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The parasitic nematode Crassicauda sp. was initially described in kogiid whales from specimens collected within cervical tissues, uncommon sites of infection for this parasite. Crassicauda sp. has only been reported in Kogia breviceps to date, but no study has yet investigated a large sample of both kogiid species. A 15 yr record of 104 kogiid strandings (K. sima, n = 40; K. breviceps, n = 64) in North Carolina and Virginia, U.S.A. was used to determine the prevalence of Crassicauda sp. across species, within species across sex, and within sex across length and life history categories. Crassicauda sp. was confirmed to be a species-specific parasite among kogiids infecting only K. breviceps (prevalence = 45%). Within K. breviceps, prevalence was similar (45%) in both immature and mature males, but increased from 10% in immature to 76% in mature females. This study confirmed the cervico-thoracic distribution of the parasite, and identified a novel site of infection in a previously undescribed exocrine gland associated with the pigmented “false gill slit.” The species-specific nature of Crassicauda sp. infection, the exocrine gland, and the distinct features of the false gill slit pigmentation associated with the gland, are all useful characters to identify kogiid species in the field.

Whales are important model systems for understanding the physiological and ecological consequences of extreme body size. However, whales are also some of the most difficult animals to study because their large size precludes experimental studies under controlled conditions. Here we review a wide range of morphological studies that enable greater inference of physiological processes. In particular, we focus on baleen whales that exhibit extensive diving and foraging adaptations. Using morphological data, we (i) explore the biomechanics and sensory physiology of lunge-feeding rorqual whales (Balaenopteridae), (ii) determine the effects of scale and diving pressures on the circulatory physiology of fin whales (Balaenoptera physalus (L., 1758)), and (iii) better understand the adaptations of the cetacean respiratory system that facilitate a fully aquatic life history. These studies underscore the value of understanding functional morphology in animals that cannot be studied using traditional laboratory techniques.

Marine mammals are repeatedly exposed to elevated extra-thoracic pressure and alveolar collapse during diving and readily experience alveolar expansion upon inhalation – a unique capability as compared to terrestrial mammals. How marine mammal lungs overcome the challenges of frequent alveolar collapse and recruitment remains unknown. Recent studies indicate that pinniped lung surfactant has more anti-adhesive components compared to terrestrial mammals, which would aid in alveolar opening. However, pulmonary surfactant composition has not yet been investigated in odontocetes, whose physiology and diving behavior differ from pinnipeds. The aim of this study was to investigate the phosphatidylcholine (PC) composition of lung surfactants from various marine mammals and compare these to a terrestrial mammal. We found an increase in anti-adhesive PC species in harp seal (Pagophilus groenlandicus) and California sea lion (Zalophus californianus) compared to dog (Canus lupus familiaris), as well as an increase in the fluidizing PCs 16:0/14:0 and 16:0/16:1 in pinnipeds compared to odontocetes. The harbor porpoise (a representative of the odontocetes) did not have higher levels of fluidizing PCs compared to dog. Our preliminary results support previous findings that pinnipeds may have adapted unique surfactant compositions that allow them to dive at high pressures for extended periods without adverse effects. Future studies will need to investigate the differences in other surfactant components to fully assess the surfactant composition in odontocetes.

Cetaceans span a large range of body sizes and include species with the largest known locomotor muscles. To date, force output and thrust production have only been directly measured in the common bottlenose dolphin (Tursiops truncatus), although thrust forces have been hydrodynamically modeled for some whales. In this study, two metrics of epaxial muscle size—cross-sectional area (CSA) and mass—were used to estimate force output for 22 species (n = 83 specimens) ranging in size from bottlenose dolphins to blue whales (Balaenoptera musculus). Relative to total body length (TL), maximum force output estimated based upon both muscle CSA (TL1.56 ± 0.05) and mass (TL2.64 ± 0.07) scaled at rates lower than those predicted by geometric scaling, suggesting relative force output decreases with increasing body size in cetaceans. Estimated maximal force outputs were compared to both published drag forces and to the breaking strengths of commercial fishing lines known to entangle whales. The breaking strengths of these lines are within the same order of magnitude, and in some cases, exceed the estimated maximal force output of whales. These results suggest that while powerful animals, large whales may be unable to break the extremely strong fishing line used today.

The tongue of rorqual (balaenopterid) whales slides far down the throat into the expanded oral pouch as an enormous mouthful of water is engulfed during gulp feeding. As the tongue and adjacent oral floor expands and slides caudoventrally, it glides along a more superficial (outer) layer of ventral body wall musculature, just deep to the accordion-like ventral throat pleats. We hypothesize that this sliding movement of adjacent musculature is facilitated by a slick, stretchy layer of loose areolar connective tissue that binds the muscle fibers and reduces friction: fascia. Gross anatomical examination of the gular region of adult minke, fin, and humpback whales confirms the presence of a discrete, three-layered sublingual fascia interposed between adhering fasciae of the tongue and body wall. Histological analysis of this sublingual fascia reveals collagen and elastin fibers loosely organized in a random feltwork along with numerous fibroblasts in a watery extracellular matrix. Biomechanical testing of tissue samples in the field and laboratory, via machine-controlled or manual stretching, demonstrates expansion of the sublingual fascia and its three layers up to 250% beyond resting dimensions, with slightly more extension observed in anteroposterior (rather than mediolateral or oblique) stretching, and with the most superficial of the fascia's three layers. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:735-744, 2019. © 2018 Wiley Periodicals, Inc.

Cetaceans possess diverse adaptations in respiratory structure and mechanics that are highly specialized for an array of surfacing and diving behaviors. Some of these adaptations and air management strategies are still not completely understood despite over a century of study. We have compiled the historical and contemporary knowledge of cetacean lung anatomy and mechanics in regards to normal lung function during ventilation and air management while diving. New techniques are emerging utilizing pulmonary mechanics to measure lung function in live cetaceans. Given the diversity of respiratory adaptations in cetaceans, interpretations of these results should consider species-specific anatomy, mechanics, and behavior.

SUMMARYFin whales have an incompliant aorta, which, we hypothesize, represents an adaptation to large, depth-induced variations in arterial transmural pressures. We hypothesize these variations arise from a limited ability of tissues to respond to rapid changes in ambient ocean pressures during a dive. We tested this hypothesis by measuring arterial mechanics experimentally and modelling arterial transmural pressures mathematically. The mechanical properties of mammalian arteries reflect the physiological loads they experience, so we examined a wide range of fin whale arteries. All arteries had abundant adventitial collagen that was usually recruited at very low stretches and inflation pressures (2–3 kPa), making arterial diameter largely independent of transmural pressure. Arteries withstood significant negative transmural pressures (−7 to −50 kPa) before collapsing. Collapse was resisted by recruitment of adventitial collagen at very low stretches. These findings are compatible with the hypothesis of depth-induced variation of arterial transmural pressure. Because transmural pressures depend on thoracic pressures, we modelled the thorax of a diving fin whale to assess the likelihood of significant variation in transmural pressures. The model predicted that deformation of the thorax body wall and diaphragm could not always equalize thoracic and ambient pressures because of asymmetrical conditions on dive descent and ascent. Redistribution of blood could partially compensate for asymmetrical conditions, but inertial and viscoelastic lag necessarily limits tissue response rates. Without pressure equilibrium, particularly when ambient pressures change rapidly, internal pressure gradients will develop and expose arteries to transient pressure fluctuations, but with minimal hemodynamic consequence due to their low compliance.

Cetaceans possess diverse adaptations in respiratory structure and mechanics that are highly specialized for an array of surfacing and diving behaviors. Some of these adaptations and air management strategies are still not completely understood despite over a century of study. We have compiled the historical and contemporary knowledge of cetacean lung anatomy and mechanics in regards to normal lung function during ventilation and air management while diving. New techniques are emerging utilizing pulmonary mechanics to measure lung function in live cetaceans. Given the diversity of respiratory adaptations in cetaceans, interpretations of these results should consider species-specific anatomy, mechanics, and behavior.

Shallow-diving, coastal bottlenose dolphins (Tursiops truncatus) and deep-diving, pelagic pygmy and dwarf sperm whales (Kogia breviceps and K. sima) will experience vastly different ambient pressures at depth, which will influence the volume of air within their lungs and potentially the degree of thoracic collapse they experience. This study tested the hypotheses that lung size will be reduced and/or thoracic mobility will be enhanced in deeper divers. Lung mass (T. truncatus, n = 106; kogiids, n = 18) and lung volume (T. truncatus, n = 5; kogiids, n = 4), relative to total body mass, were compared. One T. truncatus and one K. sima were cross-sectioned to calculate lung, thoracic vasculature, and other organ volumes. Excised thoraxes (T. truncatus, n = 3; kogiids, n = 4) were mechanically manipulated to compare changes in thoracic cavity shape and volume. Kogiid lungs were half the mass and one-fifth the volume of those of similarly sized T. truncatus. The lungs occupied only 15% of the total thoracic cavity volume in K. sima and 37% in T. truncatus. The kogiid and dolphin thoraxes underwent similar changes in shape and volume, although the width of the thoracic inlet was relatively constrained in kogiids. A broader phylogenetic comparison demonstrated that the ratio of lung mass to total body mass in kogiids, physeterids, and ziphiids was similar to that of terrestrial mammals, while delphinids and phocoenids possessed relatively large lungs. Thus, small lung size in deep-diving odontocetes may be a plesiomorphic character. The relatively large lung size of delphinids and phocoenids appears to be a derived condition that may permit the lung to function as a site of respiratory gas exchange throughout a dive in these rapid breathing, short-duration, shallow divers.

Most mammals possess stamina because their locomotor and respiratory (i.e. ventilatory) systems are mechanically coupled. These systems are decoupled, however, in bottlenose dolphins (Tursiops truncatus) as they swim on a breath-hold. Locomotion and ventilation appear to be coupled only during their brief surfacing event, when they respire explosively (up to 90% of total lung volume in approximately 0.3s) (Ridgway et al., 1969). The predominantly slow-twitch fiber profile of their diaphragm (Dearolf, 2003) suggests that this muscle does not likely power their rapid ventilatory event. Based upon Bramble’s (1989) biomechanical model of locomotor-respiratory coupling in galloping mammals, I hypothesized that muscles located within the cranial-cervical and lumbo-pelvic units, which act upon the thoracic unit, function to power ventilation in bottlenose dolphins. I also hypothesized that these muscles would be composed predominantly of fast-twitch fibers to facilitate the bottlenose dolphin’s rapid ventilation. The gross morphology (n=6) of cranio-cervical (sternomastoid, sternohyoid, scalenes), thoracic (intercostals), and lumbo-pelvic (rectus abdominis, abdominal obliques, hypaxialis) muscles and the fiber-type profiles (n=6) of selected muscles (sternohyoid, sternomastoid, and rectus abdominis) of bottlenose dolphins were investigated. Physical manipulations of excised thoracic units were carried out to investigate potential actions of these muscles. Results suggest that the cranio-cervical muscles act to draw the sternum and associated ribs cranio-dorsally, which flares the ribs laterally, and increases thoracic cavity volume required for inspiration. The thoracic muscles physically link the ribs to create a single functional unit; these muscles can also act to control the size of the intercostal space. The lumbo-pelvic muscles act to draw the sternum and caudal ribs caudally, which decreases the volume of the thoracic and abdominal cavities required for expiration. All muscles investigated were composed predominantly of fast-twitch fibers (range 72-88% by area) and appear histochemically poised for rapid contraction. These combined results suggest that dolphins utilize muscles, similar to those used by galloping mammals, to power their explosive ventilation. However, the mechanisms that permit dolphins to selectively couple and uncouple their locomotor and ventilatory systems, depending upon whether they are respiring at the surface or swimming on a breath-hold, remain unknown.

SummaryRorqual whales (Balaenopteridae) are among the largest vertebrates that have ever lived and include blue (Balaenoptera musculus) and fin (Balaenoptera physalus) whales. Rorquals differ from other baleen whales (Mysticeti) in possessing longitudinal furrows or grooves in the ventral skin that extend from the mouth to the umbilicus. This ventral grooved blubber directly relates to their intermittent lunge feeding strategy, which is unique among vertebrates and was potentially an evolutionary innovation that led to gigantism in this lineage [1]. This strategy involves the rorqual whale rapidly engulfing a huge volume of prey-laden water and then concentrating the prey by more slowly expelling the water through baleen plates (Figure 1A). The volume of water engulfed during a lunge can exceed the volume of the whale itself [2]. During engulfment, the whale accelerates, opens its jaw until it is almost perpendicular to the rostrum, and then the highly compliant floor of the oral cavity is inflated by the incoming water [3]. The floor of the oral cavity expands by inversion of the tongue and ballooning of the adjacent floor of the mouth into the cavum ventrale, an immense fascial pocket between the body wall and overlying blubber layer that reaches as far back as the umbilicus. The ventral grooved blubber in fin whales expands by an estimated 162% in the circumferential direction and 38% longitudinally [4]. In fin whales, multiple lunges can occur during a single dive, and the average time between lunges is just over forty seconds [3]. Here, we show that nerves in the floor of the oral cavity of fin whales are highly extensible.