Variation of hyoid morphology in geoemydid terrapins

Susann Richter1, Markus Auer2, Uwe Fritz2,∗

Abstract. The hyoid apparati of 25 geoemydid species in 16 genera (including aquatic, semiterrestrial and terrestrialtaxa) are compared, and for Cuora galbinifrons bourreti ontogenetic development of the hypoid apparatus is described.Generally, ossification of the hyoid apparatus increases with age. The majority of terrestrial species maintain cartilaginousor partially cartilaginous hyoid bodies and second branchial horns throughout life however. Also in tortoises (Testudinidae)hyoid body and second branchial horns remain cartilaginous, suggesting a positive correlation between mode of life andhyoid morphology (terrestrial species with partly cartilaginous hyoid apparatus vs. aquatic species with fully ossified hyoidapparatus).

While skull morphology of chelonians is fre-quently used for taxonomic purposes (e.g. Mc-Dowell, 1964; Gaffney, 1979; Meylan, 1987;Bour, 1989), morphology of the hyoid apparatusis rarely investigated. The most comprehensivestudies were published in the late 19th and early20th centuries (Siebenrock, 1898; Fürbringer,1922; Gräper, 1932); earlier works treating hy-oid morphology were reviewed in these pa-pers as well as in Schumacher (1973). OnlySiebenrock (1898) compared hyoid morphol-ogy of more than a few taxa (40 species from10-11 families using contemporary taxonomy)and found variation among different taxa. In thepresent study we investigate taxonomic varia-tion within the hyoid apparatus of the Geoemy-didae.

The hyoid apparatus plays an important rolein breathing (Siebenrock, 1898) and feeding ofchelonians (e.g. van Damme and Aerts, 1997;Wochesländer and Weisgram, 1999; Lemell etal., 2000) and, in aquatic and terrestrial terrapinsbreathing (Seymour, 1982) and feeding mecha-nisms (Bramble and Wake, 1985; Wochesländerand Weisgram, 1999; Lemell et al., 2000) dif-fer significantly. Therefore, differences in hyoid

1 - Anna-Siemsen-Str. 17, D-07745 Jena, Germany2 - Museum of Zoology, Natural History State Collections

Dresden, A.B. Meyer Building, Königsbrücker Landstr.159, D-01109 Dresden, Germany∗ Corresponding author;e-mail: uwe.fritz@snsd.smwk.sachsen.de

morphology are expected. Siebenrock (1898)studied only four aquatic (Cuora amboinensis,Mauremys caspica, Orlitia borneensis, Rhin-oclemmys punctularia) and one semiterrestrialgeoemydid species (Cyclemys sp.) and reportedno significant differences of hyoid apparati. Inthis paper, the hyoid apparati of a considerablyhigher number of species is studied.

Here we compare the hyoid apparatus of 46 skeletonsrepresenting 25 geoemydid species in 16 genera, includingaquatic, semiterrestrial and terrestrial taxa (table 1), anddescribe ontogenetic development of the hyoid apparatusin Cuora galbinifrons bourreti. Hyoid nomenclature followsSheil and Greenbaum (2005).

Hyoid shape is similar within the Geoemydi-dae (figs 1-2). Differences in the extent of ossifi-cation correspond to age- and taxon-dependentvariation. Generally, juveniles and subadultshave mainly cartilaginous hyoid apparati, aspointed out by Siebenrock (1898). This is exem-plified by a series of Cuora galbinifrons bour-reti comprising specimens of different size andage (fig. 3): In juveniles with straight line cara-pace lengths of approximately 10 cm, the hy-oid apparatus consists mostly of cartilaginoustissue and only the first branchial horn (cornubranchiale I) is ossified. In subadults with cara-pace length of 15-16 cm the hyoid body (cor-pus hyoidis) and second branchial horn (cornubranchiale II) ossify. Ossification of the hyoidbody starts from four nuclei, two on the marginof each side of the body. One is located ante-rior to the articulation of the first branchial horn

© Koninklijke Brill NV, Leiden, 2007. Amphibia-Reptilia 28 (2007): 148-153Also available online - www.brill.nl/amre

Short Notes 149

Figure 1.

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Figure 2. Hyoid apparati of semiterrestrial and terrestrial geoemydid terrapins (adults). Dorsal aspect. Cartilaginous partsgrey. For further explanation see fig. 1. From top to bottom and left to right, first row (semiterrestrial species): Cyclemysatripons-pulchristriata complex (MTD 42548), Cyclemys dentata (MTD 41949), Cyclemys shanensis (MTD 40390); secondrow (terrestrial species): Cuora flavomarginata (MTD 45159), Cuora galbinifrons galbinifrons × bourreti (MTD 44417),Cuora mouhotii obsti (MTD 44922); third row (terrestrial species): Geoemyda spengleri (MTD 40796), Leucocephalonyuwonoi (MTD 44789), Vijayachelys silvatica (MTD 46415). Scale bars = 5 mm. Drawings: S. Richter.

Figure 1. Hyoid apparati of aquatic geoemydid terrapins (adults). Dorsal aspect. Cartilaginous parts grey. Differences ininflection of first branchial horns due to perspective bias. Different size and shape of second branchial horns dependentupon extent of ossification; cartilaginous elements, in part, shrunk. Cartilaginous hyoid horn (cornu hyoidis) not shownbecause this structure is rarely preserved in skeletons; the cartilaginous processus lingualis is also lost in some specimens.Drawings were made using a stereo microscope with drawing tube. From top to bottom and left to right, first row: Cuoraamboinensis kamaroma (MTD 43356), Cuora zhoui (MTD 45163), Hieremys annandalii (MTD 40863); second row:Malayemys subtrijuga (MTD 42522), Mauremys caspica caspica (MTD 40854), Mauremys leprosa (MTD 43362); thirdrow: Mauremys mutica (MTD 43365), Mauremys rivulata (MTD 40855), Melanochelys trijuga thermalis (MTD 38993);fourth row: Morenia petersi (MTD 28068), Notochelys platynota (MTD 41948), Ocadia sinensis (MTD 40539); fifth row:Pangshura smithii (MTD 43355), Sacalia bealei (MTD 42812), Siebenrockiella crassicollis (MTD 40860). Scale bars =5 mm. Drawings: S. Richter.

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Table 1. Specimens and shell lengths (SCL: straight line carapace length). MTD: Museum für Tierkunde (Museum ofZoology), Dresden, SMF: Senckenberg-Museum, Frankfurt/M.; a: aquatic, st: semiterrestrial, t: terrestrial.

Taxon Voucher SCL (cm) Mode of Life

Chinemys reevesii MTD 41541 13.6 aCuora amboinensis kamaroma MTD 43356 16.2 aCuora flavomarginata MTD 45159 13.7 tCuora flavomarginata MTD 45372 14.3 tCuora galbinifrons galbinifrons MTD 36695 16.6 tCuora galbinifrons galbinifrons MTD 44267 17.4 tCuora galbinifrons galbinifrons × bourreti MTD 44417 18.7 tCuora galbinifrons bourreti MTD 40489 16.3 tCuora galbinifrons bourreti MTD 40851 9.6 tCuora galbinifrons bourreti MTD 41939 15.7 tCuora galbinifrons bourreti MTD 44122 16.4 tCuora galbinifrons bourreti MTD 44172 16.4 tCuora galbinifrons bourreti MTD 44241 15.4 tCuora galbinifrons bourreti MTD 44269 12.2 tCuora galbinifrons bourreti MTD 45369 17.3 tCuora galbinifrons bourreti MTD 45370 16.2 tCuora galbinifrons bourreti MTD 45371 16.9 tCuora galbinifrons picturata MTD 42633 16.7 tCuora galbinifrons picturata MTD 44126 16.5 tCuora mouhotii mouhotii MTD 43909 16.9 tCuora mouhotii obsti MTD 44922 15.9 tCuora zhoui MTD 45163 16.8 aCyclemys atripons-pulchristriata complex MTD 42548 19.0 stCyclemys dentata MTD 41949 19.3 stCyclemys dentata SMF 74909 16.4 stCyclemys shanensis MTD 40390 21.2 stGeoemyda spengleri MTD 39970 11.6 tGeoemyda spengleri MTD 40796 9.7 tGeoemyda spengleri MTD 42952 9.0 tGeoemyda spengleri MTD 43000 10.2 tHieremys annandalii MTD 40863 24.8 aLeucocephalon yuwonoi MTD 44789 24.0 tMalayemys subtrijuga MTD 42522 20.3 aMalayemys subtrijuga MTD 43351 9.9 aMauremys caspica caspica MTD 40854 20.9 aMauremys leprosa MTD 43362 16.8 aMauremys mutica MTD 43365 17.4 aMauremys rivulata MTD 40855 18.0 aMelanochelys trijuga thermalis MTD 38993 24.4 aMorenia petersi MTD 28068 19.1 aNotochelys platynota MTD 41948 19.4 aOcadia sinensis MTD 40539 24.7 aPangshura smithii MTD 43355 18.7 aSacalia bealei MTD 42812 14.5 aSiebenrockiella crassicollis MTD 40860 15.9 aVijayachelys silvatica MTD 46415 10.5 t

and the second, appearing earlier during onto-genesis, is located between articulations of firstand second branchial horns. Ossification pro-ceeds inside from along the lateral and posteriormargins of the hyoid body. Before complete os-sification is achieved, a small cartilaginous win-

dow behind the processus lingualis may remain.Ossification of the second branchial horn startsfrom the junction to the hyoid body and extendsfrom there to the distal free horn tip.

In most aquatic species, and in the three semi-terrestrial Cyclemys species we studied, the hy-

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Figure 3. Ontogenetic increase of hyoid ossification in Cuora galbinifrons bourreti. Dorsal aspect. Cartilaginous parts grey.For further explanation see fig. 1. From left to right (bracketed straight line carapace length), top: MTD 40851 (9.6 cm), MTD44241 (15.4 cm; missing part of second branchial horn stippled), MTD 44122 (16.4 cm); bottom: MTD 41939 (15.7 cm),MTD 45370 (16.2 cm). Scale bars = 5 mm. Drawings: S. Richter.

oid apparatus is well-ossified in adults; more orless ossified second branchial horns are mostprobably due to age-dependent variation (figs1-2). However, in an aged but undersized fe-male of Hieremys annandalii hyoid body andsecond branchial horns were still fully carti-laginous while in an adult female Siebenrock-iella crassicollis, another aquatic species, bothbranchial horn pairs were ossified and only theanterior part of the hyoid body was mainly car-tilaginous.

Most terrestrial geoemydids maintain carti-laginous or partially cartilaginous hyoid bod-ies and second branchial horns throughout life,suggesting retention of a juvenile trait. Sieben-rock (1898) reported that hyoid body and sec-ond branchial horns remain also cartilaginousin adult tortoises (Testudinidae). This suggestsa positive correlation between mode of lifeand hyoid morphology (terrestrial species withpartly cartilaginous hyoid apparatus vs. aquaticspecies with fully ossified hyoid apparatus).

The well-ossified hyoid apparatus of adultCuora galbinifrons, a terrestrial species, does

not contradict our hypothesis because in C.galbinifrons the plesiomorphic character statecould be preserved, as in semiterrestrial Cy-clemys species. On the other hand, the twoaquatic species with partly cartilaginous hy-oid apparati, Hieremys annandalii and Sieben-rockiella crassicollis, are closely related to, orcongeneric with, terrestrial or semiterrestrialspecies (Heosemys, Siebenrockiella leytensis;Spinks et al., 2004; Diesmos et al., 2005). Itcould be speculated that hyoid morphology inHieremys annandalii and Siebenrockiella cras-sicollis indicates, therefore, that both are de-rived from terrestrial ancestors.

Further research should be conducted to de-termine functional differences between fully os-sified and partially cartilaginous hyoid apparatiwith regard to breathing and feeding of geoemy-did terrapins.

Acknowledgements. Thanks go to Gunther Köhler (For-schungsinstitut und Naturmuseum Senckenberg, Frank-furt/M.) for the loan of one skeleton. Stephen D. Busackassisted with our presentation of this information.

Short Notes 153

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Received: January 25, 2006. Accepted: March 20, 2006.