Early Development and Orientation of the Acoustic Funnel Provides Insight into the Evolution of Sound Reception Pathways in Cetaceans

Whales receive underwater sounds through a fundamentally different mechanism than their close terrestrial relatives. Instead of hearing through the ear canal, cetaceans hear through specialized fatty tissues leading to an evolutionarily novel feature: an acoustic funnel located anterior to the tympanic aperture. We traced the ontogenetic development of this feature in 56 fetal specimens from 10 different families of toothed (odontocete) and baleen (mysticete) whales, using X-ray computed tomography. We also charted ear ossification patterns through ontogeny to understand the impact of heterochronic developmental processes. We determined that the acoustic funnel arises from a prominent V-shaped structure established early in ontogeny, formed by the malleus and the goniale. In odontocetes, this V-formation develops into a cone-shaped funnel facing anteriorly, directly into intramandibular acoustic fats, which is likely functionally linked to the anterior orientation of sound reception in echolocation. In contrast, the acoustic funnel in balaenopterids rotates laterally, later in fetal development, consistent with a lateral sound reception pathway. Balaenids and several fossil mysticetes retain a somewhat anteriorly oriented acoustic funnel in the mature condition, indicating that a lateral sound reception pathway in balaenopterids may be a recent evolutionary innovation linked to specialized feeding modes, such as lunge-feeding.     

Morphological variation among the inner ears of extinct and extant baleen whales (Cetacea: Mysticeti)

Living mysticetes (baleen whales) and odontocetes (toothed whales) differ significantly in auditory function in that toothed whales are sensitive to high‐frequency and ultrasonic sound vibrations and mysticetes to low‐frequency and infrasonic noises. Our knowledge of the evolution and phylogeny of cetaceans, and mysticetes in particular, is at a point at which we can explore morphological and physiological changes within the baleen whale inner ear. Traditional comparative anatomy and landmark‐based 3D‐geometric morphometric analyses were performed to investigate the anatomical diversity of the inner ears of extinct and extant mysticetes in comparison with other cetaceans. Principal component analyses (PCAs) show that the cochlear morphospace of odontocetes is tangential to that of mysticetes, but odontocetes are completely separated from mysticetes when semicircular canal landmarks are combined with the cochlear data. The cochlea of the archaeocete Zygorhiza kochii and early diverging extinct mysticetes plot within the morphospace of crown mysticetes, suggesting that mysticetes possess ancestral cochlear morphology and physiology. The PCA results indicate variation among mysticete species, although no major patterns are recovered to suggest separate hearing or locomotor regimes. Phylogenetic signal was detected for several clades, including crown Cetacea and crown Mysticeti, with the most clades expressing phylogenetic signal in the semicircular canal dataset. Brownian motion could not be excluded as an explanation for the signal, except for analyses combining cochlea and semicircular canal datasets for Balaenopteridae. J. Morphol. 277:1599–1615, 2016. © 2016 Wiley Periodicals, Inc.     

Fin Whale Sound Reception Mechanisms: Skull Vibration Enables Low-Frequency Hearing

Hearing mechanisms in baleen whales (Mysticeti) are essentially unknown but their vocalization frequencies overlap with anthropogenic sound sources. Synthetic audiograms were generated for a fin whale by applying finite element modeling tools to X-ray computed tomography (CT) scans. We CT scanned the head of a small fin whale (Balaenoptera physalus) in a scanner designed for solid-fuel rocket motors. Our computer (finite element) modeling toolkit allowed us to visualize what occurs when sounds interact with the anatomic geometry of the whale’s head. Simulations reveal two mechanisms that excite both bony ear complexes, (1) the skull-vibration enabled bone conduction mechanism and (2) a pressure mechanism transmitted through soft tissues. Bone conduction is the predominant mechanism. The mass density of the bony ear complexes and their firmly embedded attachments to the skull are universal across the Mysticeti, suggesting that sound reception mechanisms are similar in all baleen whales. Interactions between incident sound waves and the skull cause deformations that induce motion in each bony ear complex, resulting in best hearing sensitivity for low-frequency sounds. This predominant low-frequency sensitivity has significant implications for assessing mysticete exposure levels to anthropogenic sounds. The din of man-made ocean noise has increased steadily over the past half century. Our results provide valuable data for U.S. regulatory agencies and concerned large-scale industrial users of the ocean environment. This study transforms our understanding of baleen whale hearing and provides a means to predict auditory sensitivity across a broad spectrum of sound frequencies.     

Cetaceans on a molecular fast track to ultrasonic hearing

The early radiation of cetaceans coincides with the origin of?their defining ecological and sensory differences [1, 2]. Toothed whales (Odontoceti) evolved echolocation for hunting 36-34 million years ago, whereas baleen whales (Mysticeti) evolved filter feeding and do not echolocate [2]. Echolocation in toothed whales demands exceptional high-frequency hearing [3], and both echolocation and ultrasonic hearing have also evolved independently in bats [4, 5]. The motor protein Prestin that drives the electromotility of the outer hair cells (OHCs) is likely to be especially important in ultrasonic hearing, because it is the vibratory response of OHC to incoming sound waves that confers the enhanced sensitivity and selectivity of the mammalian auditory system [6, 7]. Prestin underwent adaptive change early in mammal?evolution [8] and also shows sequence convergence between bats and dolphins [9, 10], as well as within bats [11]. Focusing on whales, we show for the first time that the extent of protein evolution in Prestin can be linked directly to the evolution of high-frequency hearing. Moreover, we find that independent cases of sequence convergence in mammals have involved numerous identical amino acid site replacements. Our findings shed new light on the?importance of Prestin in the evolution of mammalian hearing.     

Snake bioacoustics: toward a richer understanding of the behavioral ecology of snakes

Snakes are frequently described in both popular and technical literature as either deaf or able to perceive only groundborne vibrations. Physiological studies have shown that snakes are actually most sensitive to airborne vibrations. Snakes are able to detect both airborne and groundborne vibrations using their body surface (termed somatic hearing) as well as from their inner ears. The central auditory pathways for these two modes of "hearing" remain unknown. Recent experimental evidence has shown that snakes can respond behaviorally to both airborne and groundborne vibrations. The ability of snakes to contextualize the sounds and respond with consistent predatory or defensive behaviors suggests that auditory stimuli may play a larger role in the behavioral ecology of snakes than was previously realized. Snakes produce sounds in a variety of ways, and there appear to be multiple acoustic Batesian mimicry complexes among snakes. Analyses of the proclivity for sound production and the acoustics of the sounds produced within a habitat or phylogeny specific context may provide insights into the behavioral ecology of snakes. The relatively low information content in the sounds produced by snakes suggests that these sounds are not suitable for intraspecific communication. Nevertheless, given the diversity of habitats in which snakes are found, and their dual auditory pathways, some form of intraspecific acoustic communication may exist in some species.     

Auditory temporal resolution and evoked responses to pulsed sounds for the Yangtze finless porpoises (<Emphasis Type="Italic">Neophocaena phocaenoides asiaeorientalis</Emphasis>)

Temporal cues are important for some forms of auditory processing, such as echolocation. Among odontocetes (toothed whales, dolphins, and porpoises), it has been suggested that porpoises may have temporal processing abilities which differ from other odontocetes because of their relatively narrow auditory filters and longer duration echolocation signals. This study examined auditory temporal resolution in two Yangtze finless porpoises (Neophocaena phocaenoides asiaeorientalis) using auditory evoked potentials (AEPs) to measure: (a) rate following responses and modulation rate transfer function for 100 kHz centered pulse sounds and (b) hearing thresholds and response amplitudes generated by individual pulses of different durations. The animals followed pulses well at modulation rates up to 1,250 Hz, after which response amplitudes declined until extinguished beyond 2,500 Hz. The subjects had significantly better hearing thresholds for longer, narrower-band pulses similar to porpoise echolocation signals compared to brief, broadband sounds resembling dolphin clicks. Results indicate that the Yangtze finless porpoise follows individual acoustic signals at rates similar to other odontocetes tested. Relatively good sensitivity for longer duration, narrow-band signals suggests that finless porpoise hearing is well suited to detect their unique echolocation signals.     

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.     

Distribution and development of the highly specialized lipids in the sound reception systems of dolphins

Fat bodies in the heads of toothed whales, which serve to transmit and receive sound, represent extraordinary examples of physiological specialization in adipose tissues among mammals, yet we know surprisingly little about their biochemical composition. We describe the spatial distributions and development of unusual endogenous lipids (branched-chain [“iso”] molecules and wax esters) in the mandibular fat bodies of bottlenose dolphins (Tursiops truncatus) using an ontogenetic series (fetus to adult; n = 10). Although concentrations of iso-acids, iso-alcohols and waxes were lower in younger dolphins than in adults, the same relative spatial arrangement was present in all age classes, implying a set “pattern” of acoustic lipid distribution that is established very early in life. In all age classes, a small region of blubber overlying the lateral region contained unusually high concentrations of iso-acids, exhibiting a tenfold increase over “normal” adjacent blubber. Being chemically more similar to the acoustic fat bodies, this region may serve as an entry point for sound into the head. Developmental accumulations of some iso-acids and iso-alcohols occurred more rapidly than others, implying that not only are the spatial distributions of branched-chain molecules under extremely fine-scale control, but the regulatory mechanisms controlling acoustic lipid synthesis are also highly complex.     

Hearing loss in stranded odontocete dolphins and whales

The causes of dolphin and whale stranding can often be difficult to determine. Because toothed whales rely on echolocation for orientation and feeding, hearing deficits could lead to stranding. We report on the results of auditory evoked potential measurements from eight species of odontocete cetaceans that were found stranded or severely entangled in fishing gear during the period 2004 through 2009. Approximately 57% of the bottlenose dolphins and 36% of the rough-toothed dolphins had significant hearing deficits with a reduction in sensitivity equivalent to severe (70-90 dB) or profound (>90 dB) hearing loss in humans. The only stranded short-finned pilot whale examined had profound hearing loss. No impairments were detected in seven Risso's dolphins from three different stranding events, two pygmy killer whales, one Atlantic spotted dolphin, one spinner dolphin, or a juvenile Gervais' beaked whale. Hearing impairment could play a significant role in some cetacean stranding events, and the hearing of all cetaceans in rehabilitation should be tested.     

STRUCTURE AND FUNCTION IN WHALE EARS

ABSTRACT

Ultrasonic echolocation abilities are well documented in several dolphin species, but hearing characteristics are unknown for most whales. Vocalization data suggest whale hearing spans infra- to ultrasonic ranges. This paper presents an overview of whale ear anatomy and analyzes 1) how whale ears are adapted for underwater hearing and 2) how inner ear differences relate to different hearing capacities among whales.

Whales have adaptations for rapid, deep diving and long submersion; e.g., broad- bore Eustachian tubes, no pinnae, and no air-filled external canals, that impact sound reception. In odontocetes, two soft tissue channels conduct sound to the ear. In mysticetes, bone and soft tissue conduction are likely. The middle ear is air-filled but has an extensible mucosa. Cochlear structures are hypertrophied and vestibular components are reduced. Auditory ganglion cell densities are double land mammal averages (2000–4000/mm). Basilar membrane lengths range 20–70 mm; gradients are larger than in terrestrial mammals. Odontocetes have 20–60% bony membrane support and basal ratios >0.6, consistent with hearing >150 kHz. Mysticetes have apical ratios <0.002 and no bony lateral support, implying acute infrasonic hearing. Cochlear hypertrophy may be adaptive for high background noise. Vestibular loss is consistent with cervical fusion. Exceptionally high auditory fiber counts suggest both mysticetes and odontocetes have ears “wired” for more complex signal processing mechanisms than most land mammals.     

Potential effects of underwater noise from wind turbines on the marbled rockfish (Sebasticus marmoratus)

Environmental assessments of underwater noise on marine species must be based on species-specific hearing abilities. This study was to assess the potential impact of underwater noise from the East China Sea Bridge wind farm on the acoustic communication of the marbled rockfish. Here, the 1/3 octave frequency band of underwater noise was 125 Hz with the level range of 78–96 dB re 1 μPa, recorded at distances between 15-20m from the foundation at wind speed of 3–5 m/s. Auditory evoked potential (AEP) and passive acoustic techniques were used to determine the hearing abilities and sound production of the fish. The resultes showed the lowest auditory threshold of Sebastiscus marmoratus was 70 dB at 150 Hz matching the disturbance sound ranging 140–180 Hz, which indicating the acoustic communication used in this species. However, the frequency and level of turbine underwater noise overlapped the auditory sensitivity and vocalization of Sebastiscus marmoratus. The wind turbine noise could be detected by fish and may have a masking effect on their acoustic communication. This result can be applied for further to the assessent of fish species released into offshore wind farm marine ranch.     

Clicking in Shallow Rivers: Short-Range Echolocation of Irrawaddy and Ganges River Dolphins in a Shallow,Acoustically Complex Habitat

Toothed whales (Cetacea, odontoceti) use biosonar to navigate their environment and to find and catch prey. All studied toothed whale species have evolved highly directional, high-amplitude ultrasonic clicks suited for long-range echolocation of prey in open water. Little is known about the biosonar signals of toothed whale species inhabiting freshwater habitats such as endangered river dolphins. To address the evolutionary pressures shaping the echolocation signal parameters of non-marine toothed whales, we investigated the biosonar source parameters of Ganges river dolphins (Platanista gangetica gangetica) and Irrawaddy dolphins (Orcaella brevirostris) within the river systems of the Sundarban mangrove forest. Both Ganges and Irrawaddy dolphins produced echolocation clicks with a high repetition rate and low source level compared to marine species. Irrawaddy dolphins, inhabiting coastal and riverine habitats, produced a mean source level of 195 dB (max 203 dB) re 1 µPa_pp whereas Ganges river dolphins, living exclusively upriver, produced a mean source level of 184 dB (max 191) re 1 µPa_pp. These source levels are 1–2 orders of magnitude lower than those of similar sized marine delphinids and may reflect an adaptation to a shallow, acoustically complex freshwater habitat with high reverberation and acoustic clutter. The centroid frequency of Ganges river dolphin clicks are an octave lower than predicted from scaling, but with an estimated beamwidth comparable to that of porpoises. The unique bony maxillary crests found in the Platanista forehead may help achieve a higher directionality than expected using clicks nearly an octave lower than similar sized odontocetes.     

Calling under pressure: short-finned pilot whales make social calls during deep foraging dives

Toothed whales rely on sound to echolocate prey and communicate with conspecifics, but little is known about how extreme pressure affects pneumatic sound production in deep-diving species with a limited air supply. The short-finned pilot whale (Globicephala macrorhynchus) is a highly social species among the deep-diving toothed whales, in which individuals socialize at the surface but leave their social group in pursuit of prey at depths of up to 1000 m. To investigate if these animals communicate acoustically at depth and test whether hydrostatic pressure affects communication signals, acoustic DTAGs logging sound, depth and orientation were attached to 12 pilot whales. Tagged whales produced tonal calls during deep foraging dives at depths of up to 800 m. Mean call output and duration decreased with depth despite the increased distance to conspecifics at the surface. This shows that the energy content of calls is lower at depths where lungs are collapsed and where the air volume available for sound generation is limited by ambient pressure. Frequency content was unaffected, providing a possible cue for group or species identification of diving whales. Social calls may be important to maintain social ties for foraging animals, but may be impacted adversely by vessel noise.     

200 kHz Commercial Sonar Systems Generate Lower Frequency Side Lobes Audible to Some Marine Mammals

The spectral properties of pulses transmitted by three commercially available 200 kHz echo sounders were measured to assess the possibility that marine mammals might hear sound energy below the center (carrier) frequency that may be generated by transmitting short rectangular pulses. All three sounders were found to generate sound at frequencies below the center frequency and within the hearing range of some marine mammals, e.g. killer whales, false killer whales, beluga whales, Atlantic bottlenose dolphins, harbor porpoises, and others. The frequencies of these sub-harmonic sounds ranged from 90 to 130 kHz. These sounds were likely detectable by the animals over distances up to several hundred meters but were well below potentially harmful levels. The sounds generated by the sounders could potentially affect the behavior of marine mammals within fairly close proximity to the sources and therefore the exclusion of echo sounders from environmental impact analysis based solely on the center frequency output in relation to the range of marine mammal hearing should be reconsidered.     

Individual right whales call louder in increased environmental noise

The ability to modify vocalizations to compensate for environmental noise is critical for successful communication in a dynamic acoustic environment. Many marine species rely on sound for vital life functions including communication, navigation and feeding. The impacts of significant increases in ocean noise levels from human activities are a current area of concern for the conservation of marine mammals. Here, we document changes in calling behaviour by individual endangered North Atlantic right whales (Eubalaena glacialis) in increased background noise. Right whales, like several bird and primate species, respond to periods of increased noise by increasing the amplitude of their calls. This behaviour may help maintain the communication range with conspecifics during periods of increased noise. These call modifications have implications for conservation efforts for right whales, affecting both the way whales use sound to communicate and our ability to detect them with passive acoustic monitoring systems.     

Contribution to the study of acoustic communication in two Belgian river bullheads (<Emphasis Type="Italic">Cottus rhenanus and C. perifretum</Emphasis>) with further insight into the sound-producing mechanism

Background

The freshwater sculpins (genus Cottus) are small, bottom-living fishes widely distributed in North America and Europe. The taxonomy of European species has remained unresolved for a long time due to the overlap of morphological characters. Sound production has already been documented in some cottid representatives, with sounds being involved in courtship and agonistic interactions. Although the movements associated with sound production have been observed, the underlying mechanism remains incomplete. Here, we focus on two closely related species from Belgium: C. rhenanus and C. perifretum. This study aims 1) to record and to compare acoustic communication in both species, 2) to give further insight into the sound-producing mechanism and 3) to look for new morphological traits allowing species differentiation.

Results

Both Cottus species produce multiple-pulsed agonistic sounds using a similar acoustic pattern: the first interpulse duration is always longer, making the first pulse unit distinct from the others. Recording sound production and hearing abilities showed a clear relationship between the sound spectra and auditory thresholds in both species: the peak frequencies of calls are around 150 Hz, which corresponds to their best hearing sensitivity. However, it appears that these fishes could not hear acoustic signals produced by conspecifics in their noisy habitat considering their hearing threshold expressed as sound pressure (~ 125 dB re 1 μPa). High-speed video recordings highlighted that each sound is produced during a complete back and forth movement of the pectoral girdle.

Conclusions

Both Cottus species use an acoustic pattern that remained conserved during species diversification. Surprisingly, calls do not seem to have a communicative function. On the other hand, fish could detect substrate vibrations resulting from movements carried out during sound production. Similarities in temporal and spectral characteristics also suggest that both species share a common sound-producing mechanism, likely based on pectoral girdle vibrations. From a morphological point of view, only the shape of the spinelike scales covering the body allows species differentiation.

     

Comparing marine mammal acoustic habitats in Atlantic and Pacific sectors of the High Arctic: year-long records from Fram Strait and the Chukchi Plateau

During the International Polar Year (IPY), acoustic recorders were deployed on oceanographic moorings in Fram Strait and on the Chukchi Plateau, representing the first coordinated year-round sampling of underwater acoustic habitats at two sites in the High Arctic. Examination of species-specific marine mammal calls recorded from autumn 2008–2009 revealed distinctly different acoustic habitats at each site. Overall, the Fram Strait site was acoustically complex compared with the Chukchi Plateau site. In Fram Strait, calls from bowhead whales (Balaena mysticetus) and a variety of toothed whales (odontocetes) were recorded year-round, as were airgun pulses from seismic surveys. In addition, calls from blue whales (Balaenoptera musculus) and fin whales (B. physalus) were recorded from June to October and August to March, respectively. Conversely, at the Chukchi Plateau site, beluga (Delphinapterus leucas) and bowhead whale calls were recorded primarily from May to August, with airgun signals detected only in September–October. Ribbon seal (Phoca fasciata) calls were detected in October–November, with no marine mammals calls at all recorded from December to February. Of note, ice-adapted bearded seals (Erignathus barbatus) were recorded at both sites, primarily in spring and summer, corresponding with the mating season for that species. Differences in acoustic habitats between the two sites were related to contrasts in sea ice cover, temperature, patterns of ocean circulation and contributions from anthropogenic noise sources. These data provide a provisional baseline for the comparison of underwater acoustic habitats between Pacific and Atlantic sectors of the High Arctic.     

Observation and analysis of sonar signal generation in the bottlenose dolphin (Tursiops truncatus): Evidence for two sonar sources

Indirect evidence for multiple sonar signal generators in odontocetes exists within the published literature. To explore the long-standing controversy over the site of sonar signal generation, direct evidence was collected from three trained bottlenose dolphins (Tursiops truncatus) by simultaneously observing nasal tissue motion, internal nasal cavity pressure, and external acoustic pressure. High-speed video endoscopy revealed tissue motion within both sets of phonic lips, while two hydrophones measured acoustic pressure during biosonar target recognition. Small catheters measured air-pressure changes at various locations within the nasal passages and in the basicranial spaces. Video and acoustic records demonstrate that acoustic pulses can be generated along the phonic fissure by vibrating the phonic labia within each set of phonic lips. The left and right phonic lips are capable of operating independently or simultaneously. Air pressure in both bony nasal passages rose and fell synchronously, even if the activity patterns of the two phonic lips were different. Whistle production and increasing sound pressure levels are generally accompanied by increasing intranarial air pressure. One acoustic “click” occurred coincident with one oscillatory cycle of the phonic labia. Changes in the click repetition rate and cycles of the phonic labia were simultaneous, indicating that these events are coupled. Structural similarity in the nasal apparatus across the Odontoceti suggests that all extant toothed whales generate sonar signals using the phonic lips and similar biomechanical processes.     

Ear Structure and Function in Modern Mammals

The acoustic portions of the mammalian ear display greater morphologicaldiversity in peripheral than in central portions. In many mammalsthe pinna is of negligible auditory significance. The tympano-ossicularsystem of all mammals sensitive to air-borne sounds must transformair vibrations to fluid vibrations in the inner ear by matchingthe acoustical impedances. Within the cochlea the energy ofthe fluid vibrations is transduced into nerve impulses. In highly specialized mammals the morphology of these transformerand transducer mechanisms is adapted for the reception of extremefrequencies. Echolocating bats and whales possess different,but effective, specializations for the reception of ultrasonicfrequencies. Moles and kangaroo rats, on the other hand, havespecialized ear structures for the reception of low frequencies.