Sophie Dennison

Deadly diving? Physiological and behavioural management of decompression stress in diving mammals

Decompression sickness (DCS; ‘the bends’) is a disease associated with gas uptake at pressure. The basic pathology and cause are relatively well known to human divers. Breath-hold diving marine mammals were thought to be relatively immune to DCS owing to multiple anatomical, physiological and behavioural adaptations that reduce nitrogen gas (N2) loading during dives. However, recent observations have shown that gas bubbles may form and tissue injury may occur in marine mammals under certain circumstances. Gas kinetic models based on measured time-depth profiles further suggest the potential occurrence of high blood and tissue N2 tensions. We review evidence for gas-bubble incidence in marine mammal tissues and discuss the theory behind gas loading and bubble formation. We suggest that diving mammals vary their physiological responses according to multiple stressors, and that the perspective on marine mammal diving physiology should change from simply minimizing N2 loading to management of the N2 load. This suggests several avenues for further study, ranging from the effects of gas bubbles at molecular, cellular and organ function levels, to comparative studies relating the presence/absence of gas bubbles to diving behaviour. Technological advances in imaging and remote instrumentation are likely to advance this field in coming years.

Gas Bubbles in Seals, Dolphins, and Porpoises Entangled and Drowned at Depth in Gillnets

Gas bubbles were found in 15 of 23 gillnet-drowned bycaught harp (Pagophilus groenlandicus), harbor (Phoca vitulina) and gray (Halichoerus grypus) seals, common (Delphinus delphis) and white-sided (Lagenorhyncus acutus) dolphins, and harbor porpoises (Phocaena phocaena) but in only 1 of 41 stranded marine mammals. Cases with minimal scavenging and bloating were chilled as practical and necropsied within 24 to 72 hours of collection. Bubbles were commonly visible grossly and histologically in bycaught cases. Affected tissues included lung, liver, heart, brain, skeletal muscle, gonad, lymph nodes, blood, intestine, pancreas, spleen, and eye. Computed tomography performed on 4 animals also identified gas bubbles in various tissues. Mean ± SD net lead line depths (m) were 92 ± 44 and ascent rates (ms-1) 0.3 ± 0.2 for affected animals and 76 ± 33 and 0.2 ± 0.1, respectively, for unaffected animals. The relatively good carcass condition of these cases, comparable to 2 stranded cases that showed no gas formation on computed tomography (even after 3 days of refrigeration in one case), along with the histologic absence of bacteria and autolytic changes, indicate that peri- or postmortem phase change of supersaturated blood and tissues is most likely. Studies have suggested that under some circumstances, diving mammals are routinely supersaturated and that these mammals presumably manage gas exchange and decompression anatomically and behaviorally. This study provides a unique illustration of such supersaturated tissues. We suggest that greater attention be paid to the radiology and pathology of bycatch mortality as a possible model to better understand gas bubble disease in marine mammals.

Hyperbaric computed tomographic measurement of lung compression in seals and dolphins.

SUMMARY Lung compression of vertebrates as they dive poses anatomical and physiological challenges. There has been little direct observation of this. A harbor and a gray seal, a common dolphin and a harbor porpoise were each imaged post mortem under pressure using a radiolucent, fiberglass, water-filled pressure vessel rated to a depth equivalent of 170 m. The vessel was scanned using computed tomography (CT), and supported by a rail and counterweighted carriage magnetically linked to the CT table movement. As pressure increased, total buoyancy of the animals decreased and lung tissue CT attenuation increased, consistent with compression of air within the lower respiratory tract. Three-dimensional reconstructions of the external surface of the porpoise chest showed a marked contraction of the chest wall. Estimation of the volumes of different body compartments in the head and chest showed static values for all compartments except the lung, which showed a pressure-related compression. The depth of estimated lung compression ranged from 58 m in the gray seal with lungs inflated to 50% total lung capacity (TLC) to 133 m in the harbor porpoise with lungs at 100% TLC. These observations provide evidence for the possible behavior of gas within the chest of a live, diving mammal. The estimated depths of full compression of the lungs exceeds previous indirect estimates of the depth at which gas exchange ceases, and concurs with pulmonary shunt measurements. If these results are representative for living animals, they might suggest a potential for decompression sickness in diving mammals.

Neuroanatomy and Volumes of Brain Structures of a Live California Sea Lion (Zalophus californianus) From Magnetic Resonance Images

The California sea lion (Zalophus californianus) has been a focal point for sensory, communication, cognition, and neurological disease studies in marine mammals. However, as a scientific community, we lack a noninvasive approach to investigate the anatomy and size of brain structures in this species and other free‐ranging, live marine mammals. In this article, we provide the first anatomically labeled, magnetic resonance imaging‐based atlas derived from a live marine mammal, the California sea lion. The brain of the California seal lion contained more secondary gyri and sulci than the brains of terrestrial carnivores. The olfactory bulb was present but small. The hippocampus of the California sea lion was found mostly in the ventral position with very little extension dorsally, quite unlike the canids and the mustelids, in which the hippocampus is present in the ventral position but extends dorsally above the thalamus. In contrast to the canids and the mustelids, the pineal gland of the California sea lion was strikingly large. In addition, we report three‐dimensional reconstructions and volumes of cerebrospinal fluid, cerebral ventricles, total white matter (WM), total gray matter (GM), cerebral hemispheres (WM and GM), cerebellum and brainstem combined (WM and GM), and hippocampal structures all derived from magnetic resonance images. These measurements are the first to be determined for any pinniped species. In California sea lions, this approach can be used not only to relate cognitive and sensory capabilities to brain size but also to investigate the neurological effects of exposure to neurotoxins such as domoic acid. Anat Rec, 2009.

Algal toxin impairs sea lion memory and hippocampal connectivity, with implications for strandings

Red tides make dinner hard to find Domoic acid (DA) is a neurotoxin produced by marine algae. When present in large amounts, it is harmful to marine organisms and to humans. Cook et al. tested California sea lions being treated at a marine mammal rescue facility. Animals that had evidence of exposure to DA had lesions in their hippocampus and displayed reduced performance on spatial memory tasks. Because such tasks are essential to foraging in a marine environment, increasing exposure to DA may be contributing to increasing sea lion strandings. Science, this issue p. 1545 Domoic acid reduces spatial memory and, likely, foraging ability in California sea lions. Domoic acid (DA) is a naturally occurring neurotoxin known to harm marine animals. DA-producing algal blooms are increasing in size and frequency. Although chronic exposure is known to produce brain lesions, the influence of DA toxicosis on behavior in wild animals is unknown. We showed, in a large sample of wild sea lions, that spatial memory deficits are predicted by the extent of right dorsal hippocampal lesions related to natural exposure to DA and that exposure also disrupts hippocampal-thalamic brain networks. Because sea lions are dynamic foragers that rely on flexible navigation, impaired spatial memory may affect survival in the wild.

Bubbles in live-stranded dolphins

Bubbles in supersaturated tissues and blood occur in beaked whales stranded near sonar exercises, and post-mortem in dolphins bycaught at depth and then hauled to the surface. To evaluate live dolphins for bubbles, liver, kidneys, eyes and blubber–muscle interface of live-stranded and capture-release dolphins were scanned with B-mode ultrasound. Gas was identified in kidneys of 21 of 22 live-stranded dolphins and in the hepatic portal vasculature of 2 of 22. Nine then died or were euthanized and bubble presence corroborated by computer tomography and necropsy, 13 were released of which all but two did not re-strand. Bubbles were not detected in 20 live wild dolphins examined during health assessments in shallow water. Off-gassing of supersaturated blood and tissues was the most probable origin for the gas bubbles. In contrast to marine mammals repeatedly diving in the wild, stranded animals are unable to recompress by diving, and thus may retain bubbles. Since the majority of beached dolphins released did not re-strand it also suggests that minor bubble formation is tolerated and will not lead to clinically significant decompression sickness.

Magnetic resonance imaging quality and volumes of brain structures from live and postmortem imaging of California sea lions with clinical signs of domoic acid toxicosis

Our goal in this study was to compare magnetic resonance images and volumes of brain structures obtained alive versus postmortem of California sea lions Zalophus californianus exhibiting clinical signs of domoic acid (DA) toxicosis and those exhibiting normal behavior. Proton density-(PD) and T2-weighted images of postmortem-intact brains, up to 48 h after death, provided similar quality to images acquired from live sea lions. Volumes of gray matter (GM) and white matter (WM) of the cerebral hemispheres were similar to volumes calculated from images acquired when the sea lions were alive. However, cerebrospinal fluid (CSF) volumes decreased due to leakage. Hippocampal volumes from postmortem-intact images were useful for diagnosing unilateral and bilateral atrophy, consequences of DA toxicosis. These volumes were similar to the volumes in the live sea lion studies, up to 48 h postmortem. Imaging formalin-fixed brains provided some information on brain structure; however, images of the hippocampus and surrounding structures were of poorer quality compared to the images acquired alive and postmortem-intact. Despite these issues, volumes of cerebral GM and WM, as well as the hippocampus, were similar to volumes calculated from images of live sea lions and sufficient to diagnose hippocampal atrophy. Thus, postmortem MRI scanning (either intact or formalin-fixed) with volumetric analysis can be used to investigate the acute, chronic and possible developmental effects of DA on the brain of California sea lions.

Radiographic determination of proventricular diameter in psittacine birds

OBJECTIVE To establish an objective method of determining proventricular diameter in psittacine birds by assessment of lateral whole-body radiographic views. DESIGN Retrospective case-control study. ANIMALS 100 parrots with no signs of gastric disease and 19 parrots with signs of gastric disease. PROCEDURES Measurements were obtained for the following variables: proventricular diameter at the level of the junction between the last thoracic vertebra and synsacrum, maximum distance between the dorsal serosa of the proximal aspect of the proventriculus and dorsal border of the sternum, maximum coelomic cavity height at the level of the proximal aspect of the proventriculus, and maximum dorsoventral height of the keel of the sternum. The ratio of proventricular diameter to each of those measurements was calculated and compared among species within the group without signs of gastric disease and between the gastric and nongastric disease groups. RESULTS No significant differences were seen among species of parrots without signs of gastric disease for any ratio, but there were significant differences between parrots with gastric signs and those without gastric signs for all ratios. Only the proventricular diameterto-maximum dorsoventral height of the keel of the sternum ratio had no numeric overlap between groups. Sensitivity and specificity of the ratio for detection of proventricular enlargement were both 100%. Six causes associated with proventricular enlargement were identified. CONCLUSIONS AND CLINICAL RELEVANCE Evaluation of the proventricular diameter-to-keel height ratio is a new method for evaluating proventricular size in psittacines. Ratio values < 0.48 indicate normal proventricular diameter and the absence of proventricular disease.

URATE NEPHROLITHIASIS IN A NORTHERN ELEPHANT SEAL (MIROUNGA ANGUSTIROSTRIS) AND A CALIFORNIA SEA LION (ZALOPHUS CALIFORNIANUS)

Abstract Nephrolithiasis has rarely been reported in marine mammals. During 2004 and 2005, two cases of nephrolithiasis were diagnosed during routine necropsy examination, one in a northern elephant seal (Mirounga angustirostris) and one in a California sea lion (Zalophus californianus). Nephroliths were found throughout both kidneys during necropsy examination, varying in size from 1–10 mm in diameter in the northern elephant seal and from 1–15 mm in diameter in the California sea lion. Necropsy and histopathology revealed nephroliths in association with renal pelvic dilation and pyelonephritis in both animals. In addition, hydronephrosis was noted in the sea lion. Nephroliths were composed of uric acid and ammonium urate in the northern elephant seal and of ammonium urate in the California sea lion. The underlying disease leading to nephrolith formation was not determined; however, it is hypothesized that unknown metabolic derangements due to morphologic or physiologic differences may have played a role. This is the first report of urate nephrolithiasis in the California sea lion and northern elephant seal.

Evidence of injury caused by gas bubbles in a live Marine Mammal: Barotrauma in a California sea lion Zalophus californianus

A yearling male California sea lion Zalophus californianus with hypermetric ataxia and bilateral negative menace reflexes was brought to The Marine Mammal Center, Sausalito, California, U.S.A., in late 2009 for medical assessment and treatment. The clinical signs were due to multiple gas bubbles within the cerebellum. These lesions were intraparenchymal, multifocal to coalescing, spherical to ovoid, and varied from 0.5 to 2.4 cm diameter. The gas composed 21.3% of the total cerebellum volume. Three rib fractures were also noted during diagnostic evaluation and were presumed to be associated with the gas bubbles in the brain. The progression of clinical signs and lesion appearance were monitored with magnetic resonance imaging, cognitive function testing and computed tomography. Gas filled voids in the cerebellum were filled with fluid on follow up images. Clinical signs resolved and the sea lion was released with a satellite tag attached. Post release the animal travelled approximately 75 km north and 80 km south of the release site and the tag recorded dives of over 150 m depth. The animal re-stranded 25 d following release and died of a subacute bronchopneumonia and pleuritis. This is the first instance of clinical injury due to gas bubble formation described in a living pinniped and the first sea lion with quantifiable cerebellar damage to take part in spatial learning and memory testing.