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Functional Morphology of the Mouth of the Bowhead Whale and Its Implications for Conservation

Richard H. Lambertsen , Kerry J. Rasmussen , Winston C. Lancaster , Raymond J. Hintz
DOI: http://dx.doi.org/10.1644/BER-123.1 342-352 First published online: 15 April 2005

Abstract

Bowhead whales (Balaena mysticetus) hauled out on shore-fast ice by Inupiat whale hunters off Barrow, Alaska were examined. Anatomical observations confirmed the occurrence of a large, well-muscled tongue. Temporomandibular articulations were synovial. The mandibular symphysis was unfused. Standard measurement of baleen plates and close-range photogrammetry of a baleen rack confirmed that the anterior portion of the baleen rack is strongly convex, in contrast to its shape in balaenopterids. Moderate force applied to the lower lip in a lateral direction caused a pronounced abduction of the lower jaw. These observations support a conclusion that during feeding, the tongue may deflect the incoming flow of prey-laden water from side to side in the mouth, to convey prey slurries into the postlingual recess. Abduction of the lower lip likely would establish a channel for acceleration of flow around the outside of the baleen racks, reducing external pressures and drawing water out through the baleen. Thus, the shape of the baleen rack in the bowhead appears to be an adaptation to reduce the amplitude of the bow wave projected during feeding, the simultaneous advantage being concentration of prey slurries inside the mouth. It may also impart a configuration to the bow wave that stimulates countereffective evasive effort by actively mobile prey. Final compaction of a concentrated prey slurry in the postlingual recess probably involves retraction of the tongue against the oropharyngeal wall. These insights notably enable consideration of certain threats to bowheads and right whales (Balaenidae) associated with oil spills and oral entanglement. Previous research on the “physiologic” effects of fouling of baleen with oil is judged to be inadequate with respect to this taxonomic family. Oral entanglement with nonbiodegradable marine debris is predicted to be lethal because of interference with a critical hydrostatic oral seal.

Key words
  • Cetacea
  • conservation biology
  • entanglement
  • feeding
  • marine debris
  • oil pollution

The feeding mechanism of the bowhead whale (Balaena mysticetus) is a specialized system for filtering small prey organisms from seawater and concentrating these into a physiologically useful form. In its better known features, it is recognizable as an extreme adaptation in a taxon of adaptive extremes. The suborder Mysticeti, baleen whales, is one typified by gigantism. In this taxon, the bowhead has the largest mouth in proportion to body length (Ridgway and Harrison 1985). This accommodates main baleen plates that can exceed 4 m long (Reeves and Leatherwood 1985). Along with minor baleen plates, baleen hairs, baleen bristles, and various supporting tissues, these plates form the baleen apparatus. Two racks or “sides” of baleen develop, 1 per maxillary bone.

Bowhead whales evidently feed at all levels of the water column (Lowry 1993). Species of Zooplankton that are swallowed include the smallest known prey of any cetacean. Examination of stomach contents has revealed copepods 3.5 mm in length with total body volumes as little as 0.002 ml (Lowry and Frost 1984). Other prey species comprise a wide variety of planktonic and benthic invertebrates, including eu-phausiids, mysids, hyperiid amphipods, gammarid amphipods, pteropods, isopods, polychaetes, crabs, snails, and echinoderms (Hazard and Lowry 1984; Lowry 1993; Lowry and Burns 1980; Tomilin 1967). An occasional fish may be ingested (Lowry and Burns 1980). Analyses of stomach contents indicate that copepods, along with the larger euphausiids, represent the dominant prey; with few exceptions, benthic organisms composed a very small proportion of total identifiable prey mass (Lowry and Burns 1980; Lowry and Frost 1984).

Complementing their extreme length, the number of main plates per side of baleen in the bowhead whale is prodigious. The maximal number in adult individuals may be as high as 370 (Scammon fl., 1874, 1969), and values of 310 (Eschricht and Reinhardt 1866) and 305–311 (Nishiwaki and Kasuya 1970) have been reported in bowhead juveniles. To accommodate this serial array of keratinaceous plates, the cranial bones of the skull are extensively telescoped, as is typical to some extent in all cetaceans (Gaskin 1976, 1982; Kellogg 1928; Miller 1923). As a result, the skull of the bowhead can span nearly two-fifths the length of the body in adult males and slightly less in females (Eschricht and Reinhardt 1866). It is the high arch of the braincase and rostrum that gives this animal its common name. This accommodates especially the length, as well as the number, of baleen plates.

Extreme arching of the bones of the skull also distinguishes the bowhead from its closest relatives, the northern and southern right whales of temperate seas (Eubalaena species—Allen 1916; Berta and Sumich 1999; Omura et al. 1969), the pygmy right whale of the Southern Hemisphere (Caperea marginata— Berta and Sumich 1999; Kellogg 1928), the bottom feeding gray whale of the North Pacific (Eschrichtius robustusAndrews 1916), and the fleet rorquals, or grooved baleen whales (Balaenopteridae—Berta and Sumich 1999; Carte and MacAlister 1868; Hunter 1787; Schulte 1916; True 1904). Of these taxa, both the rorquals and the gray whale have relatively short baleen plates. Those of the rorquals are comparatively broad-based. The baleen plates of the northern and southern right whales are of intermediate length and, like those of the bowhead, are narrow-based (Andrews 1916; Pivorunas 1979; Scammon 1969; True 1904). Narrow-based baleen plates thus correlate with slower swimming, and probably lower filtration pressures, because right whales and gray whales are not fleet, at least in comparison with rorquals (Sanderson and Wassersug 1993; Scammon 1969; Scoresby 1811; Werth 2000). Filter area is enhanced in balaenids (right whales); filter pressure probably is greater in balaenopterids (rorquals).

However, little is known about how the baleen apparatus of the bowhead whale actually functions. Like other balaenids, the bowhead whale is a “continuous” ram feeder (Pivorunas 1979; Sanderson and Wassersug 1993). By swimming slowly through concentrations of prey for long periods with their jaws held open, the whale causes prey-laden water to flow into its mouth through a central gap between the 2 baleen racks. This presumably creates a filtration pressure that, on 1st approximation, would be proportional to the square of the velocity of the whale (as in a Pitot tube). However, hydrodynamic phenomena outside the mouth could contribute. If pressures outside the baleen racks were reduced by water accelerating over their external surfaces, for example, this would increase net filtration pressure and lessen the amplitude of the bow wave projected by the whale. The result could be highly adaptive because actively mobile prey then would be less likely to perceive and evade the advancing predator.

The present study investigates this possibility. It follows up on the early report of Fabricius (fl., 1780, 1929), who, during his tenure as monk in Greenland, observed feeding bowhead whales at close range from a kayak. Fabricius (1929:76) noted that the small crustaceans forming the dominant prey of the bowhead apparently “found pleasure” in its baleen, for they seemed to seek it out, going into the mouth “from all directions more or less by themselves.” This observation suggests that the baleen rack of the bowhead whale may be shaped to produce hydrodynamic pressures that promote entry of prey into the mouth.

Such a shape in fact is suggested by various published and unpublished photographs of the mouths of balaenids (e.g., True 1904, plate 46, figure 1). To further test this hypothesis, we used close-range photogrammetry and other morphological methods to characterize the feeding apparatus of the bowhead whale. The resultant data are interpreted with the aim of identifying relations between structure, function, and risk. Conservation implications emerge for right whales generally, because Eubalaena species are morphologically and ecologically similar to B. mysticetus (Berta and Sumich 1999; Gaskin 1982). Also, the likely mode of prehension and deglutition of prey is proposed on the basis of the anatomical findings. The result serves as a basis to consider the risk of ingestion of petroleum hydrocarbons from oil spills and well blowouts, and pathological effects likely associated with fouling of the baleen bristles with oil. Last, mortality caused by fouling of the mouth with nonbiodegradable marine debris is predicted on the basis of comparative anatomical evidence that a hydrostatic oral seal is a critical locomotor adaptation in Mysticeti (Lambertsen and Hintz 2004).

Fig. 1

Scale anatomic drawing of baleen lamina from a 15.7-m female bowhead whale showing standard measures and measurement sites according to Williamson (1973). Each baleen lamina consists of 1 main baleen plate with its medially adjacent minor plates and baleen hairs. These are embedded in the gingival epithelium or gum. The epithelial gum and baleen laminae are attached to the fibrous periosteum of the maxillary bone by means of a richly vascular connective tissue. Papillated leaves of this connective tissue (not shown) penetrate the proximal ends of the baleen plates (Pivorunas 1979; Tullberg 1883).

Materials and Methods

General anatomy.—Anatomic observations were conducted on whales taken by Inupiat whale hunters in the Arctic Ocean off Barrow, Alaska. Three female bowhead whales, 7.5, 8.2, and 8.3 m long, were examined after they were hauled out by Barrow natives onto the shore-fast ice by block and tackle (whales 88B8, 88B7, and 88B6, respectively, according to accession numbers of the Department of Wildlife Management, North Slope Borough, Barrow, Alaska). Photography was conducted in tandem with the butchering process. The tongue of 1 individual, the 8.2-m female, was photographed whole after removal from the mouth, and after being sectioned longitudinally at the midline. The skull of the 7.5-m female was sectioned transversely with a saw and photographed. Projected photographs were used to generate cross-sectional illustrations. We also examined the defleshed skulls of a 9.3-m male, a 8.9-m female, and an 11.0-m male, all taken off Barrow (whales 87B1, 87B2, and 87B3, respectively). Last, we measured the longest baleen lamina taken from a 15.7-m female bowhead whale landed in Gambell, Alaska (whale 88G1). Terminology used for different portions of the baleen apparatus follows that of Williamson (1973).

Baleen laminae are predominantly epithelial structures. Each consist of 1 main baleen plate and any medially adjacent minor plate(s) and baleen hair(s), along with a minor internal investment of vascularized connective tissue (Fig. 1).

The main baleen plate is the primary shaft of the baleen lamina visible from the lateral side when the mouth is open. That portion of the main baleen plate that is exposed is roughly triangular in outline. It has a base that is embedded in the gum. Baleen bristles extend from its inner, lingual border.

The minor baleen plate is a secondary shaft of the baleen lamina that often is found medial to the main baleen plate. Its exposed portion is roughly quadrangular in outline. Its base is embedded in the gum. Baleen bristles extend from its distal border. By definition, the transverse width of a minor baleen plate measured at the gum line must equal or exceed 3 times its maximal thickness. More than 1 minor baleen plate may occur in a single baleen lamina.

The baleen hair is a baleen platelet sometimes found to the medial side of minor baleen plates. The exposed portion of this component of the baleen lamina is quadrangular in outline. Its base is embedded in the gum, and baleen bristles extend from its distal border. By definition, the maximal transverse width of a baleen hair is less than 3 times its maximal thickness measured at the gum. More than 1 baleen hair may occur in a single baleen lamina.

Baleen bristles are structures that extend from the distal borders of baleen hairs, minor baleen plates, and the medial border of each main baleen plate. They are commonly called baleen fringe (e.g., Sekiguchi et al. 1992). Bristles from adjacent baleen laminae form a mat over the internal surface of each side of baleen and establish the porous filter used in feeding.

A rack or side of baleen consists of all the baleen laminae from either the right or left side of the mouth still embedded in the gum.

The gum or gingiva is a predominantly epithelial structure that surrounds the bases of the baleen laminae, holding them in a regular position with respect to each other.

Morphometry of the baleen laminae followed the scheme proposed by Williamson (1973) for standardized measurement of baleen. In applying this method, however, we found it impossible to obtain reliable results for his proposed curvilinear measures. This was because of the need for continuous adjustment of the angle of measuring tapes over long distances on a slippery specimen. For this reason the measures Williamson (1973) proposed for the curved length of a baleen lamina along its inner edge, and for the curved median length of a main baleen plate, were not taken.

A more detailed set of measurements were made on the longest baleen lamina taken from the 15.7-m female. This lamina was taped to a flat surface alongside a fixed reference line. By using a framing square and a measuring tape, the outline of the lamina was established with point samplings at 20-cm intervals. The resultant data were used to reestablish the outline of the lamina for a scale anatomical drawing (Fig. 1).

Determination of the shape of the baleen apparatus.—We employed close range photogrammetry to determine precisely the shape of the left rack of baleen from the 7.8-m female. For this, the rack was excised from the skull with its baleen plates still embedded in their supporting gingival epithelium. Stereophotography in 70-mm format was performed after positioning the rack of baleen on a wooden platform with the tips of the main baleen plates oriented vertically. Twin Hasselblad cameras (Hasselblad USA, Inc., Fairfield, New Jersey) fitted with 40-mm Zeiss Distagon photogrammetric lenses and dual electronic shutter controls were used. Two range poles set vertically between the specimen and the photographic apparatus established an arbitrary datum for determination of rack shape. Stereoplotting utilized a Kern Swiss DSR 11 stereoplotter (Leica Geosystems A. G., Heerbrugg, St. Gallen, Switzerland) interfaced with an IBM PC-AT 286 operating and data storage system (IBM Corporation, White Plains, New York). Spot elevations were collected at about 10-cm intervals across the surface of the specimen as viewed in the stereoplotter. The data captured were used to develop a contour map of the external surface of the rack by using standard mapping methods (Wolf and Dewitt 2000). Elevations shown in this contour map reflect distances measured between the datum and the surface of the baleen rack.

For completeness, a contour map of the internal surface of the left baleen rack of the 7.8-m female also was generated photogrammetri-cally. The same method used to develop the external contour map was employed, with an arbitrary datum established by range poles set between the specimen and photographic apparatus. This 2nd datum was approximately, but not necessarily exactly, parallel to that used to determine the external contour, but placed on the lingual side of the baleen rack. The resultant elevations reflect distances measured between this 2nd datum and the inner surface of the rack.

Appendix I gives a microphotometric description of the baleen bristles of the baleen rack of the 7.8-m female. Baleen bristles were collected from every 50th plate, numbering in the rostral to caudal direction. To minimize breakage, the bristles collected were taped to a flat sheet of cardboard after being cut from the plate's edge. In particular, bristle samples were cut from a 1-cm-long section at 3 different locations along the inner or lingual border of the main plate, per the protocol of Williamson (1973). One-centimeter sections were taken from the dorsal extreme of the inside plate edge (proximal bristles), halfway to the plate tip (mesial bristles), and at the tip of the plate (distal bristles). Bristle diameters were measured with a Nikon Labophot microscope equipped with the Bioquant Morphometry Package (R&M Biometrics Co., Nashville, Tennessee) calibrated to a stage micrometer. Bristle lengths were measured with a machinist's rule.

Results and Discussion

Anatomy of the tongue.—Tarpley (1985) gives information on the structure of the tongue of the bowhead based on brief inspections of this organ in situ and more detailed histological studies. Tarpley (1985) concurs with the view of Eschricht and Rheinhardt (1866) that the tongue of this species is a large muscular organ whose height exceeds its width and whose margins become sharply defined toward the apex. We examined the tongue of the 8.2-m female both inside the mouth and after it had been removed by Inupiat whale hunters (Fig. 2). It was evident that a significant portion of the floor of the mouth consisted of a nonlingual intermandibular lining homologous to that previously described in balaenopterids (Lambertsen 1983). The tongue proper was freely moveable at its tip, or apex, where it was defined by a horizontal sulcus. Posterior to the apex this sulcus gradually decreased in depth and ultimately disappeared. The tongue curved sharply downward at the back of the mouth, forming a distinct postlingual recess in front of the esophagus. A less prominent feature was a broad but shallow longitudinal indentation on its dorsal midline (Fig. 2). This central lingual furrow, not as distinct or as deep as in rorquals, was outlined by a thick, rough-surfaced mucosa; it disappeared at the apex as the mucosal specialization converged at the midline. The very tip of the tongue was deeply pigmented, as if exposed repeatedly to sunlight during feeding. Lacking opportunities for more extensive investigation, it is here assumed that these are general features. The existence of a well-developed tongue in balaenids is widely known (J. C. George, pers. comm.; M. J. Moore, pers. comm.; Eschricht and Rheinhardt 1866; Slijper 1962).

Fig. 2

Front view of tongue and nonlingual intermandibular lining of an 8.2-m female bowhead whale after removal from mouth. An indentation, or central furrow, occurs in dorsal midline of organ. To either side of this central furrow is an area of thickened and roughened mucosa.

In comparison, it has been claimed that in balaenopterids (rorquals) the tongue disappears during fetal development (Pivorunas 1979). However, this is an exaggeration. In adult rorquals, there is a distinct but poorly muscled, flaccid tongue. This organ contributes in an important way to the remarkable engulfment feeding mechanism of that taxonomic family (Lambertsen 1983).

A schematic illustration of the tongue of a young bowhead whale inside the mouth is given in Fig. 3. During ram feeding the voluminous tongue would serve at least to deflect flow along the inner surfaces of the baleen racks. On section, the tongue also had a rich and intricate structure of muscle fascicles ramifying extensively through adipose connective tissue. These muscle fibers surrounded a fusiform central body composed of soft fat. The mobility implied by this internal structure suggests a likely role of the large tongue of balaenids in dynamically controlled flow. Passive control would be imposed by its large volume and shape. Deflection of flow by side-to-side or rotary motions might also sweep prey posteriorly, into the postlingual recess. The rich intrinsic musculature, probably in association with muscles attached to the mandibles and hyoid apparatus, would be responsible for this function.

Fig. 3

Lateral schematic of mouth of a young bowhead whale. A) Tongue. B) Lingual sulcus. C) Outline of baleen rack. D) Outline of orolabial sulcus. E) Esophagus. F) Postlingual recess. G) Position of temporomandibular articulation.

Morphometry of baleen laminae.—Figure 1 illustrates the longest baleen lamina from the 15.7-m female, identifying the standard measurements taken on every 10th baleen lamina in the young, 7.8-m female. Examination of the morphometric data demonstrates that the main baleen plates varied in length with serial location (see Table 1). This variation also is evident in data presented by Nishiwaki and Kasuya (1970) for a 6.4-m bowhead whale, and by Eschricht and Reinhardt (1866) for a 6.8-m whale. Generally, there is a rapid increase in length of the baleen plates over the course of the first 60 laminae of a side. Maximal plate lengths are reached at about the 120th lamina. Plate length is nearly constant over the course of the next 100 laminae, with slight diminution. Near the back of the mouth, beyond lamina 250, plate length decreases precipitously.

View this table:
Table 1

Measurements of baleen plates from left rack of baleen from a 7.8-m female bowhead whale. Data are presented in centimeters. Measurements of spacing between plates represent distance between extreme lateral edge of every nth baleen plate and that of next higher number measured at gingiva. AB = length of main plate measured to intersection of its labial edge with gingival; AD = length of main plate measured to intersection of its lingual edge with gingival; BE = width of main plate measured at gingival; BD = width of baleen lamina measured at gingiva. See Fig. 1 for illustration of individual measures. Tabular data given in parentheses indicate measurements taken to a line extended across a minor artifactual discontinuity in dorsal inner edge of the baleen laminae between plates 190 and 220. Blanks indicate measurements that could not be made because of absence of portions of inner edge of rack examined.

Plate numberaPlate spacingABADBEBDPlate thicknessb
111.314.52.15.60.06
100.6026.126.93.58.30.07
200.6538.538.37.010.80.12
300.7049.047.68.812.00.13
400.6557.755.210.013.80.12
500.7563.062.011.014.60.13
600.7668.767.711.615.50.14
700.7773.273.912.115.80.14
800.8176.778.212.416.20.15
900.8279.883.012.216.40.17
1000.8181.286.312.617.00.15
1100.7883.589.012.717.30.16
1200.8284.590.312.817.20.15
1300.8182.691.213.017.40.15
1400.7682.391.812.816.80.15
1500.8482.391.712.517.00.16
1600.8481.591.612.716.70.15
1700.8380.591.512.717.00.15
1800.7979.591.312.917.30.15
1900.8378.3(90.7)13.30.15
2000.8176.7(90.2)13.00.15
2100.7774.7(89.1)13.60.14
2200.7772.9(87.0)12.50.15
2300.7570.084.312.317.70.14
2400.7667.881.812.317.10.14
2500.8165.579.111.416.00.14
2600.7962.475.310.715.10.14
2700.7858.171.110.215.30.13
2800.6454.566.38.814.60.13
2900.7147.261.27.714.80.12
3000.7241.954.06.317.80.14
3100.6330.73.80.12
3200.366.40.50.08
  • a Numbered from rostral end of rack.

  • b Measured 2cm from tip of baleen plate.

Thus, even in the young, 7.8-m animal examined, the baleen apparatus presented a large functional surface over which hydrodynamic phenomena might act. The inner or filtration surface of the left baleen rack of this whale had an area of 1.75 m2, determined by interpolation of the 2-cm contour map shown in Fig. 4 (Kreiton 1990). Extrapolated with respect to the length of the main plate measured to the intersection of its lingual edge with the gingiva (Fig. 1; Table 1), the total filtration surface of the 15.7-m female would have been 10.82 m2, assuming symmetrical baleen racks of similar shape. The area of the external, hydrodynamically active surface would be approximately the same.

Fig. 4

Two-centimeter contour map of the internal surface of the left baleen rack of a 7.8-m female bowhead whale. This map was developed from stereoplotted measurements consisting of 230–250 spot elevations taken from the surface of the anatomical specimen by using close-range photogrammetric technique (Kreiton 1990).

Cross-sectional shape of main baleen plates.—The cross-sectional shape of the main baleen plates was not a subject of quantitative investigation in this study. However, we detected a striking difference in the cross-sectional shape of bowhead baleen compared with that of rorquals that could have important functional implications. In particular, the lateral edges of most plates in the rack diverge abruptly in a posterior direction. As noted by Eschricht and Reinhardt (1866), this posterior deviation is sufficiently pronounced to obscure from view the lamina of next higher number when viewed from the side, and is useful for determining the location in the rack from which a detached lamina originates. However, the actual cross-sectional shape of a plate is complex. A plate varies in the degree of posterior curvature along the length of the baleen plate (compare sections Z and Z′ in Fig. 1). In all the whales examined, the posterior curvature of the lateral edge of the main baleen plates was most pronounced in the longest of the laterally convex baleen plates found in the anterior one-half of the baleen rack.

Functionally, the cross-sectional shape noted appears at least to establish a means by which the very long baleen plates typical of bowhead whales can be maintained in regular alignment during feeding. This would be critical for maintenance of the integrity of the baleen filter, and is consistent with the observation that longer baleen plates had a more pronounced posterior deviation of their lateral edges. Possibly of equal importance, the same configuration might generate a Venturi effect as water flows along the outside of the baleen rack, such that water is drawn out of the mouth at greater rates than if the plates were flat. Fluid dynamical studies aimed at measuring this effect consequently would appear warranted, and may be pivotal to understanding feeding function in balaenids. The variation in cross-sectional shape noted probably also enhances plate stiffness.

Contour of the external surface of the baleen rack.—The external surface of the baleen rack is of special interest not only because of its exposure to the water flow associated with ram feeding but because of its readily predictable influence on that flow. The external surface is moderately complex (see Fig. 5) and is distinct from that seen in balaenopterids. Over most of the anterior one-half of its external surface, the rack is strongly convex. The grade of convexity is obliquely oriented toward its distal front extremity. Maximal elevation relative to the datum employed occurs at the proximal border of the rack, approximately halfway between its rostral and caudal ends. The changing elevation evident proximally reflects in part the changing width of individual baleen laminae (see the width of baleen lamina measured at the gingiva [BD] in Table 1). In contrast, in the rorqual species examined thus far (Balaenoptera physalus, B. borealis, B. acutorostrata, and Megaptera novaeangliaeLambertsen 1983; Lambertsen et al. 1995), all main baleen plates have been laterally concave.

Fig. 5

Two-centimeter contour map of external surface of left baleen rack of a 7.8-m female bowhead whale. This map was developed from stereoplotted measurements consisting of 230–250 spot elevations taken from the surface of the anatomical specimen by using close-range photogrammetric technique (Kreiton 1990).

The slight concavity evident in the caudal portion of the rack in the 7.8-m female (see Fig. 5) reflects the profile of the lateral edges of the main baleen plates in this region. In this case, the transition between the convex rostral and concave caudal portions began in the region of plate 165. Plates of serial number less than 165 all curved medially toward their tips. The outside edge of plate 165 was virtually straight. The outside edges of main baleen plates of higher number very gradually became concave, such that their tips ultimately pointed outward.

These observations indicated that the baleen rack of the bowhead whale studied should function as a hydrofoil during continuous ram feeding. Further, the evidently similar shape of the anterior portion of the baleen rack in other balaenid species (Slijper 1962; True 1904) should enable the same function. Water accelerating around the convex external surface of the anterior portion of the rack should reduce pressure outside the baleen apparatus, enhancing net filtration flow. Thus, the critical question remaining is whether the external surface of the baleen rack is extensively exposed to water flow during feeding. For this the large lower lips would need to be abducted, or rotated outward, from the baleen racks.

Cranial articulations and mandibular kinesis.—In their dissection of a fetal specimen of B. mysticetus, Eschricht and Reinhardt (1866) noted that the bowhead's temporomandibular articulation, like that of most mammals, has a dual synovial cavity. Van Beneden (1882) confirmed this observation and provided additional description of the internal fibrous disc, or meniscus, of this important joint. We dissected the tissues of the temporomandibular joint of the 8.9-m female bowhead, and also found a double synovial cavity separated by a large, platelike meniscus. This joint thus contrasted with that of balaenopterids, in which an expanded mass of fibroelastic tissue directly connects the mandibular condyle to the temporal bone (Beauregard 1882; Lambertsen et al. 1995).

Furthermore, the distal ends of the paired mandibles were not fused, reflecting the general mysticete condition (Ridgway and Harrison 1985; True 1904). The mandibles instead were joined by a fibrocartilaginous mandibular symphysis that was flexible. Thus, in the postmortem state, the bowed mandibles fell some distance away from the lateral surface of the baleen apparatus. Because of the large lower lip, this created a gutter for water flow that deviated from the whale's longitudinal axis with respect to both the midsagittal and midhorizontal planes. Moderate force provided by volunteer assistants revealed a marked ability of the lower jaw and lip to rotate outward (Fig. 6). This type of rotation also is evident in balaenopterids (Lambertsen et al. 1995). However, in balaenids the lower lip is gigantic in correlation with the prominent arch of the rostrum, creating a longitudinal gutter for water flow.

Fig. 6

Front view of mouth of a 7.5-m female bowhead whale showing the extraordinarily well-developed lower lip, the high arch of the rostrum, the convex outer surface of the anterior portion of the baleen rack, the position of the eye with the mouth partially open, and the scooplike configuration of the lower jaw. At the dorsal margin of the baleen there is a thin band of white tissue, a protrusion of the gingival epithelium. A pale crescent-shaped area on the rostrum adjacent to this tissue is the site where apposition with the lower lip and rostrum occurs when the mouth is closed. This is the specialized anatomical zone where a hydrostatic oral seal would be established as part of the normal mechanism for maintaining mouth closure during swimming. Immediately below the exposed baleen plates is a bulging mass of oral tissue that is continuous behind with the tongue (not shown). At the right of this mass is a deep crevasse, the left orolabial sulcus. The mandibular symphysis, which connects the right and left mandibles at the chin, is a flexible joint. Before photography, moderate force applied by volunteer assistants (to right) resulted in the significant outward displacement of the jaw and lip shown. During feeding, it is therefore expected that a channel for water flow along the outside of the baleen rack would be established, as illustrated in Fig. 7. Photograph reproduced with permission from Lambertsen et al. (1990).

Fig. 7

Cross-sectional reconstruction of head of a young bowhead whale showing structural relations of lower jaw, rostrum, baleen racks, and tongue at the level of baleen plate 165. Contact between tips of baleen plates and inner surface of lower jaw maintains integrity of the baleen filter. When mandibles are rotated outward with lower lips abducted, a channel for flow would be established along the external surface of the baleen rack. Acceleration of flow is expected given the convexity of the anterior portion of the baleen rack (Fig. 5). P, premaxilla; M, maxilla; C, cartilage; V, vomer; F.B., fat body; Z.O.S., zone of hydrostatic oral seal.

We surmise from these observations that when the mouth of a swimming bowhead whale is opened, the large lower lip would provide little if any obstruction to water flow out through the baleen plates. Instead, the large lower lip evidently would channel water flow along the outside of the baleen rack. A transverse section of the open mouth at plate 165 in a yearling, filter-feeding bowhead is expected to resemble that illustrated in Fig. 7. Because water flow necessarily would accelerate around the baleen racks through the channel illustrated, the Venturi effect expected from plate cross section (see above) would be enhanced.

Conclusions regarding function.—If in general bowhead whales have baleen racks similar in shape to that characterized photogrammetrically for the 7.8-m individual, the shape that is mostly evident in photographs of northern right whales (Eubalaena glacialis) given in True (1904) and Slijper (1962), and also was apparent in the 2 other bowheads here examined intact, and is thought to be typical in bowheads by field biologists with extensive experience in the Inupiat hunt (J. C. George, pers. comm.), acceleration of water flow over the anterior portion of the baleen apparatus might account for the interesting early claim that planktonic prey enters the bowhead's mouth from all directions (Fabricius 1929). Such acceleration of water flow of course would be associated hydrodynamically with a reduction in external pressure. The possible additional contribution to net filtration pressure of a Venturi effect induced by the shape of the lateral edges of the baleen laminae also has been noted. However, it is challenging to imagine that oral suction could be established as the whale moves forward, as Fabricius's direct observations seem to suggest. Fluid dynamical studies aimed at evaluating this possibility would be warranted, and related experimental research is forthcoming (A. J. Werth, pers. comm.). It may be that the shape of the bow wave of a feeding bowhead whale is dimpled in its central region just in front of the mouth as a result of the morphology of the head (including the baleen apparatus). This configuration of the bow wave might account for the intriguing motion of prey that Fabricius observed. That is, actively mobile prey might be stimulated to swim from all directions into the mouth in a countereffective evasive effort. A dimpled pressure field in front of the swimming whale would be the explanation.

Once prey-laden water enters the mouth of a bowhead, there probably is continuous concentration of a slurry of prey toward the oropharynx. In this process, prey likely would tumble continuously in a posterior direction along the inside of the baleen racks. Such tumbling is perhaps promoted by a side-to-side sweeping action of the tongue (see above). Side-to-side motions of the tongue, for example, have been filmed in feeding northern right whales (E. glacialisWerth 1990, 2001). Thus, a concentrated slurry of prey ultimately is expected to accumulate in the postlingual recess just anterior to the esophagus (Fig. 3F).

It is envisioned that elevation and retraction of the tongue would then compact the prey slurry, perhaps even resulting in reversed water flow. Water could be conveyed in a forward direction through the dorsal channel contributed by the tongue's central furrow (Figs. 1 and 2). Using this channel (which likely is employed in the neonate for conveyance of milk to the esophagus), the whale could well squirt seawater out of the front of its mouth. This would be 1 variation of a physiological mechanism to minimize consumption of salt. However, routes of water flow out the sides of the mouth may be used more commonly, because these would not require interruption of the ram-feeding process. Finally, a compacted and essentially dry mass of prey probably is pressed toward the esophageal orifice by retraction of the tongue. Thereafter, multiple boli of prey probably are formed and delivered to the stomach by esophageal peristalsis. The esophagus is richly lubricated by mucoserous glands to facilitate peristaltic action (Tarpley 1985). Oroesophageal muscles presumably would regulate the size of food boli and the frequency of their formation.

Prey that might become trapped in the baleen bristles, if any, might be removed by any of the 3 interesting possible mechanisms hypothesized by Werth (2001). However, we suspect that in balaenids few if any prey ever become trapped in the baleen bristles. They are probably swept into the postlingual recess by dynamically controlled flow. In the morphologically distinct balaenopterids, in contrast, masses of prey probably are in fact compacted against the inside of the baleen racks. This action would be driven by elevation of the tongue (probably by contraction of the mylohyoideus muscle), with its forceful spreading to either side of the well-developed, wedge-shaped vomer and hard palate that characterizes these species (Lambertsen 1983). Further, the compacted prey mass may be removed from the inner surface of the rack in cakes, with the fibrous tip of the tongue working something like a spatula; the anatomical details of the genioglossus-hyoglyossus muscle complex in rorquals support this view (Lambertsen 1983). In contrast, the process by which prey slurries are compacted in balaenids appears likely to be quite different, not the least because these species do not have a wedge-shaped vomer-palatine complex (Ridgway and Harrison 1985; True 1904). As already alluded to, the process of prey compaction in the bowhead and other balaenids probably occurs between the base of the tongue and the oropharyngeal wall.

In summary, these studies have demonstrated the capability of the lower jaw and lip of the bowhead whale to rotate outward. Our photogrammetric results have also indicated the convex shape of the external surface of the anterior portion of the baleen rack. These findings, extending early photographic studies (True 1904), indicate that low hydrodynamic pressure developing along the outside surfaces of the baleen apparatus may be critical to the normal function of the mouth in members of the Balaenidae. This is interpreted as a probable adaptation to minimize the amplitude of the pressure wave that must develop in front of the swimming whale during feeding and that could prompt evasive action by actively mobile prey; the simultaneous advantage is concentration of prey slurries inside the mouth. We furthermore suggest that head and baleen rack morphology may determine advantageously the 3-dimensional shape of the pressure wave projected by the whale, such that countereffective evasive effort by prey is stimulated. This might explain the early observation that prey appear to seek out the mouth of the bowhead from all directions (Fabricius 1929).

Conservation.—Conservation implications of these findings highlight the imperfect nature of our understanding of the impact of oil spills and marine debris on mysticete species. Experimental assessment of the effects of oil on baleen function by contractors of the Minerals Management Service of the United States thus far has considered exclusively the role of hydraulic pressure in powering baleen function (Geraci 1990). This provides useful information for Balaenopteridae (rorquals, or grooved baleen whales) because of the engulfment feeding strategy of this taxonomic family, which uses hydraulic pressure to drive prey filtration. However, our present results indicate that more subtle hydrodynamic pressures may play a critical role in the function of the baleen in the seriously endangered balaenids (including the critically endangered northern right whale, E. glacialis).

For this reason, the current state of knowledge of how oil would affect the function of the mouth of right whales and bow-heads can be considered to be poor, despite considerable past research on the effects of oil on cetaceans. What can be said is that, if droplets or globules of oil behave similarly to prey once inside the mouth, efficient ingestion of this toxicant would occur. However, if the oil is of low viscosity and does not adhere to prey organisms, it might be ingested only in small quantities. With these 2 stipulations (which are of questionable validity), much oil probably would be squeezed out of the mouth during the normal process by which prey is compacted before bolus formation. But if fouling of the baleen bristles with oil significantly increases the resistance of the baleen filter, as in other mysticetes (“up to 260%”—J. R. Geraci and D. J. St. Aubin, in litt.; same finding revised [?] to “more than 100%,” by Geraci [1990:186]), there may be a precipitous adverse effect. The effect here considered most likely would be a substantial reduction in capture of larger, more actively mobile species, that is, euphausiids, with possible reductions in capture of copepods and other prey. This follows from the aberrant increase expected in the amplitude of the bow wave projected by the whale.

Important related questions, therefore, are how fast oil would depurate from the baleen to the environment at the near-zero ambient temperatures characterizing the bowhead's habitat, and whether normal function would be restored. Surprisingly, no study has looked at these processes at temperatures close to being realistic, or with baleen samples taken from any balaenid species. Moreover, this shortcoming persists despite the fact that measurements of the pathological effect of oil on resistance to flow through the baleen of several mysticetes, as noted by Geraci (1990), do indicate greater adverse impacts at lower temperatures. Given this temperature dependence, and the extremely fine character of the baleen bristles of balaenids (Sekiguchi et al. 1992; Appendix I), baleen fouling thus remains a major conservation concern despite Geraci's premature—and possibly invalid—argument to the contrary (Geraci 1990:188). That argument notably is based principally on depuration experiments on samples of oil-fouled baleen from balaenopterid and eschrichtiid species at relatively high temperatures (these temperatures went unspecified in all supporting text, tables, and figures in the work of Geraci [1990], which was widely disseminated; but see relevant data included in table 6.6 and figure 6.4 of his unpublished 1985 contract report [J. R. Geraci and D. J. St. Aubin, in litt.]).

Moreover, Geraci's analysis of the “physiologic” effects of oil on Cetacea considered baleen function to be powered solely by hydraulic pressure (Geraci 1990; see also J. R. Geraci and D. J. St. Aubin, in litt.). However, examination of our photo-grammetric data (Fig. 5) and the results of 1 simple functional experiment (Fig. 6) indicate that this is a gross oversimplification of the relevant physiology.

Marine debris caught in the baleen racks, by interfering with a hydrostatic oral seal, might present greater probability of lethal consequence than oil pollution. This is because in all baleen whales, a hydrostatic oral seal is likely critical for carriage of the massive lower jaw during normal swimming without large expenditure of energy by the muscles that elevate the mandibles (Lambertsen and Hintz 2004). A hydrostatic oral seal allows the development of a negative pressure inside the mouth relative to ambient such that the mouth can be held closed by suction. The anatomical zone of this seal is clearly evident on the rostrum of the bowhead whale shown in Fig. 6, and is labeled Z.O.S. in Fig. 7. Permanent breaching of the seal by nonbiodegradable debris can be expected to lead to impaired swimming performance, depletion of energy reserves, reproductive failure, and death. Therefore, when debris such as rope is observed to be fouling the mouth of a northern right whale (as reviewed by Caswell et al. [1999], 70% of northern right whales show evidence of some form of entanglement), efforts to remove the debris should be strongly encouraged. Funding of the specialized technical capability needed to do so should be given highest priority in the whale conservation programs of both Canada and the United States.

In fact, recalcitrant debris in the marine environment may be a major contributor in the declining survival probability of the northern right whale empirically resolved by Caswell et al. (1999; see also Moore et al., in press). This is because as continuous ram feeders (Sanderson and Wassersug 1993), right whales face a higher risk than rorquals of encountering various forms of marine debris with their mouths open. Advanced efforts to alert the Congress of the United States to this threat to the northern right whale have been successful (E. Buck, pers. comm.; Buck 2000). Whether this will have any effect on the survivorship of right whales remains to be seen, however. The enormous magnitude of the marine debris problem is suggested by 1 study of 32 sperm whales (Physeter macrocephalus) caught in the Denmark Strait, a remote area between Iceland and Greenland (Lambertsen 1990, 1997). Twelve (37.5%) of these whales, a species that feeds by suction at or near the bottom (Lockyer 1997), contained in their stomachs some form of plastic or metallic debris. Nonbiodegradable debris that either floats on the surface or is suspended in the water poses the greatest threat to mysticetes, including the northern right whale.

Fishing gear of various sorts of course poses an identical problem. Therefore, research and regulations designed to diminish the probability of fishing gear entanglement in critically endangered balaenids should be strongly encouraged, and afforded highest funding priority.

Acknowledgments

Our efforts in the field were greatly aided by T. F. Albert, C. Brower, J. C. George, and M. Philo, Department of Wildlife Management, North Slope Borough, Barrow, Alaska; and L. Banish, National Zoological Park, Washington, D.C. The authors extend their sincere thanks to A. Brower, Sr., A. Brower, Jr., and G. N. Ahmaogak, Sr., of Barrow, Alaska, for access to anatomical samples; C. Moor, Howling-bird Studios, Falmouth, Massachusetts, for her skillful renditions of our pencil drawings; A. Hirons, University of Florida, Gainesville, for her quality laboratory assistance; Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts, for library privileges; C. Potter, United States National Museum of Natural History, Washington, D.C, for bibliographic assistance; and M. Peterson, University of Copenhagen Museum of Zoology, Copenhagen, Denmark, both for translation of relevant parts of Fabricius's Fauna Groenlandica, and for bringing this important reference to our attention. A. Dubois, J. B. Pierce Foundation Laboratory, Yale University, New Haven, Connecticut, and B. Leadon, College of Engineering, University of Florida, Gainesville, provided valuable discussion concerning fluid dynamics. J. C. George, M. J. Moore, and 1 additional (but anonymous) reviewer kindly read and commented on the manuscript. We thank especially the Alaska Eskimo Whaling Commission and the Barrow Whaling Captain's Association for their cooperation and support of our work. This research was funded under contract with the Department of Wildlife Management, North Slope Borough, Alaska. Given an advanced report of the findings of this study, employees of the United States Minerals Management Service requested advice on how to improve knowledge of the effects of oil on baleen whales. This contribution is a formal response.

Appendix I

View this table:

Morphometries of baleen bristles on baleen plates of 7.8-m female bowhead whale. Values are given as mean ± SD(except for number of bristles).

Plate numbera
Position on plate550100150200250300Mean
Proximal
Number of bristles1928398268834552
Diameter (µm)146 ± 31116 ± 48113 ± 25109 ± 24114 ± 23108 ± 26123 ± 21118 ± 28
Length (mm)29 ± 2436 ± 2647 ± 2852 ± 3049 ± 3244 ± 2331 ± 1741 ± 26
Mesial
Number of bristles2414271123263923
Diameter (µm)160 ± 66127 ± 36137 ± 58182 ± 58162 ± 55125 ± 37150 ± 50149 ± 51
Length (mm)67 ± 4270 ± 5276 ± 6599 ± 53112 ± 5583 ± 5136 ± 2578 ± 49
Distal
Number of bristles3513416716714815349122
Diameter (µm)210 ± 48181 ± 59170 ± 45171 ± 49171 ± 47193 ± 58229 ± 65189 ± 53
Length (mm)65 ± 2719 ± 728 ± 1418 ± 518 ± 1047 ± 1567 ± 1937 ± 14
  • a Numbered from rostral end, left baleen rack.

Footnotes

  • Associate Editor was Eric A. Rickart.

Literature Cited

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