Information is scarce on gray whale (Eschrichtius robustus) anatomy and that of mysticetes in general. Dissection of the head of a neonatal gray whale revealed novel anatomical details of the eye, blowhole, incisive papilla with associated nasopalatine ducts, sensory hairs, and throat grooves. Compared to a similar sized right whale calf, the gray whale eyeball is nearly twice as long. The nasal cartilages of the gray whale, located between the blowholes, differ from the bowhead in having accessory cartilages. A small, fleshy incisive papilla bordered by two blind nasopalatine pits near the palate's rostral tip, previously undescribed in gray whales, may be associated with the vomeronasal organ, although histological evidence is needed for definitive identification. Less well known among mysticetes are the numerous elongated, stiff sensory hairs (vibrissae) observed on the gray whale rostrum from the ventral tip to the blowhole and on the mandible. These hairs are concentrated on the chin, and those on the lower jaw are arranged in a V-shaped pattern. We confirm the presence of two primary, anteriorly converging throat grooves, confined to the throat region similar to those of ziphiid and physeteroid odontocetes. A third, shorter groove occurs lateral to the left primary groove. The throat grooves in the gray whale have been implicated in gular expansion during suction feeding. Anat Rec, 298:648–659, 2015. © 2014 Wiley Periodicals, Inc.

INTRODUCTION

In this report, we provide observations based on dissection, scanning electron microscopy (SEM), and histology (light microscopy) of the head of a neonatal gray whale (Eschrichtius robustus). For most anatomical regions, very little has been published for the gray whale or for most mysticetes in general. A noteworthy exception is a detailed account of the natural history, external morphology, and skeletal anatomy of the gray whale provided by Andrews (1914). Although this study did not include observations on myology, dissection of a stranded young male gray whale provided an opportunity to examine some poorly known or undescribed anatomical features, especially those relevant to understanding the evolution and specialized suction feeding strategy of the gray whale (Johnston et al., 2010). The objectives of our study were to investigate the external morphology of the eye, blowholes, sensory hairs (vibrissae), incisive papilla with associated nasopalatine ducts, and throat grooves. Our observations are compared with information about the external anatomy of other mysticetes as well as odontocetes and other mammals. Results indicate some novel anatomical detail, as well as confirmation of previous observations.

MATERIALS AND METHODS

The specimen examined in this study was the head of a neonate female gray whale (Eschrichtius robustus) SDNHM 25307 obtained from a live stranding in Moss Landing, Monterey County, California. The specimen was collected and transported to San Diego, kept frozen at the San Diego Natural History Museum (SDNHM), and later dissected at San Diego State University (SDSU) in San Diego, California in 2012 and 2013 (for more details see Introduction to Thematic papers). Relevant structures were photographed to provide a permanent record. Regions of the rostrum containing sensory hairs, as well as transverse sections through the ventral throat grooves, were histologically sampled and examined using a light microscope. Plugs of integument containing hairs were dissected from around the rostral tip and kept frozen until histological preparation. Unfortunately, the base of the hair follicle was not included during sampling and thus was not visible in the histological slices. Tissue sampled for histological examination of throat grooves was separated at the fascia, dividing the hypodermis from the underlying superficial muscle layers. Thus, neither the muscle nor the fascia immediately superficial to the muscle was included within the histological slices. Samples were taken from the left main groove and the ridge between the left main groove and the lateral, accessory groove. Artifacts from tissue preservation (freezing) include some damage to the fine structures of the sample such as separation of the tissue layers. As such, some measurements are given as approximations. The tissues were fixed in 10% formalin, paraffin embedded, and sectioned at standard light microscope thickness (10–20 μm). Integumentary samples were stained with hematoxylin and eosin for general observations and Verhoeff-Van Geison stain to test for the presence of elastic fibers. Images were taken using a Nikon Microphot camera mounted on a light microscope. Scanning electron micrographs of sensory hairs were prepared and examined by Daniel Silva at the Electron Microscope Facility at SDSU. Samples were first dehydrated using a critical point dryer and then carbon coated using an EMS 150T ES hi res coater before being imaged with an FEI Quanta 450 SEM.

RESULTS

Eye

The eyeballs in SDNHM 25307 were positioned laterally and external to the bony orbit (Fig. 1A,B). The anterior edge of the orbit was located at a curvilinear distance of 67 cm from the tip of rostrum. The orbicularis oculi with its distinctive circular fibers was well developed and located within the connective tissue of the eyelids (Fig. 1A). Also visible were several extraocular muscles. Dorsal and ventral palpebrae (eyelids) surrounded the eye (Fig. 1A,C). There were slightly discolored (light) streaks on the ventral palpebrae of both eyes, and a bit of discoloration around the eye. Margins of each eyelid possessed two antero-posterior oriented furrows (Fig. 1C). A small nerve (a branch of CN III occulomotor nerve) extended ventral to the eyeball and led to the inferior oblique muscle. Neither eyeball was perfectly spherical, but rather each were longer rostrocaudally than in any other dimension (Table 1). The eyeballs were removed for histological analysis by other investigators.

Details are in the caption following the image — **Figure 1**
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Superficial morphology of the left eye of *Eschrichtius robustus* (SDNHM 25307). (A) Entire orbital area in dorsolateral view. (B) Specimen in dorsolateral view. (C) Close up of specimen in lateral view.

Table 1. Eye measurements (mm) for similar sized mysticete species

	Eschrichtius robustus SDNHM 25307
	Right	Left	Eubalaena australis Buono et al. 2012	Megaptera novaeangliae Rodrigues et al. 2014
Eyeball length	50	60	25	69
Eyeball width	40	38		45
Eyeball height	49	45	44	6.4
Palebral aperture length	64	19	–	–
Palebral fissure length	90	80	–	–
Cornea width	24	17	–	–
Cornea height	23	18	–	–

E. robustus: body length = 395 cm; Eu. australis body length= 410 cm.

Blowholes

The paired blowholes (external nares) of SDNHM 25307 were developed as two elongate and narrow slit-like openings that converge anteriorly (Fig. 2A; Table 2). The slits were not linear in dorsal view but instead were laterally concave with the posterior limbs oriented anteromedially, and the anterior limbs oriented parasagittally. The blowholes are separated by two folds with a shallow median groove along the midline (Fig. 2A). Through an incision made within the median groove between the external nares, we observed that the nasal cartilages were surrounded by muscle medially (Fig. 2B). A fleshy muscle (anteroexternus?) originating from each premaxillary eminence extended dorsomedially to attach to the posterior and lateral walls of the nasal cartilages. The muscle fibers were oriented dorsomedially and organized in layered sheets.

Table 2. Blowhole measurements (cm) for the neonate gray whale (SDNHM 25307)


Anterior distance between slits	3.0	–	–	–	–
Posterior distance between slits	7.0	–	–	–	–
Median groove length	7.05	–	–	–	–
Left external naris—straight length	7.6	–	–	–	–
Length of posterior arm	5.0	–	–	–	–
Length of anterior arm	2.5	–	–	–	–
Right external naris—straight length	7.0	–	–	–	–
Length of posterior arm	4.0	–	–	–	–
Length of anterior arm	3.0	–	–	–	–

In general, the nasal cartilages were held in place anteriorly by a fibrous raphe connecting to a dorsal keel of the mesorostral cartilage and posteriorly by the robust blowhole ligament (Fig. 2B,C). The blowhole ligament measured 75 mm in anteroposterior length from the anterior edge of the nasal cartilages to the anterior apex of the paired nasal bones at the midline. The posterior extension between the cartilages and nasal bones is cord-like, with a diameter of at least 4.5 mm, although it may be larger. Anterior to the nasal cartilages, the ligament extends at least 41 mm and fans out transversely for approximately 33 mm.

The nasal cartilages were 10 mm long (anteroposterior), and the nasal passages were approximately 40 mm deep. The dorsal profile of the nasal cartilages was not level but rather flared dorsally (Fig. 2C). The dorsal edge of the medial side of the nasal cartilage rose dorsally to within 10 mm of the external surface in the blowhole area. The main nasal cartilage, at a depth of 60 mm below the surface, descended from the midline in a curvilinear arc parallel to the posterior margin of the narial passage. At its anterodorsal termination, the cartilage contacted the nasal ligament. The cartilages were anteriorly concave in dorsal view. The main cartilage continued dorsally to the surface, and it joined anteriorly with isolated blocks of accessory cartilages. The main cartilage is 4–6 mm thick moving mediolaterally. The posterolateral cartilage formed an arc that was 35 mm in diameter and 3 mm thick. The curvilinear length of the cartilage was 80 mm.

The fleshy nasal plugs were composed of papillary tissue on the anterior and lateral walls of the external nares (Fig. 2D). Sand grains were found in the nasal passage, although it is not clear whether this occurred pre- or postmortem.

Incisive Papilla and Nasopalatine Ducts

A small, fleshy protuberance that we identify as an incisive papilla was located near the rostral tip of the palate of SDNHM 25307 (Fig. 3A). Occurrence of incisive papillae are previously undescribed in gray whales. Two small, slit-like openings leading to blind incisive or nasopalatine ducts (14–15 mm in depth) were identified on either side of the incisive papilla (11 mm deep dorsoventrally; Fig. 3B). The papilla consisted of four tissue layers, each of which was approximately 1 mm in depth, with the exception of the body of the papilla. The innermost layer was comprised of a fleshy red papilla, followed by a thin lighter colored layer, separated from the external epidermis by a thinner red ribbon of tissue (Fig. 3C).

Sensory Hairs (Vibrissae)

Many elongated, stiff hairs were observed on the rostrum and lower jaw of SDNHM 25307 (Figs. 4 and 5A,B). The location of each hair on the rostrum and lateral side of the mandible was marked by a broad roughly circular depression in the epidermis that gave the skin a somewhat dimpled surface texture (Fig. 5C). The hairs on the rostrum were arranged in irregular rows along the either side of the midline from the anterior tip to the blowholes (Fig. 4A,B). A different arrangement occurred on the lateral surface of the rostrum in which a more diffuse series of hairs (27 hairs on the left side) spread over the rostrum from near the midline almost to the upper lip (Figs. 4B and 5A). The tip of the rostrum contained a concentration of approximately 20 hairs (Fig. 4A,C). The vibrissae pattern on the lower jaws was more regular and consisted of two, anteriorly converging linear rows of hairs (Figs. 4B and 5A). On the left mandible the upper row was approximately 34 cm long and contained nine hairs in a line that roughly paralleled the lower lip approximately 8 cm below the dorsal margin (Fig. 5A). The lower row was approximately 32 cm long and contained seven hairs. The caudal terminus of this row was placed 13 cm below the caudal end of the upper row, while the anterior end was coincident with the anterior end of the upper row. The vibrissae pattern in symphyseal region of the lower jaws contained more than 30 hairs (Figs. 4C and 5B) arranged in a vertically oriented row on either side of the midline. Several hairs were found emerging from the ventral surface of the tip of the rostrum (Figs. 4C and 5A,B). Each hair on the rostrum and lower jaws was rooted deep within the hypodermis and emerged from a circular pit (Fig. 5C) averaging approximately 5 mm in diameter. A scanning electron photomicrograph of the vibrissal shaft of a rostral hair reveals that the surface is smooth with straight edges and the shaft is circular in cross-section (Fig. 5D-F).

The general thickness of the integumentary layers was similar to that seen in other regions of the skin (e.g., the ridges between throat grooves as discussed below). The specialized hair follicle is a double–walled structure that contains blood sinuses between inner and outer connective tissue sheaths (Fig. 6A). The entire follicle measured 1.7 mm in diameter including the capsule, while the hair shaft was approximately 0.2 mm in diameter. The capsule was composed of stratified squamous epidermal tissue surrounded externally by reticulated dermal connective tissue, which extended deep to the general dermal–hypodermal layer division (Fig. 6A). Sebaceous glands, previously reported as absent in cetaceans (Ling, 1974), and a capsular muscle were not found associated with the hairs, though in the case of the capsular muscle, this was likely due to an insufficiently deep sampling of the hair follicle. The sinus separated from the shaft and outer sheath of the hair during the histological preparation (Fig. 6A).

The tissue around the sensory hairs on the rostrum was highly innervated, in comparison to the throat groove integumentary tissue (discussed below), with nerves present from the reticulated dermis through the hypodermis. Along with high degrees of innervation, there also seemed to be several lamellated sensory corpuscles in the sinus (Fig. 6B-D). Given their size and structure, the corpuscles were likely Herbst's corpuscles as observed by Nakai and Shida (1948) in the sei whale, Balaenoptera borealis (de Bakker et al., 1997).

Throat Grooves

We confirm the presence of two primary, anteriorly converging throat grooves, confined to the throat region and terminating at about the level of the orbit. A third, shorter groove occurred lateral to the left primary groove (Fig. 7A). Both primary grooves commenced approximately 22 cm behind the tip of the lower jaw, while the accessory groove began approximately 49 cm behind the tip. The right primary groove measured 49 cm in length, the left primary groove measured 53 cm in length, and the accessory groove measured 15 cm in length. The maximum depth of the right groove was 26 mm, the left groove 31 mm deep, and the accessory groove 24 mm deep. The curvilinear distance from the highest point on the right lower lip to the middle of the right primary groove was 42 cm, to the left primary groove 53 cm, and to the accessory groove is 58.6 cm (Table 3).

Table 3. Throat groove measurements (cm) among neonate gray whales

Measurements	SDNHM 25307	LACM 95548
Body length	395	517	435
Right throat groove	49	64	59 (longest)
Left throat groove	53	62	–
Left second groove	15	9	–
Depth	∼3	2–3	–
Distance apart anteriorly	–	–	6
Distance apart posteriorly	–	–	16

Measurement data for LACM 95548 taken from Johnston et al. (2010).

A transverse section through the ventral throat tissues revealed that the throat grooves are composed of layers of epidermis and fatty blubber (Fig. 7B). In general, the tissue layers are thicker in the ridges than within the bases of the grooves. The epidermis, from the surface of the stratum corneum to the base of the epidermal rete, measures approximately 4.0 mm in the groove and 7.2 mm on the ridges with the dermal papillae infiltrating the epidermis up to the border between the stratum corneum and stratum spinosum (Fig. 7C-E). These dermal papillae appear to infiltrate deep into the epidermis, but this is more likely a function of the thickness of the stratum spinosum, the strata where these structures are known to persist. The stratum corneum was approximately 0.9 mm thick on the ridges, but only 0.6 mm in the groove. The stratum spinosum was approximately 6.1 mm and 3.3 mm, respectively. The stratum basale is also present (Fig. 7D). As noted in other mysticetes (Haldiman and Tarpley, 1993), the cells of the stratum corneum in SDNHM 25307 are nucleated (Fig. 7E), unlike those found in terrestrial mammals (Spearman, 1972). As observed by Haldiman and Tarpley (1993) in the bowhead Balaena mysticetus, the stratum granulosum was absent.

The papillary dermis makes up the dermal papillae and ends directly after the termination of the epidermal rete. The reticular dermis was approximately 0.9 mm in the groove and 1.7 mm in the ridges. Elastic fibers were observed within the reticular dermis and some penetrated the dermal papillae (Fig. 7F). The hypodermis was 27 mm and 49 mm thick, respectively. Blood vessels were observed from the hypodermis to the dermal papillae. There was significantly less innervation of the throat region in comparison to the integument surrounding the sensory hairs on the rostrum (Figs. 6B and 7C). On the rostrum, the presence of nerves greatly outnumbered the presence of blood vessels, but the opposite was true for the throat tissue. There was no clear organization or directionality to the collagen fibers in the dermis and hypodermis, but the hypodermis had approximately equal concentrations of collagen and adipose tissue (Fig. 7C).

DISCUSSION

Although there is a growing literature on the ecology, behavior and conservation of extant mysticetes (e.g. Mann et al., 2000; Estes et al., 2006), detailed studies of the soft and hard tissue anatomy of these animals, are, for the most part, lacking. By comparing the observations and measurements described above with the limited published data that is available for other cetaceans, we can lay the foundation for future studies exploring the evolution of sensory physiology and feeding behaviors in gray whales in particular and mysticetes in general.

Most studies on the morphology of the eye and vision in cetaceans focus on odontocetes (reviewed in Kröger and Katzir, 2008). The anatomy of the eye and the eye muscles of mysticetes are lesser known. Previous studies included descriptions for adults and a fetus of the bowhead (Zhu et al., 2000, 2001) and for adults and calves of the southern right whale, Eubalaena australis (Buono et al., 2012). Several studies have described the eye anatomy of the minke whale, Balaenoptera acutorostrata (Vasilyevskaya, 1988; Murayama et al., 1992) and the fin whale, Balaenoptera physalus (Pilleri and Wandeler, 1964). Cursory observations of the gray whale eye were previously reported (Andrews, 1914) as were results of a more detailed investigation of the ocular anatomy and visual capabilities in this species (Mass and Supin, 2007).

Some features of the eyes of SDNHM 25307 are similar to what has been described for other taxa. For example, the eyeballs of the gray whale are situated lateral and external to the bony orbit, which has been observed in another mysticete (Eubalaena glacialis (Buono et al., 2012). However, in a humpback (Megaptera novaeangliae) the eyeball is reportedly located within the orbit (Rodrigues et al., 2014). Compared to a similar sized right whale calf, the gray whale eyeball is nearly twice as long (Table 1). Similar to studies of the eye morphology of the southern right whale (Buono et al., 2012). The bowhead (Zhu et al., 2001) and the humpback (Rodrigues et al., 2014) and irrespective of ontogenetic age, the gray whale eyeball is shorter mediolaterally (width) than in either dorsoventral (height) or rostro-caudal (length) directions (Table 1). Unfortunately, anatomy of internal ocular structures and histological samples of the retina were unavailable for comparative purposes and determination of visual acuity of Eschrichtius. However, the results of previous studies indicate that the retina of mysticetes and odontocetes are similar (Kröger and Katzir, 2008), and the retinas of the gray whale and odontocetes apparently lack most types of cone pigments (Reuter and Peichl, 2008). Broad comparisons of retinal microstructure are needed to fully assess the range of visual physiology among mysticetes and cetaceans in general.

The anatomy of the external nares or blowhole is better known in odontocetes (e.g., Heyning, 1989) than in mysticetes. For mysticetes, brief observations of the external morphology and muscles of the blowholes were provided for the sei whale (Schulte, 1916), minke whale (Carte and Macalister, 1868) and the gray whale (Andrews, 1914). Only the blowholes of the bowhead whale have been previously described in some detail (Haldiman and Tarpley, 1993). In general, the anatomy of the blowholes and nasal cartilages of SDNHM 25307 are similar to that described for other mysticetes, although the orientation of the nasal cartilages in dorsal view in SDNHM 25307 differed when compared with a neonate fin whale (SDSU S-970). The nasal cartilages were posteriorly oriented in the fin whale rather than anteriorly oriented as in the gray whale. This same posterior orientation was described and illustrated in the minke whale by Carte and Macalister (1868, Pl 7 Fig. 3). Additionally, nasal cartilages in the bowhead were not reported to possess the accessory cartilages seen in the gray whale. The function (and ultimate taxonomic distribution among mysticetes) of accessory cartilages is unknown at this time.

Presence of the incisive papilla and nasopalatine ducts often are associated with the vomeronasal system in mammals (Døving and Trotier, 1998). In terrestrial artiodactyls, the slits on either side of the central incisive papilla lead to the nasopalatine ducts that connect the surface of the palate to the vomeronasal organ within the nasal cavity (Nickel et al., 1973; Salazar et al., 1997), which is an accessory olfactory structure found only in tetrapods. The vomeronasal system is composed of the vomeronasal (Jacobsen's) organ, vomeronasal nerve fibers, and the accessory olfactory bulb (Pihlström, 2008). It has been suggested that the vomeronasal system is specialized for detecting nonvolatile stimuli including pheromones and thus may play an important role in mammalian reproductive behavior (Pihlström, 2008).

Most previous studies of baleen and toothed whales found evidence for embryonic development of an accessory olfactory and terminalis system, but the absence of a vomeronasal organ (Buhl and Oelschläger, 1986; Oelschläger, 1989). Those anatomical observations are supported by pseudogenization within vomeronasal gene sequences of fin whales and bottlenose dolphins (Yu et al., 2010). However, the structures that we identify at the rostral end of the palate, namely the incisive papilla and nasopalatine ducts, may indicate that a vomeronasal organ is present, even if vestigial. Several studies suggest that the vomeronasal organ has other functions including an overlap with the main olfactory system (e.g., Trinh and Strom, 2003), and recently it has been suggested that the presence of olfaction among mysticetes, but not odontocetes, may facilitate filter feeding and the location of their prey (Thewissen et al., 2011). Further genetic studies demonstrate that mysticetes possess more functional olfactory receptor genes than odontocetes (Kishida et al., 2007). Although the nasopalatine ducts are developed as blind pits in SDNHM 25307, which might suggest a loss of functionality of the vomeronasal system, the ducts are developed in most ungulates (Zapico, 1999). In extant horses the ducts are developed as blind pits (Salazer et al., 1997). The Flehmen response is a behavioral mechanism to collect chemical information (Weeks et al., 2002), which indicates that sensory information is transported to the organ despite the absence of an open and direct connection. We hypothesize that the same might be possible in the gray whale if the vomeronasal organ is present.

Our observations of the incisive papilla and nasopalatine ducts follow gross morphological descriptions for terrestrial mammals (e.g., Nickel et al., 1973; Young, 1981; Chan and Byers, 1985; Evans, 1993; Asher, 1998) and even other mysticetes (e.g., Lillie, 1910; Schulte, 1916). Honigmann (1917) reported possible remnants of the vomeronasal organ (epithelial pouch, paraseptal cartilages) in baleen whales but he did not mention a vomeronasal nerve or accessory olfactory bulb. Michalev (1979) described small pits that likely are the nasopalatine ducts at the tip of the rostrum in baleen whales, and he suggested that the structures might have some sensory-related structure. However, Quay and Mitchell (1971) noted a lack of chemosensory endings in the nasopalatine ducts of the fin whale. Nasopalatine ducts have been described for several Balaenoptera species, including B. borealis (Freund, 1912; Schulte, 1916), B. musculus (Lillie, 1910), B. physalus (Lillie, 1910; Freund, 1912; Quay and Mitchell, 1971), as well as the humpback, Megaptera novaeangliae (Freund, 1912). To date, nasopalatine ducts have not been reported previously for E. robustus. Variation was noted among and within balaenopterid species, as has been observed in humans (Jacob et al., 2000). For example, Lillie (1910) reported that the nasopalatine ducts were better developed in B. musculus than B. physalus. Additionally Lillie (1910) found that the structures were not equally developed in all specimens of B. physalus, but rather that they were reduced depressions in one individual similar to those of B. musculus. Lillie (1910) reported the presence of nasopalatine ducts in both B. physalus and the blue whale, Balaenoptera musculus, with the structures better developed in B. musculus than in B. physalus. Additionally Lillie (1910) found that the structures were not equally developed in all specimens of B. physalus, but rather that they were reduced depressions in one individual similar to those of B. musculus. Schulte (1916) illustrated the incisive papilla and nasopalatine ducts in the fetus of a sei whale and he described the complex as consisting of sulci with pits on either side of a median elevated ridge. Schulte (1916) reported that the nasopalatine pits are deeper in older fetuses than in adults (see also references cited by Pihlström, 2008). This ontogenetic variation might be the same for Eschrichtius given the prominence of the structures in SDNHM 25307, although the presence or absence of the structures in adult gray whale individuals has yet to be reported.

Although the presence of the papilla and ducts may suggest the presence of the vomeronasal organ in the gray whale, those structures may be inadequate to accurately locate the position of the organ within the head (Jacob et al., 2000; Smith et al., 2001; Bhatnagar et al., 2002). Unfortunately, the histological data that are needed to accurately identify the organ (Døving and Trotier, 1998) were unavailable for the appropriate anatomical region in our study of SDNHM 25307. One area of future research is to fully explore the rostral region of the palate through deeper dissections and histological analysis in other mysticete individuals. Further investigations of the nasopalatine structures in E. robustus as well as behavioral observations are needed to confirm aspects of the presence, ontogeny and potential function of the vomeronasal system in the gray whale and additional mysticete species.

Sensory hairs or vibrissae, commonly termed whiskers, have been previously described for a number of odontocete species (references cited in Dehnhardt and Mauck, 2008). Among mysticetes, vibrissae are less well known and have been described in some detail previously only for the bowhead (Haldiman and Tarpley, 1993) and the sei whales (Nakai and Shida, 1948). These authors suggested that the hairs are of the follicle sinus type and serve an apparent tactile function. We found that the internal microanatomy of the rostral and mandibular hairs in SDNHM 25307 suggests a type of sinus hair, which in turn suggests an apparent tactile function. A tactile function for these facial hairs would aid in prey detection, especially for gray whales that are benthic feeders. However, psychophysical experiments are necessary to test such a hypothesis of a mechanosensory function.

Lillie (1910) noted and illustrated the arrangement of vibrissae on the rostrum and lower jaw of fin and blue whales. Although Lillie examined numerous specimens, it is unclear whether his sample included both adults and calves. In either case, however, the distribution pattern of facial hairs described by Lillie (1910) differs in notable respects with the pattern observed in the neonate gray whale. In the first place the number of hairs on the rostrum is greater in the gray whale than reported in balaenopterids (over 40 per side in SDNHM 25307 and approximately 17 in balaenopterids). Lillie (1910) noted that the rostral hairs were organized into two subparallel rows, one just lateral to the medial rostral ridge and another just medial to the lateral rostral margin. Our observations of the neonate gray whale found a more diffuse pattern of rostral hairs (see Fig. 4A). The mandibular hairs reported by Lillie (1910) in balaenopterids consisted of a single row of approximately five hairs running longitudinally and subparallel to the lower lip. In the neonate gray whale there are two anteriorly converging rows of mandibular hairs. On the left mandible the upper row consisted of nine hairs while the lower row consisted of only seven hairs. The pattern of facial hairs in the symyphseal region of the lower jaw, however, was similar in both the neonate gray whale and the balaenopterids reported by Lillie (1910), consisting of a bilaterally symmetrical vertical row of hairs on either side of the midline,

Schulte (1916) described the occurrence of vibrissae in the same anatomical regions on fetal specimens of the sei whale. Vibrissae have not been described in detail in gray whales, although Andrews (1914) reported more numerous hairs on the tip of rostrum and symphyseal region of the mandible than elsewhere on the head in gray whales. Our observations agree with Andrews' previous descriptions.

We identify the hair follicles as being of the sinus type, and structures such as the ring sinus and cavernous sinus, noted in the sinus hairs of pinnipeds and terrestrial mammals (Dehnhardt and Mauck 2008), were not observed because the sample was not cut deeply enough into the hypodermis. This is likely since both Nakai and Shida (1948) and Haldiman and Tarpley (1993) observed these type of structures in sei and bowhead whales, respectively. None of those authors noted sebaceous glands in their descriptions of sei or bowhead whales, which is consistent with our observations of SDNHM 25307. Thus it appears that the sinus hairs of mysticetes, and perhaps more generally cetaceans lack the sebaceous glands that are present in terrestrial mammals and pinnipeds (Dehnhardt and Mauck, 2008).

To our knowledge, the structure of cetacean vibrissae has not been described in much detail. However, macro- and microstructural morphology of facial vibrissae for other marine mammals are better known. In harbor seals and other pinnipeds, vibrissal hair shafts have an undulating surface and are flattened or oval in cross-section (Dehnhardt and Mauck, 2008). The condition in pinnipeds contrasts with our observations in SDNHM 25307 in which the vibrissae are circular with smooth and straight surfaces. In this respect, the vibrissae of the gray whale are more structurally similar to terrestrial mammals than pinnipeds (Dehnhardt and Mauck, 2008).

Throat grooves occur in several lineages of odontocetes (ziphiids and physeteroids) and mysticetes (gray whales and balaenopterids). All extant ziphiids possess at least one pair of anteriorly converging throat grooves that are located between the mandibular symphysis and the hyoid apparatus (Heyning and Mead, 1996; Heyning, 1989). Accessory throat grooves are developed in some specimens of Baird's beaked whale, Berardius bairdii (Omura et al., 1955). Throat grooves of varying number are also found in physeterids (sperm whales) and kogiids (pygmy and dwarf sperm whales; references cited in Heyning and Mead, 1989). Andrews (1914) reported that although gray whales typically possess two throat grooves confined to the gular region, three grooves are not infrequent and one specimen that he observed possessed four throat grooves. Johnston et al. (2010) reported two large throat grooves and a third, smaller accessory groove lateral to the right groove.

The throat grooves described here and previously for the gray whale differ from the more numerous and extensive ventral grooves or pleats found in balaenopterids (ranging from 14–35 in the humpback to 60–88 in the blue whale) that extend from the chin to the umbilicus (Jefferson et al., 2008). Rather, the throat grooves of the gray whale are similar to those of ziphiid odontocetes (see Heyning and Mead, 1996) and are confined to the gular region between the chin and hyoid. As in some odontocetes, the throat grooves in the gray whale have been implicated in gular expansion during suction feeding (Werth, 2000). In balaenopterids, the heavily pleated ventral groove blubbers (VGB) accommodate the extreme oral expansion of the cavum ventral that occurs during engulfment feeding (Goldbogen, 2010).

Some microstructural differences between the gray whale and rorqual throat grooves might reflect the differences in feeding behavior as well. Histological analysis of the throat grooves is scarce in the published literature, but a previous study of the histology of the ventral groove blubber of the minke whale, Balaenoptera acutorostrata is the only detailed account (de Bakker et al., 1997). In the minke whale, numerous Golgi-Mazzoni and Pacinian-type corpuscles were primarily observed within a layer of thick elastic bundles separating the blubber and underlying muscle. The section of the throat grooves sampled from SDNHM 25307 did not include the muscle layer, and therefore we were unable to locate the highly innervated elastic layer in the histological slices. Although it is possible that sampling of the gular tissue did not capture the innervated layer, we hypothesize that the layer is absent in the gray whale given the paucity of lamellated corpuscles in the throat region compared to the rostrum.

The thick corpuscular layer with elastic bundles that was observed in the minke whale throat grooves may relate to the timing of closure of the oral cavity (de Bakker et al., 1997). Because rorquals employ extreme oral expansion during feeding to a much greater extent than gray whales, increased sensitivity and elastic properties of the throat becomes a greater necessity. Increased innervation of the throat grooves might act in concert with the recently described sensory organ within the mandibular symphysis of rorquals that appears to play a role in lunge feeding (Pyenson et al., 2012). We were unable to locate the symphyseal organ in SDNHM 25307. Our results indicate that additional studies of the microstructure of gular tissues will greatly improve our understanding of the sensory and mechanical physiology of the throat during feeding in balaenopteroids. This understanding, in turn, will aid in the evolutionary reconstruction of feeding behaviors within Mysticeti as a whole.

ACKNOWLEDGEMENTS

The authors thank Daniel Silva for photographic assistance. The authors also acknowledge Melvin Clemente at Pacific Histology in San Diego for assistance in preparation of tissue slides for histological examination. Finally, we thank William Ary and Reagan Furbish for helpful comments that improved the article.

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Citing Literature

Volume298, Issue4

Special Issue:Thematic Papers: Anatomical Investigations of the California Gray Whale

April 2015

Pages 648-659

Eye, Nose, Hair, and Throat: External Anatomy of the Head of a Neonate Gray Whale (Cetacea, Mysticeti, Eschrichtiidae)

ABSTRACT

INTRODUCTION

MATERIALS AND METHODS

RESULTS