- Leonard Dewaele ORCID:orcid.org/0000-0003-1188-25151,2,
- Olivier Lambert2,
- Michel Laurin3,
- Tim De Kock4,
- Stephen Louwye1 &
- …
- Vivian de Buffrénil3
673Accesses
13Altmetric
1Mention
Abstract
In the fossil record, it has been shown that various clades of secondarily aquatic tetrapods experienced an initial densification of their bones in the early stages of their evolution, and developed spongier and lighter bones only later in their evolution, with the acquisition of more efficient swimming modes. Although the inner bone structure of most secondarily aquatic tetrapods has already been studied, no research hitherto focused on true seals, or Phocidae. However, preliminary observations previously made on a Miocene species,Nanophoca vitulinoides, suggested that this taxon showed pronounced specialization of bone structure as compared to other seals. This feature justifies a specific comparative study, which is the purpose of this article. Microanatomical analysis of bones ofN. vitulinoides shows compactness values nearing 100%, which is much higher than in other semi-aquatic mammals, pinnipeds included. Osteohistological analyses show virtually complete remodeling of the medullary territory by Haversian substitution. Extreme bone compactness locally resulted from an imbalance, towards reconstruction, of this process. Cortical regions were less intensely remodeled. In a number of specimens, the cortex shows clear growth marks as seasonal lines of arrested growth. The results suggest that, despite the extreme compactness of long bones ofN. vitulinoides and the small size of this taxon, the growth rate of the cortex, and that of the bones in general, did not differ strongly from that of other, larger phocids. Extreme skeletal compaction and densification must have increased body density inNanophoca. Consequently, speed, acceleration, and maneuverability must have been low, and this taxon was most likely a near-shore bottom-dwelling seal. Consequently, dietary preferences were most likely oriented towards benthic food sources.
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References
Amprino R (1947) La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l’accroissement. Arch Biol 58:315–330
Amson E, Muizon C de (2014) A new durophagous phocid (Mammalia: Carnivora) from the late Neogene of Peru and considerations on monachine seal phylogeny. J Syst Palaeontol 12:523–548. doi:https://doi.org/10.1080/14772019.2013.799610
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 Biol Soc 281:20140192. doi:https://doi.org/10.1098/rspb.2014.0192
Beentjes MP (1990) Comparative terrestrial locomotion of the Hooker's sea lion (Phocarctos hookeri) and the New Zealand fur seal (Arctocephalus forsteri): evolutionary and ecological implications. Zool J Linn Soc 98:307–325. doi:https://doi.org/10.1111/j.1096-3642.1990.tb01204.x
Berta A, Kienle S, Bianucci G, Sorbi S (2015) A reevaluation ofPliphoca etrusca (Pinnipedia, Phocidae) from the Pliocene of Italy: phylogenetic and biogeographic implications. J Vertebr Paleontol 35:e88944. doi:https://doi.org/10.1080/02724634.2014.889144
Bininda-Emonds ORP, Russell AP (1996) A morphological perspective on the phylogenetic relationships of the extant phocid seals (Mammalia: Carnivora: Phocidae). Bonn Zool Monogr 41:1–256
Boness DJ, Bowen WD (1996) The evolution of maternal care in pinnipeds. Bioscience 46:645–654
Burr DB (1993) Remodeling and the repair of fatigue damage. Calcif Tissue Internatl 53 (suppl 1):S75–S81. doi:https://doi.org/10.1007/BF01673407
Burr DB, Allen MR (eds) (2014) Basic and Applied Bone Biology. Elsevier/Academic Press, London
Burr DB, Martin RB, Schaffler MB, Radin EL (1985) Bone remodeling in response toin vivo fatigue microdamage. J Biomech 18:189–200. doi:https://doi.org/10.1016/0021-9290(85)90204-0
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.doi:https://doi.org/10.1007/s10914-010-9130-1
Buffrénil V de, Casinos A (1995) Observations histologiques sur le rostre deMesoplodon densirostris (Mammalia, Cetacea, Ziphiidae): le tissu osseux le plus dense connu. Ann Sci Nat Zool 13ème Ser 16:21–32
Buffrénil V de, Mazin J-M (1989) Bone histology ofClaudiosaurus germaini (Reptilia, Claudiosauridae) and the problem of pachyostosis in aquatic tetrapods. Hist Biol 2:311–322. doi:https://doi.org/10.1080/08912968909386509
Buffrénil V de, Rage J-C (1993) La ‘pachyostose’ vertébrale deSimoliophis (Reptilia, Squamata): données comparatives et considérations fonctionnelles. Ann Paleontol (Vertebr) 79:315–335
Buffrénil V de, Ricqlès A de, Ray CE, Domning, DP (1990) Bone histology of the ribs of the archaeocetes (Mammalia: Cetacea). J Vertebr Paleontol 10:455–466. doi:https://doi.org/10.1080/02724634.1990.10011828
Buffrénil V de, Schoevaert D (1988) On how the bone of the delphinid humerus becomes cancellous: ontogeny of an histological specialisation. Journal of Morphology 198:149–164
Buffrénil V de, Schoevaert D (1989) Données quantitatives et observations histologiques sur la pachyostose du squelette du dugong,Dugong dugon (Müller) (Sirenia, Dugongidae). Can J Zool 67:2107–2119. doi:https://doi.org/10.1139/z89-300
Canoville A, Laurin M (2010) Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences. Biol J Linn Soc 100:384–406. doi:https://doi.org/10.1111/j.1095-8312.2010.01431.x
Canoville A, Buffrénil V de, Laurin M (2016) Microanatomical diversity of amniote ribs: an exploratory quantitative study. Biol J Linn Soc 118:706–733. doi:https://doi.org/10.1111/bij.12779
Castanet J (2006) Time recording in bone microstructures of endothermic animals; functional relationships. CR Palevol 5:629–636. doi:https://doi.org/10.1016/j.crpv.2005.10.006
Castanet J, Curry Rogers C, Cubo J, Boisard J (2000) Periosteal bone growth rates in extant ratites (ostrich and emu). Implications for assessing growth in dinosaurs. CR Acad Sci Paris, Sci Vie 323:543–550. doi:https://doi.org/10.1016/S0764-4469(00)00181-5
Castanet J, Grandin A, Abourachid A, Ricqlès A de (1996) Expression de la dynamique de croissance dans la structure de l’os périostique chezAnas platyrhynchos. CR Acad Sci Paris, Sci Vie 319:301–308
Charles JF, Aliprantis AO (2014) Osteoclasts: more than ‘bone eaters’. Trends Mol Med 20:449–459. doi:https://doi.org/10.1016/j.molmed.2014.06.001
Cozzuol MA (2001) A “northern” seal from the Miocene of Argentina: implications for phocid phylogeny and biogeography. J Vertebr Paleontol 21:415–421. doi: https://doi.org/10.1671/0272-4634(2001)021[0415:ANSFTM]2.0.CO;2
Danova NA, Colopy SA, Radtke CL, Kalscheur VL, Markel MD, Vanderby R Jr, McCabe RP, Escarcega AJ, Muir P (2003) Degradation of bone structural properties by accumulation and coalescence of microcracks. Bone 33:197–205. doi:https://doi.org/10.1016/S8756-3282(03)00155-8
Dehn L-A, Sheffield GG, Follmann EH, Duffy LK, Thomas DL, O’Hara TM (2006) Feeding ecology of phocid seals and some walrus in the Alaskan and Canadian Arctic as determined by stomach contents and stable isotope analysis. Polar Biol 30:167–181. doi:https://doi.org/10.1007/s00300-006-0171-0
Deméré TA (1994a) Two new species of fossil walruses (Pinnipedia: Odobenidae) from the upper Pliocene San Diego Formation. Proc San Diego Soc Nat Hist 29:77–98
Deméré TA (1994b) The family Odobenidae: a phylogenetic analysis of fossil and living taxa. Proc San Diego Soc Nat Hist 29:99–123
Dempster DW, Compston JE, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR, Parfitt AM (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 28:1–16. doi:https://doi.org/10.1002/jbmr.1805
Dewaele L, Amson E, Lambert O, Louwye S (2017a) Reappraisal of the extinct seal “Phoca”vitulinoides from the Neogene of the North Sea basin, with bearing on its geological age, phylogenetic affinities, and locomotion. PeerJ 5:e3316. doi:https://doi.org/10.7717/peerj.3316
Dewaele L, Lambert O, Louwye S (2017b) OnProphoca andLeptophoca (Pinnipedia, Phocidae) from the Miocene of the North Atlantic realm: redescription, phylogenetic affinities and paleobiogeographic implications. PeerJ 5:e3024. doi:https://doi.org/10.7717/peerj.3024
Domning D, Buffrénil V de (1991) Hydrostasis in the Sirenia: quantitative data and functional interpretation. Mar Mammal Sci 7:331–368. doi:https://doi.org/10.1111/j.1748-7692.1991.tb00111.x
Dumont M, Buffrénil V de, Mijan I, Lambert O (2016) Structure and growth pattern of the bizarre hemispheric prominence of the rostrum of the fossil beaked whaleGlobicetus huberus (Mammalia, Cetacea, Ziphiidae). J Morphol 277:1292–1308. doi:https://doi.org/10.1002/jmor.20575
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. doi:https://doi.org/10.1002/jmor.20122
Evans RA, Hughes WG, Dunstan CR, Lennon WP, Kohan L, Hills E, Wong SYP(1983) Adult osteosclerosis. Metab Bone Dis Relat 5:111–117. doi:https://doi.org/10.1016/0221-8747(83)90011-5
Fawcett DW, Jensh RP (1997) Bloom and Fawcett: Concise Histology. Chapman and Hall, New York
Fay FH (1982) Ecology and biology of the Pacific walrus,Odobenus rosmarus divergens Illiger. N Am Fauna 74:1–279. doi:https://doi.org/10.3996/nafa.74.0001
Fiala P (1980) Structure of the long limb bones and its significance in determining age in man. Folia Morphol 28:259–263
Fish FE, Hurley J, Costa DP (2003) Maneuverability by the sea lionZalophus californianus: turning performance of an unstable body design. J Exp Biol 206:667–674. doi:https://doi.org/10.1242/jeb.00144
Fish FE, Stein BR (1991) Functional correlates of differences in bone density among terrestrial and aquatic genera in the family Mustelidae (Mammalia). Zoomorphology 110:339–345. doi:https://doi.org/10.1007/BF01668024
Francillon-Vieillot H, Buffrénil V de, Castanet J, Geraudie J, Meunier JF, Sire JY, Zylberberg L, Ricqlès A de (1990) Microstructure and mineralization of vertebrate skeletal tissues. In: Carter JG (ed) Skeletal Biomineralizations: Patterns, Processes and Evolutionary Trends, Vol. 1. Van Nostrand Reinhold, New York, pp 471–530.
Frost HM (1969) Tetracycline-based histological analysis of bone remodeling. Calc Tiss Res 33:211–237. doi:https://doi.org/10.1007/BF02058664
Fulton TL, Strobeck C (2010) Multiple markers and multiple individuals refine true seal phylogeny and bring molecules and morphology back in line. Proc Roy Soc B–Biol Sci 277:1065–1070. doi:https://doi.org/10.1098/rspb.2009.1783
Germain D, Laurin M (2005) Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zool Scr 34:335–350. doi:https://doi.org/10.1111/j.1463-6409.2005.00198.x
Giles S, Rücklin M, Donoghue PCJ (2013) Histology of “placoderm” dermal skeletons: implications for the nature of the ancestral gnathostomes. J Morphol 274:627–644. doi:https://doi.org/10.1002/jmor.20119
Girondot M, Laurin M (2003) Bone Profiler: a tool to quantify, model and statistically compare bone section compactness profiles. J Vertebr Paleontol 23:458–461. doi: https://doi.org/10.1671/0272-4634(2003)023[0458:BPATTQ]2.0.CO;2
Gjertz I, Wiig Ø (1992) Feeding of walrusOdobenus rosmarus in Svalbard. Polar Record 28:57–59. doi:https://doi.org/10.1017/S0032247400020283
Godfrey SJ (1985) Additional observations of subaqueous locomotion in the California Sea Lion (Zalophus californianus). Aquat Mammal 11:53–57
Higdon JW, Bininda-Emonds ORP, Beck RMD, Ferguson SH (2007) Phylogeny and divergence of the pinnipeds (Carnivora: Mammalia) assessed using a multigene dataset. BMC Evol Biol 7 :216. doi:https://doi.org/10.1186/1471-2148-7-216
Houssaye A (2009) “Pachyostosis” in aquatic amniotes: a review. Integr Zool 4:325–340. doi:https://doi.org/10.1111/j.1749-4877.2009.00146.x
Houssaye A (2013) Palaeoecological and morphofunctional interpretation of bone mass increase: an example in late Cretaceous shallow marine squamates. Biol Rev 88:117–139.
Houssaye A, Fish FE (2016) Functional (secondary) adaptation to an aquatic life in vertebrates: an introduction to the symposium. Integr Comp Biol 56:1266–1270. doi:https://doi.org/10.1093/icb.icw129
Houssaye A, Lindgren J, Pellegrini R, Lee AH, Germain D, Polcyn MJ (2013) Microanatomical and histological features in the long bones of mosasaurine mosasaurs (Reptilia, Squamata)–implications for aquatic adaptation and growth rates. PLoS One 8:e76741. doi:https://doi.org/10.1371/journal.pone.0076741
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. doi:https://doi.org/10.1093/icb/icw120
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. doi:https://doi.org/10.1371/journal.pone.0118409
Jaworski ZFG (1992) Haversian system and Haversian bone. In: Hall BK (ed) Bone Metabolism and Mineralization. CRC Press, Boca Raton, pp 21–45
Kaiser HE (1967) Pachyostotic bone conditions in certain regions of skull ofOdobenus rosmarusL. in relation to weight distribution. Anatomical Record 157, 366
Kaiser HE (1974) Morphology of the Sirenians. A Macroscopic X-Ray Atlas of the Morphology of Recent Species. S. Karger, Basel
Köhler M, Marin-Moratalla N, Jordana X, Aanes R (2012) Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487:358–361. doi:https://doi.org/10.1038/nature11264
Koretsky IA (2001) Morphology and systematics of the Miocene Phocinae (Mammalia: Carnivora) from Paratethys and the North Atlantic Region. Geol Hung Ser Palaeontol 54:1–109
Koretsky IA, Peters N (2008)Batavipusa (Carnivora, Phocidae, Phocinae): a new genus from the eastern shore of the North Atlantic Ocean (Miocene seals of the Netherlands, part II). Deinsea 12:53–62
Koretsky IA, Peters N, Rahmat SJ (2015) New species ofPraepusa (Carnivora, Phocidae, Phocinae) from the Netherlands supports east to west Neogene dispersal of true seals. Vestn Zool 49:57–66
Koretsky IA, Rahmat SJ (2013) First record of fossil Cystophorinae (Carnivora, Phocidae): middle Miocene seals from the northern Paratethys. Riv Ital Paleontol S 119:325–350. doi:https://doi.org/10.13130/2039-4942/6043
Koretsky IA, Rahmat SJ (2017) Preliminary report of pachyosteosclerotic bones in seals. Open Acc Res Anat 1:1–3
Koretsky IA, Ray CE (2008) Phocidae of the Pliocene of Eastern North America. Virginia Mus Nat Hist Spec Pub 14:81–140
Kühn C, Frey E (2012) Walking like caterpillars, flying like bats––pinniped locomotion. Palaeobio Palaeoenv 92:197–210. doi:https://doi.org/10.1007/s12549-012-0077-5
Lafage-Proust M-H, Roche B, Langer M, Cleret D, Vanden Bossche A, Olivier T, Vico L (2015) Assessment of bone vascularization and its role in bone remodeling. BoneKEy Rep 4, art no 662:1–8. doi:https://doi.org/10.1038/bonekey.2015.29
Lambert O, Muizon C de, Buffrénil V de (2011) Hyperdense rostral bones of ziphiid whales: diverse processes for a similar pattern. CR Palevol 10:453–468. doi:https://doi.org/10.1016/j.crpv.2011.03.012
Lamm ET (2013) Preparation and sectioning of specimens. In: Padian K, Lamm ET (eds) Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation. University of California Press, Berkeley, pp 55–160
Landrigan MD, Li J, Turnbull TL, Burr DB, Niebur GL, Roeder RK (2011) Contrast-enhanced micro-computed tomography of fatigue microdamage accumulation in human cortical bone. Bone 48:443–450. doi:https://doi.org/10.1016/j.bone.2010.10.160
Laurin M, Canoville A, Germain D (2011) Bone microanatomy and lifestyle: a descriptive approach. CR Palevol 10:381–402. doi:https://doi.org/10.1016/j.crpv.2011.02.003
Laurin M, Girondot M, Loth M-M (2004) The evolution of long bone microanatomy and lifestyle in lissamphibians. Paleobiology 30:589–613. doi:https://doi.org/10.1666/0094-8373(2004)030<0589:TEOLBM>2.0.CO;2
Lee TC, Mohsin S, Taylor D, Parkesh R, Gunnlaugsson T, O’Brien FJ, Giehl M, Gowin W (2003) Detecting microdamage in bone. J Anat 203:161–172. doi:https://doi.org/10.1046/j.1469-7580.2003.00211.x
Lieberman DE, Pearson OM, Polk JD, Demes B, Crompton AW (2003) Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs. J Exp Biol 206:3125–3138. doi:https://doi.org/10.1242/jeb.00514
Liu XS, Bevill G, Keaveny TM, Sajda P, Guo XE (2009) Micromechanical analyses of vertebral trabecular bone based on individual trabeculae segmentation of plates and rods. J Biomech 42:249–256. doi:https://doi.org/10.1016/j.biomech.2008.10.035
Margerie E de, Cubo J, Castanet J (2002) Bone typology and growth rate: testing and quantifying “Amprino’s rule” in the mallard (Anas platyrhynchos). CR Biol 325:221–230. doi:https://doi.org/10.1016/S1631-0691(02)01429-4
Marks SC, Popoff SN (1988) Bone cell biology: the regulation of development, structure and function of the skeleton. Am J Anat 183:1–44. doi:https://doi.org/10.1002/aja.1001830102
Martin RB (2000) Toward a unifying theory of bone remodeling. Bone 26:1–6. doi:https://doi.org/10.1016/S8756-3282(99)00241-0
Masschaele B, Dierick M, Loo DV, Boone MN, Brabant L, Pauwels E, Cnudde V, Hoorebeke LV (2013) HECTOR: a 240kV micro-CT setup optimized for research. J Phys Conf Ser 463:012012. doi:https://doi.org/10.1088/1742-6596/463/1/012012
Michou L, Brown JP (2011) Genetics of bone diseases: Paget’s disease, fibrous dysplasia, osteopetrosis and osteogenesis imperfecta. Joint Bone Spine 78: 252–258. doi:https://doi.org/10.1016/j.bspin.2010.07.010
Mohsin S, O’Brien FJ, Lee TC (2006) Osteonal crack barriers in ovine compact bone. J Anat 208: 81–89
Muizon C de (1981) Les vertébrés fossiles de la Formation Pisco (Pérou). Première partie: deux nouveaux Monachinae du Pliocène de Sud Sacaco. Inst Franc Etud Andines Mem 6 20–161
Nakajima Y, Endo H (2013). Comparative humeral microanatomy of terrestrial, semiaquatic, and aquatic carnivorans using micro-focus CT scan. Mammal Study 38:1–8
Parfitt AM (1981) Bone effect of spaceflight: analysis by quantum concept of bone remodeling. Acta Astronaut 8:1083–1090. doi:https://doi.org/10.1016/0094-5765(81)90082-5
Parfitt AM (1982) The coupling of bone formation to bone resorption: a critical analysis of the concept and of its relevance to the pathogenesis of osteoporosis. Metab Bone Dis Relat 4:1–6. doi:https://doi.org/10.1016/022-8747(82)90002-9
Pierce SE, Clack JA, Hutchinson JR (2011) Comparative axial morphology in pinnipeds and its correlation with aquatic locomotory behaviour. J Anat 219:502–514. doi:https://doi.org/10.1111/j.1469-7580.2011.01406.x
Polig E, Jee WSS (1990) A model of osteon closure in cortical bone. Calcif Tissue Internatl 47:261–269. doi:https://doi.org/10.1007/BF02555907
Prondvai E, Stein KHW, Ricqlès A de, Cubo J (2014) Development-based revision of bone tissue classification: the importance of semantics for science. Biol J Linn Soc 112:799–816. doi:https://doi.org/10.1111/bio.12323
Pyenson ND, Kelley NP, Parham JF (2014) Marine tetrapod macroevolution: physical and biological drivers on 250 Ma of invasions and evolution in ocean ecosystems. Palaeogeogr Palaeoclimatol Palaeoecol 400:1–8. doi:https://doi.org/10.1016/j.palaeo.2014.02.18
Qiu S, Fyhrie DP, Palnitkar S, Sudhaker Rao D (2003) Histomorphometric assessment of Haversian canal and osteocyte lacunae in different-sized osteons in human ribs. Anat Rec 272A:520–525. doi:https://doi.org/10.1002/ar.a.10058
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. doi:https://doi.org/10.1111/bij.12066
Ralston SH (2008) Pathogenesis of Paget’s disease of bone. Bone 43: 819–825.doi:https://doi.org/10.1016/j.bone.2008.06.015
Ricqlès A de (1989). Les mécanismes hétérochroniques dans le retour des tétrapodes au milieu aquatique. Geobios Mem Spec 12:337–348. doi:https://doi.org/10.1016/S0016-6995(89)80034-8
Ricqlès A de, Buffrénil V de (1995) Sur la présence de pachyostéosclérose chez la rhytine de Steller [Rhytina (Hydrodamalis) gigas], sirénien récent éteint. Ann Sci Nat Zool Paris, 13e Ser 16:47–53
Ricqlès A de, Buffrénil V de (2001) Bone histology, heterochronies and the return of tetrapods to life in water: w[h]ere are we? In: Mazin J-M, Buffrénil V de (Eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr. Friedrich Pfeil, München, pp 289–310
Schaffler MB, Choi K, Milgrom C (1995) Aging and matrix microdamage accumulation in human compact bone. Bone 17:521–527. doi:https://doi.org/10.1016/8756-3282(95)00370-3
Stein BR (1989) Bone density and adaptation in semiaquatic mammals. J Mammal 70:467–476. doi:https://doi.org/10.2307/1381418
Storå J (2000) Skeletal development in the Grey sealHalichoerus grypus, the Ringed sealPhoca hispida botnica, the Harbour sealPhoca vitulina vitulina and the Harp sealPhoca groenlandica. Epiphyseal fusion and life History. Archaeozoologia 11:199–222.
Taylor MA (2009) Functional significance of bone ballast in the evolution of buoyancy control strategies by aquatic tetrapods. Hist Biol 14:15–31. doi:https://doi.org/10.1080/10292380009380550
Turner CH (1998) Three rules for bone adaptation to mechanical stimuli. Bone 23:399–407. doi:https://doi.org/10.1016/S8756-3282(98)00118-5
Uhen MD (2007) Evolution of marine mammals: back to the sea after 300 million years. Anat Rec 290:514–522. doi:https://doi.org/10.1002/ar.20545
Van Beneden P-J (1871) Les phoques de la mer scaldisienne. Bul Acad R Sci Let b-Arts Belg 2ième Ser 32:5–19
Van Beneden P-J (1877) Description des ossements fossiles des environs d’Anvers, première partie. Pinnipèdes ou amphithériens. Ann Mus R Hist Nat Belg 1:1–88
Voide R, Schneider P, Stauber M, van Lenthe GH, Stampanoni M, Müller R (2011) The importance of murine cortical bone microstructure for microcrack initiation and propagation. Bone 49:1186–1193. doi:https://doi.org/10.1016/j.bone.2011.08.011
Wall WP (1983) The correlation between high limb-bone density and aquatic habits in recent mammals. J Paleontol 57:197–207
Webb P, Buffrénil V de (1990) Locomotion in the biology of large aquatic vertebrates. Trans Am Fish Soc 119:629–641. doi:https://doi.org/10.1577/1548-8659(1990)119<0629:LITBOL>2.3.CO;2
Zylberberg L, Traub W, Buffrénil V de, Alizard F, Arad T, Weiner S (1998) Rostrum of a toothed whale: ultrastructural study of a very dense bone. Bone 23:241–247. doi:https://doi.org/10.1016/S8756-3282(98)00101-X
Acknowledgements
The research presented in this study is in partial fulfillment of the PhD research of LD, conducted at Ghent University, Ghent, Belgium, and in collaboration with the Royal Belgian Institute of Natural Sciences, Brussels, Belgium. This PhD research is funded by the Research Foundation – Flanders (FWO) through an FWO PhD Fellowship to LD. This research is also partly funded by the Society of Vertebrate Paleontology’s 2016 Steven Cohen Award for Excellent Student Research, awarded to LD. TDK holds a postdoctoral Fellowship at the FWO.
We also want to thank S Bruaux, C Cousin, and A Folie from the RBINS for providing access to the collections. We thank R Fraaije and N Peters from the Oertijdmuseum Groene Poort, Boxtel, Netherlands, for allowing access to the holotypes ofBatavipusa neerlandica andPraepusa boeska. We are grateful to M Bosselaers for donating specimens from his private collection for the elaboration of thin sections. Special thanks to JR Wible (editor-in-chief), RW Boessenecker (reviewer) and A Houssaye (reviewer) for helpful comments that improved the quality of this work.
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Vakgroep Geologie, Universiteit Gent, Ghent, Belgium
Leonard Dewaele & Stephen Louwye
Directorate “Earth and History of Life”, Institut Royal des Sciences Naturelles de Belgique, Brussels, Belgium
Leonard Dewaele & Olivier Lambert
Département Origines et Evolution, Muséum National d’Histoire Naturelle, Paris, France
Michel Laurin & Vivian de Buffrénil
PProGRess, Vakgroep Geologie, Universiteit Gent, Ghent, Belgium
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Correspondence toLeonard Dewaele.
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Dewaele, L., Lambert, O., Laurin, M.et al. Generalized Osteosclerotic Condition in the Skeleton ofNanophoca vitulinoides, a Dwarf Seal from the Miocene of Belgium.J Mammal Evol26, 517–543 (2019). https://doi.org/10.1007/s10914-018-9438-9
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