As a top predator, together with the contemporaneous giant shark Carcharocles megalodon, it probably had a profound impact on the structuring of Miocene marine communities. The development of a vast supracranial basin in Leviathan, extending on the rostrum as in Physeter, might indicate the presence of an enlarged spermaceti organ in the former that is not associated with deep diving or obligatory suction feeding.

Relationship between sperm whale (Physeter macrocephalus) click structure and size derived from videocamera images of a depredating whale (sperm whale prey acquisition).

Sperm whales have learned to depredate black cod (Anoplopoma fimbria) from longline deployments in the Gulf of Alaska. On May 31, 2006, simultaneous acoustic and visual recordings were made of a depredation attempt by a sperm whale at 108 m depth. Because the whale was oriented perpendicularly to the camera as it contacted the longline at a known distance from the camera, the distance from the nose to the hinge of the jaw could be estimated. Allometric relationships obtained from whaling data and skeleton measurements could then be used to estimate both the spermaceti organ length and total length of the animal. An acoustic estimate of animal length was obtained by measuring the inter-pulse interval (IPI) of clicks detected from the animal and using empirical formulas to convert this interval into a length estimate. Two distinct IPIs were extracted from the clicks, one yielding a length estimate that matches the visually-derived length to within experimental error. However, acoustic estimates of spermaceti organ size, derived from standard sound production theories, are inconsistent with the visual estimates, and the derived size of the junk is smaller than that of the spermaceti organ, in contradiction with known anatomical relationships.

Neuromuscular anatomy and evolution of the cetacean forelimb.

The forelimb of cetaceans (whales, dolphins, and porpoises) has been radically modified during the limb-to-flipper transition. Extant cetaceans have a soft tissue flipper encasing the manus and acting as a hydrofoil to generate lift. The neuromuscular anatomy that controls flipper movement, however, is poorly understood. This study documents flipper neuromuscular anatomy and tests the hypothesis that antebrachial muscle robustness is related to body size. Data were gathered during dissections of 22 flippers, representing 15 species (7 odontocetes, 15 mysticetes). Results were compared with published descriptions of both artiodactyls and secondarily aquatic vertebrates. Results indicate muscle robustness is best predicted by taxonomic distribution and is not a function of body size. All cetaceans have atrophied triceps muscles, an immobile cubital joint, and lack most connective tissue structures and manus muscles. Forelimbs retain only three muscle groups: triceps (only the scapular head is functional as the humeral heads are vestigal), and antebrachial extensors and flexors. Well-developed flexor and extensor muscles were found in mysticetes and basal odontocetes (i.e., physeterids, kogiids, and ziphiids), whereas later diverging odontocetes (i.e., monodontids, phocoenids, and delphinids) lack or reduce these muscles. Balaenopterid mysticetes (e.g., fin and minke whales) may actively change flipper curvature, while basal odontocetes (e.g., sperm and beaked whales) probably stiffen the flipper through isometric contraction. Later diverging odontocetes lack musculature supporting digital movements and are unable to manipulate flipper curvature. Cetacean forelimbs are unique in that they have lost agility and several soft tissue structures, but retain sensory innervations.

Measuring the off-axis angle and the rotational movements of phonating sperm whales using a single hydrophone.

The common use of the bent-horn model of the sperm whale sound generator describes sperm whale clicks as the pulse series {p0, p1, p2, p3,...}. Clicks, however, deviate from this standard when recorded using off-axis hydrophones. The existence of additional pulses within the {p0, p1, p2, p3, ...} series can be explained still using the bent-horn model. Multiple reflections on the whale's frontal and distal sacs of the p0 pulse lead to additional sets of pulses detectable using a farfield, off-axis hydrophone. The travel times of some of these additional pulses depend on the whale's orientation. The authors propose a method to estimate the off-axis angle of sperm whale clicks. They also propose a method to determine the nature of the movement (if it is pitch, yaw, or roll) of phonating sperm whales. The application of both methods requires the measurement of the travel time differences between pulses composing a sperm whale click. They lead, using a simple apparatus consisting of a single hydrophone at an unknown depth, to new measurements of the underwater movements of sperm whales. Using these methods shows that sperm whales would methodically scan seawater while searching for prey, by making periodic pitch and yaw movements in sync with their acoustic activity.