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Home , Allopleuron, Archelon, Eochelone, Eosphargis, Notochelone, Osteopygis

The Island Arc (1994) 8, 270-284

Thematic Article Phylogenetic systematics of chelonioid sea

REN HIRAYAMA Faculty of Information, Teik:yo Heisei University of Technology, 2289, Uruido, Ichihara, Chiba 290-01, Japan

Abstract Chelonioid sea turtles ( ; Superfamily Chelonioidea) first appear in the early (Aptian-Albian). Their long fossil record is excellent compared to most marine tetrapods. Nonetheless, there has been no inclusive attempt to provide an analysis of cladistic relationships among this group. In this paper, the following chelonioid classification is proposed, based on 76 characters among 20 fossil and six living well- represented genera: (1) (Coniacian to Recent); ·roxochelys, Ctenochelys, , Erquelinnesia, , Argillochelys, Puppigerus, , Syllomus, Natator, Eretmochelys, Chelonia, Ca·retta, Lepidochelys (2) Family (Aptian to ?); 'Santana new protostegid', Rhino­ chelys, , Desmatochelys, Chelosphargis, , (3) Family (Santonian? to Recent); Corsochelys, 'HMG new dermo­ chelyid', , , Dermochelys.

Key words: Cheloniidae, Chelonioidea, classification, Dermochelyidae, osteology, Protostegidae, Reptilia, Testudinata.

INTRODUCTION The chelonioid sea turtles have a long history from METHODS the (Aptian- Albian; Hirayama 1993) as marine tetrapods. Their fossils are com­ During the course of this study the author exam­ mon in shallow water marine sediments. Although ined over 500 fossil and Recent chelonioid speci­ their morphological diversity in the past has been mens. A list of specimens examined is available well documented by many students (summarized in upon request. Zanger! 1980), the phylogenetic relationships of Although numerous fossil genera and chelonioids based on detailed morphology has not have been allocated to the Chelonioidea (Kuhn been published, as reviewed by Gaffney and Maylan 1964), many of them were based on poor materials (1988). More recently, Hirayama (1992a) pub­ or poor descriptions. Thus, I have selected 26 gen­ lished the tentative results of a phylogenetic analy­ era, including 20 plesions, as terminal basic taxa sis at the generic level among the chelonioids; among chelonioids. Of them, two new unnamed ple­ however, the study used only humeral morphology. sions, the 'Santana protostegid' (TUTg1386) and After the IGC symposium (Hirayama 1992d), a the Japanese 'HMG dermochelyid' (Hirayama & beautifuJly preserved complete skeleton of the old­ Chitoku 1994) are included here because of their est known chelonioid from the Santana Formation importance to chelonioid phylogeny. of Brazil became available to the author and was A survey of 76 osteological characters was carefully prepared with acid (Hirayama 1993), and developed for these 26 genera. Character polarities t he previous conclusions about chelonioid relation­ were determined primarily using out-group com­ ships were necessarily changed after this new parisons. After hypotheses of polarity were formu­ discovery. In this paper the character analysis of lated, these decisions were summarized and ex­ chelonioids is summarized and conclusions are pressed in cladograms. My choice of the final made about the relationships and the systematics cladogram was made by an a posteriori weighting of this spectacular group of marine tetrapods. of characters. Phylogeny of chelonioid sea turtles 271 OBSERVATIONS AND RESULTS (13) Anterior vomer-palatine contact; aper­ tura narium interna entirely formed by vomer The derived characters used in analysis of the and palatines. phylogeny of chelonioids are as follows: (14} Primary palate involving vomer. Cranial and lower jaw elements (Figs 1-5) (15) Palatines medially meeting; reduction of (1) Cranial scute sulci present on dermal roof­ posterior portion of vomer. ing elements. (16} Foramen palatinum posterius reduced (2) Loss of nasal bone. and lost. (3) Loss of nasal-frontal contact; medial sep­ (17) Latellay open foramen palatinum poste­ aration of prefrontals. rius. ( 4) Prefrontal-postorbital contact; exclusion (18} Loss of processus pterygoideus externus. of frontal from orbital rim. (19) Pterygoid extending onto mandibular ar- (5) Parietal-squamosal contact. ticulating surface of quadrate. (6) Shallow superior temporal emargination. (20) Narrow middle portion of pterygoids. (7) Jugal-quadrate contact; exclusion of quad- (21) Large processus trochlearis oticum. ratojugal from lower cheek margin. (22) Short crista supraoccipitalis, not project­ (8) Jugal-squamosal contact; loss of post­ ing beyond parietal. orbital-quadratojugal contact. (23) Foramen posterius canalis carotici in­ (9) Medial process of jugal lost. terni between pterygoid and basisphenoid. (10} Loss of foramen praepalatinum. (24) Ventral surface of basisphenoid with (11) Secondary palate involving palatines. prominent V-shaped crest. (12) Secondary palate involving vomer in addi­ (25) Large basisphenoid, lying beneath the sig­ tion to palatines. nificant portion of pterygoids.

(a)

(e) (f)

(g) (h)

Fig. 1 Skulls of chelonioids, left lateral view; (a) latiremis (largely based on AMNH 51 18, condyle-premaxilla length 123 mm, with additions from YPM3602, modified from Gaffney 1979; Senonian of USA); (b) A/lopleuron hoffmanni (NHMM 9017, 258 mm; Upper Maastrichtian of Holland); (c) Osteopygis emarginatus (NJSM 11872, 122 mm; Upper Maastrichtian? of USA); (d) Chelonia mydas (after easier 1968; Recent). (e) 'Santana protostegid' (TUTg 1386, 37 mm; Upper Aptian or Lower Albian of Brazil); (f) pu/chriceps (largely based on BM(NH) R2226. 62 mm, reversed , with additions from BM(NH) 46371 and 46371a; Upper Albian of England); (g) Desmatoche/ys lowi (primarily based on KUVP 1200, 191 mm as estimated; Lower Turonian of USA; with additions from TUTg 262; Middle Turonian of Japan); (h) Protostega gigas(based on FMNH PR65, PR170, PR197 and P27314. about350 mm; lower of USA); (i) Dermochelys coriacea (after Gaffney 1979, reversed; Recent). 272 R. Hirayama

(a)

(f) (g) (h)

•• Fig. 2 Skulls of chelonioids, dorsal view. The dotted line shows lhe scule sulci on lhe dermal roofing elements; (a) Toxoche/ys /atiremis (largely based on AMNH 5118, with additions from YPM 3602, modified from Gaffney 1979); (b) Ctenochelys stenoporus (largely based on USNM 11639, 128 mm; Senonian of USA) . (c) Allopleuron hoffmanni(NHMM 9017); (d) Osteopygis emarginatus (NJSM 11872); (e) Chelonia mydas (after easier, 1966); (f) 'Santana prolostegid' (TUTg 1386); (g) Rhinochelys pulchriceps (largely based on BM (NH) R2226); (h) Oesmatochelys /owi(KUVP1200); (i) Protostega gigas (based on FMNH PR65, PR170, PR197 & P27314); (j) Dermochelys coriacea (after Gaffney 1979).

(26) High dorsum sellae, not concealing poste­ (39) Double cervical central articulation be­ rior portion of sella turcica. tween 7th and 8th centra. (27) Rod-like ossification of rostrum basisphen­ (40) Platycoelous cervical central articulation oidale. between 6th and 7th centra. (28) Reduced ossification of rostrum basisphen­ ( 41) First thoracic with anterior artic­ oidale. ulation facing anteroventrally. (29) Foramen caroticum laterale larger than Appendicular skeleton (Figs 6- 10) foramen anterius canalis carotici interni. (30)Foramen caroticum laterale confluent with (42) Elongate 3rd to 5th digits of manus and

( canalis cavernosum. pes, without movable articulation; carpal and tarsal (31) Broad and flat lower triturating surface, elements flattened, with restricted joint surfaces; with enlarged, deep lateral concavity of dentary as long as femur, with nearly straight where adductor mandibular muscle attaches. shaft, and lateral process is located distal to caput (32) High lingual and symphyseal ridge of den- humerus. tary, visible from lateral view. ( 43) Movable articulations of first and second (33) Denticulated labial ridge of dentary. digits lost. (34) Denticulated lingual ridge of the dentary. ( 44) Coracoid longer than humerus, often with (36) Surangular process extending anteriorly a high dorso-median keel for the M supracora­ onto dentary. coideus. (37) Loss of coronoid and articular bones. ( 45) Elongate coracoid thickened, showing Vertebrae column-like appearance. (38) Longer with much ( 46) Scapular angle, formed by scapular prong wider central articulations. and acromion, larger than 110 o. Phylogeny of chelonioid sea turtles 273 (a) ,. (b) ..

Fig. 3 Skulls of chelonioids, ventra l view; (a) Toxochelys /aliremis (largely based on AMNH 5118, with additions from AMNH 1024, modified from Gaffney 1979); (b) Ctenoche/ys stenoporus (largely based on USNM 11639; Senonian of USA); (c) Allopleuron hoffmanni (based on NHMM 9017 and IRScNB, an uncatalogued specimen); (d) Osteopygis emarginatus (NJSM 11872); (e) Chelonia mydas (alter easier 1966); (f) 'Santana protostegid' (TUTg 1386); (g) Rhinochelys pu/chriceps (largely based on BM(NH) 1606, 36 mm, with additions from BM(NH) R2224, R2276, 46371 and R8339; Middle to Upper Albian of England); (h) Desmatochelys lowi (KUVP 1200); (i) Protostega gigas (based on FMNH PR 170, PR65. P27385 and CM 26593). (j) Dermochelys coriacea (after Gaffney 1979).

(4 7) 'Cheloniid' humerus; the V-shaped struc­ (59) Tibia pit forM pubotibialis and M flexor ture of lateral process. tibialis internus. (48) 'Protostegid' humerus; lateral process of Shell (Figs 8-10) humerus restricted onto the anterior portion of (60) Loss of shell scute sulci. shaft, not well visible from ventral view, with a (61) Nuchal with anterior emargination. median concavity, exclusive of the 'Santana proto­ (62) Nuchal with ventral knob for 8th cervical stegid'. vertebra. (49) 'Dermochelyid' humerus; lateral process (63) Thick keeled neurals equal-sided. of humerus antero-posteriorly elongate, with ante­ (64) Keeled epineural elements. rior projection. (65) Reduced neural elements; medial meeting (50) Ulna-radius contact through distal rugos­ of pleurals. ities. (66) Pleural ossification reduced. (51) Radius with middle portion bent toward (67) Epithecal ossification of carapace. anterior. (68) Loss of bony elements of carapace. (52) Huge lateral process of pubis, projecting (69) Medial serrations of peripherals. anteriorly beyond medial portion of pubis. (70) Additional peripheral and marginal ele- (53) Large, confluent obturator foramen. ments. (54) Lateral process of ischium reduced. (71) Subdivision of costals. (55) Iliac blade with medial curvature. (72) Large plastron, with broad bridge. (56) Large pelvic girdle, nearly touching cora­ (73) Huge star-shaped plastron. coids. (7 4) Reduced, elongate plastral elements, with (57) Femoral trochanters connected by ridge. huge central fontanel. (58) Major trochanter of femur much higher (75) Fusion of epiplastron and entoplastron. than minor one. (76) Loss of entoplastron. 274 R. Hirayama ,. (c) (a) ,. ,.

(f)

Fig. 4 Skulls of chelonioids, with dermal bones removed; (a) Toxochelys latiremis (largely based on AMNH 1024. with additions from USNM 11560 and YPM 1386); (b) Clenoche/ys stenoporus (largely based on FMNH PR444, with additions from SM 894606; Campanian of USA and England); (c) Os/eopygis emarginatus (NJSM 11872); (d) Chelonia mydas (alter Gaffney 1979); (e) Desmatochelys lowi (KUVP 1200); (f) Dermoche/ys coriacea (after Gaffney 1979).

Figure 11 is the most parsimonious final clado­ ming mode of 'flying under water' that is charac­ gram showing the relationships among the 26 teristic of the chelonioids among turtles (Zangerl selected chelonioid genera made from the observed 1953; Walker 1973). Although Gaffney (1976) pro­ character distribution (Table 1). posed that the were the oldest known chelonioids based on their braincase structure, this family has been treated as rather DISCUSSION primitive , much isolated from the che­ lonioids, in more recent work (Gaffney & Maylan As summarized by Gaffney and Maylan (1988) and 1988) based on their more primitive postcranial Hirayama (1992a), the monophyly of the chelonioid characters. Thus, there are no previously reported sea turtles is justified by the following synapo­ pre-Cretaceous chelonioids. The 'Santana Forma­ morphies: foramen praepalatinum lost; coracoid tion protostegid' of Apto-Albian age from Brazil, as long as humerus; humerus as long as femur, therefore, is now the oldest known member of the with nearly straight shaft, and lateral process chelonioids (Hirayama 1993). Figure 11 shows that distal to caput humerus; third to fifth digits elon­ the chelonioids should be classified into just three gate, without movable articulations; carpal and families, the Cheloniidae, the Protostegidae and tarsal elements flattened, with restricted joint sur­ the Dermochelyidae. Any smaller divisions, such as faces. This modification of the limbs into a paddle subfamilies, are not proposed in this paper. is a uniquely derived condition reflecting the swim- The family Cheloniidae is defined by the follow- Phylogeny of chelonioid sea turtles 275

cor (b)~corrt . -

In(

aur (e~"- art den '

cor (g)

.. ,

(j) cor (I} ~ (k}·~• art • I -~. dea ~u• ', den ' ' · .., .., ana Fig. 5 Lower jaws of chelonioids, left lateral view; (a) Toxochelys laliremis (AMNH 511 8); (b) Erquelinnesia gosseleti (IRScNB Ht.R7, holotype; Upper Paleocene of Belgium; modified from Zangerl 1971 ); (c) Allop/euron hoffmanni (IRScNB uncatalogued specimen; Upper Maastrichtian of Holland); (d) Eochelone brabanlica (IRScNB Ht.R1 , holotype; Middle of Belgium); (e) Puppigerus camperi (IRScNB EF.R77; Middle Eocene of Belgium); (I) Syl/omus aegyptiacus (USNM 187382; Middle Miocene of USA); (g) Nata tor depressus (BBM 8299; Recent); (h) Lepidoche/ys kempi (after Hay 1908); (i) Oesmatochelys cl. lowi (TUT g 262); (j) Protostega gigas (FMNH P27385; Lower Campanian of USA); (k) 'HMG dermochelyld' (HMG 369; Lower Maastrichtian of Japan). (I) Dermochelys coriacea (alter Gaffney 1979). ing synapomorphies: incipient secondary palate in­ associated with the poor development of the pecto­ volving palatine; apertura narium interna entirely ral and pelvic girdles of these turtles (Fig. 8a- d). formed by palatines and vomer; basisphenoid with Chelonioids with more advanced limb characters ventral V-s haped crest; cervicals relatively longer, show a much enlarged plastron. Gaffney and May­ with much wider central articulations than in pro­ Ian (1988) and Hirayama (1992a) regarded Tox­ tostegids and dermochelyids; double cervical cen­ ochelys as the most primitive of the chelonioids tral articulation between 7th and 8th centra; first because of its braincase morphology such as the thoracic vertebra with anterior articulation facing persistent subdivided rostrum basisphenoidale, anteroventrally; ulna and radius in tight contact at and the sella turcica concealed by the dorsum distal end with prominent rugosities; large, con­ sellae. Nonetheless, Corsochelys is another exam­ fluent obturator foramen. Zangerl (1953) reviewed ple of a chelonioid with a subdivided rostrum, the Toxochelys and its allies from North although the ossification of the rostrum is higly America, and classified them in the Family Toxo­ reduced in this , as in the living Dermochelys. chelyidae. Zangerl later (1971) gave information The sella turcica not concealed by the dorsum about European Paleogene toxochelyids. However, sellae is reported in some plesiochelyids, and this more recent studies emphasizing its braincase character is not unique to the chelonioids. The structure (Gaffney 1979; Fastvosky 1985; other characters adopted by Gaffney and Maylan Hirayama 1992a) show that this family appears to (1988) as plesiomorphic for Toxochelys, such as the be paraphyletic, not monophyletic. The small plas­ relative size of the foramen caroticum laterale, are tron, with a narrow bridge, which was the most difficult to justify because of the certain variability important character of toxochelyids, seems simply among chelonioids. As listed above, more unique to be primitive among chelonioids, very possibly characters are shared by Toxochelys and the other 276 R Hirayama

{a) {b) (c) (d) {e) {f) {g) {h) {i)

Fig. 6 Le ft humeri of chelonioids (after Hirayama 1992a). Upper row in dorsal view, middle row in ventral view, and lower row in anterior view; (a) Osteopygis emarginatus (YPM 778 and 783); (b) Allopleuron hoffmanni (NHMM 9016); (c) Eochelone brabantica (IRScN8 Ht.R.1); (d) Caretta caretta (RH 786); (e) Desmatochelys lowi (FMNH PR385); (I) ct. Chelosphargis advena (AMNH 1975); (g) Archelon ischyros (based on YPM uncatalogued specimen and YPM1 783; Upper Campanian of USA); (h) 'HMG dermochelyid' (HMG 5); (i) after Volker 1913 and Walker 1973, with additions from RH 31 .

{a) (b) {c) (d) {e) (f) quired among the protostegids and the more ad­ vanced cheloniids, its acquisition occurring twice among the chelonioids. I have found no evidence showing that any dermochelyid has ever had this character. Allopleuron is known from a number of nearly complete skeletons, and has usually been classified in the family Cheloniidae. However, recent studies (Gaffney & Meylan 1988; Hirayama 1992a) pro­ posed that this aberrant turtle should be treated as being more closely related to the protostegids and dermochelyids. Weems (1988) placed it in the der­ mochelyids simply based on shell similarities. This unique plesion is the most problematical in my classification, because it shows a complex combina­ Fig. 7 Left humeri of Albian English chelonioids. Upper row in dorsal view, tion both of presumed primitive and apomorphic middle row in ventral view. and lower row in anterior view (alter Hirayama characters, often shared by the protostegids and 1992a). (a) 'Toxochelyid' type (8M(NH)R22 & R23). (b) 'Cheloniid' type (SM dermochelyids. Its skull and appendicular skeleton, 855970). (c) 'Desmatochelys' type (8M(NH)R2917). (d) cf. Rhinochelys pulchriceps (8M(NH)351 75) . (e) 'Protostega' ang/ica (SM 855988). (f) an however, show clear cheloniid affinities, and would aberrant chenioid (SM 855975, with additions from SM 855987). provide a more parsimonious result. Dodd and Morgan (1992) showed that living cheloniid gen­ era, exclusive of Natator, were well established by cheloniids. Therefore, I prefer the hypothesis that the Early Pliocene. The cheloniids seem to be the genus Toxochelys is a cheloniid rather than a adapted to feed on various benthonic foods, as more primitive kind of chelonioid. If so, the rod-like demonstrated by their highly variable palatal mor­ rostrum basisphenoidale was independently ac- phology (Hendrickson 1980), although their limbs Phyloge:ny of chelonioid sea turtles 277

(c) ~

(b)

(d) @

(e) 278 R. Hirayama

Fig. 9 Reconstructed skeletons of Allopleuron, protostegids and dermochelyids, ventral view. The stippled area shows the coracoid and pelvic girdle; (a) Allopleuron hoffmanni(largely based on IRScNB 3901, with additions from IRScNB 3668 and NHMM 9017, maximum shell length 130 em; Upper Maastrichtian of Belgium and Holland). (b) Desmatochelys lowi(after Zangerl & Sloan 1960, with additions from KUVP 1200 and TUTg 262, maximum shell length about 120 em). (c) Archelon ischyros (modified from Wieland 1909, maximum shell length 193 em); (d) Protostega gigas (after Zangerl1953 and Wieland 1906, maximum shell length about 180 em). (e) Dermochelys coriacea (modified from Volker 1913). (f) "HMG dermochelyid' (after Hirayama & Chitoku 1994, maximum shell length about 150 em). are not so specialized for a pelagic mode as are meeting medially; pterygoid thickened, reaching to those of the dermochelyids or advanced protoste­ mandibular articulating surface of quadrate; fora­ gids. Although no cheloniid is known with certainty men posterius canalis carotici interni lying be­ before the Coniacian of North America, some Jtoxo­ tween basisphenoid and pterygoid; lateral process chelyid' humeri from the English Albian (Fig. 7) of humerus restricted to anterior portion of shaft, might represent primitive members of this family. not well visible in ventral view; middle portion of The family Protostegidae is defined by the fol­ radius bent anteriorly; large hyo-hypoplastra star lowing autapomorphies: large jugal reaching to shaped. Giant sea turtles, such as Archelon of the quadrate, with nearly straight ventral border; pos­ family Protostegidae, have been a major topic for terior portion of vomer reduced, with palatines North American research (Wieland 1896, 1909;

Fig. 8 Reconstructed skeletons of cheloniids, ventral view. The stippled area shows the coracoid and pelvic girdle; (a) Toxochelys latiremis (based on AMNH 5843, FMNH PR123, YPM 3602. YPM 3604 and YPM 3609; maximum shell length about 90 em). (b) Ctenochelys stenoporus (largely based on AMNH 6137, USNM 6013 and USNM 357166, maximum shell length about 80 em); (c) Erquelinnesia gosseleti(after Zangerl1971 ; largely based on holotype, with additions from IRScNB 1634 and 1683. shell length 63 em); (d) Osteopygis emarginatus (largely based on YPM 783 of Hay 1908, with additions from UCMP 123616 of Foster 1980; maximum shell length 69 em; Maastrichtian and Lower Paleocene of USA); (e) Eoche/one brabantica (largely based on holotype, shell length 71 em, with additions from IRScNB 1691 ); (f) Puppigerus camperi (largely based on IRScNB EF.R73. shell length 355 mm, with additions from BMNH 28853, Eocene of Belgium and England); (g) Syllomus aegypliacus (based on AMNH 1661, AMNH 6134, USNM 13859, USNM 24880 and USNM 187382, maximum shell length about 53 em); (h) Natator depressus (after Zangerf eta/. 1988, with additions from BBM 8292 and 8295. shell length 83 em and 81 em); (i) Lepidochelys olivacea (shell based on FMNH 52351 of Zangerl1958, shell length 67 em; other parts based on RH 32, shell length 50 em. Recent); (j) Chelonia mydas (FMNH 22066, shell after Zangerl1958, shell fength 105 em; Recent). Phylogeny of chelonioid sea turtles 279

r------Toxoche lys r----- Ctenochel ys OsteOPYiill Erque J. J nnesl a r----Allopleuron

,..-.-- Pupplge rU 8

f'am il y C helo n i idae SyllODIUIJ

Nata tor Eretmoch elys A Chelonia Le p l doche lys Ca r et ta

Chelosphar~tls l'ami ly Notochelone Protostegldae Desmatochelys Pro tostel• A rchelon

"HMG-l11d" Fam lly Eos phar1Js Oe rmoc h e Jydidae Psephophorus Dermochelys Fig. 10 Skeleton of 'Santana protostegid' (TUTg1386) from the Santana Formation, Upper Aptian or Lower Albian of Brazil. (a} Ven tral and (b) dorsal Fig. 11 A hypothetical relationship among chelonioids. Only ch aracter views after acid preparation. Parts of the plastral elements are still embedded numbers are shown here. See text for explanation of each character. Charac­ in the matrix. ters supporting monophyly at indicated nodes are as follows. ( + , more apomorphic condition, •, presumed character reversal; ', apomorphic char­ acter presumed to be acquired more than twice among chelonioids.) Node A: Zangerl 1953). Desmatochelys has been classified Chelonioidea (1 0, 42). Node B: Cheloniidae (3', 5' , 11, 13, 24, 38, 39, 41, in its own family (Hay 1908) as a primitive chelo­ 50, 53). b1: (2' ' 6' ' 12, 16'' + 24, 27' ' 72'). b2: (43 '' 44', 47' ' 54' , 72'). niid (Zanger) & Sloan 1960), or even even as a b3: (1 '' + 16'' 29'' 59, 62'). b4: (32). b5: (30'' 40' . + 44 ' . 46'' + 47). dermochelyid (Weems 1988). Its holotype skull b6: (36'' +54'. 57 ' . *59). b7: ( + 36). b8: (*3 2, *44, • 46, 70, 71 ). b9: ( + 12 ', + 32). b10: (58). Node C: Protostegidae and Dermochelyidae (17, (KUVO 1200) has now been beautifully prepared 35, + 44 ', 46' , + 72). Node 0: Protostegidae (1', 6' , 7, 9', 15, 19. 23 ', with acid. Hirayama (1992a) first classified Des­ 27', 48, 51 , 73). d1 : ( + 48). d2: (*1 , 14 ' , 16' , 21 , 43' , 52 ' , 54', 57 ', 66'). matochelys as a protostegid. Because a number of d3: (2 ', 3', 4', 5', 18', 20, 45', +51 , +54', 56, 60 ' , 62', +66', +73, unique features, as listed above, are shared by 75). d4: (4' ). Node E: Dermochelyidae (18 '. 28, 29', 30'. 43 ' . 60 ', 66' ). e1 : (22. 36 ' . 49. 52' , +54' , 57 ' , 62'). e2 : (3 ' , 4' , 5' , 6'. 8' , + 14. + 16', 25, Desmatochelys and Protostega, I have no hesita­ + 49. + 66' ,74). e3: (37 . ++ 66, 67, 68,76). tion in placing both together in the family Pro­ tostegidae. A referable new specimen of Desmato­ chelys (TUTg262), including a large portion of the cheloniid Toxochelys and the 'Santana protoste­ skull and complete cervicals, was recently un­ gid'. The protostegids were the dominant cheloni­ earthed from Middle Turonian rocks in Hokkaido, oids from Albian to Turonian time; about 80% of north Japan (Hirayama 1992b). The full descrip­ material examined from that period is from pro­ tion of the 'Santana protostegid', the oldest known tostegids. The protostegids, however, seem to have chelonioid, is in preparation by myself. This speci­ drastically declined after the Campanian. An iso­ men, very importantly, shows that the movable lated right humerus (ANSP 9234), named as At­ articulations of the first and second digits were lantochelys mortoni, seems to be the last known primitively retained in this early protostegid. Hith­ survivor of this family, showing a clear protostegid erto, among chelonioids, this primitive feature was lateral process with median concavity (Leidy known only in the 'toxochelyids' (Zanger) 1953, 1865). Its age is presumed to be Maastrichtian or 1971). In fact, however, the complete paddle struc­ Paleocene (Weems 1988). Hirayama (1992c) pro­ ture seems to have been independently acquired posed that the protostegid turtles were specialized among the three chelonioid families, as shown by to feed on hard shelled planktonic such as 280 R Hirayama

Table 1 Character distribution among selected chelonioids.

a b c d e f g h k m n o p q r s t u v w x y z (1) 1 1 1 1 1 1 1 1 1 2 2 1 1 1 1 ? (2) 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 ? ? 1 1 1 (3) 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 ? ? 1 1 1 (4) 1 1 1 1 1 ? 1 1 1 (5) 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 ? 1 1 1 (6) 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 ? 1 1 1 (7) 1 1 1 ? 1 1 1 ? 1 1 1 (8) 1 ? 1 1 1 (9) 1 1 1 1 1 ? 1 1 1 ? ? 1 1 1 (10) 1 1 1 1 1 1 1 1 ? 1 1 1 1 1 1 1 1 1 1 1 1 ? ? 1 1 1 (11) 1 1 1 1 1 1 1 ? 1 1 1 1 1 ? ? (12) 1 2 3 1 2 1 ? 1 1 1 1 1 ? ? (13) 1 1 1 1 1 1 1 1 1 1 1 1 1 1 ? ? (14) 1 1 1 ? 7 2 2 2 (15) 1 1 1 ? 1 1 1 ? ? (16) 1 2 2 1 2 2 2 ? 2 2 2 2 2 ? 2 2 2 ? 2 2 2 (17) ? 1 1 1 7 1 ? (18) 1 1 1 ? 1 1 1 (19) 1 1 1 1 1 1 1 ? (20) 1 1 ? (21) 1 1 1 ? (22) 1 1 1 1 (23) 1 1 1 ? 1 1 ? ? ? 7 1 (24) 1 2 2 2 2 2 2 2 2 2 2 2 2 2 7 (25) ? 1 1 1 (26) 1 1 ? 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 ? 7 1 ? ? ? 1 (27) 1 1 ? 1 1 1 1 ? 1 1 1 1 1 1 1 1 ? 1 ? ? ? ? ? (28) ? ? 1 ? ? 7 2 (29) 1 1 1 1 1 1 1 1 1 1 1 ? 1 ? ? ? 1 (30) 1 1 1 1 1 1 1 ? ? ? 1 (31) 2 3 1 1 ? (32) 1 1 1 1 1 ? (33) 1 ? (34) 2 1 ? (35) 1 1 1 1 1 1 1 ? 1 ? 1 1 (36) 1 2 2 2 ? 1 ? ? 1 (37) ? ? ? 1 (38) 1 ? 1 ? 1 1 1 1 1 1 1 1 1 1 ? 7 7 (39) 1 1 ? 1 1 ? 1 1 1 1 1 1 ? (40) 1 1 1 1 1 1 7 1 (41) 1 7 ? ? 1 ? 1 7 ? 1 1 1 1 1 ? ? ? ? ? 7 (42) 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 ? 1 1 1 1 1 1 1 1 1 1 (43) 1 1 1 1 1 1 1 1 1 1 ? ? ? 1 1 1 1 1 1 ? 1 (44) ? 2 1 1 ? 2 2 2 2 1 1 2 ? 2 2 2 2 2 2 2 2 ? 2 (45) ? ? ? 1 1 ? 1 (46) 1 ? 1 1 1 1 1 ? 1 1 1 1 1 1 1 1 ? 1 (47) 1 1 1 1 2 2 2 2 2 2 ? (48) 1 2 2 2 2 3 3 (49) ? 1 2 2 2 (50) 1 1 1 1 1 1 1 ? 1 1 1 1 1 1 ? ? ? (51) ? 1 ? 1 ? 1 2 2 ? (52) ? 1 ? ? ? 7 1 1 ? 1 1 7 1 (53) 1 1 1 1 1 ? ? 1 1 1 1 1 1 7 ? ? ? ? (54) 2 1 ? ? 1 1 2 2 2 2 1 ? ? ? 1 2 2 ? 2 2 ? 2 (55) ? ? ? ? 7 1 7 (56) 7 ? 7 ? 1 1 ? 7 (57) ? 1 1 1 1 1 ? ? ? 1 1 1 ? 1 1 ? 1 (58) ? 1 1 7 7 ? ? 7 (59) 2 2 2 1 1 ? ? ? (60) 1 1 1 1 1 1 1 1 (61) 1 ? ? ? 1 r

Phylogeny of chelonioid sea turtles 281

Table 1 (Continued)

a b c d e f g h k m n o p q r s t u v w x y z (62) 1 1 1 1 1 1 1 1 1 1 ? ? ? ? 1 1 1 1 1 1 ~~ 1 1 (64) 1 (65) 1 (66) 1 1 2 2 1 2 3 3 (67) 1 1 (68) 1 1 (69) 1 (70) 1 1 (71) 1 1 (72) 1 1 1 1 1 1 1 1 1 1 2 2 2 2 2 2 2 2 2 2 2 2 (73) 1 1 1 1 2 2 (74) 1 1 1 (75) 1 1 ~~ ? 1 The character is shown as a number from 1 to 76. See text for explanation. Blank, primitive condition; 1, derived condition; 2 and 3, more derived condition; ?, indeterminable. Taxons are shown as a, TOXQchelys; b, Ctenochelys; c; Osteopygis; d; Erquelinnesia; e, Allopleuron; f, Puppigerus; g, Eochelone; h, Argillochelys; i, Syllomus; j, Natator; k, Eretmochelys; I, Chelonia; m, Caretta; n, Lepidochelys; o, Santana protostegid; p, Rhinochelys; q, Notochelone; r, Chelosphargis; s, Desmatochelys; t, Protostega gigas; u, Archelon ischyros; v, Corsochelys; w, HMG dermocbelyid; x, Eosphargis; y, Psephophorus; z, Dermochelys.

ammonites because of their cranial structure, being most abundant Cretaceous chelonioid in Japan, and similar to some living molluscivorous turtles such new material has been discovered from various as (Hirayama 1984), and because of localities since its first report (Hirayama & Suzuki their well-developed limb skeletons. A prominent 1985), although is not yet fully described evolutionary trend toward the huge, massive head (Hirayama & Chitoku 1994). A lower jaw and the and limb skeletons, the reduced shell ossification, nearly complete postcranial skeleton of this plesion and gigantism characterize this group. have been recovered (Fig. 10f). There is no char­ The living Dermochelys coriacea, the only survi­ acter among these sea turtles to argue vor of the Dermochelyidae, is specialized to feed against dermochelyid affinities (Table 1). These mainly on (Hendrickson 1980). The living Mesozoic dermochelyids demonstrate their early species is quite an aberrant turtle, showing numer­ specialization of appendicular skeleton and the ous autoapomorphies. Its fossil relatives have been scute loss, whereas the shell ossification was rather poorly described, mainly due to a lack of good prominent. material (Gaffney & Maylan 1988). Mesozoic der­ A number of presumed convergences or parallel­ mochelyids are poorly known. Hirayama (1992a) isms can be found within the chelonioid phylogeny. first proposed that two Mesozoic turtles, Corso­ The most important parallelism might be the inde­ chelys and the 'HMG dermochelyid', were early pendent acquisition of a paddle lacking any mov­ dermochelyids. Because these presumed Creta­ able articulation of the digits in all three chelonioid ceous dermochelyids lack significant portions of the families, as discussed above. The complete loss of skulls, the diagnosis of this family remain incom­ the scutes seems to have independently occurred in plete, as follows: ossification of rostrum basis­ Allopleuron (Cheloniidae), Protostega-Archelon phenoidale much reduced (confirmed only in Cor­ (Protostegidae), and the Dermochelyidae. Some sochelys and Dermochelys); lateral process of cranial characters, such as a rod-like rostrum basis­ humerus antero-posteriorly elongate, with strong phenoidale, also seems to be a result of conver­ anterior projection (not seen in Corsochelys). All gence. known dermochelyids, even in the Cretaceous, are As reported by Hirayama (1992a), various iso­ fairly large turtles, with shell lengths exceeding lated humeri, including 'toxochelyid', 'cheloniid' over 1.3 m. Corsochelys was considered to be an (Fig. 7b), and several 'protostegid' types, are aberrant cheloniid by Zanger! (1960). Its determi­ known from the English Albian deposits (Gault nation as a dermochelyid is based mainly on its less Clay and Cambridge Greensand Fms.). One hum­ ossified rostrum basisphenoidale as is present in eral type (Fig. 7f) suggests a quite curious early the living species. The 'HMG dermochelyid' is the chelonioid. 282 R. HirayarTUL CONCLUSIONS (3) Family Dermochelyidae Diagnosis: ossification of rostrum basisphenoidale A phylogenetic analysis of 26 selected genera of much reduced (confirmed only in Corsochelys and chelonioids using 76 osteological characters shows De:rmochelys); lateral process of humerus antero­ that the chelonioids can be classified into just three posteriorly elongate, with strong anterior projec­ families: Cheloniidae, Protostegidae and Dermo­ tion (not seen in Corsochelys). Corsochelys (Cam­ chelyidae. A classification of chelonioids is pro­ panian), 'HMG new dermochelyid' (Maastrichtian), posed as follows (only autoapomorphic characters Eosphargis (Eocene), Psephophorus (Eocene­ are given as diagnostic of each taxon): Pliocene), De:rmochelys (Recent) Supe:rfamily Chelonioidea The variable humeri from English Albian age Diagnosis: foramen praepalatinum lost; coracoid and the Apto-Albian 'Santana protostegid' demon­ as long as humerus; humerus as long as femur, strate that the origin and basic radiation of the with nearly straight shaft, and lateral process chelonioid sea turtles must have occurred during a distal to caput humerus; third to fifth digits elon­ much earlier time, possibly prior to the Aptian. gate, without movable articulations; carpal and Whereas most living chelonioid genera are cosmo­ tarsal elements flattened, with restricted articular politan in the world's oceans, the world-wide dis­ surfaces. tribution of fossil chelonioids is rare, particularly (1) Family Cheloniidae during the Cretaceous. Exploration of such earlier Diagnosis: incipient secondary palate involving pa­ diversification and paleobiogeographical problems latine; ape:rtura na1'ium interna entirely formed of the chelonioids would be a good future subject of by palatines and vomer; basisphenoid with ventral investigation, and one that would require the avail­ V-shaped crest; cervicals relatively longer, with ability of new and better material. much wider central articulations than in protoste­ The obvious parallelism seen within chelonioid gids and dermochelyids; double cervical central phylogeny might be rather common, as expressed articulation between 7th and 8th centra; first tho­ in another turtle group, the Family Bataguridae racic vertebra with anterior articulation facing (Hirayama 1984). Thus, any phylogenetic analysis anteroventrally; ulna and radius tightly joined dis­ shou]d be based on as complete a data set as tally with prominent rugosities; large, confluent possible. In this sense, the chelonioids seem to be a obturator foramen. good subject for study because both living and Toxochelys (Coniacian-Campanian), Ctenochelys relatively complete fossil materials would be avail­ (Coniacian-Campanian), Osteopygis (Maastrich­ able for students. tian-Paleocene), Erquelinnesia (Paleocene­ Eocene), Allopleuron (Maastrichtian), Puppige1·us (Eocene), Eochelone (Eocene), Argillochelys ACKNOWLEDGEMENTS (Paleocene-Eocene), Syllomus (Miocene-Pliocene), Natator (Recent), Eretmochelys (Pliocene­ This work was partially supported by a Grant-in­ Recent), Chelonia (Pliocene-Recent), Caretta Aid from Teikyo University of Technology. I thank (Pliocene-Recent), Lepidochelys (Pliocene-Recent) the curators of paleontology and/or herpetology of (2) Family Protostegidae the following institutions for access to material in Diagnosis: large jugal reaching to quadrate, with their care: American Museum of Natural History; nearly straight ventral border; posterior portion of British Museum (Natural History); Bishop Mu­ vomer reduced, with palatines meeting medially; seum; Carnegie Museum; Field Museum of Natural pterygoid thickened, reaching to mandibular artic­ History, Chicago; Geological Survey of Japan; Ho­ ulating surface of quadrate; fommen posterius betsu Museum; Institut Royal des Sciences Na­ canalis carotici interni lying between basisphe­ turelles de Belgique; Museum of Human Activity noid and pterygoid; lateral process of humerus and Nature, Sanda; Naturhistorisch Museum, restricted to anterior portion of shaft, not well Maastricht; New Jersey State Museum; Sedgwick visible in ventral view; middle portion of radius Museum; Teyler Museum; Teikyo University of bent anteriorly; large hyo-hypoplastra star shaped. Technology; United States National Museum of 'Santana new protostegid' (Apto-Albian), Rhi­ Natural History; University of Kansas (Natural nochelys (Albian-Turonian), Notochelone {Albian), History Museum); and Yale Peabody Museum. I Desmatochelys (?-Turonian), Chelos­ wish to express my special thanks to Dr Eugene S. phargis (Coniacian-Campanian), Protostega (Cam­ Gaffney (AMNH) for his assistance and thought­ panian), Archelon (Campanian) provoking comments. Reviews of the manuscript Phylcgeny of chelonioid sea turtles 283 by Dr Lawrence G. Barnes greatly improved this HIRAYAMA R. 1993. A chelonioid sea-turtle discovered paper. from the Santana Formation (Lower Cretaceous; Apto- Albian) of eastern part of Brazil. Abstracts of the JOOth Annual Meeting of the Geological Society REFERENCES of Japan p. (in Japanese). HmAYAMA R. & CHITOKU T. 1994. Fossil turtles of CASIER E. 1968. Le squelette cephalique de Eochelcne Japanese marine Cretaceous strata. In Kobayashi I. brabantica L. Dollo du Bruxellien (Lutetien Infe.rieur) ed. Evolution and Adaptation of Marine Verte­ de Belgiquen et sa comparaison avec celui de Che­ brates Vol. 2. Monograph of the Association for the lonemydas Linne. B1tlletin de l 'lnstitut Royal des Geological Collaboration in Japan 43 (in Japanese Sciences na.turelles de Belgique 44, 1- 22. with English abstract). DODD C. K. JR & MORGAN G. S. 1992. Fossil sea turtles from the Early Pliocene Bone Valley Formation, HIRAYMA R. & SUZUKI S. 1985. Upper Cretaceous sea Central Florida. Journal of Herpetology 26, 1- 8. turtle from the Hakobuchi Group, Central Hokkaido, FASTVOSKY D. E. 1985. A skull of the Cretaceous Japan: A preliminary report. Bulletin of the Hobetsu cheloniid turtles Osteopygis and the classification. Museum 2, 17- 30 (in Japanese with English arac­ tract). Investigation; New Jersey State Museum 3, 1-28. FOSTER D. E. 1980. Osteopygis sp., a marine turtle from KUHN 0. 1964. Fossilium Catalogus. 1. Ani?rta.lia, the of California. Pars 107, Testudines. Junk, The Hague. PaleoBios 34, 1- 15. LEIDY J. 1865. Memoir on the extinct of the GAFFNEY E. S. 1976. Cranial morphology of the Euro­ Cretaceous formations of the United States. Smith­ pean Jurassic turtles Po1·tlandemys and . sonian Contributions to Knowledge 14, 1-165. Bulletin of the American Mu..seum of Natu1·al His­ VOLKER H. 1913. Uber das Stamm-, Gliedmassen-, und tory 157, 487-544. Hauskelet von Dermochelys coriacea L. Zoologische GAFFNEY E. S. 1979. Comparative cranial morphology Jahrbuche1·, Anatomie Band 33, 431- 552. of recent and fossil turtles. Bulletin of the American WALKER W. E. JR 1973. The locomotor apparatus of Museum of Natural History 164, 65- 375. testudines. In Gans C. and Parsons T. S. eds. Biology GAFFNEY E. S. & MA YLAN P. A. 1988. A phylogeny of of Reptilia, Vol. 4, pp. 1- 100. Academic Press, turtles. In Benton M. J. ed. The Phylogeny ami London. Classification of Tetrapods, VoL. 1, Amphibians, WEEMS R. E. 1988. Paleocene turtles from the Aquia Reptiles and Birds, pp. 157- 219. Oxford, Clarendon and Brightseat formations, with a discussion of their Press. bearing on evolution and phylogeny. Pro­ HAY 0. P. 1908. The fossil turtles of North America. ceedings of the Biological Society of Washington Cm"Mgie Institution of Washington Publication 15, 101 , 109- 45. 1-668, pis 1- 113. WIELAND G. R. 1896. A1·chelon ischyros: A new gigan­ HENDRICKSON J. R. 1980. The ecological strategies of tic cryptodiran testudinate from the Fort Pierre Cre­ sea turtles. American Zoologist 20, 597-608. taceous of South Dakota. American Jou.rnal of Sci­ HIRAYAMA R. 1984. Cladistic analysis of batagurine ence 4, 399- 415. turtles (Batagurinae: : ): A WIELAND G. R. L. 1909. Revision of the Protostegidae. preliminary result. Studia Geologica Salmanticensia, Ame1ican Jwmal of Science 4, 101-30. volumen especial l , 141-5 7. ZANGERL R. 1953. The vertebrate fauna of the Selma HTRAYAMA R. 1992a. Humeral morphology of chelonioid Formation of Alabama. Part 3. The turtles of the sea-turtles: Its functional analysis and phylogenetic family Protostegidae. Part 4. The turtles of the implications. Bulletin of the Hobetsu Museum 8, family Toxochelyidae. 17-57 (in Japanese with English abstract). Fieldiana, Geology Memoirs 3, 61-277. HIRAYAMA R. 1992b. Desmatochelys lowi Family Proto­ stegidae; from Upper Cretaceous (Salru Fm., Middle ZANGERL R. 1958. Die oligozanen Meerschildkroten von Yezo Group; Middle Turonian) of Yuubari, Hokkaido, Glarus. Schweizerische Palaontologische Abhand­ · North Japan. Abstracts of the 141th Regu.lar Meet­ lungen 73, 1- 56. ing of the Palaeontological Society of Japan (in ZANGERL R. 1960. The vertebrate fauna of the Selma Japanese). Formation of Alabama. Part 5. An advanced cheloniid HIRAYAMA R. 1992c. Functional morphology and phylo­ sea turtle. Fieldiana., Geology Memoirs 3, 281- 312. genetic systematics of Family Protostegidae (Super­ ZANGERL R. 1971. Two toxochelyid sea turtles from the family Chelonioidea; Order Testndinata). Abstracts of Landenian Sands of the Erquelinnes (Hainaut) of the 141 th Regu.lar Meeting of the Palaeontological Belgium. Memoires de l'lnstitut Royal des Sciences Society of Japan p. 13 (in Japanese). na.turelles de Belgique 169, 1-32. HTRAYAMA R. 1992d. Phylogenetic systematics of Che­ ZANGERL R. 1980. Patterns of phylogenetic differentia­ lonioid sea-turtles. Abstracts of the 29th Interna­ tion in the toxochelyid and cheloniid sea turtles. tional Geological Congress Vol. 3, p. 351. American Zoologist 20, 585-96. r 284 R. Hirayama ZANGERL R., HENDRICKSON L. P. & HENDRICKSON J. R. APPENDIX 1 ANATOMICAL ABBREVIATIONS USED IN 1988. A redescription of the Australian fiatback sea FIGURES. turtle, Nataror depressus. Bishop Museum Bulletin of Zoology 1, 1- 69. Ang, angular; art, articular; bo, basioccipital; bs, ZANGERL R & SLOAN R. E. 1960. A new specimen of basisphenoid; cor, coronoid; den, dentary; dm,jora­ Desmatochelys lowii Williston: A primitive sea turtle men dentofaciale majus; ex, exoccipital; facci, from the Cretaceous of South Dakota. fuldiana, foramen anterior canalis carotici interni; fc, Geology 14, 7- 40. foramen cavernosus; fcl, foramen caroticum lat­ erale; fon, foramen orbito-nasale; fpp, foramen palatinum posterius; fr, frontal; ju, jugal; mx, maxilla; na, nasal; op, opisthotic; pa, parietal; pal, palatine; pf, prefrontal; pm, premaxilla; po, postor­ bital; pr, prootic; pt, pterygoid; qj, quadratojugal; qu, quadrate; rb, rostrum basisphenoidal; sc, sul­ cus cavernosus; so, supraoccipital; sq, squamosal; st, sella turcica; sur, surangular; vo, vomer.