Fiber Architecture and Histology of the Melon in bottlenose dolphins (Tursiops truncatus)
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1 1 December 6, 2005 Fiber Architecture and Histology of the Melon in bottlenose dolphins (Tursiops truncatus) The melon rests on the dorsal surface of the bony rostrum and lies rostral to the nasal passages and most of the facial muscles (reviewed in Mead, 1975). The sound generators, fixed within the nasal passages, also lie caudal to the melon (Cranford et al., 1996). The melon is longer than it is wide giving it an oval shape and rests at a slight angle with respect to the bony rostrum. The melon has been described to be composed of specialized fat, called acoustic fat, wrapped in a fibrous outer core (Norris and Harvey, 1974; Varanasi and Malins, 1971 as sited in Cranford et al., 1996). The so-called acoustic fat of the melon is composed of specific fatty acids (e.g. wax esters and triglycerols) that are generally toxic to mammals and energetically costly to deposit (reviewed in Cranford et al., 1996). The melon consists of an inner and outer core (Norris and Harvey, 1974). The inner core contains short chain fatty acids which transmit sound at a slow velocity whereas the outer region contains longer fatty acid chains which transmit sound at a high velocity (Norris and Harvey, 1974). Due to its location and fatty acid composition, the melon acts as a boundary between seawater and the sound generators of odontocetes and is believed to function in focusing and propagating sound to the surrounding aquatic environment. The location of the melon within the odontocete forehead has been well defined by Mead (1975) and Cranford et al. (1996). The nasal passages, located dorsally on the skull, form a portion of the caudal boundary of the melon. The nasal passages can be defined as a series of blind diverticula (sacs), extending from a common passageway called the spiracular cavity. All diverticula are found in bilateral pairs and are lined with pigmented epithelium. Mead (1975) discussed four sacs in the nasal passages the vestibular sacs, the inferior vestibules, the
2 2 December 6, 2005 nasofrontal sacs, and the premaxillary sacs. The broad, flat vestibular sacs are laterally oriented and lie just deep to the blowhole. Mead (1975) observed these sacs in fresh specimens to be wrinkled in texture, which is indicative of their ability to change shape. The small diameter nasofrontal sacs are paired, U-shaped sacs that are placed like parentheses around the nasal passage. These diverticula only open to the nasal passage through small slits leading to the inferior vestibule, which lie along the caudal wall of the nasal passage, ventral to the vestibular sacs. The nasal passage continues ventrally from the nasofrontal sacs and inferior vestibules until it diverges into the two internal nares, bisected by both a fleshy and bony septum. The premaxillary sacs, just dorso-rostral to the bony nares, are flattened paired diverticula that follow the contours of the bony rostrum and rest directly on the periosteum of the premaxillae. The premaxillary sacs are extremely asymmetrical in shape, with the right larger than the left. Mead (1975) hypothesized that the sacs in the nasal passage play a role in sound production by acting as sound reflectors to shield the posterior portion of the head from the emitted sound field and as air reservoirs to recycle air during sound production. Cranford et al. (1996) supported this functional hypothesis by stating that the mechanism for sound production in odontocetes is pneumatic. They hypothesized that sound is produced in the odontocete forehead when air is forced through the sound generators. There has been a long standing debate over the structures involved in sound generation and the location of the generators in the odontocete forehead. Cranford et al. (1996) introduced the monkey lip dorsal bursae (MLDB) complex. They used density measurements obtained from non-invasive CT scans to visualize the structures in the forehead. The scans were then used as a road map during their gross dissections. This powerful technique revealed two pairs of fat bodies within the walls of the spiracular cavity, which Cranford et al. (1996) termed the dorsal
3 3 December 6, 2005 bursae. Two fat bodies are embedded in the posterior wall of the spiracular cavity and two in the anterior wall. Both posterior bursae align with the anterior bursae such that both the right and left side of the spiracular cavity contain a pair of bursae. Each bursa is contained in a connective tissue capsule and is located at the dorsal edge of the spiracular cavity, just deep to the vestibular sacs. The dorsal bursae are not directly exposed to the lumen of the spiracular cavity, but instead lie within small, lip-like structures. These lips are called monkey lips (Poughet and Beauregard, 1885 as cited in Cranford et al., 1996). The monkey lips are darkly pigmented epithelium structured as a series of ridges and grooves. Each monkey lip is associated with a fat body to form a functional unit called the MLDB complex (Cranford et al., 1996). These lips are pressed tightly together and seal off the dorsal portion of the spiracular cavity. However, Cranford et al. (1996) proposed that sound is produced when pressurized air from the nares is passed over the MLDB complex. The flow of air causes the monkey lips to vibrate which sets the dorsal bursae in motion. The MLDB complex uses air flow and air pressure to create vibrations in soft tissue. These tissue borne vibrations constitute the sound generated by the MLDB complex. The melon lies rostral to these proposed sound generators. Thus, the sounds or vibrational energy produced by the MLDB complex must travel to the melon before it can be emitted into the external environment. Cranford et al. (1996) suggested that there is a potential acoustic pathway (PAP) between the MLDB complex and the melon. The PAP is a channel which extends from the anterior dorsal bursae caudally and merges with the posterior region of the melon rostrally. This channel is made of low density, short chain fatty acids (Cranford et al., 1996). CT scans revealed that the PAP diverges from the posterior melon into a right and left branch. In Tursiops truncatus and in Delphinus delphis, the right arm of the PAP lies along the midline and terminates at the anterior dorsal bursae on the right side of the spiracular cavity.
4 4 December 6, 2005 However, Cranford et al. (1996) found that the left arm of the PAP diverged from the midline in both species of odontocetes. Cranford et al (1996) also found that the branch orientation varied across different species of odontocetes. For example, they found that in Lagenorhynchus obliquidens, both the right and left branches of the PAP diverged from the midline whereas in Pontoporia blainvvillei, the PAP is oriented as a series of twists and turns. Cranford et al. (1996) hypothesized that when air is pushed past the monkey lips, the dorsal bursae begin to vibrate. These vibrations are propagated through the PAP and into the melon. The bony rostrum, the rostral muscles, and the nasal plug muscle form the ventral floor of the melon. The rostral muscles lie ventrolaterally to the melon and can be separated into two distinct portions, the lateral portion and the medial portion (Mead, 1975). Both portions are considered a fraction of the same muscle; however Mead (1975) gave them different names because each portion contained different muscle fiber orientations. The lateral portion of the rostral muscle originates on the maxillae and inserts primarily onto the lip and outer region of the melon. The medial portion of the rostral muscle also originates on the maxillae, but it only inserts onto the melon. Although Mead (1975) separately named the rostral muscles, he also notes that they are cranial extensions of the two facial muscles. There is also a muscle mass located ventrocaudally to the melon and dorsorostral to the premaxillary sacs called the nasal plug muscle. Mead (1975) described the nasal plugs as rounded, irregularly shaped soft tissue structures that serve to occlude the bony nares. These two large fleshy bodies also have small protrusions or nodes on their far lateral corners, which fit easily into the opening of the inferior vestibules. The nasal plugs function to seal off the opening to the internal nares during a dive. During inspiration and expiration, the animal must retract the nasal plugs to permit air flow. These large fleshy bodies must open to allow oxygen to enter the
5 5 December 6, 2005 body during inspiration and close quickly and tightly to prevent water from entering the respiratory system. The nasal plug muscle, which originates from the premaxillae, is responsible for the dynamic movement of the nasal plugs over the internal nares. Mead (1975) found that the nasal plug muscle interfaces and grades into the ventral floor of the melon. Both the ventral floor and the caudal wall of the melon have been carefully described by Mead (1975) and by Cranford et al. (1996), however, a description of the dorsorostral portion of the melon is still under debate. The fundamental question in this debate is: what structure lies along the dorsal and dorsorostral portion of the melon, blubber or a specialized connective tissue? Mead (1975) observed a distinct interface between the dorsal portion of the melon and the overlying dermis, but does not classify the overlying dermis as blubber or as specialized connective tissue. Cranford et al. (1996) on the other hand, does not offer any sort of description of this region of the melon. However, Cranford et al. (1996) did describe a connective tissue capsule surrounding the caudal portion of the melon which they termed the connective tissue theca. Cranford et al. (1996) described this sheath-like structure as a casing for the melon, which ventrally graded into the nasal plug muscle. This structure can be seen in CT scans because it is marked by a sharp increase in density between the fat of the melon and the surrounding connective tissue and muscle. However, the connective tissue theca was not identified in dissections by Mead (1975). The existence of the connective tissue theca is still being debated because it has not been identified histologically or in gross dissection. Thus far, the nasal passages, the sound generators, and some of the musculature within the odontocete head has been described using the work by Mead (1975) and Cranford et al. (1996). Mead s approach seems tightly bounded to anatomical convention in that he provided
6 6 December 6, 2005 extremely detailed descriptions of the nasal passages and facial musculature. Cranford et al. (1996), on the other hand, published their work twenty years later and utilized non-invasive CT imaging coupled with dissections to describe structures in the odontocete head and to determine how those structures function in sound production. However, an anatomical description of the melon, itself, is lacking in the literature. Mead (1975) describes the melon based on its location to surrounding musculature whereas Cranford et al. (1996) defines the melon by reviewing the literature on its fatty acid composition and by discussing its role in sound propagation. Neither one of these descriptions creates a sufficient and accurate representation of the internal topography of the melon. In a seminal paper describing sound transmission in the porpoise head, Norris and Harvey (1974) described two layers of the melon the central melon and the outer melon. They observed that the central melon is composed of oily fat whereas the outer melon was characterized by a blubber-like, fibrous connective tissue. As mentioned previously, this interface between the inner and outer portion of the melon was observed by Mead (1975). The fiber architecture within the melon and how these fibers interact with the surrounding muscle has not yet been described. Fiber architecture, however, has been described in other sites along the odontocete body. The caudal keel is an interesting structure because it can withstand large amounts of longitudinal deformation and maintain a constant shape. Hamilton et al. (2004) examined the caudal keels of harbor porpoises (Phocoena phocoena) and measured keel strain, characterized the shape of the tailstock, and examined the orientation, diameter, and density of the structural fibers found within the keel. They found that the orientation of the fibers differed along the length of the keel which gives evidence for why the caudal keel can undergo such large scale deformation.
7 7 December 6, 2005 At the anus, there were two types of fibers called the rung fibers, which lie perpendicular to the body wall, and the central oblique fibers, which are right and left leaning fibers in the center of the transverse plane of the keel. Hamilton et al. (2004) concluded that the rung fibers function as tensile stays used to maintain the shape of the caudal keel. The central oblique fibers also help to maintain the shape of the caudal keel by preventing lateral deformation during locomotion. The fiber architecture at the mid keel was similar to that of the anus; except helically wound fibers were also present. At the insertion, the site of the least strain in the keel, there were four fiber orientations found. The rung fibers and the central oblique fibers were also found in the anus as well as columnar fibers and longitudinal fibers. The columnar fibers lie parallel to the body wall whereas the longitudinal fibers exist parallel to the long axis of the body. Therefore, Hamilton et al. (2004) concluded that the increased fiber density at the insertion and the orientation of the fibers along the axis of deformation causes the insertion to strain less than the anus and mid keel. The study by Hamilton et al. (2004) shows that fiber orientation can be used to describe the morphology of structures and the mechanical movement of complex composites. The goal of my research is to describe the fiber architecture and histological structure of the melon. Fiber densities, fiber orientation, and fiber diameter will be measured in three orthogonal planes throughout the entire length of the melon. The outer and inner core of the melon, the rostral muscle and the nasal plug muscle will be examined histologically in order to gain a better understanding of the biological components of the melon.
8 8 December 6, 2005 Literature Cited Cranford, T.W., Amundin, M. Norris, K.S Functional morphology and homology in the odontocete nasal complex: Implications for sound generation. Journal of Morphology: 228, pp Hamilton, J.L., Dillaman, R.M., McLellan, W.A., Pabst, D.A Structural fiber reinforcement of keel blubber in harbor porpoise (Phocoena phocoena). Journal of Morphology: 261, pp Mead, J Anatomy of the external nasal passages and facial complex in the Delphinidae (Mammalia: Cetacea). Smithsonian Contributions to Zoology: 207, pp Norris, K.S., Harvey, G.W Sound transmission in the porpoise head. Journal of the Acoustic Society of America: 56(2), pp
Morphology of the odontocete melon and its implications for acoustic function
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