Melon and rostral muscle morphology of Gervais' beaked whale (Mesoplodon europaeus): Alternating patterns of bilateral asymmetry.

Toothed whales utilize specialized nasal structures such as the lipid-rich melon to produce sound and propagate it into the aquatic environment. Very little nasal morphology of mesoplodont beaked whales has been described in the literature, and the anatomy of the melon and associated musculature of Gervais' beaked whale (Mesoplodon europaeus) remains undescribed. Heads of three (n = 3) Gervais' beaked whales were examined in detail via dissection as well as computed tomography (CT) and magnetic resonance imaging (MRI). Two additional Gervais' beaked whale individuals (n = 2) were studied via archived CT and MRI scans. Representative transverse dissection sections of the melon were processed for polarized light imaging to verify the presence of tendons inserting into the melon tissue. Three-dimensional (3D) CT reconstructions of the melon, rostral muscles, and associated structures were performed to assess morphology and spatial relationships. In all individuals, the melon's main body demonstrated a bilaterally asymmetrical, curvilinear geometry. This curvilinear shape was defined by a pattern of alternating asymmetry in the medial rostral muscles that projected into the melon's tissue. In transverse polarized light imaging, a network of tendons originating from these asymmetrical rostral muscle projections was observed permeating the melon's lipid tissue. This curvilinear melon morphology and associated asymmetrical musculature suggest a means of lengthening the lipid pathway within a relatively short dimensional footprint. In addition, the species-specific arrangement of muscular projections suggests complex fine-tuning of the melon's geometry during echolocation. Further studies may lend additional insight into the function of this unusual melon morphology.

Fatal entanglements of sea turtles caused by widely deployed weather instruments.

Sea turtles have been found to interact with discarded fishing gear, plastic bags, and balloons, among other anthropogenic materials. One infrequently documented interaction is entanglement in scientific research instruments, which presents a unique management and mitigation challenge. This paper highlights two Kemp's ridley sea turtles that stranded ~10 years apart, deceased and entangled in weather balloons in Virginia, USA. The turtles were recovered 11 and 20 days after the balloons were launched from two different facilities along the Virginia coast in 2009 and 2019, respectively. Based on external evaluation and necropsy findings, both animals were assigned a probable cause of death of debris entanglement. This paper seeks to inform other stranding response organizations, as well as stakeholders like manufacturers and users of weather balloons, of the threats these instruments can pose to marine life. With strengthened education, collaboration, and changes in instrument design, future entanglements may be mitigated.

Gross and histological morphology of the cervical gill slit gland of the pygmy sperm whale (Kogia breviceps).

Odontocete cetaceans have undergone profound modifications to their integument and sensory systems and are generally thought to lack specialized exocrine glands that in terrestrial mammals function to produce chemical signals (Thewissen & Nummela, 2008). Keenan-Bateman et al. (2016, 2018), though, introduced an enigmatic exocrine gland, associated with the false gill slit pigmentation pattern in Kogia breviceps. These authors provided a preliminary description of this cervical gill slit gland in their helminthological studies of the parasitic nematode, Crassicauda magna. This study offers the first detailed gross and histological description of this gland and reports upon key differences between immature and mature individuals. Investigation reveals it is a complex, compound tubuloalveolar gland with a well-defined duct that leads to a large, and expandable central chamber, which in turn leads to two caudally projecting diverticula. All regions of the gland contain branched tubular and alveolar secretory regions, although most are found in the caudal diverticula, where the secretory process is holocrine. The gland lies between slips of cutaneous muscle, and is innervated by lamellar corpuscles, resembling Pacinian's corpuscles, suggesting that its secretory product may be actively expressed into the environment. Mature K. breviceps display larger gland size, and increased functional activity in glandular tissues, as compared to immature individuals. These results demonstrate that the cervical gill slit gland of K. breviceps shares morphological features of the specialized, chemical signaling, exocrine glands of terrestrial members of the Cetartiodactyla.

A Baseline Model For Estimating the Risk of Gas Embolism in Sea Turtles During Routine Dives.

Sea turtles, like other air-breathing diving vertebrates, commonly experience significant gas embolism (GE) when incidentally caught at depth in fishing gear and brought to the surface. To better understand why sea turtles develop GE, we built a mathematical model to estimate partial pressures of N2 (PN2), O2 (PO2), and CO2 (PCO2) in the major body-compartments of diving loggerheads (Caretta caretta), leatherbacks (Dermochelys coriacea), and green turtles (Chelonia mydas). This model was adapted from a published model for estimating gas dynamics in marine mammals and penguins. To parameterize the sea turtle model, we used values gleaned from previously published literature and 22 necropsies. Next, we applied this model to data collected from free-roaming individuals of the three study species. Finally, we varied body-condition and cardiac output within the model to see how these factors affected the risk of GE. Our model suggests that cardiac output likely plays a significant role in the modulation of GE, especially in the deeper diving leatherback turtles. This baseline model also indicates that even during routine diving behavior, sea turtles are at high risk of GE. This likely means that turtles have additional behavioral, anatomical, and/or physiologic adaptions that serve to reduce the probability of GE but were not incorporated in this model. Identifying these adaptations and incorporating them into future iterations of this model will further reveal the factors driving GE in sea turtles.

Comparative morphology of the spinal cord and associated vasculature in shallow versus deep diving cetaceans.

The cetacean vertebral canal houses the spinal cord and arterial supply to and venous drainage from the entire central nervous system (CNS). Thus, unlike terrestrial mammals, the cetacean spinal cord lies within a highly vascularized space. We compared spinal cord size and vascular volumes within the vertebral canal across a sample of shallow and deep diving odontocetes. We predicted that the (a) spinal cord, a metabolically expensive tissue, would be relatively small, while (b) volumes of vascular structures would be relatively large, in deep versus shallow divers. Our sample included the shallow diving Tursiops truncatus (n = 2) and Delphinus delphis (n = 3), and deep diving Kogia breviceps (n = 2), Mesoplodon europaeus (n = 2), and Ziphius cavirostris (n = 1). Whole, frozen vertebral columns were cross-sectioned at each intervertebral disc, scaled photographs of vertebral canal contents acquired, and cross-sectional areas of structures digitally measured. Areas were multiplied by vertebral body lengths and summed to calculated volumes of neural and vascular structures. Allometric analyses revealed that the spinal cord scaled with negative allometry (b = 0.51 ± 0.13) with total body mass (TBM), and at a rate significantly lower than that of terrestrial mammals. As predicted, the spinal cord represented a smaller percentage of the total vertebral canal volume in the deep divers relative to shallow divers studied, as low as 2.8% in Z. cavirostris. Vascular volume scaled with positive allometry (b = 1.2 ± 0.22) with TBM and represented up to 96.1% (Z. cavirostris) of the total vertebral canal volume. The extreme deep diving beaked whales possessed 22-35 times more vascular volume than spinal cord volume within the vertebral canal, compared with the 6-10 ratio in the shallow diving delphinids. These data offer new insights into morphological specializations of neural and vascular structures that may contribute to differential diving capabilities across odontocete cetaceans.

Macroscopic and Histopathologic Findings From a Mass Stranding of Rough-Toothed Dolphins (Steno bredanensis) in 2005 on Marathon Key, Florida, USA.

On March 2, 2005 ~70 rough-toothed dolphins (Steno bredanensis) mass stranded along mud flats and associated canals on the Atlantic Ocean side of Marathon Key, Florida. Forty-six were necropsied and placed into two groups for analysis: Group-1 animals (N = 34; 65%) that died prior to medical intervention and rehabilitative efforts and Group-2 animals (N = 12; 35%) that died in rehabilitation. Thirty-four animals were females (18 adults, 5 juvenile/subadult, 7 calves, and 4 of undetermined age) and 12 were males (6 adults, 4 juvenile/subadults, 1 calf, and 1 of undetermined age). Body condition overall was fair to good in Group-1 and fair to poor in Group-2. Lesions were observed in multiple body systems. Greater than 90% of animals in both groups had respiratory lesions. Verminous sinusitis and bronchopneumonia were 2-3 times more prevalent in Group-2. Capture/exertional rhabdomyolysis was observed in Group-2 (42%). Vacuolar hepatopathies were observed in both groups including hepatic lipidosis (Group-1) and mixed etiologies (Group-2). Pancreatic and gastrointestinal tract pathologies were prevalent in Group-2 animals 56 and 75%, respectively, and included gastritis, gastric ulceration, enterocolitis, pancreatic atrophy, and pancreatitis related to physiologic stress. Group-2 more frequently had evidence of hemorrhagic diathesis present which included increased extramedullary hematopoiesis in various organs, increased hemosiderosis, and hemorrhage and hemorrhagic drainage in various organs. Central nervous system disease, primarily edema, and mild inflammation were equally prevalent. Renal proteinuria, tubular necrosis, and pigmentary deposition were observed in Group-2. Dental attrition was observed in ~40% of the groups. Gammaherpesviral-associated pharyngeal plaques were observed in 46 and 54% of Group-1 and 2 animals, respectively. Other lesions observed were mild and incidental with a frequency rate <20%. The findings from this Steno stranding provide a unique window into baseline individual and population clinical conditions and additional perspective into potential clinical sequelae of rehabilitation efforts.

Surgical Management of a Chronic Neck Abscess in a U.S. Navy Bottlenose Dolphin.

Surgical intervention on cetaceans is rarely performed due to challenges including general anesthesia and post-operative wound healing. This report describes the evaluation and treatment of an adult female bottlenose dolphin (Tursiops truncatus) with the US Navy Marine Mammal Program, with a chronic ventral cervical abscess caused by Candida glabrata. Despite aspiration and lavage along with multiple antifungal drugs, the patient developed inspiratory stridor with decreased performance level and surgical treatment was pursued. Under general anesthesia with the dolphin in dorsal recumbency position a 12-cm longitudinal ventral midline neck incision was used for exploration. Intraoperative ultrasound aided the identification of surgical landmarks and the abscess cavity. After adequate drainage and curettage, a closed-suction drain was placed in the surgical site. Retention sutures were used to close the incision and the external drain bulb was secured to a pectoral fin strap. One-year post-op, the dolphin was clinically normal and follow-up imaging showed no significant recurrence of the abscess. This case demonstrates a novel surgical approach of managing abscesses in dolphins, including placement and management of a negative suction drain in a submerged patient. The successful collaboration between veterinary anesthesiology, veterinary medicine, radiology, and general surgery allowed the patient to continue her normal activities as a full-duty service member.

The extracranial venous system in the heads of beaked whales, with implications on diving physiology and pathogenesis.

Beaked whales are a poorly known but diverse group of whales that have received considerable attention due to strandings that have been temporally and spatially associated with naval sonar deployment. Postmortem studies on stranded carcasses have revealed lesions consistent with decompression sickness, including intravascular gas and fat emboli. These findings have been supported by analyses of intravascular gas emboli showing composition dominated by nitrogen gas. To increase our understanding of the pathophysiology of nitrogen bubble formation and intravascular embolization, we examined the gross and microscopic anatomy of the venous system in the head of beaked whales. Since the potential sources of intravascular fat and gas emboli were of greatest interest, focus was placed on the acoustic fat bodies and pneumatic accessory sinus system. Herein, we describe intimate arteriovenous associations with specialized adipose depots and air sinuses in beaked whales. These vascular structures comprise an extensive network of thin-walled vessels with a large surface area, which is likely to facilitate exchange of nitrogen gas and may, therefore, form anatomic regions that may be important in physiological management of diving gases. These structures may also be vulnerable to pathologic introduction of emboli into the vascular system. Expansive, thin-walled venous lakes are found within the pterygoid region, which suggest the potential for nitrogen exchange as well as for compensation of middle-ear pressures during descent on a dive. These findings warrant further research into the structure and function of this morphology as it relates to normal and pathologic physiology.

The extracranial arterial system in the heads of beaked whales, with implications on diving physiology and pathogenesis.

Beaked whales are medium-sized toothed whales that inhabit depths beyond the continental shelf; thus beaked whale strandings are relatively infrequent compared to those of other cetaceans. Beaked whales have been catapulted into the spotlight by their tendency to strand in association with naval sonar deployment. Studies have shown the presence of gas and fat emboli within the tissues and analysis of gas emboli is suggestive of nitrogen as the primary component. These findings are consistent with human decompression sickness (DCS) previously not thought possible in cetaceans. Because, tissue loading with nitrogen gas is paramount for the manifestation of DCS and nitrogen loading depends largely on the vascular perfusion of the tissues, we examined the anatomy of the extracranial arterial system using stranded carcasses of 16 beaked whales from five different species. Anatomic regions containing lipid and/or air spaces were prioritized as potential locations of nitrogen gas absorption due to the known solubility of nitrogen in adipose tissue and the nitrogen content of air, respectively. Attention was focused on the acoustic fat bodies and accessory sinus system on the ventral head. We found much of the arterial system of the head to contain arteries homologous to those found in domestic mammals. Robust arterial associations with lipid depots and air spaces occurred within the acoustic fat bodies of the lower jaw and pterygoid air sacs of the ventral head, respectively. Both regions contained extensive trabecular geometry with small arteries investing the trabeculae. Our findings suggest the presence of considerable surface area between the arterial system, and the intramandibular fat bodies and pterygoid air sacs. Our observations may provide support for the hypothesis that these structures play an important role in the exchange of nitrogen gas during diving.

A comparative analysis of marine mammal tracheas.

In 1940, Scholander suggested that stiffened upper airways remained open and received air from highly compressible alveoli during marine mammal diving. There are few data available on the structural and functional adaptations of the marine mammal respiratory system. The aim of this research was to investigate the anatomical (gross) and structural (compliance) characteristics of excised marine mammal tracheas. Here, we defined different types of tracheal structures, categorizing pinniped tracheas by varying degrees of continuity of cartilage (categories 1-4) and cetacean tracheas by varying compliance values (categories 5A and 5B). Some tracheas fell into more than one category along their length; for example, the harbor seal (Phoca vitulina) demonstrated complete rings cranially, and as the trachea progressed caudally, tracheal rings changed morphology. Dolphins and porpoises had less stiff, more compliant spiraling rings while beaked whales had very stiff, less compliant spiraling rings. The pressure-volume (P-V) relationships of isolated tracheas from different species were measured to assess structural differences between species. These findings lend evidence for pressure-induced collapse and re-inflation of lungs, perhaps influencing variability in dive depth or ventilation rates of the species investigated.

Methods used during gross necropsy to determine watercraft-related mortality in the Florida manatee (Trichechus manatus latirostris).

Between 1993 and 2003, 713 (24%) of 2,940 dead Florida manatees (Trichechus manatus latirostris) recovered from Florida waters and examined were killed by watercraft-induced trauma. It was determined that this mortality was the result of watercraft trauma because the external wound patterns and the internal lesions seen during gross necropsy are recognizable and diagnostic. This study documents the methods used in determining watercraft-related mortality during gross necropsy and explains why these findings are diagnostic. Watercraft can inflict sharp- and blunt-force trauma to manatees, and both types of trauma can lead to mortality. This mortality may be a direct result of the sharp and blunt forces or from the chronic effects resulting from either force. In cases in which death is caused by a chronic wound-related complication, the original incident is usually considered to be the cause of death. Once a cause of death is determined, it is recorded in an extensive database and is used by Federal and state managers in developing strategies for the conservation of the manatee. Common sequelae to watercraft-induced trauma include skin lesions, torn muscles, fractured and luxated bones, lacerated internal organs, hemothorax, pneumothorax, pyothorax, hydrothorax, abdominal hemorrhage and ascites, and pyoperitoneum.