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Intracellular substrates stores.: (A) Intramyofiber glycogen. Adult male of pygmy sperm whale (Kogia breviceps). PAS stain, 100× magnification. (B) Intramyofiber glycogen. Neonate female of sperm whale (Physeter macrocephalus). PAS stain, 40× magnification. (C) Intramyofiber lipids were visualised as small droplets with a variable staining pattern ranging from olive green to black. Calf male of short-finned pilot whale (Globicephala macrorhynchus). Osmium tetroxide postfixation, 100× magnification. (D) Small fibres typically had a greater lipid concentration as revealed by OT. Adult female of Blainville’s beaked whale (Mesoplodon densirostris). Osmium tetroxide postfixation, 200× magnification.
Source publication
Different marine mammal species exhibit a wide range of diving behaviour based on their breath-hold diving capabilities. They are classically categorized as long duration, deep-diving and short duration, shallow-diving species. These abilities are likely to be related to the muscle characteristics of each species. Despite the increasing number of p...
Contexts in source publication
Context 1
... substrates were readily evident on tissue sections by means of the PAS technique (for glycogen), and the OT technique (for lipids). Glycogen was detected in 17/148 (11.5%) animals, and was visualised as uniformly distributed pink granules throughout the sarcoplasm of the myofibres in those animals with a very fresh/fresh decomposition code ( Fig. 2A,B). In tissue sections having incipient autol- ysis, the glycogen was largely confined to the periphery of the ...
Context 2
... lipids were visualised as small droplets with a variable staining pattern ranging from olive green to black (Fig. 2C,D). Small fibres typically had a greater lipid concentration as revealed by OT. Lipids were visualized in 24/148 (16.2%) animals from 7 different cetacean species, the majority of which (95.8%) belonged to the deep-diving group (Table 1). The OT also stained the lipids contained in the interstitium as well as the myelin sheaths of the ...
Citations
... With regarding to the muscular system, the overall histological structure of the muscular tissue of the dugong was similar to that of other marine mammals including cetaceans (Sierra et al., 2015;Suárez-Santana et al., 2020) and other closely related species, namely the manatee (Grossman, Hamilton & De Wit, 2014;Reynolds & Rommel, 1996), and the Asian elephant (Thitaram et al., 2018). In this study, the diameter of the visceral striated muscle found in the esophagus of the dugong was at the same size of the striated muscle in the body of the vocal cord of the Florida manatee by cross section in the histological study (Grossman, Hamilton & De Wit, 2014). ...
Background
Dugongs are marine mammals with a crescent-shaped tail fluke and a concave trailing margin that belong to the family Dugongidae ., They are distributed widely in the warm coastal waters of the Indo-Pacific region. Importantly, the population of dugongs has decreased over the past decades as they have been classified as rare marine mammals. Previous studies have investigated the habitat and genetic diversity of dugongs. However, a comprehensive histological investigation of their tissue has not yet been conducted. This study provides unique insight into the organs of dugongs and compares them with other mammal species.
Methods
Tissue sections were stained with Harris’s hematoxylin and eosin Y. The histological structure of 17 organ tissues obtained from eight systems was included in this study. Tissue sections were obtained from the urinary system (kidney), muscular system (striated skeletal muscle and smooth muscle), cardiovascular system (cardiac muscle (ventricle), coronary artery, and coronary vein), respiratory system (trachea and lung), gastrointestinal system (esophagus, stomach, small intestine, liver, and pancreas), reproductive system (testis), lymphatic system (spleen and thymus), and endocrine system (pancreas).
Results
While most structures were similar to those of other mammal species, there were some differences in the tissue sections of dugongs when compared with other mammalian species and manatees. These include the kidneys of dugongs, which were non-lobular and had a smooth, elongated exterior resulting in a long medullary crest, whereas the dugong pyloric epithelium did not have overlying stratified squamous cells and was noticably different from the Florida manatee.
Discussion
Histological information obtained from various organs of the dugong can serve as an essential foundation of basal data for future microanatomical studies. This information can also be used as high-value data in the diagnosis and pathogenesis of sick dugongs or those with an unknown cause of death.
... All images were taken at 100X magnification and stained with hematoxylin and eosin. Scale bar 150 µm species and Cuvier's beaked whales) also have very large muscle fibers, ranging in cross-sectional area from 601 to 7324 µm 2 (Velten et al. 2013;Sierra et al. 2015). Large body size and the ability to store large amounts of oxygen enable these animals to achieve low diving mass-specific metabolic rates (Noren and Williams 2000;Davis 2014;Pabst et al. 2016). ...
Adipose tissue has many important functions including metabolic energy storage, endocrine functions, thermoregulation and structural support. Given these varied functions, the microvascular characteristics within the tissue will have important roles in determining rates/limits of exchange of nutrients, waste, gases and molecular signaling molecules between adipose tissue and blood. Studies on skeletal muscle have suggested that tissues with higher aerobic capacity contain higher microvascular density (MVD) with lower diffusion distances (DD) than less aerobically active tissues. However, little is known about MVD in adipose tissue of most vertebrates; therefore, we measured microvascular characteristics (MVD, DD, diameter and branching) and cell size to explore the comparative aerobic activity in the adipose tissue across diving tetrapods, a group of animals facing additional physiological and metabolic stresses associated with diving. Adipose tissues of 33 animals were examined, including seabirds, sea turtles, pinnipeds, baleen whales and toothed whales. MVD and DD varied significantly (P < 0.001) among the groups, with seabirds generally having high MVD, low DD and small adipocytes. These characteristics suggest that microvessel arrangement in short duration divers (seabirds) reflects rapid lipid turnover, compared to longer duration divers (beaked whales) which have relatively lower MVD and greater DD, perhaps reflecting the requirement for tissue with lower metabolic activity, minimizing energetic costs during diving. Across all groups, predictable scaling patterns in MVD and DD such as those observed in skeletal muscle did not emerge, likely reflecting the fact that unlike skeletal muscle, adipose tissue performs many different functions in marine organisms, often within the same tissue compartment.
... As was observed for the spinal cord, the slope of this allometric relationship is similar for the shallow and deep diving species. specializations that extend dive duration (e.g., Martin-Lopez et al., 2015;Sierra et al., 2015;Velten et al., 2013). This study adds to our understanding of the body composition of these deep divers. ...
The cetacean vertebral canal houses the spinal cord and arterial supply to and venous drainage from the entire central nervous system (CNS). Thus, unlike terrestrial mammals, the cetacean spinal cord lies within a highly vascularized space. We compared spinal cord size and vascular volumes within the vertebral canal across a sample of shallow and deep diving odontocetes. We predicted that the (1) spinal cord, a metabolically expensive tissue, would be relatively small, while (2) volumes of vascular structures would be relatively large, in deep versus shallow divers. Our sample included the shallow diving Tursiops truncatus (n=2) and Delphinus delphis (n=3), and deep diving Kogia breviceps (n=2), Mesoplodon europaeus (n=2), and Ziphius cavirostris (n=1). Whole, frozen vertebral columns were cross-sectioned at each intervertebral disc, scaled photographs of vertebral canal contents acquired, and cross-sectional areas of structures digitally measured. Areas were multiplied by vertebral body lengths and summed to calculated volumes of neural and vascular structures. Allometric analyses revealed that the spinal cord scaled with negative allometry (b = 0.51 ± 0.13) with total body mass (TBM), and at a rate significantly lower than that of terrestrial mammals. As predicted, the spinal cord represented a smaller percentage of the total vertebral canal volume in the deep divers relative to shallow divers studied, as low as 2.8% in Z. cavirostris. Vascular volume scaled with positive allometry (b = 1.2 ± 0.22) with TBM and represented up to 96.1% (Z. cavirostris) of the total vertebral canal volume. The extreme deep diving beaked whales possessed 22-35 times more vascular volume than spinal cord volume within the vertebral canal, compared to the 6-10 ratio in the shallow diving delphinids. These data offer new insights into morphological specializations of neural and vascular structures that may contribute to differential diving capabilities across odontocete cetaceans. This article is protected by copyright. All rights reserved.
... Mammals and other endotherms are constrained in their diving lengths and durations (63,88), though many species are capable of extended dives ∼2 hours in some seals and whales (276,575). Tolerance of hypoxia during extended dive durations are largely due to blood and tissue adaptations, including locomotor muscle fiber-type differences (626,667), unrelated to the neural control of breathing (130,369,481,636). Obviously, limiting the chemoreceptor associated inspiratory drive is pertinent while submerged, yet, during sleep, seals experience bouts of apnea that can exceed 20 min, with no pathology or deleterious effects (97), and do not awaken to cease these bouts of apnea, with sleeping eupnea-apneaeupnea cycles occurring uninterrupted (98). ...
Symmorphosis is a concept of economy of biological design, whereby structural properties are matched to functional demands. According to symmorphosis, biological structures are never over designed to exceed functional demands. Based on this concept, the evolution of the diaphragm muscle (DIAm) in mammals is a tale of two structures, a membrane that separates and partitions the primitive coelomic cavity into separate abdominal and thoracic cavities and a muscle that serves as a pump to generate intra‐abdominal (Pab) and intrathoracic (Pth) pressures. The DIAm partition evolved in reptiles from folds of the pleural and peritoneal membranes that was driven by the biological advantage of separating organs in the larger coelomic cavity into separate thoracic and abdominal cavities, especially with the evolution of aspiration breathing. The DIAm pump evolved from the advantage afforded by more effective generation of both a negative Pth for ventilation of the lungs and a positive Pab for venous return of blood to the heart and expulsive behaviors such as airway clearance, defecation, micturition, and child birth. © 2019 American Physiological Society. Compr Physiol 9:715‐766, 2019.
... Locomotor muscle mass in True's, Blainville's and Sowerby's BWs is around 50% of total body mass compared with 28-30% in shallower diving species [46]. Recent studies in deep-diving cetaceans suggest that they share muscle features such as large muscle fibres, high myoglobin content, low mitochondrial volume densities, intramyocyte lipid droplets and higher percentage of intramuscular adipose tissue [50,52]. Cuvier's BW present one of the largest fibre sizes for any marine mammal to date [52]. ...
... Recent studies in deep-diving cetaceans suggest that they share muscle features such as large muscle fibres, high myoglobin content, low mitochondrial volume densities, intramyocyte lipid droplets and higher percentage of intramuscular adipose tissue [50,52]. Cuvier's BW present one of the largest fibre sizes for any marine mammal to date [52]. Mesoplodonts have one of the highest myoglobin concentration values reported for any mammal [46], and their muscle is composed primarily of fast, glycolytic fibres [50]. ...
Mass stranding events (MSEs) of beaked whales (BWs) were extremely rare prior to the 1960s but increased markedly after the development of naval mid-frequency active sonar (MFAS). The temporal and spatial associations between atypical BW MSEs and naval exercises were first observed in the Canary Islands, Spain, in the mid-1980s. Further research on BWs stranded in association with naval exercises demonstrated pathological findings consistent with decompression sickness (DCS). A 2004 ban on MFASs around the Canary Islands successfully prevented additional BW MSEs in the region, but atypical MSEs have continued in other places of the world, especially in the Mediterranean Sea, with examined individuals showing DCS. A workshop held in Fuerteventura, Canary Islands, in September 2017 reviewed current knowledge on BW atypical MSEs associated with MFAS. Our review suggests that the effects of MFAS on BWs vary among individuals or populations, and predisposing factors may contribute to individual outcomes. Spatial management specific to BW habitat, such as the MFAS ban in the Canary Islands, has proven to be an effective mitigation tool and mitigation measures should be established in other areas taking into consideration known population-level information. © 2019 The Author(s) Published by the Royal Society. All rights reserved.
... Proprioceptors are found in nearly all motile animals, from pubic lice (Graber, 1882) to sperm whales (Sierra et al., 2015). Single-unit electrophysiological recordings have revealed that proprioceptors can vary widely in their mechanical sensitivity and stimulus tuning, even within a single limb segment or muscle. ...
Animals rely on an internal sense of body position and movement to effectively control motor behavior. This sense of proprioception is mediated by diverse populations of mechanosensory neurons distributed throughout the body. Here, we investigate neural coding of leg proprioception in Drosophila, using in vivo two-photon calcium imaging of proprioceptive sensory neurons during controlled movements of the fly tibia. We found that the axons of leg proprioceptors are organized into distinct functional projections that contain topographic representations of specific kinematic features. Using subclass-specific genetic driver lines, we show that one group of axons encodes tibia position (flexion/extension), another encodes movement direction, and a third encodes bidirectional movement and vibration frequency. Overall, our findings reveal how proprioceptive stimuli from a single leg joint are encoded by a diverse population of sensory neurons, and provide a framework for understanding how proprioceptive feedback signals are used by motor circuits to coordinate the body.
... Regular reliance on anaerobic respiration may also account for several intriguing findings in previous studies [21,74,91] where high proportions of Type II glycolytic muscle fibers were found in the epaxial muscles of Mesoplodon spp. and Z. cavirostris relative to other deep diving species (e.g., G. macrorhychus). ...
... and Z. cavirostris exhibit large-diameter muscle fibres, which reduce cellular surface-area-to-volume ratios and may thus minimize the metabolic demand of the active ion pumps needed to maintain muscle fibre membrane potential [74,96,97]. Finally, these species exhibit considerably lower mitochondrial densities in muscle tissues relative to G. macrorhynchus [74,91]. These metabolic adaptations likely contribute to longer, more efficient dives and are also consistent with the more limited evasive capacities of target prey species. ...
... We hypothesize that the smaller body masses and other traits such as high mitochondrial densities [60,74,91], may limit the duration of G. macrorhynchus and P. electra dives, and thus their access to lower meso-and bathypelagic niches. However, these traits may also enable them to pursue more evasive and potentially more nutritious components of the DSL [16]. ...
Dive capacity among toothed whales (suborder: Odontoceti) has been shown to generally increase with body mass in a relationship closely linked to the allometric scaling of metabolic rates. However, two odontocete species tagged in this study, the Blainville’s beaked whale Mesoplodon densirostris and the Cuvier’s beaked whale Ziphius cavirostris, confounded expectations of a simple allometric relationship, with exceptionally long (mean: 46.1 min & 65.4 min) and deep dives (mean: 1129 m & 1179 m), and comparatively small body masses (med.: 842.9 kg & 1556.7 kg). These two species also exhibited exceptionally long recovery periods between successive deep dives, or inter-deep-dive intervals (M. densirostris: med. 62 min; Z. cavirostris: med. 68 min). We examined competing hypotheses to explain observed patterns of vertical habitat use based on body mass, oxygen binding protein concentrations, and inter-deep-dive intervals in an assemblage of five sympatric toothed whales species in the Bahamas. Hypotheses were evaluated using dive data from satellite tags attached to the two beaked whales (M. densirostris, n = 12; Z. cavirostris, n = 7), as well as melon-headed whales Peponocephala electra (n = 13), short-finned pilot whales Globicephala macrorhynchus (n = 15), and sperm whales Physeter macrocephalus (n = 27). Body mass and myoglobin concentration together explained only 36% of the variance in maximum dive durations. The inclusion of inter-deep-dive intervals, substantially improved model fits (R² = 0.92). This finding supported a hypothesis that beaked whales extend foraging dives by exceeding aerobic dive limits, with the extension of inter-deep-dive intervals corresponding to metabolism of accumulated lactic acid. This inference points to intriguing tradeoffs between body size, access to prey in different depth strata, and time allocation within dive cycles. These tradeoffs and resulting differences in habitat use have important implications for spatial distribution patterns, and relative vulnerabilities to anthropogenic impacts.
... weddellii), and northern elephant seal (M. angustirostris); (Kanatous et al. 2002;Williams et al. 2011;Kielhorn et al. 2013;Moore et al. 2014;Sierra et al. 2015). ...
... weddellii), mesoplodonts, and the northern elephant seal (M. angustirostris) all possess large muscle fibers (62-119 mM) as compared to the short duration, shallow diving T. truncatus (55 mM); (Kanatous et al. 2002;Williams et al. 2011;Kielhorn et al. 2013;Velten et al. 2013;Moore et al. 2014;Sierra et al. 2015). We know of only two groups of deep diving marine mammals for which mitochondrial volume densities have been directly measured-L. ...
... The differential use of these two muscle fiber types is consistent with swimming patterns recorded for beaked whales, which include more frequent, low amplitude strokes, but also abrupt, high amplitude, shorter duration strokes followed by gliding, which occur during deep dive ascents (Martín Ló pez et al. 2015). These fast fibers, which are rich in myoglobin, do not utilize oxygen to fuel contraction, and possess very low mitochondrial volume densities (Velten et al. 2013;Sierra et al. 2015). Velten et al. (2013) thus hypothesize that they may provide a large, metabolically inexpensive oxygen store for the slow oxidative fibers. ...
Mesoplodont beaked whales are extreme divers, diving for over 45 mins and to depths of over 800 m. These dives are of similar depth and duration to those of the giant sperm whale (Physeter macrocephalus) whose body mass can be 50 times larger. Velten et al. (2013) provided anatomical data that demonstrated that on-board oxygen stores were sufficient to aerobically support the extreme dives of mesoplodonts if their diving metabolic rates are low. Because no physiological data yet exist, we utilized an anatomical approach—the body composition technique—to examine the relative metabolic rates of mesoplodonts. We utilized a systematic mass dissection protocol to compare the body composition of mesoplodonts with those of two short duration, shallow divers—the harbor porpoise (Phocoena phocoena) and bottlenose dolphin (Tursiops truncatus). We then investigated the body composition of two other extreme divers, the southern elephant seal (Mirounga leonina) and P. macrocephalus using data from the literature. Our results demonstrate that extreme divers invest a smaller percentage of their total body mass (TBM) in metabolically expensive brain and viscera, and a larger percent of their TBM in inexpensive integument, bone, and muscle, than do the shallow divers. Deep divers also share features of their locomotor muscle that contribute to relatively low tissue metabolic rates and high oxygen storage capacity, including large muscle fiber diameters, low mitochondrial volume densities, and high myoglobin concentrations. One feature of the locomotor muscle of mesoplodonts, though, is unique among deep divers investigated to date. Rather than having an endurance athlete’s muscle fiber profile, dominated by slow oxidative fibers, mesoplodonts possess a sprinter’s profile, dominated by fast glycolytic fibers. Velten et al. (2013) hypothesized that these fibers are likely inactive during routine swimming and provide a large, metabolically inexpensive oxygen store for the slow oxidative fibers to aerobically power swimming. We suggest that future anatomical analyses, coupled with performance data transduced through tagging studies, will enhance our understanding of the extreme diving capabilities of marine mammals.
... Variations in fiber type composition among marine mammals have been proposed to result from differences in routine dive duration and swimming speed, as well as from age. 16,75,77 Intramyofiber inclusions/deposits were identified with the HE and PAS stains. PAS-positive, diastase-resistant inclusions within skeletal muscles are consistent with deposits of abnormal glycogen, often referred to as a complex polysaccharide. ...
... 36 A variable fatty component in the interstitial connective tissue has been observed in the deep-diving cetaceans that were examined in this study (mainly pygmy sperm whales, shortfinned pilot whales, sperm whales, and the Ziphiidae family) compared with that of other species. 77 The disruption of interstitial fat depots may result in the release of nitrogen gas bubbles from supersaturated tissues and could explain the acute muscle degenerative lesions observed in this group of animals when suffering from decompression sickness. ...
Despite the profound impact that skeletal muscle disorders may pose for the daily activities of wild terrestrial and marine mammals, such conditions have been rarely described in cetaceans. In this study, the authors aimed to determine the nature and prevalence of skeletal muscle lesions in small and large odontocetes and mysticetes (n = 153) from 19 different species. A macroscopic evaluation of the epaxial muscle mass and a histologic examination of the longissimus dorsi muscle were performed in all cases. The only macroscopically evident change was variable degrees of atrophy of the epaxial muscles (longissimus dorsi, multifidus, spinalis) in emaciated specimens. The histopathological study revealed single or combined morphological changes in 91.5% of the cases. These changes included the following: degenerative lesions (75.2%), muscle atrophy (37.9%), chronic myopathic changes (25.5%), parasitic infestation (9.2%), and myositis (1.9%). The skeletal muscle is easily sampled during a necropsy and provides essential microscopic information that reflects both local and systemic conditions. Thus, skeletal muscle should be systematically sampled, processed, and examined in all stranded cetaceans.
