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Diaphragm Structure and Function in the Florida Manatee (Trichechus manatus latirostris)
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SENTIEL ROMMEL1,2,3* AND JOHN E. REYNOLDS III3 Marine Mammal Pathobiology Lab, Florida Marine Research Institute, Florida Fish and Wildlife Conservation Commission, St. Petersburg, Florida 33711 2 Division of Mammals, Smithsonian Institution, Washington, DC 20560 3 Marine Science Department; Eckerd College, St. Petersburg, Florida 33711
ABSTRACT Relative to many other mammals, little is known about the functional morphology of the four extant species of the order Sirenia. In this study, 166 Florida manatee (Trichechus manatus latirostris) carcasses fresh enough to collect detailed anatomical information were examined to describe the gross anatomy of the diaphragm. Our results show that the Florida manatees diaphragm differs from those of other mammals in that it: lies in a dorsal plane, rather than in the more typical transverse plane; is located dorsal to the heart and does not attach to the sternum; and attaches medially at the Ishaped central tendon to bony projections extending ventrally from the vertebral bodies, forming two distinct hemidiaphragms. The manatees transverse septum is a separate structure that lies at a right angle to the diaphragm and separates the heart from the liver and other viscera. The extreme muscularity of the diaphragm and the ability of manatees to adjust their position in the water column with minimal external movement suggest that diaphragmatic contractions may change the volume of each pleural cavity to affect buoyancy, roll, and pitch. We also hypothesize that such contractions, in concert with contractions of powerful abdominal muscles, may compress gas in the massive large intestine, and thereby also contribute to buoyancy control. Anat Rec 259: 4151, 2000. 2000 Wiley-Liss, Inc.
Key words: manatee; Sirenia; diaphragm; transverse septum; buoyancy; functional morphology
The Florida manatee (Trichechus manatus latirostris; Order Sirenia) is endangered due to a variety of human activities that degrade habitat or directly kill animals (Reynolds and Odell, 1991). Although manatees are enormous, with individuals occasionally approaching 4 meters in length and weighing more than 1.5 tons, their secretive behavior has historically hindered eld studies; further, their very bulk, and the fact that they exist in a warm environment where decomposition occurs quickly, have made anatomical studies challenging. Interestingly, Muries classic studies (Murie, 1872, 1880) continue to provide important insights into manatee morphology. For endangered species to be conserved well, it is important to gain as thorough an understanding of species biology as possible. Among the marine mammals, manatees and their sirenian relatives are unique due to their herbivorous diet. Manatee functional morphology has been shaped by both the constraints imposed by occupying
an aquatic habitat (e.g., adaptations to facilitate diving, thermoregulation, navigation, osmoregulation) and those associated with nding, consuming, and digesting foods which can be highly abrasive and are of relatively low nutrient quality (Reynolds and Rommel, 1996).
*Correspondence to: Sentiel Rommel, Marine Mammal Pathobiology Lab; 3700 54th Ave. South, St. Petersburg, FL 33711. E-mail: rommelsa@eckerd.edu Received 25 September 1998; Accepted 10 January 2000
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Fig. 1. Schematic illustrations of the dog diaphragm (after Evans, 1993; Evans and de Lahunta, 1988; Schaller, 1992; Schummer and Nickel, 1979; Schummer et al., 1981). Roman numerals identify ribs. A: Cranial view of the dog diaphragm. The central tendon is Y-shaped and pierced by the caval foramen. The central portion of the pars
muscularis is pierced by the aortic and esophageal hiatuses. B: Left lateral schematic of the dog diaphragm, cut along the midline. The diaphragm attaches ventrally to the caudal aspect of the sternum and dorsally to the lumbar vertebral bodies via the diaphragmatic crura.
primary muscle of inspiration (Schaller, 1992), there is a substantial nonmuscular region of the diaphragm. In most mammals, the relatively thin central tendon (centrum tendineum), which is pierced by the esophagus, caudal vena cava, and aorta, distributes the forces of the muscular portion and positions these apertures in locations that are relatively stable biomechanically (Hildebrand, 1995; Schummer and Nickel, 1979). (Parenthetical terms in italics follow the Nomina Anatomica Veterinaria as illustrated by Schaller, 1992.) The shape, orientation, and distribution of muscle and tendon bers can vary, depending upon the species. The central tendon of the dog (used here to represent a well studied, terrestrial mammal, see Pabst et al., 1999) occupies approximately 21% of the surface of the diaphragm; the remainder is muscular (Gordon et al., 1989). The dogs central tendon is also Yshaped, with the arms of the Y directed dorsolaterally to become tendons of the crura (plural of crus; Fig. 1A). The peripheral muscular portion (pars muscularis) attaches at
or near the distal ends of the vertebral ribs and to the caudal aspect of the sternum (pars sternalis). In most mammals, the muscular portion provides the contractile forces needed to move the diaphragm caudad and ventradincreasing the volume of the thoracic cavity and decreasing the volume of the abdominal cavity (Bramble and Jenkins, 1993, 1998). The diaphragm subdivides the bony thorax in a roughly diagonal transverse plane into a thoracic cavity, located cranial and lateral to the diaphragm, and an intrathoracic (bounded by ribs) portion of the abdominal cavity, located immediately caudal and medial to the diaphragm. At rest, the intrathoracic abdominal organs press against the diaphragm making it bow craniad (Fig. 1B). Only in mammals is the diaphragm prehepatic, separating the heart from the liver (Kardong, 1995). Thus, in the typical mammal, the umbrella-shaped (concave caudally) diaphragm separates the thoracic (pleural and pericardial) and the abdominal (peritoneal) cavities. The lungs of typical mam-
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Fig. 2. Schematic representations of the development of the diaphragm. A: Left lateral view of a typical early mammalian embryo. The coelomic cavity is subdivided by three folds that arise from the ventral and lateral aspects of the coelom. Ventrad from the body wall is the transverse septum; craniolaterad from the lateral walls are the pleuroperitoneal membranes; and slightly caudad to the transverse septum are the pleuroperitoneal membranes. B: Left lateral view of a typical mam-
mal, the transverse septum joins with the pleuroperitoneal membrane to form the diaphragm. The pleuropericardial membrane is not part of the diaphragm. The diaphragm is prehepatic and is anchored to the sternum. C: Transverse view of the early development of the typical mammalian diaphragm. Non-locomotory hypaxial muscle migrates on to the pleuroperitoneal fold as a secondary ingrowth from the body wall.
mals extend beyond the diaphragm cranially, to either side of the heart ventrolaterally, and toward the distal rib tips caudally. In some species, accessory lobes of the lung insert between the heart and the diaphragm (Schummer and Nickel, 1979). Because it isolates the thoracic and abdominal cavities, a diaphragm must be perforated by structures associated with the digestive, nervous, and circulatory systems (Fig. 1A). The esophageal hiatus (hiatus esophageus) on the midline is surrounded by muscle of the diaphragm (Evans, 1993). In the dog, the esophageal hiatus is located dorsal to the heart near the caval foramen (foramen venae cavae), which penetrates the diaphragm just to the right of the midline (Schummer and Nickel, 1979). The caval foramen is not typically surrounded by muscle (the vena cava of the seal does have a muscular sphincter; Harrison and Tomlinson, 1956; Elsner et al., 1971); rather it crosses through the right wing of the central tendon and is associated with or bounded by the pleuropericardial membrane. The third large aperture of the diaphragm, the aortic hiatus (hiatus aorticus), is located on the midline and is bordered by mus-
cles (Schaller, 1992). The aortic hiatus is located at the level of the lumbar vertebraewhich is at the caudal extent of the diaphragm. There are also smaller apertures for the passage of nerves and the azygos vein (Nickel et al., 1986).
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Fig. 3. Photographs of ventral views of dissected manatee carcasses. A: After removal of the ventral skin, fat, and musculature the full extent of the large intestine becomes apparent. The large intestine (LI) with contents accounts for 10% of the total body weight and can measure 20 m in length. The ruler is 15 cm in length. The stomach (S) and the liver (L) are visible caudal to the three sternal ribs. B: Removal of the
GI tract reveals the hemidiaphragms (He), the liver (L), the right kidney (K), and the transverse septum (T). C: The two central tendons (C) of the hemidiaphragms attach medially to the hypapophyses. The pars muscularis (M) attaches laterally to the ribs. The cranialmost bers of the hemidiaphragms pass dorsal to the heart and attach to the ribs.
which isolates the pleural cavity from the peritoneal cavity, is formed (Fig. 2A). In most mammals, the transverse septum joins with the pleuroperitoneal membrane to form part of the diaphragm (Goodrich, 1930; Fig. 2B). The diaphragm in the typical
mammal is thus postcardiac and prehepatic because it extends from the caudal aspect of the sternum to the dorsal body wall between the heart and the liver. The phrenic nerves (Fig. 2C), which innervate the diaphragmatic muscles, arise in the cervical region of the fetus
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Fig. 4. Schematic illustrations of the manatee diaphragm and lung. A: In left lateral view, the manatee lung is a relatively attened and elongate structure that occupies the dorsal region of the pleural cavity. B: In cross section the manatee body is an ellipse, with the diaphragm stretched almost horizontally from the hypapophyses at the midline to the ribs at mid shaft.
the location of the fetal pleuroperitoneal fold at that time in development. Subsequent changes in the positions of the muscles and folds drag the nerves with them (Goodrich, 1930).
Fig. 5. Left lateral schematic representations of the development of the diaphragm of the manatee. The transverse septum persists in separating the heart and the liver but is not part of the diaphragm. The manatee diaphragm does not attach to the sternum and thus is not prehepatic.
the parietal peritoneum, that extend along the right and left dorsal aspects of the liver. The falciform ligament (falciforme hepatis) is a midline fusion of the two layers (right and left) of peritoneum covering the ventral and
Figure 6.
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cranial aspects of the liver and the caudal aspect of the diaphragm and the ventral body wall. The falciform ligament tethers the umbilical vein in the fetus and newborn to the ventral aspect of the body cavity. The serosal surface of the lung, the pulmonary pleura (pleura pulmonalis, also referred to as the visceral pleura), extends between the lung and the midline as the pulmonary serosal ligament. In the typical mammal the pulmonary ligament supports the lung at its hilus near the heart. The heart is surrounded by a membrane made of three layers: the brous pericardium (pericardium brosum) and two serosal layers, one on each side of the pericardium. The pericardium surrounds the heart, isolating it from the surrounding tissues and secreting lubricating uid. The sternopericardial ligament (sternopericardiaca) is found between the sternum and the pericardium at the apex of the heart (there may be one or two such ligaments in domestic mammals). A phrenicopericardial ligament (phrenicopericardiacum) is found between the pericardium and the diaphragm in some mammals (Schaller, 1992; Schummer and Nickel, 1979).
Inc., Roswell, GA). Subsequent edits were effected with a mouse by comparing printouts with photographs and sketches. Tissues from hemidiaphragms and related structures of three (one adolescent, one sub-adult, and one adult) manatees were collected for histological examination. Samples were collected from the transverse septum of three carcasses and from the diaphragm, dorsal to the heart and mid-thorax, of two. Tissues were xed in 10% buffered formalin, embedded in parafn, sectioned at 8 for light microscopy, and stained with hematoxylin and eosin.
RESULTS
The results of our study are summarized in Figures 4 6.
Fig. 6. A: Left lateral illustration of the heart, transverse septum, hiatuses for the aorta and esophagus, and the caval foramen. Note that the transverse septum is composed of elements of the pericardium and parietal peritoneum and that the diaphragm does not attach to the sternum. The hypapophyses, to which the central tendons of the hemidiaphragms attach along the midline, start at T5. B: Ventral illustration of the abdominal cavity after removal of the GI tract, liver, and urogenital systems. Structures in Figure 6A align with those in Figure 6B. The central tendons of the hemidiaphragms attach to the hypapophyses of
the vertebral column along the midline and the diaphragm muscles attach laterally to the ribs. The transverse septum is a separate structure from the hemidiaphragms. The cranial-most bers of the hemidiaphragms continue cranial to the transverse septum; muscle bers extend cranial to the transverse septum and attach to the rst ribs; these muscle bers are illustrated with broken lines to show the trajectories of the orthogonal tendinous bers. C: Ventral illustration of the lungs and their serosal ligaments. The circle and box have the same relative proportions as those above.
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of the peritoneal cavity is referred to as intrathoracic. The intrathoracic abdominal organs press against the ventral aspect of the diaphragm, making it bow dorsad. This bowing forms a ventrally concave separator between the pleural cavities and the peritoneal cavity. The central tendon bers insert onto and/or cross over the ventral aspects of the vertebrae and the ventral, midsagittal vertebral processes, which are called hypapophyses (Fig. 4; Flower, 1885). The cranial-most hypapophysis is on thoracic vertebra ve (T5). Hypapophyses gradually enlarge to be most robust in the caudal portion of the thorax. They get abruptly smaller on the last one or two thoracic vertebrae and are absent from the ventral aspects of the post-thoracic vertebrae. In the manatee there are few hypaxial locomotor muscle bers that extend into the thorax and attach to the hypapophyses.
cle bers are actually longer and continue parallel to the ribs (Fig. 4B). The remainder of the transverse extent is tendinous. The muscle bers terminate on the distal tips of most ribs in neonates. As animals get older and the ribs grow in length, the muscle attachments do not remain at the tips; instead, the positions of the muscle insertions become more proximal along the rib shafts as the animal grows. The ribs also grow in width and thickness, with the most robust parts at or near the attachment sites of the muscles. Almost all of the grossly visible bers of the diaphragm run parallel to the long ribs1 except at the diaphragms caudal margin where additional, orthogonal bers appear. These orthogonal bers extend caudally from the caudal margin of the hemidiaphragm and cranially for a short distance. Medially, the orthogonal bers are well dened and extend to the midline at or near the last hypapophysis. More laterally the bers are less regular and blend with the fascia on the ventral aspect of the hypaxial locomotory muscles. The caudal-most hemidiaphragm bers bow caudally over the last short rib and rejoin the last long rib where the muscle bers of the diaphragm begin. They extend cranio-laterally from there to anchor on the penultimate long rib. This departure from a path that parallels the last long rib creates the so-called hypogastric fossa (Fig. 6B; Murie, 1872) near the distal tips of the last two long ribs. There is some variation among individuals in terms of specic points of attachment. The robustness and density of the bers of the central tendon is greatly reduced caudal to the last rib at what is essentially the caudal margin of each pleural cavity. The medial portion of each pleural cavity ends at about the caudal margin of the last long rib; the lateral portion ends at the level of the caudal margin of the penultimate long rib.
1 The distinction of long and short ribs is necessitated by the variable nature of the last ribs in Florida manatees; it is common to nd a well formed transverse process on one side and a distinct, articulated rib on the other side of the same vertebra.
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There are small, crescent-shaped hiatuses in the ber mesh of the central tendon as it crosses the midline, each at roughly the level of an intervertebral disc, through which pass the segmental arteries that branch from the aorta.
intact at their caudal margins and were attached to the vertebral midline as in older specimens (the cranial portion of the diaphragm was destroyed before the specimen was obtained). The embryonic model we provide is based on the assumption that the pathway of the phrenic nerve is conserved. We have not actually examined embryos small enough to verify the development of the transverse septum empirically.
DISCUSSION
The manatees diaphragm differs from the diaphragms of other mammals. In manatees, bers of the central tendon attach to bony hypapophyses extending ventrally from the vertebral bodies to produce two hemidiaphragms. Manatees have an elongate diaphragm with an I shaped central tendon rather than the Y shaped tendon of other mammals. The hypapophyses begin on thoracic vertebra ve (T5) and gradually enlarge to be most robust in the caudal portion of the thorax (Fig. 4). They get abruptly smaller on the last one or two thoracic vertebrae and are absent from the ventral aspects of the post-thoracic vertebrae. There are few hypaxial muscle bers (typically associated with the locomotion of some marine mammals; Arkowitz and Rommel, 1985) that extend into the thorax and attach to the hypapophyses. Thus, the primary function of the hypapophyses is not locomotion, but rather to support the diaphragm and respiration. The separate hemidiaphragms lie horizontally and extend virtually the entire length of the body cavity. Interestingly, the physical isolation of the two pleural cavities and the mechanical separation of the two hemidiaphragms decreases the possibility that the function of both lungs will be decreased after collision with a boat, thus increasing the probability that the manatee will survive (such collisions account for about 25% of all Florida manatee deathsAckerman et al., 1995). The MMPL often necropsies carcasses with well healed multiple rib breaks on one side of the body that must have impaired function of the ipsilateral lung until healed. The manatee diaphragm does not attach to the sternum; rather the cranial-most bers attach to the ribs dorsal to the heart. Thus the diaphragm cannot separate the heart from the liver as it does in all other mammalian orders. In the typical mammal, the transverse septum separates the heart and the liver and is a component of the diaphragm (Figs. 1 and 2B). In the manatee, the transverse septum separates the heart and liver but is not a component of the diaphragm (Figs. 5 and 6). In light of the expected attachment of the diaphragm to the sternum and the presence of the transverse septum in that position, coupled with the large volume of material that has to be moved around during necropsy, it would be reasonable to mistake the manatee transverse septum for a diaphragm (e.g., Bonde et al., 1983; Rowlatt and Marsh, 1985). The transverse septum, consisting of pericardium cranially and parietal peritoneum caudally, extends between the diaphragm dorsally and the sternum ventrally. The transverse septum is a mechanically weak barrier, unlike the prehepatic musculotendinous diaphragm of other mammals. The presence of a weak transverse septum suggests that manatees have a reduced requirement for the mechanically stabilizing effects used in locomotion that are associated with the diaphragm during parts of the respiratory cycle observed in terrestrial mammals (Bramble, 1989; Bramble and Jenkins, 1993, 1998).
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The mediastinum is an artefact of the downward expansion of the lungs on either side of the heart in the typical mammal (Romer and Parsons, 1986). In humans the mediastinum is the space left in the middle of the chest between the two pleurae (Osol, 1972). In domestic mammals it is dened as a sagittally placed partition consisting of two serous membranes extending from the thoracic inlet in front to the diaphragm behind, and attaching dorsally to the thoracic vertebrae and ventrally to the sternum (Schummer and Nickel, 1979, p. 6). Schaller (1992, p. 192) adds it contains most of the structures in the thoracic cavity except the lungs. The traditional definition of the mammalian mediastinum does not apply to manatees. The positions of the aortic hiatus, caval foramen, and esophageal hiatus are unusual because of the conguration of the diaphragm. The relationships between the heart and the lungs suggest that the manatees mediastinum be dened differently than the mediastinum of other mammalian orders. We recommend that the manatee mediastinum refer to the midline region dorsal to where the pericardium attaches to the heart and ventral to the diaphragm, cranial to the transverse septum up to approximately the level of C1. This is essentially what constitutes the cranial mediastinum of other mammals, as dened by Schummer and Nickel (1979). The thyroid, thymus, tracheobronchial lymph nodes, and the tracheobronchial bifurcation of the trachea are in the region we dene as mediastinal. The pericardium has two serosal layers. The inner parietal layer (lamina parietalis) secretes and absorbs pericardial uid. The outer layer, termed the pleurapericardiaca in other mammals, should be renamed for the manatee since it is not within the pleural cavity. The cranial portions of the pericardium are intrathoracic and the caudal portion is juxtaposed to parietal peritoneum to make the transverse septum. Perhaps lamina intrathoracica is appropriate.
diaphragms to the dorsal (pleural) aspects of the hemidiaphragms at this level. In other mammals the phrenic nerves follow the dorsal aspect of the pericardium to join the diaphragm at the margins of the pericardium (Fig. 1A) to follow the diaphragmatic pleura.
Evolutionary Thoughts
What evolutionary advantages could a horizontal diaphragm provide the manatee? Manatees are sluggish and relatively inactive. Their very low metabolic rates, even for animals of their large size (Irvine, 1983), suggest energy conservation mechanisms that might include minimizing energy expenditure while changing depth. Manatees are herbivores that feed on vegetation in shallow salt and fresh water habitatssuch food doesnt struggle much to get away. Manatees are capable of changing depth by using their locomotory muscles and uke but they commonly change their depth without noticeable muscular action. The commonplace release of gas from the anus but not the nose or mouth is something to consider. Domning (1977) suggests extensive use of the diaphragm in hydrostatic adjustments during diving. Domning and de Buffrenil (1991) extend this idea with a de-
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tailed analysis of the hydrostatic contributions of the elongate lungs and dense bones of the manatee. They consider the assumptions that the heavy bones and horizontal lungs are adaptations for maintaining neutral buoyancy and horizontal trim. We would add the considerable but changeable volume of intestinal gas, the heavy skin (part of another MMPL study), and the abdominal muscles to the list of hydrostatic elements. A thin and horizontal lung would be advantageous for minimizing hydrostatic pressures from the surrounding water when inating the lungs during inspiration. Perhaps the attachment of the cranial-most diaphragm bers to the rst ribs is a mechanical adaptation to allow greater forces to be applied to the central tendons of the hemidiaphragms. Thus the mechanically weak transverse septum, rather than the diaphragm, attaches to the sternum to maintain the separate integrity of the two pleural cavities in order to isolate the abdominal organs from the heart. A more detailed analysis of buoyancy in the manatee is the subject of another study and will be reported at another time. Recall that in the manatee the lungs do not extend to either side of the heart as is found in most other mammals. In mammals, the major factor determining cardiac output is venous return, which can be inuenced by lung and diaphragm mechanics (Bramble, 1989; Bramble and Jenkins, 1993, 1998). This coupling of circulatory performance with respiration is unlikely in manatees and may be related to the very low metabolic rate of the manatee. The manatee diaphragm may be different from that of the dugong (Dugong dugon), a sirenian with a more dolphin-like body than the manatee (Domning, 1977). Domning describes the eshy origins of the diaphragm starting at rib III and forming a transverse line across the rib cartilages and the posterior border of the sternum in the dugong. Further research comparing the diaphragms of the sirenia would clarify structural and functional similarities and differences.
ACKNOWLEDGMENTS
We thank Meghan Bolen, Tim Evans, Llyn French, Judy Leiby, Erin Nill, Tom Pitchford, and Dr. James Quinn at the Florida Marine Research Institute, Drs. James Mead at the US National Museum of Natural History, Daryl Domning at Howard University, D. Ann Pabst at University of North Carolina at Wilmington, Joy Reidenberg and Jeff Laitman at Mt. Sinai School of Medicine for their helpful comments on the manuscript. We thank Llyn French for the photographic art work.
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