J. CETACEAN RES. MANAGE. 7(3): 189-209, 2006 189 Elements of beaked whale anatomy and diving physiology and some hypothetical causes of sonar-related stranding S.A. ROMMEL*, A.M. COSTIDIS*, A. FERNANDEZ*, P.D. JEPSON* DA. PABSTA , W.A. MCLELLANA, D.S. HOUSER**, T.W. CRANFORD++, A.L. VAN HELDENAA, D.M. ALLEN++ AND N.B. BARROS? Contact e-mail: sentiel.rommel@myfwc.com ABSTRACT A number of mass strandings of beaked whales have in recent decades been temporally and spatially coincident with military activities involving the use of midrange sonar. The social behaviour of beaked whales is poorly known, it can be inferred from strandings and some evidence of at-sea sightings. It is believed that some beaked whale species have social organisation at some scale; however most strandings are of individuals, suggesting that they spend at least some part of their life alone. Thus, the occurrence of unusual mass strandings of beaked whales is of particular importance. In contrast to some earlier reports, the most deleterious effect that sonar may have on beaked whales may not be trauma to the auditory system as a direct result of ensonification. Evidence now suggests that the most serious effect is the evolution of gas bubbles in tissues, driven by behaviourally altered dive profiles (e.g. extended surface intervals) or directly from ensonification. It has been predicted that the tissues of beaked whales are supersaturated with nitrogen gas on ascent due to the characteristics of their deep-diving behaviour. The lesions observed in beaked whales that mass stranded in the Canary Islands in 2002 are consistent with, but not diagnostic of, decompression sickness. These lesions included gas and fat emboli and diffuse multiorgan haemorrhage. This review describes what is known about beaked whale anatomy and physiology and discusses mechanisms that may have led to beaked whale mass strandings that were induced by anthropogenic sonar. Beaked whale morphology is illustrated using Cuvier's beaked whale as the subject of the review. As so little is known about the anatomy and physiology of beaked whales, the morphologies of a relatively well-studied delphinid, the bottlenose dolphin and a well-studied terrestrial mammal, the domestic dog are heavily drawn on. KEYWORDS: BEAKED WHALES; STRANDINGS; BOTTLENOSE DOLPHIN; ACOUSTICS; DIVING; RESPIRATION; NOISE; METABOLISM INTRODUCTION Strandings of beaked whales and other cetaceans that are temporally and spatially coincident with military activities involving the use of mid-frequency (1-20kHz) active sonars have become an important issue in recent years (Nascetti et al, 1997; Frantzis, 1998; Anon., 2001; 2002; Balcomb and Claridge, 2001; Jepson et al, 2003; Fernandez, 2004; Fernandez et al, 2004; 2005; Crum et al, 2005). This review describes the relevant aspects of beaked whale anatomy and physiology and discusses mechanisms that may have led to the mass strandings of beaked whales associated with the use of powerful sonar. The anatomy and physiology of marine mammals are not as well studied as are those of domestic mammals (Pabst et al, 1999) and within the cetacean family of species even less is known about the beaked whales than about the more common delphinids (e.g. the bottlenose dolphin, Tursiops truncatus). Furthermore, many of the morphological and physiological principles that are applied to pathophysiological evaluations of marine mammals were developed on small terrestrial mammals such as mice, rats and guinea pigs (e.g. Anon., 2001). Predictions and interpretations of functional morphology, physiology and pathophysiology must therefore be handled cautiously when applied to the relatively large diving mammals (Fig. 1). Interpolation is a relatively accurate procedure, but extrapolation, particularly when it involves several orders of magnitude in size, is less so (K. Schmidt-Nielsen, pers. comm. to S. Rommel). Beaked whales are considered deep divers based on their feeding habits, deep-water distribution and dive times (Heyning, 1989b; Hooker and Baird, 1999; Mead, 2002). Observations from time-depth recorders on some beaked 10 10' 10" Cuvier's beaked whale J<=C2S 10"2 101 10? 101 102 Body weight (kg) 103 104 105 Fig. 1. Body size, expressed as weight and length for a variety of mammals. Marine mammals are large when compared to most other mammals and beaked whales are relatively large marine mammals. * Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Marine Mammal Pathobiology Lab, 3700 54th Ave. South, St. Petersburg, FL 33711, USA. + Unit of Histology and Pathology, Institute for Animal Health, Veterinary School, Universidad de Las P almas de Gran Canaria, Montana Cardones, Arucas, Las Palmas, Canary Islands, Spain. # Institute of Zoology, Zoological Society of London, Regent's Park, London, NW1 4RY, UK. A Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC 28403, USA. ** BIOMIMETICA, 7951 Shantung Drive Santee, CA 92071, USA. ++ Department of Biology, San Diego State University, San Diego CA, USA. AA Museum of New Zealand Te Papa Tongarewa, Wellington, New Zealand. ++ National Museum of Natural History, Smithsonian Institution, Washington, DC, 20560, USA. ? Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236 USA. 190 ROMMEL et al: SOME HYPOTHETICAL CAUSES OF SONAR-RELATED STRANDING whales have documented dives to 1,267m and submergence times of up to 70min (Baird et al, 2004; Hooker and Baird, 1999; Johnson et al, 2004). Notably, beaked whales spend most of their time (more than 80%) at depth, typically surfacing for short intervals of one hour or less. Virtually no physiological information on beaked whales exists and information on any cetacean larger than the bottlenose dolphin is rare. Given this paucity of data this review relies on information obtained from both terrestrial mammals and other marine mammal species. In particular it draws heavily from the morphology of a well-studied terrestrial mammal, the domestic dog (Canis familiaris) and a relatively well- studied cetacean, the bottlenose dolphin, referred to herein as Tursiops (Fig. 2). Beaked whale morphology is illustrated using Cuvier's beaked whale {Ziphius cavirostris), further referred to as Ziphius. Ziphius, based on stranding records (they are rarely identified at sea), is the most cosmopolitan of the 21 beaked whale species (within 6 genera: Berardius, Hyperoodon, Indopacetus, Mesoplodon, Tasmacetus and Ziphius) (Baird et al, 2004; Dalebout and Baker, 2001; Mead, 2002; Rice, 1998). ANATOMY/PHYSIOLOGY Before considering the potential mechanism by which sounds may affect beaked whales, it is important to review what is known and can be inferred of their anatomy and physiology. External morphology Aside from dentition and conspecific scarring between males, there are few external morphological differences between the genders of Ziphius (Mead, 2002). The head is relatively smooth (Figs 2 and 3) and the average adult total body length is 6.1m (Heyning, 2002). The throats of all beaked whales have a bilaterally paired set of grooves associated with suction feeding (Heyning and Mead, 1996). Ziphius bodies are robust and torpedo-like in shape, with small dorsal fins approximately 1/3 of the distance from the tail to the snout. The relatively short flippers can be tucked into shallow depressions of the body wall (Heyning, 2002). Specialised lipids Marine mammals have superficial lipid layers called blubber (Fig. 3). Blubber in non-cetaceans is similar to the subcutaneous lipid found in terrestrial mammals; in contrast, the blubber of cetaceans is a thickened, adipose-rich hypodermis (reviewed in Pabst et al, 1999; Struntz et al, 2004). Cetacean blubber makes up a substantial proportion (15-55%) of the total body weight (Koopman et al, 2002; McLellan et al, 2002) and the lipid content can vary depending upon the species and the sample site (Koopman et al, 2003a). Blubber is richly vascularised to facilitate heat loss (Kanwisher and Sundes, 1966; Parry, 1949) and is easily bruised by mechanical insult. Since blubber has a density that can be different from those of water and muscle, it may respond to ensonification differently, particularly if conditions of vascularisation (i.e. volume and temperature of blood) vary. The roles blubber (and other lipids) may play in whole-body acoustics should be the subject of further research. As in other odontocetes, the hollowed jaw is surrounded by acoustic lipids1, although the beaked whale acoustic lipids are chemically different from those of other odontocetes (Koopman et al, 2003b). These acoustic lipids conduct sound to the pterygoid and peribullar sinuses and ears (Koopman et al, 2003a; Norris and Harvey, 1974; Wartzog and Ketten, 1999) and may function as an acoustical amplifier, similar to the pinnae of terrestrial 1 Evidence from anatomical, morphological, biochemical and behavioural studies all support the role of the melon and mandibular lipids in the transmission and reception of sound by odontocetes (Norris and Harvey, 1974; Koopman et al., 2003b; Ketten et al., 2001;Varanasi etal, 1975; Wartzog and Ketten, 1999). Thus, these fats are collectively referred to here as the 'acoustic lipids'. 1m (g^g^X (a) Cuvier's beaked whale (e) California sea lion L (g) Domestic dog (f) Bottlenose dolphin Fig. 2. The skeleton of a Cuvier's beaked whale, (a) compared to selected marine mammal skeletons: sea otter, Enhydra lutris (b); harbour seal, Phoca vitulina (c), Florida manatee, Trichechus manatus latirostris (d); California sea lion, Zalophus californianus (e); bottlenose dolphin (f) and the domestic dog, Canis familiaris (g). Each skeleton was scaled proportionately to the beaked whale. The Ziphius skeleton was drawn from photographs of Smithsonian Institution skeleton #504094 and from photographs courtesy of A. van Helden; other skeletons were re-drawn from Rommel and Reynolds (2002). J. CETACEAN RES. MANAGE. 7(3): 189-209, 2006 191 Melon Blowhole Eye /t." Dorsal fin Flukes Throat groove (a) Flipper Umbilicus \ - Anus Female urogenital opening Male urogenital opening Dorsal fin Blowhole Flukes Melon (b) Umbilicus Blubber at midline s*5 Anus Female urogenital opening Male urogenital opening Blubber at midline (c) (d) Rostral muscles Sound reception Blowhqje 7^ (e) Air sac Acoustic fat (melon) External ear opening (f) Acoustic fats Fig. 3. The external morphology of a Cuvier's beaked whale (a) compared with that of the bottlenose dolphin (b). When compared to terrestrial mammals, Odontocetes have extensive and atypical fat deposits and fat emboli have been implicated in some beaked whale mass strandings; thus, their potential sources (such as well-vascularised fat deposits) are of special interest. Skin lipids (or blubber) perform several functions: for example, buoyancy, streamlining and thermoregulation. (c) This drawing illustrates the thickness of the blubber of a dolphin along the midline of the body, (d-f) Odontocetes have specialised acoustic lipids, represented by contours in f, which are found in the melon and lower jaw. These lipids have physical characteristics that guide sound preferentially. mammals (Cranford et al., 2003). The ziphiid melon is similar in size, shape and position to that of other odontocetes (Heyning, 1989b), but Koopman et al. (2003b) have shown that like the jaw fat, the acoustic lipids of the ziphiid melon are also chemically different. This suggests potential differences in sound propagation properties and perhaps in response to anthropogenic ensonification. Thus, understanding the role and composition of acoustic lipids may be important in interpreting lesions in mass stranded beaked whales. Extensive fat deposits are also found in the skeleton. Most cetacean bones are constructed of spongy, cancellous bone, with a thin or absent cortex (de Buffrenil and Schoevaert, 1988). Like the fatty marrow found in terrestrial mammal bones, the medullae of cetacean bones are rich in lipids and up to 50% of the wet-weight of a cetacean skeleton may be attributed to lipid. Since it has been demonstrated that individual lipids within the same, as well as different, parts of the cetacean body may be structurally distinct, it may be of value to analyse the composition of fat emboli to determine if the sources are from general or specific lipid deposits. Thus, lipid characterisation of fat emboli may help pinpoint the source of lipids and therefore the site of injury. The skeletal system There is a pronounced sexual dimorphism in the skulls of Ziphius; the species name {cavirostris) is derived from the deep excavation (prenarial basin) on the rostrum that occurs in mature males (Heyning, 1989a; Heyning, 2002; Kernan, 1918; Omura et al, 1955). The bones of male beaked whale 192 ROMMEL et al.: SOME HYPOTHETICAL CAUSES OF SONAR-RELATED STRANDING rostra (the premaxillaries, maxillaries and vomer) may become densely ossified (in the extreme, up to 2.6g cm~3 in Blainville's beaked whale, Mesoplodon densirostris), thought to be an adaptation for conspecific aggression (de Buffrenil and Zyberberg, 2000; MacLeod, 2002). Both genders have homodont dentition (teeth are all the same shape) and a caudally hollowed, lipid-filled, lower jaw, as do other odontocetes. The premaxillary, maxillary and vomer bones are elongated rostrally and the premaxillaries and maxillaries are also extended dorsocaudally over the frontal bones (Fig. 4b; telescoping, Miller, 1923). The narial passages are essentially vertical in all cetaceans and the nasal bones are located at the vertex of the skull, dorsal to the braincase. In Tursiops, the nasal bones are relatively small vestiges that lie in shallow depressions of the frontal bones (Rommel, 1990). Conversely, the nasal bones of beaked whales are robust and are part of the prominent rostral projections of the skull apex (Fig. 4; Kernan, 1918; Heyning, 1989a). Odontocetes have larger, more complex pterygoid bones than terrestrial mammals. In delphinids, the pterygoid and palatine bones form thin, almost delicate, medial and lateral walls lining the bilaterally paired pterygoid sinuses. The pterygoid sinuses of Tursiops are narrow structures that are constrained by the margins of the pterygoid bones. In contrast, the pterygoid bones of beaked whales are thick and robust (Figs 4 and 5) and their pterygoid sinuses are very large (measured by Scholander (1940) each to be approximately a litre in volume in the northern bottlenose whale, Hyperodon ampullatus). Beaked whale (and physeteroid) pterygoid sinuses lack bony lateral laminae (Fraser and Purves, 1960). These morphological characteristics of the pterygoid region imply differences in mechanical function and perhaps response to ensonification by anthropogenic sonar, and thus may be important in interpreting lesions found in beaked whales. In most mammals, there is a temporal 'bone', which is a compound structure made up of separate bony elements and/or ossification centres (Nickel et al, 1986). In many mammals, the squamosal bone is firmly ankylosed to the periotic (petrosal, petrous), tympanic (or parts thereof) and mastoid bones to form the temporal bone (Kent and Miller, 1997). However, this is not the case in fully aquatic marine mammals (cetaceans and sirenians), where the squamosal, periotic and tympanic bones (there is some controversy over the nature of the mastoid as a separate 'bone') remain separate (Rommel, 1990; Rommel et al, 2002). Unlike the skulls of most other mammals in which the periotic bones are part of the inner wall of the braincase, the cetacean tympano-periotic bones are excluded from the braincase (Fig. 5; Fraser and Purves, 1960; Geisler and Lou, 1998). The beaked whale tympano-periotic is a dense, compact bone (as in other cetaceans), whereas its mastoid process (caudal process of the tympanic bulla) is trabecular2 (like most other cetacean skull bones). The Ziphius mastoid process, unlike that of the delphinids (and some other beaked whales), is relatively large and interdigitates with the mastoid process of the squamosal bone (Fraser and Purves, 1960). The beaked whale basioccipital bone is relatively massive, with thick ventrolateral crests, in contrast to the basioccipital crests in delphinids, which are relatively tall but thin and laterally cupped (Fig. 5). In odontocetes, there are large, vascularised air spaces (peribullar sinuses) between the tympano-periotics and basioccipital crests. In 2 A trabecular mastoid is also observed in some physeteroids. Tursiops, the pathway from the braincase for the 7th and 8th cranial nerves is a short (parallel to these nerves), open cranial hiatus (Rommel, 1990) bordered by relatively thin bones. In Ziphius, this path is a narrow, relatively long channel through the basioccipital bones (Fig. 5). It is similar in position, but not homologous to the internal acoustic (auditory) meatus of terrestrial mammals. The morphology of the pterygoid and basioccipital bones and the size and orientation of the cranial hiatus likely contribute to differences in acoustical properties and mechanical compliance of the beaked whale skull. These bony structures are therefore of potential importance in the effects of acoustical resonance. The vertebral column supports the head, trunk and tail (Figs 2 and 6). In Tursiops the first two cervical vertebrae are fused, but the rest are typically unfused (Rommel, 1990); in contrast, the first four cervicals of Ziphius are fused. There is more individual variation in the numbers of vertebrae in each of the postcervical regions of cetaceans than in the dog. The numbers of thoracic vertebrae vary between Tursiops and Ziphius: there are 12-14 thoracics in Tursiops and 9-11 in Ziphius. In cetaceans, the lumbar region has more vertebrae than that of many terrestrial mammals, significantly more so in Tursiops (16-19) than in Ziphius (7-9), however the lumbar section of Ziphius is greater in length than that of Tursiops. As in all other cetaceans, there has been a substantial reduction of the pelvic girdle and subsequent elimination (by definition) of the sacral vertebrae. The caudal regions have also been elongated to varying degrees. The vertebral formula that summarises the range of these numbers for Tursiops is C7:T12-14:L16-19:S0:Ca24-28 and for Ziphius is C7:T9- ll:L7-9:S0:Cal9-22 (Figs 6b and 6c). There is a bony channel, the neural canal (Fig. 6b), located within the neural arches, along the dorsal aspects of the vertebral bodies of the spinal column. In most mammals the neural canal is slightly larger than the enclosed spinal cord (Nickel et al., 1986). In contrast, some marine mammals (e.g. seals, cetaceans and manatees) have considerably larger (i.e. 10-30X) neural canals, which accommodate the relatively large masses of epidural vasculature and/or fat (Rommel and Lowenstein, 2001; Rommel and Reynolds, 2002; Rommel et al., 1993; Tomlinson, 1964; Walmsley, 1938). These epidural vascular masses are largest in deeper diving cetaceans (Ommanney, 1932; Vogl and Fisher, 1981; Vogl and Fisher, 1982; S. Rommel, pers. obs. in beaked whales and sperm whales). In the tail, there is a second bony channel formed by the chevron bones, which is located on the ventral aspect of the spinal column (Pabst, 1990; Rommel, 1990). The chevron bones form a chevron (hemal) canal, which encompasses a vascular countercurrent heat exchanger, the caudal vascular bundle (Figs 6b and 6c; Rommel and Lowenstein, 2001). The ribs of cetaceans are positioned at a more acute angle to the long axis of the body than those of terrestrial mammals in order to accommodate decreases in lung volume with depth. The odontocete thorax has costovertebral joints that allow a large swing of the vertebral ribs, which substantially increases the mobility of the rib cage (Rommel, 1990). This extreme mobility of the rib cage presumably accommodates the lung collapse that accompanies depth-related pressure changes (Ridgway and Howard, 1979). In cetaceans, the single-headed rib attachment is at the distal tip of the relatively wide transverse processes instead of the centrum as it is in other mammals (Rommel, 1990). In contrast to Tursiops, in which 4-5 ribs are double-headed, 7 of the ribs in Ziphius are J. CETACEAN RES. MANAGE. 7(3): 189-209, 2006 193 frontal & nas. parietal pmx, soc & max j^s <*t / jug pal P"y bulla nas fn max pmx fm pmx soc max pal ., ?"- orbit ntu W bulla par exo sqa no mas boc crest max pmx frn pmx max pal Ju9 V m pty Wla ?, ?exo ?qa mas exo pmx (c) lac jug soc mandibular fm Ml fossa r boc I _ boc crest cranial sqa hiatus exo mandibular fm fossa osp \ ?J bub als als sqa Fig. 4. Bones of the domestic dog skull (a) compared with a schematic illustration (b) showing telescoping in odontocetes and with the skull bones of Tursiops (c) and Ziphius (d). Telescoping refers to the elongation of the rostral elements (both fore and aft in the case of the premaxillary and maxillary bones), the dorso-rostral movement of the caudal elements (particularly the supraoccipital bone) and the overlapping of the margins of several bones. One major consequence of telescoping is the displacement of the external nares (and the associated nasal bones) to the dorsal apex of the skull. One of the most striking differences between the Tursiops and Ziphius skulls is the relatively massive pterygoid bones of the latter. The nasal bones of beaked whales are more prominent and extend from the skull apex. Tursiops has extensive tooth rows; in contrast Ziphius has no maxillary teeth. The dog and Tursiops skulls are adapted from Rommel et ul. (2002). The Ziphius skull was drawn from skulls S-95-Zc-21 and SWF-Zc-8681-B (courtesy of N. Barros and D. Odell), from photographs of Smithsonian Institution skull #504094 and from photographs courtesy of A. van Helden and D. Allen. double-headed. This arrangement may contribute to the function (e.g. mechanical support or pumping action) of thoracic retia mirabilia located on the dorsal aspect of the thoracic cavity (Fig. 7) by placing the costovertebral hinges closer to the lateral margins of the retia. Delphinids have bony sternal ribs, whereas those of beaked whales are cartilaginous. The sternum of Tursiops is composed of 3-4 sternabrae, whereas that of Ziphius is 5-6. These morphological differences might produce different dynamics during changes of the thorax in response to diving and thus alter some of the physical properties of the air- filled spaces. This is an area requiring further research, particularly because we do not know at what depth beaked whale lungs collapse. The air-filled spaces In addition to the flexible rib cage, cetacean respiratory systems possess morphological specialisations supportive of an aquatic lifestyle (Pabst et ai, 1999). These specialisations involve the blowhole, the air spaces of the head, the larynx and the terminal airways of the lung. The single blowhole (external naris) of most odontocetes is at the top of the head (Fig. 7). During submergence, the air passages are closed tightly by the action of the nasal plug that covers the internal respiratory openings (Fig. 8). The nasal plug sits tightly against the superior bony nares and seals the entrance to the air passages when the nasal plug muscles are relaxed (Lawrence and Schevill, 1956; Mead, 1975). 194 ROMMEL et al.\ SOME HYPOTHETICAL CAUSES OF SONAR-RELATED STRANDING Supraoccipital Parietal- \-l? Squamosal Tympanoperiotic Basioccipital (a) Nasal Frontal Vomer Premaxilla Supraoccipital a. Braincase Maxilla palatine Frontal Supraoccipital Braincase (c) Pterygoid J . Basioccipital Ja Basisphenoid Presphenoid Maxilla (d) 1 Basioccipital Pterygoid , Basisphenoid Presphenoid Fig. 5. Cross-sections of the skulls of Tursiops (a) and Ziphius (b). The cross sections (at the level of the ear) are scaled to have similar areas of braincase. In Tursiops, the pathway out of the braincase for the Vllth &VIIIth cranial nerves is a short open cranial hiatus (Rommel, 1990) bordered by relatively thin bones, whereas in Ziphius it is a narrow, relatively long channel. The ziphiid basioccipital bones are relatively massive with thick ventrolateral crests; in contrast, delphinid basioccipital bones are relatively long and tall, but thin and laterally cupped. Note that in contrast to the Ziphius calf cross-section, the adult head would have a greater amount of bone and the brain size would be different. The cross section of an adult Tursiops is after Chapla and Rommel (2003) and that of Ziphius is after a scan of a calf (courtesy of T Cranford). Midsagittal sections of an adult Tursiops (c; after Rommel, 1990) and an adult Ziphius (d; drawn from photographs of a sectioned skull at the Museum of New Zealand Te Papa Tongarewa). The anatomy of the blowhole vestibule and its associated air sacs varies within, as well as between, odontocete species (Mead, 1975), yet the overall echolocating functions are believed to be similar. In Ziphius, the vestibule is longer and more horizontal than in Tursiops (Fig. 8) and Ziphius has no vestibular sacs, no rostral components of the nasofrontal sacs and the right caudal component of the nasal sacs extends up and over the apex of the skull (Heyning, 1989a). In some Ziphius males, there are relatively small, left (caudal) nasal sacs, which are vestigial or absent in females (Heyning, 1989b). The premaxillary sacs, which lie on the dorsal aspect of the premaxillary bones, just rostral to the bony nares, are asymmetrical, the right being several times larger than the left. In adult Ziphius males, there is a rostral extension of the right premaxillary sac that is (uniquely) not in contact with the premaxillary bone (Heyning, 1989a). In Tursiops, there are small accessory sacs on the lateral margins of the premaxillary sacs (Schenkkan, 1971; Mead, 1975). In contrast, Ziphius has no well-defined accessory sacs (Heyning, 1989a). Based on simple physics, these differences in air sac geometry may influence the mechanical responses of the head to anthropogenic ensonification. Odontocetes have air sinuses surrounding the bones associated with hearing; the peribullar and pterygoid sinuses (Figs 8 and 9). These air sinuses are continuous with each other (Chapla and Rommel, 2003) and have been described by Boenninghaus (1904) and Fraser and Purves (1960) as highly vascularised (see below; Fig. 9) and filled with a coarse albuminous foam, which may help these air-filled structures resist pressures associated with depth as well as with acoustic isolation. The odontocete larynx is very specialised - its cartilages form an elongate goosebeak (Reidenburg and Laitman, 1987). The laryngeal cartilages fit snugly into the nasal passage and the palatopharyngeal sphincter muscle keeps the goosebeak firmly sealed in an almost vertical intranarial position (Lawrence and Schevill, 1956). These morphological features effectively separate the respiratory tract from the digestive tract to a greater extent than is J. CETACEAN RES. MANAGE. 7(3): 189-209, 2006 195 Skeletons scaled to equivalent distance between T1 and Ca1 T11 Ca1 T Cervical: 7 Lumbar: 7 Sacral: 3 Cartilagenous sternal ribs Caudal: 6-23 Neural canal Neura| arch C4 Transverse process Thoracic: 12-14 Cervical: 7 Ca6 Lumbar: 16-19 Ca14U Ca18^ O Caudal: 24-28 Bony sternal ribs Chevron bones Thoracic: 9-11 Cervical: 7 Cartilagenous sternal ribs Chevron bones Fig. 6. The axial skeletons and rib cages of the domestic dog (a) compared to those of Tursiops (b) and Ziphius (c). The caudal region of Tursiops has 24-28 vertebrae while that of Ziphius, 19-22, depending on the individual. The neural canals are the dorsal, vertebral bony channels extending from the base of the skull to the tail, in which are contained the spinal cord and associated blood vessels. The ventrally located chevron bones enclose the chevron canal, in which are found the arteries and veins of the caudal vascular bundle. (Redrawn after Rommel and Reynolds, 2002). found in any other mammal (Figs 7b and 7c; Reidenburg and Laitman, 1987). The complex head and throat musculature manipulates the gas pressures in the air spaces of the head and thus can change the acoustic properties of the air spaces and the adjacent structures (Coulombe et al, 1965). The thoracic cavity (Figs 7a and 7b) contains (among other structures) the heart, lungs, great vessels and in cetaceans and sirenians, the thoracic retia (McFarland et al, 1979; Rommel and Lowenstein, 2001). In Tursiops, the cranial aspect of the lung extends significantly beyond the level of the first rib (Fig. 7a), in close proximity to the skull (McFarland et al, 1979). The terminal airways of cetacean lungs are reinforced with cartilage up to the alveoli (Fig. 7d; e.g. Ridgway et al, 1974). Additionally, the cetacean bronchial tree has circular muscular and elastic sphincters at the entrance to the alveoli (Fig. 7d; Drabek and Kooyman, 1983; Kooyman, 1973; Scholander, 1940). It has been hypothesised that bronchial sphincters regulate airflow to and from the alveoli during a dive (reviewed in Drabek and Kooyman, 1983). Under compression, the alveoli in the cetacean lung collapse and gas from them can be forced into the reinforced upper airways of the bronchial tree. Thus, nitrogen is isolated from the site of gas exchange, reducing its uptake into tissues and mitigating against potentially detrimental excess nitrogen absorption (reviewed in Pabst et al, 1999; Ponganis et al, 2003). The microanatomy of beaked whale lungs has not been described and is therefore an area requiring future research. In cetaceans, the ventromedial margins of the lungs embrace the heart (Fig. 7e), so the heart influences the geometry of the lungs. These single-lobed lungs change shape with respiration and depth and the heart affects the size and shape of the lungs because gas distribution in the lungs changes, but the shape of the heart remains relatively unchanged. Additionally, because of the mobility of the ribs, the size and shape of the lungs change in a manner different than do those of a terrestrial animal with a rigid rib cage and multilobed lung (Rommel, 1990). Since respiratory systems contain numerous gas- 196 ROMMEL et al.: SOME HYPOTHETICAL CAUSES OF SONAR-RELATED STRANDING Lung Blowhole lnr|er ear Melon j w-- ~'~^^nMw?Mm;iiiM^H Eye Hyoid Trachea^V apparatus Heart Blowhole Thoracic Esophagus rete Aorta ' Trachea Heart \ ^v?- \ Anus Liver Stomachs Colon Goose beak (c) Thoracic rete Epidural rete Cartilage (d) Sphincter muscle Alveolae Lungs Heart (e) Fig. 7. The major respiratory and thoracic arterial pathways are illustrated for Tursiops (a, b). Note the structure of the oesophagus and trachea (b, c) and the reinforced terminal airways of the cetacean lung with sphincter muscles surrounding the distal bronchioles (d). The lungs with a heart in between (e) are a complex shape that will have different resonant responses to ensonification from a simple spherical model, (a-b adapted from Rommel and Lowenstein, 2001; c-d adapted from Pabst et al., 1999; e adapted from Rommel et al., 2003). filled spaces, the pressure exerted on them at depth affects their volume, shape and thus their resonant frequencies. The shapes of compressed cetacean lungs and the thorax are also influenced by small changes in blood volume within the thoracic retia mirabilia (Figs 7e and 10c- e; Hui, 1975). Although the thoracic retia have not yet been described in beaked whales, it has been assumed (because they are deep divers and their retia are relatively large) that filling these retia with blood may have a noticeable influence on internal thoracic shape, particularly with depth. The actions of the liver and abdominal organs pressing against the diaphragm, in concert with abdominal muscle contractions, affect gas pressure in and the distribution of mechanical forces on the lungs. Appendicular-muscle- dominated locomotors (such as the dog) couple different sorts of respiratory and locomotory abdominal forces (Bramble and Jenkins, 1993) compared to axial-muscle- dominated locomotors (such as the cetaceans; Pabst, 1990). This action has not been investigated in cetaceans, but it is likely that it plays some role in altering the physical properties of the pleural cavity and the flow of venous blood and therefore may be important in any mechanical analysis of this region. The vascular system The mammalian brain and spinal cord are sensitive to low oxygen levels, subtle temperature changes and mechanical insult (Baker, 1979; Caputa et al, 1967; McFarland et al, 1979). The vascular system helps avoid these potential problems. Mammalian brains are commonly supplied either solely by, or by combinations of the following paired vessels: internal carotid, external carotid and vertebral arteries and less commonly by the supreme intercostal arteries (Fig. 10; Nickel et al, 1981; Rommel, 2003; Slijper, 1936). In cetaceans, the internal carotid terminates within the tympanic bulla but contributes blood to the fibro-venous plexus (FVP), which is associated with the pterygoid and peribullar sinuses (Fig. 9, Fraser and Purves, 1960). These FVPs do contain some arteries (Fraser and Purves, 1960) but J. CETACEAN RES. MANAGE. 7(3): 189-209, 2006 197 Caudal nasal sac Accessory Vertex Premaxillary Melon Pterygoid Peculiar sinus sinus (a) Accessory sac Blowhole Premaxillary sac Nasofrontal sac Vestibular sac (perimeter only) Vestibule Premaxillary sac partly hidden Vertex Melon Pterygoid (b) Blowhole Caudal nasal sac (right side only) Premaxillary Fig. 8. Left lateral and dorsal views of the extracranial sinuses in Tursiops (a) and Ziphius (b). Arrows point to the blowholes and are parallel to the vestibules. The dorsocranial/supraorbital air sacs and sinuses associated with vocalisation and echolocation are much more extensive and convoluted in delphinids than in ziphiids. The pterygoid and peribullar sinuses of ziphiids are much larger than those of delphinids. The dorsal and lateral views of the air sacs of Tursiops are adapted from Mead (1975), those of Ziphius from Heyning (1989a). are mostly venous vascular structures3. The cetacean brain is supplied almost exclusively by the epidural retia via the thoracic retia (Breschet, 1836; Boenninghaus, 1904; Fraser and Purves, 1960; Galliano et al, 1966; Nagel et al, 1968; McFarland et al, 1979). These vascular structures have not yet been fully described for beaked whales. In most cetaceans, the blood delivered to the brain leaves the thoracic aorta via the supreme intercostal arteries and supplies the thoracic retia from their lateral margins (Figs lOd and lOe). The blood then flows towards the midline and into the epidural (spinal) retia mirabilia of the neural canal (Wilson, 1879; McFarland et al, 1979) and is directed 3 FVPs have been described as retia mirabilia but should be classed by themselves. Retia mirabilia (singular- rete mirabile) in the thoracic and cranial regions have been studied by many workers (Breschet, 1836; Wilson, 1879; Boenninghaus, 1904; Ommanney, 1932; Slijper, 1936; Walmsley, 1938; Fawcett, 1942; Fraser and Purves, 1960; Nakajima, 1961; Hosokawa and Kamiya, 1965; Galliano et al., 1966; McFarland etal, 1979; Vogl and Fisher, 1981; 1982; Shadwick and Gosline, 1994; they were reviewed by Geisler and Lou, 1998), but they are still poorly understood, in part because of the variety of terms (e.g. basicranial rete, opthalmic rete, orbital rete, fibro-venous plexus, carotid rete, internal carotid rete, rostral rete, blood vascular bundle) used to describe them; in some references (e.g. McFarland et al., 1979), several different terms are used to label the same structure; conversely, the same term has been used to describe different structures in different individuals. The pterygoid and opthalmic venous plexuses and the maxillary arterial rete mirabile of the cat and the palatine venous plexus of the dog (Schaller, 1992), which are involved with heat exchange, could be homologous to the FVP. The arterial plexuses of the cetacean braincase may be homologous to the rostral internal carotid arterial plexus of terrestrial mammals (Geisler and Lou, 1998). towards the head to supply the brain (Fig. 10c). Interestingly, it has been suggested that the sperm whale (Physeter macrocephalus) brain may be supplied in a slightly different manner (Melnikov, 1997) and because of their phylogenetic proximity (Rice, 1998), it is reasonable to assume that beaked whale morphology approximates that of the condition in Physeter. This is a potentially important area for future research. In the cetaceans for which thoracic and epidural retia have been described, the right and left sides of these vascular structures have little or no communication and there is an incomplete circle of Willis, potentially supplying the right and left sides of the brain independently (McFarland et al, 1979; Nakajima, 1961; Vogl and Fisher, 1981; 1982; Walmsley, 1938; Wilson, 1879). This bilateral isolation of paired supplies may have profound implications on hemispherical sleep (Baker, 1979; Baker and Chapman, 1977; McCormick, 1965; Oleg et al, 2003; Ridgway, 1990) and other important physiological processes. Blood flow is not only separated at the brain. In general, mammals possess two venous returns from their extremities: one deep and warmed; one superficial and cooled (Fig. 11). In the deep veins, which are adjacent to nutrient arterial supplies, countercurrent heat exchange (CCHE) occurs if the temperature of the arteries is higher than that of the veins (Figs 11-13; Schmidt-Nielsen, 1990; Scholander, 1940; Scholander and Schevill, 1955); warmed blood is returned and body heat is trapped in the core. Arteriovenous anastomoses (AVAs), can bypass the capillaries and bring relatively large volumes of blood close to the skin surface to 198 ROMMEL et al: SOME HYPOTHETICAL CAUSES OF SONAR-RELATED STRANDING V PTS pterygoid sinus PT pterygoid bone / PTS pterygoid sinus FVP fibro-venous plexus Middle sinus - PTS pterygoid sinus ? Peribullar sinus -?? TB ET eustacean tube (auditory tube) J.W..OV/7; TB tympanic bulla AMI internal maxillary artery APT pterygoid artery Fig. 9. Skull of a young pilot whale in which the peribullar and pterygoid air sinus system (left) and its vascular system have been injected (on the right) with polyester resin (Fraser and Purves, 1960). The peribullar and pterygoid sinuses extend from the hollow cavity of the pterygoid bone caudally to the region surrounding the tympanic bulla. The FVP is a mostly-venous plexus that surrounds these air sinuses. Both the air sinuses and the FVP are surrounded by a mass of acoustic lipids that extend from the hollow channel of the mandible to the pterygoid and tympano-periotic bones medially. Beaked whale pterygoid sinuses and associated fat structures are massive (Cranford et al., 2003; Koopman et al., 2003b) and their FVPs are presumed to be correspondingly larger than those of the delphinids. maximise heat exchange with the environment (Fig. lib; Bryden and Molyneux, 1978; Eisner et al, 1974). Blood returning in these veins is relatively cool (Hales, 1985). In most mammals, the warmed and cooled venous returns are usually mixed at the proximal end of the extremity. In some cases, such as the brain coolers of ungulates and carnivores, evaporatively cooled blood from the nose is used to reduce the temperature of blood going to the brain (Fig. lie) before joining with the central venous return, thereby allowing the brain to operate at a temperature lower than that of the body core (reviewed in Baker, 1979; Schmidt-Nielsen, 1990; Taylor and Lyman, 1972). In mammals, CCHEs have many configurations in addition to the venous lake surrounding the arterial rete at the base of the brain (Caputa et al, 1967; Caputa et al, 1983; Taylor and Lyman, 1972; illustrated for the antelope in Fig. lie). Increasing the surface area of contact between the arteries and veins in different ways optimises these CCHEs. Three examples of CCHEs found in cetaceans are illustrated in Fig. lid. On the left is a flat array of juxtaposed arteries and veins found in the reproductive coolers of cetaceans (Rommel et al., 1992; Pabst et al., 1998), in the middle is a vascular bundle, an array of relatively straight, parallel channels, an optimum configuration for CCHE (Scholander, 1940), such as is found in the chevron canals of cetacea (Fig. 13c; Rommel and Lowenstein, 2001). On the right (Fig. lid) is a periarterial venous rete (PAVR), which is a rosette of veins surrounding an artery. These CCHEs are found in the circulation of cetacean fins (Figs 13d and 13e), flukes and flippers (Scholander, 1940; Scholander and Schevill, 1955). Superficial veins of a cetacean can supply cooled blood to the body core (Fig. 12a). The veins carrying this blood feed into bilaterally paired reproductive coolers (Figs 12d-g) (Rommel et al, 1992; Pabst et al, 1998). In addition to providing thermoregulation for the reproductive system, cooled blood from the periphery is also returned to the heart via large epidural veins (Figs 12d; Figs 13 and 14), which perform some of the functions of the azygous system in other mammals (Rommel et al, 1993; Tomlinson, 1964). In deep divers, such as beaked whales and sperm whales, these epidural veins are even larger than those observed in delphinids (S. Rommel, pers. obs.). In Tursiops, the epidural venous blood may return to the heart via five very enlarged, right intercostal veins to join the cranial vena cava (Figs 13a; 14b and 14c). Alternatively, during a dive, epidural blood may continue to flow in a caudal direction beyond the intercostal veins so that blood from the brain pools as far away from the brain as possible, as has been hypothesised for seals (Rommel et al, 1993; Ronald et al, 1977). Cooled blood supplied by superficial veins to the epidural veins could potentially exchange heat with the epidural (arterial) retia and/or return cooled blood to the cranial thorax. Additionally, it may cause a change in the local temperature of the spinal cord and juxtaposed veins (Rommel et al, 1993). This hypothesis is supported by the regional heterothermy observed in colonic temperature profiles for seals, dolphins and manatees (Rommel et al, 1992; 1994; 1995; 1998; 2003; Pabst et al, 1995; 1996; 1998). Additionally, superficial veins cranial to the dorsal fin (Fig. 12a) may provide cooled blood that can be juxtaposed to the arterial retia in the head and neck. This morphology has not been described in sufficient detail in J. CETACEAN RES. MANAGE. 7(3): 189-209, 2006 199 Dog brains are supplied by: - internal carotid arteries - basilar artery (via vertebrals) (a) Lateral view Internal carotid artery Internal carotid artery Circle of Willis Intercostal arteries Dolphin brains are supplied by - epidural retia via thoracic retia ? I , . v - y