sign in sign up
<<
Home , Balaena, Bowhead whale, Sotalia, Whale, Whiskers

THE ANATOMICAL RECORD 00:00–00 (2015)

Sensory in the Bowhead , mysticetus (, Mammalia)

SUMMER E. DRAKE,1,2 SAMUEL D. CRISH,3 JOHN C. GEORGE,4 4 1 RAPHAELLA STIMMELMAYR, AND J.G.M. THEWISSEN * 1Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, Ohio 2School of Biomedical Sciences, Kent State University, Kent, Ohio 3Department of Pharmaceutical Sciences, Northeast Ohio Medical University, Rootstown, Ohio 4Department of Wildlife Management, North Slope Borough, Barrow,

ABSTRACT We studied the histology and morphometrics of the hairs of bowhead (Balaena mysticetus). These whales are hairless except for two patches of more than 300 hairs on the rostral tip of the lower lip and chin, the rostral tip of the upper lip, and a bilateral row of approximately ten hairs caudal to the . Histological data indicate that hairs in all three of these areas are vibrissae: they show an outermost connective tissue capsule, a circumferential sinus system surrounding the shaft, and dense innervation to the follicle. Morphometric data were col- lected on hair diameters, epidermal recess diameters, length, and external hair lengths. The main difference between the hairs in the different regions is that blowhole hairs have larger diameters than the hairs in the chin and rostrum regions. We speculate that the hair shaft thickness patterns in bowheads reflect functional specializations. Anat Rec, 00:000–000, 2015. VC 2015 Wiley Periodicals, Inc.

Key words: hair; vibrissa; whale; Cetacea; anatomy

The presence of hair is a defining characteristic of 2001, 2002, 2011) and nearly absent in cetaceans (Kel- . However, there are some orders that are logg, 1928; Ling, 1977, Berta et al., 2015). Hair in sire- nearly devoid of hair. In these , specialized hairs nians is found both on the face and body, with the hairs with a mechanoreceptive function are commonly promi- on the face being 30 times as dense as hairs on the rest nent. The mechanoreceptive function of hairs has been of the body (Marshall et al., 1998a, 1998b). These tactile studied extensively in subterranean mammals, including hairs serve a specialized mechanoreceptive role (Reep the nearly hairless naked mole-rat (Heterocephalus gla- et al., 2001, 2002, 2011; Dehnhardt and Mauck, 2008; bus), which utilizes approximately 40 tactile face and body hairs to assist in mechanosensory-guided orienta- tion (Crish et al., 2003). Park et al. (2003) studied the Abbreviations used: F-SC 5 follicle-sinus complex anatomy of vibrissae, guard hairs, and body hair in sev- Grant sponsor: Kent State University School of Biomedical eral , using a series of antibody stain to Science, NEOMED, the NSB-DWM, the NSB-Shell Baseline distinguish innervation differences. Crish et al. (2003) Research Program. demonstrated the importance of these hairs in naked *Correspondence to: J.G.M. Thewissen, Department of Anatomy mole-rat mechanoresponse. Rice et al. (1986, 1993, 1997) and Neurobiology, Northeast Ohio Medical University, Rootstown, studied facial vibrissae in rats in detail, identifying spe- OH 44272. E-mail: [email protected] cific functions for distinct bundles. Medium to Received 18 August 2014; Revised 4 March 2015; Accepted 4 large sized myelinated axons run to the follicle-sinus March 2015. complex (F-SC), enabling tactile sensitivity. DOI 10.1002/ar.23163 Among marine mammals, hair is abundant in pinni- Published online 00 Month 2015 in Wiley Online Library peds, but is greatly reduced in sirenians (Reep et al., (wileyonlinelibrary.com).

VC 2015 WILEY PERIODICALS, INC. 2 DRAKE ET AL.

Fig. 1. (A) Head of fetus (2007B16F) with regions hairs are implanted in a left and right arch posterior to this. Photo by with hair marked by yellow polygons. (B) Patch of adult bowhead Olga Shpak. (D) Close-up of paired blowhole postmortally, rostral to with hairs emerging from epidermal recesses. (C) Photo of living bow- left (2013B1). Arrows indicate position of all blowhole hairs, but skin head whale while at the surface swimming away from camera. Left tears are postmortem artifacts. and right blowholes are located on an elevated area of the head, and

Sarko et al., 2011) that is complementary to their other mechanoreceptive function, this function could account , and these hairs are actually used in food manip- for the high density of hairs found there (Japha, 1910). ulation (Marshall et al., 1998a,b, 2003). For aquatic Hairs on chin and rostrum are dispersed over a large mammals that live in marine or riverine environments area (Fig. 1B), and, in addition, bowheads have a single with reduced visibility, vibrissae or vibrissal crypts pro- bilateral, rostrally concave row of approximately 10 vide an important supplement to vision for sensing the hairs just caudal to the blowhole (Tomilin, 1957; Haldi- environment (Dehnhardt et al., 1999). man et al., 1981; Henry et al., 1983; Fig. 1C), the only In species where the distribution of hair is uneven species to be described that possesses hair in this posi- over the body, hairs are highest in density in locations tion. Naked molerats have rows of sensory hairs sepa- where stimulus detection is most likely, such as around rated by expanses of naked skin on the lateral side of the eyes, chin, neck, and wrists (Sarko et al., 2011). their trunk and abdomen, similar to the hair arrays of Facial hair is more common in mysticetes than in odon- bowhead whales near their blowhole (Park et al., 2003). tocetes, although the number of hairs and their spatial Bowheads have a paired blowhole, located on an ele- distribution differs greatly between different species vation called a (Eschricht and Reinhardt, 1866), (Yablokov and Klevezal, 1964). Slijper (1962) reports 50– positioned one fourth of the body length caudal to its 60 hairs on the face of (Balaenopteridae), rostral tip. The bilateral rows of hairs are located just implanted in three rows on the head. The same author caudal to the crown (Fig. 1C,D). Bowhead eyes are reports the bowhead whale (Balaena mysticetus) as the located low on the sides of their head, just above the most hairy cetacean with about 250 “bristles” on the tips temporomandibular joint (Tomilin, 1957; Fig. 1A). Tradi- of the lower and upper jaw and caudal to the blowhole tional knowledge has long understood that bow- (Fig. 1A). The chin of the bowhead whale is the most for- head whales have large blind spots, due to the eyes’ ward projecting part of its body and, if the hairs serve a lateral placement, and this has been important in SENSORY HAIRS IN THE BOWHEAD WHALE 3 approaching the whale when . This is reiterated guianensis (Dehnhardt and Mauck, 2008), the kogiid by Slijper (1962), who postulated that much of a whale’s breviceps, the platanistid Platanista gangetica surrounding environment is beyond its field of vision, (Norman and Fraser, 1948) and the iniid geoffren- including the area directly in front of, beneath, and sis (Dehnhardt and Mauck, 2008). In these species above the . (Tomilin, 1957; Sterba et al., 2000), there is a row of Although Kukenthal€ (1893) stated that mysticete hair fewerthantenhairsoneithersideoftherostrum(The- was vestigial, modern authors disagree. Nakai and wissen and Heyning, 2007), and these hairs are usually Shida (1948) postulated that whales use vibrissae lost soon postpartum (Nakai and Shida, 1948; Sokolov, as water current receptors, aiding in navigating the 1982), although there are reports on captive individuals open , and somehow in the location of food. Upon where hairs persist and may serve a mechanoreceptive viewing whales feeding, Yablokov and Klevezal (1964) function (Sylvestre, 1985). Norman and Fraser (1948) felt that vibrissae were serving as “closest range reported that the Ganges , Platanista gangetica, receptors” that are sensitive to direct contact from retains facial vibrissae throughout life. In the dolphin objects and less likely to be used in orientation. Bow- , hair follicles also remain into adulthood and head whales are skim feeders, meaning that they swim possess a sinus system (Mauck et al., 2000), and these at the water’s surface and passively allow their prey to are thought to be electroreceptors due to high tempera- filter through their baleen in a somewhat continuous ture output and innervation (Mauck et al., 2000; Wilk- manner. However, rorquals are lunge feeders and eat in ens and Hofmann, 2008; Czech-Damal et al., 2012). It discrete lunges, taking in a large amount of water and is worth noting that the , Monodon monoceros, prey at one time, then filtering large increments at a and beluga, Delphinapterus leucas, never have hairs, time (Croll et al., 2002). Due to the large amount of time even in fetuses (Slijper, 1962; Herman and Tavolga, that bowheads spend at the interface between the water 1980; Sokolov, 1982). In spite of a consistent view that and the air, it is possible that the hair caudal to the whale hairs are important in environmental detection blowhole is relaying spatial information about the envi- (Japha, 1910), documentation and analysis of precise ronmental interface, and the chin and rostral hairs could function has been weak. It is possible that the hairs be sensing the presence of prey. Herman and Tavolga could serve a role as water flow detectors. It is neces- (1980) suggested a correlation between the persistence sary for whales to surface to breathe, the blowhole of vibrissae into adulthood and the slimness and length hairs could be functioning to relay the approach of the of the snout in the different families of mysticetes, water’s surface, especially since this is an species reflecting a difference in feeding behavior. However, known to migrate under sea ice (George et al., 1989). they stopped short of speculating the mechanism for this The hairs on the chin and rostrum do not breach the association. water level, and could serve a mechanoreceptive role, Japha (1910) described ( mus- different from the blowhole hairs. The importance of culus) hairs as vibrissal due to their stiffness and pres- mechanoreception has been shown in seals and musk- ence of a sinus complex. Mercado (2014) described hairs rats, as this can supplement or substitute for implanted on the tubercles on the other senses (Dehnhardt et al., 1998; Dehnhardt and (Megaptera novaeangliae) head and proposed a sensory Mauck, 2008). function for these, and Berta et al (2015) assumed the Purves (1967) speculated that mysticetes may possess same for gray whales (Eschrichtius robustus). Haldiman the ability to smell the wind in search of . This et al. (1986) discussed the hairs in the bowhead and hypothesis assumes new importance in light of the identified them as vibrissae based on the increased hair recent finding that the sense of olfaction of bowheads is follicle diameter and the presence of and blood better developed than in most other cetaceans (Thewis- sinuses within the wall of the follicle, however, they did sen et al., 2011), which has long been part of traditional not describe these observations with figures or quantita- Eskimo knowledge. It is suggested that bowheads may tively. Haldiman and Tarpley (1993) speculated that the detect clouds of by the specific airborne odor of hairs are tactile, due to the presence of innervated sen- dimethyl sulfide that is released when krill feeds on sory follicles, as described by Nakai and Shida (1948) in (Dacey and Wakeham, 1986; Savoca and sei whales (Balaenoptera borealis). These observations Nevitt, 2014). These odors could be transported by the are consistent with statements by Slijper (1962), Ling wind across the surface and give a bowhead whale (1977), and Sokolov (1982) about hair function in other downwind cues to a potential food source (Hagelin et al., mysticetes. 2012). However, olfaction is not a directional sense. Bowhead whale integument is similar to skin in other Therefore, the whale would need to ascertain the wind mammals, although there are well understood differen- direction in to locate the food, difficult for a mostly ces (Nakai and Shida, 1958; Haldiman et al., 1981; Hal- submerged animal. It is here that the vibrissae could diman and Tarpley, 1993). The external skin is generally play an important role, relaying the wind direction to black in pigmentation, but it displays areas of white the whale. skin on the eyelids, insertions, genitoanal area, Here, we are testing the hypotheses by Tomilin and the chin and occasionally the rostrum (Haldiman (1957), Henry et al. (1983), Haldiman et al. (1986), and and Tarpley, 1993). White spots on the lower jaw are Haldiman and Tarpley (1993) that the bowhead’s hairs often arranged around a hair in their center (Haldiman are vibrissae. We also hypothesize that hairs near the et al., 1981). blowhole, rostrum, and chin have different functions. In Odontocetes are naked except for a few hairs particular, we propose that the hairs on the blowhole dif- implanted on the face of fetuses of most species (Japha, fer from the hairs on the chin and rostrum and will use 1910; Ling, 1977), such as the phocoenid pho- morphometrics on the hair, hair follicle, and epidermal coena, the delphinids Delphinus delphis, and Sotalia recess, to test this. 4 DRAKE ET AL. of the village where it was caught (e.g., B for Barrow), and a serial number (e.g., 10, the tenth whale caught in a ). An F is appended to indicate that the specimen was a fetus. For histological study, samples were twice rinsed in 1% phosphate buffered saline, and extraneous fat and skin were trimmed away from the follicle. Follicles were dehydrated and embedded in paraffin, cut at 10 micro- meters thickness on a microtome, in a plane perpendicu- lar to the skin’s surface, then mounted on slides (Fisher Scientific Fisherbrand Colorfrost Plus). Slides were deparaffinized and stained with hematoxylin and eosin, Fig. 2. (A) Close-up of bowhead chin hair (2012B7.20c). (B) Close- up of hairs and epidermal recesses (2012B7.21). White bars indicate or with Lapham’s Stain (Lapham et al., 1964). Lapham’s how hair thickness and epidermal recess diameters were determined. stain is of particular use in visualizing myelin and glia associated with neurons. Hair diameters were measured on preserved samples We consider all keratinous filamentous structures in under a Zeiss SteREO DiscoveryV8 microscope using an mammals as hair, and this includes vibrissae. Vibrissae AxioCam MRc camera and AxioVision 4.8.1 11-2009 soft- are a distinct type of hair in mammals and are character- ware (Fig. 2A). The diameter of each hair was measured ized by a series of morphological specializations (Burgess at the point where it emerged from the epidermis. The and Perl, 1973; Marshall et al., 2006). Vibrissae are diameters of the epidermal recesses were measured as thicker and stiffer than pelagic hairs and display a F-SC shown in Fig. 2B. The total length of the hairs, from their consisting of a dermal papilla wrapped in a dense connec- epidermal base to the tip, was measured using calipers, tive tissue capsule, surrounded by a prominent circumfer- although it is possible that some some hairs were dam- ential blood sinus complex, and with dense innervation aged after death. The dermal length of the hair follicle (Reep et al., 2001). A vibrissal hair is associated with dis- was measured, with calipers, before histological staining. placement detection (Burgess and Perl, 1973), and it con- Data were analyzed using Systat 11, using a one way ducts external stimuli down the shaft to transmit ANOVA with covariate for the hair thickness, epidermal vibrotactile information from the surrounding environ- recess, and hair length data sets. A one way ANOVA ment to these receptors at the base of the F-SC (Burgess was used for the follicle data set. A Tukey post-hoc anal- and Perl, 1973; Gottschaldt et al., 1973; Dykes, 1975; ysis was utilized for all tests. Halata, 1975). RESULTS MATERIALS AND METHODS Histology Bowhead hair and skin samples were obtained from Mammalian hair forms as an epidermal proliferation six adult bowhead whales harvested as part of the that protrudes into the underlying dermis as the epithe- Inupiat~ subsistence hunt in Barrow, Alaska. This lial sheet of the hair shaft. This fact can be well appreci- occurred under the supervision of the North Slope Bor- ated in the developing hair of a bowhead fetus (Fig. 3G). ough, Department of Wildlife Management, and with In the postnatal individuals, bowhead hairs have a thick permission from the captains, the Barrow connective tissue capsule (Fig. 3A–C), along their entire Whaling Captains’ Association and the Alaska Eskimo extent from base of the epidermis to hair follicle. This Whaling Commission under federal permit NOAA- capsule is distinct from the surrounding adipose tissue NMFS 814-1899-01. Whales are captured in the ocean and loose connective tissue (Fig. 3A–C). The hair follicle and towed back to stable ground (ice or land) where the displays a dermal papilla (Fig. 3B) and a root sheath subsistence harvest takes place there. At the harvest (Fig. 3B,F). We did not observe any smooth or striated site, skin sections of epidermal and dermal layers with muscle tissue near the hair follicle or any associated hairs and follicles are excised from the tip of the lower glandular structures. (chin) and upper (rostrum) jaw and the region of the Inside the dense capsule, surrounding the hair fol- blowhole. Samples were preserved in 10% paraformal- licle are endothelially lined spaces with some erythro- dehyde solution for several weeks. In the laboratory, cytes (Fig. 3C, F, and H). These venous sinuses extend samples were subsampled and analyzed. We did not use mostly along the deeper half of the length of the fol- frozen samples. We also report length of the studied licle, and are scarce more superficially. They are not whales, which is coarsely correlated with age (Lubetkin one continuous space, and instead they are divided by et al., 2008). The six adult specimens include: 2012B7 trabeculae (Fig. 3C, H, and J). These sinuses also do (8.99 meters, female), 2012B9 (8.79 m, unknown gender not fully surround the follicle at all the levels of the due to position of whale on the ice,), 2012B18 (9.4 m, follicle. At the level of the papilla, approximately half female), 2012B16 (10.31 m, male), 2013B1 (16.46 m, of the circumference of the follicle is surrounded by female), and 2013B8 (6.78 m, female). In addition to vessels (Fig. 3J), whereas at higher levels (Fig. 3D) the postnatal specimens, we also studied the hair of a less than one quarter of the follicle is invested with a bowhead whale fetus (40.3 cm total length, 2000B3F). sinus. Small corpuscles are embedded in the dense con- Samples are part of the collection of the North Slope nective tissue capsule especially near its base (Fig. 3C, Borough, Department of Wildlife Management in Bar- E, F, and I), and a large nerve enters the capsule near row, Alaska. Specimen numbers are indicated by the its midpoint (Fig. 3C). We identify this nerve as the year that the whale was caught (e.g., 2000), the initial deep vibrissal nerve. Fig. 3. Histological sections of bowhead vibrissae. (A)Fulllongitudinal section of chin hair through papilla (2013B1, sl. 46, Lapham’s stain). (G) sections through two rostrum hairs, one with papilla, in rectangle Hair of chin region of bowhead fetus (2000B3F, slide 26, H&E), approxi- (2011B8, slide 33, H&E). (B) Enlarged view of hair papilla, shown in rec- mately 4 months of gestation. (H) Detail of longitudinal section of chin tangle of A. (C) Full longitudinal section through one rostum hair hair showing venous sinuses and erythrocytes (2013B18.70, slide 32, (2012B18.70, slide 32, Lapham’s stain). (D) Transverse section of chin 203, Lapham’s stain). (I) Detail of transverse section of chin hair, show- hair near the middle of the follicle (2013B1, slide 20, H&E). (E) Enlarged ing corpuscle (2013B1.A, slide 46, 403, Lapham’s stain). (J)Detailof view of middle part of hair follicle, shown in rectangle in C. (F) Transverse papilla area, showing distribution of sinuses (2013B1.A, slide 50, H&E). 6 DRAKE ET AL.

Fig. 4. Box plots of thickness of hairs (A), diameter of epidermal recess (B), follicle length (C), and length of protruding part of hair (D) of bowhead whales. Horizontal line is median, box indicates first and third quartile, and vertical line (also called whiskers) show the range of values that fall within 1.5 Hspreads of the box. Numbers indicate number of hairs measured.

The hair follicle of the fetal bowhead is surrounded by neighbors (Figs. 1B and 2B). The hairs are straight or mesenchyme, and the dense connective tissue capsule is slightly curved, do not have appreciable variation in in the process of forming (Fig. 3G). At this stage there is thickness along their shaft, do not curl, and display no no ring sinus surrounding the hair follicle, and the pigmentation. Aside from the circular epidermal innervation seen in adults is not observed. recesses, the skin is smooth, lacking depressions (Fig. 1B). Nakai and Shida (1948) accurately described the recesses as funnel shaped, and similar structures have Morphometrics been observed in other mysticetes (Mercado, 2014). Hairs in all areas of the bowhead whale head are There is a considerable difference among the thick- implanted singly, or occasionally paired, in epidermal ness (diameter) of hairs in different regions of the whale recesses, and recesses are widely separated from their (Fig. 4A). The hairs surrounding the blowhole are SENSORY HAIRS IN THE BOWHEAD WHALE 7 significantly thicker at their base than the hairs on the is also possible that there are regional differences in rostrum (P < 0.001) and the chin (P < 0.001). Chin and hair thickness across the face in cetacean ancestors and rostrum hairs are not statistically different in thickness that these differences have been retained. The closest (P 5 0.986). There is no difference among the diameter of relatives of modern cetaceans are artiodactyls (Thewis- the epidermal recesses in the different regions (Fig. 4B), sen et al. 2001). While many artiodactyls have vibrissae and the size of these recesses varies considerably. on the rostrum and tip of the mandible (Pocock, 1914), it The dermal portion of the hair follicle is longer in the is not obvious to which area the hairs posterior to the region of the blowhole and chin than in the region of the blowhole in whales are homologous. Comparisons of rostrum ((P < 0.001; Fig. 4C). The blowhole follicles are regional differences in hair thickness across the face not significantly different than the chin follicles have been carried out by Yanli et al. (1998) for carni- (P 5 0.083). In bowheads studied by Haldiman and Tarp- vores, perissodactyls, rodents, and , and there ley (1993) the total hair follicle length was approxi- are no regional trends in these groups. mately 50–60 mm, whereas our samples ranged from On the other hand, variability in hair shaft diameter 21 mm to 42 mm. There is no difference among the three is known to occur in mammals with hair patches that regions in the lengths of the exposed part of the hair have specialized functions. Reep et al. (2001) studied shaft, external to the epidermis (Fig. 4D). hair diameters in various regions of the face, and they found a distinct characteristic range in hair diameter for each of the facial regions. The hairs that DISCUSSION correspond to mystacial and mental hairs are used more While cetaceans had ancestors that were generalized often for grasping during the feeding process, and the land mammals with bodies covered by hair (Chen et al., bristle-like hairs of the oral disk are used for tactile 2013), all modern cetaceans are hairless or nearly so. exploration. Fossil evidence does not pinpoint exactly when hair Regional variation in hair shaft diameters also occurs became sparse on the bodies of cetaceans (Gatesy and in bearded seals (Erignathus barbatus; Marshall et al., O’Leary, 2001), but it has been suggested that the 2006). Vibrissae are well studied in earless seals (Phoci- mechanosense of the snout was important in the earliest dae), which use them to sense waves in the water cetaceans (Thewissen and Nummela, 2008). Bowhead (Dehnhardt et al., 1998). In eared seals (Otariidae), wal- whales are the hairiest of modern cetaceans, and the ruses (Odobenidae), and some earless seals, the diameter purpose of this paper is to determine whether bowhead of the vibrissae varies along the hair shaft, with thicker hair displays the characteristics of vibrissae, and and thinner regions alternating in a sinusoidal profile whether there are regional differences between the (Watkins and Wartzok, 1985; Hyvarinen,€ 1989; Dehn- hairs. Reep et al. (2001) identified three histological hardt and Kaminski, 1995). The morphometrics of the characteristics of vibrissae: dense connective tissue cap- beaded vibrissae differ among species, but crests and sule, circumferential blood ring sinus, and extensive sen- troughs of the hair shaft may increase sensitivity of sory innervation. Our work indicates that all three of wave reception or reduce drag and signal interference these characteristics are found in bowhead hair, support- (Ginter et al., 2010, 2012). ing the inferences from Haldiman et al. (1986) and Hal- We did not observe striated muscular tissue associated diman and Tarpley (1993) for bowheads, and consistent with the hair follicles, suggesting that hairs are not with similar suggestions in other mysticetes (Japha, mobile, unlike the active whisking virbirissae are not 1910; Lillie, 1910; Nakai and Shida, 1948; Slijper, 1962; under active muscle control of land mammals (Williams Yablokov and Klevezal, 1964; Ling, 1977; Sokolov, 1982; and Kramer, 2010), the protracting vibrissae of pinni- Berta et al., 2015). The venous sinuses associated with peds (Yablokov and Klevezal, 1964) and the highly the the hairs in bowhead whales cover neither the full mobile sirenian vibrissae (Reep et al., 2001). circumference of the follicle, not its full length. Cer- Our data are most consistent with the hypothesis that tainly, they are smaller than in some other mysticeters, bowhead hairs are a passive receptive system that detects such as the (Berta et al., 2015). Given that flow or substrate interfaces (such as water-air, water-ice), bowhead live in near freezing water their entire life, and not unlike the lateral line system of or the mechanor- that their skin is replete with adaptations related to con- eceptive organs in the skin of Crocodilia (Soares, 2002). serving heat (reviewed by Ford et al., 2013), it is not Indeed, among mammals, there are parallels with the tac- surprising that blood flow close to the body surface is tile hairs of fossorial rodents (Crish et al., 2003; Park minimal. The presence of small corpuscles that resemble et al., 2003). We interpret the differences in shaft thick- sensory receptors near the hair papilla (Fig. 3I) also sug- ness for hairs from different areas as suggestive of differ- gests a specialized function for these hairs. These cor- ent functions for these hairs. Thewissen et al. (2011) puscles resemble those described by Berta et al. (2015) found bowheads have a good sense of smell, and it is possi- in gray whales, although their identification as Herbst ble that the hairs associated with the blowhole determine corpuscles seems premature. air flow and thus wind direction, since olfaction, by itself, Our measurements show that, in most characteristics, is not a directional sense. In contrast, vibrissae near ros- hairs are variable and that there are no consistent dif- trum and mandible may detect water flow related to feed- ferences in hairs between the different anatomical ing, or the presence of hard structures, such as ice. regions. This is true for epidermal recess diameter, fol- licle length, and external hair length (Fig. 4). The excep- ACKNOWLEDGEMENTS tion is hair thickness: the hairs posterior to the blowhole are thicker than those in the other areas (Fig. 4A). It is The authors thank the whaling captains of Barrow, possible that the regional thickness variation is an adap- Alaska, and the Alaska Eskimo Whaling Commission for tation for specific functions of these hair patches, but it allowing sampling of whales, and Robert Suydam, Todd 8 DRAKE ET AL.

Sformo, Leslie Pierce, Cyd Hanns, and Brian Person of Gottschaldt KM, Iggo A, Young DW. 1973. Functional characteris- tics of in sinus hair follicles of the . the North Slope Borough, Department of Wildlife Man- J Physiol 235:287–315. agement for assistance in sampling. They are grateful to Hagelin JC, Straley JM, Nielson LB, Szabo A. 2012. Baleen whales Denise McBurney and Sharon Usip for their support in and tubenose seabirds—a colossal chemosensory convergence? the research laboratory. They thank Olga Shpak for Abstr 34th Assoc Chemorecep Sci. Huntington Beach, California. allowing us to use her photo (Fig. 1C) and April 25–28. Macrander for comments on the manuscript. Research Halata Z. 1975. The mechanoreceptors of the mammalian skin reported here was done in partial fulfillment of the con- ultrastructure and morphological classification. In: Brodal A, Hild ditions for a M.S. degree for S.E. Drake, who thanks W, van Limborgh J, Ortmann R, Schiebler TH, Tondury€ G, Wolff Chris Vinyard and Samuel Crish for their help. E, editors. Adv Anat Embryol Cell Biol 50:5–75. Haldiman JT, Abdelbaki YZ, Al-Bagdadi FK, Duffield DW, Henk WG, Henry RW. 1981. Determination of the gross and microscopic structure of the lung, kidney, , and skin of the bowhead LITERATURE CITED whale, Balaena mysticetus (RU 1380). In: Albert T, editor. Tissue Berta A, Ekdale EG, Zellmer NT, Demere TA, Kiele SS, Smallcomb structural studies and other investigations on the biology of M. 2015. Eye, nose, hair, and throat: external anatomy of the endangered whales in the . Final Report to the head of a neonate gray whale (Cetacea, Mysticeti, ). Bureau of Land Management from the Department of Veterinary Anat Rec 298:648–659. Science. VolI. Maryland: University of Maryland. NTIS No. PB86- Burgess PR, Perl ER. 1973. Cutaneous mechanoreceptors and noci- 153582/AS. p 305–662. ceptors. In: Iggo A, editor. Handbook of sensory physiology, 2: Haldiman JT, Henk WG, Henry RW. 1986. Skin. In: Haldiman JT, edi- somatosensory systems. Berlin: Springer-Verlag. p 29–78. tor. Continued studies on the determination of the morphology of Chen Z, Wang Z, Xu S, Zhou K, Yang G. 2013. Characterization of the skin, respiratory system, urinary system, vascular system, hairless (hr) and fgf5 genes provides insights into the molecular brain and eye of the bowhead whale, Balaena mysticetus. Final basis of hair loss in cetaceans. BMC Evol Biol 13:34- report from the Department of Veterinary Anatomy and Fine Struc- Crish SD, Rice FL, Park TJ, Comer CM. 2003. Somatosensory orga- ture, Louisiana State University and A&M College to the Depart- nization and behavior in naked mole-rats I: vibrissa-like body ment of Wildlife Management, North Slope Borough. p 11–31. hairs comprise a sensory array that mediates orientation to tac- Haldiman JT, Tarpley RJ. 1993. Anatomy and physiology. In: Burns tile stimuli. Brain Behav Evol 62:141–151. JJ, Montague JJ, Cowles CJ, editors. The bowhead whale. Special Croll DA, Tershy BR, Newton K. 2002. Filter Feeding. In: Perrin Publication Number 2. The Society for Marine Mammalogy. New WF, Wursig€ B, Thewissen JGM, editors. Encyclopedia of marine York: Allen Press Inc. p 71–156. mammals. London: Academic. p 422–423. Henry RW, Haldiman JT, Albert TF, Henk WG, Abdelbaki YZ, Czech-Damal NU, Liebschner A, Miersch L, Klauer G, Hanke FD, Duffield DW. 1983. Gross anatomy of the respiratory system of Marshall C, Dehnhardt G, Hanke W. 2012. in the the bowhead whale, balaena mysticetus. Anat Rec 207:435–449. (sotalia guianensis). Proc R Soc B 279:663–668. Herman LM, Tavolga WN. 1980. The Communication Systems of Dacey JW, Wakeham SG. 1986. Oceanic dimethylsulfide: production Cetaceans. In: Herman LM, editor. Cetacean behavior: mecha- during grazing on phytoplankton. Science 223:1314– nisms and functions. New York: John Wiley and Sons. p 149–209. 1316. Hyvarinen€ H. 1989. Diving in darkness: whiskers as sense organs Dehnhardt G, Hyvarinen€ H, Palviainen A, Klauer G. 1999. Struc- of the (phoca hispida saimensis). J Zool 218:663–678. ture and innervation of the vibrissal follicle-sinus complex in the Japha A. 1910. Die haare der waltiere. Zool jb. Abt Anat Ontog australian water rat, hydromys chrysogaster. J Comp Neurol 41: Tiere 32:1–42. 550–562. Kellogg R. 1928. The history of whales—their adaptation to life in Dehnhardt G, Kaminski A. 1995. Sensitivity of the mystacial vibris- the water. Q Rev Biol 3:29–76. sae of harbor seals (phoca vitulina) for size differences of actively Kukenthal€ W. 1893. Vergleichend anatomische und entwicklungsge- touched objects. J Exp Biol 198:2317–2323. schichtliche Untersuchungen an Waltiere. Vol.2. Denkschr Mediz Dehnhardt G, Mauck B. 2008. Mechanoreception in Secondarily Naturwiss Ges, Jena. p 1–148. Aquatic Vertebrates. In: Thewissen JGM, Nummela S, editors. Lapham LW, Johnstone MA, Brunjar KH 1964. A new paraffin Sensory evolution on the threshold: adaptations in secondarily method for the combined staining of myelin and glial fibers. aquatic vertebrates. Berkeley and Los Angeles, California: Uni- J Neuropath 23:156–160. versity of California Press. p 295–314. Ling JK. 1977. Vibrissae of marine mammals. In: Harrison RJ, edi- Dehnhardt G, Mauck B, Bleckmann H. 1998. Seal whiskers detect tor. Functional anatomy of marine mammals 3. London: Academic water movements. Nature 394:235–236. Press. p 387–415. Dykes RW. 1975. Afferent fibers from mystacial vibrissae of Lillie DG. 1910. Observations on the anatomy and general biology and seals. J Neurophysiol 38:650–662. of some members of the larger cetacea. Proc Zool Soc London Eschricht DF, Reinhardt J. 1866. On the right-whale 1910:779–792. (Balaena mysticetus). In: Flower WH, editor. Recent memoirs on Lubetkin SC, Zeh JE, Rosa C, George JC. 2008. Age estimation for the Cetacea. The Ray Society. London: Robert Hardwicke. p 1–50. young bowhead whales (balaena mysticetus) using annual baleen Ford TJ, Jr, Werth AJ, George JC. 2013. An intraoral thermoregula- growth increments. Can J Zool 86:525–538. tory organ in the bowhead whale (balaena mysticetus), the corpus Marshall CD, Amin H, Kovacs KM, Lydersen C. 2006. Microstruc- cavernosum maxillaris. Anat Rec 296:701–708. ture and innervation of the mystacial vibrissal follicle-sinus com- Gatesy J, O’Leary M. 2001. Deciphering whale origins with mole- plex in bearded seals, erignathus barbatus (pinnipedia: phocidae). cules and fossils. Tr Ecol Evol 16:562–570. Anat Rec Part A 288A:13–25. George JC, Clark C, Carroll GM, Ellison WT. 1989. Observations on Marshall CD, Clark LA, Reep RL. 1998a. The muscular hydrostat the ice-breaking and ice navigation behavior of migrating bow- of the florida manatee (trichechus manatus latirostris) and its head whales (balaena mysticetus) near , alaska, role in the use of perioral bristles. Mar Sci 14:290–303. spring 1985. Arctic 42:24–30. Marshall CD, Huth GD, Edmonds VM, Halin DL, Reep RL. 1998b. Ginter CC, DeWitt TJ, Fish FE, Marshall CD. 2012. Fused tradi- Prehensile use of perioral bristles during feeding and associated tional and geometric morphometrics demonstrate behaviors of the florida manatee (trichechus manatus latirostris). whisker diversity. PLoS ONE 7:1–10. Mar Mammal Sci 14:274–289. Ginter CC, Fish FE, Marshall CD. 2010. Morphological analysis of Marshall CD, Maeda H, Iwata M, Furuta M, Asano A, Rosas F, the bumpy profile of phocid vibrissae. Mar Mammal Sci 26:733– Reep RL. 2003. Orofacial morphology and feeding behaviour of 743. the dugong, amazonian, west african and antillean SENSORY HAIRS IN THE BOWHEAD WHALE 9

(mammalia: ): functional morphology of the muscular- producers and top predators. Proc Natl Acad Sci USA 111:4157– vibrissal complex. J Zool (London) 259:1–16. 4161. Mauck B, Eysel U, Dehnhardt G. 2000. Selective heating of vibris- Slijper EJ. 1962. Whales. New York: Basic Books. sal follicles in seals (phoca vitulina) and (sotalia fluviati- Soares D. 2002. An ancient sensory organ in crocodilians. Nature lis guianensis). J Exp Biol 203:2125–2131. 417:241–242. Mercado E. 2014. Short note: tubercles: what sense is there. Aq Sokolov VE. 1982. Mammal skin. Berkeley: University of California Mamm 40:95–103. Press. Nakai J, Shida T. 1948. Sinus-hairs of the sei-whale (Balaenoptera Sterba O, Klima M, Schildger B. 2000. Embryology of dolphins: borealis). Sci Rep Whales Res Inst, Tokyo 1:41–47. staging and ageing of embryos and fetuses of some cetaceans. Adv Norman Jr JR, Fraser FC. 1948. Giant whales dolphins. Lon- Anat Embryol Cell Biol 157:1–132. don: Putnam Press. Sylvestre JP. 1985. Some observations on behavior of two orinoco Park TJ, Comer C, Carol C, Lu Y, Hong HS, Rice FL. 2003. Somato- dolphins (inia geoffrensis humboldtiana, pilleri and gihr 1977), in sensory organization and behavior in naked mole-rats: II. Periph- captivity, at duisburg . Aq. Mamm. 11:58–65. eral structures, innervation, and selective lack of neuropeptides Thewissen JGM, George J, Rosa C, Kishida T. 2011. Olfaction and associated with and pain. J Comp Neurol 465: in the bowhead whale (balaena mysticetus). Mar Mam- 104–120. mal Sci 27:282–294. Pocock RI. 1914. On the facial vibrissae of mammalia. J Zool (Lon- Thewissen JGM, Heyning J. 2007. Embryogenesis and Development in don) 84:889–912. attenuata and other cetaceans. In: Miller DL, editor. Repro- Purves PE. 1967. Anatomical and experimental observations on the ductive biology and phylogeny of Cetacea: Whales, Dolphins and Por- cetacean system. In: Busnel RG, editor. Animal sonar sys- poises. Vol.7. In: Jamieson BGM, editor. Reproductive biology and tems: biology and bionics. Jouy-en-Josas 78, France: Laboratoire phylogeny. Enfield, New Hampshire: Science Publishers. p 307–329. de Physiologie Acoustique. p 197–270. Thewissen JGM, Nummela S. 2008. Toward an integrative Reep RL, Gaspard JC, Sarko D, Rice FL, Mann DA, Bauer GB. approach. In: Thewissen JGM, Nummela S, editors. Sensory evo- 2011. Manatee vibrissae: evidence for a “lateral line” function. lution on the threshold, adaptations in secondarily aquatic verte- Ann NY Acad Sci 1225:101–109. brates. Berkeley, University of California Press. p 333–340. Reep RL, Marshall CD, Stoll ML. 2002. Tactile hairs on the postcra- Thewissen JGM, Williams EM, Roe LJ, Hussain ST. 2001. Skeletons nial body in florida manatees: a mammalian lateral line?. Brain of terrestrial cetaceans and the relationships of whales to artio- Behav Evol 59:141–154. dactyls. Nature 413:277–281. Reep RL, Stoll ML, Marshall CD, Homer BL, Samuelson DA. 2001. Tomilin AG. 1957. Mammals of the USSR and adjacent countries. Microanatomy of facial vibrissae in the florida manatee: the basis Cetacea. Vol 9. Translated by the Israel Program for Scientific for specialized sensory function and oripulation. Brain Behav Translations, , 1967 (NTIS No. TT 65-500867). Evol 58:1–14. Watkins WA, Wartzok D. 1985. Sensory biophysics of marine mam- Rice FL, Fundin BT, Arvidsson J, Aldskogius H, Johansson O. mals. Mar Mammal Sci 1:219–260. 1997. Comprehensive immunofluorescence and lectin binding Wilkens LA, Hofmann MH. 2008. Electroreception. In: Thewissen analysis of vibrissal follicle sinus complex innervation in the mys- JGM, Nummela S, editors. Sensory evolution on the threshold: tacial pad of the rat. J Comp Neurol 385:149–184. adaptations in secondarily aquatic vertebrates. Berkeley and Los Rice FL, Kinnman E, Aldskogius H, Johansson O, Arvidsson J. Angeles, California: University of California Press. p 325–332. 1993. The innervation of the mystacial pad of the rat as revealed Williams CM, Kramer EM. 2010. The advantages of a tapered by PGP 9.5 immunofluorescence. J Comp Neurol 337:366–385. whisker. PLoS One 5:1- Rice FL, Mance A, Munger BL. 1986. A comparative light micro- Yablokov AV, Klevezal GA. 1964. Vibrissae of whales and seals, scopic analysis of the innervation of the mystacial pad. I. Vibris- their distribution, structure, and significance. In: Kleinenberg SE, sal Follicles. J Comp Neurol 252:154–174. editor. Morfoloficheskie osobennosti vodnykh mlekopitaiuschikh. Sarko DK, Rice FL, Reep RL. 2011. Mammalian tactile hair: diver- : Akad Nauk SSSR. p 48–81. gence from a limited distribution. Ann NY Acad Sci 1225:90–100. Yanli B, Wei Z, Yanchun X, Jun Z, Xiaoming T. 1998. Relationship Savova MS, Nevitt GA. 2014. Evidence that dimethyl sulfide between structure and function of mammalian vibrissa. J Forest facilitates a tritrophic mutualism between marine primary Res 9:273–276.