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The Hind Limbs of Sobrarbesiren cardieli (Eocene, Northeastern Spain) and New Insights into the Locomotion Capabilities of the Quadrupedal Sirenians

  • Ester Díaz-BerenguerEmail author
  • Alexandra Houssaye
  • Ainara Badiola
  • José Ignacio Canudo
Original Paper

Abstract

In the transition from a terrestrial to an aquatic environment, sirenian marine mammals reduced and lost their hind limbs and developed a horizontal caudal fin, the main propulsive organ in extant sirenians. Quadrupedal forms are only known from the Eocene and are represented by three different clades: the amphibious “prorastomids,” the aquatic quadrupedal protosirenids, and Sobrarbesiren cardieli, a four-legged sirenian from the middle Eocene of Spain, considered the sister taxon of the fully aquatic Dugongidae. This ecological shift from terrestrial to an aquatic environment was naturally associated with adaptations, among others, of the skeleton. However, sirenian hind limb bones have been poorly studied because of the scarce material available in the fossil record. Here, we describe in detail the hind limb bones of Sobrarbesiren, analyzing their functional morphology and comparing them with other basal sirenians and cetaceans, and with related terrestrial mammals such as proboscideans and hyracoids. The hind limbs of Sobrarbesiren were capable of a great variety of movements. Based on the presence of a strong sacroiliac articulation, we propose that it swam by dorsoventral pelvic undulation combined with pelvic paddling analogous to extant otters and the “prorastomid” Pezosiren. We also conduct the first microanatomical analysis of hind limb bones of an Eocene sirenian. Data reveal extreme inner compactness in the Sobrarbesiren innominate and femur, with the first description of osteosclerosis in an amniote innominate combined with the highest degree of osteosclerosis observed in amniote femora. The results confirm that the microanatomical changes precede the external morphological changes in such ecological transitions. The process of adaptation of sirenians to an aquatic life was thus a more complex process than previously thought.

Keywords

Marine mammals Aquatic adaptation Bone microanatomy Functional morphology 

Supplementary material

10914_2019_9482_MOESM1_ESM.docx (202 kb)
ESM 1 (DOCX 201 kb)

References

  1. Abel O (1904) Die Sirenen der mediterranen Tertiärbildungen Österreichs. Abh Geol Reichsanst Wien 19 (2):1–223Google Scholar
  2. Abel O (1907) Die Stammesgeschichte der Meeressäugetiere. Meereskunde 1:1–36Google Scholar
  3. Abel R, Macho GA (2011) Ontogenetic changes in the internal and external morphology of the ilium in modern humans. J Anat 218:324–335.  https://doi.org/10.1111/j.1469-7580.2011.01342.x
  4. Adam PJ (2018) Hind limb anatomy. In: Kovacs K, Würsig B, Thewissen JGM (eds) Encyclopedia of Marine Mammals, Third Edition. Academic-Elsevier Press, London, pp 470–472CrossRefGoogle Scholar
  5. Amson E, Argot C, McDonald HG, Muizon C de (2015) Osteology and functional morphology of the hind limb of the marine sloth Thalassocnus (Mammalia, Tardigrada). J Mammal Evol 22:355–419.  https://doi.org/10.1007/s10914-014-9274-5
  6. Amson E, Muizon C de, Laurin M, Argot C, Buffrénil V de (2014) Gradual adaptation of bone structure to aquatic lifestyle in extinct sloths from Peru. Proc R Soc Lond B: Biol Sci 281:20140192.  https://doi.org/10.1098/rspb.2014.0192
  7. Andrews CW (1902) Preliminary note on some recently discovered extinct vertebrates from Egypt, part III. Geol Mag 9:291–295CrossRefGoogle Scholar
  8. Andrews CW (1904) Further notes on the mammals of the Eocene of Egypt. Geol Mag 1:211–215CrossRefGoogle Scholar
  9. Andrews CW (1906) A Descriptive Catalogue of the Tertiary Vertebrata of the Fayum, Egypt. British Museum of Natural History, LondonGoogle Scholar
  10. Arita HT (2016) Crónicas de la extinción. La vida y la muerte de las especies animales. Fondo de Cultura Económica, MéxicoGoogle Scholar
  11. Astibia H, Bardet N, Pereda-Suberbiola X, Payros A, Buffrénil V de, Elorza J, Tosquella J, Berreteaga A, Badiola A (2010) New fossils of Sirenia from the middle Eocene of Navarre (western Pyrenees): the oldest West European sea cow record. Geol Mag 147:665–673.  https://doi.org/10.1017/S0016756810000130
  12. Astibia H, Payros A, Suberbiola XP, Elorza J, Berreteaga A, Etxebarria N, Badiola A, Tosquella J (2005) Sedimentology and taphonomy of sirenian remains from the middle Eocene of the Pamplona Basin (Navarre, western Pyrenees). Facies 50:463–475.  https://doi.org/10.1007/s10347-004-0026-5 CrossRefGoogle Scholar
  13. Bajpai S, Domning DP, Das DP, Mishra VP (2009) A new middle Eocene sirenian (Mammalia, Protosirenidae) from India. Neues Jahrb Geol Paläontol - Abh 11:257–267CrossRefGoogle Scholar
  14. Balaguer J, Alba DM (2016) A new dugong species (Sirenia, Dugongidae) from the Eocene of Catalonia (NE Iberian Peninsula). C R Palevol 15:489–500.  https://doi.org/10.1016/j.crpv.2015.10.002 CrossRefGoogle Scholar
  15. Barone R (1976) Antomie comparée des mammifères domestiques. Vigot Freres, ParisGoogle Scholar
  16. Beatty BL, Geisler J (2010) A stratigraphically precise record of Protosiren (Protosirenidae, Sirenia) from North America. Neues Jahrb Geol Paläontol-Abh 258:185–194CrossRefGoogle Scholar
  17. Bebej RM, ul-Haq M, Zalmout IS, Gingerich PD (2012) Morphology and function of the vertebral column in Remingtonocetus domandaensis (Mammalia, Cetacea) from the middle Eocene Domanda Formation of Pakistan. J Mammal Evol 19:77–104.  https://doi.org/10.1007/s10914-011-9184-8 CrossRefGoogle Scholar
  18. Bebej RM, Zalmout IS, El-Aziz AAA, Sameh M, Antar M, Gingerich PD (2015) First remingtonocetid archaeocete (Mammalia, Cetacea) from the middle Eocene of Egypt with implications for biogeography and locomotion in early cetacean evolution. J Paleontol 89:882–893.  https://doi.org/10.1017/jpa.2015.57 CrossRefGoogle Scholar
  19. Benoit J, Adnet S, El Mabrouk E, Khayati H, Ben Haj Ali M, Marivaux L, Merzeraud G, Merigeaud M, Vianey-Liaud M, Tabuce R (2013) Cranial remain from Tunisia provides new clues for the origin and volution of Sirenia (Mammalia, Afrotheria) in Africa. PLoS One 8:e54307.  https://doi.org/10.1371/journal.pone.0054307
  20. Berta A, Ray CE (1990) Skeletal morphology and locomotor capabilities of the archaic pinniped Enaliarctos mealsi. J Vertebr Paleontol 10:141–157.  https://doi.org/10.1080/02724634.1990.10011803 CrossRefGoogle Scholar
  21. Berta A, Sumich JL, Kovacs KM (2015) Marine Mammals: Evolutionary Biology, Third Edition. Academic Press, LondonGoogle Scholar
  22. Bodkin J (2001) Sea otters. In: Steele JH, Turekian KK, Thorpe SA (eds) Encyclopedia of Ocean Sciences. Academic Press, Oxford, pp 2614–2621CrossRefGoogle Scholar
  23. Buchholtz EA (1998) Implications of vertebral morphology for locomotor evolution in early Cetacea. In: Thewissen JGM (ed) The Emergence of Whales: Evolutionary Patterns in the Origin of Cetacea. Springer US, Boston, pp 325–351CrossRefGoogle Scholar
  24. Buffrénil V de, Astibia H, Pereda Suberbiola X, Berreteaga A, Bardet N (2008) Variation in bone histology of middle Eocene sirenians from western Europe. Geodiversitas 30:425–432Google Scholar
  25. Buffrénil V de, Canoville A, D’Anastasio R, Domning DP (2010) Evolution of sirenian pachyosteosclerosis, a model-case for the study of bone structure in aquatic tetrapods. J Mammal Evol 17:101–120.  https://doi.org/10.1007/s10914-010-9130-1
  26. Canudo JI (2018) The collection of type fossils of the Natural Science Museum of the University of Zaragoza (Spain). Geoheritage 10:385–392.  https://doi.org/10.1007/s12371-017-0228-1
  27. Court N (1994) Limb posture and gait in Numidotherium koholense, a primitive proboscidean from the Eocene of Algeria. Zool J Linn Soc 111:297–338.  https://doi.org/10.1111/j.1096-3642.1994.tb01487.x CrossRefGoogle Scholar
  28. Cunningham CA, Black SM (2009) Anticipating bipedalism: trabecular organization in the newborn ilium. J Anat 214:817–829.  https://doi.org/10.1111/j.1469-7580.2009.01073.x
  29. Davis DD (1964) The giant panda. A morphological study of evolutionary mechanism. Fieldiana: Zool Mem 3:1–334Google Scholar
  30. Dewaele L, Lambert O, Laurin M, de Kock T, Louwye S, Buffrénil V de (2018) Generalized osteosclerotic condition in the skeleton of Nanophoca vitulinoides, a dwarf seal from the Miocene of Belgium. J Mammal Evol.  https://doi.org/10.1007/s10914-018-9438-9
  31. Díaz-Berenguer E, Badiola A, Moreno-Azanza M, Canudo JI (2018) First adequately-known quadrupedal sirenian from Eurasia (Eocene, Bay of Biscay, Huesca, northeastern Spain). Sci Rep 8:5127.  https://doi.org/10.1038/s41598-018-23355-w CrossRefGoogle Scholar
  32. Domning DP (1978) Sirenian evolution in the North Pacific Ocean. Univ Calif Publ Geol Sci 118:1–179Google Scholar
  33. Domning DP (1996) Bibliography and index of the Sirenia and Desmostylia. Smithsonian Contrib Paleobiol 80:1–611Google Scholar
  34. Domning DP (2000) The readaptation of Eocene sirenians to life in water. Hist Biol 14:115–119.  https://doi.org/10.1080/10292380009380559
  35. Domning DP (2001a) Sirenians, seagrasses, and Cenozoic ecological change in the Caribbean. Palaeogeogr Palaeoclimatol Palaeoecol 166:27–50.  https://doi.org/10.1016/S0031-0182(00)00200-5 CrossRefGoogle Scholar
  36. Domning DP (2001b) The earliest known fully quadrupedal sirenian. Nature 413:625–627.  https://doi.org/10.1038/35098072 CrossRefGoogle Scholar
  37. Domning DP (2002) The terrestrial posture of desmostylians. Smithsonian Contrib Paleobiol 93:99–111Google Scholar
  38. Domning DP, Buffrénil V de (1991) Hydrostasis in the Sirenia: quantitative data and functional interpretations. Mar Mam Sci 7:331–368Google Scholar
  39. Domning DP, Gingerich PD (1994) Protosiren smithae, new species (Mammalia, Sirenia) from the late middle Eocene of Wadi Hitan, Egypt. Contrib Mus Paleontol Univ Mich 29:69–87Google Scholar
  40. Domning DP, Heal GJ, Sorbi S (2017) Libysiren sickenbergi, gen. et sp. nov.: a new sirenian (Mammalia, Protosirenidae) from the middle Eocene of Libya. J Vertebr Paleontol 37:e1299158.  https://doi.org/10.1080/02724634.2017.1299158
  41. Domning DP, Morgan GS, Ray CE (1982) North American Eocene sea cows (Mammalia: Sirenia). Smithsonian Contrib Paleobiol 52:1-69Google Scholar
  42. Domning DP, Zalmout IS, Gingerich PD (2010) Sirenia. In: Wenderlin L, Sanders WJ (eds) Cenozoic Mammals of Africa. University of California Press, Berkeley, pp 147–160Google Scholar
  43. Dreyer T, Corregidor J, Arbues P, Puigdefabregas C (1999) Architecture of the tectonically influenced Sobrarbe deltaic complex in the Ainsa Basin, northern Spain. Sediment Geol 127:127–169.  https://doi.org/10.1016/S0037-0738(99)00056-1 CrossRefGoogle Scholar
  44. Dumont M, Laurin M, Jacques F, Pellé E, Dabin W, Buffrénil V de (2013) Inner architecture of vertebral centra in terrestrial and aquatic mammals: a two-dimensional comparative study. J Morphol 274:570–584.  https://doi.org/10.1002/jmor.20122
  45. Fish FE (1994) Association of propulsive swimming mode with behaviour in river otters (Lutra canadensis). J Mammal 75:989–997CrossRefGoogle Scholar
  46. Fish FE (1996) Transitions from drag-based to lift-based propulsion in mammalian swimming. Integr Comp Biol 36:628–641.  https://doi.org/10.1093/icb/36.6.628 Google Scholar
  47. Getty R, Sisson S (1975) Sisson and Grossman’s The Anatomy of the Domestic Animals. Saunders, PhiladelphiaGoogle Scholar
  48. Gingerich PD (2003) Land-to-sea transition in early whales: evolution of Eocene Archaeoceti (Cetacea) in relation to skeletal proportions and locomotion of living semiaquatic mammals. Paleobiology 29:429–454.  https://doi.org/10.1666/00948373(2003)029<0429:LTIEWE>2.0.CO;2
  49. Gingerich PD, Arif M, Bhatti MA, Anwar M, Sanders WJ (1997) Basilosaurus drazindai and Basiloterus hussaini, new Archaeoceti (Mammalia, Cetacea) from the middle Eocene Drazinda Formation, with a revised interpretation of ages of whale bearing strata in the Kirthar group of the Sulaiman range, Punjab (Pakistan). Contrib Mus Paleontol Univ Mich 30:55–81Google Scholar
  50. Gingerich PD, Arif M, Bhatti MA, Raza HA, Raza SM (1995) Protosiren and Babiacetus (Mammalia, Sirenia and Cetacea) from the middle Eocene Drazinda Formation, Sulaiman Range, Punjab (Pakistan). Contrib Mus Paleontol Univ Mich 29:331–357Google Scholar
  51. Gingerich PD, Cappetta H (2014) A new archaeocete and other marine mammals (Cetacea and Sirenia) from lower middle Eocene Phosphate Deposits of Togo. J Paleontol 88:109–129.  https://doi.org/10.1666/13-040
  52. Gingerich PD, Domning DP, Blane CE, Uhen MD (1994a) Cranial morphology of Protosiren fraasi (Mammalia, Sirenia) from the middle Eocene of Egypt: a new study using computed tomography. Contrib Mus Paleontol Univ Mich 29:41–67Google Scholar
  53. Gingerich PD, Raza SM, Arif M, Anwar M, Zhou X (1994b) New whale from the Eocene of Pakistan and the origin of cetacean swimming. Nature 368:844–847.  https://doi.org/10.1038/368844a0 CrossRefGoogle Scholar
  54. Gingerich PD, Smith BH, Simons EL (1990) Hind limbs of Eocene Basilosaurus: evidence of feet in whales. Science 249:154–157.  https://doi.org/10.1126/science.249.4965.154 CrossRefGoogle Scholar
  55. Gingerich PD, ul-Haq M, Khan IH, Zalmout IS (2001) Eocene stratigraphy and archaeocete whales (Mammalia, Cetacea) of Drug Lahar in the Eastern Sulaiman Range, Balochistan (Pakistan). Contrib Mus Paleonto Univ Mich 30:269–319Google Scholar
  56. Gingerich PD, ul-Haq M, Koenigswald W von, Sanders WJ, Smith BH, Zalmout IS (2009) New protocetid whale from the middle Eocene of Pakistan: birth on land, precocial development, and sexual dimorphism. PLoS One 4:e4366.  https://doi.org/10.1371/journal.pone.0004366
  57. Gray N-M, Kainec K, Madar S, Tomko L, Wolfe S (2007) Sink or swim? Bone density as a mechanism for buoyancy control in early cetaceans. Anat Rec 290:638–653.  https://doi.org/10.1002/ar.20533 CrossRefGoogle Scholar
  58. Hardt AB, Jee WSS (1982) Trabecular bone structural variation in biopsy sites of the beagle ilium. Calcified Tissue Internatl 34(1):391–395CrossRefGoogle Scholar
  59. Harrison TJ (1961) The influence of the femoral head on pelvic growth and acetabular form in the rat. J Anat 95(Pt 1):12Google Scholar
  60. Hautier L, Sarr R, Lihoreau F, Tabuce R, Hameh PM (2014) First record of the family Protocetidae in the Lutetian of Senegal (West Africa). Palaeovertebrata 38 (2):1-7.  https://doi.org/10.18563/pv.38.2.e2
  61. Hautier L, Sarr R, Tabuce R, Lihoreau F, Adnet S, Domning DP, Samb M, Hameh PM (2012) First prorastomid sirenian from Senegal (western Africa) and the Old World origin of sea cows. J Vertebr Paleontol 32:1218–1222.  https://doi.org/10.1080/02724634.2012.687421 CrossRefGoogle Scholar
  62. Hayashi S, Houssaye A, Nakajima Y, Chiba K, Ando T, Sawamura H, Inuzuka N, Kaneko N, Osaki T (2013) Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria). PLoS One 8:e59146.  https://doi.org/10.1371/journal.pone.0059146 CrossRefGoogle Scholar
  63. Hooijer DA (1952) Fact and fiction in Hippopotamology (sampling the history of scientific error). Osiris 10:109–116CrossRefGoogle Scholar
  64. Houssaye A (2009) “Pachyostosis” in aquatic amniotes: a review. Integr Zool 4:325–340.  https://doi.org/10.1111/j.1749-4877.2009.00146.x CrossRefGoogle Scholar
  65. Houssaye A (2013) Palaeoecological and morphofunctional interpretation of bone mass increase: an example in Late Cretaceous shallow marine squamates. Biol Rev 88:117–139.  https://doi.org/10.1111/j.1469-185X.2012.00243.x CrossRefGoogle Scholar
  66. Houssaye A, Botton-Divet L (2018) From land to water: evolutionary changes in long bone microanatomy of otters (Mammalia: Mustelidae). Biol J Linn Soc 125:240–249.  https://doi.org/10.1093/biolinnean/bly118 CrossRefGoogle Scholar
  67. Houssaye A, Sander PM, Klein N (2016) Adaptive patterns in aquatic amniote bone microanatomy—more complex than previously thought. Integr Comp Biol 56:1349–1369.  https://doi.org/10.1093/icb/icw120
  68. Houssaye A, Tafforeau P, Muizon C de, Gingerich PD (2015) Transition of Eocene whales from land to sea: evidence from bone microstructure. PLoS One 10:e0118409.  https://doi.org/10.1371/journal.pone.0118409
  69. Hulbert RC, Petkewich RM, Bishop GA, Bukry D, Aleshire DP (1998) A new middle Eocene protocetid whale (Mammalia: Cetacea: Archaeoceti) and associated biota from Georgia. J Paleontol 72:907–927.  https://doi.org/10.1017/S0022336000027232 CrossRefGoogle Scholar
  70. Jenkins FA Jr, Camazine SM (1977) Hip structure and locomotion in ambulatory and cursorial carnivores. J Zool 181:351–370.  https://doi.org/10.1111/j.1469-7998.1977.tb03249.x CrossRefGoogle Scholar
  71. Kaiser HE (1960) Untersuchungen zur vergleichenden Osteologie der fossilen und rezenten Pachyostosen. Palaeontographica A 114:113–196Google Scholar
  72. Kaup JJ (1838) Über Zähnen von Halytherium und Pugmeodon aus Flonheim. Neues Jahrbuch für Geognosie, Geologie und Petrefactenkunde 318–320Google Scholar
  73. Kordos L (1977) A new upper Eocene Sirenian (Paralitherium tarkanyense n.g., n.sp.) from Felsötrárkány, NE Hungary. Magyar Állami Földtani Intézet Évi Jelentése az 1975 Évröl 1977: 349–367Google Scholar
  74. Kordos L (1979) Major finds of scattered fossils in the palaeovertebrate collection of the Hungarian Geological Institute (communication No. 4). Magyar Állami Földtani Intézet Évi jelentése az 1977 Evröl 1979: 313–326Google Scholar
  75. Kordos L (2002) Eocene sea cows (Sirenia, Mammalia) from Hungary. Fragm Palaeontol Hung 20:43–48Google Scholar
  76. Kretzoi M (1941) Sirenavus hungaricus n. g., n. sp., ein neuer Prorastomide aus dem Mitteleozän (Lutetium) von Felsőgalla in Ungarn. Ann Musei Natl Hung Pars Mineral Geol Palaeontol 34:146–156Google Scholar
  77. Laurin M, Canoville A, Germain D (2011) Bone microanatomy and lifestyle: a descriptive approach. C R Palevol 10:381–402.  https://doi.org/10.1016/j.crpv.2011.02.003 CrossRefGoogle Scholar
  78. Madar SI (2007) The postcranial skeleton of early Eocene pakicetid cetaceans. J Paleontol 81:176–200.  https://doi.org/10.1666/0022-3360(2007)81[176:TPSOEE]2.0.CO;2 CrossRefGoogle Scholar
  79. Madar SI, Thewissen JGM, Hussain ST (2002) Additional holotype remains of Ambulocetus natans (Cetacea, Ambulocetidae), and their implications for locomotion in early whales. J Vertebr Paleontol 22:405–422.  https://doi.org/10.1671/0272-4634(2002)022[0405:AHROAN]2.0.CO;2 CrossRefGoogle Scholar
  80. Mahboubi M, Ameur R, Crochet JY, Jaeger JJ (1986) El Kohol (Saharan Atlas, Algeria): a new Eocene mammal locality in North−West Africa. Palaeontographica A 192: 15–49.Google Scholar
  81. McDonald HG, Muizon C de (2002) The cranial anatomy of Thalassocnus (Xenarthra, Mammalia), a derived nothrothere from the Neogene of the Pisco Formation (Peru). J Vertebr Paleontol 22(2): 349–365Google Scholar
  82. Mochales T, Barnolas A, Pueyo EL, Serra-Kiel J, Casas AM, Samsó JM, Ramajo J, Sanjuán J (2012) Chronostratigraphy of the Boltana anticline and the Ainsa Basin (southern Pyrenees). Geol Soc Am Bull 124:1229–1250.  https://doi.org/10.1130/B30418.1 CrossRefGoogle Scholar
  83. Muizon C de, McDonald HG (1995) An aquatic sloth from the Pliocene of Peru. Nature 375:224–227.  https://doi.org/10.1038/375224a0
  84. Murie J, Mivart GJ (1865) On the myology of Hyrax capensis. Proc Zool Soc Lond 33 (1):329–352CrossRefGoogle Scholar
  85. Owen R (1855) On the fossil skull of a mammal (Prorastomus sirenoides Owen) from the island of Jamaica. Q J Geol Soc London 11:541–543Google Scholar
  86. Pales L, Lambert C (1971) Atlas ostéologique pour servir à la identification des mammifères du quaternaire. Éditions du Centre national de la recherche scientifique, ParisGoogle Scholar
  87. Palmer TS (1899) Catalogus Mammalium tam viventium quam fossilium. Science 10:491–495CrossRefGoogle Scholar
  88. Pérez-García A, Díaz-Berenguer E, Badiola A, Canudo JI (2019) An unexpected finding: identification of the first complete shell of the Franco-Belgian middle Eocene littoral pleurodiran turtle Eocenochelus eremberti in Spain Hist Biol.  https://doi.org/10.1080/08912963.2019.1644330  
  89. Pilleri G, Biosca J, Via L (1989) The Tertiary Sirenia of Catalonia. Brain Anatomy Institute, University of Berne, OstermundingenGoogle Scholar
  90. Quemeneur S, Buffrénil V de, Laurin M (2013) Microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates. Biol J Linn Soc 109:644–655.  https://doi.org/10.1111/bij.12066
  91. Ricqlès A de, Buffrénil V de (2001) Bone histology, heterochronies and the return of tetrapods to life in water: where are we? In: Mazin J-M, Buffrénil V de (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr. Friedrich Pfeil, München, pp 289–310Google Scholar
  92. Sagne C (2001) Halitherium taulannense, nouveau sirénien (Sirenia, Mammalia) de l’Éocène supérieur provenant du domaine Nord-Téthysien (Alpes-de-Haute-Provence, France). Comptes Rendus de l’Académie des Sciences - Series IIA - Earth and Planetary Science 333:471–476.  https://doi.org/10.1016/S1251-8050(01)01661-5 Google Scholar
  93. Savage RJ (1976) Review of early Sirenia. Syst Zool 25:344–351CrossRefGoogle Scholar
  94. Shil SK, Quasem MA, Rahman ML, Kibria ASMG, Uddin M, Ahasan ASML (2013) Macroanatomy of the bones of pelvis and hind limb of an Asian Elephant (Elephas maximus). Internatl J Morphol 31:1473–1478CrossRefGoogle Scholar
  95. Sickenberg O (1934) Beiträge zur Kenntnis Tertiärer Sirenen. I. Die eozänen Sirenen des Mittelmeergebietes. II. Die Sirenen des Belgischen Tertiärs. Mém Mus R d’Hist Nat Belg 63:1–352Google Scholar
  96. Siegfried P (1967) Das femur von Eotheroides libyca (Owen) (Sirenia). Paläontol Z 41:165–172CrossRefGoogle Scholar
  97. Smuts MM, Bezuidenhout AJ (1994) Osteology of the pelvic limb of the African elephant (Loxodonta africana). Onderstepoort J Vet Res 61:51–66Google Scholar
  98. Stromer von Reichenbach E (1921) Untersuchungen der Hüftbeine und Hüftgelenke von Sirenia und Archaeoceti. Sitzb Bayer Akad Wiss 1:41–59Google Scholar
  99. Thewissen JGM, Williams EM, Roe LJ, Hussain ST (2001) Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls. Nature 413:277–281.  https://doi.org/10.1038/35095005 CrossRefGoogle Scholar
  100. Uhen MD (1998) New protocetid (Mammalia, Cetacea) from the late middle Eocene Cook Mountain Formation of Louisiana. J Vertebr Paleontol 18(3):664–668CrossRefGoogle Scholar
  101. Uhen MD (2004) Form, function, and anatomy of Dorudon atrox (Mammalia, Cetacea): an archaeocete from the middle to late Eocene of Egypt. Univ Mich Mus Paleontol Pap Paleontol 34:1–222Google Scholar
  102. Uhen MD (2008a) Marine mammals summary. In: Janis CM, Gunnell GF, Uhen M (eds) Evolution of Tertiary Mammals of North America, Volume 2: Small Mammals, Xenarthrans, and Marine Mammals. Cambridge University Press, Cambridge, pp 507–522CrossRefGoogle Scholar
  103. Uhen MD (2008b) New protocetid whales from Alabama and Mississippi, and a new cetacean clade, Pelagiceti. J Vertebr Paleontol 28:589–593.  https://doi.org/10.1671/0272-4634(2008)28[589:NPWFAA]2.0.CO;2 CrossRefGoogle Scholar
  104. Uhen MD (2014) New material of Natchitochia jonesi and a comparison of the innominata and locomotor capabilities of Protocetidae. Mar Mamm Sci 30:1029–1066.  https://doi.org/10.1111/mms.12100
  105. Van Beneden PJ (1876) Les phoques fossiles du bassin d’Anvers. Bull Acad R Sci Lettr Beaux-Arts Belg 41:783–803Google Scholar
  106. Volpato V, Viola TB, Nakatsukasa M, Bondioli L, Macchiarelli R (2008) Textural characteristics of the iliac-femoral trabecular pattern in a bipedally trained Japanese macaque. Primates 49:16–25.  https://doi.org/10.1007/s10329-007-0053-2 CrossRefGoogle Scholar
  107. Watkins J (1999) Mechanical characteristics of musculoskeletal components. In: Watkins J (ed) Structure and Function of the Musculoskeletal System. Human Kinetics, Champaign, pp 285–308Google Scholar
  108. Weissengruber GE, Fuss FK, Egger G, Stanek G, Hittmair KM, Forstenpointner G (2006) The elephant knee joint: morphological and biomechanical considerations. J Anat 208:59–72.  https://doi.org/10.1111/j.1469-7580.2006.00508.x CrossRefGoogle Scholar
  109. Zalmout IS, Gingerich PD (2012) Late Eocene seacows (Mammalia, Sirenia) from Wadi Al Hitan in the Western Desert of Fayum, Egypt. Univ Mich Pap Paleontol 387:1–158Google Scholar
  110. Zigno A de (1887) Quelques observations sur les Siréniens fossiles. Bull Soc Géol Fr 15:728–732Google Scholar
  111. Zimmermann EA (1780) Geographische Geschichte des Menschen und der Allgemein verbreiteten vierfüssigen Thiere. Weygandschen Buchhandlung, LeipzigGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Grupo Aragosaurus-IUCA, Departamento de Ciencias de la Tierra, Área de PaleontologíaUniversidad de ZaragozaZaragozaSpain
  2. 2.Département Adaptations du VivantUMR 7179 CNRS/Muséum National d’Histoire NaturelleParisFrance
  3. 3.Departamento de Estratigrafía y Paleontología, Facultad de Ciencia y TecnologíaUniversidad del País Vasco (UPV/EHU)BilbaoSpain

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