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Manatee Facial Vibrissae

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  ©2001 S.KargerAG,Basel0006–8977/01/0581–0001$17.50/0Fax +41 61 306 12 34E-Mail karger@karger.chAccessible online at:www.karger.comwww.karger.com/journals/bbe Microanatomy of Facial Vibrissae in theFloridaManatee: The Basis forSpecializedSensory Function and Oripulation R.L. Reep a M.L. Stoll a C.D. Marshall d B.L. Homer b D.A. Samuelson c a Department of Physiological Sciences and Brain Institute, b Department of Pathobiology, c Department of SmallAnimal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, Fla., d Departmentof Orthodontics/Burke Museum of Natural History University of Washington, Seattle, Wash., USA Original Paper Brain Behav Evol 2001;58:1–14 Dr. R.L. ReepDepartment of Physiological Sciences, Box 100144, HSCUniversity of Florida, Gainesville, FL 32610 (USA)Tel. +1 352 392-4700, ext. 3859, Fax +1 352 392-5145E-Mail reep@ufbi.ufl.edu Key Words Mammals ã Sirenia ã Manatee ã Vibrissae ã Hair ã Bristles ã Face Abstract Sirenians, including Florida manatees, possess an arrayof hairs and bristles on the face. These are distributedina pattern involving nine distinct regions of the face,unlike that of any other mammalian order. Some of thesebristles and hairs are known to be used in tactile explo-ration and in grasping behaviors. In the present study wecharacterized the microanatomical structure of the hairand bristle follicles from the nine regions of the face.Allfollicles had the attributes of vibrissae, including adense connective tissue capsule, prominent blood sinuscomplex, and substantial innervation. Each of the nineregions of the face exhibited a distinct combination of these morphological attributes, congruent with the pre-vious designation of these regions based on location andexternal morphological criteria. The present data sug-gest that perioral bristles in manatees might have atactile sensory role much like that of vibrissae in othermammals, in addition to their documented role in grasp-ing of plants during feeding. Such a combination of motor and sensory usages would be unique to sirenians.Finally, we speculate that the facial hairs and bristlesmay play a role in hydrodynamic reception. Copyright © 2001 S. Karger AG, Basel Introduction Sirenians possess a varied array of modified facial hairsthat are used in tactile exploration, interactions with con-specifics, and feeding [Hartman, 1979; Marshall, 1997;Marshall et al., 1998a, 2000; Bachteler and Dehnhardt,1999]. In manatees these include six types of perioral bris-tles and bristle-like hairs on the oral disk [Reep et al., 1998].These are distinguished from other body hairs by theirgreater stiffness, which appears to result from smallerlength/diameter ratios rather than from compositional dif-ferences. Hair having the external appearance of body hairis located on the supradisk portion of the face posterior tothe orofacial ridge and on the chin [Reep et al., 1998].As illustrated in figure 1, the six fields of perioral bristleson the face of the Florida manatee consist of four (U1–U4)on each side of the upper lips and oral cavity and two(L1–L2) on each side of the lower lip pad along the lip mar-gin [Reep et al., 1998]. Each field has a characteristic loca-tion, number of bristles, and range of external bristle lengthand diameter. Branches of the infraorbital nerve innervatethe bases of the largest bristles (U2 group) on the upper bris-tle pad, and the inferior alveolar nerve supplies the L1–L2bristles of the lower bristle pad. These innervation patternsand the topographical locations of the six bristle fields sug-gest that the U1–U4 bristles are homologous to the mysta-cial vibrissae of other mammals, whereas the L1–L2 bristlescorrespond to the mental vibrissae [Reep et al., 1998]. Dor-sal and ventral buccal branches of the facial nerve innervate Received: June 21, 2001Returned for revision: July 24, 2001Accepted after revision: August 10, 2001  the superficial facial musculature, which is likely to beinvolved in bristle eversion and other movements that occurduring feeding behavior [Marshall et al., 1998b; Reep et al.,1998].Sirenians use the modified hairs of the face in a varietyofbehaviors. Uniquely among mammals, they use some of the perioral bristles (primarily those of the U2 and L1 fields)in a grasping fashion during feeding and oripulation of objects [Marshall et al., 1998a, 2000]. (We have coined theterm ‘oripulation’ to refer to use of the mobile lips and asso-ciated perioral bristles in coordinated rhythmic graspingbehaviors. This seems preferable to the term ‘manipulation’,which connotes use by the manus, or hand.) Tactile explo-ration without grasping typically involves the bristle-likehairs of the oral disk [Hartman, 1979; Marshall et al., 1998a;Bachteler and Dehnhardt, 1999]. Most mammals use theirvibrissae in a purely sensory fashion, primarily to detectprey or to orient in low light environments. Vibrissae arecapable of providing detailed textural information aboutsurfaces and objects in the immediate environment [Dykes1975; Brecht et al., 1997]. Psychophysical measures indi-cate that harbor seals may be able to use their vibrissae insensory detection as effectively as monkeys use their handsin touch discrimination [Dehnhardt and Kaminski, 1995]. Inrats the geometry of vibrissal lengths within a row and theangular arrangements of the vibrissae of each row relative tothe body axis and the other rows are important variablesinfluencing the behavioral use of the vibrissae [Brecht et al.,1997].Among non-sirenians, movement of vibrissae occurs inseveral contexts. Rodents engage in whisking behavior inwhich the mystacial vibrissae are swept in a rhythmic fash-ion during tactile exploration of the external environment[Welker, 1964; Wineski, 1985; Carvell and Simons, 1990].Pinnipeds move their long vibrissae during display behav-iors and tactile exploration [Peterson and Bartholomew,1967; Miller, 1975; Kastelein and Van Gaalen, 1988; Dehn-hardt, 1994; Dehnhardt and Kaminski, 1995; Dehnhardt andDucker, 1996]. When out of water with the snout pointedupward, walruses have been observed to move pieces of fishin the direction of the mouth by passing them from vibrissato vibrissa in a wave-like manner [Marshall et al., 1998a],but they engage in no grasping. Freshwater river dolphins(Platanistidae) have reduced visual systems and relativelywell developed bristle-like vibrissae along the upper andlower jaws. These non-mobile vibrissae are reportedly usedto detect fish and crustacean prey along river bottoms [Nor-man and Fraser, 1948 as cited in Ling, 1977; Layne andCaldwell, 1964]. Collectively, these findings indicate thatsensory detection in non-sirenians is often accompaniedbymovements of the vibrissae, but not by grasping.One of the defining features of vibrissae in non-sirenianmammals is their organization as sinus hairs, in which ablood-filled sinus encircles the hair shaft and contains alongits wall a substantial number of sensory nerve endings.Vibrissae in rodents, rabbits, and cats are innervated by asingle deep vibrissal nerve containing 100–200 axons thatascend along the inner margin of the sinus wall and ter-minate in receptors located in the outer root sheath andmesenchymal sheath [Rice et al., 1986, 1997]. In monkeysthe deep vibrissal nerve supplies each vibrissae with80–100axons entering through 2–3 nerve fascicles [Halataand Munger, 1980]. In addition to the deep vibrissal nerve,a superficial vibrissal nerve containing 20–30 unmyelinatedaxons innervates the rete ridge collar and outer conicalbody, components of the follicle located near the skin sur-face [Mosconi et al., 1993].There has been no comparable study of hair folliclemorphology and innervation in sirenians. Earlier studiesreported morphological attributes of some of the facial bris-tles and hairs, but these were not based on systematic sam-pling methods and did not include nerve counts. Dosch[1915] reported that all body hairs on sirenians were sinushairs, intermediate in form between pelage hairs and vibris-sae. He expanded upon the earlier studies of Kükenthal andothers [referenced in Dosch, 1915], and even used some of the same specimens used by Kükenthal. His conclusion hasbeen supported in dugongs by the findings of Bryden et al.[1978], Kamiya and Yamasaki [1981], and Sokolov [1982],and in Antillean manatees by Sokolov [1986]. However, in 2 Brain Behav Evol 2001;58:1–14 Reep/Stoll/Marshall/Homer/Samuelson Abbreviations appring sinus appendagesepiepidermisorsouter root sheathblbloodgmglassy membranersring sinuscapfollicle capsulehshair shafttrbtrabeculae of cavernous sinusderdermislcslower cavernous sinusucsupper cavernous sinusdpdermal papillamsmesenchymal sheath  most of these cases a lack of regional specification togetherwith a paucity of figures make it impossible to determine thelocation from which follicle samples were taken. Sokolov[1986] did provide some quantitative morphological charac-terization of the ‘thick vibrissae of the upper and lower lips’(probably corresponding to bristle fields U2 and L1) in theAntillean manatee (T. manatus manatus) but did not sys-tematically explore other subfields of the face.The nine regions of the manatee face are distinguishablebased on location, distribution of bristles or hairs, externalmorphology of bristles or hairs, and the behavioral roleplayed by the bristles and hairs during feeding and otherbehaviors. Therefore, in the present study we sought todefine internal follicle microanatomy and innervation inthese regions of the face. One goal was to determinewhether all the facial hairs of the Florida manatee possessthe structural characteristics of sinus hairs, as would beexpected if they were homologous to the vibrissae of othermammals. A second goal was to obtain estimates of inner-vation density for the follicles in each of the nine regions of the face. Materials and Methods A total of 166 follicles were processed and 82 of these were ana-lyzed quantitatively in this study (tables 1 and 2). They were collectedfrom eleven fresh (w/in 24 h) postmortem manatee carcasses in con- junction with the statewide manatee carcass salvage program managedby the Marine Mammal Pathobiology Laboratory in St. Petersburg,Fla., USA (USFWS permit PRT-684532). All but one of the carcasseswere in the subadult-adult range of body length, corresponding to 1.5+years of age, as determined by the USGS Sirenia Project (unpubl.data). However, specimen SWFTM 9515 was much smaller, in therange of a small calf 1–6 months of age. As shown in table 1, follicleswere taken from nine regions of the face which were defined in a pre-vious study [Reep et al., 1998]. Bristle-like hairs were found in twolocations; most were located on the oral disk (BLHod) but occasionallyone was found among the bristles (BLHbr) in the U1 or U2 field.A #11 scalpel blade was used to extract blocks of tissue (~5  × 5 mmat the surface and ~10–15 mm in length) that included single folliclesand the immediately surrounding connective tissue. Specimens werestored in 4% phosphate buffered formalin (pH 7.4) then cut frozen at40 µm on a Lipshaw sliding microtome. Serial longitudinal or crosssections were stored in dilute fixative in 24-well plastic tissue cultureplates. Sections were mounted on gelatin coated glass slides, using avery dilute (0.5%) gelatin mixture to minimize background staining inthe case of silver staining.After drying overnight, slides with sections were hydrated andstained using hematoxylin and eosin, Masson’s trichrome stain, or amodified Bodian stain. The longitudinal sections were used for mea-surements of follicle morphology and to identify deep vibrissal nervebundles and their trajectories. The cross sections were used for count-ing the number of axons innervating a follicle.Approximately 30 follicles were prepared using paraffin embed-ding and stained using Masson’s trichrome or hematoxylin and eosin.Bodian staining of paraffin sections did not prove as reliable as thatperformed on frozen sections. The paraffin embedded sections werenot used for quantitative measurements of follicle geometry, in order toavoid shrinkage artifacts.In 57 selected longitudinal sections we measured maximum fol-liclelength, maximum total sinus length (upper + ring + lower sinus),maximum ring sinus width, maximum follicle capsule thickness, andmaximum hair shaft diameter at the level of the ring sinus. These mea-surements were made on an AIS/C imaging workstation (ImagingResearch, Inc.) interfaced with a Zeiss Axiophot 2 microscope andDage 72 video camera. Sections used for measurement were chosenbased on their orientation as near as possible to the central longitudinalaxis of the hair shaft. The left and right sides of each section were mea-sured, and we retained only the maximum values. Data are presented asranges due to low sample sizes and high variability.3 Microanatomy of Facial VibrissaeintheManatee Brain Behav Evol 2001;58:1–14 Fig.1. Schematic diagram of the perioral region, showing the loca-tion of the upper (U1–4) and lower (L1–2) bristle fields, bristle-likehairs (BLH), supradisk, and chin. Dotted lines indicate cuts made in thecheek muscles to allow a fuller view of the oral cavity.  For making axon counts, we used 33 cross sections in which axonsappeared well stained by the modified Bodian procedure. We alsorequired that these sections be located just apical relative to the regionof nerve entry, in order to estimate the maximum number of axonsperfollicle. In such material one observes spaced bundles of axons,and individual axons are separately identifiable by their myelin sheath(fig.4). However, due to the capricious nature of silver staining, itwasrare that a section exhibited well defined staining throughout thecircumference of the follicle. Rather, some axon bundles appeareddark and others appeared too light to permit accurate counting. In thesecases we capitalized on the fact that just apical to their entry, the 2–6large nerve bundles innervating each follicle disperse into smaller bun-dles of 2–5 axons each. These smaller bundles are uniformly spacedaround the circumference of the follicle as they ascend toward theirsites of termination along the sinus wall. Therefore, in many cases weestimated total axon number by performing direct axon counts on half of the total 360°and multiplying the result by two. In order to assessrelationships between nerve counts and follicle geometry, we mea-sured the perimeter of the innervated ring sinus wall and estimated thelength of the ring sinus on the same follicles from which nerve countswere obtained. Perimeters were measured on the same sections fromwhich axon counts were obtained, using the imaging system describedabove. Ring sinus length was estimated by counting the number of cross sections on which the ring sinus appeared as a distinct entitycharacterized by large width and a lack of trabeculae, then multiplyingthis number by section thickness. The beginning and end of the ring4 Brain Behav Evol 2001;58:1–14 Reep/Stoll/Marshall/Homer/Samuelson Table 1. Number of follicle samples taken from eleven specimensAnimalSexWeightLengthU1U2U3U4L1L2BLHodBLHbrChinSupradisk (kg)(cm)MNW 9425M45830123522231SWFTM 9515M311191111SWFTM 9530M2482432SWFTM 9534M37026733332SWFTM 9607M38727821MEC 9903M3002573335MSE 9210MNA2581MSW 9524F33024759554756MSE 9807F321250596766525MSTM 9908F1342203MEC 9952F1231714 Table 2. Microanatomical attributes of perioral bristles and bristle-like hairs U1U2U3U4L1L2BLHBLHBLHSupra-Chin(total)odbrdisk Follicle length8.63–9.6810.66–18.528.19–10.056.54–9.567.33–8.833.30–7.406.11–9.365.41–8.775.41–8.773.51–5.804.62–8.22(mm)Max total sinus5.72–5.915.90–9.344.57–5.623.95–6.253.82–6.672.17–4.214.90–7.204.15–6.785.5–7.21.83–5.142.65–6.49length (mm)Max ring sinus509–698546–1123445–534403–592469–698338–600300–690277–546390–690262–511462–485width (µm)Max capsule601–655588–866385–503394–591396–761198–529225–560225–548504–560144–423263–586thickness (µm)Axons per follicle61–84210–25489–11688–100184–20282–10849–7449–6050–7434–4240–48Hair diameter (µm)362–428720–1800486–662435–494315–798328–546131–36292–218131–36262–118108–362Hair length/dia ratio62–5371–713232NA80var# samples for21446451410453geometry# samples for nerve23222353232counts Data for external hair length/diameter ratios are from Reep et al. [1998]. Top row gives abbreviations for the perioral fields described in thetext.

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Jul 23, 2017
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