ORYCTOS,Vol.3 : 7I -17. Décembre2000 SecondaryAdaptation to Life in Watertr, Copenhagen,1999

PRELIMINARYREPORT ON TI{E EVOTUTIONOFAQUATIC ADAPTATION IN DESMOSTYLIANS(MAMMALIA, TETHYTHERIA)

Norihisa INUZUKA

Department of Cell Biology & Anatomy, GraduateSchool of Medicine, University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo, 113-0033Japan

Abstract : Forty nine trends indicating aquatic adaptationare recognized based on the distribution of osteological charactersin 16 speciesof four living mammalian taxa. Among them, 39 trends are also found in desmostylians.In the present paper their distribution is examined in four genera of Desmostylia, for which skeletonsare known, i.e. Behemotops and Paleoparadoxia (family Paleoparadoxiidae), and Ashoroa and Desn'tostylus (family Desmostylidae).Characters inserted on the phylogenetic tree elucidatethe evolution of aquatic adaptationwithin the order Desmostylia. The present paper introduces preliminary results: although the phylogenetic divergence of the two families shows no relation to aquatic adaptation,the Desmostylidaebecame more adaptedto aquatic life than did the Paleoparadoxiidae,with Desmostylusrepresenting the highest level of aquatic specializationon presentfos- sil evidence.

Key words: Desmostylia, aquatic adaptation, comparative rnorphology,functional morphology

Observations préliminaires sur l'évolution vers I'adaptation au mode de vie aquatique chez les Desmostyliens (Mammalia, Tethytheria)

Résumé : Quarante-neuftendances indiquant une adaptationà la vie aquatique sont reconnuesgrâce à la distribu- tion de caractèresostéologiques chez 16 espècesappartenant à quatre taxons différents de mammifères actuels. Parmi ces caractères,39 sont égalementprésents chez les desmostyliens.Le présent article examine la distribution de ces caractèreschez quatre genres de Desmostylia pour lesquels des squelettessont connus : Behemotops et Paleoparadoxia (famille Paleoparadoxiidae),et Ashoroa et Desmostylas(famille Desmostylidae).Le placementdes caractèressur un arbre phylogénétiqueindique les modalités de l'évolution vers un mode de vie aquatiqueà I'inté- rieur de l'ordre des Desmostylia. Des résultats préliminaires sont présentésici : bien que la divergence des deux familles ne soit pas liée à I'adaptation au mode de vie aquatique,les Desmostylidaedeviennent mieux adaptésà la vie aquatiqueque les Paleoparadoxiidae,Desmostylus représentant la plus forte adaptationau milieu aquatiquesur la base des restesfossiles disponibles.

Mots clés : Desmostylia, adaptation aquatique, morphologie cornparative,morphologie fonctionnelle

INTRODUCTION closely related to the terrestrialProboscidea and the purely aquatic Sirenia, together constituting the Members of the extinct mammalian order Tethytheria(McKenna, 1975; Domning et a1.,1986). Desmostylia inhabited the northern Pacific coasts Questions concerning the ecological adaptationof and are found in Japan, Sakhalin and Kamchatka as the dentition and body form of the desmostylians well as in western North America from the Late havebeen dealt with by, i.a.,Inuzuka(1984;2000a), Oligoceneto the late Middle Miocene (Inuzukaet aI., but remain unresolved 7994).Among living mammals,the Desmostyliaare Osteological characters that indicate aquatic 71 ORYCTOS,Vol.3,2000 adapatationof the desmostylians(Inuzuka, 2000b) (1959)noted that "... evidencefrom newly described are studiedin the four generaof Desmostylidaeand desmostylidssuggests that there are forms, transitio- Paleoparadoxiidaefor which larger parts of the ske- nal in locomotion and habitat, which may have ran- leton are known. The aim is to demonstratediffe- ged from terrestrial to amphibious to completely rences in the manifestation of aquatic adaptation aquatichabit ... all membersof this group were chie- within the two families, and in the progressionof the fly amphibious." He also speculated that adaptationwithin eachfamily. The aquaticadaptation "Paleoparadoxia may have been more terrestrial in trendsare sortedinto sevencategories by distribution its habits than the other desmostylids" becauseits pattem and are, finally, mapped onto a simplified lower incisors are close-set. From the standpointof phylogenetictree sensuInuzuka (2000c). comparativecraniology, Ijiri & Kamei (1961) consi- As a result, it was proved that : morphological deredboth desmostylidsand paleoparadoxiidsto be differences between Paleoparadoxiidae and marine mammals,more adaptedfor aquaticlife than Desmostylidaeare mostly not relatedto aquaticadap- the hippopotamusor tapir, with fur like seals and tation; the differencesof degreeof adaptationin each more or less webbed skin between digits. Shikama body part betweenthe two families are slight; por- (1966) surmisedthat the desmostylianswere amphi- tions more adaptedfor aquatic life are more nume- bious to semiaquaticcoast dwellers similar to the pin- rous in the family Desmostylidae,namely in the evo- nipeds,since no remainshad beenfound in terrestrial lutionary processfrom Ashoroa to D esmo s tylus, than deposits. Inuzuka (2000b), through comparative in the Paleoparadoxiidae;and the most highly adap- functional morphology of extant mammals,corrobo- ted animal for aquaticlife was Desmostylus. rated that osteologyshows desmostylians to be adap- Institutional abbreviations: AMR Ashoro ted for aquatic life at least more than Hippopotamus Museum of Paleontology,Japan; UCMR University amphibius. of California Museum of Paleontology,Berkeley; In 1996, when the first symposium on NSM-PV National ScienceMuseum, Paleontology, "SecondaryAdaptation to Life in Water" was held in Vertebrate, Tokyo, Japan; UHR, University of Poitiers, France,the desmostylianswere believed to Hokkaido, Rigakubu, Sapporo, Japan; GSJ-R constitute a single, monophyletic evolutionary line GeologicalSurvey of Japan,Fossil, Tsukuba,Japan. (Domning et al., 1986). This was based on Behemotops, Paleoparadoxia and Desmostylus. Subsequently,Inuzuka (2000c) describeda new, pri- SOME PREVIOUS STUDIBS mitive desmostylian,Ashoroa, found togetherwith a ON ADAPTATION AND RELATIONSHIP new speciesof Behemotopsin Ashoro, Hokkaido, Japan.The new genericname, Ashoroa, corresponds VanderHoo f (1937) sug gested that " D es mo s ty Iu s to the first Ashoro specimen referred by Inuzuka and Cornwallius are aquatic because: (a) their (2000b). Phylogeneticanalysis of eleven speciesin remainsare alwaysfound in formationsknown to be six generamade Inuzuka (2000c)divide Desmostylia marine; (b) certaincharacters in the skull, suchas the into two families, Paleoparadoxiidae and absenceof a lacrymal foramen, appeil to be aquatic Desmostylidae, of which the former includes adaptations;(c) the structure of the forefoot is like Behemotops and Paleoparadoxia and the latter that of the largerpinnipeds and of the Sirenia".When includesAshoroa, Cornwallius, Kronokotheriumand a complete skeleton was discovered in Saghalien, Desmostylus(Fig. 1). The Paleoparadoxiidaeare cha- Japan in 1933, however, it differed in many ways mcteized by an extremely long dental root and rela- from that of the Sirenia, such as by the presenceof tively steepmedial inclination of the calcanealtuber, stout limb boneslike thoseof the hippopotamus,and whereasthe Desmostylidaeis distinguishedby a rela- the animal was regardedto be amphibious (Nagao, tively reduced molar cingulum, a well-expanded 1941). Shikama (L957) assumedthat desmostylians braincasè,a relatively recurved coronoid process, dived in water like a tapir or a hippopotamus,and that thirteen thoracic vertebrae,elongation and origina- they inhabitedshallow seas,lagoons or estuaries,and ting from the lower level of the thoracic transverse were not purely aquatic like the sea cow. Reinhart processes,and steep backward inclination of the 72 INUZUKA- AQUATIQUEADAPTATTON IN DESMOSTYLIANS thoracic vertebralspinous processes. Because advan- ced stylodont teeth evolved independentlyfrom pri- mitive bunodontteeth in both families, the presence of stylodont cheek teeth which was previously used to define the Desmostylia is a parallel character within this order.

Figure 1. Phylogenetic tree of eleven species in the Desmostylia (after Inuzuka, 2000c).

Paleoparadoxiidae Desmostylidae

MIDDLE A-, MIOCENE \ .---) L:---)"=-Jt -=-^-*f\ P sP'nov' D. hesperus D. coalingensis Paleoparadoxia 15.8Ma Desmostylus Fq.Æi-f .r\-)11 1

Behemotops ,!"'

UPPER OLIGOCENE Cornwallîus

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MATERIALS AND METHODS [2] Trend occurred in the evolutionary process from Behemotops to Paleoparadoxia in the The fossil remains of seven individuals pertai- Paleoparadoxiidae(unknown in Desmostylidae). ning to five specieswere examined:Behemotops kat- [3] Trend occurred in the evolutionary process suiei (ANIP 22), Paleoparadoxiasp. (Stanfordspeci- from Ashoroa to Desmostylusin the Desmostylidae men:UCMP 81302),and P tabatai(Izumi specimen: (unknown or did not changein Paleoparadoxiidae). NSM-PV 05601 and the Tsuyamaspecimen) repre- [4] Trends observedin Ashoroa and in a more senting Paleoparadoxiidae;and Ashoroa laticosta pronouncedstate in Desmostylus. (AMP 2I), and Desmostylushesperus (Keton speci- [5] Trend evolved in both families in parallel. men: UHR 18466 and Utanobori specimen:GSJ-F [6] Trend is seenonly in genusPaleoparadoxia. 77 43) representingDesmostylidae. [7] Trend is seenonly in genusDesmostylus. In a previous study 49 charactersor trends of Figure 2 shows a simplified phylogenetic tree aquaticadaptation were recognizedbased on compa- of only four generaof the order, and the numbersin rative and functional morphological analysesof six- bracketsrefer to the sevendistribution categorieslis- teenspecies in four living mammaliantaxa, and 39 of ted above. thesetrends were chosenon the basisthat eachtrend Common aquatic adaptationtrends observedin was recognizedin threeto four of the extantorders or all four desmostyliangenera [1] include: shortening families, was present also in the Desmostylia, and of the lumbar vertebralbodies, horizontal projection was not affected by size (Inuzuka, 2000b). For the of lumbar vertebraltransverse processes, reduction of presentstudy, for each trend, presenceor absenceis the ischial tuberosity,and widening and thinning of noted in each of the four generaof the Desmostylia, all the femoral epiphyses.No adaptivecharacter was as well as degree of development, if any. seen in only the two genera of either Furthermore,some of the trends are grouped accor- Paleoparadoxiidaeor Desmostylidae.The trend pro- ding to distribution patternand by inserting the cate- ducing an evolutionary sequencefrom Behemotops gories on a simplified phylogenetictree it is specula- to Paleoparadoxia observed in the family ted at which stageof evolution the trendswere acqui- Paleoparadoxiidaebut unknown in Desmostylidae red. For instance,trends for which Behemotopsand [2] was only shallowing of the trochlea tali groove Paleoparadoxiashow one distribution and Ashoroa (Inuzuka,2000b: fig.8). Four trendswere observedin andDesmostylus show anotherare differencesat the the Desmostylidae fr om A sho ro a to D es mo s ty lu s [3] : family level, and it is surmisedthat the differentiation reductionof the scapularcoracoid process, widening took place at an early stagein desmostylianevolu- of the radioulnar epiphyses,lengthening of the ole- tion. In cases where Paleoparadoxia and cranon, and shallowing of the acetabulum.Seven Desmostylusshare the samecharacteristics or trends, charactersalready observedin Ashoroa increasedin or characteristicsof Paleoparadoxia compared to degree of aquatic adaptation in Desmostylusl4l : Behemotopsand those of Desmostylusto Ashoroa weakeningof the occipital condyle transverseridges, indicate the same tendencv. these are considered widening of the axis, shorteningand steeperinclina- parallelisms. tion of the mid-thoracic vertebral spinousprocesses, shallowing of the scapularglenoid cavity, thickening of the radioulnar shaft, and enlargementof the femo- RESULTS ral head.Three trends evolved in parallel in the two families [5] : shallowing of the atlantal fossa,enlar- Table 1 lists charactersand trends of aquatic gementof the sacralforamina, and dorsoventralflat- adaptationin desmostylians.Some of the featuresare tening of the femoral shaft.Adaptations observed in divided.into the following seven categories,which Paleoparadoxia only [6] is a relatively gentle incli- are mufually exclusive,to servethe purposeof evo- nation of the lumbar vertebralarticular surfaces.and lutionary description. in Desmostylusonly [7] is an increaseof the cervical [1] Common aquaticadaptation trend confirmed lordosis. in all four generaof the order.

74 INUZUKA _ AQUATIQUEADAPIATION IN DESMOSTYLI.ANS

Trends Paleoparadoxiidae Desmostylidae [Adaptationcategory #] Behemolops Paleoparadoxia Ashoroa Desmostvlus

Wideningof cranium + + Regressionof nasalbones . + + Rise of orhit + + + Weakeningof ridge of occipital condyles [4] + ++

Shorteningof cervicalvertebrae...... + + Strengtheningof cervicallordosis [7] + Shorteningof vertebralbodies + + + Shallowingof atlantalfossa [5] ...... + + Widenino of rxis f4l + + ++ Enlargementof densof axis + + Shorteningof spinousprocess of thoracicv. [4] + + ++ Steeperinclination of spinein midthoracicv. [4] + + ++ Shorteningof lumbarvertebral body [1] + + + + Increasein distancebetween zygapophyses ..... + + ++ ++ Gentlerinclination of articularsurfaces [61 + Horizontalprojection of transverseprocesses [1] + + + + Enlargementof sacralforamina t5l .... ++ + Shorteningof spinousprocess in sacrum + + +

Reductionof coracoidprocess t3l .. -+ Shallowingof glenoidcavity t4l ...... ++ +++ Thickening of humeralshaft . + ++ Loweringof capitulumbelow trochlea + ++ Wideningof antebrachialepiphyses [3] + + -+ Thickeningofantebrachial shaft [4] ... + +++ Extensionof olecranonI3l .... + -+

Reduction of sacroiliac angle + Shallowing of acetabulum [3] + + Advanceof acetabulum...... + + F.xtensionof nrrhis + + Reductionof ischialtuberosity tll ... + + + Reductionof horizontalangle of pelvic symphysis + + Shorfenins of femrrr + + + Wideningand thinning of femoralepiphyses [1] + + + + Enlargementof femoral head [4] + + + ++ Flatteningof femoral shaft [5] + ++ + ++ Shallowingof patellarsurface of femur + + + Widening of patellar surfaceof femur + + + Wideningof tibial epiphyses + + + Shallowingof ffochleatali groovel2l ... + + Tablel. Charactersand trends of aquaticadaptation in theDesmostylia +, ++ indicateabsence, presence, or conspicuouspresence, respectively,of the adaptivecharacter or trend.Blank indicatesno fossil evidence.

75 ORYCTOS,Vol.3,2000

For many featuresobserved in Paleoparadoxia andDesmostylus the evolutionarystage at which they Figure 2. Simplified phylogenetic tree were acquiredcannot be suggested,because the same of four desmostylian genera. bonesare not preservedin Behemotopsand Ashoroa. Illustrated life restorations Also, theseassigned categories may be newly set or are after Ijiri & Inuzuka (1989). changedwith future fossil discoveries.

Paleoparadoxiidae Desmostylidae

MIOCENE Paleoparadoxia Desmostylus 171 23 Ma

UPPER OLIGOCENE Behemotops Ashoroa t4l

DISCUSSION AND CONCLUSION mammals.The changefrom ventrolateralto horizon- tal projection of the lumbar vertebraltransverse pro- Because there are so few specimensto work cessessuggests increased development of the psoas with, the significanceof the quantitativecomparison major which, when accompaniedby proper dorsal of adaptationcharacteristics is not strong.Therefore, muscles,would probably be the primary muscle for it will be attemptedhere to assignfunctional signifi- dorso-ventralmovement of the trunk. Widening and canceto the adaptivecharacters based on joint kine- thinning of the distofemoral epiphysesmay imply not siology,functional morphology of the musculoskele- only flexion and extensionbut also somerotation in tal system, and comparative morphology of living the kneejoint.

76 INUZUKA _ AQUATIQIJEADAPTATION IN DESMOSTYLIANS

Shallowing of the trochleatali groove may indi- Desmostylusprobably restedmore easily on the sur- cate a capacity for rotation in the ankle joint. Since face of the water owing to the strong cervical lordo- the scapularcoracoid process in desmostyliansjoins sis. Therefore,among the Desmostylia,Desmostylus the anteriormargin of the glenoid cavity, a reduction was the animal most adaptedfor aquaticlife. of the process means a shallowing of the glenoid cavity and increasedfreedom of movement in the shoulderjoint. Lengtheningof the olecranonchanges ACKNO\ryLEDGEMENT the lever ratio of the tricepsbrachii muscle,thus may strengthenelbow joint extension.Shallowing of the I would like to thank the Ashoro Museum of acetabulumincreases freedom of movement in the Paleontology for allowing me accessto specimens hip joint. Weakeningof the occipital condyle trans- for comparison. verseridges makesdorso-ventral movement possible at the atlantooccipitaljoint, which correlateswith a shortening of the cervical region, as observed in REFERENCES DOMNING, D.P.;RAY, C.E. & MCKENNA, M.C. 1986.Tlvo new whalesand elephants. Short and steeplyinclined spi- Oligocenedesmostylians and a discussionof tethytheriansyste- nous processesof the mid+horacic vertebraeflatten matics.Smithsonian Contributions to Paleobiolo gy, 59: I -56. the outline of the back at its highest point and may UIRI, S. & INUZUKA, N. 1989.Extinct giant mammalsin Japan. add to a streamliningof the trunk. Shallowing of the 242 p., Tsukiji Shokan,Tokyo. atlantalfossa would relateto an increaseddorso-ven- & KAMEI, T. 1961.On the skullsof Desmostylusmirabi- tral movementof the head,as doesthe weakeningof /is Nagao from south Sakhalin and of Paleoparadoxiatabatai (Tokunaga)from Gifu Prefecture,Japan. Earth Science,53: l-27. the occipital condyle ridges. Enlargement of the INUZUKA, N. 1984. Studies and problems on the order sacral foramina reduces the weight of the sacrum, Desmostylia.The Association for the GeologicalCollaboration and may signify a reducedrole in bodily supportdue in Japan,Monograph,2S: l-12. to the buoyancyof water.Increased cervical lordosis -- 2000a.Research trends and scopeof the means that the head is held higher than the trunk, order Desmostylia.Bulletin of AshoroMuseum of Paleontology, which correlatsswith a floating postureat the surfa- l:9-24. 2000b. Aquatic Adaptations in ce of the water. The functional significance of the Desmostylians. Historical Biology, 14:. 97 -113. other morphologicalchanges remains unclear. - 2000c.Primitive Late Oligocenedesmosty- Many characters that distinguish the liansfrom Japanand the phylogenyof theDesmostyba. Bulletin Desmostylidae from the Paleoparadoxiidaeor of AshoroMuseum of Paleontology,l: 9L-123. Desmostylusfrom Paleoparadoxia are observedin DOMNING, D.P. & RAX C.E. 1994. the dentition and crania, and neither thesenor most Summary of taxa and morphological adaptationsof the Desmostylia.The Island Arc, 3: 522-537. postcranial features are regarded to be related to MCKENNA, M.C. 1975.Toward a phylogeneticclassification of the aquatic adaptation.Therefore, it is assumedthat the Mammalia;pp. 2l-46.1n LUCKETT, W.P. & SZALAY, F.S. divergenceof the two families was not primarily cau- (eds.) Phylogeny of the Prtmates, New York and London, sed by factors connected with aquatic habitats. PlenumPublishing Corporation. Differencesbetween these families in degreeof adap- NAGAO, T. 1941.On the skeletonof Desmostylus;pp. 43-52.In tation in eachbody part are slight. It appearsthat the Jubilee Publication in the Commemorationof Prof. H. Yabe's 60th Birthday. Paleoparadoxiidaeincreased rotational function of REINHART,R.H. 1959.A review of the Sireniaand Desmostylia. the ankle,whereas the Desmostylidaeincreased free- Universityof California Publicationsin GeologicalSciences, dom of movementin the fore- and hindlimbs and in 36: l-L46. the power of elbow extension.Adaptations for aqua- SHIKAMA, T. 1957.On the desmostylidskeleton. Natural Science tic life are more numerous in the family andMuseum,?A (l-2): 16-21. Desmostylidae,i.e., in the evolutionaryprocess from : 1966. Postcranialskeletons of Japanese Desmostylia.P alaeontolo gical Society of Japan,Sp ecîal Pape7 Ashoroa to Desmostylus, than in the 12: l-202. Paleoparadoxiidae.For instance, the desmostylids VANDERHOOR V.L. 1937. A study of the Miocene sirenian could swim more effectively than paleoparadoxiids, Desmostylus. University of Califurnia Publications in because the back became flatter. Moreover. Geolo gical Science s, 24: 169-262.

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