Stangl, Jr., Frederick B.

English

OSU Journals (Oklahoma State University)

25Proc. Okla. Acad. Sci. 74: 25-29 (1994)Gross Morphology and Distribution Patterns of Lingual Papillae in SomeGeomyid and Heteromyid RodentsFrederick B. Stangl, Jr. and Russell S. PfauDepartment of Biology, Midwestern State University, Wichita Falls, TX 76308Received: 1993 Aug 02; Revised: 1994 Mar 11There have been few studies of lingual morphology and associated papillae of rodents since a 1924 study restricted mostly toOld World taxa (1). This is especially applicable to the North American superfamily Geomyoidea. We examined thedistribution patterns and types of lingual papillae for three geomyids and 12 heteromyid rodent species. All member taxa havea single circunivallate papilla, widespread filiform papillae, and fungiform papillae, which are restricted anteriorly on thetongue surface. The two families can be distinguished on the basis of variation of these characters. No further resolution isafforded within the geomyids. However, subfamilial levels of variation can be distinguished within the Heteromyidae, andfindings are suggestive of specific differences between member species of the genera Perognathus, Chaetodipus, and Dipodomys.INTRODUCTIONThe rodent superfamily Geomyoidea is an ancient assemblage comprised of two distinct families. Thegophers (Geomyidae) are heavily built, fossorial animals which feed primarily on subterranean roots and leafyvegetation. The kangaroo rats, pocket mice, and their allies (Heteromyidae) are more delicate in structure, andrange from bipedal to scansorial forms which forage mostly for seeds.Many aspects of the anatomy of heteromyid rodents have been investigated, from the molecular andcytogenetic levels to gross morphology. Three rather distinct subfamilial lineages are recognized by Hafner andHafner (2): the primitive Heteromyinae (Heteromys and Liomys), the Perognathinae (Perognathus andChaetodipus), and the relatively derived Dipodomyinae (Dipodomys and Microdipodops). Perceptions ofinterrelationships among the more specious genera (Perognathus, Chaetodipus, and Dipodomys) are lessobvious. There is no recent study of comparable breadth for the Geomyidae.A superficial but taxonomically diverse survey of the external lingual morphology for 11 families ofrodents led Sonntag (1) to conclude that distinctive lingual characters are observable at the familial and oftengeneric level, and that little variation occurs at the specific level. Few subsequent studies have detailed externalaspects of tongue structure for other mammals (3-8). Particularly neglected have been the distribution and typesof lingual papillae among rodents. Additionally, the only pertinent reference in the literature for any member ofthe superfamily Geomyoidea is Sonntag's (1) citation of an 1888 observation that a single circumvallate papillaoccurs in the gopher, Geomys bursarius.The purpose of this study was twofold: first, to provide the first preliminary assessment of variation in thesurface anatomy of representative geomyoid rodents, especially as pertains to lingual papillae; and second, todetermine if such differences are as taxonomically distinct for the Geomyoidea as has been reported for otherrodent taxa.METHODS AND MATERIALSSpecimens were collected from wild populations or were borrowed from the collections of the Museum ofTexas Tech University (TTU) and the Museum of Natural History of Los Angeles County, CA (LACM). Giventhe destructive nature of the technique employed (below), we were reluctant to borrow more than singlerepresentatives of each species.  Emphasis was therefore placed on taxonomic diversity, although more than onespecimen of some species were examined where possible. The lower jaw and hyoid musculature of each fluid-preserved whole specimen was exposed by first peeling back the skin from the lower jaw. The base of thetongue was then26 F.B. STANGL, Jr. and R.S. PFAUProc. Okla. Acad. Sci. 74: 25-29 (1994)carefully severed with a scalpel, far enough back to include theentire field of surface lingual papillae. The severed tissue was thengently pulled back from between the jaws with forceps. Followingremoval from the body, each tongue was stored in a glass vial of60:40 2-propanol:water with a tag containing specificidentification, and acronym and catalog number for the originatinginstitution. Examinations took place with a light microscope undervariable magnifications. Tongues were kept moist duringexaminations and illustration sessions, and Giemsa stain wasapplied to the surface of each tongue to provide the contrastnecessary for illustration of the surface anatomy with a cameralucida attachment.Tongues in vials were retained with those specimens ondeposit at Midwestern State University, or were returned to thelending institutions.RESULTS and DESCRIPTIVE ACCOUNTSThe geomyoid tongue is characterized by a tapered tip whichis divided dorsally along the distal fourth of the tongue by ashallow, terminal groove. The intermolar eminence, an elevatedregion situated between the cheek teeth and described by Sonntag(1) as typical of most rodents, is not readily discernible when thetongue is extended. However, if the tongue is sufficiently contracted, this region protrudes prominently. It isthen bordered anteriorly by a U- or V-shaped sulcus.Lingual papillae cover the dorsum of the tongue and continue onto the sides. The most widespreadstructural type of these are the filiform papillae, which envelop the top, sides, and anterior tip of the tongue.These tiny structures are mostly monofid, and the sharp and tapered tips generally project posteriorly. Larger,circular-shaped fungiform papillae are prominently and somewhat uniformly distributed over at least the distalone-third of the tongue.Largest and most conspicuous of lingual structures is the posteromedial circumvallate papilla. It is quitevariable in shape, size, and surface topography, even between con-specific individuals. The shape is generallycircular to ovoid. The dorsum is typically marked by minute bumps or projections which are difficult to resolvewith light microscopy. This papilla resides in a craterlike depression bordered by marginal folds. Its prominencemay be a transient feature. In some specimens, it is distinctly protruded, while in others it appears to be retractedinto the depression. Given the extent of individual variation and the lack of resolving power with lightmicroscopy, we are reluctant to attempt further detailed descriptions of this character. Distribution of thefiliform papillae diverge around, and terminate, near the circumvallate papilla.Family GeomyidaeLingual morphology among gophers is conservative, for no consistent differences were found to distinguishthe tongues of Thomomys bottae (n = 2), Geomys bursarius (n = 3), or Cratogeomys castanops (n = 2).  Thegeomyid tongue is elongate and rather fusiform (Figure 1). From a dorsal perspective it is broadest at the base,becomes gradually constricted anteriorly, then broadens and tapers to the tip. In cross-section of the terminalthird of the tongue, the sides are noticeably concave before flaring out to form a shelf usually visible fromabove.27 LINGUAL PAPILLAE in GEOMYID and HETEROMYID RODENTSProc. Okla. Acad. Sci. 74: 25-29 (1994)Fungiform papillae are small and most abundant near thetip of the tongue.  Filiform papillae are monofid, with theminor exception of a few bi- and trifurcate papillae along themargins of the ventrolateral ridge. These are quite elongateand thorn-like along the lateral margins at the midbody of thetongue. Filiform papillae are smallest at the tongue tip andwithin a shallow trough in the vicinity of the midbody constriction, but also become smaller in size towards theposterior extent of their distribution. Most filiform papillae are oriented posteriorly, except for the vicinity of theapex of the intermolar eminence. This region, even if not elevated, is marked by a radiation of papillae outwardsfrom a focal point just posterior to the midbody trough to form a whorl-like pattern.Family HeteromyidaeThe heteromyid tongue (e.g., Figure 2) is a short, broad and tapered organ which also differs from thegeomyid condition in the following ways: 1) body tapered, with less conspicuous midbody constriction; 2)ventral shelf less prominent, as visible in cross-section or from the dorsal perspective; 3) fungiform papillaewith greater variation in size and distribution (over anterior half or more of dorsal surface); 4) ventrolateralridge smooth, rather than with filiform papillae; and 5) intermolar eminence marked by broad polyfid (mostlybi- and trifurcate) filiform papillae, which are more uniformly oriented posteriorly. The circumvallate papillaappears to be especially variable, although this may be an artifact of preservation.Subfamily Dipodomyinae. Characterization of the lingual morphology of this subfamily is based on sixspecies of kangaroo rats: Dipodomys agilis (n = 1); D. compactus (n = 1); D. deserti (n = 1); D. elator (n = 3);D. merriami (n = 1); D. microps (n = 1); D. ordii (n = 4); and D. spectabilis (n = 1). Fungiform papillae occurover the anterior half of the tongue surface, and are especially concentrated at the tip. The considerable inter-specific variation among representatives of this assemblage seems restricted to the intermolar eminence, asmarked by the distribution of polyfid filiform papillae (Figure 3). For example, the distribution of these28 F.B. STANGL, Jr. and R.S. PFAUProc. Okla. Acad. Sci. 74: 25-29 (1994)papillae is quite broad in the single example of D. deserti, but issparse and irregular among each of two specimens of D. microps.Subfamily Perognathinae. In most respects, the lingualmorphology of Perognathus flavus (n = 1), Chaetodipus nelsoni(n = 1), and C. hispidus (n = 2) are essentially similar to theDipodomyinae (Figure 4). Nevertheless, some consistentdifferences were noted. The fungiform papillae are distributedover the surface of the tongue, except for the intermolareminence, and many of these are proportionally quite large in C.nelsoni.  Additionally, the broad polyfid filiform papillacomprising the intermolar eminence are less deeply forked thanin the genus Dipodomys.Subfamily Heteromyinae. Only a single specimen ofLiomys irroratus was available to represent this tropical-to-subtropical subfamily. In most respects, the lingualmorphology resembles that of the Perognathinae, although the filiform papillae do not extend nearly so farposteriorly as in other geomyoid taxa. Furthermore, these are either small and blunted or are very weakly forked,rather than being simple conical structures (Figure 5). Although this subfamilial sample is restricted, theuniqueness of these distinguishing features lead us to believe that they likely characterize the species, andperhaps also the entire genus.SUMMARY and CONCLUSIONSBecause the tongue is such a muscular and pliant organ, overall shape and certain morphological featuresare transient characters in life. Among preserved tongues of specimens, we found distortions due to dehydration,state of flexion at time of fixation, and molding against the palate or teeth— any of which are capable ofconfounding comparative analyses. The qualified definitions of such lingual features as overall shape, sulci, andprominences must therefore be accepted with caution. However, morphology and general patterns of distributionof filiform and fungiform papillae are not affected by such factors, and they are sufficiently variable to affordsome systematic resolution among member taxa of the rodent superfamily Geomyoidea.The family Geomyidae is distinguished by filiform papillae which are elongated and are almost entirelymonofid. The ventrolateral ridge is marked by a few bi- and trifurcate filiform papillae. Fungiform papillae aresmall, and are restricted to the anterior one-third of the tongue. Representative species of Thomomys, Geomys,and Cratogeomys are indistinguishable for these familial characters.Filiform papillae among the Heteromyidae are relatively short and stout. The intermolar eminence isadorned with broadened, polyfurcate filiform papillae, which contrast with the monofid condition elsewhere.The ventrolateral ridge is devoid of papillae. Each of the three subfamilies can be distinguished by the assessedcharacters. The potential of certain lingual features for specific or species group discrimination among pocketmice (size, distribution of fungiform papillae) and kangaroo rats (distribution patterns of polyfid papillae on theintermolar eminence) are deserving of further study.ACKNOWLEDGMENTSRobert J. Baker of Texas Tech University and Sarah George of the Natural History Museum of Los AngelesCounty (CA) kindly permitted the use of specimens housed in those respective institutions. Walter W. Dalquestand two anonymous reviewers provided constructive criticisms on an earlier draft of the manuscript. We alsothank Steve Kasper for his assistance in the packaging and transport of specimens.REFERENCES1. Sonntag, C.F., The Comparative Anatomy of the Tongue of the Mammalia.29 LINGUAL PAPILLAE in GEOMYID and HETEROMYID RODENTSProc. Okla. Acad. Sci. 74: 25-29 (1994)X. Rodentia. Proc. Zool. Soc. London  1924, 725-739 (1924).2. Hafner, J.C., and Hafner, M.S., Evolutionary Relationships of Heteromyid Rodents. Great Basin Nat. Mem.7, 3-29 (1983).3. Agarwal, K.A., and Gupta, B.B., The Structure and Histology of the Tongue in Two Indian BatsRhinopoma kinneari (Rhinopomatidae) and Scotophilus heathi (Vespertilionidae). Folia Morphol. 30,26-41 (1982).4. Griffiths, T.A., Systematics of the New World Nectar-Feeding Bats (Mammalia, Phyllostomidae), Based onthe Morphology of the Hyoid and Lingual Regions. Am. Mus. Novitates 2742, 1-45 (1982).5. Kobayashi, S., Shimoda, T., and Shimamura, A., Comparative Anatomical Observations on the Tongue ofthe Insectivora. Okajimas Folia Anat. Jpn. 60, 211-218 (1983).6. Krause, W.J., and Cutts, J.H., Morphological Observations on the Papillae of the Opossum Tongue. ActaAnat. 113, 159-168 (1982).7. Kubota, K., Kubota, J., Fukuda, N., and Asakura, S., Comparative Anatomical and NeurohistologicalObservations on the Tongue of the Great Anteater (Myrmecophaga jubata Linne). Anat. Rev. 143, 15-19(1962).8. Yamasaki, F., Komatsu, S., and Kamiya, T., A Comparative Morphological Study on the Tongues ofManatee and Dugong (Sirenia). Sci. Rep. Whales Res. Inst. 32, 127-144 (1980).

Gross Morphology and Distribution Patterns of Lingual Papillae in Some Geomyid and Heteromyid Rodents

https://ojs.library.okstate.edu/osu/index.php/OAS/article/download/5539/5164

Gross Morphology and Distribution Patterns of Lingual Papillae in Some Geomyid and Heteromyid Rodents

Abstract

Similar works

Full text

Available Versions

OSU Journals (Oklahoma State University)