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The structure and function of the small airways
Abstract
We have looked at the structure of the small airways from the lungs of 58 marine mammals. Six were from sea otters, the others were from 14 of the 21 pinniped genera. In comparison with the terminal airways of terrestrial mammals all showed reinforcement by muscle and/or cartilage. The small airways of phocid seal lungs were reinforced by a moderately slender tube of oblique muscle. Those of otariid seals were strengthened by very much thicker pieces of cartilage. The airways of sea-otter and walrus lungs were of an intermediate pattern.Both types of reinforcement seem to appear late in foetal life rather than by arrest of development. Calculations suggest the reinforcement in otariid lungs may be excessive for limiting nitrogen absorption during deep dives and behavioural observations indicate that strengthened airways may also be required for rapid ventilation at the surface between dives.
... The balloon-pipe model suggested that the alveolar collapse depth could be estimated from the relative volume of each of the parts of the respiratory system using Boyle's law (Scholander, 1940). Later, calculations showed that even if the upper airways did compress, there was movement of air from the alveoli into the upper airways as long as the conducting airways were stiffer as compared with the alveolar space (Denison and Kooyman, 1973). Two independent models were developed to estimate how the respiratory system behaves during breathhold dives in humans (Fitz-Clarke, 2009a) and air breathing marine vertebrates (Bostrom et al., 2008). ...
... Recent studies in the California sea lion (Zalophus californianus) provided empirical evidence for these theoretical results, and suggested that the alveolar collapse depth occurs at depths exceeding 200 m (McDonald and Ponganis, 2012Ponganis, , 2013. The theoretical modeling (Bostrom et al., 2008;Fahlman et al., 2009Fahlman et al., , 2018bHodanbosi et al., 2016), based on data from studies that defined the structural properties of the respiratory system (Denison et al., 1971;Denison and Kooyman, 1973;Leith, 1976;Piscitelli et al., 2010;Fahlman et al., 2011Fahlman et al., , 2014aFahlman et al., , 2015Fahlman et al., , 2018aFahlman et al., ,c, 2020aMoore C. et al., 2014;Fahlman and Madigan, 2016;Denk et al., 2020), agrees with these empirical estimates for alveolar collapse depths and cessation of gas exchange in the California sea lion, and also the elephant seal (Mirounga angustirostris), and Weddell seal (Leptonychotes weddellii) (Kooyman et al., 1972;Kooyman and Sinnett, 1982;Fahlman et al., 2009;Hodanbosi et al., 2016). ...
... Initial studies used parameters for the structural properties of the respiratory system from terrestrial mammals, resulting in model estimates that suggested that symptomatic gas bubbles should occur more than 50% of the time (Figure 3 blue symbols). Measurement of species-specific structural properties for the respiratory system in the sea lion and bottlenose dolphin for excised tissues (Denison et al., 1971;Denison and Kooyman, 1973;Kooyman and Sinnett, 1982;Fahlman et al., 2011Fahlman et al., , 2014aMoore C. et al., 2014), in live animals under human care (Fahlman et al., , 2019a(Fahlman et al., ,b, 2020cFahlman and Madigan, 2016), and in the wild (Hurley and Costa, 2001;Fahlman et al., 2008Fahlman et al., , 2013Fahlman et al., , 2018aHindle et al., 2010) have shown that both the anatomy and physiology of marine mammals help to minimize N 2 exchange (Figure 3 red symbols). ...
Decompression theory has been mainly based on studies on terrestrial mammals, and may not translate well to marine mammals. However, evidence that marine mammals experience gas bubbles during diving is growing, causing concern that these bubbles may cause gas emboli pathology (GEP) under unusual circumstances. Marine mammal management, and usual avoidance, of gas emboli and GEP, or the bends, became a topic of intense scientific interest after sonar-exposed, mass-stranded deep-diving whales were observed with gas bubbles. Theoretical models, based on our current understanding of diving physiology in cetaceans, predict that the tissue and blood N2 levels in the bottlenose dolphin (Tursiops truncatus) are at levels that would result in severe DCS symptoms in similar sized terrestrial mammals. However, the dolphins appear to have physiological or behavioral mechanisms to avoid excessive blood N2 levels, or may be more resistant to circulating bubbles through immunological/biochemical adaptations. Studies on behavior, anatomy and physiology of marine mammals have enhanced our understanding of the mechanisms that are thought to prevent excessive uptake of N2. This has led to the selective gas exchange hypothesis, which provides a mechanism how stress-induced behavioral change may cause failure of the normal physiology, which results in excessive uptake of N2, and in extreme cases may cause formation of symptomatic gas emboli. Studies on cardiorespiratory function have been integral to the development of this hypothesis, with work initially being conducted on excised tissues and cadavers, followed by studies on anesthetized animals or trained animals under human care. These studies enabled research on free-ranging common bottlenose dolphins in Sarasota Bay, FL, and off Bermuda, and have included work on the metabolic and cardiorespiratory physiology of both shallow- and deep-diving dolphins and have been integral to better understand how cetaceans can dive to extreme depths, for long durations.
... The lungs of diving mammals are often reinforced with cartilage and smooth muscle (Kooyman 1973) (Fig. 4). Pinnipeds generally have less reinforcement than cetaceans (Denison and Kooyman 1973), and phocids have more smooth muscle in the smaller airways than otariids (Gray et al. 2006), although the final few millimeters of pinniped terminal airways are without cartilaginous reinforcement, and the alveoli are organized in lobules protected by thin stroma (Denison and Kooyman 1973). Smooth muscle reinforcement may be related to diving depth, as the deeper-diving Weddell seal (Leptonychotes weddellii) has greater amounts of smooth muscle than the crabeater seal (Lobodon carcinophaga) (Welsch and Drescher 1982). ...
... The lungs of diving mammals are often reinforced with cartilage and smooth muscle (Kooyman 1973) (Fig. 4). Pinnipeds generally have less reinforcement than cetaceans (Denison and Kooyman 1973), and phocids have more smooth muscle in the smaller airways than otariids (Gray et al. 2006), although the final few millimeters of pinniped terminal airways are without cartilaginous reinforcement, and the alveoli are organized in lobules protected by thin stroma (Denison and Kooyman 1973). Smooth muscle reinforcement may be related to diving depth, as the deeper-diving Weddell seal (Leptonychotes weddellii) has greater amounts of smooth muscle than the crabeater seal (Lobodon carcinophaga) (Welsch and Drescher 1982). ...
... Smooth muscle reinforcement may be related to diving depth, as the deeper-diving Weddell seal (Leptonychotes weddellii) has greater amounts of smooth muscle than the crabeater seal (Lobodon carcinophaga) (Welsch and Drescher 1982). In the eared seals (Otariidae), cartilage lines the terminal airways all the way to the alveolar sacs, which are surrounded by thick stroma (20-30 mm), whereas terminal bronchi of sea otters and walruses have thick stroma and alveoli with and without cartilaginous ducts (Denison and Kooyman 1973). Compared with dog lungs, sea lion lungs collapse more completely at pressure (Denison et al. 1971) because cartilage maintains airway patency even at low pressures, allowing all of the air to escape the alveoli before conducting airways collapse. ...
Although the airways of vertebrates are diverse in shape, complexity, and function, they all contain visceral smooth muscle. The morphology, function, and innervation of this tissue in airways is reviewed in actinopterygians, lungfish, amphibians, non-avian reptiles, birds, and mammals. Smooth muscle was likely involved in tension regulation ancestrally, and may serve to assist lung emptying in fishes and aquatic amphibians, as well as maintain internal lung structure. In certain non-avian reptiles and anurans antagonistic smooth muscle fibers may contribute to intrapulmonary gas mixing. In mammals and birds, smooth muscle regulates airway caliber, and may be important in controlling the distribution of ventilation at rest and exercise, or during thermoregulatory and vocal hyperventilation. Airway smooth muscle is controlled by the autonomic nervous system: cranial cholinergic innervation generally causes excitation, cranial non-adrenergic, non-cholinergic innervation causes inhibition, and spinal adrenergic (SA) input causes species-specific, often heterogeneous contractions and relaxations.
... The presence of MESs and cartilage reinforcement in the terminal bronchi contrasts with terrestrial and semiaquatic mammals (Denison and Kooyman, 1973), where the spiraling smooth muscle traverses between the cartilage and epithelium (Supporting Information, appendix 3 and appendix 6). Terminal airways in terrestrial mammals, however, completely lack cartilage and consist of lamina propria subjacent to the respiratory epithelium. ...
... Fanning and Whitting, gross and microscopic anatomy of respiratory system River otter (Lontra canadensis) Tarasoff and Kooyman, 1973a,b gross anatomy of respiratory system Walrus (Odobenus rosmarus) Denison and Kooyman, 1973 microscopic airway structure Murie, 1871b;Sleptsov, 1940;Fay, 1960;Schevill et al., 1966;Sokolov et al., 1968;Ridgway and Harrison, 1981a gross anatomy of the respiratory system and air sacs ...
... No Denison and Kooyman, 1973;Kooyman, 1973 Steller's sea lion (Eumetopias jubatus) Thick, heavy plates of cartilage extended throughout the terminal bronchi and continued down into the alveolar sacs. ...
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. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.
... Phocid seals are also the only group of marine mammals to regularly dive on expiration, allowing their lungs to collapse on each dive and then reinflating them on inspiration at surfacing. They have the least modified airways of all the marine mammals [11,12] yet include the deepest diving seal species, such as the Southern elephant (Mirounga leonina) and Weddell seals (Leptonychotes weddellii), which can withstand the hydrostatic pressure at depths of between ,600 and ,2000 m respectively [13,14]. In contrast, all other marine mammal Families have highly modified airways compared to their terrestrial counterparts [11]. ...
... They have the least modified airways of all the marine mammals [11,12] yet include the deepest diving seal species, such as the Southern elephant (Mirounga leonina) and Weddell seals (Leptonychotes weddellii), which can withstand the hydrostatic pressure at depths of between ,600 and ,2000 m respectively [13,14]. In contrast, all other marine mammal Families have highly modified airways compared to their terrestrial counterparts [11]. Otariids and cetaceans are known to dive on inspiration, which helps to minimize the potential for nitrogen narcosis [15]. ...
... The single amino acid differences at positions 15 and 85 in each seal species are conservative and do not affect the hydrophobic cleft formation necessary for binding [25,26] (Fig. 3B). Residues 4,5,8,11,13,78,79, 81 and 89, which surround the hydrophobic cleft, are all predicted to be buried within the leptin and LEPR interface and are highly conserved in all mammals including the phocids. The one exception is the alanine at residue 81 which is unique to the phocids: all other mammals have a glutamic acid at this position. ...
The cytokine hormone leptin is a key signalling molecule in many pathways that control physiological functions. Although leptin demonstrates structural conservation in mammals, there is evidence of positive selection in primates, lagomorphs and chiropterans. We previously reported that the leptin genes of the grey and harbour seals (phocids) have significantly diverged from other mammals. Therefore we further investigated the diversification of leptin in phocids, other marine mammals and terrestrial taxa by sequencing the leptin genes of representative species. Phylogenetic reconstruction revealed that leptin diversification was pronounced within the phocid seals with a high dN/dS ratio of 2.8, indicating positive selection. We found significant evidence of positive selection along the branch leading to the phocids, within the phocid clade, but not over the dataset as a whole. Structural predictions indicate that the individual residues under selection are away from the leptin receptor (LEPR) binding site. Predictions of the surface electrostatic potential indicate that phocid seal leptin is notably different to other mammalian leptins, including the otariids. Cloning the grey seal leptin binding domain of LEPR confirmed that this was structurally conserved. These data, viewed in toto, support a hypothesis that phocid leptin divergence is unlikely to have arisen by random mutation. Based upon these phylogenetic and structural assessments, and considering the comparative physiology and varying life histories among species, we postulate that the unique phocid diving behaviour has produced this selection pressure. The Phocidae includes some of the deepest diving species, yet have the least modified lung structure to cope with pressure and volume changes experienced at depth. Therefore, greater surfactant production is required to facilitate rapid lung re-inflation upon surfacing, while maintaining patent airways. We suggest that this additional surfactant requirement is met by the leptin pulmonary surfactant production pathway which normally appears only to function in the mammalian foetus.
... Studies on respiratory function and mechanics in marine mammals have used different approaches. Some studies have used anaesthetized or post-mortem animals and excised tissues (Denison and Kooyman, 1973;Denk et al., 2020;Fahlman et al., 2011Fahlman et al., , 2014Kooyman and Sinnett, 1979;Leith et al., 1972;Moore et al., 2011), which may not reflect respiratory function in a realistic biological scenario (Fahlman et al., 2017). Other studies have used restrained Linear mixed-effects models including expiratory (exp) and inspiratory (insp) tidal volume (V T , l), respiratory flow ( _ V, l s −1 ) and respiratory frequency (f R , breaths min −1 ) measured for all body positions (sitting supported by the front flippers, lying down, and floating at rest in water) and spontaneous breaths. ...
... In addition to a flexible thorax and compliant lungs, previous studies on the anatomy and mechanical properties of the respiratory system in marine mammals showed that many species have reinforced conducting airways (Bagnoli et al., 2011;Cozzi et al., 2005;Denison and Kooyman, 1973;Fahlman et al., 2017;Kooyman, 1973;Moore et al., 2014;Piscitelli et al., 2013). These anatomical features would allow for alveolar compression during diving and also adequate gas exchange during high _ V exp and short T tot as compared with terrestrial mammals (Fahlman et al., 2017;Kooyman and Sinnett, 1982;Piscitelli et al., 2010;Stahl, 1967). ...
In the present study, we examined lung function in healthy resting adult (born in 2003) Pacific walruses ( Odobenus rosmarus divergens ) by measuring respiratory flow ( V̇ ) using a custom-made pneumotachometer. Three female walruses (670 – 1025 kg) voluntarily participated in spirometry trials while spontaneously breathing on land (sitting and lying down in sternal recumbency) and floating in water. While sitting, two walruses performed active respiratory efforts, and one animal participated in lung compliance measurements. For spontaneous breaths, V̇ was lower when lying down (e.g. expiration: 7.1±1.2 l · s ⁻¹ ) as compared to when in water (9.9±1.4 l · s ⁻¹ ), while tidal volume ( V T , 11.5±4.6 l), breath duration (4.6±1.4 s), and respiratory frequency (7.6±2.2 breaths · min ⁻¹ ) remained the same. The measured V T and specific dynamic lung compliance (0.32±0.07 cmH 2 O ⁻¹ ) for spontaneous breaths, were higher than those estimated for similarly sized terrestrial mammals. The V T increased with body mass (allometric mass-exponent=1.29) and ranged from 3 to 43% of the estimated total lung capacity (TLC est ) for spontaneous breaths. When normalized for TLC est , the maximal expiratory V̇ ( V̇ exp ) was higher than that estimated in phocids, but lower than that reported in cetaceans and the California sea lion. The V̇ exp was maintained over all lung volumes during spontaneous and active respiratory manoeuvres. We conclude that location (water or land) affects lung function in the walrus and should be considered when studying respiratory physiology in semi-aquatic marine mammals.
... Human lungs are alveolar and the terminal airways are not reinforced (Denison and Kooyman 1973). Pulmonary surfactant is a mixture of lipids and proteins. ...
... This means that the amount of nitrogen brought to the depth is minimized. Their terminal airways are reinforced with muscle tissue and/or cartilage (Denison and Kooyman 1973). When the ambient pressure increases, only the alveoli collapse and the air in the lung will be constrained to the dead space. ...
The frequency of decompression illness was high among the extinct marine “reptiles” and very low among the marine mammals. Signs of decompression illness are still found among turtles but whales and seals are unaffected. In humans, the risk of decompression illness is five times increased in individuals with Patent Foramen Ovale; this condition allows blood shunting from the venous circuit to the systemic circuit. This right-left shunt is characteristic of the “reptile” heart, and it is suggested that this could contribute to the high frequency of decompression illness in the extinct reptiles.
... The relationship between estimated total lung capacity (TLC est ; broken line, Kooyman, 1973) and M b for marine mammals reveals that the volume of most breaths of marine mammals is not close to the vital capacity of the animal. References: bottlenose dolphin (Fahlman et al., 2015b), gray seal (Reed et al., 1994), Weddell seal (Kooyman et al., 1971), harbor porpoise (Reed et al., 2000), California sea lion (Kerem et al., 1975;Matthews, 1977), pilot whale (Olsen et al., 1969), killer whale (Spencer et al., 1967;Kasting et al., 1989), beluga whale (Kasting et al., 1989;Epple et al., 2015), walrus (Fahlman et al., 2015a), Patagonia sea lion (Fahlman and Madigan, 2016) Denison and Kooyman, 1973;Kooyman, 1973;Tarasoff and Kooyman, 1973;Leith, 1976;Kooyman and Sinnett, 1979;Kooyman and Cornell, 1981;Fahlman et al., 2011Fahlman et al., , 2014Fahlman et al., , 2015bMoore et al., 2011Moore et al., , 2014. Studies using trained marine mammals that voluntarily participate have been used to define flowvolume characteristics (Olsen et al., 1969;Kooyman and Cornell, 1981;Fahlman et al., 2015b;Fahlman and Madigan, 2016). ...
... The reinforced conducting airway of marine mammals is a good example. Marine mammals are reported to have reinforced airways (Kooyman and Sinnett, 1982), and there appears to be significant variability between orders and species (Wislocki, 1929(Wislocki, , 1942Bélanger, 1940;Wislocki and Belanger, 1940;Goudappel and Slijper, 1958;Denison and Kooyman, 1973;Henk and Haldiman, 1990;Wessels and Chase, 1998;Ninomiya et al., 2005;Bagnoli et al., 2011). In the sea lion and cetaceans, the cartilaginous reinforcement extends down to the entrance of the alveoli or alveolar sacthere are no respiratory bronchioleswhereas in the seal the last few millimeters of the conducting airway are reinforced with muscle and appear to be much more compliant (Tarasoff and Kooyman, 1973;Cozzi et al., 2005;Bagnoli et al., 2011;Moore et al., 2014). ...
In this Review, we focus on the functional properties of the respiratory system of pinnipeds and cetaceans, and briefly summarize the underlying anatomy; in doing so, we provide an overview of what is currently known about their respiratory physiology and mechanics. While exposure to high pressure is a common challenge among breath-hold divers, there is a large variation in respiratory anatomy, function and capacity between species textendash how are these traits adapted to allow the animals to withstand the physiological challenges faced during dives? The ultra-deep diving feats of some marine mammals defy our current understanding of respiratory physiology and lung mechanics. These animals cope daily with lung compression, alveolar collapse, transient hyperoxia and extreme hypoxia. By improving our understanding of respiratory physiology under these conditions, we will be better able to define the physiological constraints imposed on these animals, and how these limitations may affect the survival of marine mammals in a changing environment. Many of the respiratory traits to survive exposure to an extreme environment may inspire novel treatments for a variety of respiratory problems in humans.
... However, compression of the rib cage does not prove that the alveoli have collapsed and that gas exchange has stopped. Depth of collapse has been estimated by assuming a rigid trachea and highly compliant lung (Denison & Kooyman, 1973;Stephenson, 2005). This assumption is questionable, as the trachea in Weddell and elephant seals showed significant compression at a depth of only 54 m (Ridgway, 1968). ...
... At a depth of 90 m, the shunt exceeded 70% in the harbour seal and complete alveolar collapse and termination of gas exchange was estimated to occur between 160 m and 170 m (Kooyman & Sinnett, 1982). The species used for this study (California sea lion and harbour seal) were chosen as they show the most divergent airway structure from those measured in pinnipeds (Denison & Kooyman, 1973). Despite this, the compression shunts at pressures below 70 m were not remarkably different from each other (between dolphins and California sea lions, for example) (Kooyman & Sinnett, 1982). ...
Although it has been generally assumed that the risk of decompression sickness is virtually zero during a single breath-hold dive in humans, repeated dives may result in a cumulative increase in the tissue and blood nitrogen tension. Many species of marine mammals perform extensive foraging bouts with deep and long dives interspersed by a short surface interval, and some human divers regularly perform repeated dives to 30-40 m or a single dive to more than 200 m, all of which may result in nitrogen concentrations that elicit symptoms of decompression sickness. Neurological problems have been reported in humans after single or repeated dives and recent necropsy reports in stranded marine mammals were suggestive of decompression sickness-like symptoms. Modelling attempts have suggested that marine mammals may live permanently with elevated nitrogen concentrations and may be at risk when altering their dive behaviour. In humans, non-pathogenic bubbles have been recorded and symptoms of decompression sickness have been reported after repeated dives to modest depths. The mechanisms implicated in these accidents indicate that repeated breath-hold dives with short surface intervals are factors that predispose to decompression sickness. During deep diving, the effect of pulmonary shunts and/or lung collapse may play a major role in reducing the incidence of decompression sickness in humans and marine mammals.
... Diving for sea otters is energetically costly because of their inefficient swimming mode, large lungs, buoyant fur and the high cost of thermoregulating at depth (Denison and Kooyman, 1973;Kooyman, 1973;Yeates et al., 2007;Ponganis, 2011). Sea otters typically forage at depths less than 25 m, and spend most of their time grooming, resting and eating at the surface (Riedman and Estes, 1990;Cashman, 2002). ...
Sea otters are extremely positively buoyant and spend most of their time resting at the water surface. It is understood that some of this buoyancy comes from the air layer that sea otters maintain in their pelage, with the lungs providing an additional source of positive buoyancy. Past studies have investigated the fur buoyant force in adult sea otters; however, little is known about the fur buoyant force in younger age classes. This study compared ontogenetic changes in the fur buoyant force of southern sea otter (Enhydra lutris nereis) pelage. We measured the fur buoyant force of pelt samples, scaled that to the whole animal, and calculated mass-specific fur buoyant force for six age classes: neonates (<1 month), small pups (1–2 months), large pups (3–5 months), juveniles (6 months–1 year), subadults (1–3 years) and adults (4–9 years). Each pelt sample was measured under three conditions: control, oiled and washed with Dawn® dish soap. Oiled and washed pelts had a lower fur buoyant force compared with the control pelts across all age classes. When oiled, the air layer of the pelt is ruined and no longer provides sufficient positive buoyancy. Pelts washed with Dawn® had higher variability in buoyant force compared with other conditions, and the air layer was not restored consistently. When we scaled up, we found that younger age classes were more buoyant because of their larger surface area to volume ratio. These differences in buoyancy may underlie variations in energetic costs and behavior among sea otters across development.
... In our study, the respiratory apparatus of all histologically examined otters showed the presence of calcified tracheal and bronchiolar cartilage. Previous studies reported the presence of cartilage in the final airways of sea otters (Enhydra lutris) [65], considering these features as an anatomical adaptation of terrestrial animals to water immersion, in order to prevent collapse of the last airways, thus allowing better gas exchanges. However, the consistent presence of calcification areas in the tracheal and bronchial walls described herein, not related to the age of the animals, is an unusual aspect, not reported so far in the literature, that could also represent a peculiar anatomical feature of Lutra lutra. ...
Dead specimens provide valuable data for the conservation of threatened species, allowing investigations of mortality, health conditions, and demographic parameters. The Eurasian otter (Lutra lutra) is a semiaquatic carnivore listed as endangered in Italy. In 2009, we started the first post mortem (PM) study of otters in Italy, through collaborative research between mammal ecologists and veterinary pathologists, using standardized protocols. Twenty-eight otters, mostly collected between 2009 and 2017, were examined. Most otters were males (67%), between 1 and 3 years old (64%), and predominantly in good nutritional condition. Adult males were significantly larger than adult females (p < 0.02), as expected for the species, although both sexes appeared to be smaller than otters examined in Central–northern Europe. The youngest sexually mature female was 3 years old. Road traffic collisions were the major cause of death, especially in young individuals, and mainly occurred in autumn–winter, particularly for females. Investigations of the scene of death contributed to revealing factors forcing otters to travel out of the water and move over the road, suggesting appropriate measures to reduce vehicle collision risk. Other causes of death included blunt chest trauma of uncertain origin, dog and conspecific attacks, or diseases of infectious or non-infectious origin, such as ulcerative gastritis, pleuropneumonia and peritonitis. Other diagnosed diseases included lymphoma. Ecto- and endoparasites were rarely detected, although we report the first documentation of heartworm and Ixodes hexagonus infestation in Italian otters. It is important to continue comprehensive, standardized PM investigations of otters in Italy to define baseline health, biometric and demographic parameters, collect biological samples for comparative analyses, and to reduce road-kill mortality. The present study suggests that the timely collection of carcasses and collaborative and coordinated research efforts are essential for obtaining useful data for the conservation of otters.
... TLC was determined as the volume of the inflated lungs at 30 mmHg. This pressure is higher than the standard of 22 mmHg (30 cm H 2 O) used to measure TLC in other mammalian studies (Denison and Kooyman, 1973;Denison et al., 1971;Kooyman and Sinnett, 1982;Loring et al., 2016;Moore et al., 2011;Weibel, 1973), but was necessary for the clinical diagnostic protocol. Specifically, the ringed seals' lungs were hyperinflated to ensure that no atelectasis ( partial or full collapse) or scarring of lung tissue was present. ...
Marine mammals rely on oxygen stored in blood, muscle, and lungs to support breath-hold diving and foraging at sea. Here, we used biomedical imaging to examine lung oxygen stores and other key respiratory parameters in living ringed seals ( Pusa hispida ). Three-dimensional models created from computed tomography (CT) images were used to quantify total lung capacity (TLC), respiratory dead space, minimum air volume, and total body volume to improve assessments of lung oxygen storage capacity, scaling relationships, and buoyant force estimates. Results suggest that lung oxygen stores determined in vivo are smaller than those derived from postmortem measurements. We also demonstrate that—while established allometric relationships hold well for most pinnipeds—these relationships consistently overestimate TLC for the smallest phocid seal. Finally, measures of total body volume reveal differences in body density and net vertical forces in the water column that influence costs associated with diving and foraging in free-ranging seals.
... The trachea, while not necessarily forming a complete lock, would collapse in whole or in part at its caudal extent, encouraging the air to flow towards the head. Caudal to cranial collapse patterns of this kind may require only minor differences in compliance between the components; Denison and Kooyman (1973) calculated that the airways theoretically require compliance only five times that of the alveoli to facilitate efficient alveolar collapse. These changes represent isolation of air as far away from the regions of gas exchange as possible and further protection from backflow at depth. ...
Assessment of the compressibility of marine mammal airways at depth is crucial to understanding vital physiologic processes such as gas exchange during diving. Very few studies have directly assessed changes in cetacean and pinniped trachea-bronchial shape, and none have quantified changes in volume with increasing pressure. A freshly deceased harbor seal, grey seal, harp seal, harbor porpoise, and common dolphin were imaged post mortem via CT in a radiolucent hyperbaric chamber as previously described in Moore et al (2011). Volume reconstructions were performed of segments of the trachea and bronchi of the pinnipeds and bronchi of the cetaceans for each pressure treatment. All specimens examined demonstrated significant decreases in volume with increasing pressure, with the harbor seal and common dolphin nearing complete collapse at the highest pressures. The common dolphin bronchi demonstrated distinctly different compression dynamics between 50% and 100% lung inflation treatments, indicating the importance of air in maintaining patent airways, and collapse occurred caudally to cranially in the 50% treatment. Dynamics of the harbor seal and grey seal airways indicated that the trachea was less compliant than the bronchi. These findings indicate potential species-specific variability in airway compliance, and cessation of gas exchange may occur at greater depths than those predicted in models assuming rigid airways. This may potentially increase the likelihood of decompression sickness in these animals during diving.
... The gross, histologic, and radiographic anatomy of the sea lion lung has been well described (Denison et al., 1971;Denison & Kooyman, 1973;Dennison et al., 2009), but there is limited published information available with regard to function (Denison et al., 1971;Kerem et al., 1975;Matthews, 1977;Fahlman et al., 2011Fahlman et al., , 2014. Studies involving excised lungs have estimated the TLC, airway structure, and alveolar emptying as well as inflation and deflation pressures (Lenfant et al., 1970;Denison et al., 1971;Fahlman et al., 2011Fahlman et al., , 2014. ...
Respiratory flow, expired O2, and CO2 were measured during voluntary participation while spontaneously breathing in 13 confirmed healthy, male California sea lions (Zalophus californianus; body mass [Mb] range: 49 to 130 kg). Expiratory and inspiratory flow (and), tidal volume (VTexp and VTinsp), and breath durations (Texp, Tinsp, and Ttot) were collected on land (lying down in sternal recumbency and sitting up) and floating in water to test the hypothesis that lung function changes with body position and on land vs in water. For sea lions on land, no differences were seen in any of the lung function values when comparing lying down versus sitting up. However, when comparing animals on land versus in water, both Texp and Tinsp decreased and and increased, while the VTexp and VTinsp remained the same. The resting mass-specific VT (25.1 ± 1.7 ml kg-1) in the current study was approximately 24 to 30% of the estimated total lung capacity. We also measured breath-by-breath gas uptake to determine the O2 consumption rates () and CO2 production rates () during rest on land and in water. There were no differences in or on land as compared with water, and the average estimated values were 0.58 ± 0.22 l O2 min-1 (range: 0.24 to 1.01 l O2 min −1) and 0.50 ± 0.19 l CO2 min-1 (range: 0.22 to 0.89 l CO2 min-1), respectively, which agrees with results from other studies on otariids. Additionally, the allometric mass-exponent for VT and were 1.13 to 1.20 and 0.86, respectively. These data are the first reported estimates of metabolic rate and lung function in confirmed healthy California sea lions.
... The anatomical basis of such reinforcement varies in different species, and includes the presence of (A) cartilaginous structures in the distal airway walls of cetaceans and sea lions, (B) prominent muscle fibres in the bronchial walls of seals, and (C) large vascular plexuses that have been postulated to become engorged at depth to reinforce the airways in deepdiving whales. [13][14][15][16] Lastly, a recent report of high collateral ventilation flow rates in the unicameral dolphin lung should be of interest in relation to the role of collateral ventilation in emphysema and to its effects on outcomes from endoscopic lung volume reduction procedures. 17 In a novel hypothesis, it has been postulated that high collateral flow and constriction of the dolphin's peribronchiolar sphincter muscles during a dive contribute to optimisation of ventilation-perfusion matching. ...
Anatomical and physiological adaptations of animals to extreme environments provide insight into basic physiological principles and potential therapies for human disease. In that regard, the diving physiology of marine mammals and seabirds is especially relevant to pulmonary and cardiovascular function, and to the pathology and potential treatment of patients with hypoxaemia and/or ischaemia. This review highlights past and recent progress in the field of comparative diving physiology with emphasis on its potential relevance to human medicine.
... Strengthening of the airways also allows extremely rapid, forced expiration without collapse of the airways and the subsequent trapping of air in the alveoli (291). This means that the alveoli undergo severe, protracted collapse, yet they are able to reinflate without any apparent side-effects (121). Hence, unlike in terrestrial mammals, the surfactant system of diving mammals has to cope with repeated collapse and reinflation of the lung which necessitates the reestablishment following each dive of an air-liquid interface and a functional surfactant film. ...
Surfactant lipids and proteins form a surface active film at the air-liquid interface of internal gas exchange organs, including swim bladders and lungs. The system is uniquely positioned to meet both the physical challenges associated with a dynamically changing internal air-liquid interface, and the environmental challenges associated with the foreign pathogens and particles to which the internal surface is exposed. Lungs range from simple, transparent, bag-like units to complex, multilobed, compartmentalized structures. Despite this anatomical variability, the surfactant system is remarkably conserved. Here, we discuss the evolutionary origin of the surfactant system, which likely predates lungs. We describe the evolution of surfactant structure and function in invertebrates and vertebrates. We focus on changes in lipid and protein composition and surfactant function from its antiadhesive and innate immune to its alveolar stability and structural integrity functions. We discuss the biochemical, hormonal, autonomic, and mechanical factors that regulate normal surfactant secretion in mature animals. We present an analysis of the ontogeny of surfactant development among the vertebrates and the contribution of different regulatory mechanisms that control this development. We also discuss environmental (oxygen), hormonal and biochemical (glucocorticoids and glucose) and pollutant (maternal smoking, alcohol, and common "recreational" drugs) effects that impact surfactant development. On the adult surfactant system, we focus on environmental variables including temperature, pressure, and hypoxia that have shaped its evolution and we discuss the resultant biochemical, biophysical, and cellular adaptations. Finally, we discuss the effect of major modern gaseous and particulate pollutants on the lung and surfactant system. (C) 2016 American Physiological Society.
... Due to increased positive buoyancy, large lungs are a benefit at the surface as they allow individuals to float high out of the water, thus limiting heat loss to the marine environment while performing essential behaviors such as resting, feeding, and nursing. Large lungs are also beneficial at depth because they function as an important O 2 store (Kenyon 1969;Denison and Kooyman 1973;Tarasoff and Kooyman 1973). In contrast, large lungs become an energetic burden at depth for foraging sea otters because high positive buoyancy associated with large lung capacity increases the effort required while diving (Cashman 2002;Yeates et al. 2007). ...
Small body size, large lungs, and dense pelage contribute to the unique challenges faced by diving sea otters (Enhydra lutris) when compared to other marine mammals. Here we determine the consequences of large lungs on the development of diving ability in southern sea otters (Enhydra lutris nereis) by examining the ontogeny of blood, muscle, and lung oxygen stores and calculating aerobic dive limits (cADL) for immature and mature age classes. Total oxygen storage capacity matures rapidly in sea otters, reaching adult levels by 2 mo postpartum. But this result is driven by exceptional lung capacity at birth, followed by a decrease in mass-specific lung volume with age. Blood and muscle oxygen stores remain well below adult values before weaning, with large pups exhibiting 74% and 54% of adult values, respectively. Slow muscle development limits the capacity of immature sea otters to dive against high positive buoyancy due to comparatively large lungs. Immature sea otters diving with total lung capacity (TLC) experience up to twice the mass-specific positive buoyancy as adults diving with TLC but can reduce these forces to comparable adult levels by using a smaller diving lung volume (DLV). The cADL of a juvenile with DLV is 3.62 min, while the cADL of an adult with TLC is 4.82 min. We find that the magnitude of positive buoyancy experienced by sea otters changes markedly with age and strongly influences the ontogeny of diving ability in this species.
... Bubbles in stranded marine mammals Denison and Kooyman, 1973; Kooyman, 1973). Indirect measurements of nitrogen uptake and removal have suggested that alveolar collapse occurs at between 30 m (Falke et al., 1985) in the Weddell seals and 70 m in the bottlenose dolphins (Ridgway and Howard, 1979). ...
Gas embolic lesions linked to military sonar have been described in stranded cetaceans including beaked whales. These descriptions suggest that gas bubbles in marine mammal tissues may be more common than previously thought. In this study we have analyzed gas amount (by gas score) and gas composition within different decomposition codes using a standardized methodology. This broad study has allowed us to explore species-specific variability in bubble prevalence, amount, distribution, and composition, as well as masking of bubble content by putrefaction gases. Bubbles detected within the cardiovascular system and other tissues related to both pre-and port-mortem processes are a common finding on necropsy of stranded cetaceans. To minimize masking by putrefaction gases, necropsy, and gas sampling must be performed as soon as possible. Before 24 h post mortem is recommended but preferably within 12 h post mortem. At necropsy, amount of bubbles (gas score) in decomposition code 2 in stranded cetaceans was found to be more important than merely presence vs. absence of bubbles from a pathological point of view. Deep divers presented higher abundance of gas bubbles, mainly composed of 70% nitrogen and 30% CO 2 , suggesting a higher predisposition of these species to suffer from decompression-related gas embolism.
... Bubbles in stranded marine mammals Denison and Kooyman, 1973; Kooyman, 1973). Indirect measurements of nitrogen uptake and removal have suggested that alveolar collapse occurs at between 30 m (Falke et al., 1985) in the Weddell seals and 70 m in the bottlenose dolphins (Ridgway and Howard, 1979). ...
Gas embolic lesions linked to military sonar have been described in stranded cetaceans including beaked whales. These descriptions suggest that gas bubbles in marine mammal tissues may be more common than previously thought. In this study we have analyzed gas amount (by gas score) and gas composition within different decomposition codes using a standardized methodology. This broad study has allowed us to explore species-specific variability in bubble prevalence, amount, distribution, and composition, as well as masking of bubble content by putrefaction gases. Bubbles detected within the cardiovascular system and other tissues related to both pre- and port-mortem processes are a common finding on necropsy of stranded cetaceans. To minimize masking by putrefaction gases, necropsy, and gas sampling must be performed as soon as possible. Before 24 h post mortem is recommended but preferably within 12 h post mortem. At necropsy, amount of bubbles (gas score) in decomposition code 2 in stranded cetaceans was found to be more important than merely presence vs. absence of bubbles from a pathological point of view. Deep divers presented higher abundance of gas bubbles, mainly composed of 70% nitrogen and 30% CO2, suggesting a higher predisposition of these species to suffer from decompression-related gas embolism.
... Strengthening of the airways also allows extremely rapid, forced expiration without collapse of the airways and the subsequent trapping of air in the alveoli (Kooyman 1989). This means that the alveoli undergo severe, protracted collapse, yet they are able to reinflate without any apparent side effects (Denison and Kooyman 1973). ...
Recent findings are reported about certain aspects of the structure and function of the mammalian and avian lungs that include (a) the architecture of the air capillaries (ACs) and the blood capillaries (BCs); (b) the pulmonary blood capillary circulatory dynamics; (c) the adaptive molecular, cellular, biochemical, compositional, and developmental characteristics of the surfactant system; (d) the mechanisms of the translocation of fine and ultrafine particles across the airway epithelial barrier; and (e) the particle-cell interactions in the pulmonary airways. In the lung of the Muscovy duck Cairina moschata, at least, the ACs are rotund structures that are interconnected by narrow cylindrical sections, while the BCs comprise segments that are almost as long as they are wide. In contrast to the mammalian pulmonary BCs, which are highly compliant, those of birds practically behave like rigid tubes. Diving pressure has been a very powerful directional selection force that has influenced phenotypic changes in surfactant composition and function in lungs of marine mammals. After nanosized particulates are deposited on the respiratory tract of healthy human subjects, some reach organs such as the brain with potentially serious health implications. Finally, in the mammalian lung, dendritic cells of the pulmonary airways are powerful agents in engulfing deposited particles, and in birds, macrophages and erythrocytes are ardent phagocytizing cellular agents. The morphology of the lung that allows it to perform different functions-including gas exchange, ventilation of the lung by being compliant, defense, and secretion of important pharmacological factors-is reflected in its "compromise design."
... The magnitude of these changes appears to be associated with morphological modifications coincident with adaptations for a marine lifestyle (Fig. 4). A unique feature of the lungs of marine adapted mammals is cartilaginous reinforcement of the small airways (Scholander, 1940; Denison and Kooyman, 1973). Such reinforcement provides a rigid system to the level of the alveoli that permits the progressive collapse of the airways in response to increases in pressure. ...
The evolutionary history of marine mammals involved marked physiological and morphological modifications to change from terrestrial to aquatic locomotion. A consequence of this ancestry is that swimming is energetically expensive for mammals in comparison to fish. This study examined the use of behavioral strategies by marine mammals to circumvent these elevated locomotor costs during horizontal swimming and vertical diving. Intermittent forms of locomotion, including wave-riding and porpoising when near the water surface, and prolonged gliding and a stroke and glide mode of propulsion when diving, enabled marine mammals to increase the efficiency of aquatic locomotion. Video instrumentation packs (8-mm camera, video recorder and time-depth microprocessor) deployed on deep diving bottlenose dolphins ( Tursiops truncatus ), northern elephant seals ( Mirounga angustirostris ), and Weddell seals ( Leptonychotes weddellii ) revealed exceptionally long periods of gliding during descent to depth. Glide duration depended on depth and represented nearly 80% of the descent for dives exceeding 200 m. Transitions in locomotor mode during diving were attributed to buoyancy changes with compression of the lungs at depth, and were associated with a 9–60% reduction in the energetic cost of dives for the species examined. By changing to intermittent locomotor patterns, marine mammals are able to increase travelling speed for little additional energetic cost when surface swimming, and to extend the duration of submergence despite limitations in oxygen stores when diving.
Analysing the physiological adaptations of marine mammals and seabirds, this book provides a comprehensive overview of what allows these species to overcome the challenges of diving to depth on a single breath of air. Through comparative reviews of texts on diving physiology and behaviour from the last seventy-five years, Ponganis combines this research into one succinct volume. Investigating the diving performance of marine mammals and seabirds, this book illustrates how physiological processes to extreme hypoxia and pressure are relevant to the advancement of our understanding of basic cellular processes and human pathologies. This book underscores the biomedical and ecological relevance of the anatomical, physiological and molecular/biophysical adaptations of these animals to enable further research in this area. An important resource for students and researchers, this text not only provides an essential overview of recent research in the field, but will stimulate further research into the behaviour and physiology of diving.
The lungs of cetaceans undergo anatomical and physiological adaptations that facilitate extended breath‐holding during dives. Here, we present new insights on the ontogeny of the microscopic anatomy of the terminal portion of the airways of the lungs in five cetacean species: the fin whale (Balaenoptera physalus); the sperm whale (Physeter macrocephalus), the Cuvier's beaked whale (Ziphius cavirostris); the bottlenose dolphin (Tursiops truncatus); and the striped dolphin (Stenella coeruleoalba). We (a) studied the histology of the terminal portion of the airways; (b) used immunohistochemistry (IHC) to characterize the muscle fibers with antibodies against smooth muscle (sm‐) actin, sm‐myosin, and desmin; (c) the innervation of myoelastic sphincters (MESs) with an antibody against neurofilament protein; and (d) defined the diameter of the terminal bronchioles, the diameter and length of the alveoli, the thickness of the septa, the major and minor axis, perimeter and section area of the cartilaginous rings by quantitative morphometric analyses in partially inflated lung tissue. As already reported in the literature, in bottlenose and striped dolphins, a system of MESs was observed in the terminal bronchioles. Immunohistochemistry confirmed the presence of smooth muscle in the terminal bronchioles, alveolar ducts, and alveolar septa in all the examined species. Some neurofilaments were observed close to the MESs in both bottlenose and striped dolphins. In fin, sperm, and Cuvier's beaked whales, we noted a layer of longitudinal smooth muscle going from the terminal bronchioles to the alveolar sacs. The morphometric analysis allowed to quantify the structural differences among cetacean species by ranking them into groups according to the adjusted mean values of the morphometric parameters measured. Our results contribute to the current understanding of the anatomy of the terminal airways of the cetacean lung and the role of the smooth muscle in the alveolar collapse reflex, crucial for prolonged breath‐holding diving.
Respiration refers to gas exchange between an animal and the environment. Except for sea otters, which have unusually large lungs, the lung volumes of marine and terrestrial mammals scale isometrically with body mass. Compared with terrestrial mammals, marine mammals have a larger tidal volume (relative to total lung volume), exhibit high tidal flows (especially in small Odontoceti), and breathe apneustically in which there are periods of apnea. When averaged over periods of eupnea and apnea, marine mammals have a resting respiratory rate that is much less than predicted for but an average tidal volume that is threefold larger than predicted. Barotrauma is physical damage to tissues caused by a difference in pressure between gas in the respiratory system and the surrounding fluid or tissue, and this can be avoided if the pressure equalizes. Marine mammals have a very compliant thorax that enables their lungs (primarily the alveoli) to collapse under pressure. To prevent a high partial pressures of nitrogen in blood and tissues resulting in decompression sickness and nitrogen narcosis, reinforcement of the terminal airways in the lungs of pinnipeds and Cetacea allows the alveoli to collapse eventually isolating residual gas in the non-gas-exchanging airways. There is no clear effect of pressure on enzyme and membrane structure and function in marine mammals, but how they tolerate high pressures remains unknown.
Breath-hold diving is practiced by recreational divers, seafood divers, military divers, and competitive athletes. It involves highly integrated physiology and extreme responses. This article reviews human breath-hold diving physiology beginning with an historical overview followed by a summary of foundational research and a survey of some contemporary issues. Immersion and cardiovascular adjustments promote a blood shift into the heart and chest vasculature. Autonomic responses include diving bradycardia, peripheral vasoconstriction, and splenic contraction, which help conserve oxygen. Competitive divers use a technique of lung hyperinflation that raises initial volume and airway pressure to facilitate longer apnea times and greater depths. Gas compression at depth leads to sequential alveolar collapse. Airway pressure decreases with depth and becomes negative relative to ambient due to limited chest compliance at low lung volumes, raising the risk of pulmonary injury called "squeeze," characterized by postdive coughing, wheezing, and hemoptysis. Hypoxia and hypercapnia influence the terminal breakpoint beyond which voluntary apnea cannot be sustained. Ascent blackout due to hypoxia is a danger during long breath-holds, and has become common amongst high-level competitors who can suppress their urge to breathe. Decompression sickness due to nitrogen accumulation causing bubble formation can occur after multiple repetitive dives, or after single deep dives during depth record attempts. Humans experience responses similar to those seen in diving mammals, but to a lesser degree. The deepest sled-assisted breath-hold dive was to 214 m. Factors that might determine ultimate human depth capabilities are discussed.
The existing different modes of reproduction in monotremes, marsupials and placentals are the main source for our current understanding of the origin and evolution of the mammalian reproduction. The reproductive strategies and, in particular, the maturity states of the neonates differ remarkably between the three groups. Monotremes, for example, are the only extant mammals that lay eggs and incubate them for the last third of their embryonic development. In contrast, marsupials and placentals are viviparous and rely on intra-uterine development of the neonates via choriovitelline (mainly marsupials) and chorioallantoic (mainly placentals) placentae. The maturity of a newborn is closely linked to the parental care strategy once the neonate is born. The varying developmental degrees of neonates are the main focus of this study. Monotremes and marsupials produce highly altricial and nearly embryonic offspring. Placental mammals always give birth to more developed newborns with the widest range from altricial to precocial. The ability of a newborn to survive and grow in the environment it was born in depends highly on the degree of maturation of vital organs at the time of birth. Here, the anatomy of four neonates of the three major extant mammalian groups is compared. The basis for this study is histological and ultrastructural serial sections of a hatchling of Ornithorhynchus anatinus (Monotremata), and neonates of Monodelphis domestica (Marsupialia), Mesocricetus auratus (altricial Placentalia) and Macroscelides proboscideus (precocial Placentalia). Special attention was given to the developmental stages of the organs skin, lung, liver and kidney, which are considered crucial for the maintenance of vital functions. The state of the organs of newborn monotremes and marsupials are found to be able to support a minimum of vital functions outside the uterus. They are sufficient to survive, but without capacities for additional energetic challenges. The organs of the altricial placental neonate are further developed, able to support the maintenance of vital functions and short-term metabolic increase. The precocial placental newborn shows the most advanced state of organ development, to allow the maintenance of vital functions, stable thermoregulation and high energetic performance. The ancestral condition of a mammalian neonate is interpreted to be similar to the state of organ development found in the newborns of marsupials and monotremes. In comparison, the newborns of altricial and precocial placentals are derived from the ancestral state to a more mature developmental degree associated with advanced organ systems.
Mainly for fun, this talk became an exercise in communicating by diagrams. Now its luck is being pushed further by being printed in essentially the same form. It attempts to cover a field that may be unfamiliar to some people, and begins with a man standing in a tall but empty bath.
Vertebraten, die im Wasser leben, werden als aquatisch bezeichnet. Leider gibt es keine besonderen Bezeichnungen für die Experten unter ihnen, die mit besonderer Gewandtheit, Geschwindigkeit oder Ausdauer schwimmen. Alle Fische sind primäre Schwimmer - ihre Vorfahren sind ebenfalls geschwommen. Andere schwimmende Vertebraten sind sekundäre Schwimmer - ihre Vorfahren haben ein terrestrisches Stadium durchlaufen. Deshalb haben sie morphologische und physiologische Einschränkungen, welche die meisten von ihnen daran gehindert haben, wieder vollständig aquatisch zu werden.
During the last 15 years, there has been an intense effort to study diving animals in their own habitat. These studies have been, and continue to be, a necessary extension of the laboratory experiments that first defined some of the basic adaptations involved in diving biology and biochemistry. Field studies have outlined how diving behavior is a critical component to understanding the physiological and biochemical impact of breath-hold exercise underwater. While metabolic limits define the outer boundaries of diving, behavioral patterns place the diving animal at certain points inside that window. For example, Weddell seals can dive for over an hour, but most dives are considerably shorter (Kooyman et al. 1980). Likewise, elephant seals are capable of diving over 1000 m deep, but the majority of dives are to lesser depths (Le Boeuf et al. 1986, 1988). Diving animals do not push themselves to their ultimate capabilities of depth and duration on every dive. While this reasoning may seem obvious, the experimental work necessary to link natural behavior with metabolic requirements is extremely difficult. This due primarily to the problems associated with conducting complex biochemical, physiological, and behavioral studies on large animals in thier own environment. Nevertheless, the number of “synthesis” studies are increasing rapidly on a wide range of diving species. This chapter seeks to summarize how the study of diving biology has proceeded to this point and moves in a mostly chronological organization. It is concerned mainly with the marine mammals because most work has been with this group.
Red cell count, haemoglobin concentration, haematocrit, mean cell volume, and mean cell haemoglobin concentration were recorded for the fur seal Arctocephalus forsteri (Lesson). The data did not indicate haematological adaptations for deep diving nor for extended periods of submergence. Two distinct haemoglobin types were isolated from the red cells by electrophoresis. The oxygen affinity of the blood was low as measured by half-saturation values (p50) of 42.3 mm Hg at pH 7.1 and 26.2 mm Hg at pH 7.4 and 37°c. The low oxygen affinity was mediated by erythrocytic 2,3-diphosphoglycerate, and on this basis a high turnover of oxygen to the tissues is postulated. The role of the blood in oxygen transport appears to be suited for feeding near the surface rather than by deep diving.
The diving physiology of aquatic animals at sea began 50 years ago with studies of the Weddell seal. Even today with the advancements in marine recording and tracking technology, only a few species are suitable for investigation. The first experiments were in McMurdo Sound, Antarctica. Following are examples of what was learned in Antarctica and elsewhere. Some methods employed relied on willingness of Weddell seals and emperor penguins to dive under sea ice. Diving depth and duration were obtained with a time depth recorder. Some dives were longer than an hour and as deep as 600m. From arterial blood samples lactate and nitrogen concentrations were obtained. These results showed how Weddell seals manage their oxygen stores, that they become reliant on a positive contribution of anaerobic metabolism during a dive duration of more than 20 min, and that nitrogen blood gases remain so low that lung collapse must occur at about 25 to 50 m. This nitrogen level was similar to that determined in elephant seals during forcible submersion with compression to depths greater than 100m. These results led to further questions about diving mammal's terminal airway structure in the lungs. Much of the strengthening of the airways is not for avoiding the "bends", by enhancing lung collapse at depth, but for reducing the resistance to high flow rates during expiration. The most exceptional examples are the small whales that maintain high expiratory flow rates throughout the entire vital capacity, which represents about 90% of their total lung capacity.
Copyright © 2014, American Journal of Physiology - Regulatory, Integrative and Comparative Physiology.
SUMMARYA technique has been developed which will permit fusible metal (Wood's metal) casts to be made of lung tissue previously fixed by formalin inflation.
Tracheobronchial airways from Otaria flavescens routinely
were processed for histological, histochemical, and
immunohistochemical methods to study individual mucusproducing
cells (IMPC and submucosal glands. The IMPCs
were interspersed in the epithelium of the trachea. They
showed neutral and weakly acidic and carboxylated glycoconjugates.
Only IMPCs in the trachea secrete sialylated
glycoconjugates. Submucosal glands were formed by 1)
collecting duct lined by a ciliated pseudostratified to simple
columnar epithelium without cilias. They showed neutral
and carboxylic glycoconjugates. 2) Glandular sinus, a
branched secretory unit in which the lining epithelium
showed two possible secretory mechanisms: merocrine type
of neutral glycoconjugates and apocrine type of sialylated
and sulphated or carboxylated glycoconjugates, with positive
reaction for proteins. 3) Glandular branched tubules
emerging from glandular sinuses were lined by columnar
cells with an apical cytoplasm containing neutral and carboxylated
glycoconjugates. Myoepithelial cells surrounded
both glandular sinuses and tubules. Cytokeratin 7 was specific
for glandular sinus and for a few ciliated cells of the
trachea, whereas cytokeratin 19 was observed in glandular
sinuses, glandular tubules, and in some tracheal cells.
These results showed that the secretory cells of glandular
sinuses and tubular glands are well differentiated and that a
possible common origin may be inferred.
A histological study by light microscopy on the development of the terminal airways in fetal lungs of the harbor seal (Phoca vitulina), northern sea lion (Eumetopias jubatus), and sea otter (Enhydra lutris) showed the development of muscle and cartilaginous rings to occur late in gestation. At term they were still much less developed than in the terminal airways seen in adults. The most extensive reinforcement with cartilage of the terminal airways was observed in the sea lion lungs and the least in the seal lungs. The fetal lung development was contrasted with that of the porpoise. We conclude that unlike the porpoise, much further development of the terminal airways in pinnipeds and sea otters occurs during the neonatal stage when the animal is nondiving in a "terrestrial" environment.
The ability of diving mammals to forage at depth on a breath hold of air is dependent on gas exchange, both in the lung and in peripheral tissues. Anatomical and physiological adaptations in the respiratory system, cardiovascular system, blood and peripheral tissues contribute to the remarkable breath-hold capacities of these animals. The end results of these adaptations include efficient ventilation, enhanced oxygen storage, regulated transport and delivery of respiratory gases, extreme hypoxemic/ischemic tolerance, and pressure tolerance. © 2011 American Physiological Society. Compr Physiol 1:447-465, 2011.
The pulmonary circulation is subject to direct challenge from both altered pressure and altered gravity. To efficiently exchange gas, the pulmonary capillaries must be extremely thin-walled and directly exposed to the alveolar space. Thus, alterations in ambient pressure are directly transmitted to the capillaries with the potential to alter pulmonary blood flow. To produce ventilation, the mammalian lung must expand and contract, and so it is a highly compliant structure. Thus, because the capillaries are contained in the alveolar walls, alterations in the apparent gravitational force deform the lung and directly affect pulmonary blood flow both through lung deformation and through changes in the hydrostatic pressure distribution in the lung. High gravitational forces are encountered in the aviation environment, while gravity is absent in spaceflight. Diving subjects the lung to large increases in ambient pressure, while large reductions in pressure occur, often associated with alterations in oxygen level and airway pressure, in aviation. This article reviews the effects of alterations in both gravity and ambient pressure on the pulmonary circulation. © 2011 American Physiological Society. Compr Physiol 1:319-338, 2011.
Halarachne halichoeri Allman (Halarachnidae: Anactinotrichida), a parasitic mite occuring in the nasal cavities of the grey seal, Halichoerus grypus, has an unusual apneustic respiratory system, which is described in detail. The main functions of this system are to facilitate gaseous (tracheal) respiration and prevent foreign material being forced into the tracheae under increased pressure experience when the host seal dives. Possible responses of the system to the rapidly changing pressure regimes are described.
The sections in this article are:
A light microscopic investigation of the histological development of the terminal airways of 18 Stenella attenuata and two S. longirostris showed the lungs to be in a glandular stage of development until 3 months postimplantation (p.i.) age. By 3.5 months (p.i.) the lung was at the canalicular stage. At 4 months mesenchymal rings and muscular bands were in a sphincterlike arrangement around terminal bronchioles. At 7 months (p.i.) the alveolar stage occured. About 8–9 months cartilaginous rings were present and in association with myoelastic sphincters. Their function remains an enigma, even though many hypotheses as to function have been proposed. We suggest that the presence of well-developed sphincters and cartilage in the neonate may give clues to their function as well as offer potential experiments that would not be as suitable in the adult porpoise.
Four species of Phocidae, or true seals, inhabit the waters surrounding the Antarctic continent. These animals are thought to have different diving capabilities. The Weddell seal, Leptonychotes weddelli, is known to be capable of attaining depths up to 600 meters.
The respiratory system of the Weddell seal shows the usual adaptations to an aquatic environment characteristic of other marine mammals. These include lungs that undergo compression collapse at depths greater than 70 meters; hyaline cartilage in the tracheo-bronchial tree as far as the terminal bronchioles; and large amounts of smooth muscle surrounding the distal-most bronchioles. The collapsible lungs provide a mechanism by which air is forced from the alveoli adjacent to the pulmonary capillary beds thereby preventing the absorption of nitrogen gas into the bloodstream. The presence of hyaline cartilage throughout most of the tracheo-bronchial tree increases the effective dead air space that accommodates most of the air forced from the collapsed lungs. The smooth muscle surrounding the respiratory bronchioles prevents their collapse while under the pressures of a deep dive. Collapse of the respiratory bronchioles not supported by cartilage would trap air in the lung alveoli during a dive.
In addition, large-sac-like “diverticulae” are found in the submucosa throughout the tracheo-bronchial tree. These diverticulae, which open directly into the lumen of the tree, appear to be modified glands whose cells, in most cases, do not appear to be specialized for secretory function. They are most numerous in the more distal bronchi and terminal bronchioles where they are situated on both the luminal and adventitial sides of the hyaline cartilage supporting the walls of the air passages. Diverticulae are not found in the respiratory bronchioles or in the respiratory portion of the lungs.
Presented on 12 December 2005 San Diego, California
This paper reviews past and current work on diving behavior, effects of pressure, and the aerobic diving limit from the perspective of the Ken Norris Lifetime Achievement Award. Because of the influence of Norris to marine mammalogy in general, and to my career in particular, I want to emphasize the important tradition of mentors and colleagues as keystones to a successful career in science, and ultimately to the success of science itself. These two related activities are illustrated by studies on marine mammals that were conducted in an endeavor to understand: (1) the behavioral traits associated with deep diving, (2) the mechanical and physiological effects of pressure during routine dives to great depth, and (3) the degree of oxygen depletion that they routinely endure while diving. The search for answers has resulted in numerous physiological and ecological experiments, along with accompanying theoretical analyses. Currently it appears that some deep-diving mammals may suffer from bends, and some may resort more often than what seems physiologically possible to anaerobic metabolism while diving. Above all, the way divers manage their nitrogen and oxygen stores remains a mystery.
The lung of the deep diving Weddell Seal is characterized by an unusually well developed periacinar dense collagenous connective tissue, and a thick coat of smooth musculature particularly in the distal bronchioli. Both, collagen and smooth musculature appear to be functionally interrelated, the first serving presumably as site of origin or attachment for the latter. The orientation of the bronchiolar smooth muscle cells is complex: there exists a basic pattern of two crisscrossing helical bundles that wind in opposite direction. In addition, longitudinal bundles are frequent both at the inside and the outside of the muscular coat. Furthermore, more or less complete ringshaped bundles occur as well as groups of muscle fibres running radially into the collagenous tissue of the surroundings of a bronchiolus. This complex architecture presumably allows active adjustment to various physiological needs of the Weddell Seal including as extremes both closing and widening of the bronchiolar lumen. Isometric contractions of the smooth musculature may stiffen the wall of the distal airways while diving. In the Crabeater Seal which dives for shorter durations and by far less deeply than the Weddell Seal, both periacinar collagen and bronchiolar smooth musculature are of similar arrangement, however, occur in considerably reduced amounts. A rich supply of autonomie nerve fibres with abundant varicosities controls the smooth muscle cells, which are interconnected by gap junctions and receive their innervation par distance (visceral type of smooth musculature). The majority of varicosities contains small clear vesicles, as is typical for cholinergic nerves, suggesting a strong parasympathetic influence. Other varicosities are presumably of peptidergic type. Mast cells and epithelial endocrine cells may exert additional influence on the musculature.
The terminal airways of two antarctic seals (Leptonychotes weddelli, Lobodon carcinophagus) are composed of typical small bronchi and bronchioles the initial segment of which contains cells probably representing Clara cells. The respiratory bronchioles are of considerable length. Their wall contains a highly developed system of spirally arranged bundles of smooth muscle cells. This is interpreted to represent the main means which by being closed before diving prevents the reabsorption of nitrogen while returning to the surface. The amount of smooth muscles evidently is greater in the deep diving Weddell seal than in the crabeater seal. The pneumocytes II occur both within the respiratory bronchioles and in the alveoli, their number seems to be relatively high in both species. The diameter of thin parts of the blood-air barrier in both species is 0.3–0.4 m (0.19–0.22 m in terrestrial mammals). The alveolar septa contain myofibroblasts and one layer of capillaries. The connective tissue of both seals lung is highly developed forming a dense, strong meshwork of septa and a thick pleura visceralis. The septa contain bundles of smooth muscle cells and extensive lymphatic vessels. Due to its particularly thick septa the lobulaton of the lung tissue of the Weddell seal is more obvious than in the crabeater seal, however, in both species the amount of connective tissue in the interlobular septa and the pleura visceralis is greater than in terrestrial carnivores.
Excised lungs from eight marine mammal species [harp seal (Pagophilus groenlandicus), harbor seal (Phoca vitulina), gray seal (Halichoerus grypush), Atlantic white-sided dolphin (Lagenorhynchus acutus), common dolphin (Delphinus delphis), Risso's dolphin (Grampus griseus), long-finned pilot whale (Globicephala melas) and harbor porpoise (Phocoena phocoena)] were used to determine the minimum air volume of the relaxed lung (MAV, N=15), the elastic properties (pressure-volume curves, N=24) of the respiratory system and the total lung capacity (TLC). Our data indicate that mass-specific TLC (sTLC, l kg(-1)) does not differ between species or groups (odontocete vs phocid) and agree with that estimated (TLC(est)) from body mass (M(b)) by applying the equation: TLC(est)=0.135 M(b)(0.92). Measured MAV was on average 7% of TLC, with a range from 0 to 16%. The pressure-volume curves were similar among species on inflation but diverged during deflation in phocids in comparison with odontocetes. These differences provide a structural basis for observed species differences in the depth at which lungs collapse and gas exchange ceases.
Appropriate oxygen supply is crucial for organisms. Here we examine the evolution of structures associated with the delivery of oxygen in the pre- and postnatal phases in mammals. There is an enormous structural and functional variability in the placenta that has facilitated the evolution of specialized reproductive strategies, such as precociality. In particular the cell layers separating fetal and maternal blood differ markedly: a non-invasive epitheliochorial placenta, which increases the diffusion distance, represents a derived state in ungulates. Rodents and their relatives have an invasive haemochorial placental type as optimum for the diffusion distance. In contrast, lung development is highly conserved and differences in the lungs of neonates can be explained by different developmental rates. Monotremes and marsupials have altricial stages with lungs at the early saccular phase, whereas newborn eutherians have lungs at the late saccular or alveolar phase. In conclusion, the evolution of exchange structures in the pre- and postnatal periods does not follow similar principles.
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.
In 1929 I reported the histological structure of the lungs of the porpoise (Tursiops truncalus) and discussed the findings in relation to the aquatic mode of life of whales. The present report concerns the finer structure of the lungs of another aquatic mammal, the manatee (Trichechus latirostris), belonging to the order of Sirenia or sea cows. Concerning the histology of the sirenian lungs, the only previous account is a description by Pick (1907) of the lungs of Halicore dugong, which omits a very complete account of its finer histology. The ultimate aim of these studies is to obtain a knowledge of the modification of the respiratory tract in mammals which have adopted an aquatic mode of life. To date, in addition to the observations of Pick on the dugong, fuller accounts exist for certain Cetacea, namely, three of the porpoises, Deiphinus (Fiebiger, 1916, and Lacoste and Baudrimont, 1926), Tursiops Iruncatus, the bottle-nosed porpoise (Wislocki, 1929), and Phocaena coinmunis, the harbour porpoise (Lacoste and Baudrimont, 1933). The present account of the lungs of the manatee adds the new world representative of the order Sirenia to the observations of Pick on the old world form, the dugong, and makes it possible to undertake a wider comparison of the Sirenia with the porpoises of the order Cetacea. Anticipating the results of our examination of Trichechus, it may be said that they resemble rather closely the account given for the dugong by Pick. Turning to the Cetacea, comparison of Deiphinus and Tursiops (both Delphininae) has shown that these two species agree with one another in almost every detail. On the other hand, the smaller harbour porpoise, Phocaena, representing the Phocaeninae, exhibits, according to Lacoste and Baudrimont, a number of major differences from the Delphininae. The latter finding suggests that there may be a number of modes of specialization of the lungs within the order Cetacea. Finally, a comparison of the two types of Sirenia (which in regard to lung structure show a close resemblance) with the two types encountered thus far in the porpoises, should allow us in a
ONE of the most remarkable structures in the lungs of Cetacea are the sphincters in the respiratory bronchioles. In a number of toothed whales (Odontoceti) the mucosa of these terminal bronchioles shows 8 to 40 consecutive ring-like folds with a circular layer of smooth muscle fibres acting as a sphincter. They may close the passage in the bronchiole completely. They divide the lumen in a number of small consecutive chambers. When the musculature relaxes the passage is re-opened by a system of radially directed elastic fibres, running from the muscular layer to the peripheral layer of cartilage. The sphincters have been described in the common porpoise (Phocaena phocaena (L.)), the bottlenose dolphin (Tursiops truncatus (Mont.)), the common dolphin (Delphinus delphis L.), Prodelphinus caeruleo-albus Meyen, the white whale (Delphinapterus leucas (Pallas)) and in Berardius bairdii Stejneger1 4–9. Several authors showed that these sphincters are not present in baleen whales (Mystacoceti)2,6 7 9. These animals show a very well-developed mass of muscular fibres in the tips of the alveolar septa. Probably these fibres are able to close the alveoles completely.
Minute volume, tidal volume, dead space volume (E, VT, VD), and diving lung volume were measured in adult, unrestrained Weddell seals, Leptonychotes weddelli, whose mean weight was 425 kg. The effects of oxygen ventilation on dive duration were observed in four adult seals. E ranged from 19.5 L/min while resting to 224 L/min after a dive, VT was 5.4 L to 15.2 L, the average VD for two animals was 1.6 L, and lung volumes ranged from 5 L during a dive to 21 L after inspiration. Dive durations of 66 min and probably 87 min were observed after oxygen ventilation. The results indicate that the ability to increase ventilation rate above the resting value, is less than that in terrestrial mammals. Diving lung volumes are large enough that blood and tissue inert gas tensions could increase to several atmospheres during deep dives if small airways closed at low pressures and most of the gases were trapped in the lungs. Blood oxygen tensions may play a primary role in influencing the length of the dive.
The pressure-volume characteristics of the lungs excised from four California sea lions (Zaiophus californianus) and six dogs have been compared by spirometry during cyclic changes of inflation pressure from + 30 to−30 cm H2O and histologically after recompression to atmospheric pressure from an absolute pressure of 112 mm Hg. In comparison with the dog lungs, the sea lion lungs emptied more completely on mild compression and much more completely on severe compression. These findings support Scholander's hypothesis that some marine mammals are protected from decompression sickness by cartilaginous reinforcement of the small airways which permits alveolar emptying during a dive, so isolating compressed gas from pulmonary capillary blood.
Radiograms of the upper portion of the respiratory system were obtained at pressures up to 31.6 atmospheres absolute in the
Weddell seal, Leptonychotes weddelli, and the northern elephant seal, Mirounga angustirostris. The trachea was considerably compressed but not fully collapsed at the highest pressures. No measurable change in the size
of the bronchioles and smaller bronchi was observed. Measurements of total lung volume obtained simultaneously showed that
the seals consistently dived with a small volume.
Pulmonary mechanics were measured in a pilot whale (using blowhole-esophageal pressure for transpulmonary pressure and ventilation at the blowhole for changes of lung volume). Absolute lung volumes were obtained by dilution of helium; alveolar gas concentrations were obtained from end-expired samples of gases.Conductance and compliance (as functions of lung volume) and maximal lung volume (as a function of body weight) have the same magnitudes in this whale as in man. In contrast to man this whale renews as much as 88% of lung air with a single breath and appears to have a more effective defense against aspiration of water. In response to an alveolar CO2 of 303 mm Hg and to inhaled carbachol, average pulmonary resistance increased 20% and 24% respectively (both changes not statistically significant).
On the histological structure of cetacean lungs
- Haynes
Haynes, F. and A. H. Laurie (1937). On the histological structure of cetacean lungs. Discovery Reports 17 : l-6.
Mammals of the Seas Seals, Sea Lions and Walruses. California, Stanford Univ Experimental observations of the respiratory function in diving mammals and birds. Hvoalradets Skrifter; Norske Videnskaps-Akad
- Ridgway S H Springfield
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- V B Scheffer
Ridgway. S. H. (1972). Mammals of the Seas. Springfield, Ill., C. C. Thomas. Scheffer, V. B. (1958). Seals, Sea Lions and Walruses. California, Stanford Univ. Press. Scholander. P. F. (1940). Experimental observations of the respiratory function in diving mammals and birds. Hvoalradets Skrifter; Norske Videnskaps-Akad. Oslo 22: 1-131.
Histological studies of the respiratory portions of the lungs of cetacea
- H Fenn
- Rahn
- D C Washington
Fenn and H. Rahn. Washington D.C., American Physiological Society, pp. 411428. Murata, T. (1951). Histological studies of the respiratory portions of the lungs of cetacea. Whale Res. Instit. (Tokyo) Sci. Rep. 6: 35-48.
Anatomy of the mammalian lung. In: Handbook of Physiology. Section 1
- V E Krahl
Krahl, V. E. (1964). Anatomy of the mammalian lung. In: Handbook of Physiology. Section 1. Respiration. Vol. 1, ed. by W.
Dynamics of breathing
- Mead
Mead, J. and E. Agostoni (1964). Dynamics of breathing. In : Handbook of Physiology. Section 1. Respira-tion. Vol. 1, ed. by W.
Zur feineren Anatomie der Lunge von Halicore dugong
- Pick
Pick. F. K. (1907). Zur feineren Anatomie der Lunge von Halicore dugong. Arch. ftir Naturgesch. 73: 245-253.
Sphincters bronchiques chez le Dauphin (Ddphinus delphis) Ad A study of the histological structure of the respiratory portion of the lungs of aquatic mammals
- J M Barbosa
Barbosa, J. M. 455458. (1914). Sphincters bronchiques chez le Dauphin (Ddphinus delphis). Ad. Sci. Paris 159 Belanger, L. F. (1940). A study of the histological structure of the respiratory portion of the lungs of aquatic mammals. Am. J. Anat. 61: 437461. Bonin, W. and L. F. Belanger (1939). Sur la structure du poumon de Delphinapterus leucas. Trans. Roy. Sot. Canada 33 : 19-22.
Sur la structure du poumon de Delphinapterus leucas
- Bonin
Histological studies of the respiratory portions of the lungs of cetacea
- Murata
Experimental observations of the respiratory function in diving mammals and birds. Hvoalradets Skrifter
- Scholander
Sphincters bronchiques chez le Dauphin Delphinus delphis
- Barbosa