Performance evaluation of humpback whale-inspired shortboard surfing fins based on ocean wave fieldwork.

We present field results revealing improved surfing performance when a novel approach ("Real Whale", RW) is used for applying several of the humpback whale's passive flow control mechanisms, including tubercles, to surfboard fins. It is also the first study presenting evidence of dynamic performance of tubercled designs rotating on all three axes. We evaluated low aspect ratio, thruster-style 3-fin configurations used in high-performance surfing. Fieldwork involved surfing almost 2,000 ocean waves from around the world, comparing standard commercial fins with straight leading edges to RW fins. We collected surfing data from instrumentation attached to surfboards, including GPS and 9-axis motion sensors. Eighteen turn performance values were measured and calculated, including novel, surfing-specific rotational power coefficients. ANOVA revealed surfers using RW fins showed significant improvements in power generation compared to when they used standard commercial fins. Turn rates using RW fins also improved, although not significantly. We found using RW fins allowed a skilled surfer to improve their surfing performance relative to a professionally ranked surfer.

Blubber cortisol levels in humpback whales (Megaptera novaeangliae): A measure of physiological stress without effects from sampling.

Baleen whales are vulnerable to environmental impacts due to low fecundity, capital breeding strategies, and their reliance on a large amount of prey resources over large spatial scales. There has been growing interest in monitoring health and physiological stress in these species but, to date, few measures have been validated. The purpose of this study was to examine whether blubber cortisol could be used as a measure of physiological stress in humpback whales. Cortisol concentrations were initially compared between live, presumably 'healthy' whales (n = 187) and deceased whales (n = 35), which had died after stranding or entanglement, or washed ashore as a carcass. Deceased whales were found to have significantly higher cortisol levels (mean ± SD; 5.47 ± 4.52 ng/g) than live whales (0.51 ± 0.14 ng/g; p < 0.001), particularly for those animals that had experienced prolonged trauma (e.g. stranding) prior to death. Blubber cortisol levels in live whales were then examined for evidence of life history-related, seasonal, or sampling-related effects. Life history group and sampling-related factors, such as encounter time and the number of biopsy sampling attempts per animal, were found to be poor predictors of blubber cortisol levels in live whales. In contrast, blubber cortisol levels varied seasonally, with whales migrating north towards the breeding grounds in winter having significantly higher levels (0.54 ± 0.21 ng/g, p = 0.016) than those migrating south towards the feeding grounds in spring (0.48 ± 1.23 ng/g). These differences could be due to additional socio-physiological stress experienced by whales during peaks in breeding activity. Overall, blubber cortisol appears to be a suitable measure of chronic physiological stress in humpback whales.

Prenatal Development of the Humpback Whale: Growth Rate, Tooth Loss and Skull Shape Changes in an Evolutionary Framework.

Extant baleen whales (Mysticeti) share a distinct suite of extreme and unique adaptations to perform bulk filter feeding, such as a long, arched skull, and mandible and the complete loss of adult dentition in favor of baleen plates. However, mysticetes still develop tooth germs during ontogeny. In the fossil record, multiple groups document the transition from ancestral raptorial feeding to filter feeding. Fetal specimens give us an extraordinary opportunity to observe when and how this macroevolutionary transition occurs during gestation. We used iodine-enhanced and traditional CT scanning to visualize the internal anatomy of five fetuses of humpback whale representing the first two-thirds of gestation, and we combine these data with previously published reports to provide the first comprehensive qualitative description of the sequence of developmental changes that characterize the skull and dentition. We also use quantitative methods based on 3D landmarks to investigate the shape changes in the fetuses in relation to a juvenile cranial morphology. We found similarities in the ossification patterns of the humpback and other cetaceans (dolphins), but there appear to be major differences when comparing them to terrestrial artiodactyls. As for the tooth germs, this developmental sequence confirms that the tooth-to-baleen transition occurs in the last one-third of gestation. Analysis of cranial shape development revealed a progressive elongation of the rostrum and a resulting posterior movement of the nasals relative to the braincase. Future work will involve acquisition of data from other species to complete our documentation of the teeth-to-baleen transition. Anat Rec, 2018. © 2018 American Association for Anatomy.

Predator-informed looming stimulus experiments reveal how large filter feeding whales capture highly maneuverable forage fish.

The unique engulfment filtration strategy of microphagous rorqual whales has evolved relatively recently (<5 Ma) and exploits extreme predator/prey size ratios to overcome the maneuverability advantages of swarms of small prey, such as krill. Forage fish, in contrast, have been engaged in evolutionary arms races with their predators for more than 100 million years and have performance capabilities that suggest they should easily evade whale-sized predators, yet they are regularly hunted by some species of rorqual whales. To explore this phenomenon, we determined, in a laboratory setting, when individual anchovies initiated escape from virtually approaching whales, then used these results along with in situ humpback whale attack data to model how predator speed and engulfment timing affected capture rates. Anchovies were found to respond to approaching visual looming stimuli at expansion rates that give ample chance to escape from a sea lion-sized predator, but humpback whales could capture as much as 30-60% of a school at once because the increase in their apparent (visual) size does not cross their prey's response threshold until after rapid jaw expansion. Humpback whales are, thus, incentivized to delay engulfment until they are very close to a prey school, even if this results in higher hydrodynamic drag. This potential exaptation of a microphagous filter feeding strategy for fish foraging enables humpback whales to achieve 7× the energetic efficiency (per lunge) of krill foraging, allowing for flexible foraging strategies that may underlie their ecological success in fluctuating oceanic conditions.

Anatomy and Functional Morphology of the Mysticete Rorqual Whale Larynx: Phonation Positions of the U-Fold.

Many Mysticetes (baleen whales) are acoustically active marine mammals. This is epitomized by rorquals, and specifically male humpback whales (Megaptera novaeangliae) whose complex songs comprise a wide range of vocalizations. The sound production mechanism of odontocetes (toothed whales, including dolphins and porpoises) is well described, in contrast to that of mysticetes whose vocalization mechanism remains a subject of active scientific investigation. Anatomical observations and acoustic signal processing have led to divergent hypotheses under the framework of a production-based approach. We attempt to unify these hypotheses by broadening existing data with our new anatomical investigation, interpreted in light of known acoustical properties of mysticete vocalizations. We examined 15 specimens of four rorqual species: sei whale (Baleanoptera borealis), fin whale (Baleanoptera physalus), minke whale (Baleanoptera acutorostrata), and humpback whale (Megaptera novaeangliae). Based on these data and on previous literature, we propose a description of three functional positions (rest, breathing, and recirculation), unidirectional egressive airflow for sound production (from lungs to laryngeal sac), and new nomenclature for different parts of the U-fold (distal section, midsection, and corniculate flaps). Each of these sections has specific morphological and acoustical properties that support the concept of "mode variation" in baleen whale vocalizations. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:703-717, 2019. © 2018 Wiley Periodicals, Inc.

Body density of humpback whales (Megaptera novaengliae) in feeding aggregations estimated from hydrodynamic gliding performance.

Many baleen whales undertake annual fasting and feeding cycles, resulting in substantial changes in their body condition, an important factor affecting fitness. As a measure of lipid-store body condition, tissue density of a few deep diving marine mammals has been estimated using a hydrodynamic glide model of drag and buoyancy forces. Here, we applied the method to shallow-diving humpback whales (Megaptera novaeangliae) in North Atlantic and Antarctic feeding aggregations. High-resolution 3-axis acceleration, depth and speed data were collected from 24 whales. Measured values of acceleration during 5 s glides were fitted to a hydrodynamic glide model to estimate unknown parameters (tissue density, drag term and diving gas volume) in a Bayesian framework. Estimated species-average tissue density (1031.6 ± 2.1 kg m-3, ±95% credible interval) indicates that humpback whale tissue is typically negatively buoyant although there was a large inter-individual variation ranging from 1025.2 to 1043.1 kg m-3. The precision of the individual estimates was substantially finer than the variation across different individual whales, demonstrating a progressive decrease in tissue density throughout the feeding season and comparably high lipid-store in pregnant females. The drag term (CDAm-1) was estimated to be relatively high, indicating a large effect of lift-related induced drag for humpback whales. Our results show that tissue density of shallow diving baleen whales can be estimated using the hydrodynamic gliding model, although cross-validation with other techniques is an essential next step. This method for estimating body condition is likely to be broadly applicable across a range of aquatic animals and environments.

Inner ear development in cetaceans.

Cetaceans face the challenge of maintaining equilibrium underwater and obtaining sensory input within a dense, low-visibility medium. The cetacean ear represents a key innovation that marked their evolution from terrestrial artiodactyls to among the most fully aquatic mammals in existence. Using micro-CT and histological data, we document shape and size changes in the cetacean inner ear during ontogeny, and demonstrate that, as a proportion of gestation time, the cetacean inner ear is precocial in its growth compared with that of suid artiodactyls. Cetacean inner ears begin ossifying and reach near-adult shape as early as at 32% of the gestation period, and near-adult dimensions as early as at 27% newborn total length. Our earliest embryos with measurable inner ears (13% newborn length) exhibit a flattened cochlea (i.e. smaller distance from cochlear apex to round window) compared with later and adult stages. Inner ears of Sus scrofa have neither begun ossifying nor reached near-adult dimensions at 55% of the gestation period, but have an adult-like ratio of cochlear diameters to each other, suggesting an adult-like shape. The precocial development of the cetacean inner ear complements previous work demonstrating precocial development of other cetacean anatomical features such as the locomotor muscles to facilitate swimming at the moment of birth.

The neocortex of cetartiodactyls: I. A comparative Golgi analysis of neuronal morphology in the bottlenose dolphin (Tursiops truncatus), the minke whale (Balaenoptera acutorostrata), and the humpback whale (Megaptera novaeangliae).

The present study documents the morphology of neurons in several regions of the neocortex from the bottlenose dolphin (Tursiops truncatus), the North Atlantic minke whale (Balaenoptera acutorostrata), and the humpback whale (Megaptera novaeangliae). Golgi-stained neurons (n = 210) were analyzed in the frontal and temporal neocortex as well as in the primary visual and primary motor areas. Qualitatively, all three species exhibited a diversity of neuronal morphologies, with spiny neurons including typical pyramidal types, similar to those observed in primates and rodents, as well as other spiny neuron types that had more variable morphology and/or orientation. Five neuron types, with a vertical apical dendrite, approximated the general pyramidal neuron morphology (i.e., typical pyramidal, extraverted, magnopyramidal, multiapical, and bitufted neurons), with a predominance of typical and extraverted pyramidal neurons. In what may represent a cetacean morphological apomorphy, both typical pyramidal and magnopyramidal neurons frequently exhibited a tri-tufted variant. In the humpback whale, there were also large, star-like neurons with no discernable apical dendrite. Aspiny bipolar and multipolar interneurons were morphologically consistent with those reported previously in other mammals. Quantitative analyses showed that neuronal size and dendritic extent increased in association with body size and brain mass (bottlenose dolphin < minke whale < humpback whale). The present data thus suggest that certain spiny neuron morphologies may be apomorphies in the neocortex of cetaceans as compared to other mammals and that neuronal dendritic extent covaries with brain and body size.

Morphology of the eyeball from the Humpback whale (Megaptera novaeangliae).

Aquatic mammals underwent morphological and physiological adaptations due to the transition from terrestrial to aquatic environment. One of the morphological changes regards their vision since cetaceans' eyes are able to withstand mechanical, chemical, osmotic, and optical water conditions. Due to insufficient information about these animals, especially regarding their sense organs, this study aimed to describe the morphology of the Humpback whale (Megaptera novaeangliae) eyeball. Three newborn females, stranded dead on the coast of Sergipe and Bahia, Brazil, were used. Samples were fixed in a 10% formalin solution, dissected, photographed, collected, and evaluated through light and electron microscopy techniques. The Humpback whale sclera was thick and had an irregular surface with mechanoreceptors in its lamina propria. Lens was dense, transparent, and ellipsoidal, consisting of three layers, and the vascularized choroid contains melanocytes, mechanoreceptors, and a fibrous tapetum lucidum. The Humpback whale eyeball is similar to other cetaceans and suggests an adaptation to diving and migration, contributing to the perception of differences in temperature, pressure, and lighting.

Morphology and size of stem cells from mouse and whale: observational study.

OBJECTIVE: To compare the morphology and size of stem cells from two mammals of noticeably different body size. DESIGN: Observational study. SETTING: The Netherlands. PARTICIPANTS: A humpback whale (Megaptera novaeangliae) and a laboratory mouse (Mus musculus). MAIN OUTCOME MEASURES: Morphology and size of mesenchymal stem cells from adipose tissue. RESULTS: Morphologically, mesenchymal stem cells of the mouse and whale are indistinguishable. The average diameter of 50 mesenchymal stem cells from the mouse was 28 (SD 0.86) µm and 50 from the whale was 29 (SD 0.71) µm. The difference in cell size between the species was not statistically significant. Although the difference in bodyweight between the species is close to two million-fold, the mesenchymal stem cells of each were of similar size. CONCLUSIONS: The mesenchymal stem cells of whales and mice are alike, in both morphology and size.

Understanding the intentional acoustic behavior of humpback whales: a production-based approach.

Following a production-based approach, this paper deals with the acoustic behavior of humpback whales. This approach investigates various physical factors, which are either internal (e.g., physiological mechanisms) or external (e.g., environmental constraints) to the respiratory tractus of the whale, for their implications in sound production. This paper aims to describe a functional scenario of this tractus for the generation of vocal sounds. To do so, a division of this tractus into three different configurations is proposed, based on the air recirculation process which determines air sources and laryngeal valves. Then, assuming a vocal function (in sound generation or modification) for several specific anatomical components, an acoustic characterization of each of these configurations is proposed to link different spectral features, namely, fundamental frequencies and formant structures, to specific vocal production mechanisms. A discussion around the question of whether the whale is able to fully exploit the acoustic potential of its respiratory tractus is eventually provided.

The tubercles on humpback whales' flippers: application of bio-inspired technology.

The humpback whale (Megaptera novaeangliae) is exceptional among the large baleen whales in its ability to undertake aquabatic maneuvers to catch prey. Humpback whales utilize extremely mobile, wing-like flippers for banking and turning. Large rounded tubercles along the leading edge of the flipper are morphological structures that are unique in nature. The tubercles on the leading edge act as passive-flow control devices that improve performance and maneuverability of the flipper. Experimental analysis of finite wing models has demonstrated that the presence of tubercles produces a delay in the angle of attack until stall, thereby increasing maximum lift and decreasing drag. Possible fluid-dynamic mechanisms for improved performance include delay of stall through generation of a vortex and modification of the boundary layer, and increase in effective span by reduction of both spanwise flow and strength of the tip vortex. The tubercles provide a bio-inspired design that has commercial viability for wing-like structures. Control of passive flow has the advantages of eliminating complex, costly, high-maintenance, and heavy control mechanisms, while improving performance for lifting bodies in air and water. The tubercles on the leading edge can be applied to the design of watercraft, aircraft, ventilation fans, and windmills.

Quantitative computed tomography of humpback whale (Megaptera novaeangliae) mandibles: mechanical implications for rorqual lunge-feeding.

Rorqual whales (Balaenopteridae) lunge at high speed with mouth open to nearly 90 degrees to engulf large volumes of prey-laden water. This feeding process is enabled by extremely large skulls and mandibles that increase mouth area, thereby facilitating the flux of water into the mouth. When these mandibles are lowered during lunge-feeding, they are exposed to high drag, and therefore, may be subject to significant bending forces. We hypothesized that these mandibles exhibited a mechanical design (shape and density distribution) that enables these bones to accommodate high loads during lunge-feeding without exceeding their breaking strength. We used quantitative computed tomography (QCT) to determine the three-dimensional geometry and density distribution of a pair of subadult humpback whale (Megaptera novaeangliae) mandibles (length = 2.10 m). QCT data indicated highest bone density and cross-sectional area, and therefore, high resistance to bending and deflection, from the coronoid process to the middle of the dentary, which then decreased towards the anterior end of the mandible. These results differ from the caudorostral trends of increasing mandibular bone density in mammals, such as humans and the right whale, Eubalaena glacialis, indicating that adaptive bone remodeling is a significant contributing factor in establishing mandibular bone density distributions in rorquals.

Sound production by singing humpback whales.

Sounds from humpback whale songs were analyzed to evaluate possible mechanisms of sound production. Song sounds fell along a continuum with trains of discrete pulses at one end and continuous tonal signals at the other. This graded vocal repertoire is comparable to that seen in false killer whales [Murray et al. (1998). J. Acoust. Soc. Am. 104, 1679-1688] and human singers, indicating that all three species generate sounds by varying the tension of pneumatically driven, vibrating membranes. Patterns in the spectral content of sounds and in nonlinear sound features show that resonating air chambers may also contribute to humpback whale sound production. Collectively, these findings suggest that categorizing individual units within songs into discrete types may obscure how singers modulate song features and illustrate how production-based characterizations of vocalizations can provide new insights into how humpback whales sing.

Sisters of the sinuses: cetacean air sacs.

This overview assesses some distinguishing features of the cetacean (whale, dolphin, porpoise) air sac system that may relate to the anatomy and function of the paranasal sinuses in terrestrial mammals. The cetacean respiratory tract has been modified through evolution to accommodate living in water. Lack of paranasal sinuses in modern cetaceans may be a diving adaptation. Bone-enclosed air chambers are detrimental, as their rigid walls may fracture during descent/ascent due to contracting/re-expanding air volumes. Flexible-walled "sinuses" (extracranial diverticula) are a logical adaptation to diving. Odontocetes (toothed whales) exhibit several pairs of paranasal air sacs. Although fossil evidence indicates that paranasal sinuses occur in archaeocetes (ancestors/relatives of living cetaceans), it is not known whether the paranasal sacs derive from these sinuses. Sac pigmentation indicates that they derived from invaginations of the integument. Unlike sinuses, paranasal sacs are not circumferentially enclosed in bone, and therefore can accommodate air volume changes that accompany diving pressure changes. Paired pterygoid sacs, located ventrally along the cetacean skull, connect the pharynx and middle ear cavities. Mysticetes (baleen whales) have a large midline laryngeal sac. Although cetacean air sacs do not appear to be homologous to paranasal sinuses, they may serve some analogous respiratory, vocal, or structural functions. For example, these sacs may participate in gas exchange, thermoregulation, resonance, and skeletal pneumatization. In addition, they may subserve unique aquatic functions, such as increasing inspiratory volume, mitigating pressure-induced volume change, air shunting to reduce respiratory dead space, and facilitating underwater sound production and transmission.

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.

Blowing bubbles: an aquatic adaptation that risks protection of the respiratory tract in humpback whales (Megaptera novaeangliae).

Cetaceans (whales, dolphins, and porpoises) have developed extensive protective barriers to exclude water or food from the respiratory tract, including valvular nostrils, an intranarial elongated larynx, and a sphincteric soft palate. A barrier breach can be lethal, as asphyxiation may occur from incursions of water (drowning) or food (choking). Humpback whales (Megaptera novaeangliae), however, exhibit a possibly unique and paradoxical behavior concerning respiratory protection: they release a "bubble cloud" (a cluster of tiny bubbles) underwater from the mouth. How they do this remains unclear. This study tests the hypothesis that the larynx plays a role in enabling bubble cloud emission. The anatomy and position of the larynx was examined in seven specimens of Megaptera novaeangliae. Results indicate that the epiglottis can be manually removed from behind the soft palate and placed in the oral cavity during dissection. Unlike that of toothed whales (odontocetes), the humpback whale larynx does not appear to be permanently intranarial. The elongated and trough-shaped epiglottis may function as a tube when placed against the undersurface of the soft palate and, thus, facilitate channeling air from the larynx to the oral cavity. The pointed tip and lateral edges of the epiglottis fit tightly against the undersurface of the soft palate, perhaps functioning as a one-way valve that lets air out but prevents water from entering. Bubble cloud generation likely involves air passing directly from the larynx into the oral cavity, and then expulsion through the mesh of the baleen plates. A laryngeal-oral connection, however, compromises the anatomical aquatic adaptations that normally protect the respiratory tract. A potential for drowning exists during the critical interval in which the larynx is intraoral and during re-insertion back to the normal intranarial position. The retention of this risky behavior indicates the importance of bubble clouds in predator avoidance, prey capture, and/or social signaling.

Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae).

Cetaceans diverged from terrestrial mammals between 50 and 60 million years ago and acquired, during their adaptation to a fully aquatic milieu, many derived features, including echolocation (in odontocetes), remarkable auditory and communicative abilities, as well as a complex social organization. Whereas brain structure has been documented in detail in some odontocetes, few reports exist on its organization in mysticetes. We studied the cerebral cortex of the humpback whale (Megaptera novaeangliae) in comparison to another balaenopterid, the fin whale, and representative odontocetes. We observed several differences between Megaptera and odontocetes, such as a highly clustered organization of layer II over the occipital and inferotemporal neocortex, whereas such pattern is restricted to the ventral insula in odontocetes. A striking observation in Megaptera was the presence in layer V of the anterior cingulate, anterior insular, and frontopolar cortices of large spindle cells, similar in morphology and distribution to those described in hominids, suggesting a case of parallel evolution. They were also observed in the fin whale and the largest odontocetes, but not in species with smaller brains or body size. The hippocampal formation, unremarkable in odontocetes, is further diminutive in Megaptera, contrasting with terrestrial mammals. As in odontocetes, clear cytoarchitectural patterns exist in the neocortex of Megaptera, making it possible to define many cortical domains. These observations demonstrate that Megaptera differs from Odontoceti in certain aspects of cortical cytoarchitecture and may provide a neuromorphologic basis for functional and behavioral differences between the suborders as well as a reflection of their divergent evolution.