Variation of Hyoid Morphology in Geoemydid Terrapins

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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 terrestrial taxa) 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 cartilaginous or 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 and hyoid morphology (terrestrial species with partly cartilaginous hyoid apparatus vs. aquatic species with fully ossiﬁed hyoid apparatus).

While skull morphology of chelonians is fre- morphology are expected. Siebenrock (1898) quently used for taxonomic purposes (e.g. Mc- studied only four aquatic (Cuora amboinensis, Dowell, 1964; Gaffney, 1979; Meylan, 1987; Mauremys caspica, Orlitia borneensis, Rhin- Bour, 1989), morphology of the hyoid apparatus oclemmys punctularia) and one semiterrestrial is rarely investigated. The most comprehensive geoemydid species (Cyclemys sp.) and reported studies were published in the late 19th and early no significant differences of hyoid apparati. In 20th centuries (Siebenrock, 1898; Fürbringer, this paper, the hyoid apparati of a considerably 1922; Gräper, 1932); earlier works treating hy- higher number of species is studied. oid morphology were reviewed in these pa- Here we compare the hyoid apparatus of 46 skeletons pers as well as in Schumacher (1973). Only representing 25 geoemydid species in 16 genera, including Siebenrock (1898) compared hyoid morphol- aquatic, semiterrestrial and terrestrial taxa (table 1), and ogy of more than a few taxa (40 species from describe ontogenetic development of the hyoid apparatus in Cuora galbinifrons bourreti. Hyoid nomenclature follows 10-11 families using contemporary taxonomy) Sheil and Greenbaum (2005). and found variation among different taxa. In the present study we investigate taxonomic varia- Hyoid shape is similar within the Geoemydi- tion within the hyoid apparatus of the Geoemy- dae (figs 1-2). Differences in the extent of ossifi- didae. cation correspond to age- and taxon-dependent The hyoid apparatus plays an important role variation. Generally, juveniles and subadults in breathing (Siebenrock, 1898) and feeding of have mainly cartilaginous hyoid apparati, as chelonians (e.g. van Damme and Aerts, 1997; pointed out by Siebenrock (1898). This is exem- Wochesländer and Weisgram, 1999; Lemell et plified by a series of Cuora galbinifrons bour- al., 2000) and, in aquatic and terrestrial terrapins reti comprising specimens of different size and breathing (Seymour, 1982) and feeding mecha- age (fig. 3): In juveniles with straight line cara- nisms (Bramble and Wake, 1985; Wochesländer pace lengths of approximately 10 cm, the hy- and Weisgram, 1999; Lemell et al., 2000) dif- oid apparatus consists mostly of cartilaginous fer significantly. Therefore, differences in hyoid tissue and only the first branchial horn (cornu branchiale I) is ossified. In subadults with carapace length of 15-16 cm the hyoid body (cor- 1 - Anna-Siemsen-Str. 17, D-07745 Jena, Germany pus hyoidis) and second branchial horn (cornu 2 - Museum of Zoology, Natural History State Collections branchiale II) ossify. Ossification of the hyoid Dresden, A.B. Meyer Building, Königsbrücker Landstr. body starts from four nuclei, two on the margin 159, D-01109 Dresden, Germany ∗ Corresponding author; of each side of the body. One is located ante- e-mail: [email protected] rior to the articulation of the first branchial horn

Figure 1. 150 Short Notes

Figure 2. Hyoid apparati of semiterrestrial and terrestrial geoemydid terrapins (adults). Dorsal aspect. Cartilaginous parts grey. For further explanation see fig. 1. From top to bottom and left to right, first row (semiterrestrial species): Cyclemys atripons-pulchristriata complex (MTD 42548), Cyclemys dentata (MTD 41949), Cyclemys shanensis (MTD 40390); second row (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), Leucocephalon yuwonoi (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 in inflection of first branchial horns due to perspective bias. Different size and shape of second branchial horns dependent upon extent of ossification; cartilaginous elements, in part, shrunk. Cartilaginous hyoid horn (cornu hyoidis) not shown because 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: Cuora amboinensis 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); third row: 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. Short Notes 151

Table 1. Specimens and shell lengths (SCL: straight line carapace length). MTD: Museum für Tierkunde (Museum of Zoology), 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 a Cuora amboinensis kamaroma MTD 43356 16.2 a Cuora flavomarginata MTD 45159 13.7 t Cuora flavomarginata MTD 45372 14.3 t Cuora galbinifrons galbinifrons MTD 36695 16.6 t Cuora galbinifrons galbinifrons MTD 44267 17.4 t Cuora galbinifrons galbinifrons × bourreti MTD 44417 18.7 t Cuora galbinifrons bourreti MTD 40489 16.3 t Cuora galbinifrons bourreti MTD 40851 9.6 t Cuora galbinifrons bourreti MTD 41939 15.7 t Cuora galbinifrons bourreti MTD 44122 16.4 t Cuora galbinifrons bourreti MTD 44172 16.4 t Cuora galbinifrons bourreti MTD 44241 15.4 t Cuora galbinifrons bourreti MTD 44269 12.2 t Cuora galbinifrons bourreti MTD 45369 17.3 t Cuora galbinifrons bourreti MTD 45370 16.2 t Cuora galbinifrons bourreti MTD 45371 16.9 t Cuora galbinifrons picturata MTD 42633 16.7 t Cuora galbinifrons picturata MTD 44126 16.5 t Cuora mouhotii mouhotii MTD 43909 16.9 t Cuora mouhotii obsti MTD 44922 15.9 t Cuora zhoui MTD 45163 16.8 a Cyclemys atripons-pulchristriata complex MTD 42548 19.0 st Cyclemys dentata MTD 41949 19.3 st Cyclemys dentata SMF 74909 16.4 st Cyclemys shanensis MTD 40390 21.2 st Geoemyda spengleri MTD 39970 11.6 t Geoemyda spengleri MTD 40796 9.7 t Geoemyda spengleri MTD 42952 9.0 t Geoemyda spengleri MTD 43000 10.2 t Hieremys annandalii MTD 40863 24.8 a Leucocephalon yuwonoi MTD 44789 24.0 t Malayemys subtrijuga MTD 42522 20.3 a Malayemys subtrijuga MTD 43351 9.9 a Mauremys caspica caspica MTD 40854 20.9 a Mauremys leprosa MTD 43362 16.8 a Mauremys mutica MTD 43365 17.4 a Mauremys rivulata MTD 40855 18.0 a Melanochelys trijuga thermalis MTD 38993 24.4 a Morenia petersi MTD 28068 19.1 a Notochelys platynota MTD 41948 19.4 a Ocadia sinensis MTD 40539 24.7 a Pangshura smithii MTD 43355 18.7 a Sacalia bealei MTD 42812 14.5 a Siebenrockiella crassicollis MTD 40860 15.9 a Vijayachelys silvatica MTD 46415 10.5 t and the second, appearing earlier during onto- dow behind the processus lingualis may remain. genesis, is located between articulations of first Ossification of the second branchial horn starts and second branchial horns. Ossification pro- from the junction to the hyoid body and extends ceeds inside from along the lateral and posterior from there to the distal free horn tip. margins of the hyoid body. Before complete os- In most aquatic species, and in the three semi- sification is achieved, a small cartilaginous win- terrestrial Cyclemys species we studied, the hy- 152 Short Notes

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), MTD 44241 (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 or not contradict our hypothesis because in C. less ossified second branchial horns are most galbinifrons the plesiomorphic character state probably due to age-dependent variation (figs could be preserved, as in semiterrestrial Cy- 1-2). However, in an aged but undersized fe- clemys species. On the other hand, the two male of Hieremys annandalii hyoid body and aquatic species with partly cartilaginous hy- second branchial horns were still fully carti- oid apparati, Hieremys annandalii and Sieben- laginous while in an adult female Siebenrock- rockiella crassicollis, are closely related to, or iella crassicollis, another aquatic species, both congeneric with, terrestrial or semiterrestrial branchial horn pairs were ossified and only the species (Heosemys, Siebenrockiella leytensis; anterior part of the hyoid body was mainly car- Spinks et al., 2004; Diesmos et al., 2005). It tilaginous. could be speculated that hyoid morphology in Most terrestrial geoemydids maintain carti- Hieremys annandalii and Siebenrockiella cras- laginous or partially cartilaginous hyoid bod- sicollis indicates, therefore, that both are de- ies and second branchial horns throughout life, rived from terrestrial ancestors. suggesting retention of a juvenile trait. Sieben- Further research should be conducted to de- rock (1898) reported that hyoid body and sec- termine functional differences between fully os- ond branchial horns remain also cartilaginous sified and partially cartilaginous hyoid apparati in adult tortoises (Testudinidae). This suggests with regard to breathing and feeding of geoemy- a positive correlation between mode of life did terrapins. and hyoid morphology (terrestrial species with partly cartilaginous hyoid apparatus vs. aquatic species with fully ossified hyoid apparatus). Acknowledgements. Thanks go to Gunther Köhler (For- schungsinstitut und Naturmuseum Senckenberg, Frank- The well-ossified hyoid apparatus of adult furt/M.) for the loan of one skeleton. Stephen D. Busack Cuora galbinifrons, a terrestrial species, does assisted with our presentation of this information. Short Notes 153

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