Comparisons With Odontocetes
The upper respiratory tract of humpback whales differs from odontocetes in many respects, including the configuration of the nasal region. There are two blowhole openings (as opposed to one blowhole opening in odontocetes), and the nasal region does not contain any diverticulae. The humpback nasal region is thus relatively simple in construction compared with the complex anatomy of the odontocete nasal passageways (e.g., Mead, 1975; Cranford, 1996). Air released from the humpback's blowholes is, therefore, unlikely to produce the tiny bubbles characteristic of a bubble cloud. The humpback oral cavity, however, is well suited for dividing the emerging air into multiple, smaller units as its opening is modified by the presence of baleen plates suspended from the upper jaw (Fig. 4). When the mouth is partially opened, baleen form a sieve-like barrier through which exiting air would have to pass, in turn breaking it into many very small units that could be released simultaneously to produce a mist-like bubble cloud.
Figure 4. a: Ventral–oblique view of a humpback calf head being lifted by a crane during necropsy at the Caven Point Army Corps of Engineers Station in NJ. Note the separate plates of baleen that comprise the baleen racks (particularly visible where the hoisting rope has broken or parted the baleen plates). The baleen has the appearance of a brush on the lingual (medial) aspect, and the appearance of a comb on the labial (lateral) aspect. b: Close-up of a rack of baleen plates photographed from the lingual aspect, showing the parallel alignment of the plates and the gaps through which bubbles may exit the baleen.
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The humpback larynx is largely composed of the same muscles and cartilages as the larynx of a typical terrestrial mammal. Differences include a lack of cuneiform cartilages, and the caudal edge of the cricoid cartilage was usually fused dorsally to the first four to eight tracheal cartilage rings (Reidenberg and Laitman, 2007, this issue). It also shares some unique characteristics with odontocetes, most notably the ventrally incomplete cricoid cartilage and ventrocaudally elongated processes of the arytenoid cartilages. There were several gross structural differences found which distinguish the humpback larynx from that of odontocetes. Whereas the odontocete larynx has a narrow aditus (Fig. 3a), the humpback larynx has a very large aditus between the epiglottic and corniculate cartilages that leads into the laryngeal lumen (Fig. 3b). The ventral luminal surface of the odontocete larynx usually has a trabeculated appearance with numerous small ventral diverticulae and a midline laryngeal fold, whereas the humpback larynx has only one large ventral diverticulum (laryngeal sac) and no prominent midline laryngeal fold.
The humpback's larynx is not closed dorsally to form a complete tube, as in odontocetes (Fig. 3a,c,e). Rather, the dorsal aspect of the humpback epiglottis is unopposed due to a great height difference between the long epiglottis and the short corniculate cartilages (Fig. 3b,d,f). In terrestrial mammals, the epiglottis is flexible and can come into opposition with the laryngeal inlet as the larynx is raised cranially toward the tongue during a swallow. The odontocete epiglottis is rigid and fused to the thyroid cartilage, and thus has little or no independent movement. The humpback's epiglottis is also rigid, but it is not fused to the thyroid cartilage as in odontocetes. Although it cannot be easily folded caudally over the laryngeal inlet, it does have some movement at the base and, thus, could be dislodged from the nasal region and inserted into the oral cavity while manually elevating the soft palate above the epiglottic tip (Fig. 3f). The tip of the humpback's epiglottis is pointed (Fig. 3b,d,f), while the tip of the odontocete epiglottis is rounded, curled rostrally, and enlarged laterally for interlocking with the palatopharyngeal sphincter (Fig. 3a,c,e). The muscles of the soft palate and palatopharyngeal fold of the humpback collectively form the palatopharyngeal sphincter, but it is not as well developed as the muscular palatopharyngeal sphincter of odontocetes (Fig. 3e).
Intranarial vs. Intraoral Larynx
Channeling air to the mouth from the lungs entails redirection of air from the nasolaryngeal portion of the respiratory tract to the oral cavity. This overlap between the respiratory and digestive tracts is counterintuitive, particularly in mammals adapted to protect the airway. Many mammals (excluding adult humans) have effectively separated the respiratory and digestive tracts (Laitman and Reidenberg, 1988). In the typical mammalian configuration, the epiglottis of the larynx interlocks behind the soft palate (Negus, 1949; Harrison, 1995). This arrangement helps channel air from the nose directly to the trachea and lungs, while food usually passes lateral to the larynx in the food channels (piriform sinuses) en route to the esophagus (Laitman and Reidenberg, 1993). For example, herbivores do not appear to unlock the larynx during swallowing, but rather, pass their liquid and semisolid foods around it in the above manner (Laitman and Reidenberg, 1998). Although baleen whales (mysticetes) are not herbivorous, the consistency of their swallowed food is probably somewhat similar, as it is composed of relatively small organisms (e.g., zooplankton, small fish). Thus, mysticetes probably ingest their food in much the same way as terrestrial mammals, maintaining an intranarial larynx during deglutition. The capability to unlock the larynx from the nasal region for a brief period of time, however, can occur among some terrestrial mammals. For example, a momentary unlocking of the larynx can enlarge the food passageway when swallowing a large piece of meat, or enable communication with the oral cavity as occurs during panting (Laitman and Reidenberg, 1993). While laryngeal unlocking does occur briefly in some terrestrial mammals, it has not been documented in aquatic mammals.
In order to channel air into the mouth for production of a bubble cloud, the ability to unlock the larynx in humpback whales would have to differ from the pattern in other cetaceans. Toothed whales (odontocetes) have a larynx that is held in a permanently intranarial position, which isolates and protects the respiratory tract from the digestive tract (Reidenberg and Laitman, 1987). The elongated, rigid, and arrowhead shape of the rostral laryngeal cartilages facilitates interlocking with the encircling palatopharyngeal sphincter (Reidenberg and Laitman, 1994). Humpback whales also have an elongated larynx and a palatopharyngeal sphincter, although the musculature is not as prominent as that of odontocetes. The humpback's corniculate cartilages curve caudally, and appear to facilitate interlocking with the palatopharyngeal fold. The epiglottis, however, is not as rigid nor is it swollen into an arrowhead shape as it is in odontocetes. As these laryngeal features differ from odontocetes, it appears that the humpback whale's larynx may unlock from behind the soft palate. This unlocking of the epiglottis places the laryngeal aditus intraorally, creating a laryngeal–oral connection that facilitates oral release of air to generate bubble clouds.
An oral mechanism for air release is a dangerous behavior for a marine mammal because is increases risk of drowning. Most terrestrial mammals (except adult humans) have a larynx that is positioned intranarially (Laitman and Reidenberg, 1998). This protects it from accidental incursions of food or liquid from the digestive tract, and even enables simultaneous breathing or vocalizing while swallowing. Aquatic mammals have a particular need to protect the larynx from such incursions due to the added danger of feeding underwater. Odontocetes have exaggerated the terrestrial pattern and have a larynx that is permanently intranarial (Reidenberg and Laitman, 1994). Modifications of the odontocete's rostral laryngeal cartilages and soft palate create an interlock that ensures that the laryngeal aditus remains connected to the nasal region (for breathing and/or vocalizing) and is sealed off from the digestive tract even while pursuing prey, open mouthed, underwater, upside down (MacLeod et al, 2007, this issue; Werth, 2007, this issue).
Although the humpback larynx is normally positioned intranarially (Fig. 5a), we suggest that the epiglottis may be unlocked to be transiently intraoral. Elevation of the soft palate could expose the laryngeal inlet to the oral cavity, as the epiglottis is directed rostrally rather than dorsally. In this arrangement, the soft palate would lie over the deeply concave, dorsal surface of the epiglottis. A tubular channel is thus formed between these structures, allowing air stored in either the lungs or the ventrally located laryngeal sac to be channeled directly into the oral cavity (Fig. 5b). It should be noted that the intraoral position may be maintained only very briefly for the purpose of expelling air, and the larynx then immediately reinserted above the soft palate to re-establish nasolaryngeal patency. Any prolonged exposure of the laryngeal inlet into the oral cavity, particularly after air expulsion, could be risky as water or remnant food could inadvertently enter the unprotected larynx.
Figure 5. a: Schematic representation of the head and neck of a humpback whale viewed in the midsagittal plane during normal respiration. The respiratory tract is shown in red, and the digestive tract is shown in blue. The larynx is depicted in its usual intranarial position with the epiglottis (E) overlapping above the soft palate (SP). This nasolaryngeal connection directs air between the blowholes and the lungs. There is a large laryngeal inlet between the epiglottis and the fused corniculate/arytenoid cartilages (C). The corniculates do not oppose the epiglottis, but rather curl caudally over the cricoid cartilage (Cr). A laryngeal sac (S) is located ventrally between the thyroid cartilage (T) and the trachea (Tr). During swallowing, food would be directed around the larynx in lateral food channels (not shown), which connect the oral cavity with the esophagus (Es). The fused corniculate/arytenoid cartilages are not shown in white, as they are paired and parasagittally positioned. Only cartilages cut in the midsagittal plane are shown in white. b: Hypothesized anatomical position of the larynx during bubble cloud production. The respiratory tract is shown in red, and the digestive tract is shown in blue. Yellow arrows indicate the path of air from the trachea, through the larynx, into the mouth, and through the baleen. The baleen of the right side, although not a midsagittal structure, is included in this figure and diagrammatically represented lateral to the tongue. The larynx is depicted with the epiglottis in a transient intraoral position. The nasal cavity is closed dorsally at the blowhole, and ventrally by the elevated soft palate. In this situation, air may pass either rostrally from the trachea directly over the epiglottis, or ventrally from the trachea into the laryngeal sac and then rostrally over the epiglottis. The tubular channel formed between the epiglottis and the oral surface of the soft palate would then conduct air into the oral cavity. As shown here, the mouth is closed thereby trapping air in the expandable oral cavity. Once a sufficient amount of air is accumulated, the whale could return the epiglottis back to the intranarial position above the soft palate. The whale could then open the mouth slightly to expose only the baleen and elevate the tongue. This action would force the air to exit through the mesh created by the baleen, thereby breaking the air mass into many small bubbles to produce a bubble cloud.
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Air entering the oral cavity through the intraoral epiglottic connection may be stored there due to the nature of the expanding throat pleats. If the mouth is opened only slightly, so that the gape is completely blocked by the exposed baleen plates, air would be forced to exit laterally through the mat of bristly fibers that comprise the lingual surface of the stacked baleen plates (Fig. 4). The exiting air would be disrupted by passage through these bristles, breaking it into many small bubbles. The above-described mechanisms of laryngeal transport of air and its subsequent oral emission may, thus, produce the large volume of very small bubbles in one location underwater that comprise a bubble cloud.
Field observations and video analysis of humpback whales surface feeding in waters off New England confirm the transport of air from the lungs into the mouth as a probable source for the production of bubble clouds (F. Sharpe, personal communication). The “gulping” of air at the surface is unlikely, because feeding whales appear to dive with a streamlined, as opposed to distended, throat before bubble cloud release. Furthermore, the throat decreases in size throughout the surfacing and filtering is completed with the jaws nearly closed (water exits through the lateral and caudal aspects of the mouth). Air accidentally captured during prey engulfment has been observed forcefully exiting the posterior corners of the mouth after prey capture. This behavior, seen repeatedly in several recognized animals that have been studied over a long period of time, always occurred before diving, and without any previous “air gulping” (M. Weinrich, personal communication).
Underwater still photographs (T. Kieckhefer, personal communication) and underwater video footage (D. Salden, personal communication) also confirm oral air release by humpback whales in Hawaiian waters in a nonfeeding context (Figs. 6, 7). These whales were not noted to have gulped air at the surface before these underwater air releases, thus supporting a laryngeal–oral air transport mechanism.
Figure 6. a: Underwater video footage of a humpback whale (on right) bubbling while in the presence of another humpback whale (on left). The whale on the right has previously released a small puff of air from the blowholes (seen rising above whale's head), and is now releasing air from the mouth. Note 3 puffs of bubbles on each side of the head, forming a U-shape that matches the opening of the mouth dorsally. b: This frame is taken 2 seconds later in the same video sequence, and shows how the orally released bubbles form a cloud large enough to hide all of the whale's head and most of the whale's body. Only the whale's white pectoral flippers are visible on either side of the cloud. Both frames are courtesy of Dan Salden and Harrison Stubbs, Hawaii Whale Research Foundation.
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Figure 7. a: Close-up underwater video footage of a dorsal view of a humpback whale's head. The whale is releasing air bubbles from near the tip of its mouth. b: This frame is approximately 2 seconds later than the frame shown in a, and shows the whale releasing more air from the mouth while swimming through the orally released bubble cloud. c: This frame is approximately 2 seconds after the frame shown in b, and shows the whale continuing to swim through the bubble cloud. d: This frame is approximately 2 seconds after the frame shown in c, and shows the whale lifting its tail into the bubble cloud. e: This frame is approximately 2 seconds after the frame shown in d, and shows the expansion of the bubble cloud after the tail has dispersed it. The whale is right behind the bubble cloud, but is no longer discernable to the videographer (except for its right pectoral flipper barely visible at the lower right corner of the image). All frames of this sequence are courtesy of Dan Salden and Harrison Stubbs, Hawaii Whale Research Foundation.
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Humpback whales have developed a unique epiglottic shape that may facilitate laryngeal–oral air transport behavior without risking excessive compromise. The trough-shape may enable the humpback whale to channel air through the lumen of the epiglottis as it is positioned against the undersurface of the soft palate (Fig. 5b). This arrangement creates a tunnel connecting the laryngeal aditus with the oral cavity. The pointed and relatively narrow tip of the epiglottis fits tightly against the soft palate, but if it is slightly depressed ventrally, it can allow air to easily escape over its surface in an oral “exhale.” It can be quickly re-sealed against the soft palate to prevent water incursion once air release is accomplished. Pressure from water or prey entering the oral cavity would force the epiglottis up against the soft palate, thus closing the aditus. The critical period for the whale would thus be limited to the interval during which the larynx is re-inserted back over the hard palate to its normal position for respiration or deglutition.
Purpose of Bubble Clouds
The retention of the risky behavior of bubble cloud generation indicates its survival importance. Although bubble clouds have been observed in conjunction with prey capture and feeding, they have also been observed during nonfeeding behaviors. Bubble clouds might serve an important function in conspecific social signaling including aggression, mate attraction, or play. Humpbacks have been noted to release large quantities of bubbles from the mouth, particularly while in the presence of another humpback whale. Oral air releases form a bubble cloud large enough to hide the whale's body (Fig. 6). This cloud can be enlarged by swimming through it and dispersing it with the tail (Fig. 7). It is not clear whether the visual signal is the most important characteristic, or whether bubble clouds have associated sonic characteristics that serve an important role in communication. The most important use of bubbles is probably in self preservation. Bubbles can be used to confound predators or aggressive conspecifics. Just as the fleeing squid uses ink to distract a predator, a bubble cloud can serve as an underwater “smoke screen” to hide the humpback whale or confuse the predator. Bubbles may function as both a visual screen as well as an acoustic screen. For example, schools of herring have been observed to generate extensive gas bubble releases from the anus (flatulence) while pursued by orcas (Nottestad, 1998). The herring gas bubbles create a barrier that, due to the density difference from water, disrupts orca echolocation (Miller et al., 2006). Humpback whales are similarly vulnerable to attacks by orcas in the open ocean, where there are no obstacles to camouflage their large bodies. Thus, a humpback may defend against predation by hiding behind its bubble clouds, screening it from both visual and auditory detection.
Other species of mysticetes have also been documented to produce bubble emissions. It is not clear, however, whether these air emissions can be orally released. Further research on the laryngeal anatomy other mysticete species is necessary to establish whether the ability for laryngeal–oral air transport is unique to humpback whales, or can be generalized to other mysticetes. Future studies linking the anatomy of the mysticete respiratory tract with growing behavioral data should help clarify the mechanism(s) of mysticete air releases and the various situations in which they are produced and used.