A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales

Extant baleen whales (Cetacea, Mysticeti) are all large filter-feeding marine mammals that lack teeth as adults, instead possessing baleen, and feed on small marine animals in bulk. The early evolution of these superlative mammals, and their unique feeding method, has hitherto remained enigmatic. Here, I report a new toothed mysticete from the Late Oligocene of Australia that is more archaic than any previously described. Unlike all other mysticetes, this new whale was small, had enormous eyes and lacked derived adaptations for bulk filter-feeding. Several morphological features suggest that this mysticete was a macrophagous predator, being convergent on some Mesozoic marine reptiles and the extant leopard seal (Hydrurga leptonyx). It thus refutes the notions that all stem mysticetes were filter-feeders, and that the origins and initial radiation of mysticetes was linked to the evolution of filter-feeding. Mysticetes evidently radiated into a variety of disparate forms and feeding ecologies before the evolution of baleen or filter-feeding. The phylogenetic context of the new whale indicates that basal mysticetes were macrophagous predators that did not employ filter-feeding or echolocation, and that the evolution of characters associated with bulk filter-feeding was gradual.     

Status of the world's baleen whales

No global synthesis of the status of baleen whales has been published since the 2008 IUCN Red List assessments. Many populations remain at low numbers from historical commercial whaling, which had ceased for all but a few by 1989. Fishing gear entanglement and ship strikes are the most severe current threats. The acute and long‐term effects of anthropogenic noise and the cumulative effects of multiple stressors are of concern but poorly understood. The looming consequences of climate change and ocean acidification remain difficult to characterize. North Atlantic and North Pacific right whales are among the species listed as Endangered. Southern right, bowhead, and gray whales have been assessed as Least Concern but some subpopulations of these species ‐ western North Pacific gray whales, Chile‐Peru right whales, and Svalbard/Barents Sea and Sea of Okhotsk bowhead whales ‐ remain at low levels and are either Endangered or Critically Endangered. Eastern North Pacific blue whales have reportedly recovered, but Antarctic blue whales remain at about 1% of pre‐exploitation levels. Small isolated subspecies or subpopulations, such as northern Indian Ocean blue whales, Arabian Sea humpback whales, and Mediterranean Sea fin whales are threatened while most subpopulations of sei, Bryde's, and Omura's whales are inadequately monitored and difficult to assess.     

Anisakis spp. in toothed and baleen whales from Japanese waters with notes on their potential role as biological tags

In this study, Anisakis nematodes isolated from toothed and baleen whales from localities around Japan were molecularly (PCR-RFLP) identified. In Wakayama, common bottlenose dolphins (Tursiops truncatus) were infected with A. simplex sensu stricto (s.s.), A. typica and A. pegreffii, while A. typica was the only species found in pantropical spotted dolphin (Stenella attenuata) and striped dolphin (S. coeruleoalba). Offshore common minke whales (Balaenoptera acutorostrata) and sei whales (B. borealis) were almost exclusively infected with A. simplex s.s.. However, in common minke whales from two Hokkaido localities, mature worms mostly consisted of A. simplex s.s. in some individuals and of A. pegreffii in others, but immature worms were mainly A. simplex s.s.. Gross and histopathological examination on gastric mucosa attached by anisakids resulted in mild and superficial reactions by the two baleen whale species in contrast to severe inflammatory reaction associated with ulcer formations by common bottlenose dolphin. Host specificity and adaptability of Anisakis spp. in these baleen and toothed whales were discussed from the points of view of adult worm size, worm population and pathological reactions by hosts. Interestingly, most of the common minke whales predominantly harboring mature A. pegreffii adults belonged to the Yellow Sea – East China Sea stock (J stock), which migrates through the Sea of Japan, whereas most of those mainly parasitized by mature A. simplex s.s. adults were from the Okhotsk Sea – West Pacific stock (O stock), mostly inhabiting the Pacific side, suggesting that these sibling species may have utility as biological tags to differentiate whale stocks. These results represent the first definitive host records for A. pegreffi in the Northwestern Pacific Ocean.     

Selection-delayed population dynamics in baleen whales and beyond

While it is known that population cycles are driven by delayed density-dependent feedbacks, the search for a common feedback mechanism in natural populations with cyclic dynamics has remained unresolved for almost a century. To identify the existence and cause of delayed feedbacks I apply six age- and sex-structured population dynamics models to seven species of baleen whales (suborder Mysticeti) that were heavily depleted by past commercial whaling. The six models include a predator–prey model with killer whale (Orcinus orca) as the predator, and five singe-species models based on (1) exponential growth, (2) density-regulated growth, (3) density-regulated growth with depensation, (4) delayed density-regulated growth and (5) selection-delayed dynamics. The latter model has a density-regulated growth rate that is accelerated and decelerated by the intra-specific natural selection that arises from the density-dependent competitive interactions between the individuals in the population. Essential parameters are estimated by a Bayesian statistical framework, and it is shown that baleen whales have a delayed recovery relative to density-regulated growth. The time-lag is not explained by depensation, or by interactions with prey or predators. It is instead resolved by a selection-delayed acceleration of the intrinsic growth rate. The results are discussed in relation to the literature on cyclic dynamics, and it is noted (1) that selection-delayed dynamics is both theoretically and empirically sufficient for cyclic population dynamics, (2) that it is widespread in natural populations owing to the widespread occurrence of otherwise unexplained phenotypic cycles in populations with cyclic dynamics, and (3) that there is a lack of empirical evidence showing that predator–prey interactions is a sufficient cause for the cyclic dynamics of natural populations. The conclusion stresses the importance of intra-specific delays in cyclic dynamics, and suggests that it is the acceleration of the growth rate, and not the growth rate itself, that is determined by the density-dependent environment.     

Fight or flight: antipredator strategies of baleen whales

• 1 The significance of killer whale Orcinus orca predation on baleen whales (Mysticeti) has been a topic of considerable discussion and debate in recent years. Discourse has been constrained by poor understanding of predator‐prey dynamics, including the relative vulnerability of different mysticete species and age classes to killer whales and how these prey animals avoid predation. Here we provide an overview and analysis of predatory interactions between killer whales and mysticetes, with an emphasis on patterns of antipredator responses.
• 2 Responses of baleen whales to predatory advances and attacks by killer whales appear to fall into two distinct categories, which we term the fight and flight strategies. The fight strategy consists of active physical defence, including self‐defence by single individuals, defence of calves by their mothers and coordinated defence by groups of whales. It is documented for five mysticetes: southern right whale Eubalaena australis, North Atlantic right whale Eubalaena glacialis, bowhead whale Balaena mysticetus, humpback whale Megaptera novaeangliae and grey whale Eschrichtius robustus. The flight strategy consists of rapid (20–40 km/h) directional swimming away from killer whales and, if overtaken and attacked, individuals do little to defend themselves. This strategy is documented for six species in the genus Balaenoptera.
• 3 Many aspects of the life history, behaviour and morphology of mysticetes are consistent with their antipredator strategy, and we propose that evolution of these traits has been shaped by selection for reduced predation. Fight species tend to have robust body shapes and are slow but relatively manoeuvrable swimmers. They often calve or migrate in coastal areas where proximity to shallow water provides refuge and an advantage in defence. Most fight species have either callosities (rough and hardened patches of skin) or encrustations of barnacles on their bodies, which may serve (either primarily or secondarily) as weapons or armour for defence. Flight species have streamlined body shapes for high‐speed swimming and they can sustain speeds necessary to outrun pursuing killer whales (>15–20 km/h). These species tend to favour pelagic habitats and calving grounds where prolonged escape sprints from killer whales are possible.
• 4 The rarity of observed successful attacks by killer whales on baleen whales, especially adults, may be an indication of the effectiveness of these antipredator strategies. Baleen whales likely offer low profitability to killer whales, relative to some other marine mammal prey. High‐speed pursuit of flight species has a high energetic cost and a low probability of success while attacks on fight species can involve prolonged handling times and a risk of serious injury.

     

Estimating morphometric attributes of baleen whales with photogrammetry from small UASs: A case study with blue and gray whales

Small unmanned aircraft systems (sUASs) are fostering novel approaches to marine mammal research, including baleen whale photogrammetry, by providing new observational perspectives. We collected vertical images of 89 gray and 6 blue whales using low cost sUASs to examine the accuracy of image based morphometry. Moreover, measurements from 192 images of a 1 m calibration object were used to examine four different scaling correction models. Results indicate that a linear mixed model including an error term for flight and date contained 0.17 m less error and 0.25 m less bias than no correction. We used the propagation uncertainty law to examine error contributions from scaling and image measurement (digitization) to determine that digitization accounted for 97% of total variance. Additionally, we present a new whale body size metric termed Body Area Index (BAI). BAI is scale invariant and is independent of body length (R² = 0.11), enabling comparisons of body size within and among populations, and over time. With this study we present a three program analysis suite that measures baleen whales and compensates for lens distortion and corrects scaling error to produce 11 morphometric attributes from sUAS imagery. The program is freely available and is expected to improve processing efficiency and analytical continuity.     

Feeding ecology of gray whales inferred from stable-carbon and nitrogen isotopic analysis of baleen plates

Stable-carbon and nitrogen isotopic compositions (δ¹³C, δ¹⁵N) of baleen plates of two juvenile and four adult gray whales (Eschrichtius robustus) were examined. High variance in isotopic composition of baleen plates was detected among individuals and, unlike other migratory species of baleen whales examined isotopically, δ¹³C and δ¹⁵N values of most whales showed no regular oscillations. Only one baleen plate reflected the assumed principal Arctic prey (ampeliscid amphipods) during growth on the summer grounds. The rate of baleen growth inferred for one of the juveniles in the last 5 months of life (4.7 mm/week) was similar to the rate calculated previously for a rehabilitating gray whale calf. Autumn corresponded to the timing of the formation of lowest δ¹⁵N values measured along plates. We estimate that the baleen length in all adult gray whales recorded around a year of information (1.3 ± 0.3; Mean ± SD). This short period of dietary integration precludes long time series analyses in this species and reflects the extensive wear on baleen plates due to benthic foraging. Handling editor: M. Power     

Future recovery of baleen whales is imperiled by climate change

Historical harvesting pushed many whale species to the brink of extinction. Although most Southern Hemisphere populations are slowly recovering, the influence of future climate change on their recovery remains unknown. We investigate the impacts of two anthropogenic pressures—historical commercial whaling and future climate change—on populations of baleen whales (blue, fin, humpback, Antarctic minke, southern right) and their prey (krill and copepods) in the Southern Ocean. We use a climate–biological coupled “Model of Intermediate Complexity for Ecosystem Assessments” (MICE) that links krill and whale population dynamics with climate change drivers, including changes in ocean temperature, primary productivity and sea ice. Models predict negative future impacts of climate change on krill and all whale species, although the magnitude of impacts on whales differs among populations. Despite initial recovery from historical whaling, models predict concerning declines under climate change, even local extinctions by 2100, for Pacific populations of blue, fin and southern right whales, and Atlantic/Indian fin and humpback whales. Predicted declines were a consequence of reduced prey (copepods/krill) from warming and increasing interspecific competition between whale species. We model whale population recovery under an alternative scenario whereby whales adapt their migratory patterns to accommodate changing sea ice in the Antarctic and a shifting prey base. Plasticity in range size and migration was predicted to improve recovery for ice‐associated blue and minke whales. Our study highlights the need for ongoing protection to help depleted whale populations recover, as well as local management to ensure the krill prey base remains viable, but this may have limited success without immediate action to reduce emissions.     

Morphological specializations of baleen whales associated with hydrodynamic performance and ecological niche

Feeding behavior, prey type, and habitat appear to be associated with the morphological design of body, fluke, and flippers in baleen whales. Morphometric data from whaling records and recent stranding events were compiled, and morphometric parameters describing the body length, and fluke and flipper dimensions for an "average" blue whale Balaenoptera musculus, humpback whale Megaptera novaeangliae, gray whale Eschrichtius robustus, and right whale Eubalaena glacialis were determined. Body mass, body volume, body surface area, and fluke and flipper surface areas were estimated. The resultant morphological configurations lent themselves to the following classifications based on hydrodynamic principles: fast cruiser, slow cruiser, fast maneuverer, and slow maneuverer. Blue whales have highly streamlined bodies with small, high aspect ratio flippers and flukes for fast efficient cruising in the open ocean. On the other hand, the rotund right whale has large, high aspect ratio flukes for efficient slow speed cruising that is optimal for their continuous filter feeding technique. Humpbacks have large, high aspect ratio flippers and a large, low aspect ratio tail for quick acceleration and high-speed maneuvering which would help them catch their elusive prey, while gray whales have large, low aspect ratio flippers and flukes for enhanced low-speed maneuvering in complex coastal water habitats.     

Phylogenetic relationships among the baleen whales based on maternally and paternally inherited characters

Phylogenetic relationships in the Cetacean suborder Mysticeti (baleen whales) have recently been the focus of increased attention. Here, we examine the evolutionary history of this group by comparing genealogies derived from Y chromosome and mitochondrial DNA sequences. We generated topologies based on paternally and maternally inherited characters for males from nine baleen whale species, including representatives of three families (Balaenidae, Eschrichtiidae, and Balaenopteridae) and four genera (Balaena, Eschrichtius, Balaenoptera, and Megaptera). Divergence among species was fifteen times greater for mtDNA than for Y-specific DNA. Both mtDNA and yDNA topologies revealed the family Balaenopteridae to be paraphyletic, but this relationship was neither strongly supported nor consistent across phylogenetic analysis methodologies. Humpback and fin whales, representing different genera, were reciprocally monophyletic sister species according to mtDNA. Although the monophyly of fin whales decayed for yDNA, a close relationship between fin and humpback whales was retained in yDNA trees. The paraphyly of fin whales and the long branch leading to humpback whales for the yDNA marker may suggest life history differences between these species. Specifically, male humpback whales showed higher than average divergence from other baleen whales at yDNA, although not at mtDNA, suggesting a potential for smaller effective population sizes among male humpbacks on an evolutionary timescale. The observation that those species that have been found to hybridize in nature (blue/fin and blue/humpback) do not reveal evidence for paraphyly for either maternal or paternal markers suggests that introgressive hybridization has not historically been extensive and thus may not represent a substantial source of phylogenetic error for Mysticeti.     

Parallel evolution of auditory genes for echolocation in bats and toothed whales

The ability of bats and toothed whales to echolocate is a remarkable case of convergent evolution. Previous genetic studies have documented parallel evolution of nucleotide sequences in Prestin and KCNQ4, both of which are associated with voltage motility during the cochlear amplification of signals. Echolocation involves complex mechanisms. The most important factors include cochlear amplification, nerve transmission, and signal re-coding. Herein, we screen three genes that play different roles in this auditory system. Cadherin 23 (Cdh23) and its ligand, protocadherin 15 (Pcdh15), are essential for bundling motility in the sensory hair. Otoferlin (Otof) responds to nerve signal transmission in the auditory inner hair cell. Signals of parallel evolution occur in all three genes in the three groups of echolocators--two groups of bats (Yangochiroptera and Rhinolophoidea) plus the dolphin. Significant signals of positive selection also occur in Cdh23 in the Rhinolophoidea and dolphin, and Pcdh15 in Yangochiroptera. In addition, adult echolocating bats have higher levels of Otof expression in the auditory cortex than do their embryos and non-echolocation bats. Cdh23 and Pcdh15 encode the upper and lower parts of tip-links, and both genes show signals of convergent evolution and positive selection in echolocators, implying that they may co-evolve to optimize cochlear amplification. Convergent evolution and expression patterns of Otof suggest the potential role of nerve and brain in echolocation. Our synthesis of gene sequence and gene expression analyses reveals that positive selection, parallel evolution, and perhaps co-evolution and gene expression affect multiple hearing genes that play different roles in audition, including voltage and bundle motility in cochlear amplification, nerve transmission, and brain function.     

Age estimation in bowhead whales using tympanic bulla histology and baleen isotopes

Tympanic bullae and baleen plates from bowhead whales of the Western Arctic population were examined. Growth layer groups (GLGs) in the involucrum of the tympanic bone were used to estimate age of the whales, and compared to stable isotope signatures along transects of baleen plates and the involucrum. The involucrum of the tympanic bone consists of three regions that form in utero, during nursing in the first year, and during the first decades of life, respectively. Life history events, such as annual migration, are recorded in the bowhead tympanic bulla. It is likely that bone growth in the bowhead tympanic occurs during periods of high food intake, while slow or arrested growth occurs during periods of low food intake. Comparisons between numbers of GLGs in the tympanic, number of isotopic oscillations in a baleen plate, length of the baleen plate, and total whale length show correlation coefficients as high as 0.97. The tympanic GLG method is particularly useful for estimating the age of whales up to 20 yr old.     

Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales

The origin of baleen in mysticete whales represents a major transition in the phylogenetic history of Cetacea. This key specialization, a keratinous sieve that enables filter-feeding, permitted exploitation of a new ecological niche and heralded the evolution of modern baleen-bearing whales, the largest animals on Earth. To date, all formally described mysticete fossils conform to two types: toothed species from Oligocene-age rocks ( approximately 24 to 34 million years old) and toothless species that presumably utilized baleen to feed (Recent to approximately 30 million years old). Here, we show that several Oligocene toothed mysticetes have nutrient foramina and associated sulci on the lateral portions of their palates, homologous structures in extant mysticetes house vessels that nourish baleen. The simultaneous occurrence of teeth and nutrient foramina implies that both teeth and baleen were present in these early mysticetes. Phylogenetic analyses of a supermatrix that includes extinct taxa and new data for 11 nuclear genes consistently resolve relationships at the base of Mysticeti. The combined data set of 27,340 characters supports a stepwise transition from a toothed ancestor, to a mosaic intermediate with both teeth and baleen, to modern baleen whales that lack an adult dentition but retain developmental and genetic evidence of their ancestral toothed heritage. Comparative sequence data for ENAM (enamelin) and AMBN (ameloblastin) indicate that enamel-specific loci are present in Mysticeti but have degraded to pseudogenes in this group. The dramatic transformation in mysticete feeding anatomy documents an apparently rare, stepwise mode of evolution in which a composite phenotype bridged the gap between primitive and derived morphologies; a combination of fossil and molecular evidence provides a multifaceted record of this macroevolutionary pattern.     

Analysis of the C4 genes in baleen whales using a human cDNA probe

We have used a human C4 cDNA probe to investigate the complement component C4 gene in four members of the family Balaenopteridae: fin whale (Balaenoptera physalus), sei whale (B. borealis), minke whale (B. acutorostrata), and bryde's whale (B. edeni). Restriction mapping of genomic DNA from the first three species suggests the presence of only one locus in these species, and also shows that the C4 genes in the three species are very similar. We have used 14 restriction endonucleases to investigate the restriction fragment length polymorphism (RFLP) of fin whales, 13 enzymes for sei whales, and 8 enzymes for the minke whale. No polymorphism was seen in DNA from the five minke whale samples, but Rsa I and Taq I restriction enzymes gave polymorphism in fin and sei whales whereas Hind III and Msp I restriction enzymes showed polymorphism in sei whales only. Only one bryde's whale sample was available for investigation. The study of DNA available from mother-fetus pairs from the two polymorphic species demonstrated a simple, two-allele transmission of RFLP alleles.     

Determinants of echolocation click frequency characteristics in small toothed whales: recent advances from anatomical information

1. The pulse-like clicking sounds made by odontocetes for echolocation (biosonar) can be roughly classified by their frequency characteristics into narrow-band high-frequency (NBHF) clicks with a sharp peak at around 130 kHz and wide-band (WB) clicks with a moderate peak at 30–100 kHz. Structural differences in the sound-producing organs between NBHF species and WB species have not been comprehensively discussed, nor has the formation of NBHF and WB clicks.
2. A review of the sound-producing organs, including the latest findings, could lead to a new hypothesis about the sound production mechanisms. In the current review, data on echolocation click characteristics and on the anatomical structure of the sound-producing organs were compared in 33 species (14 NBHF species and 19 WB species).
3. We review interspecific information on the characteristics of click frequencies and data from computed tomography scans and morphology of the sound-producing organs, accumulated in conventional studies. The morphology of several characteristic structures, such as the melon, the dense connective tissue over the melon (the ‘porpoise capsule’), and the vestibular sacs, was compared interspecifically.
4. Interspecific comparisons suggest that the presence or absence of the porpoise capsule is unlikely to affect echolocation frequency. Folded structures in the vestibular sacs, features that have been overlooked until now, are present in most species with NBHF sound production and not in WB species; the vestibular sacs are therefore likely to be important in determining echolocation click frequency characteristics. The acoustical properties of the shape of the melon and vestibular sacs are important topics for future investigations about the relationship between anatomical structure and sound-producing mechanisms for echolocation clicks.

     

Molecular cloning and characterization of two novel fructose-specific transporters from the osmotolerant and fructophilic yeast Candida magnoliae JH110

Sugar transport is very critical in developing an efficient and rapid conversion process of a mixture of sugars by engineered microorganisms. By using expressed sequence tag data generated for the fructophilic yeast Candida magnoliae JH110, we identified two fructose-specific transporters, CmFSY1 and CmFFZ1, which show high homology with known fructose transporters of other yeasts. The CmFSY1 and CmFFZ1 genes harbor no introns and encode proteins of 574 and 582 amino acids, respectively. Heterologous expression of the two fructose-specific transporter genes in a Saccharomyces cerevisiae, which is unable to utilize hexoses, revealed that both transporters are functionally expressed and specifically transport fructose. These results were further corroborated by kinetic analysis of the fructose transport that showed that CmFsy1p is a high-affinity fructose–proton symporter with low capacity (K _M?=?0.13?±?0.01 mM, V _max?=?2.1?±?0.3 mmol h^?1 [gdw]^?1) and that CmFfz1p is a low-affinity fructose-specific facilitator with high capacity (K _M?=?105?±?12 mM, V _max?=?8.6?±?0.7 mmol h^?1 [gdw]^?1). These fructose-specific transporters can be used for improving fructose transport in engineered microorganisms for the production of biofuels and chemicals from fructose-containing feedstock.     

Odontobius (Nematoda, Monhysteridae) from the baleen plates of whales and its relationship to Gammarinema living on crustaceans

Based on new material, the poorly known nematode species Odontobius ceti Roussel de Vauzème, 1834 is redescribed. It lives on the baleen plates of the baleen whales. It is argued that it belongs to the Monhysteridae sensu Lorenzen. Within this family, Odontobius appears to be most closely related to Gammarinema, species of which live externally on peracarid and decapod crustaceans. It is suggested that Odontobius ceti or its ancestor lived externally on crustaceans which were (or still are?) of nutritional importance to baleen whales and that in the course of feeding on these crustaceans the nematode became adapted to its current biotope.     

Intense ultrasonic clicks from echolocating toothed whales do not elicit anti-predator responses or debilitate the squid Loligo pealeii

Toothed whales use intense ultrasonic clicks to echolocate prey and it has been hypothesized that they also acoustically debilitate their prey with these intense sound pulses to facilitate capture. Cephalopods are an important food source for toothed whales, and there has probably been an evolutionary selection pressure on cephalopods to develop a mechanism for detecting and evading sound-emitting toothed whale predators. Ultrasonic detection has evolved in some insects to avoid echolocating bats, and it can be hypothesized that cephalopods might have evolved similar ultrasound detection as an anti-predation measure. We test this hypothesis in the squid Loligo pealeii in a playback experiment using intense echolocation clicks from two squid-eating toothed whale species. Twelve squid were exposed to clicks at two repetition rates (16 and 125 clicks per second) with received sound pressure levels of 199-226 dB re1 microPa (pp) mimicking the sound exposure from an echolocating toothed whale as it approaches and captures prey. We demonstrate that intense ultrasonic clicks do not elicit any detectable anti-predator behaviour in L. pealeii and that clicks with received levels up to 226 dB re1 microPa (pp) do not acoustically debilitate this cephalopod species.     

Comparative morphology and evolution of the otic region in toothed whales (Cetacea, Mammalia)

The otic region in the skull of archeocetes and odontocetes is compared and interpreted with special emphasis on the morphology and suspension of the ear bones. In archeocetes, the periotic was obviously separate from the mastoid but still integrated within the skull via a long anterior and posterior process. The rotation of the cochlear part of the periotic was already obvious. The tympanic bone was attached to a decreasing number of neighboring elements, with the periotic becoming more and more important in the later archeocetes. The accessory air sacs of the tympanic cavity had invaded some of the adjacent skeletal elements and attained a moderate-to-remarkable extension. In the evolution of the odontocetes, the periotic and tympanic were successively uncoupled from the skull and combined to a new morphological and functional unit (tympanoperiotic complex). This uncoupling was mainly achieved by shortening the periotical processes and simultaneously extending the tympanic air sacs. For functional reasons, however, the periotic (posterior process) stayed in immediate contact with the mastoid, the latter remaining in the lateral wall of skull. In advanced marine dolphins, the bony sheaths of the accessory air sacs are largely reduced, presumably because of volume fluctuations in the tympanic cavity during diving. The perfect uncoupling of the ear bones from the skull obviously was an essential prerequisite for directional hearing, for effective ultrasound orientation and communication, and finally, for the striking development of the dolphin brain.