comparative skull osteology of karsenia koreana (amphibia ... et al 2010 osteology... ·...

Comparative Skull Osteology of Karsenia koreana(Amphibia, Caudata, Plethodontidae)

David Buckley,* Marvalee H. Wake, and David B. Wake

Department of Integrative Biology and Museum of Vertebrate Zoology, University of California,Berkeley, California 94720-3140

ABSTRACT The recent discovery of a plethodontid sal-amander, Karsenia koreana, in Korea challenged ourunderstanding of the biogeographic history of the familyPlethodontidae, by far the largest family of salamanders,which otherwise is distributed in the New World with afew European species. Molecular studies suggest thatKarsenia forms a clade with Hydromantes (sensu lato),which includes among its species the only other OldWorld plethodontids. We studied the skull of K. koreanaand compared it with that of other plethodontid genera,especially members of the subfamily Plethodontinae,which it resembles most closely in general anatomy. Theanatomy of its skull corresponds to the most generalizedand apparently ancestral condition for plethodontids. Noclearly autapomorphic states were detected, and no syn-apomorphies can be found that would link it to othergenera. The Karsenia skull is cylindrical and well ossi-fied, giving an impression of strength. In contrast, theskull of Hydromantes is highly derived; the skull is flat-tened and the bones are weakly ossified and articulated.Hydromantes and Karsenia share no unique anatomicalfeatures; differences between them are especially evi-dent in the hyobranchial skeleton, which is generalizedin Karsenia but highly modified in Hydromantes, whichis well known for its highly projectile tongue. Plethodonand Plethodon-like species, including Karsenia and to alesser degree Ensatina, represent the more generalizedand apparently ancestral plethodontid morphology. Spe-cialized morphologies have evolved along only a fewmorphological axes within the Plethodontidae, resultingin a pattern of rampant homoplasy. Our analysis of theanatomy of the new Asiatic lineage illuminates somepotential mechanisms underlying adaptive morphologi-cal evolution within the Plethodontidae. J. Morphol.271:533–558, 2010. � 2009 Wiley-Liss, Inc.

KEY WORDS: evolution; morphology; bones; lunglesssalamanders; hyobranchial apparatus

INTRODUCTION

The order Caudata comprises 583 species of sal-amanders (AmphibiaWeb, http://amphibiaweb.org/index.html, September 2009). The family Pletho-dontidae, with 394 species, is the most diversefamily, both in number of species and in ecologicaland morphological variability. Plethodontid sala-manders occupy a vast array of ecological niches,adapting to very different habitats (e.g., aquatic,fossorial, arboreal, stream, terrestrial or cave;

Wake, 1966). Most plethodontids lay eggs on land,which develop directly into miniatures of theadults without a larval stage. Species with the ba-sal amphibian biphasic life cycle, as well as pedo-morphic (permanently larval) forms, also occur,but at least in the Plethodontinae the larvae aresecondarily derived (e.g., species of Desmognathus;Chippindale et al., 2004; Mueller et al., 2004). De-spite morphological variability related to the eco-logical diversification of the group, synapomorphictraits characterize the family, such as the absencein adults of lungs, pterygoid and lacrimal bones,and the presence of a naso-labial groove and largeposterior patches of vomerine teeth (Wake, 1966).

Several principal evolutionary lineages are rec-ognized within the family, arrayed taxonomicallyin different groups depending on the authors (e.g.,Wake, 1966; Lombard and Wake, 1986; Chippin-dale et al., 2004; Mueller et al., 2004; Frost et al.,2006; Vieites et al., 2007). The most recent revisionof the group recognized two subfamilies withinPlethodontidae: i) Hemidactyliinae, which includesthe supergenus Bolitoglossa (12 genera; >250 spe-cies of tropical salamanders), the western NorthAmerican genus Batrachoseps (20 species), thetribe Spelerpini (Eastern North American species,genera Eurycea, Gyrinophilus, Pseudotriton, Ster-eochilus, and Urspelerpes), and the genus Hemi-dactylium (monotypic genus), the last a distinctlineage whose taxonomic position has been rathercontroversial; ii) Plethodontinae, which includesthe supergenus Desmognathus (genera Desmogna-thus and Phaeognathus), the North Americangenera Aneides, Ensatina, and Plethodon, the

Contract grant sponsor: National Science Foundation; Contractgrant number: EF-0334939.

*Correspondence to: David Buckley, Department of IntegrativeBiology and Museum of Vertebrate Zoology, 3060 Valley Life ScienceBuilding, University of California, Berkeley, CA 94720-3140.E-mail: [email protected]

Received 16 July 2009; Revised 1 October 2009;Accepted 5 October 2009

Published online 9 December 2009 inWiley InterScience (www.interscience.wiley.com)DOI: 10.1002/jmor.10816

JOURNAL OF MORPHOLOGY 271:533–558 (2010)

� 2009 WILEY-LISS, INC.

supergenus Hydromantes (genera Atylodes,Hydromantes, and Speleomantes), and the recentlydescribed genus Karsenia (Vieites et al., 2007).

Karsenia is a monotypic genus that contains theonly known Asiatic plethodontid, Karsenia kore-ana, recorded from only a few localities in SouthKorea, where individuals can be found under rockson the humid slopes of montane woodlands withlimestone soils (hardwoods and mixed hardwood/pine; Min et al., 2005). The species has the charac-teristic features of plethodontid salamanders (theabsence of lungs, pterygoid and lacrimal bones inadults, and the presence of a naso-labial grooveand large posterior patches of vomerine teeth).The first molecular analyses carried out confirmedthe singularity of the new lineage (Min et al.,2005). This, together with some morphological par-ticularities such as an attached protrusible tongueand a derived tarsus, as well as its geographic dis-tribution, led to the description of a new genus forthe species (Min et al., 2005). A thorough molecu-lar study confirmed the inclusion of K. koreanawithin the plethodontine salamanders (Vieiteset al., 2007). In that phylogenetic analysis, Karse-nia forms a clade with the species from the super-genus Hydromantes, the clade being sister to theremaining plethodontines (see Fig. 1). Further-more, K. koreana shares synapomorphic karyologi-cal characteristics with Hydromantes (Sessionset al., 2008).

Plethodontid salamanders are distributed pri-marily in the New World (99% of species). Most ofthe species are found in North and Middle Amer-ica, with the exception of the eight that occur inthe Mediterranean region. Several hypotheseshave been proposed to explain the current geo-graphic distribution and the patterns of diversifi-cation in Plethodontidae (e.g., Wilder and Dunn,1920; Wake, 1966, 1987). However, these evolu-tionary and biogeographic scenarios were chal-lenged by the discovery of the Asian species Karse-nia koreana (Min et al., 2005; Vieites et al., 2007).This discovery has led to an acceptance of a postu-lated early connection across the Bering Straitbetween species in western North America andtheir relatives in Western Europe.

In addition to its relevance for recovering thebiogeographic history of the family, K. koreanamay also play an important role in understandingthe patterns of morphological evolution and ecolog-ical diversification within the group. Plethodontidsalamanders are the most speciose and diversifiedgroup of salamanders, but the diversity and dis-parity of forms are unevenly distributed withinthe family (Wake, 1966). Levels of specializationand speciation are not directly correlated, andhighly specialized and generalist forms coexistwithin the different plethodontid lineages. Thegeneral morphology of the group is highly con-served, and the specialized forms have diversified

along a few similar morphological axes (Wake andLarson, 1987; Wake, 1991). Recurrent evolution ofsimilar morphological traits across lineages, i.e.homoplasy, is a common theme among the Pletho-dontidae (Wake, 1991).

Given the singularity and importance of the newlineage, we describe the osteology of the skull of K.koreana. We compare the results with the charac-teristics of other members of the Plethodontinae(Hydromantes, Aneides, Ensatina, Plethodon, Des-mognathus, and Phaeognathus). Superficially, Kar-senia resembles members of Plethodon, as well asfemale Aneides hardii, and such members of Des-mognathus as D. ochrophaeus and relatives, butwe focus especially on Hydromantes because of itsputative close phylogenetic relationship and itshypothetically shared biogeographic history. So far,little is known about the natural history, biology,morphological variability, and anatomical charac-teristics of K. koreana, so a detailed and compara-tive anatomical description may shed some lighton the biology and evolution of the species. Wealso discuss the results in terms of the morphologi-cal variability, biology, and evolution of plethodon-tid salamanders in the framework of the molecule-based phylogenetic hypotheses recently proposed.

MATERIALS AND METHODS

Descriptions are based on high-resolution X-ray CT (HRXCT)scans of Karsenia koreana (DRV 5033, 50.0 snout-vent length(SVL) mm, female, Sanan-Ri, South Korea) and Hydromantesplatycephalus (SMR 271, 67.2 mm SVL, male, Inyo Creek, InyoCounty, CA) performed at the HRXCT Facility at The Univer-sity of Texas (Austin). The specimen of K. koreana was scannedunder the following conditions. A FeinFocus microfocal X-raysource operating at 180 kV, 0.13 mA, and with no filter wasused. The source-to-object distance was 39 mm. For each slice,1,400 views were taken, with four samples per view. The fieldof image reconstruction was 9 mm, with an offset of 6,500 anda reconstruction scale of 4,600. The final dataset consisted of

Fig. 1. Phylogenetic relationships within Plethodontinae.The phylogenetic tree has been simplified from Vieites et al.(2007) and is based on nuclear DNA markers. Karsenia, theonly Asiatic plethodontid, is sister to the species of Hydro-mantes, which occur in North America and Europe. Theremaining plethodontine and hemidactyliine species are distrib-uted in the New World from southern Canada to Bolivia.

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675 slices gathered at a resolution of 1024 3 1024 pixels, withan inplane resolution of 9 lm per pixel. For the H. platycepha-lus specimen, the scanning conditions were as follows. TheFeinFocus microfocal X-ray source operated at 200 kV, 0.15 mA,and with no filter. The source-to-object distance was 55 mm.For each slice, 1,800 views were taken, with three samples perview. The field of image reconstruction was 16 mm, with an off-set of 4,100 and a reconstruction scale of 4,500. The final data-set consisted of 559 slices gathered at a resolution of 1024 31024 pixels, with an inplane resolution of 15.625 lm per pixel.The descriptions of the specimens scanned were supplementedby the study of six cleared and bone-and-cartilage-stained K.koreana (DRV 5019, 5029, 5551, 5553, 5555, 5558, Jangtae Sanand Sanan-Ri, South Korea) and two H. platycephalus (MVZ197502, 197506, Tuolumne County, CA). We compared thescanned specimens closely with the cleared individuals and,unless explicitly noted, the cleared specimens have the samemorphology as reported for the scanned specimen. Data onontogenetic or population variability of the structures describedcannot yet be provided. All the specimens studied are or will bedeposited in the Herpetological Collection of the Museum ofVertebrate Zoology (MVZ), U. C. Berkeley, and in the Herpeto-logical Collection of Southern Illinois University (SIUC).We present detailed descriptions and comparisons between

Karsenia and Hydromantes, and we contrast the skulls of thesegenera with those of the remaining plethodontines. The taxon-omy of the Hydromantes group is unstable, and Hydromanteshas been considered by different authors as a supergenus con-taining the genera Hydromantes, Speleomantes, and Atylodes(Vieites et al., 2007) and as a genus containing three subgenera(e.g., Wake et al., 2005; van der Meijden et al., 2009), but anequally acceptable taxonomy is to recognize two genera, Hydro-mantes and Speleomantes, the latter containing two subgenera(Speleomantes and Atylodes) (Crochet, 2007). The results pre-sented here are neutral with respect to taxonomy, and we findit most convenient to refer to Hydromantes (sensu lato) as aclade containing American species (Hydromantes in a restrictedsense) and European taxa (Speleomantes and Atylodes). Forcomparison with other plethodontines (Aneides, Desmognathus,Ensatina, Phaeognathus, and Plethodon), we use the publishedcomparative osteological descriptions by Wake (1963, 1966), inaddition to studies of individual genera: Aneides (Wake et al.,1983b), Hydromantes (Wiedersheim, 1875; Adams, 1942; Hilton,1945; Lanza et al., 1995), Desmognathus (Means, 1974). Werefer to Phaeognathus and Desmognathus collectively as des-mognathines. We made new observations of plethodontine taxausing the cleared and stained specimens from the collections ofthe Museum of Vertebrate Zoology, and we studied on-line CTscans of Aneides lugubris and Phaeognathus hubrichti (http://digimorph.org/). All comparative statements refer to the focaltaxon in relation to Karsenia. For the description of the anat-omy, we follow the anatomical nomenclature suggested on theAmphibian Anatomical Ontology web site (Leopold et al., 2007;Maglia et al., 2007), based largely on Francis (1934).Segmentation of the individual elements of the skull was per-

formed by tracing the sutures in the original scans, and thenreconstructing the images in three dimensions using VGStudioMAX1 1.2 (Volume Graphics, Heidelberg, Germany). Right-sideelements were segmented for paired structures. Measurementsof structures and angles were taken with the software ImageJ1.4.1 (Rasband, 2008). Contrast and brightness of the pictureswere modified in Adobe Photoshop1 7.0 (San Jose, CA).All reconstructions and labeled images will be available on

the DigiMorph website (http://digimorph.org/). High resolutionX-ray CT scans of Aneides lugubris and Phaeognathus hubrichtiare also available on the website.

RESULTS

The skull of Karsenia koreana is oval in shape,robust, and well ossified. The skull is fully articu-lated and scantly ornamented (see Fig. 2). Longitu-

dinally, the skull measures 8.1 mm from the ante-riormost tips of the premaxillae to the posteriorends of the occipital condyles. The maximumheight is 3 mm (dorsomedial articulation of frontaland parietal to the transverse plane defined by theventral surface of the dentaries), and the widesttransverse expanse of the skull is 6 mm at thelevel of the anterior ends of the coronoid processesof the prearticulars.

The skull is divided into three areas for descrip-tive purposes. First, the olfactory capsules andinvesting bones, forming the facial area, palateand upper jaws, represent one fourth of the totallength of the skull. The face is broadly roundedand it rises abruptly in the lateral plane, beingslightly rounded anteriorly; the robust alary proc-esses of the premaxillae, which rise almost perpen-dicularly, are responsible for the slight curvature.The curvature is more pronounced in the trans-verse plane, and is defined by the lateral surfacesof the nasals and the pars facialis of the maxillae,which are oriented ventrolaterally at a 608 angle(Fig. 2C,E). The second region, comprising largeorbits and the anterior braincase with its investingbones, occupies one half of the skull and is definedby the frontals, the parietals, the parasphenoid,and the orbitosphenoids. The frontals and parie-tals cover the dorsal braincase and are more orless parallel with the ventral parasphenoid, andthe lateral surfaces of the braincase are formed bythe orbitosphenoids (which articulate dorsally withthe frontals and parietals and ventrally with theparasphenoid; Fig. 2C). The otic capsules and theoccipital complex represent the third area and theremaining one fourth of the skull. The otic capsu-les are rounded and not very prominent. They donot reach the level of the dorsal frontal-parietalsurface in height. The squamosals project antero-ventrally from the otic capsules toward the articu-lars, forming a 458 angle with the midline of theskull in the dorsal plane and a 338 angle with themidsagittal plane. Finally, the mandible is rela-tively stout and planar, incorporating dentariesand prearticulars.

In comparison with Karsenia, the skull ofHydromantes platycephalus is less well ossifiedand more loosely articulated. Proportionally, theskull is wider, flatter, and less robust (see Fig. 2);it is almost spherical in frontal section (Fig. 2B)and compressed dorsoventrally. Longitudinally, theskull measures 12 mm from the anteriormost tipsof the premaxillae to the posterior ends of the occi-pital condyles. The maximum height is 4.5 mm(dorsomedial articulation of frontal and parietal tothe transverse plane defined by the ventral surfaceof the dentaries), and the widest transverseexpanse of the skull is 11 mm at the level of theposterior ends of the maxillae. The nasal capsulesare poorly ossified and less robust. The alary proc-esses of the premaxillae project vertically and

Karsenia koreana SKULL OSTEOLOGY 535


slightly anteriorly in the lateral plane, so the cur-vature is minimal. The anterior braincase regionis more compressed, especially anteriorly, and theinvesting bones are less planar. The orbitosphe-noids increase in height anteroposteriorly. The or-bital vacuity is proportionally larger and wider.The otic-occipital area is the most robust part of

the skull. The otic capsules are proportionallyhigher, more prominent and better ossified. Giventhe wider mandibular arch, the squamosals projecttoward the articulars with a different inclination,forming a 618 angle with the midline of the skullin the dorsal plane and a 498 angle in the midsa-gittal plane. The squamosals are spread more lat-

Fig. 2. General overview of the skull of Karsenia koreana (left panels: A, C, E) and Hydro-mantes platycephalus (right panels: B, D, F) in dorsal (A, B), lateral (C, D), and frontal (E, F)views, respectively (scale bars: A, C, E 5 2 mm; B, D, F 5 3 mm).



erally in the dorsal plane and less vertically in thetransverse plane. The mandibular arch is orientedventrodorsally in the lateral plane (108 angle).

Premaxillae

Premaxillae are paired structures that are wellarticulated with each other at the anteriormostend of the skull (Fig. 3A,C). Premaxillae havethree distinct regions. 1) The pars dentalis corre-sponds to the toothed area that forms the anteriorend of the maxillary arch. In the specimenscanned, the premaxillary dentition consists ofseven teeth on each bone (see ‘‘Dentition’’ section).The pars dentalis forms a rectangular trapezoid inthe transverse plane. The longest edge of the tra-pezoid corresponds to the toothed area. Medially,the two premaxillae contact squarely, whereas aslender and toothless projection of the maxillaoverlaps the flattened lateral ends. 2) The alaryprocess (pars facialis) projects posterodorsally, firstarising vertically as a robust, flattened column,then curving posteriorly and broadening into aflattened wing-like structure that overlaps the fa-cial part of the frontal bone. The alary processes ofthe two premaxillae define the lateral borders ofan oval fontanelle. The flattened portion of thealary process articulates medially with its counter-part, laterally with the nasal, and posteriorly withthe frontal. The contact between the posteriorends of the premaxillae and the frontals forms anapparent concavity, in which the ‘‘nasal gland’’ islocated. 3) The pars palatina consists of a small,flat surface that projects perpendicularly from thelongest edge of the pars dentalis to the internalcavity of the cranium. The pars palatina articu-lates laterally with the lingual edge of the maxilla.The posterior edge of the pars palatina articulateswith the anterior margin of the body of the vomer(Fig. 3A,C).

In Hydromantes platycephalus, the premaxillaeare also paired structures that are not tightlyarticulated medially with each other (Fig. 3B,D).The pars dentalis is more rectangular and propor-tionally longer than in K. koreana, articulatingsquarely with its counterpart. The pars palatina isreduced, forming a small irregular shelf, moreexpanded at the posterolateral end. It does notcontact the vomer. The lateral ends of the parsdentalis and the pars palatina merge and form asmall tongue-and-groove articulation with the an-terior end of the maxilla. The alary process isshort and thin, perpendicular to the pars dentalis,and only slightly bent posteriorly. Along its pos-terolateral border, it has a reduced articulationwith the medial border of the anterior end of thenasal. The alary processes of the premaxillae fallshort of the frontal bones and do not contact eachother posteriorly; they slightly overlap or lie imme-diately medial to anteromedial portions of the

nasals, and a large fontanelle occurs betweenthem. In European Hydromantes, the alary processis considerably longer and is expanded and flat-tened posteriorly, where it typically slightly over-laps the anteromedial process of the frontal (exceptin H. italicus, where overlap is found in only 40%of specimens; Lanza et al., 1995).

Premaxillae of Plethodon and Ensatina gener-ally resemble those of Karsenia; they are fusedmedially in Aneides, Phaeognathus, and Desmog-nathus. In some Aneides and desmognathines, thealary processes become massive and fuse to form alarge flat plate that can become heavily co-ossifiedwith the skin in both Phaeognathus and largerAneides (Wake, 1966; Means, 1974). The Europeanspecies of Hydromantes differ from the Americanspecies in having much larger alary processes thatare often expanded into wing-like structures thatreach the frontal bones in all species except H. ita-licus, in which 60% of specimens have alary proc-esses that fall short of the frontals (Adams, 1942;Wake, 1966; Lanza et al., 1995). Hydromantes dif-fers from all other genera in that the alary proc-esses never contact each other behind the fonta-nelle.

Maxillae

These paired bones, together with the anterome-dial premaxillae, form the upper jaw skeleton (Fig.3A,E,G). Three regions are recognized. 1) The elon-gated pars dentalis extends approximately half thelength of the optic fenestra. The entire extent istoothed. The anteriormost part overlaps the poste-rior area of the pars dentalis of the premaxilla.The posterior part connects to the palatopterygoidcartilage by means of the jugal ligament. 2) Thepars facialis, an ascendant process from the parsdentalis, separates the nasal cavity and the opticfenestra. The pars facialis is trapezoidal in shape;its posterodorsal edge overlaps the prefrontal. Ithas a small extension directed anteriorly andpointing toward the dorsoventral edge of the nasal,but without contacting it. 3) The pars palatina is aflattened plate that extends from the pars dentalisinto the oral cavity. It articulates with the parspalatina of the premaxilla and with the vomer, to-gether forming the roof of the palate area.

Maxillae in H. platycephalus are less robustthan in K. koreana (Fig. 3B,F,H). The pars dentalisis similar in length, extending to the middle of theoptic fenestra, and is fully toothed. The pars facia-lis is narrowly triangular and concave, the poste-rior tip of the triangle overlapping the lateralmostedge of the nasals and the partly disconnected an-terior part of the frontal (see later for descriptionof the bipartite frontal in Hydromantes). The ante-riorly directed process of the pars facialis isabsent. The pars palatina is much reduced; it doesnot contact the vomer at any point. Accordingly,



Fig. 3. Premaxillae, maxillae, and septomaxillae in K. koreana (left panels: A, C, E, G) and H. platycephalus (right panels: B,D, F, H). A, B: Frontolateral view of the skulls. Note the articulation in K. koreana between the septomaxilla and the prefrontal,and between the premaxilla, maxilla and vomer (A), articulations absent in H. platycephalus (B). C: Anterior (a), medial (m), andposterior (p) views of the premaxilla in K. koreana. D: Anterior (a), medial (m), and posterior (p) views of the premaxilla in H. pla-tycephalus. E, G: Lateral and medial views of the maxilla in K. koreana, respectively. F, H: Lateral and medial views of the maxillain H. platycephalus, respectively. appm, alary process of the premaxilla; m, maxilla; n, nasal; nld, nasolacrimal duct; pdpm, parsdentalis of the premaxilla; pdm, pars dentalis of the maxilla; pf, prefrontal; pfm, pars facialis of the maxilla; pppm, pars palatinaof the premaxilla; ppm, pars palatina of the maxilla; pm, premaxilla; sm, septomaxilla; v, vomer (scale bars: A, C, E, G 5 1 mm; B,D, F, H 5 2 mm).



the anterior palate is incomplete and the body ofthe vomer is weakly connected, if at all, to lateralparts of the palate. In European Hydromantes, thepars facialis is rectangular rather than triangularand much shorter, barely contacting the nasal andwell separated by a distinct gap from the frontal(Adams, 1942; Wake, 1966; Lanza et al., 1995).

Maxillaries of other plethodontines generallyresemble those of Karsenia, especially those of Ple-thodon and Ensatina, although the pars dentalisof Ensatina is longer and more slender. The parsfacialis of Ensatina is small and articulates onlyweakly, if at all, with the prefrontal. Maxillae ofAneides are much stouter and are more complexlyarticulated with the prefrontals and nasals; thepars dentalis is massive in the larger species andin males of smaller ones and bears enlarged teethanteriorly, whereas posteriorly it is expanded dor-soventrally and is edentulous (Wake, 1963, 1966;Wake et al., 1983b). The maxillae of desmogna-thines are stout and well articulated via the parsfacialis directly to the frontal, which it broadlyoverlaps. In Phaeognathus there is a very large,stout process that extends posteromedially, almostas far as the quadrate bone, into the ligament thatconnects the bone to the suspensorium (Wake,1966).

Septomaxillae

These paired bones, embedded in the cartilagesof the nasal capsules at the lateral edge of thenasal vacuity, are small and irregular in shape.The anteriormost part is somewhat triangular andprojects anteriorly in the dorsolateral part of thenasal cavity (Fig. 3A). The small anterior exten-sion of the pars facialis of the maxilla partiallycovers the septomaxilla. The septomaxilla articu-lates dorsally with the prefrontal at the anterioredge of the nasolacrimal duct, which passesthrough its posterior margin.

In H. platycephalus, the septomaxillae also arepaired structures, irregular in shape and smallerthan in Karsenia (Fig. 3B). The bones are weaklyossified and do not articulate with or otherwisecontact any other bone.

Septomaxillae are typically present in all pletho-dontines, but usually they are smaller than inKarsenia. They are especially small in desmogna-thines. The bones are weakly developed in Euro-pean Hydromantes and can be absent entirely (asmany as 60% of H. italicus), absent on one side, orreduced in degree of ossification (Lanza et al.,1995).

Nasals

These paired bones are triangular in shape. Thebase of the triangle forms the dorsal part of thenasal capsule, and the vertex points posterodor-

sally (Fig. 4A). The nasal is slightly convex andpresents an irregular surface. A foramen is pres-ent in the medial part of the bone, presumably forpassage of the profundus branch of nerve V. Thenasal articulates mesially with the premaxilla andfrontal; laterally, it articulates with the prefrontal,which separates it from the maxilla.

In H. platycephalus, nasals are more irregular,somewhat rectangular, and less well ossified (Fig.4B). The nasal has a medial projection thatextends anteriorly, contacting the alary process ofthe premaxilla. Laterally, the nasal articulateswith the pars facialis of the maxilla. Anteriorly,the lateral margin of the nasal is notched, forminga partial foramen for the nasolacrimal duct.Nasals are larger and more elongated, usually lon-ger than broad, in European Hydromantes.

Nasals are roughly similar in all plethodontinesbut they are very small and packed between largerbones (e.g., well articulated to the pars facialis ofthe maxilla and the alary process of the premax-illa) in desmognathines. Shape varies (often spe-cific to a given species) from triangular to quad-rangular or pentagonal, and the degree of articula-tion with the pars facialis of the maxillary variesfrom close to none among species.

Prefrontals

Prefrontals are paired bones, oval and slightlyconvex, that are irregular in shape. They partiallyto completely fill the gaps between the orbit andthe nasal vacuity, and between the frontal and thepars facialis of the maxilla (Fig. 4A). They aresmaller than the nasals. The nasolacrimal ductpasses through an elongate foramen in the ante-rior part of the prefrontal that is usually notenclosed in bone anteriorly. The prefrontal articu-lates anteriorly with the septomaxilla and latero-ventrally with the pars facialis of the maxilla. Theprefrontal is overlapped laterodorsally by thenasal; posteriorly, it broadly overlaps the frontals.

Prefrontals have been reported consistently asabsent in Hydromantes (Adams, 1942; Wake, 1966;Lanza et al., 1995). In the specimen scanned, how-ever, the anteriormost part of the frontal seemsdifferentiated as a distinct element (Fig. 4B). Thisputative element occupies space that representsthe anterior part of the frontal and at least part ofthe prefrontal (in the sense that it is overlappedby the pars facialis of the maxilla). It is not wellossified; the contact between anterior and posteriorparts of the frontal is not clearly delimited. An in-cipient break in the bone extends from the mid-line, well in advance of the orbits, posterolaterallyat about a 458 angle to the extreme anterolateralborder of the orbit. Zones of weak ossification cor-respond only roughly to the prefrontal because theanterior element extends to the midline, which dif-fers from prefrontals in all other salamanders. The



anterior element is posterior to the nasal and isirregular in shape (Fig. 4B). Long but very slenderanterior projections are present medially andshorter ones laterally, but the latter does not sepa-rate the nasal from the pars facialis of the maxilla,as is typical of prefrontals in many taxa (Wake,

1966). The developmental origin of this putativeelement should be further explored to clarify theidentity and homology of the structure.

Prefrontals are absent in desmognathines inwhich they are thought to be incorporated intoexpanded facial lobes of the frontal (Wake, 1966).

Fig. 4. Dorsolateral views of the skulls of K. koreana (A) and H. platycephalus (B), showing the articulations between, nasals,prefrontals, frontals, and parietals. An enlarged dorsal view of the nasal and prefrontal is provided. Prefrontals have been consis-tently reported absent in Hydromantes. In the specimen scanned, however, a differentiated element is found between frontals andnasal (pf in B). appm, alary process of the premaxilla; f, frontal; fpf, frontoparietal fontanelle; m, maxilla; n, nasal; nld, nasolacri-mal duct; os, orbitosphenoid; p, parietal; pdm, pars dentalis of the maxilla; pdpm, pars dentalis of the premaxilla; pf, prefrontal;ps, parasphenoid; sm, septomaxilla (scale bars: A 5 1 mm; B 5 2 mm).



The bones are well developed in Aneides, and inthe western species they are involved in a complexinterlocking articulation with the pars facialis ofthe maxilla. The bones of Ensatina and Plethodonresemble those of Karsenia.

Frontals

These are long, paired bones, which, togetherwith the parietals, form the roof of the cranial cav-ity (Fig. 4A). The frontal is rectangular in shape,although its anterior third is broader than the restof the bone. It is slightly convex and has a smoothsurface. Frontals articulate mesially with theircounterparts but do not fuse. The premaxilla,nasal, and prefrontal overlap the enlarged anteri-ormost part of the frontal. The lateral edges of thefrontal turn down laterally, articulating with theorbitosphenoid (Fig. 6A). Frontals articulate poste-riorly with parietals, slightly overlapping them lat-eroventrally. The articulation is not square, butthe contact between frontals and parietals doesnot leave a conspicuous frontoparietal fontanellein adults.

Frontals in H. platycephalus are rectangularstructures, enlarged anteriorly (Fig. 4B). They arepoorly ossified, especially medially and posteriorly,and the anterior part is weakly connected to theinterorbital part of the bone (see earlier, prefron-tal). The frontals do not articulate either withtheir counterparts or posteriomedially with theparietals, leaving a conspicuous frontoparietal fon-tanelle that has a shape reminiscent of a fleur-de-lys. Laterally, frontals articulate with the dorsalsides of the orbitosphenoids (Fig. 6C). This articu-lation extends through the anterior half of theorbitosphenoids. Posterolaterally, the frontals over-lap the parietals. In American Hydromantes, afrontal lobe extends anterolaterally, overlappedextensively by the tip of the triangular pars facia-lis of the maxilla. The lobes are absent in Euro-pean Hydromantes, but in some individuals thefrontals extend as far as the reduced pars facialisof the maxillae.

The frontals are well-ossified, large bones in ple-thodontines. They are particularly large and stoutwith expanded anterior portions in desmogna-thines, which lack prefrontals. Desmognathinesare unique in that the frontals have ventrolateralprocesses that invade the antorbital region, in thefront of the orbit between the prefrontals and pala-tal parts of the maxillae. The frontals are rela-tively massive, especially in Phaeognathus, andthey extend beyond the posterior margins of theorbitosphenoids. Usually small, diamond-shapedfontanelles separate the frontals from each otherand the parietals except in desmognathines andlarger Aneides. All of the anterior cranial elementsof Phaeognathus and Aneides lugubris (and to alesser extent A. flavipunctatus) are heavily rugose

with co-ossified skin. There is a discrete posteriorboundary in the middle of the frontals that corre-sponds to the anterior extent of the mandibularadductor muscles.

Parietals

The parietals are large, rectangular, pairedbones that cover the posterior braincase. The pari-etal is shorter than the frontal and its surface isalso more irregular (Fig. 4A). The ventrolateralborder is curved downward where it contacts theorbitosphenoid and covers the dorsal surface of theascending process of the palatoquadrate cartilageat the posterior end of the orbitosphenoid (Fig.6A). This lateral face of the parietal is more con-spicuous than that of the frontal. The anterior halfof the parietal contacts the orbitosphenoid fromthe optic fenestra to its posterior end. The broadlycurved, posterior border has complex articulations.The ventrolateral border is thickened and becomesclawlike in transverse section, articulating withinthe claw first with the ascending process and moreposteriorly with the inner margins of the otic cap-sule. The lateral edge becomes thinner posteriorlyand conforms to the medial portions of the oticcapsule. The anterior surface of the parietal formsa low dome, whereas the posterior surface, in frontof the otic capsule, is depressed and forms a broadgroove that accommodates the portion of the man-dibular adductor musculature that extends fromthe atlas vertebra to the mandible. In the scannedspecimen, there appears to be a significant gapbetween the two parietals, but in the five cleared-and-stained individuals there is no gap and thebones are sutured. In one instance, there is a clearoverlap between the bilateral counterparts. Thescanned specimen also displays a small gapbetween the frontals and the parietals, but thereis no gap in the cleared specimens (the scannedand the cleared specimens are all similar in size).The frontals overlap the parietals, especially later-ally.

In H. platycephalus, parietals are poorly ossifiedanteromedially and medially (Fig. 4A). The antero-lateral edge of each parietal projects anteriorlyand is overlapped by the frontal. Laterally, the pa-rietal does not contact the orbitosphenoid except atits posterior end (Fig. 6C). Posteriorly, the parietalenvelops the anterior half of the otic capsule. Com-pared with Karsenia, the bone is thinner, flatter,and less domed, and the depressed groove accom-modating mandibular adductor musculature is lessconspicuous.

The parietals of Plethodon and Ensatina aresimilar to Karsenia, whereas those of Aneides dif-fer mainly in having a more conspicuous postero-lateral depression. The paired bones in Aneidesare tightly sutured and become fused in largespecimens of the larger species. Parietals of des-



mognathines differ mainly in being more massiveand in having even more conspicuous adductordepressions. This reaches an extreme in Phaeogna-thus, in which the anteromedial portions of theoccipito-otic participate in the pronounced depres-sion, with the articulation between parietal andoccipito-otic lying at the midpoint of the depres-sion. The parietal and the occipito-otic are drawnout into a large ventrolateral tab that extends theosseous depression for the atlantomandibular liga-ment, which appears to be unique to desmogna-thines. The two parietals are strongly sutured indesmognathines. In Desmognathus, but to a lesserextent in Phaeognathus, the two parts of the bonecontrast strongly. The bones are relatively shortand the anterior half is high, flat, and smooth,whereas the posterior half is strongly depressed.The bones are tightly articulated to the frontalsand the occipito-otics.

Vomers

The vomers are paired bones that, together withthe pars palatina of the maxillae and premaxillae,form the anterodorsal part of the roof of the oralcavity (Fig. 5A,C,E). Four areas are distinguished.1) The anterior flattened body articulates squarelywith the maxilla and the premaxilla and projectsposterodorsally at a 458 angle. The anterior bodydoes not articulate with its counterpart, leaving aninternasal space between them. The mesial edge ofthe anterior body surrounding the internasal spaceis turned up, forming a septum-like process thatincreases in height posteriorly. 2) A short andbroad posterior projection proceeds posteriorlyfrom the vomerine body. Its ventrolateral edge sur-rounds the internal nares. The projection articu-lates posteromedially with its counterparts. Themedial posterior edge of the projection overlapsthe anterior edge of the parasphenoid. A topo-graphically limited articulation occurs between thelateral posteroventral part of the vomer and theanteroventral end of the orbitosphenoid (Figs.5A,E and 6B). 3) A conspicuous dentigerous ridge(dentigerous process, including a preorbital pro-cess) extends laterally from the posterior projec-tion toward, but falls short of, the lateral marginof the vomerine body, posterior to the internal na-res. 4) A posterior vomerine dental patch is consti-tuted by two patches that meet at the midline,separated from the vomers proper. The patches aredrop-shaped and constitute a dense extension ofvomerine teeth (see ‘‘Dentition’’ section for adetailed description). The patches, attached (butnot fused) to the ventral surface of the parasphe-noid, are separated from the dentigerous processby a narrow gap.

The anterior part of the main body of the vomerin H. platycephalus is not as well ossified as thatof K. koreana and does not contact the pars pala-

tina of the premaxilla and the maxilla (Fig.5B,D,F). The vomerine body projects posterodor-sally at a 458 angle. The curved, septum-like pro-cess on the medial border is absent, and the inter-nasal space is proportionally larger than in K.koreana. The posterior projection from the mainbody is slightly curved ventrally. The vomer doesnot articulate with its counterpart in this malespecimen. However, in females, there are articula-tions with the maxilla and premaxilla and alsowith its counterpart by means of portions of theposterior projections (Adams, 1942). The projectionarticulates posteriorly with the anteriormost endof the parasphenoid, but there is no contactbetween the vomer and the orbitosphenoid (Figs.5B and 6D). The dentigerous process projects ante-riorly toward the vomerine body; its lengthexceeds the width of the body. The posterior vo-merine dental patches are more reduced thanthose of K. koreana. They are restricted to twonarrow, widely separated strips of teeth, locatedposterolaterally on the ventral surface of the para-sphenoid (Fig. 5F). The teeth occupy barely 20% ofthe total surface of the parasphenoid, and they areseparated from the dentigerous process by a widegap, three times as great as in Karsenia.

Vomers of Plethodon, Ensatina, and Aneidesclosely resemble those of Karsenia in mostrespects. In large Aneides, the septum-like dorso-medial margin of the body may articulate with theventral surface of the alary process of the premax-illa. The bilateral counterparts articulate witheach other for the posterior half of their extent.Preorbital processes of the dentigerous processtypically fall short of the lateral extent of thevomer body, but in Ensatina, the process is espe-cially long and exceeds the lateral extent of thebody. Species of Aneides differ in structure of thepreorbital process, which is absent entirely inwestern species. The gap between the dentigerousprocess and the posterior tooth patch is typicallygreater than in Karsenia, but less than in Hydro-mantes; however in Ensatina, the gap is less andmay be completely closed. The posterior patchesare not in contact and are especially widely sepa-rated in Ensatina. The vomers of desmognathineshave features not found in other plethodontinesand also display much variability related to size oforganisms, sex, and habitat. The vomers are gen-erally robust and are tightly articulated to eachother. The internasal space is subject to much var-iation; in the most aquatic, largest species it ismuch reduced in size and the articulation of thebilateral counterparts is nearly complete. The pre-orbital process usually has few or no teeth and abony plate extends posterolaterally from the dentalarcade. The preorbital process usually falls farshort of the lateral extent of the body. The processmay articulate slightly with the peculiar antorbitalossification of desmognathines. The posterior tooth



Fig. 5. Vomers in K. koreana (left panels: A, C, E) and H. platycephalus (right panels: B, D, F). A, B: Frontal sections, showingthe dorsal surfaces of the vomers and their articulation with premaxillae, maxillae, parasphenoid, and orbitosphenoids. C, D: Dor-sal (d) and ventral (v) view of the isolated right vomers. E, F: Ventral view of the skulls, showing the ventral disposition of thevomers, and the two posterior vomerine dental patches, attached to the parasphenoid. appm, alary process of the premaxilla; c,choana; dr, dentigerous ridge; m, maxilla; n, nasal; nld, nasolacrimal duct; pdm, pars dentalis of the maxilla; pdpm, pars dentalisof the premaxilla; pf, prefrontal; v, vomer; vb, anterior vomerine body; vdp, vomerine dental patch (scale bars: A 5 1 mm; B 5 2mm; C 5 0.5 mm; D 5 1 mm; E 5 1 mm; F 5 2 mm).



patches are relatively small and are widely sepa-rated from the dentigerous portion of the vomerand from each other.

Orbitosphenoid

These paired rectangular bones are disposed ver-tically in an anterior–posterior direction (Fig.6A,B). They form the lateral sides of the braincase.They are widely separated dorsally and ventrally,and they do not contact each other at any point.Although mainly vertical, they are closer togetherventrally than dorsally so that the braincase istrapezoidal in shape anteriorly (Fig. 6B). Theinner surface is slightly concave, and the structureis thicker at the anterior and posterior borders.The bone increases in height from the anterioredge to its medial part, decreasing toward its pos-terior margin. Three foramina for cranial nerves

are present (Fig. 6A). The anterior border consistsof three projections (one dorsally and two ven-trally) that partially encircle the opening of the fo-ramen orbitonasale mediale. A conspicuous opticfenestra lies in the posterior third of the orbitos-phenoid. Very large and completely surrounded bybone, it opens at about the level of the articulationof the frontals and parietals. The third foramen, asmall foramen oculomotorium, opens posterior tothe optic fenestra and close to the posterior marginof the orbitosphenoid. The anteriormost lateraland ventral margins of the orbitosphenoid contactthe posterior edges of the vomers. With the excep-tion of this anterior contact, the ventral surface ofthe orbitosphenoid contacts the dorsal surface ofthe parasphenoid (Fig. 6B). Dorsally, the orbitos-phenoid articulates with the frontal and parietal.

The orbitosphenoids in H. platycephalus aremore curved and inclined laterally, the cranial cav-

Fig. 6. Braincase in K. koreana (A, B) and H. platycephalus (C, D). A, C: Lateral view of the skulls, showing the orbitosphe-noids and their contact and articulation with vomers, parasphenoid, frontals, and parietals. B, D: Transverse section of the skulls,about the level of the anterior end of the orbitosphenoids. The braincases in the two species are very different in shape. Note alsothe absence of contact between vomers and orbitosphenoids in H. platycephalus. f, frontal; foc, foramen oculomotorium; fom, fora-men orbitonasale mediale; of, optic fenestra; os, orbitosphenoid; p, parietal; ps, parasphenoid; v, vomer (scale bars: A, B 5 1 mm; C,D 5 2 mm).



ity being more oval and flattened (Fig. 6C). The fo-ramen orbitonasale mediale is not evident in theanterior part of the orbitosphenoid, and only aslight indication of the anterior part of the fora-men oculomotorium is evident at the posterior endof the bone. A conspicuous optic fenestra occupiesthe posterior area of the orbitosphenoids. The orbi-tosphenoid articulates ventrally with the anteriorhalf of the parasphenoid; it does not contact thevomer anteriorly (Fig. 6D). The anterior half of thedorsal surface of the orbitosphenoid articulates lat-erally with the frontal; the posterior half approxi-mates the parietal, although it contacts only at theposterolateral end.

Orbitosphenoids are basically similar in all ple-thodontines, differing mainly in size and degree ofrobustness. In Aneides lugubris, the bilateral coun-terparts are in contact posteroventrally.

Parasphenoid

The parasphenoid is an unpaired, median, sym-metrical bone, which forms the ventral surface ofthe braincase. Elongated and semirectangular, thebone is square and narrow at the anterior marginand wider and more rounded at its posterior end(Fig. 5E). Its anteriormost margin is thin and flat,but becomes dorsally concave toward the posteriormargin. Several foramina perforate the lateralmargin of the parasphenoid in the third quarter ofits length. One of these may be the carotid canal,which is not well defined in salamanders; alterna-tively, all three might carry different branches ofthe internal carotid. Ventrally, the parasphenoidsustains the vomerine tooth patch, which occupies�85% of its surface. The parasphenoid articulateslaterally with the orbitosphenoids. The posterioredges curve dorsally, enveloping the anterior bor-ders of the occipito-otic. The posterior end of thebone is expanded dorsoventrally and serves as theattachment for subvertebral muscles.

The parasphenoid in H. platycephalus is nearlytriangular, with a narrow anterior end (Fig. 5F). It isflat anteriorly, but quickly becomes internally con-cave, especially at the level of the area occupied bythe vomerine tooth patches. The posterodorsal endsarticulate with much of the occipito-otic complex.

Plethodontines do not differ much with respectto the parasphenoid, but in desmognathines, thebone is shortened, thickened, and articulatessquarely with the ends of the vomer, although asmall, flattened process extends forward dorsally.The posterior part of the parasphenoid is greatlyexpanded and extends far laterally, finally contact-ing a dorsomedial process of the quadrate.

Occipito-Otic Complex

The posterior portion of the skull is a massiveamalgamation of elements associated with the otic

capsules and the occipital complex (Fig. 7A,C). Thebulbous otic capsules enclose the vestibular-audi-tory system; they have dorsal and ventral medialconnections to each other and the exoccipitalregion. The otic region is irregular in shape andbears the impressions of the semicircular canals.These impressions form prominent crests, whichbear additional projections. The capsule is con-nected to the braincase by two processes thatextend to the base of the ascending process of thesuspensorium, by another to the ventral surface ofthe lateral part of the parietal, and by processesextending to the parasphenoid; it also connects tothe basal part of the suspensorium. In addition,there is a ridge on the outer surface of the capsulethat articulates with the anterior edge of the squa-mosal, which also articulates with the capsulebehind this ridge. A conspicuous crest, locatedmesially on the surface of the capsule above theanterior semicircular canal, is v-shaped, the vertexof the ‘‘v’’ pointing anteriorly. Posterolaterally isanother prominent crest, directed outward towardthe area above the middle of the squamosal. Thiscrest is drawn into a stout process. The posteriorpart of the capsule is less well ossified. Many fo-ramina pierce the capsule medially toward the cra-nial cavity, ventrally and posteriorly (the foraminaacustica, foramen endolymphaticum, foramen per-ilymphaticum, and foramen post-oticum). Theoperculum covering the fenestra ovalis, the parsmedia plectri, is a circular, well-ossified plate (Fig.7C). Associated with its lateral side is the columel-lar stylus of the pars media plectri. The stylus isroughly L-shaped, with an enlarged area in thepars media plectri that connects to the operculumand a relatively large, cylindrical, rod-like portionthat proceeds anterolaterally toward the articula-tion between the squamosal and the quadrate. Itdoes not directly contact these elements, appa-rently (based on study of cleared specimens) con-necting to a long, slender process of the cartilagi-nous suspensorium and indirectly by a ligament tothe squamosal. The exoccipitals form the posterior-most part of the occipito-otic complex, encirclingthe foramen magnum and articulating via the occi-pital condyles with the first vertebra. Well ossifiedand completely fused to the otic capsules, the exoc-cipitals are in contact dorsally by means of the fi-brous tectum synoticum, but they are in direct con-tact at the posteriormost point. Conspicuous,rounded occipital condyles are concave posteriorlyand articulate with the atlantal cotyles. The inter-nal walls of the foramen magnum articulate bymeans of distinct facets with the large tuberculuminterglenoideum of the atlas. The exoccipitals donot contact ventrally, but instead are connected bya rectangular, cartilaginous hypochordal commis-sure. The ventral part of each exoccipital is over-lapped slightly by the posterior part of the para-sphenoid.



In H. platycephalus, the otic capsules areenlarged, flattened, and well ossified, but disposedsimilarly to those of K. koreana (Fig. 7B,D). Thelateral walls of the capsules are swollen and heav-ily ossified anteromedially at the level of the con-nections to the orbitosphenoids. The otic capsuleshave conspicuous dorsal crests that end in smallprojections and align with the crests of the squa-mosals.

This complex differs little in all plethodontinesexcept for the presence of crests of different sizesand shapes. These reach extremes in the case ofhigh, wing-like crests in large species of Aneidesand in males of all species of that genus (Wake,1963). Crests of the desmognathines have uniqueconfigurations and shapes (Wake, 1966). The occi-pital condyles of desmognathines are massive andprominently stalked (Wake, 1966; Schwenk andWake, 1993). The opercular-columellar system inplethodontines is relatively uniform. There is a rel-

atively large opercular footplate that appears to befused (often so completely as to give the impres-sion of a single element) to a more anterior unitcomprised of a partial footplate and a distinct rod-like projection. These vary in shape and lengthamong taxa (Monath, 1965; Wake, 1966).

Squamosal

The paired squamosals extend from the otic cap-sules to the quadrates, covering the suspensorium(Fig. 8A). The relatively robust, flattened bonearises just behind the prominent crests on the cap-sule and descends laterally and slightly anteriorly.Along its path, it undergoes a twist of about 458 ormore. Two-thirds of the internal-proximal surfaceof the squamosal is also in contact with theenlarged ascending process of the quadrate.

The squamosal of Hydromantes platycephalus isdog-legged in shape and it is smaller and more

Fig. 7. Occipito-otic complex in K. koreana (A, C) and H. platycephalus (B, D). A, B: Dorsal view of the posterior part of theskull. Note the different articulations between exoccipitals and atlas vertebrae, which correspond to differences in the relative sizeof the tuberculum interglenoideum of the atlas in the two species. C, D: Posterolateral view of the skull. Note the different shapeof the stylus of the pars media plectri. cr, crest; ex, exoccipital; fo, fenestra ovalis; oc, otic capsule; occ, occipital condyle; p, parietal;pmp, pars media plectri; st, stylus of the pars media plectri; ti, tuberculum integlenoideum (scale bars: A, C 5 1 mm; B, D 5 2mm).



slender (Fig. 8B). It is attached to the otic capsuleposterior to a prominent crest. It is directed ante-rolaterally and at about its midpoint it bendssharply laterally and ventrally to articulate withthe quadrate.

The squamosals of plethodontines are generallysimilar, differing mainly in the degree of robust-ness, which is largely related to the overallstrength of jaws and size of the mandibular adduc-tor muscles and associated otic and squamosalcrests. The bones reach a maximal size and com-plexity in large Aneides (Wake, 1963), in whichthey participate in extended otic crests. The bonesare relatively robust in desmognathines, in whichthe relatively straight bones are tucked behind an

otic crest and wedged up against another morehorizontally oriented crest of the otic capsule.

Suspensorium

The suspensorium of Karsenia is largely carti-laginous and we have been able to visualize it wellwith doubly cleared and stained specimens. Theonly ossified portion is the quadrate and itsascending process, whereas the basal, otic, ascend-ing, and pterygoid portions are cartilaginous. Theleast well-visualized and smallest portion is theslender, elongate process that connects to the col-umellar stylus. The quadrate is conspicuous andwell ossified, and is a blocky bone (Fig. 8A). It has

Fig. 8. Anterior, lateral, posterior, and medial views of the right squamosal and the quadrate, the only ossified element in thesuspensorium, in K. koreana (A) and H. platycephalus (B). The medial view (m) corresponds to a sagittal section at the level of thearticulation between the otic capsule and the squamosal. Note the different articulation between quadrate and articular in the twospecies. art, articular; den, dentary; prart, prearticular; oc, otic capsules; qu, quadrate; sq, squamosal; st, stylus of the pars mediaplectri (scale bars: A 5 0.5 mm; B 5 1 mm).



a relatively long and very thin ascending process,which is completely covered by the squamosal. Theventral end of the quadrate is capped by a thickcartilage that forms a concave surface, which artic-ulates with the articular portion of the mandible.The posterior end of the ventral surface forms asmall bony projection, the insertion point for thehyoquadrate ligament. Proximally (interior sur-face), the quadrate is also enlarged, forming anattachment surface for the jugal ligament.

In H. platycephalus, the quadrates are smallerand less robust, although they retain the samegenerally blocky form (Fig. 8B). The ascendingprocess is shorter.

Quadrates of all plethodontids are generally sim-ilar, differing mainly in size and degree of develop-ment, which is correlated with the overall size of

the taxon studied. In desmognathines, the quad-rates have extended dorsal and medial processesthat articulate with the otic capsule and the carti-laginous parasphenoid.

Lower Jaw

The paired mandibulae form the lower jaw,which is relatively stout and well developed inKarsenia (Fig. 9A). Each ramus contains a well-ossified dentary surrounding a persistent Meckel’scartilage. Viewed laterally each mandible is planaron its ventral surface. The anterodorsal ends ofthe two dentaries contact at the mandibular sym-physis, and they are a bit spread apart ventrally.In transverse section, the dentary is O-shapedanteriorly, enclosing Meckel’s cartilage. It opens

Fig. 9. Lateral, medial, and dorsal views of the right lower jaw in K. koreana (A) and H. platycephalus (B). The posterior end ofthe mandible is not so robust in H. platycephalus. The coronoid process of the prearticular is less developed and the articular doesnot ossify. art, articular; cor, coronoid process of the prearticular; den, dentary; prart, prearticular; rid, ridge; sym, mandibularsymphysis (scale bars: A 5 1 mm; B 5 2 mm).



and increases in height posteriorly, forming anelongated V-shaped region exposing the cartilageat the lingual margin. A well-formed ridge arisesalong the dorsolateral surface of the dentary atabout its midpoint, before the end of the maxilla;this ridge and adjacent parts of the dentary serveas the insertion of more anterior mandibularadductors. The ridge is extended for a short dis-tance posteriorly as a small projection. The den-tary rises slightly as the ridge forms but there isno triangular process as in some other plethodon-tids. Teeth are borne on the dentary from the sym-physis region to the origin of the ridge, at the levelof the posterior tip of the maxilla, or for aboutthree-quarters of the length of the dentary. Theposterior end of the dentary is flattened, narrow,and blade-like, and is closely applied to the prear-ticular. Each of the paired well-developed preartic-ulars, located medially to the dentaries, has along, tapering process that enters the dentarycanal so that the bone is inserted into the elongatetriangular opening described earlier. A moderatelyhigh shelf-like coronoid process arises just past theposterior end of the maxilla, immediately adjacentto the dentary ridge, and is inflected dorsome-dially. The extensive surface of this shelf is theinsertion of more posterior mandibular adductormuscles. The coronoid process extends posteriorlyand then rapidly slopes ventrally and flattens,ending just before the posterior end of the prear-ticular. The posterior portion of Meckel’s cartilage,the articular, is enlarged and mineralized or ossi-fied, with a cartilaginous articular surface. Thearticular is co-ossified with the lateral and poste-rior parts of the prearticular and is also tightlyconnected to the dentary.

In H. platycephalus, the mandible is weaker andmore slender (Fig. 9B). In lateral view, it is some-what concave, with the symphyseal region beinglower than the articular region. The dentaries arenot in direct contact at the mandibular symphysis.The dentary is more slender, but a subdued dorso-lateral ridge is present. The ridge is the high pointof the dentary viewed laterally, and there is no tri-angular process. Teeth are present as in Karsenia.The prearticular is smaller and shorter in antero-posterior length, and the coronoid process is sig-moid-shaped in cross-section. The process is rela-tively low and it slopes rapidly toward the end ofthe prearticular. The posterior end of the preartic-ular is drawn into a short rod-like projection. Thearticular appears to be entirely unossified.

Mandibles of plethodontines vary greatly in sizebut not in composition. Plethodon and Ensatinaand the smaller species of Aneides closely resembleKarsenia. Aneides has an edentulous triangularextension of the dentary, anterior to the coronoidprocess of the prearticular and associated with themuscular dorsolateral ridge. It becomes very largein A. lubugris and A. flavipunctatus. The extension

is variable but generally low in Plethodon, andonly slightly evident in Ensatina. The coronoidprocess of the prearticular is generally similar toKarsenia, except in Ensatina, in which it is espe-cially low and small, and Aneides, in which it isenormously enlarged in the larger species. Teethare borne along about three-quarters of the den-tary in Ensatina, between one-half and two-thirdsthe length in Plethodon, and the sometimes verylarge teeth of Aneides are restricted to less thanone-half to less than one-quarter the length of thedentary (see Dentition section). Although the den-taries of the largest Aneides are massive, they arenot as massive, in a relative sense, as those of des-mognathines. In species such as Phaeognathushubrichti, the dentaries are very high in lateralview and densely ossified, bearing teeth along lessthan two-thirds of the length of the bone. A verylarge dorsolateral ridge provides a wide shelf forinsertion of adductor muscles. The desmognathineprearticular has a unique shape. The coronoidprocess is restricted to an anterior pointed butstout projection; this forms the posterior border ofthe unique atlantomandibular ligament, whichattaches to the dentary just in front of it (Means,1974). All plethodontids lack a significant retroar-ticular process, although there is some extensionof the prearticular slightly posterior to the articu-lation. In desmognathines and larger species ofAneides, a small ventrally oriented process of thedentary is present near the symphysis, presum-ably to serve as the point of insertion of hyoidmuscles.

Hyobranchial Apparatus

The hyobranchial apparatus in adults consists ofpaired ceratohyals, basibranchial, paired radials,paired ceratobranchials I and II, paired epibran-chials I, and a urohyal (see Fig. 10). All parts ofthe apparatus are cartilaginous, except the centralportion of the basibranchial. The latter is a solidrod of mineralized cartilage viewed laterally in thescanned specimen as floating below the skull, ori-entated posteroventrally relative to the snout andforming a 458 angle with the mandibular plane.The basibranchial is enlarged and has three dis-tinct areas. 1) A central, rod-shaped and mainlymineralized body changes to cartilage both anteri-orly and posteriorly. The mineralized portion,which constitutes about 45% of the total length ofthe basibranchial, increases in diameter towardthe ends. 2) A well-developed, knob-shaped carti-lage forms an anterior process. 3) A posterior carti-laginous enlarged area, pointed at the posterior-most end, connects to the two pairs of ceratobran-chials. The paired radials articulate at the base ofthe anterior process of the basibranchial. They arerod-shaped proximally but more flattened andirregular in outline distally. The radials are ori-



ented almost perpendicular to the basibranchial,pointing slightly anteriorly. The first ceratobran-chial is the longest articulated structure of thehyobranchial apparatus. Ceratobranchial I isnearly straight, with a relatively flat and broadanterior end, the structure becoming more cylin-drical and narrower posteriorly. The anterior endarticulates with the basibranchial at the level ofthe posterior cartilaginous area and the posteriorend articulates with epibranchials. Ceratobran-chial II is shorter, more slender, slightly sigmoidal,and cylindrical. The anterior end of the cerato-branchial articulates with the basibranchial ontwo sides of the pointed posterior end. Posterolat-erally, the ceratobranchial articulates with the epi-branchial. Ceratobranchials I and II do not overlapor contact each other. The epibranchial is a cylin-drical cone that decreases in size and curves ante-

roposteriorly; it is directed posterodorsally, in thedirection of the shoulder. The posterior end nearlyreaches the level of the pectoral girdle. The bowed,ossified urohyal lies medially, slightly posterior tothe level of the epibranchial-ceratobranchial artic-ulation. The ceratohyal is a large element that iscylindrical proximally, where it connects by liga-ments to the quadrate. It becomes flattened andrather abruptly greatly expanded distally, with abroadly rounded anterolateral margin and nearlystraight anteromedial margins parallel to themedial axis.

The ceratohyal is the longest element of the hyo-branchial apparatus (1.7 times the length of thebasibranchial), and the first ceratobranchial is thelongest of the articulated elements (1.25 times thebasibranchial). The second ceratobranchial is 1.2times the basibranchial, and the epibranchial is

Fig. 10. Ventral views of the hyobranchial apparatus in Karsenia koreana (A), Hydromantes platycephalus (B), Desmognathusmonticola (C), Plethodon neomexicanus (D), and Ensatina eschscholtzii (E). Hyobranchial parts are largely cartilaginous, with theexception of the central portion of the basibranchial in K. koreana and the urohyal in all species except H. platycephalus, whichlacks it. Ossified segments are shown in dark gray. (B–E) have been modified from Wake and Deban (2000). bb, basibranchial; cbI,ceratobranchial I; cbII, ceratobranchial II; ch, ceratohyal; eb, epibranchial; r, radial; uh, urohyal (scale bars 5 5 mm).



about 0.8 times the first ceratobranchial andessentially the same length as the basibranchial.The radials are 0.5 times the basibranchial andthe urohyal is 0.3 times the basibranchial. Theknob-like anterior extension of the basibranchial(from the midpoint of the attachment of the radi-als) is about 0.16 times the length of the element.The proportions are similar in all the specimensstudied.

The hyobranchial apparatus of Hydromantes (allmembers of the group) differs greatly from that ofall other salamanders (Wiedersheim, 1875; Lom-bard and Wake, 1977; Wake and Deban, 2000),and the contrast with Karsenia is especially great.It has the form of an extremely long projectile.The basibranchial is longer relative to body sizethan in any other plethodontid and has an ante-rior extension that is flattened at the end and flex-ible near the tip (Lombard and Wake, 1977). Thebasibranchial is expanded near its midpoint withthin lateral flanges. The epibranchials areextremely long, reaching lengths 2.7–3.2 times thebasibranchial length. In contrast, the ceratobran-chials are short and slender, with the second beingslightly shorter and slightly stouter than the first.The first ceratobranchial is only 0.52–0.54 timesbasibranchial length, whereas the epibranchial isnearly six times the length of the first ceratobran-chial. Radials and urohyal are absent. The cera-tohyals are relatively short, less than 0.9 timesbasibranchial length, and have only a narrowlyexpanded blade. The epibranchials are about threetimes longer than the ceratohyal. No parts aremineralized.

The hyobranchial apparatus of Aneides and Ple-thodon closely resembles that of Karsenia in shapeand proportions, and the basibranchial is mineral-ized in its midsection in several species. Desmog-nathus and Phaeognathus also have similar hyo-branchial structure, although the tip of the basi-branchial is not knobbed in the latter, insteadtapering to a point. The radials are somewhat lon-ger and substantially more slender in desmogna-thines than in the other plethodontines. Theurohyal is variable; it can be as long as two-thirdsthe length of the basibranchial in Desmognathus,but is much shorter and more slender in Phaeog-nathus. Ensatina differs from other plethodontinesin having longer epibranchials (about 1.8 timesbasibranchial length) and in lacking the slender,knobbed anterior extension of the basibranchial.Instead, that part of the basibranchial is short andtrapezoidal-to-triangular in shape. It is partly dis-connected from the main body and hence is flexi-ble.

Dentition

Toothed areas include the premaxillae, maxillae,dentaries, vomers, and two posterior vomerine

patches associated with the parasphenoid. Allteeth are pedicellate, small, and barely bicuspid inadults, and nearly homogeneous in size and shapein all the toothed areas. The lingual cusp is thelargest. There is scant evidence of sexual dimor-phism. Premaxillary teeth are slightly enlargedand reduced in numbers (mean of 7.9 6 1.3 totalfor both bones, range of 6–10 in 12 females, 6.4 61.1; range: 4–7 in 8 males) in comparison withsuch relatives as Plethodon and Ensatina. Maxil-lary teeth are slightly more numerous in females(mean 49.5 6 4.5; range: 40–56) than in males(45.6 6 3.3; range: 40–50). Vomerine teeth aresmall and extend only a short distance onto theotherwise toothless preorbital process. They num-ber 16.8 6 2.7; range: 12–20 in females and 15.5 62.6; range: 13–21 in males. The posterior vomerinepatch occupies most of the ventral surface of theparasphenoid, extending forward to the midpointbetween the anterior rim of the optic fenestra andthe anterior border of the orbitosphenoid; it isdensely populated with small bicuspid teeth. Teethare organized in rows that are oriented anteriorlyand form a 458 angle with the medial sagittalplane of the parasphenoid. The patch narrows to asingle tooth in width anteriorly and consists of asmany as four roughly parallel rows at the widestsite posteriorly. Teeth are difficult to count accu-rately because there are many unankylosed teeth.Numbers of ankylosed teeth range between �60and 70 per patch. Replacement teeth are found inthe lingual areas of the premaxillae, maxillae, anddentaries, and along the posterolateral margins ofthe vomerine tooth row.

In Hydromantes playcephalus (and other speciesof the genus) teeth are distributed as in Karsenia.Dentition has been described by Greven andClemen (1976) and Lanza et al. (1995). Teeth offemales and nonreproductive males are similar tothose of Karsenia in being obscurely bicuspid andsmall. The vomers bear teeth nearly to the lateralend of the preorbital process. Posterior vomerinepatches are narrower and more widely separatedthan in Karsenia, but tooth numbers vary from45–105 (mean 65.4) in H. italicus (Lanza et al.,1995). There are usually between 40 and 50 inAmerican species of Hydromantes. Significant dif-ferences in dental morphology are found betweenEuropean and American species. In the Europeanspecies, males have fewer premaxillary teeth (1–2)than females (3–5), and the teeth are enlarged andmonocuspid with sharp, conical, recurved tips thatprotrude from the mouth and function to scarifythe skin of courted females, thus delivering secre-tions of the mental glands. In the American spe-cies, females have more premaxillary teeth thatare of normal form, whereas males have fewer butmainly bicuspid teeth (but not so few as in the Eu-ropean species), although the more posterior teethare transitional to the shape of the maxillary



teeth. Females have maxillary teeth similar totheir premaxillary teeth and they number betweenabout 20 and 30 in European species, but they aremore numerous in American species (25–40).Males have typical small bicuspid teeth in Euro-pean species, with about the same numbers asfemales, but in the American species males havegreatly enlarged, monocuspid teeth that protrudeoutward from the bone and the skin forming theupper lip (Noble and Brady, 1930; Noble, 1931;Adams, 1942). These narrowly conical, sharp max-illary teeth apparently scarify the skin of femalesduring courtship to deliver secretions of mentalglands. The maxillary teeth of American malesnumber from 8 to 12. Dentary teeth of all speciesare small and bicuspid, numbering between 30and 50.

Dentition in Desmognathus and Phaeognathuswas described by Means (1974), and in generalresembles that of Karsenia. However, there is sub-stantial interspecific variation in the shape andsize of tooth crowns. Typical bicuspid teeth arepresent, but lingual cusps of some species areenlarged and recurved, and in a few species, thelabial cusp is greatly reduced in size and is nearlyimperceptible. Some species display sexual dimor-phism in cusp morphology, with females havingtypical small bicuspid teeth and males developingmonocuspid conical premaxillary teeth that projectforward, and enlarged, forward-projecting teeth atthe anterior end of the dentary that have hyper-trophied lingual cusps (Noble and Pope, 1929). Intwo species, teeth of the jaws have short flattenedcusps that have been described as fungiform(Means, 1974). The dentaries of some speciesbecome concave and may even lose most teeth atsexual maturity. Ensatina resembles Karsenia indentition but has higher numbers of generallysmaller but clearly bicuspid teeth. No sexualdimorphism has been noted. The vomerine toothseries is especially long, and the posterior vomer-ine tooth patches are large, narrowly separated,and bear high numbers of teeth. Plethodon resem-bles Karsenia in most respects, but has more di-versity of crown shapes. In general larger specieshave more teeth, with numbers of maxillary teethvarying between 30 and 80 for different species(Coss, 1974). Most teeth are simple and bicuspid,but in males of some species (eastern small group)premaxillary and anterior maxillary teeth areelongated and have enlarged labial cusps. In mostof the western species premaxillary teeth aremonocuspid and spike-like, and in some speciesthese teeth are also found on the maxilla, espe-cially anteriorly; in P. elongatus and P. stormithese anterior maxillary teeth are less elongatedbut enlarged and flattened, even in females (Coss,1974). The dentition of Aneides is similar to that ofKarsenia in respect to vomerine teeth, which aresmall and bicuspid. However, western species of

Aneides have especially small vomerine teeth andthe row is short because the preorbital process ofthe vomer is absent (Wake, 1963). Teeth of thejaws differ substantially from those of Karsenia.The species that most closely resembles Karseniais A. hardii, the females of which have relativelysmall, bicuspid premaxillary, maxillary, and den-tary teeth (Wake, 1963). Male A. hardii have pre-maxillary teeth that are monocuspid, elongatedand recurved; anterior maxillary and dentaryteeth are small and bicuspid, but posteriorly onthe maxilla the teeth become longer and are later-ally compressed with an obscure or absent labialcusp (Coss, 1974). Adult A. aeneus have monocus-pid and ‘‘spike-like’’ teeth (Coss, 1974) and bicus-pid teeth are observed only in juveniles. The west-ern species, A. ferreus, A. flavipunctatus, A. lugub-ris, and A. vagrans, all have specialized dentition,with small bicuspid premaxillary teeth in femalesbut monocuspid premaxillary teeth in males(‘‘needle-like’’ in A. flavipunctatus; Coss, 1974),and enlarged, recurved and laterally compressedmaxillary and dentary teeth, although anteriormaxillary teeth may be small and bicuspid. Theposterior part of the maxilla is toothless andgreatly expanded dorsoventrally, and the monocus-pid teeth immediately in front of this expandedportion are large and blade-like (Wake, 1963). InA. lugubris, maxillary and dentary teeth bothincrease in size and degree of compression anddecrease in number with increasing body size,with as few as five per bone in large adults (Wakeet al., 1983b). Numbers of maxillary and dentaryteeth are reduced to as few as three per bone in A.flavipunctatus (Wake, 1963).

DISCUSSION

Modern salamanders constitute an old cladethat originated by the Triassic; diversification ofthe extant families traces from the Jurassic to themid-Cretaceous (Vieites et al., 2009). Salamandershave invaded heterogeneous geographic regions,inhabiting a vast array of terrestrial and aquatichabitats. Furthermore, they have experienced verydifferent cycles of climatic and environmental con-ditions since their origin. However, the character-istic general morphology of salamanders has per-sisted for more than 160 million years (Gao andShubin, 2003). This morphological persistence de-spite profound environmental changes has beenrelated to the characteristic biology of these organ-isms (Wake et al., 1983a; Larson, 1984; Wake andLarson, 1987).

Variations, needless to say, occur. Morphologicaldiversity among salamanders reflects adaptationsto specific habitats, as well as the evolution ofhighly specialized life histories, such as direct de-velopment and pedomorphosis. These variationscharacterize the distinct families of salamanders,



and, occasionally, within-family clades (Wake,1966; Larson, 1984). Nonetheless, the morphologi-cal ‘‘solutions’’ that have evolved are, in severalcases, rather similar among clades, leading to apattern of rampant homoplasy within the group(Wake, 1991).

Homoplasy, the independent evolution of similarfeatures without a common ancestry, is ubiquitousin Caudata. Moreover, it is not restricted to anytaxonomic-phylogenetic level, but it can bedetected at diverse phylogenetic depths. Theextensive homoplasy has made phylogenetic recon-struction problematic (e.g., Wake, 1966; Muelleret al., 2004; Wiens et al., 2005). The monophyly ofthe 10 families of salamanders has been confirmedwith morphological, molecular, and paleontologicaldata. The phylogenetic relationships among fami-lies, however, have been more difficult to establish,especially when using only morphological charac-ters, because of the high levels of homoplasy. Forexample, pedomorphic forms, in which individualsare sexually mature but retain a larval morphol-ogy, have independently evolved in several familiesof salamanders. The retention of larval charactersin ‘‘adult’’ individuals and the absence of diagnos-tic adult characters in these individuals haveobscured the attempts to reconstruct the phyloge-netic relationships between families by means ofstandard morphological characters (Good andWake, 1992; Larson and Dimmick, 1993; Gao andShubin, 2001; Wiens et al., 2005). Furthermore,the evolution of homoplastic features is also sub-stantial within families, in particular, the Pletho-dontidae (Larson, 1984; Wake, 1991; Parra-Oleaand Wake, 2001).

The family Plethodontidae comprises more thantwo thirds of all the species of salamanders, and isthe most speciose clade among salamanders. Thefamily originated around 125 mya (divergencebetween Amphiumidae and Plethodontidae; Vieiteset al., 2009). The evolutionary history of pletho-dontids has been characterized by several success-ful radiations. In some cases, the radiationsentailed the geographic expansion and diversifica-tion of the group, but with no substantial changein the morphology and ecology of the lineage (non-adaptive radiation). The genus Plethodon includesmore than 50 species distributed in western andeastern North America, all occupying similar habi-tats and niches (Kozak et al., 2006). Morphology isgenerally conserved among species of Plethodon,with no significant differences except in coloration,relative sizes and proportions (Wake et al., 1983a;Kozak et al., 2006). This scenario contrasts withthe adaptive radiation that permitted the expan-sion southward and the colonization of the NewWorld tropics by the supergenus Bolitoglossa,which includes more than 250 species of pletho-dontid salamanders (Wake, 1987). The bolitoglos-sine radiation entailed the invasion of new niches

and habitats and the evolution of new behavioraland morphological specializations. Highly special-ized and derived forms also occur in smaller cladessuch as the genus Aneides, which includes specieswith the strongest and most specialized jaws of thefamily, and Phaeognathus, which has a highlyderived and heavily ossified skull related to itsburrowing behavior. Diversity and disparity arethus not correlated within the family, and general-ists and specialists are unevenly distributed acrossthe phylogeny (Larson, 1984). The diversity offorms and specializations has evolved along only afew morphological axes, constrained by a persis-tent morphological design and leading to thehomoplastic pattern observed within the family(Wake, 1991).

The discovery of Karsenia koreana, the only Asi-atic plethodontid, not only has challenged ourunderstanding of the biogeographic history of ple-thodontid salamanders, but also is of relevance incomprehending the evolution of morphological pat-terns and trends within the family. We discuss theanatomical description of K. koreana with twogoals in mind. First, we approach the biology ofthe species through its morphological description,profiting from the detailed comparative data setavailable for most plethodontid species. The gen-eral, global links among anatomical parts, func-tional morphology, and ecological characteristics ofthe different species are well understood (Wake,1966; Larson, 1984). Then, we analyze the mor-phological trends observed in K. koreana and itsclosest relatives to examine the potential factorsthat have driven the evolution of morphology inplethodontids.

Habitat in Relation to the GeneralMorphology of the Skull

There is a broad correlation between the generalmorphology of the skull and the habitat of pletho-dontine salamanders. For example, species withinPlethodon are generally ground-dwellers, and arenormally found under rocks and logs in forest hab-itats. The morphology of their skulls representsthe most generalized and likely ancestral form(Wake, 1966). The Plethodon radiation contrastswith other functionally specialized types such asoccur in Desmognathus, which has flattened andstreamlined skull morphologies adapted for livingin mountain streams, and the robust and bullet-shaped skull in the burrower Phaeognathus(Wake, 1966; Larson, 1984; Schwenk and Wake,1993).

The skull of Karsenia is compact and wellarticulated. Jaws are robust although teeth arenot enlarged. In general, the skull resembles thatof members of the genus Plethodon more than thatof other plethodontine genera. It is apparentlystronger than any Plethodon skull that we have



observed, resembling that of members of the P.elongatus group more than others in this respect.It lacks, however, the crests on the occipito-oticthat receive a peg-like projection of the squamosal,which is unique to members of that latter group(Wake, 1963). Like Plethodon, Karsenia is thoughtto be fully terrestrial, living at or near the surface,but unlike most Plethodon, it is associated withrock crevices as its vernacular name, Korean crev-ice salamander, implies. The species of Plethodonthat share this habit to some degree include P. lar-selli (P. vandykei group) and P. asupak (P. elonga-tus group; Mead et al., 2005). Although behavior ofKarsenia koreana in relation to habitat use isknown only from the observations of collectors, wesuspect that the species uses its solid skull, inpart, in relation to seeking refuge in tight spacesbetween rocks.

The skull of Hydromantes is similar to that ofKarsenia in general composition, but in overallshape and degree of ossification it is the plethodon-tine genus that is most distinct. In contrast to therounded, strong skull of Karsenia, that of Hydro-mantes platycephalus, as revealed in the CT scansand confirmed in the cleared and stained speci-mens, is dorsoventrally compressed and weaklyarticulated. The contrast is greatest in sexuallymature males: The skull is especially flattenedwith maxillae that are oriented ventrolaterallyand bear elongated, spine-like teeth that extendlaterally well beyond the margins of the head (firstnoted in the original description; Camp, 1916).Hydromantes and especially H. platycephaluswedge themselves into very tight spaces, but gen-erally in cracks in massive outcrops of granite.Rather than having evolved a heavily ossifiedskull, they appear to have followed an alternativeadaptive route in which the skull gives way topressure and conforms, to a degree, to its incom-pressible surroundings.

Feeding in Relation to Skull Form and theAnatomy of the Hyobranchial Apparatus

Feeding systems include the jaws, the dentition,the tongue, and the tongue skeleton, i.e., the hyo-branchial apparatus. Feeding systems and behav-iors are highly diverse in Plethodontidae, relatedto the different habitats and life styles of the spe-cies. The diversification of feeding mechanisms, infact, has played a substantial role in the evolutionof the family (Lombard and Wake, 1976, 1977,1986; Roth and Wake, 1985).

The hyobranchial apparatus in salamanders isinvolved in respiration and feeding during thelarval period, and in pulmonary respiration in ter-restrial adults. The evolutionary loss of lungs inplethodontid salamanders, coupled with the evolu-tion of direct development in most of the species,permitted the use of the hyobranchial apparatus

in highly specialized methods of feeding, such astongue projection. The hyobranchial apparatus,released from its functional constraints, hasrepeatedly evolved highly derived feeding mecha-nisms within the family (Wake, 1991). Feedingmechanisms are grouped in three main categories:attached protrusible tongues (ancestral condition;e.g., Plethodon, Aneides), attached projectiletongues (e.g., Ensatina, Batrachoseps, Hemidacty-lium), and free projectile tongues (most derivedcondition, e.g., Hydromantes, Eurycea, Bolito-glossa; Lombard and Wake, 1986). The structure,extent of ossification, and proportions among ele-ments of the hyobranchial apparatus are highlymodified in each of the three categories. Thesechanges are accompanied by concomitant changesin the associated jaw musculature and articulation(Hinderstein, 1971; Lombard and Wake, 1976;Schwenk and Wake, 1993).

Karsenia koreana represents the ancestral condi-tion, with a protrusible attached tongue and a hyo-branchial apparatus similar in shape and propor-tions to that of Plethodon and Aneides. We knownothing concerning the feeding behavior of Karse-nia, but based on the close resemblance of thetongue and hyobranchial apparatus to that of Ple-thodon and on the absence of the highly modifiedjaws of desmognathines, we assume that it feedsby contacting the prey with its protrusible tongueand then rapidly delivering the prey to the buccalcavity, where it is held by means of the posteriorvomerine tooth patches and the tongue (Magliaand Pyles, 1995; Wake and Deban, 2000). All ple-thodontines feed mainly on arthropods, usually ofsmall size in relation to the size of the mouth.Teeth and jaws play a minor to negligible role inprey capture and processing in other plethodon-tines, except when prey is large. While Hydro-mantes also uses tongue-feeding, it is specializedto an extreme degree and has the longest and atthe same time the most powerful tongue of anysalamander yet studied (Deban et al., 1997, 2007).Its relatively weak jaws do not appear to play arole in processing of food.

Hydromantes has been well studied with respectto visual behavior and feeding (Roth, 1976, 1987).The eyes are large and protuberant and the headis mobile. Associated with head mobility is a smalland gracile tuberculum interglenoideum on theatlas vertebra, which extends into the foramenmagnum and has small articular facets, orientedventrolaterally. We know little concerning headmobility in Karsenia, but its large and robusttuberculum interglenoideum suggests that it isassociated with less craniovertebral mobility andincreased resistance to bending than in Hydro-mantes and possibly other plethodontines as well.The extreme in reduction of the tuberculum inter-glenoideum is in desmognathines, in which theoccipital condyles are enlarged and stalked, thus



moving the head away from the vertebral columnand facilitating up-and-down movements of thehead (Schwenk and Wake, 1993).

Whereas the skull of Karsenia is rather solidlybuilt and cylindrical, with a high, well-supportedbraincase and relatively small orbits, that ofHydromantes is relatively light and flat with weakarticulations of bones, and its jaws are light andlack strong musculature and bear teeth that aredirected outside the mouth. The braincase ofHydromantes is weakly supported, the jaws areweak and the orbits are especially large. Togetherwith the flattening of the entire skull, the impres-sion is of a skull that is not involved in food proc-essing, as is appropriate for an organism with anelongate, highly specialized tongue that deliversthe prey toward the back of the buccal cavitywhere it is immobilized by the posteriorly directedvomerine tooth patches.

Secondary Sexual Traits of the Skull inRelation to Courtship and Mating Behavior

Courtship behavior is uniform among plethodon-tids (summaries in Arnold, 1977; Wells, 2007).During an elaborate tail-straddling walk, the maledelivers one or a few spermatophores that aretaken into the female’s cloaca. The tail-straddlingbehavior is usually accompanied by the delivery ofpheromones by the male. Two distinct modes ofdelivery have been described. In the first mode,which is assumed to be ancestral and more gener-alized among plethodontid salamanders, malesdeliver pheromones from their mental glands bymeans of scratching the dorsal skin of femaleswith their seasonally hypertrophied premaxillaryteeth. Species showing this ‘‘vaccination’’ behaviorhave a strong seasonal sexual dimorphism in den-tition. A second derived mode of pheromone trans-fer has evolved in a clade of the large species ofPlethodon. In this case, males do not develop theprotruding premaxillary teeth and the delivery ofpheromones is conducted by repeatedly touchingthe mental gland to a female’s nares. Courtshipand mating behavior in most of the plethodontidspecies studied to date involve the delivery ofpheromones, although a few species have second-arily lost the mental glands and the deliverybehavior (e.g., Ensatina) (Arnold, 1977; Wells,2007).

There is scant evidence of sexual dimorphism inour material of Karsenia, whereas most species ofplethodontines show at least seasonal sexualdimorphism in premaxillary teeth, males havingfewer and larger teeth (Coss, 1974). In our season-ally limited samples of Karsenia, although the pre-maxillary teeth of males are only slightly enlargedand, while fewer in number in males than infemales, the minimum number of four per bone isnot especially low. However, larger series of males

and females must be studied to assess the degreeof seasonality and sexual dimorphism in the pre-maxillary dentition of Karsenia. Nothing is knownconcerning courtship and mating in Karsenia but,given the absence of protruding premaxillary teethand the presence of mental glands in males, it isreasonable to assume that they are similar to thederived mode observed in Plethodon. The situationis similar in the European species of Hydromantes,but in the American species, sexual dimorphism isexpressed in a unique way. The maxillary teeth ofmales are at least seasonally enlarged and spine-like. Although their precise role in courtship hasnot been specifically studied, based on behavior inother plethodontids, it is likely that the teeth areused to vaccinate females with pheromonal secre-tions from the mental glands.

Morphology of the Skull with Respect toSocial and Aggressive Behavior

Patterns of social and aggressive behaviors areextremely diverse among plethodontids, involvingvisual and chemical cues in species, sexual, andindividual recognition. Agonistic behaviors are nor-mally related to intraspecific territorial combat,but also to interspecific spacing strategies and pa-rental care (Jaeger and Forester, 1993). Plethodon-tines are known to be aggressive, both towardsympatric congeners and to conspecifics (reviewedin Wells, 2007). In some cases, the morphologicalcorrelates of aggressive behavior have been stud-ied in detail (e.g., Staub, 1993; Wiltenmuth, 1996).The relatively strong jaws of Karsenia, whichmight be related either to locomotor use of thehead or to feeding, suggest that these forms maybe aggressive. However, scarring has not beenobserved in the specimens collected to date, so nofurther conclusions can be extrapolated. Aggres-sion has not been observed in Hydromantes and itis not expected, given the weakness of the jaws.One must be cautious in inferring function fromthese salamanders, however, because the relativelyweak-jawed Ensatina can be very aggressive to-ward conspecifics (Wiltenmuth, 1996; Wiltenmuthand Nishikawa, 1998).

Phylogenetic Implications of ComparativeSkull Morphology in PlethodontineSalamanders

The skulls of the genera of plethodontine sala-manders are distinctive, within a framework ofconservative composition (see later). Furthermore,even within genera such as Aneides (Wake, 1963),Desmognathus (Means, 1974), and Hydromantes(Wake, 1966; Lanza et al., 1995; this work) impor-tant differences characterize either individual spe-cies or small clades (such as the western species ofAneides, and the European as compared with the



American Hydromantes). Some multispecies gen-era, e.g., Aneides, Hydromantes, and Desmogna-thus, are characterized by numerous synapomor-phies (Wake, 1966), but Plethodon is not (Wake,1963). Plethodon is the second largest genus of sal-amanders (after Bolitoglossa), currently with 55recognized species (AmphibiaWeb, http://amphibia-web.org/index.html, September, 2009). These spe-cies are remarkably uniform, with relatively minordifferences among them; only the P. elongatusgroup has significant synapomorphies associatedwith the jaws, squamosal, and cranial crests(Wake, 1963). Furthermore, Plethodon displaysapparently plesiomorphic states for most skull andhyobranchial characters, the only exceptions beingthe somewhat strengthened jaws and slightlyreduced numbers of teeth, which distinguish itfrom Ensatina and from distant outgroups such asRhyacotriton. Karsenia also is plesiomorphic withrespect to nearly all traits of the skull and hyo-branchial apparatus, the exceptions being thestrong jaws and the ossified first basibranchial. Itshares the latter and its plesiomorphic traits withat least some species of Plethodon; with respect toskull and hyobranchial morphology Karseniawould fit well within Plethodon. The major fea-tures separating the genera relate to tarsal anat-omy (Min et al., 2005) and molecular characters(Min et al., 2005; Vieites et al., 2007).

We attempted a phylogenetic analysis of datafrom the skull and hyobranchial apparatus, withcharacters used by Wake (1963, 1966), Good andWake (1992), Larson and Dimmick (1993), andWiens et al. (2005), but to little effect (data notshown). Larson and Dimmick (1993) and Wienset al. (2005) attempted to reconstruct the phyloge-netic relationships among salamander families,but even at that phylogenetic level many of themorphological characters employed were not in-formative due to the great amount of homoplasyamong and within lineages. The majority of thecharacters used for the phylogentic analysis, asexpected, were not informative at the phylogeneticdepth of this study. There are very few synapomor-phies in the dataset, the most numerous beingthose that support the Desmognathus, Aneides,and Hydromantes clades. The sole multigenericclade supported with several synapomorphies isPhaeognathus 1 Desmognathus. This clade, longrecognized taxonomically as the subfamily Des-mognathinae (Wake, 1966), was recently and unex-pectedly found to be deeply nested within the Ple-thodontinae in all relevant molecular analyses(e.g., Chippindale et al., 2004; Mueller et al., 2004;Vieites et al., 2007). No single morphological syna-pomorphy defines a Karsenia-Hydromantes clade.

Composition of the skull of plethodontine sala-manders is remarkably conservative. The diver-gence of the two major clades of plethodontid sala-manders, Plethodontinae and Hemidactyliinae, is

�94 mya (Vieites et al., 2007; Zhang and Wake,2009). During that vast period of time, in whichthe range of the plethodontines expanded fromNorth America to East Asia and MediterraneanEurope, very little compositional change in skullconfiguration has taken place. Septomaxillarybones are variably absent from some populationsof European Hydromantes, prefrontals are absentfrom desmognathines and Hydromantes, andurohyals and radii of basibranchials are absentfrom Hydromantes. Premaxillary bones are fusedin Aneides, Desmognathus, and Phaeognathus.Otherwise all species share a common composition.There are differences in degree of ossification, gen-eral strength of the skull and in desmognathines amajor change in the jaw-opening and feeding andlocomotory mechanisms associated with the skull.The putative sister-taxon relationship of Karseniaand Hydromantes associates the apparently con-served, likely ancestral condition of the skull andhyobranchial apparatus in Karsenia with theextreme of specialization for tongue feeding andthe weakest and most compositionally deficientplethodontine skull of Hydromantes.

The pattern of generalist-specialized formswithin clades is repeated along the phylogeny ofplethodontids, and the clade comprising Karseniaand Hydromantes provides a new example to ana-lyze the processes driving morphological evolutionand specialization in Plethodontidae. As discussed,homoplasy, frequent within and between salaman-der families, makes attempts at phylogeneticreconstruction problematic at all phylogenetic lev-els. Homoplastic patterns, which are nonrandomlydistributed both among characters and amongtaxa, reflect real biological processes that underliethe recurrent evolution of morphological similar-ities among groups (Hufford, 1996; McShea, 1996).In salamanders, these processes include the modi-fication of otherwise conserved developmental pro-grams (e.g., ontogenetic repatterning, differentialmetamorphosis; Roth and Wake, 1985; Wake andRoth, 1989). In Plethodontidae, these developmen-tal modifications, coupled with extreme life historystrategies such as pedomorphosis and especiallydirect development, and morphological peculiar-ities such as the loss of lungs, created an unusualevolutionary arena that permitted the diversifica-tion of the group but within a framework of homo-plasy and morphological constraint (Wake et al.,1983a; Wake, 1991; Wake and Hanken, 1996).Descriptions of new lineages, such as K. koreana,are important because they test our understandingof the limits of morphological diversity, and pro-vide insight into the dimensions of evolutionarypatterns within bounds, or constraints, on change.Our anatomical description of the skull of the onlyAsiatic plethodontid is conducted within this con-ceptual framework. Obtaining relevant biologicalinformation for the species, such as habitat use,



feeding habits, and life history traits, will enableus to extend analysis of plethodontid evolution ina multidimensional approach (Wake and Larson,1987), enhancing our understanding of the relativeimportance of the processes that have driven theevolution and diversification of plethodontid sala-manders. A more general outcome of our studywill be progress toward an understanding of howlineage differentiation proceeds in the context oflimits to morphological expression and apparentphylogenetic and developmental constraints.

ACKNOWLEDGMENTS

The authors thank Jessica Maisano and themembers of the DigiMorph CT scan facilities atthe University of Texas, Austin, for their help withthe scanning and segmentation processes. D.Vieites and R. Bonett collected the Karsenia; SeanRovito collected the Hydromantes platycephalusthat was scanned. We also acknowledge theassistance of M. S. Min and the late S. Y. Yang,and the agencies that provided the necessary col-lecting permits. James Hanken and an anonymousreviewer contributed numerous comments thatgreatly improved the manuscript.

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