Abstract
Mammalian dental formulae often are highly conserved, at least at a generic level. In walruses (Odobenus rosmarus), the constraints of dentition in light of documented high variability in tooth counts among walrus are examined. We propose that walruses do not have a constrained dental formula in terms of tooth position or tooth count. Instead, while walrus tooth counts vary, total occlusal area (TOA) is constrained relative to body mass, independent of tooth position or count. Nearly three-fourths of the 70 individuals sampled here had dentitions deviating from the previously reported dental formula of 1/1, 1/0, 3/3, 0/0, but there is a strong relationship between body size and total occlusal area. While the positive correlation between body size and TOA is consistent between sexes, the slope of the relationship differs significantly, suggesting an important sexual dimorphism in more than just walrus body size or tusk morphology. It is unclear if walrus teeth are involved at all in feeding, so TOA may impact positioning of prey during feeding or be completely independent of prey acquisition or feeding. Limited field observations support the hypothesis that dentition may play some role in prey positioning, with males feeding on both larger species and larger individuals of bivalves than females. Differences in food availability to individuals of differing body size have implications for conservation of walruses in the face of climate change and interactions with human fisheries, as well as diagnosing fossil taxa frequently defined in part by dental count. Extant walruses also may present an example of linking increased trait variability with the relaxation of functional constraints in response to shifting ecological roles.
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All raw measurements generated or analyzed for this study are included in this published article and Online Resource 1. Original photographs of specimens are not publicly available, as it violates use agreements from museum repositories, but are available from the corresponding author on reasonable request, with the exception of the UAF specimens, which are available associated with their specimen numbers via Arctos.
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All R code is available in Online Resource 2.
References
Adam PJ, Berta A (2002) Evolution of prey capture strategies and diet in Pinnipedimorpha (Mammalia, Carnivora). Oryctos 4(3-8):3-27
Allen JA (1880) History of North American Pinnipeds. A Monograph of the Walruses, Sea Lions, Sea Bears and Seals of North America. Government Printing Office, Washington
Berta A, Churchill M (2012) Pinniped taxonomy: review of currently recognized species and subspecies, and evidence used for their description. Mammal Rev 42(3):207-234
Born EW, Rysgaard S, Ehlmé G, Sejr M (2003) Underwater observations of foraging free-living Atlantic walruses (Odobenus rosmarus rosmarus) and estimates of their food consumption. Polar Biol 26:348-357
Boessenecker RW (2017) A new early Pliocene record of the toothless walrus Valenictus (Carnivora, Odobenidae) from the Purisima Formation of northern California. PaleoBios 34. http://dx.doi.org/10.5070/P9341035289 Retrieved from https://escholarship.org/uc/item/53v080hx
Boessenecker RW (2011) New records of the fur seal Callorhinus (Carnivora: Otariidae) from the Plio-Pleistocene Rio Dell Formation of northern California and comments on otariid dental evolution. J Vertebr Paleontol 31(2):454-467
Boessenecker RW and Churchill M (2013) A reevaluation of the morphology, paleoecology, and phylogenetic relationships of the enigmatic walrus Pelagiarctos. PLoS One 8(1):e54311
Churchill M (2015) Fossil focus: seals, sea lions and walruses. Palaeontology Online 5(9). https://www.palaeontologyonline.com/articles/2015/fossil-focus-seals-sea-lions-walruses/
Churchill M, Clementz MT (2015) Functional implications of variation in tooth spacing and crown size in Pinnipedimorpha (Mammalia: Carnivora). Anat Rec 298:878-902
Clark CT, Horstmann L, de Vernal A, Jensen AM, Misarti N (2019) Pacific walrus diet across 4000 years of changing sea ice conditions. Quat Res 1:1-17. https://doi.org/10.1017/qua.2018.140
Cobb WM (1933) The dentition of the walrus Odobenus obesus. Proc Zool Soc Lond 103(3):645-668
Collins G (1940) Habits of the Pacific walrus (Odobenus divergens). J Mammal 21(2):138-144
Corruccini RS, Beecher RM (1982) Occlusal variation related to soft diet in a nonhuman primate. Science 218(4567):74-76
Crofts SB, Summers AP (2014) How to best smash a snail: the effect of tooth shape on crushing load. J R Soc Interface 11:20131053
Damuth J, MacFadden BJ (eds) (1990) Body Size in Mammalian Paleobiology: Estimation and Biological Implications. Cambridge University Press, Cambridge
Deméré TA (1994a) The family Odobenidae: a phylogenetic analysis of fossil and living taxa. In: Berta A, Deméré TA (eds) Contributions in Marine Mammal Paleontology honoring Frank C. Whitmore, Jr. Proc San Diego Soc Nat Hist 29:99–123
Deméré TA (1994b) Two new species of fossil walruses (Pinnipedia: Odobenidae) from the upper Pliocene San Diego Formation, California. In: Berta A. Deméré T (eds). Contributions in Marine Mammal Paleontology honoring Frank C. Whitmore, Jr.: Proc San Diego Soc Nat Hist 29:99–123
Deméré TA, Berta A (2001) A reevaluation of Proneotherium repenningi from the Miocene Astoria Formation of Oregon and its position as a basal odobenid (Pinnipedia: Mammalia). J Vertebr Paleontol 21(2):279-310
Drehmer CJ, Sanfelice D, Loch C (2015) Dental anomalies in pinnipeds (Carnivora: Otariidae and Phocidae): occurrence and evolutionary implications. Zoomorphology 134(2):325-338
Evans RD, Richner P, Outridge PM (1995) Micro-spatial variations of heavy metals in the teeth of walrus as determined by laser ablation ICP-MS: the potential for reconstructing a history of heavy metal exposure. Arch Environ Contan Toxicol 28(1):55-60
Fay HF (1982) Ecology and biology of the Pacific walrus, Odobenus rosmarus divergens Illiger. N Am Fauna 74:1-279
Fay HF (1985) Odobenus rosmarus. Mammal Species 238:1-7
Harington C, Anderson T, Rodrigues C (1993) Pleistocene walrus (Odobenus rosmarus) from Forteau Labrador. Géogr Phys Quatern 47(1):111-118
Harington CR, Beard G (1991) The Qualicum walrus: a late Pleistocene walrus (Odobenus rosmarus) skeleton from Vancouver Island, British Columbia Canada. Ann Zool Fenn 28(3/4):311-319
Hill E (2011) The historical ecology of walrus exploitation in the North Pacific. In: Braje TJ Rick TC (eds) Human Impacts on Seals, Sea Lions, and Sea Otters: Integrating Archaeology and Ecology in the Northeast Pacific. University of California Press, Berkeley, pp 41–64
Hillson S (2005) Teeth; Manuals in Archaeology, 2nd edn. Cambridge University Press, New York
Jones KE and Goswami A (2010) Quantitative analysis of the influences of phylogeny and ecology on phocid and otariid pinniped (Mammalia; Carnivora) cranial morphology. J Zool 280(3):297–308
Jones KE, Ruff CB, Goswami A (2013) Morphology and biomechanics of the pinniped jaw: mandibular evolution without mastication. Anat Rec 296(7):1049–1063
Kassai Y, Munne P, Hotta Y, Penttilä E, Kavanagh K, Ohbayashi N, Takada S, Thesleff I, Jernvall J, Itoh N (2005) Regulation of mammalian tooth cusp patterning. Science 309(5743):2067-2070
Kastelein RA, Gerrits NM (1990) The anatomy of the walrus head (Odobenus rosmarus) Part 1: The skull. Aquat Mammal 16.3:101-119
Kastelein RA, Gerrits NM, Dubbeldam JL (1991) The anatomy of the walrus head (Odobenus rosmarus) Part 2: Description of the muscles and of their role in feeding and haul-out behavior. Aquat Mammal 17.3:156-180
Kastelein RA, Muller M, Terlouw A (1994) Oral suction of a Pacific walrus (Odobenus rosmarus divergens) in air and under water. Z Saugetierkd 59(2):105-115
Kryukova NV (2012) Dentition in Pacific walrus (Odobenus rosmarus divergens) calves of the year. Biol Bull 39(7):618-626
Levermann N, Galatius A, Ehlme G, Rysgaard S, Born EW (2003) Feeding behavior of free-ranging walruses with notes on apparent dextrality of flipper use. BMC Ecol 3:1-13
Lindqvist C, Bachmann L, Andersen LW, Born EW, Arnason U, Kovacs KM, Lydersen C, Abramov AV, Wiig Ø (2009) The Laptev Sea walrus Odobenus rosmarus laptevi: an enigma revisited. Zoologica Scripta 38(2):113–127
Lowry LF, Fay FH (1984) Seal eating by walruses in the Bering and Chukchi Seas. Polar Biol 3(1):11-18
Lydersen C (2018) Walrus: Odobenus rosmarus. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of Marine Mammals (2nd edn), Academic Press, Cambridge, pp. 1045–1048
Massare JA (1986) Tooth morphology and prey preference of Mesozoic marine reptiles. J Vertebr Paleontol 7(2):121-137
Mazza P (1995) Evolution of ursid dentition, with inferences on the functional morphology of the masticatory apparatus in the genus Ursus. In: Mazza P, Rustioni M, Boscagli G (eds) Aspects of Dental Biology: Paleontology, Anthropology and Evolution. International Institute for the Study of Man, Florence, pp 147–157
McKenna MC (1975) Toward a phylogenetic classification of the Mammalia. In: Luckett WP, Szalay FS (eds) Phylogeny of the Primates: A Multidisciplinary Approach. Plenum Press, New York, pp 21-46
Miller ED, Sung H-C, Moulton VD, Miller GW, Finley JK, Stenson GB (2007) Variation and integration of the simple mandibular postcanine dentition in two species of phocid seal. J Mammal 88(5):1325-1334
Miller EH (1975) Walrus ethology I The social role of tusks and applications of multidimensional scaling. Can J Zool 53(5):590–613
Molina-Schiller D, Pinedo MC (2004) Using canine teeth for sex determination of South American fur seal Arctocephalus australis. LAJAM 3(1):19–24
Nores C, Pearez C (1988) The occurrence of walrus (Odobenus rosmarus) in southern Europe. J Zool 216(4):593–596
Scheffer VB, Myrick AC Jr. (1980) A review of studies to 1970 of growth layers in the teeth of marine mammals. Rep Int Whal Comm (special issue) 3:51–63
Sheffield G, Grebmeier JM (2009) Pacific walrus (Odobenus rosmarus divergens): differential prey digestion and diet. Mar Mammal Sci 25(4):761–777
Taylor N, Clark CT, Misarti N, Horstmann L (2020) Determining sex of adult Pacific walruses from mandible measurements. J Mammal 101(4):941–950
Thesleff I (2014) Current understanding of the process of tooth formation: transfer from the laboratory to the clinic. Aust Dent J 59:48–54
Thewissen JGM, Williams EM (2002) The early radiations of Cetacea (Mammalia): evolutionary pattern and development correlations. Annu Rev Ecol Syst 33:73–90
Uhen MD (2009) Dental morphology, evolution of. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of Marine Mammals, 2nd edn. Academic Press, Cambridge, p 302–307
Vilà C, Urios V, Castroviejo J (1993) Tooth losses and anomalies in the wolf (Canis lupus). Can J Zool 71(5):968–971
Werth AJ (2006) Mandibular and dental variation and the evolution of suction feeding in Odontoceti. J Mammal 87(3):579–588
Wiig Ø, Born EW, Gjertz I, Lydersen C, Stewart REA (2007) Historical sex-specific distribution of Atlantic walrus (Odobenus rosmarus rosmarus) in Svalbard assessed by mandible measurments. Polar Biol 31:69–75
Zarr JH (2010) Biostatistical Analysis, 5th edn. Prentice Hall an Imprint of Pearson Education, Upper Saddle River
Acknowledgements
Thank you to A. Nelson, for asking the questions that inspired this project. Thank you to E. White (University of Oregon) for access and photographing the University of Oregon specimen as well as her superb artwork on the walrus skull diagram, to C. Conroy for access to the UC Berkeley MVZ specimen, to P. Holroyd for access to the UCMP specimens as well as invaluable discussion and suggestions for this project, to M. Dickson for access to the AMNH material included, to A. Gunderson for many photographs of the UAM collections walruses, to K. Stilson and F. Socki for photographs of the FMNH specimens and to B. Patterson, L. Heaney, R. Banasiak, L. Smith, and B. Marks for access to those specimens. We also thank D. Reuter for taking the UWBM photographs and J. Bradley for access to the specimens. Thank you to K. Prassack for some initial review of this manuscript, and R. Boessenecker and A. Poust for their extremely helpful reviews on this manuscript. Finally, R.I.P to E.T. the walrus who not only provided inspiration for this article, but was a deciding factor in the lead author becoming a scientist.
Funding
Funding to travel to the AMNH was provided by the Theodore Roosevelt Memorial Fund of the American Museum of Natural History. Funding to travel to the UCMP was in part provided by a UCMP Samuel P. Welles Fund grant. This research was supported in part by an NSF grant (DEB-1256897) to SSBH and S. Price.
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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Win McLaughlin. Data collection was also performed by Caitlyn Boatman. Data analysis was also performed by Edward Davis. The first draft of the manuscript was written by Win McLaughlin and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Appendix
Appendix
Specimens Included in Study
USNM-6780, AMNH-19267, AMNH-19271, AMNH-20046, AMNH-77938, AMNH-77940, AMNH-90779, AMNH-90783, AMNH-90877, AMNH-207765, AMNH-41216, AMNH-1562, MNCH-D632, MVZ-184134, MVZ-106189, MVZ-106189, MVZ-119066, MVZ-184134, MVZ-96097, MVZ-125567, MVZ-96099, MVZ-125559, MVZ-57327, UAM-14793, UAM-16586, UAM-12075, UAM-99578, UAM-87009, UAM-87003, UAM-87001, UAM-16593, UAM-16592, UAM-16591, UAM-16588, UAM-12086, UAM-12085, UAM-12084, UAM-12083, UAM-12082, UAM-12081, UAM-12079, UAM-12078, UAM-12077, UAM-12076, UAM-12075, UAM-7277, UAM-11700, UAM-11696, UAM-11694, UAM-10538, FMNH-26888, FMNH-29171, FMNH-5508, FMNH-26809, FMNH-766, FMNH-140831, FMNH-26889, UWBM-34502, UWBM-36990, UWBM-82591, UWBM-82590, UWBM-51203, UWBM-82506, UWBM-82507, UWBM-12027, UWBM-12028 UWBM-51201, UWBM-41984, UWBM-35215, UWBM-80659, NMNH-550410, NMNH-16437, NMNH-402/403, NMC-38490, USNM-276030, USNM-550413, USNM-22014, USNM-267962, USNM-267965, USNM-276624, USNM-291842.
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McLaughlin, W.N.F., Boatman, C.J., Davis, E.B. et al. Total Dental Occlusal Area as a Feeding Constraint Feature in Extant Walruses (Odobenus rosmarus), and Implications for the Evolution of Molluscivory in Odobenidae. J Mammal Evol 29, 571–583 (2022). https://doi.org/10.1007/s10914-022-09603-x
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DOI: https://doi.org/10.1007/s10914-022-09603-x